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Neutrophil apoptosis and the resolution of infection

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Abstract

Polymorphonuclear leukocytes (PMNs) are the most abundant white cell in humans and an essential component of the innate immune system. PMNs are typically the first type of leukocyte recruited to sites of infection or areas of inflammation. Ingestion of microorganisms triggers production of reactive oxygen species and fusion of cytoplasmic granules with forming phagosomes, leading to effective killing of ingested microbes. Phagocytosis of bacteria typically accelerates neutrophil apoptosis, which ultimately promotes the resolution of infection. However, some bacterial pathogens alter PMN apoptosis to survive and thereby cause disease. Herein, we review PMN apoptosis and the ability of microorganisms to alter this important process.

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References

  1. Faurschou M, Borregaard N. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 2003;5:1317–27.

    PubMed  CAS  Google Scholar 

  2. Klebanoff SJ. Myeloperoxidase: friend and foe. J Leukoc Biol. 2005;77:598–625.

    PubMed  CAS  Google Scholar 

  3. Quinn MT, Ammons MC, DeLeo FR. The expanding role of NADPH oxidases in health and disease: no longer just agents of death and destruction. Clin Sci (Lond). 2006;111:1–20.

    CAS  Google Scholar 

  4. Nauseef WM. How human neutrophils kill and degrade microbes: an integrated review. Immunol Rev. 2007;219:88–102.

    PubMed  CAS  Google Scholar 

  5. Cowland JB, Borregaard N. Isolation of neutrophil precursors from bone marrow for biochemical and transcriptional analysts. J Immunol Methods. 1999;232:191–200.

    PubMed  CAS  Google Scholar 

  6. Ward AC, Loeb DM, Soede-Bobok AA, Touw IP, Friedman AD. Regulation of granulopoiesis by transcription factors and cytokine signals. Leukemia. 2000;14:973–90.

    PubMed  CAS  Google Scholar 

  7. Bjerregaard MD, Jurlander J, Klausen P, Borregaard N, Cowland JB. The in vivo profile of transcription factors during neutrophil differentiation in human bone marrow. Blood. 2003;101:4322–32.

    PubMed  CAS  Google Scholar 

  8. Friedman AD. Transcriptional regulation of granulocyte and monocyte development. Oncogene. 2002;21:3377–90.

    PubMed  CAS  Google Scholar 

  9. Theilgaard-Monch K, Jacobsen LC, Borup R, Rasmussen T, Bjerregaard MD, Nielsen FC, et al. The transcriptional program of terminal granulocytic differentiation. Blood. 2005;105:1785–96.

    PubMed  Google Scholar 

  10. Borregaard N, Theilgaard-Monch K, Sorensen OE, Cowland JB. Regulation of human neutrophil granule protein expression. Curr Opin Hematol. 2001;8:23–7.

    PubMed  CAS  Google Scholar 

  11. Bainton DF, Ullyot JL, Farquhar MG. The development of neutrophilic polymorphonuclear leukocytes in human bone marrow. J Exp Med. 1971;134:907–34.

    PubMed  CAS  Google Scholar 

  12. Baum CM, Weissman IL, Tsukamoto AS, Buckle AM, Peault B. Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci USA. 1992;89:2804–8.

    PubMed  CAS  Google Scholar 

  13. Killmann SA, Cronkite EP, Fliedner TM, Bond VP. Mitotic indices of human bone marrow cells. I. Number and cytologic distribution of mitoses. Blood. 1962;19:743–50.

    PubMed  CAS  Google Scholar 

  14. Borregaard N, Sehested M, Nielsen BS, Sengelov H, Kjeldsen L. Biosynthesis of granule proteins in normal human bone marrow cells. Gelatinase is a marker of terminal neutrophil differentiation. Blood. 1995;85:812–7.

    PubMed  CAS  Google Scholar 

  15. Athens JW, Haab OP, Raab SO, Mauer AM, Ashenbrucker H, Cartwright GE, et al. Leukokinetic studies. IV. The total blood, circulating and marginal granulocytes pools and the granulocytes turnover rate in normal subjects. J Clin Invest. 1961;40:989–95.

    PubMed  CAS  Google Scholar 

  16. Cline MJ. Production, destruction, and distribution of neutrophilic granulocytes. The white cell. Cambridge: Harvard University Press; 1975. p. 24–38.

    Google Scholar 

  17. Cronkite EP, Fliedner TM. Granulocytopoiesis. N Engl J Med. 1964;270:1347–52.

    PubMed  CAS  Google Scholar 

  18. Fliedner TM, Cronkite EP, Robertson JS. Granulocytopoiesis. I. Senescence and random loss of neutrophilic granulocytes in human beings. Blood. 1964;24:402–14.

    PubMed  CAS  Google Scholar 

  19. Savill JS, Wyllie AH, Henson JE, Walport MJ, Henson PM, Haslett C. Macrophage phagocytosis of aging neutrophils in inflammation: programmed cell death in the neutrophil leads to its recognition by macrophages. J Clin Invest. 1989;83:865–75.

    PubMed  CAS  Google Scholar 

  20. Savill JS, Henson PM, Haslett C. Phagocytosis of aged human neutrophils by macrophages is mediated by a novel “charge-sensitive” recognition mechanism. J Clin Invest. 1989;84:1518–27.

    PubMed  CAS  Google Scholar 

  21. Kobayashi SD, Voyich JM, Burlak C, DeLeo FD. Neutrophils in the innate immune response. Arch Immunol Ther Exp. 2005;53:505–17.

    CAS  Google Scholar 

  22. McPhail LC, Clayton CC, Snyderman R. The NADPH oxidase of human polymorphonuclear leukocytes. Evidence for regulation by multiple signals. J Biol Chem. 1984;259:5768–75.

    PubMed  CAS  Google Scholar 

  23. DeLeo FR, Renee J, McCormick S, Nakamura M, Apicella M, Weiss JP, et al. Neutrophils exposed to bacterial lipopolysaccharide upregulate NADPH oxidase assembly. J Clin Invest. 1998;101:455–63.

    PubMed  CAS  Google Scholar 

  24. Sengelov H, Kjeldsen L, Diamond MS, Springer TA, Borregaard N. Subcellular localization and dynamics of Mac-1 (αmβ2) in human neutrophils. J Clin Invest. 1993;92:1467–76.

    PubMed  CAS  Google Scholar 

  25. Kurt-Jones EA, Mandell L, Whitney C, Padgett A, Gosselin K, Newburger PE, et al. Role of toll-like receptor 2 (TLR2) in neutrophil activation: GM-CSF enhances TLR2 expression and TLR2-mediated interleukin 8 responses in neutrophils. Blood. 2002;100:1860–8.

    PubMed  CAS  Google Scholar 

  26. Diamond MS, Staunton DE, Marlin SD, Springer TA. Binding of the integrin mac-1 (CD11b/CD18) to the third immunoglobulin-like domain of ICAM-1 (CD54) and its regulation by glycosylation. Cell. 1991;65:961–71.

    PubMed  CAS  Google Scholar 

  27. Diamond MS, Staunton DE, de Fougerolles AR, Stacker SA, Garcia-Aguilar J, Hibbs ML, et al. ICAM-1 (CD54): a counter-receptor for Mac-1 (CD11b/CD18). J Cell Biol. 1990;111:3129–39.

    PubMed  CAS  Google Scholar 

  28. Muller WA, Weigl SA, Deng X, Phillips DM. PECAM-1 is required for transendothelial migration of leukocytes. J Exp Med. 1993;178:449–60.

    PubMed  CAS  Google Scholar 

  29. Khan AI, Kerfoot SM, Heit B, Liu L, Andonegui G, Rufell B, et al. Role of CD44 and hyaluronan in neutrophil recruitment. J Immunol. 2004;173:7594–601.

    PubMed  CAS  Google Scholar 

  30. Cooper D, Lindberg FP, Gamble JR, Brown EG, Vadas MA. Transendothelial migration of neutrophils involves integrin-associated protein (CD47). Proc Natl Acad Sci USA. 1995;92:3978–82.

    PubMed  CAS  Google Scholar 

  31. de Mendez I, Adams AG, Sokolic RA, Malech HL, Leto TL. Multiple SH3 domain interactions regulate NADPH oxidase assembly in whole cells. EMBO J. 1996;15:1211–20.

    PubMed  Google Scholar 

  32. Clark RA, Klebanoff SJ. Myeloperoxidase––H2O2––halide system: cytotoxic effect on human blood leukocytes. Blood. 1977;50:65–70.

    PubMed  CAS  Google Scholar 

  33. Odell EW, Segal AW. The bactericidal effects of the respiratory burst and the myeloperoxidase system isolated in neutrophil cytoplasts. Biochim Biophys Acta. 1988;971:266–74.

    PubMed  CAS  Google Scholar 

  34. Klebanoff SJ. Myeloperoxidase: contribution to the microbicidal activity of intact leukocytes. Science. 1970;169:1095–7.

    PubMed  CAS  Google Scholar 

  35. Rosen H, Klebanof SJ. Bactericidal activity of a superoxide anion-generating system. J Exp Med. 1979;149:27–39.

    PubMed  CAS  Google Scholar 

  36. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol. 2004;4:499–511.

    PubMed  CAS  Google Scholar 

  37. Underhill DM, Gantner B. Integration of toll-like receptor and phagocytic signaling for tailored immunity. Microbes Infect. 2004;6:1368–73.

    PubMed  CAS  Google Scholar 

  38. Brown GD, Gordon S. Immune recognition: a new receptor for β-glucans. Nature. 2001;413:36–7.

    PubMed  CAS  Google Scholar 

  39. Kennedy AD, Willment JA, Dorward DW, Williams DL, Brown GD, DeLeo FR. Dectin-1 promotes fungicidal activity on human neutrophils. Eur J Immunol. 2007;37:467–78.

    PubMed  CAS  Google Scholar 

  40. Kobayashi SD, Voyich JM, Whitney AR, DeLeo FR. Spontaneous neutrophil apoptosis and modulation of cell survival by granulocyte macrophage-colony stimulating factor. J Leukoc Biol. 2005;78:1408–18.

    Google Scholar 

  41. Whyte MK, Meagher LC, MacDermot J, Haslett C. Impairment of function in aging neutrophils is associated with apoptosis. J Immunol. 1993;150:5124–34.

    PubMed  CAS  Google Scholar 

  42. Metchnikoff E. Lecture VII. Lectures on the comparative pathology of inflammation. In: Starling FA, Starling EH, editors. London: Kegan, Paul, Trench, Trubner; 1893. p. 107–31.

  43. Leuenroth SJ, Grutkoski PS, Ayala A, Simms HH. The loss of Mcl-1 expression in human polymorphonuclear leukocytes promotes apoptosis. J Leukoc Biol. 2000;68:158–66.

    PubMed  CAS  Google Scholar 

  44. Moulding DA, Quayle JA, Hart CA, Edwards SW. Mcl-1 expression in human neutrophils: regulation by cytokines and correlation with cell survival. Blood. 1998;92:2495–502.

    PubMed  CAS  Google Scholar 

  45. Kato T, Kutsuna H, Oshitani N, Kitagawa S. Cyclic AMP delays neutrophil apoptosis via stabilization of Mcl-1. FEBS Lett. 2006;580:4582–6.

    PubMed  CAS  Google Scholar 

  46. Moulding DA, Akgul C, Derouet M, White MRH, Edwards SW. BCL-2 family expression in human neutrophils during delayed and accelerated apoptosis. J Leukoc Biol. 2001;70:783–92.

    PubMed  CAS  Google Scholar 

  47. Gardai S, Whitlock BB, Helgason C, Ambruso D, Fadok V, Bratton D, et al. Activation of SHIP by NADPH oxidase-stimulated lyn leads to enhanced apoptosis in neutrophils. J Biol Chem. 2002;277:5236–46.

    PubMed  CAS  Google Scholar 

  48. Baran CP, Tridanapani S, Helgason CD, Humphries K, Krystal G, Marsh CB. The inositol 5′-phosphate SHIP-1 and the src kinase lyn negatively regulate macrophage colony-stimulating factor-induced akt activity. J Biol Chem. 2003;278:38628–36.

    PubMed  CAS  Google Scholar 

  49. Cox D, Dale BM, Kashiwada M, Helgason CD, Greenberg S. A regulatory role for src homology 2 domain-containing inositol 5′-phosphatase (SHIP) in phagocytosis mediated by Fcγ receptors and complement receptor 3 (αMβ2; CD11b/CD18). J Exp Med. 2001;193:61–71.

    PubMed  CAS  Google Scholar 

  50. Helgason CD, Damen JE, Rosten P, Grewal R, Sorensen P, Chappel SM, et al. Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev. 1998;12:1610–20.

    PubMed  CAS  Google Scholar 

  51. Chuang PI, Yee E, Karsan A, Winn RK, Harlan JM. A1 is a constitutive and inducible Bcl-2 homologue in mature human neutrophils. Biochem Biophys Res Commun. 1998;249:361–5.

    PubMed  CAS  Google Scholar 

  52. Sawatzky DA, Willoughby DA, Colville-Nash PR, Rossi AG. The involvement of the apoptosis-modulating proteins ERK 1/2, Bcl, xL and Bax in the resolution of acute inflammation in vivo. Am J Pathol. 2006;168:33–41.

    PubMed  CAS  Google Scholar 

  53. Murphy BM, O’Neill AJ, Adrain C, Watson RWG, Martin SJ. The apoptosome pathway to caspase activation in primary human neutrophils exhibits dramatically reduced requirements for cytochrome c. J Exp Med. 2003;197:625–32.

    PubMed  CAS  Google Scholar 

  54. Maianski NA, Mul FP, van Buul JD, Roos D, Kuijpers TW. Granulocyte colony-stimulating factor inhibits the mitochondria-dependent activation of caspase-3 in neutrophils. Blood. 2002;99:672–9.

    PubMed  CAS  Google Scholar 

  55. Altznauer F, Conus S, Cavalli A, Folkers G, Simon H-U. Calpain regulates bax and subsequent smac-dependent caspase-3 activation in neutrophil apoptosis. J Biol Chem. 2004;279:5947–57.

    PubMed  CAS  Google Scholar 

  56. Dibbert B, Weber M, Nikolaizik WH, Vogt P, Schoni MH, Blaser K, et al. Cytokine-mediated Bax deficiency and consequent delayed neutrophil apoptosis: a general mechanism to accumulate effector cells in inflammation. Proc Natl Acad Sci USA. 1999;96:13330–5.

    PubMed  CAS  Google Scholar 

  57. Colotta F, Re F, Polentarutti N, Sozzani S, Mantovani A. Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood. 1992;80:2012–20.

    PubMed  CAS  Google Scholar 

  58. Baumann R, Casaulta C, Simon D, Conus S, Yousefi S, Simon H-U. Macrophage migration inhibitory factor delays apoptosis in neutrophils by inhibiting the mitochondria-dependent death pathway. FASEB J. 2003;17:2221–30.

    PubMed  CAS  Google Scholar 

  59. Wolach B, van der Laan LJ, Maianski NA, Tool AT, van Bruggen R, Roos D, et al. Growth factors G-CSF and GM-CSF differentially preserve chemotaxis of neutrophils aging in vitro. Exp Hematol. 2007;35:541–50.

    PubMed  CAS  Google Scholar 

  60. Zhang B, Hiranhashi J, Cullere X, Mayadas TN. Elucidation of molecular events leading to neutrophil apoptosis following phagocytosis: cross-talk between caspase 8, reactive oxygen species, and MAPK/ERK activation. J Biol Chem. 2003;278:28443–54.

    PubMed  CAS  Google Scholar 

  61. Yamamoto A, Taniuchi S, Tsuji S, Hasui M, Kobayashi Y. Role of reactive oxygen species in neutrophil apoptosis following ingestion of heat-killed Staphylococcus aureus. Clin Exp Immunol. 2002;129:479–84.

    PubMed  CAS  Google Scholar 

  62. Kasahara Y, Iwai K, Yachie A, Ohta K, Konno A, Seki H, et al. Involvement of reactive oxygen intermediates in spontaneous and CD95 (APO-1)-mediated apoptosis of neutrophils. Blood. 1997;89:1748–53.

    PubMed  CAS  Google Scholar 

  63. Fadeel B, Ahlin A, Henter J-I, Orrenius S, Hampton MB. Involvement of caspases in neutrophil apoptosis: regulation by reactive oxygen species. Blood. 1998;92:4808–18.

    PubMed  CAS  Google Scholar 

  64. Hampton MB, Kettle AJ, Winterbourn CC. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood. 1998;92:3007–17.

    PubMed  CAS  Google Scholar 

  65. Maianski NA, Geissler J, Srinivasula SM, Alnemri ES, Roos D, Kuijpers TW. Functional characterization of mitochondria in neutrophils: a role restricted to apoptosis. Cell Death Differ. 2004;11:143–53.

    PubMed  CAS  Google Scholar 

  66. Knepper-Nicolai B, Savill J, Brown SB. Constitutive apoptosis in human neutrophils requires synergy between calpains and the proteasome downstream of caspases. J Biol Chem. 1998;273:30530–6.

    PubMed  CAS  Google Scholar 

  67. Scheel-Toellner D, Wang K, Assi LK, Webb PR, Craddock RM, Salmon M, et al. Clustering of death receptors in lipid rafts initiates neutrophil spontaneous apoptosis. Biochem Soc Trans. 2004;32:679–81.

    PubMed  CAS  Google Scholar 

  68. Taneja R, Parodo J, Jia SH, Kapus A, Rotstein OD, Marshall JC. Delayed neutrophil apoptosis in sepsis is associated with maintenance of mitochondrial transmembrane potential and reduced caspase-9 activity. Crit Care Med. 2004;32:1460–9.

    PubMed  CAS  Google Scholar 

  69. Scheel-Toellner D, Wang K, Craddock R, Webb PR, McGettrick HM, Assi LK, et al. Reactive oxygen species limit neutrophil life span by activating death receptor signaling. Blood. 2004;104:2557–64.

    PubMed  CAS  Google Scholar 

  70. Liles WC, Kiener PA, Ledbetter JA, Aruffo A, Klebanoff SJ. Differential expression of Fas (CD95) and Fas Ligand on normal human phagocytes: implications for the regulation of apoptosis in neutrophils. J Exp Med. 1996;184:429–40.

    PubMed  CAS  Google Scholar 

  71. Brown SB, Savill J. Phagocytosis triggers macrophage release of Fas ligand and induces apoptosis of bystander leukocytes. J Immunol. 1999;162:480–5.

    PubMed  CAS  Google Scholar 

  72. Jimenez MF, Watson RW, Parodo J, Evans D, Foster D, Steinberg M, et al. Dysregulated expression of neutrophil apoptosis in the systemic inflammatory response syndrome. Arch Surg. 1997;132:480–5.

    Google Scholar 

  73. Harper N, Hughes M, MacFarlane M, Cohen GM. Fas-associated death domain protein and caspase-8 are not recruited to the tumor necrosis factor receptor 1 signaling complex during tumor necrosis factor-induced apoptosis. J Biol Chem. 2003;278:25534–41.

    PubMed  CAS  Google Scholar 

  74. Gon S, Gatanaga T, Sendo F. Involvement of two types of TNF receptor in TNF-α induced neutrophil apoptosis. Microbiol Immunol. 1996;40:463–5.

    PubMed  CAS  Google Scholar 

  75. Murray J, Barbar JAJ, Dunkley SA, Lopez AF, Van Ostade X, Condliffe AM, et al. Regulation of neutrophil apoptosis by tumor necrosis factor-α: requirement for TNFR55 and TNFR75 for induction of apoptosis in vitro. Blood. 1997;90:2772–83.

    PubMed  CAS  Google Scholar 

  76. Maianski NA, Roos D, Kuijpers TW. Tumor necrosis factor α induces a caspase-independent death pathway in human neutrophils. Blood. 2003;101:1987–95.

    PubMed  CAS  Google Scholar 

  77. van den Berg JM, Weyer S, Weening JJ, Roos D, Kuijpers TW. Divergent effects of tumor necrosis factor α on apoptosis of human neutrophils. J Leukoc Biol. 2001;69:467–73.

    PubMed  Google Scholar 

  78. D’Osualdo A, Ferlito F, Prigione I, Obici L, Meini A, Zulian F, et al. Neutrophils from patients with TNFRSF1A mutations display resistance to tumor necrosis factor-induced apoptosis. Arthritis Rheum. 2006;54:998–1008.

    PubMed  CAS  Google Scholar 

  79. Kamohara H, Matsuyama W, Shimozato O, Abe K, Galligan C, Hashimoto S-I, et al. Regulation of tumour necrosis factor-related apoptosis-inducing ligand (TRAIL) and TRAIL receptor expression in human neutrophils. Immunology. 2004;111:186–94.

    PubMed  CAS  Google Scholar 

  80. Renshaw SA, Parmar JS, Singleton V, Rowe SJ, Dockrell DH, Dower SK, et al. Acceleration of human neutrophil apoptosis by TRAIL. J Immunol. 2003;170:1027–33.

    PubMed  CAS  Google Scholar 

  81. Walczak H, Krammer PH. The CD95 (APO-1/Fas) and the TRAIL (APO-2L) apoptosis systems. Exp Cell Res. 2000;256:58–66.

    PubMed  CAS  Google Scholar 

  82. Lum JJ, Bren G, McClure R, Badley AD. Elimination of senescent neutrophils by TNF-relating apoptosis-inducing ligand. J Immunol. 2005;175:1232–8.

    PubMed  CAS  Google Scholar 

  83. Lamhamedi-Cherradi SE, Zheng SJ, Maguschak KA, Peschon J, Chen YH. Defective thymocyte apoptosis and accelerated autoimmune diseases in TRAIL−/− mice. Nat Immunol. 2003;4:255–60.

    PubMed  CAS  Google Scholar 

  84. Lamhamedi-Cherradi SE, Zheng S, Tisch RM, Chen YH. Critical roles of tumor necrosis factor-related apoptosis-inducing ligand in type 1 diabetes. Diabetes. 2003;52:2274–8.

    PubMed  CAS  Google Scholar 

  85. Hilliard B, Wilmen A, Seidel C, Liu TS, Goke R, Chen Y. Roles of TNF-related apoptosis-inducing ligand in experimental autoimmune encephalomyelitis. J Immunol. 2001;166:1314–9.

    PubMed  CAS  Google Scholar 

  86. Koga Y, Matsuzaki A, Suminoe A, Hattori H, Hara T. Neutrophil-derived TNF-related apoptosis-inducing ligand (TRAIL): a novel mechanism of antitumor effect by neutrophils. Cancer Res. 2004;64:1037–43.

    PubMed  CAS  Google Scholar 

  87. Cassatella MA, Huber V, Calzetti F, Margotto D, Tamassia N, Peri G, et al. Interferon-activated neutrophils store a TNF-related apoptosis-inducing ligand (TRAIL/Apo-2 ligand) intracellular pool that is readily mobilizable following exposure to proinflammatory mediators. J Leukoc Biol. 2006;79:123–32.

    PubMed  CAS  Google Scholar 

  88. Simons MP, Leidal KG, Nauseef WM, Griffith TS. TNF-related apoptosis-inducing ligand (TRAIL) is expressed throughout myeloid development, resulting in a broad distribution among neutrophil granules. J Leukoc Biol. 2008;83:621–9.

    Google Scholar 

  89. Bovolenta C, Gasperini S, Cassatella MA. Granulocyte colony-stimulating factor induces the binding of STAT1 and STAT3 to the IFNγ response region within the promoter of the FcγRI/CD64 gene in human neutrophils. FEBS Lett. 1996;386:239–42.

    PubMed  CAS  Google Scholar 

  90. Scapini P, Laudanna C, Pinardi C, Allavena P, Mantovani A, Sozzani S, et al. Neutrophils produce biologically active macrophage inflammatory protein-3α (MIP-3α)/CCL20 and MIP-3β/CCL19. Eur J Immunol. 2001;31:1981–8.

    PubMed  CAS  Google Scholar 

  91. Bazzoni F, Cassatella MA, Rossi F, Ceska M, Dewald B, Baggiolini M. Phagocytosing neutrophils produce and release high amounts of the neutrophil-activating peptide 1/interleukin 8. J Exp Med. 1991;173:771–4.

    PubMed  CAS  Google Scholar 

  92. Gasperini S, Marchi M, Calzetti F, Laudanna C, Vincentini L, Olsen H, et al. Gene expression and production of the monokine induced by IFN-γ (MIG), IFN-inducible T cell α chemoattractant (I-TAC), and IFN-γ-inducible protein-10 (IP-10) chemokines by human neutrophils. J Immunol. 1999;162:4928–37.

    PubMed  CAS  Google Scholar 

  93. Lapinet JA, Scapini P, Calzetti F, Perez O, Cassatella MA. Gene expression and production of tumor necrosis factor alpha, interleukin 1-β, (IL-1β), IL-8, macrophage inflammatory protein 1α (MIP-1α), MIP-1β, and gamma interferon-inducible protein 10 by human neutrophils stimulated with group b meningococcal outer membrane vesicles. Infect Immun. 2000;68:6917–23.

    PubMed  CAS  Google Scholar 

  94. Kobayashi SD, Braughton KR, Whitney AR, Voyich JM, Schwan TG, Musser JM. Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils. Proc Natl Acad Sci USA. 2003;100:10948–53.

    PubMed  CAS  Google Scholar 

  95. Kobayashi SD, Voyich JM, Buhl CL, Stahl RM, DeLeo FR. Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: cell fate is regulated at the level of gene expression. Proc Natl Acad Sci USA. 2002;99:6901–6.

    PubMed  CAS  Google Scholar 

  96. Quinn MT, Gauss KA. Structure and regulation of the neutrophil respiratory burst oxidase: comparison with non-phagocyte oxidases. J Leukoc Biol. 2004;76:760–81.

    PubMed  CAS  Google Scholar 

  97. Scapini P, Lapinet-Vera JA, Gasperini S, Calzetti F, Bazzoni F, Cassatella MA. The neutrophil as a cellular source of chemokines. Immunol Rev. 2000;177:195–203.

    PubMed  CAS  Google Scholar 

  98. Cohen JJ, Duke RC, Fadok VA, Sellins KS. Apoptosis and programmed cell death in immunity. Ann Rev Immunol. 1992;10:267–93.

    CAS  Google Scholar 

  99. DeLeo FR. Modulation of phagocyte apoptosis by bacterial pathogens. Apoptosis. 2004;9:399–413.

    PubMed  CAS  Google Scholar 

  100. Kobayashi SD, Voyich JM, Somerville GA, Braughton KB, Malech HL, Musser JM, et al. An apoptosis-differentiation programme in human polymorphonuclear leukocytes facilitates resolution of inflammation. J Leukoc Biol. 2003;73:315–22.

    PubMed  CAS  Google Scholar 

  101. Ren Y, Savill J. Apoptosis: the importance of being eaten. Cell Death Differ. 1998;5:563–8.

    PubMed  CAS  Google Scholar 

  102. Savill J. Apoptosis in resolution of inflammation. J Leukoc Biol. 1997;61:375–80.

    PubMed  CAS  Google Scholar 

  103. Walcheck B, Herrera AH, St.Hill C, Mattila PE, Whiteney AR, DeLeo FR. ADAM17 activity during human neutrophil activation and apoptosis. Eur J Immunol. 2006;36:968–76.

    PubMed  CAS  Google Scholar 

  104. Chalaris A, Rabe B, Paliga K, Lange H, Laskay T, Fielding CA, et al. Apoptosis is a natural stimulus of IL6R shedding and contributes to the proinflammatory trans-signaling function of neutrophils. Blood. 2007;110:1748–55.

    PubMed  CAS  Google Scholar 

  105. Lust JA, Donovan KA, Kline MP, Greipp PR, Kyle RA, Maihle NJ. Isolation of an mRNA encoding a soluble form of the human interleukin-6 receptor. Cytokine. 1992;4:96–100.

    PubMed  CAS  Google Scholar 

  106. Matthews V, Schuster B, Schutze S, Bubmeyer I, Ludwig A, Hunghausen C, et al. Cellular cholesterol depletion triggers shedding of the human interleukin-6 receptor by ADAM10 and ADAM17 (TACE). J Biol Chem. 2003;278:38829–39.

    PubMed  CAS  Google Scholar 

  107. Hurst SM, Wilkinson TS, McLoughlin RM, Jones S, Horiuchi S, Yamamoto N, et al. IL-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen during acute inflammation. Immunity. 2001;14:705–14.

    PubMed  CAS  Google Scholar 

  108. Bannenberg GL, Chiang N, Ariel A, Arita M, Tjonahen E, Gotlinger KH, et al. Molecular circuits of resolution: formation and actions of resolvins and protectins. J Immunol. 2005;174:4345–55.

    PubMed  CAS  Google Scholar 

  109. Claria J, Serhan CN. Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions. Proc Natl Acad Sci USA. 1995;92:9475–9.

    PubMed  CAS  Google Scholar 

  110. Serhan CN, Chiang N, Van Dyke TE. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol. 2008;8:349–61.

    PubMed  CAS  Google Scholar 

  111. el Kebir D, Jozsef L, Khreiss T, Pan W, Petasis NA, Serhan CN, et al. Aspirin-triggered lipoxins override the apoptosis-delaying action of serum amyloid a in human neutrophils: a novel mechanism for resolution of inflammation. J Immunol. 2007;179:616–22.

    PubMed  CAS  Google Scholar 

  112. Godson C, Mitchell S, Harvey K, Petasis NA, Hogg N, Brady HR. Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J Immunol. 2000;164:1663–7.

    PubMed  CAS  Google Scholar 

  113. Newman SL, Henson JE, Henson PM. Phagocytosis of senescent neutrophils by human monocyte-derived macrophages and rabbit inflammatory macrophages. J Exp Med. 1982;156:430–42.

    PubMed  CAS  Google Scholar 

  114. Yamaryo T, Oishi K, Yoshimine H, Tsuchihashi Y, Matsushima K, Nagatake T. Fourteen-member macrolides promote the phosphatidylserine receptor-dependent phagocytosis of apoptotic neutrophils by alveolar macrophages. Antimicrob Agents Chemother. 2003;47:48–53.

    PubMed  CAS  Google Scholar 

  115. Fadok VA, Haslett JSC, Bratton DL, Doherty DE, Cambell PA, Henson PM. Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. J Immunol. 1992;149:4029–35.

    PubMed  CAS  Google Scholar 

  116. Mevorach D, Mascarenhas JO, Gershov D, Elkon KB. Complement-dependent clearance of apoptotic cells by human macrophages. J Exp Med. 1998;188:2313–20.

    PubMed  CAS  Google Scholar 

  117. Platt N, Suzuki H, Kurihara Y, Kodama T, Gordon S. Role of the class A macrophage scavenger receptor in the phagocytosis of apoptotic thymocytes in vitro. Proc Natl Acad Sci USA. 1996;93:12456–60.

    PubMed  CAS  Google Scholar 

  118. Savill J, Dransfield I, Hogg N, Haslett C. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature. 1990;343:170–3.

    PubMed  CAS  Google Scholar 

  119. Savill J, Hogg N, Ren Y, Haslett C. Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J Clin Invest. 1992;90:1513–22.

    PubMed  CAS  Google Scholar 

  120. Devitt A, Moffatt OD, Raykundalia C, Capra JD, Simmonda DL, Gregory CD. Human CD14 mediates recognition and phagocytosis of apoptotic cells. Nature. 1998;392:505–9.

    PubMed  CAS  Google Scholar 

  121. Hart SP, Dougherty GJ, Haslett C, Dransfield I. CD44 regulates phagocytosis of apoptotic neutrophil granulocytes, but not apoptotic lymphocytes, by human macrophages. J Immunol. 1997;159:919–25.

    PubMed  CAS  Google Scholar 

  122. Vivers S, Heasman SJ, Hart SP, Dransfield I. Divalent cation-dependent and -independent augmentation of macrophage phagocytosis of apoptotic neutrophils by CD44 antibody. Clin Exp Immunol. 2004;138:447–52.

    PubMed  CAS  Google Scholar 

  123. Vivers S, Dransfield I, Hart SP. Role of macrophage CD44 in the disposal of inflammatory cell corpses. Clin Sci. 2002;103:441–9.

    PubMed  CAS  Google Scholar 

  124. Park S-Y, Jung M-Y, Kim H-J, Lee S-J, Kim S-Y, Lee B-H, et al. Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor. Cell Death Diff. 2008;15:192–201.

    CAS  Google Scholar 

  125. Miyanishi M, Taka K, Koike M, Uchiyama Y, Kitamura T, Nagata S. Identification of Tim4 as a phosphatidylserine receptor. Nature. 2007;450:435–9.

    PubMed  CAS  Google Scholar 

  126. Li MO, Sarkisian MR, Mehal WZ, Rakic P, Flavell RA. Phosphatidylserine receptor is required for clearance of apoptotic cells. Science. 2003;302:1560–3.

    PubMed  CAS  Google Scholar 

  127. Fadok VA, Bratton DL, Rose DM, Pearson A, Ezekewitz RAB, Henson PM. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature. 2000;405:85–90.

    PubMed  CAS  Google Scholar 

  128. Arur S, Uche UE, Rezaqul K, Fong M, Scranton V, Cowan AE, et al. Annexin I is an endogenous ligand that mediates apoptotic cell engulfment. Dev Cell. 2003;4:587–98.

    PubMed  CAS  Google Scholar 

  129. Botto M, Dell’Agnola C, Bygrave AE, Thompson EM, Cook HT, Petry F, et al. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet. 1998;19:56–9.

    PubMed  CAS  Google Scholar 

  130. Thielens NM, Tacnet-Delorme P, Arlaud GJ. Interaction of C1q and mannan-binding lectin with viruses. Immunobiology. 2002;205:563–74.

    PubMed  CAS  Google Scholar 

  131. Ogden CA, Elkon KB. Role of complement and other innate immune mechanisms in the removal of apoptotic cells. Curr Dir Autoimmun. 2006;9:120–42.

    PubMed  CAS  Google Scholar 

  132. Taylor PR, Carugati A, Fadok VA, Cook HT, Andrews M, Carroll MC, et al. A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J Exp Med. 2000;192:359–66.

    PubMed  CAS  Google Scholar 

  133. Grevink ME, Horst G, Limburg PC, Kallenberg CGM, Bijl M. Levels of complement in sera from inactive SLE patients, although decreased, do not influence in vitro uptake of apoptotic cells. J Autoimmm. 2005;24:329–36.

    CAS  Google Scholar 

  134. Greenwalt DE, Lipsky RH, Ockenhouse CF, Ikeda H, Tandon NN, Jamieson GA. Membrane glycoprotein CD36: a review of its roles in adherence, signal transduction, and transfusion medicine. Blood. 1992;80:1105–15.

    PubMed  CAS  Google Scholar 

  135. Greenberg ME, Sun M, Zhang R, Febbraio M, Silverstein R, Hazen SL. Oxidized phosphatidylserin-CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells. J Exp Med. 2006;203:2613–25.

    PubMed  CAS  Google Scholar 

  136. Navazo MDP, Daviet L, Savill J, Ren Y, Leung LLK, McGregor JL. Identification of a domain (155–183) on CD36 implicated in the phagocytosis of apoptotic neutrophils. J Biol Chem. 1996;271:15381–5.

    PubMed  CAS  Google Scholar 

  137. Teder P, Vandivier RW, Jiang D, Liang J, Cohn L, Pure E, et al. Resolution of lung inflammation by CD44. Science. 2002;296:155–8.

    PubMed  CAS  Google Scholar 

  138. Wright SD, Ramos RA, Tobias PS, Ulevitch RT, Mathison JC. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science. 1990;249:1431–3.

    PubMed  CAS  Google Scholar 

  139. Moffat OD, Devitt A, Bell ED, Simmons DL, Gregory CD. Macrophage recognition of ICAM-3 on apoptotic leukocytes. J Immunol. 1999;162:6800–10.

    Google Scholar 

  140. Gregory CD. CD14-dependent clearance of apoptotic cells: relevance to the immune system. Curr Opin Immunol. 2000;12:27–34.

    PubMed  CAS  Google Scholar 

  141. Schlegel RA, Krahling S, Callahan MK, Williamson P. CD14 is a component of multiple recognition systems used by macrophages to phagocytose apoptotic lymphocytes. Cell Death Diff. 1999;6:583–92.

    CAS  Google Scholar 

  142. Bottcher A, Gaipl US, Furnrohr BG, Herrmann M, Girkontaite I, Kalden JR, et al. Involvement of phosphatidylserine, αvβ3, CD14, CD36, and complement C1q in the phagocytosis of primary necrotic lymphocytes by macrophages. Arth Rheum. 2006;54:927–38.

    CAS  Google Scholar 

  143. Savill J, Fadok V. Corpse clearance defines the meaning of cell death. Nature. 2000;407:784–8.

    PubMed  CAS  Google Scholar 

  144. Huynh M-L, Fadok VA, Henson PM. Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-β1 secretion and the resolution of inflammation. J Clin Invest. 2002;109:41–50.

    PubMed  CAS  Google Scholar 

  145. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine-paracrine mechanisms involving TGF-β, PGE2, and PAF. J Clin Invest. 1998;101:890–8.

    PubMed  CAS  Google Scholar 

  146. Lucas M, Stuart LM, Zhang A, Hodivala-Dilke K, Febbraio M, Silverstein R, et al. Requirements for apoptotic cell contact in regulation of macrophage responses. J Immunol. 2006;177:4047–54.

    PubMed  CAS  Google Scholar 

  147. Xing L, Remick DG. Neutrophils as firemen, production of anti-inflammatory mediators by neutrophils in a mixed cell environment. Cell Immunol. 2004;231:126–32.

    PubMed  CAS  Google Scholar 

  148. Bianchi SM, Dockrell DH, Renshaw SA, Sabroe I, Whyte MKB. Granulocyte apoptosis in the pathogenesis and resolution of lung disease. Clin Sci. 2006;110:293–304.

    PubMed  CAS  Google Scholar 

  149. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature. 1997;390:350–1.

    PubMed  CAS  Google Scholar 

  150. Liu Y, Cousin JM, Hughes J, Damme JV, Seckle JR, Haslette C, et al. Glucocorticoids promote nonphlogistic phagocytosis of apoptotic leukocytes. J Immunol. 1999;162:3639–46.

    PubMed  CAS  Google Scholar 

  151. Giles KM, Ross K, Rossi AG, Hotchin NA, Haslett C, Dransfield I. Glucocorticoid augmentation of macrophage capacity for phagocytosis of apoptotic cells is associated with reduced p130Cas expression, loss of paxillin/pyk2 phosphorylation, and high levels of active Rac. J Immunol. 2001;167:976–86.

    PubMed  CAS  Google Scholar 

  152. Thieringer R, Le Grand CB, Carbin L, Cai TQ, Wong B, Wright SD, et al. 11β-hydroxysteroid dehydrogenase type 1 is induced in human monocytes upon differentiation to macrophages. J Immunol. 2001;167:30–5.

    PubMed  CAS  Google Scholar 

  153. Gilmour JS, Coutinho AE, Cailhier J-F, Man TY, Clay M, Thomas G, et al. Local amplification of glucocorticoids by 11β-hydroxysteroid dehydrogenase type 1 promotes macrophage phagocytosis of apoptotic leukocytes. J Immunol. 2006;176:7605–11.

    PubMed  CAS  Google Scholar 

  154. Heasman SJ, Giles KM, Rossi AG, Allen JE, Haslett C, Dransfield I. Interferon γ suppresses glucocorticoid augmentation of macrophage clearance of apoptotic cells. Eur J Immunol. 2004;34:1752–61.

    PubMed  CAS  Google Scholar 

  155. Hotta K, Niwa M, Hara A, Ohno T, Wang X, Matsuno H, et al. The loss of susceptibility to apoptosis in exudated tissue neutrophils is associated with their nuclear factor-κB activation. Eur J Pharmacol. 2001;433:17–27.

    PubMed  CAS  Google Scholar 

  156. Daffern PJ, Jagels MA, Hugli TE. Multiple epithelial cell-derived factors enhance neutrophil survival; regulation by glucocorticoids and tumor necrosis factor-α. Am J Respir Cell Mol Biol. 1999;21:259–67.

    PubMed  CAS  Google Scholar 

  157. Kotone-Miyahara Y, Yamashita K, Lee K-K, Yonehara S, Uchiyama T, Sasada M, et al. Short-term delay of Fas-stimulated apoptosis by GM-CSF as a result of temporary suppression of FADD recruitment in neutrophils: evidence implicating phosphatidylinositol 3-kinase and MEK1-ERK1/2 pathways downstream of classical protein kinase C. J Leukoc Biol. 2004;76:1047–56.

    PubMed  CAS  Google Scholar 

  158. Larsen GL, Mitchell BC, Harper TB, Henson PM. The pulmonary response of C5a deficient mice to Pseudomonas aeruginosa. Am Rev Respir Dis. 1982;126:306–11.

    PubMed  CAS  Google Scholar 

  159. Perianayagam MC, Balakrishnan VS, Pereira BJ, Jaber BL. C5a delays apoptosis of human neutrophils via an extracellular signal-regulated kinase and Bad-mediated signalling pathway. Eur J Clin Invest. 2004;34:50–6.

    PubMed  CAS  Google Scholar 

  160. Tamura DY, Moore EE, Partrick DA, Johnson JL, Offner PJ, Silliman CC. Acute hypoxemia in humans enhances the neutrophil inflammatory response. Shock. 2002;17:269–73.

    PubMed  Google Scholar 

  161. Hannah S, Mecklenburgh K, Rahman I, Bellingan GJ, Greening A, Haslett C, et al. Hypoxia prolongs neutrophil survival in vitro. FEBS Lett. 1995;372:233–7.

    PubMed  CAS  Google Scholar 

  162. Molloy EJ, O’Neill AJ, Doyle BT, Grantham JJ, Taylor CT, Sheridan-Pereira M, et al. Effects of heat shock and hypoxia on neonatal neutrophil lipopolysaccharide responses: altered apoptosis, toll-like receptor-4 and CD11b expression compared with adults. Biol Neonate. 2006;90:34–9.

    PubMed  CAS  Google Scholar 

  163. Bellocchio S, Montagnoli C, Bozza S, Gaziano R, Rossi G, Mambula SS, et al. The contribution of the toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J Immunol. 2004;172:3059–69.

    PubMed  CAS  Google Scholar 

  164. Ehlenberger AG, Nussenzweig V. The role of membrane receptors for C3b and C3d in phagocytosis. J Exp Med. 1997;145:357–71.

    Google Scholar 

  165. Hayashi F, Means TK, Luster AD. Toll-like receptors stimulate human neutrophil function. Blood. 2003;102:2660–9.

    PubMed  CAS  Google Scholar 

  166. Takeda K, Akira S. Microbial recognition by toll-like receptors. J Dermatol Sci. 2004;34:73–82.

    PubMed  CAS  Google Scholar 

  167. Ahmad-Nejad P, Hacker H, Rutz M, Bauer S, Vabulas RM, Wagner H. Bacterial CpG-DNA and lipopolysaccharides activate toll-like receptors at distinct cellular compartments. Eur J Immunol. 2002;32:1958–68.

    PubMed  CAS  Google Scholar 

  168. Heil F, Ahmad-Nejad P, Hemmi H, Hochrein H, Ampenberger F, Gellert T, et al. The toll-like receptor 7 (TLR7)-specific stimulus loxoribine uncovers a strong relationship within the TLR7, 8, and 9 subfamily. Eur J Immunol. 2003;33:2987–97.

    PubMed  CAS  Google Scholar 

  169. Matsumoto M, Funami K, Tanabe M, Oshiumi H, Shingai M, Seto Y, et al. Subcellular localization of toll-like receptor 3 in human dendritic cells. J Immunol. 2003;171:3154–62.

    PubMed  CAS  Google Scholar 

  170. Sabroe I, Jones EC, Usher LR, Whyte MKB, Dower SK. Toll-like receptor (TLR)2 and TLR4 in human peripheral blood granulocytes: a critical role for monocytes in leukocyte lipopolysaccharide responses. J Immunol. 2002;168:4701–10.

    PubMed  CAS  Google Scholar 

  171. Sabroe I, Prince LR, Dower SK, Chilvers ER, Whyte MKB. What can we learn from highly purified neutrophils? Biochem Soc Trans. 2004;32:468–9.

    PubMed  CAS  Google Scholar 

  172. Watson RW, Rotstein OD, Parodo J, Bitar R, Marshall JC. The IL-1 beta-converting enzyme (caspase-1) inhibits apoptosis of inflammatory neutrophils through activation of IL-1 beta. J Immunol. 1998;161:957–62.

    PubMed  CAS  Google Scholar 

  173. Sabroe I, Prince LR, Jones EC, Horsburgh MJ, Foster SJ, Vogel SN, et al. Selective roles for Toll-like receptor (TLR)2 and TLR4 in the regulation of neutrophil activation and life span. J Immunol. 2003;170:5628–75.

    Google Scholar 

  174. Lotz S, Aga E, Wilde I, van Zandbergen G, Hartung T, Solbach W, et al. Highly purified lipoteichoic acid activates neutrophil granulocytes and delays their spontaneous apoptosis via CD14 and TLR2. J Leukoc Biol. 2004;75:467–77.

    PubMed  CAS  Google Scholar 

  175. Feterowski C, Wieighardt H, Emmanuilidis K, Hartung T, Holzmann B. Immune protection against septic peritonitis in endotoxin-primed mice is related to reduced neutrophil apoptosis. Eur J Immunol. 2001;31:1268–77.

    PubMed  CAS  Google Scholar 

  176. Borjesson DL, Kobayashi SD, Whitney AR, Voyich JM, Argue CM, DeLeo FR. Insights into pathogen immune evasion mechanisms: Anaplasma phagocytophilum fails to induce an apoptosis differentiation program in human neutrophils. J Immunol. 2005;174:6364–72.

    PubMed  CAS  Google Scholar 

  177. Kobayashi SD, Voyich JM, Braughton KR, DeLeo FR. Down-regulation of proinflammatory capacity during apoptosis in human polymorphonuclear leukocytes. J Immunol. 2003;170:3357–68.

    PubMed  CAS  Google Scholar 

  178. McDonald P, Russo MP, Ferrini S, Cassatella MA. Interleukin-15 (IL-15) induces NF-κB activation and IL-8 production in human neutrophils. Blood. 1998;92:4828–35.

    PubMed  CAS  Google Scholar 

  179. McDonald PP, Gasperini S, Calzetti F, Cassatella MA. Modulation of interferon-γ of the production and gene expression of IL-1 receptor antagonist in human neutrophils. Cell Immunol. 1998;184:45–50.

    PubMed  CAS  Google Scholar 

  180. McDonald PP, Bald A, Cassatella MA. Activation of the NF-κB pathway by inflammatory stimuli in human neutrophils. Blood. 1997;9:3421–33.

    Google Scholar 

  181. Cline MJ. Phagocytosis and synthesis of ribonucleic acid in human granulocytes. Nature. 1966;212:1431–3.

    CAS  Google Scholar 

  182. Watson RW, Redmond HP, Wang JH, Condron C, Bouchier-Hayes D. Neutrophils undergo apoptosis following ingestion of Escherichia coli. J Immunol. 1996;156:3986–92.

    PubMed  CAS  Google Scholar 

  183. Matsuda T, Saito H, Inoue T. Ratio of bacteria to polymorphonuclear neutrophils (PMNs) determines PMN fate. Shock. 1999;12:365–72.

    PubMed  CAS  Google Scholar 

  184. Perskvist N, Long M, Stendahl O, Zheng L. Mycobacterium tuberculosis promotes apoptosis in human neutrophils by activating caspase-3 and altering expression of Bax/Bcl-xL via an oxygen-dependent pathway. J Immunol. 2002;168:6358–65.

    PubMed  CAS  Google Scholar 

  185. Lundqvist-Gustafsson H, Norman S, Nilsson J, Wilsson A. Involvement of p38-mitogen-activated protein kinase in Staphylococcus aureus-induced neutrophil apoptosis. J Leukoc Biol. 2001;70:642–8.

    PubMed  CAS  Google Scholar 

  186. Weiss JP. Tissue destruction by neutrophils. N Engl J Med. 1989;320:365–76.

    PubMed  CAS  Google Scholar 

  187. Firestein GS. Immunologic mechanisms in the pathogenesis of rheumatoid arthritis. J Clin Rheumatol. 2005;11:39–44.

    Google Scholar 

  188. Kobayashi SD, Voyich JM, Braughton KR, Whitney AR, Nauseef WN, Malech HL, et al. Gene expression profiling provides insight into the pathophysiology of chronic granulomatous disease. J Immunol. 2004;172:636–43.

    PubMed  CAS  Google Scholar 

  189. Guide SV. Reinfection, rather than persistent infection, in patients with chronic granulomatous disease. J Infect Dis. 2003;187:845–53.

    PubMed  Google Scholar 

  190. Firestein GS. Inhibiting inflammation in rheumatoid arthritis. N Engl J Med. 2006;354:80–2.

    PubMed  CAS  Google Scholar 

  191. Rosenzweig SD, Holland SM. Phagocyte immunodeficiencies and their infections. J Allergy Clin Immunol. 2004;113:620–6.

    PubMed  CAS  Google Scholar 

  192. William R, Watson G, Redmond PH, Wang JH, Condron C, Bouchier-Hayes D. Neutrophils undergo apoptosis following ingestion of Escherichia coli. J Immunol. 1996;1996:3986–92.

    Google Scholar 

  193. Oishi K, Machida K. Inhibition of neutrophil apoptosis by antioxidants in culture medium. Scand J Immunol. 1997;45:21–7.

    PubMed  CAS  Google Scholar 

  194. Rollet-Labelle E, Grange MJ, Elbim C, Marquetty C, Gougerot-Pociadalo MA, Pasquier C. Hydroxyl radical as a potential intracellular mediator of polymorphonuclear neutrophil apoptosis. Free Rad Biol Med. 1998;24:563–72.

    PubMed  CAS  Google Scholar 

  195. Coxon A, Rieu P, Barkalow FJ, Askari S, Sharpe AH, von Andrian UH, et al. A novel role for the β2 integrin CD11b/CD18 in neutrophil apoptosis: a homeostatic mechanism in inflammation. Immunity. 1996;5:653–66.

    PubMed  Google Scholar 

  196. Gamberale R, Giordano M, Trevani AS, Andonegui G, Geffner JR. Modulation of human neutrophil apoptosis by immune complexes. J Immunol. 1998;161:3666–74.

    PubMed  CAS  Google Scholar 

  197. Ottonello L, Frumento G, Arduino N, Dapino P, Tortolina G, Dallegri F. Immune complex stimulation of neutrophil apoptosis: investigating the involvement of oxidative and nonoxidative pathways. Free Rad Biol Med. 2001;30:161–9.

    PubMed  CAS  Google Scholar 

  198. Schettini J, Salamone G, Trevani A, Raiden S, Gamberale R, Vermeulen M, et al. Stimulation of neutrophil apoptosis by immobilized IgA. J Leukoc Biol. 2002;72:685–91.

    PubMed  CAS  Google Scholar 

  199. Nauseef WM, Clark RA. Basic principles in the diagnosis and management of infectious diseases. In: Mandell GL, Bennett JE, Dolin R, editors. Granulocytes. New York: Churchill Livingstone; 2000. p. 89–112.

    Google Scholar 

  200. Simons MP, Nauseef WM, Griffith TS, Apicella MA. Neisseria gonorrhoeae delays the onset of apoptosis in polymorphonuclear leukocytes. Cell Microbiol. 2006;8:1780–90.

    Google Scholar 

  201. Tsurubuchi T, Aratani Y, Maeda N, Koyama H. Retardation of early-onset PMA-induced apoptosis in mouse neutrophils deficient in myeloperoxidase. J Leukoc Biol. 2001;70:52–8.

    PubMed  CAS  Google Scholar 

  202. Hampton MB, Vissers MCM, Keenan JI, Winterbourn CC. Oxidant-mediated phosphatidylserine exposure and macrophage uptake of activated neutrophils: possible impairment in chronic granulomatous disease. J Leukoc Biol. 2002;71:775–81.

    PubMed  CAS  Google Scholar 

  203. Liles WC, Thomsen AR, O’Mahoney DS, Klebanoff SJ. Stimulation of human neutrophils and monocytes by staphylococcal phenol-soluble modulin. J Leukoc Biol. 2001;70:96–102.

    PubMed  CAS  Google Scholar 

  204. Moulding DA, Walter C, Hart CA, Edwards SW. Effects of staphylococcal enterotoxins on human neutrophil functions and apoptosis. Infect Immun. 1999;67:2312–8.

    PubMed  CAS  Google Scholar 

  205. Hofman V, Ricci V, Mograbi B, Brest P, Luciano F, Boquet P, et al. Helicobacter pylori lipopolysaccharide hinders polymorphonuclear leucocyte apoptosis. Lab Invest. 2001;81:375–84.

    PubMed  CAS  Google Scholar 

  206. Liu J, Akahoshi t, Sasahana T, Kitasato H, Namai R, Sasaki T, et al. Inhibition of neutrophil apoptosis by verotoxin 2 derived from Escherichia coli O157:H7. Infect Immun. 1999;67:6203–5.

    PubMed  CAS  Google Scholar 

  207. Engelich G, White M, Hartshorn KL. Neutrophil survival is markedly reduced by incubation with influenza virus and Streptococcus pneumoniae: role of respiratory burst. J Leukoc Biol. 2001;69:50–6.

    PubMed  CAS  Google Scholar 

  208. Watson RW, Redmond HP, Wang JH, Bouchier-Hayes D. Bacterial ingestion, tumor necrosis factor-alpha, and heat induce programmed cell death in activated neutrophils. Shock. 1996;5:47–51.

    Article  PubMed  CAS  Google Scholar 

  209. Mayer-Scholl A, Averhoff P, Zychlinsky A. How do neutrophils and pathogens interact? Curr Opin Cell Microbiol. 2004;7:62–6.

    CAS  Google Scholar 

  210. Aleman M, Garcia A, Saab MA, De La Barrera SS, Finiasz M, Abbate E, et al. Mycobacterium tuberculosis-induced activation accelerates apoptosis in peripheral blood neutrophils from patients with active tuberculosis. Am J Respir Cell Mol Biol. 2002;27:583–92.

    PubMed  CAS  Google Scholar 

  211. Zysk G, Gejo L, Schneider-Wald BK, Nau R, Heinz H. Induction of necrosis and apoptosis of neutrophil granulocytes by Streptococcus pneumoniae. Clin Exp Immunol. 2000;122:61–6.

    PubMed  CAS  Google Scholar 

  212. Voyich JM, Braughton KR, Sturdevant DE, Whitney AR, Said-Salim B, Porcella SF, et al. Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J Immunol. 2005;175:3907–19.

    PubMed  CAS  Google Scholar 

  213. Voyich JM, Otto M, Mathema B, Braughton KR, Whitney AR, Welty D, et al. Is Panton-Valentine Leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease? J Infect Dis. 2006;194:1761–70.

    PubMed  CAS  Google Scholar 

  214. Genestier A-L, Michallet M-C, Prevost G, Bellot G, Chalabreysse L, Peyrol S, et al. Staphylococcus aureus panton-valentine leukocidin directly targets mitochondria and induced Bax-independent apoptosis of human neutrophils. J Clin Invest. 2005;115:3117–27.

    PubMed  CAS  Google Scholar 

  215. Fridkin SK, Hageman JC, Morrison M, Sanza LT, Como-Sabetti K, Jernigan JA, et al. Methicillin-resistant Staphylococcus aureus disease in three communities. N Engl J Med. 2005;352:1436–44.

    PubMed  CAS  Google Scholar 

  216. Miller LG, Perdreau-Remington F, Rieg G, Mehdi S, Perlroth J, Bayer AS, et al. Necrotizing fasciitis caused by community-associated methicillin-resistant staphylococcus aureus in Los Angeles. N Engl J Med. 2005;352:1445–53.

    PubMed  CAS  Google Scholar 

  217. Musser JM, DeLeo FR. Toward a genome-wide systems biology analysis of host-pathogen interactions in group A Streptococcus. Am J Path. 2005;167:1461–72.

    PubMed  CAS  Google Scholar 

  218. Voyich JM, Musser JM, DeLeo FR. Streptococcus pyogenes and human neutrophils: a paradigm for evasion of innate host defense by bacterial pathogens. Microbes Infect. 2004;6:1117–23.

    PubMed  Google Scholar 

  219. Voyich JM, Braughton KR, Sturdevant DE, Vuong C, Kobayashi SD, Porcella SF, et al. Engagement of the pathogen survival response used by group A streptococcus to avert destruction by innate host defense. J Immunol. 2004;173:1194–201.

    PubMed  CAS  Google Scholar 

  220. Miyoshi-Akiyama T, Takamatsu D, Koyanagi M, Zhao J, Imanishi K, Uchiyama T. Cytocidal effect of Streptococcus pyogenes on mouse neutrophils in vivo and the critical role of streptolysin S. J Infect Dis. 2005;192:107–16.

    PubMed  Google Scholar 

  221. Ge Y, Rikihisa Y. Anaplasma phagocytophilum delays spontaneous human neutrophil apoptosis by modulation of multiple apoptotic pathways. Cell Micro. 2006;8:1406–16.

    CAS  Google Scholar 

  222. Lee HC, Goodman JL. Anaplasma phagocytophilum causes global induction of antiapoptosis in human neutrophils. Genomics. 2006;88:496–503.

    PubMed  CAS  Google Scholar 

  223. Scaife H, Woldehiwet Z, Hart CA, Edwards SW. Anaplasma phagocytophilum reduces neutrophil apoptosis in vivo. Infect Immun. 2003;71:1995–2001.

    PubMed  CAS  Google Scholar 

  224. van Zandbergen G, Gieffers J, Kothe H, Rupp J, Bollinger A, Aga E, et al. Chlamydia pneumoniae multiply in neutrophil granulocytes and delay their spontaneous apoptosis. J Immunol. 2004;172:1768–76.

    PubMed  Google Scholar 

  225. Yoshiie K, Kim HY, Mott J, Rikihisa Y. Intracellular infection by the human granulocyte Ehrlichiosis agent inhibits human neutrophil apoptosis. Infect Immun. 2000;68:1125–33.

    PubMed  CAS  Google Scholar 

  226. Carlyon JA, Latif DA, Pypaert M, Lacy P, Fikrig E. Anaplasma phagocytophilum utilizes multiple host evasion mechanisms to thwart NADPH oxidase-mediated killing during neutrophil infection. Infect Immun. 2004;72:4772–83.

    PubMed  CAS  Google Scholar 

  227. Webster P, Ijdo JW, Chicoine LM, Fikrig E. The agent of human granulocytic ehrlichiosis resides in an endosomal compartment. J Clin Invest. 1998;101:1932–41.

    PubMed  CAS  Google Scholar 

  228. Ijdo JW, Mueller AC. Neutrophil NADPH oxidase is reduced at the Anaplasma phagocyophilum phagosome. Infect Immun. 2004;72:5392–401.

    PubMed  CAS  Google Scholar 

  229. Mott J, Rikihisa Y, Tsunawaki S. Effects of Anaplasma phagocytophila on NADPH oxidase components in human neutrophils and HL-60 cells. Infect Immun. 2002;70:1359–66.

    PubMed  CAS  Google Scholar 

  230. Ge Y, Yoshiie K, Kuribayashi F, Lin M, Rikihisa Y. Anaplasma phagocytophilum inhibits human neutrophil apoptosis via upregulation of bfl-1, maintenance of mitochondrial membrane potential and prevention of caspase 3 activation. Cell Microbiol. 2005;7:29–38.

    PubMed  CAS  Google Scholar 

  231. Airenne S, Surcel HM, Tuukkanen J, Leinonen M, Saikku P. Chlamydia pneumoniae inhibits apoptosis in human epithelial and monocyte cell lines. Scand J Immunol. 2002;55:390–8.

    PubMed  CAS  Google Scholar 

  232. Rossi AG, Sawatzky DA, Walker A, Ward C, Sheldrake TA, Riley NA, et al. Cyclin-dependent kinase inhibitors enhance the resolution of inflammation by promoting inflammatory cell apoptosis. Nat Med. 2006;12:1056–64.

    PubMed  CAS  Google Scholar 

  233. Levin S, Bucci TJ, Cohen SM, Fix AS, Hardisty JF, Legrand EK, et al. The nomenclature of cell death: recommendations of an ad hoc committee of the society of toxicologic pathologists. Toxicol Pathol. 1999;27:490.

    Google Scholar 

  234. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med. 1997;185:1481–6.

    PubMed  CAS  Google Scholar 

  235. Kostin S, Pool L, Elsasser A, Hein S, Drexler HCA, Arnon E, et al. Myocytes die by multiple mechanisms in failing human hearts. Circ Res. 2003;92:715–24.

    PubMed  CAS  Google Scholar 

  236. Grasl-Kraupp B, Ruttkay-Nedecky B, Koudelka H, Bukowska K, Bursch W, Schulte-Hermann R. In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology. 1995;21:1465–8.

    PubMed  CAS  Google Scholar 

  237. Lecoeur H, Prevost M-C, Gougeon M-L. Oncosis is associated with exposure of phosphatidylserine residues on the outside layer of the plasma membrane: a reconsideration of the specificity of the annexin V/propidium iodide assay. Cytometry. 2001;44:65–72.

    PubMed  CAS  Google Scholar 

  238. Krysko O, de Ridder L, Cornelissen M. Phosphatidylserine exposure during early primary necrosis (oncosis) in JB6 cells as evidenced by immunogold labeling technique. Apoptosis. 2004;9:495–500.

    PubMed  CAS  Google Scholar 

  239. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H, et al. ER stress (PERK/eIF2α phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Diff. 2007;14:230–9.

    CAS  Google Scholar 

  240. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 1999;402:672–6.

    PubMed  CAS  Google Scholar 

  241. Yu L, Alva A, Su H, Dutt P, Freundt E, Welsh S, et al. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science. 2004;304:1500–2.

    PubMed  CAS  Google Scholar 

  242. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy. 2008;4:151–75.

    PubMed  CAS  Google Scholar 

  243. Saftig P, Beersten W, Eskelinen E-L. LAMP-2: a control step for phagosome and autophagosome maturation. Autophagy. 2008;4:510–2.

    Google Scholar 

  244. Fink SL, Cookson BT. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol. 2006;8:1812–25.

    PubMed  CAS  Google Scholar 

  245. Shao W, Yeretssian G, Doiron K, Hussain SN, Saleh M. The caspase-1 digestome identifies the glycolysis pathway as a target during infection and septic shock. J Biol Chem. 2007;282:36321–9.

    PubMed  CAS  Google Scholar 

  246. Kanneganti T-D, Lamkanfi M, Nunez G. Intracellular NOD-like receptors in host defense and disease. Immunity. 2007;27:549–59.

    PubMed  CAS  Google Scholar 

  247. Fernandes-Alnemri T, Wu J, Yu J-W, Datta P, Miller B, Jankowski W, et al. The pyroptosome: a supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation. Cell Death Diff. 2007;14:1590–604.

    CAS  Google Scholar 

  248. Mariathasan S, Weiss DS, Newton K, McBride J, O’Rourke K, Roose-Girma M, et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature. 2006;440:228–32.

    PubMed  CAS  Google Scholar 

  249. Suzuki T, Franchi L, Toma C, Ashida H, Ogawa M, Yoshikawa Y, et al. Differential regulation of caspase-1 activation, pyroptosis, and autophagy via ipaf and ASC in Shigella-infected macrophages. PLoS Pathog. 2007;3:e111.

    Google Scholar 

  250. Henry T, Monack DM. Activation of the inflammasome upon Francisella tularensis infection: interplay of innate immune pathways and virulence factors. Cell Microbiol. 2007;9:2543–51.

    PubMed  CAS  Google Scholar 

  251. Cervantes J, Nagata T, Uchijima M, Shibata K, Koide Y. Intracytosolic listeria monocytogenes induces cell death through caspase-1 activation in murine macrophages. Cell Microbiol. 2008;10:41–52.

    PubMed  CAS  Google Scholar 

  252. Bergsbaken T, Cookson BT. Macrophage activation redirects Yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis. PLoS Path. 2007;3:1570–82.

    CAS  Google Scholar 

  253. Fink SL, Bergsbaken T, Cookson BT. Anthrax lethal toxin and Salmonella elicit the common cell death pathway of caspase-1-dependent pyroptosis via distinct mechanisms. Proc Natl Acad Sci USA. 2008;105:4312–7.

    PubMed  CAS  Google Scholar 

  254. Fink SL, Cookson BT. Pyroptosis and host cell death responses during Salmonella infection. Cell Microbiol. 2007;9:2562–70.

    PubMed  CAS  Google Scholar 

  255. Trump BF, Berezesky IK. The role of altered [Ca2+]i regulation in apoptosis, oncosis, and necrosis. Biochem Biophys Acta. 1996;1313:173–8.

    PubMed  Google Scholar 

  256. Perez JF, Chemello ME, Liprandi F, Ruiz M-C, Michelangeli F. Oncosis in MA104 cells is induced by rotavirus infection through an increase in intracellular Ca2+ concentration. Virology. 1998;252:17–27.

    PubMed  CAS  Google Scholar 

  257. Pei J, Turse JE, Wu O, Ficht TA. Brucella abortus rough mutants induce macrophage oncosis that requires bacterial protein synthesis and direct interaction with the macrophage. Infect Immun. 2006;74:2667–75.

    PubMed  CAS  Google Scholar 

  258. Kalischuk LD, Inglis GD, Buret AG. Strain-dependent induction of epithelial cell oncosis by Campylobacter jejuni, is correlated with invasion ability and is independent of cytolethal distending toxin. Microbiology. 2007;153:2952–63.

    PubMed  CAS  Google Scholar 

  259. Dacheux D, Toussaint B, Richard M, Brochier G, Croize J, Attree I. Pseudomonas aeruginosa cystic fibrosis isolates induced rapid, type III secretion-dependent, but ExoU-independent, oncosis on macrophages and polymorphonuclear neutrophils. Infect Immun. 2000;68:2916–24.

    PubMed  CAS  Google Scholar 

  260. Sano G-I, Takada Y, Goto S, Maruyama K, Shindo Y, Oka K, et al. Flagella facilitate escape of Salmonella from oncotic macrophages. J Bacteriol. 2007;189:8224–32.

    PubMed  CAS  Google Scholar 

  261. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, et al. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol. 2007;176:231–41.

    PubMed  CAS  Google Scholar 

  262. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303:1532–5.

    PubMed  CAS  Google Scholar 

  263. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007;13:463–9.

    PubMed  CAS  Google Scholar 

  264. Buchanan JT, Simpson AJ, Aziz RK, Liu GY, Kristian SA, Kotb M, et al. DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr Biol. 2006;16:396–400.

    PubMed  CAS  Google Scholar 

  265. Choi K-S, Park JT, Dumler JS. Anaplasma phagocytophilum delay of neutrophil apoptosis through the p38 mitogen-activated protein kinase signal pathway. Infect Immun. 2005;73:8209–18.

    PubMed  CAS  Google Scholar 

  266. Abramson T, Kedem H, Relman DA. Proinflammatory and proapoptotic activities associated with Bordetella pertussis filamentous hemagglutinin. Infect Immun. 2001;69:2650–8.

    PubMed  CAS  Google Scholar 

  267. Basler M, Masin J, Osicka R, Sebo P. Pore-forming and enzymatic activities of Bordetella pertussis adenylate cyclase toxin synergize in promoting lysis of monocytes. Infect Immun. 2006;74:2207–14.

    PubMed  CAS  Google Scholar 

  268. Gueirard P, Druilhe A, Pretolani M, Guiso N. Role of adenylate cyclase-hemolysin in alveolar macrophage apoptosis during Bordetella pertussis infection in vivo. Infect Immun. 1998;66:1718–25.

    PubMed  CAS  Google Scholar 

  269. Khelef N, Zychlinsky A, Guiso N. Bordetella pertussis induces apoptosis in macrophages: role of adenylate cyclase hemolysin. Infect Immun. 1993;61:4064–71.

    PubMed  CAS  Google Scholar 

  270. Khelef N, Guiso N. Induction of macrophage apoptosis by Bordetella pertussis adenylate cyclase-hemolysin. FEMS Microbiol Lett. 1995;134:27–32.

    PubMed  CAS  Google Scholar 

  271. Khelef N, DeShazer D, Friedman RL, Guiso N. In vivo and in vitro analysis of Bordetella pertussis catalase and Fe-superoxide dismutase mutants. FEMS Microbiol Lett. 1996;142:231–5.

    PubMed  CAS  Google Scholar 

  272. Khelef N, Gounon P, Guiso N. Internalization of Bordetella pertussis adenylate cyclase-hemolysin into endocytic vesicles contributes to macrophage cytotoxicity. Cell Microbiol. 2001;3:721–30.

    PubMed  CAS  Google Scholar 

  273. Harvill ET, Cotter PA, Miller JF. Pregenomic comparative analysis between Bordetella bronchiseptica RB50 and Bordetella pertussis tohama I in murine models of respiratory tract infection. Infect Immun. 1999;67:6109–18.

    PubMed  CAS  Google Scholar 

  274. Boyd AP, Ross PJ, Conroy H, Mahon N, Lavelle EC, Mills KHG. Bordetella pertussis adenylate cyclase toxin modulates innate and adaptive immune responses: distinct roles for acylation and enzymatic activity in immunomodulation and cell death. J Immunol. 2005;175:730–8.

    PubMed  CAS  Google Scholar 

  275. Bylund J, Campsall PA, Ma RC, Conway BA, Speert DP. Burkholderia cenocepacia induces neutrophil necrosis in chronic granulomatous disease. J Immunol. 2005;174:3562–9.

    PubMed  CAS  Google Scholar 

  276. Hutchison ML, Poxton IR, Govan JR. Burkholderia cepacia produces a hemolysin that is capable of inducing apoptosis and degranulation of mammalian phagocytes. Infect Immun. 1998;66:2033–9.

    PubMed  CAS  Google Scholar 

  277. Punj V, Sharma R, Zaborina O, Chakrabarty AM. Energy-generating enzymes of Burkholderia cepacia and their interactions with macrophages. J Bacteriol. 2003;185:3167–78.

    PubMed  CAS  Google Scholar 

  278. Carratelli CR, Rizzo A, Catania MR, Galle F, Losi E, Hasty DL, et al. Chlamydia pneumoniae infections prevent the programmed cell death of THP-1 cell line. FEMS Microbiol Lett. 2002;215:69–74.

    PubMed  CAS  Google Scholar 

  279. Miyairi I, Byrne GI. Chlamydia and programmed cell death. Curr Opin Microbiol. 2006;9:102–8.

    PubMed  CAS  Google Scholar 

  280. Yaraei K, Campbell LA, Zhu X, Liles WC, Kuo C-C, Rosenfeld ME. Chlamydia pneumoniae augments the oxidized low-density lipoprotein-induced death of mouse macrophages by a caspase-independent pathway. Infect Immun. 2005;73:4315–22.

    PubMed  CAS  Google Scholar 

  281. Goth SR, Stephens RS. Rapid, transient phosphatidylserine externalization induced in host cells by infection with Chlamydia spp. Infect Immun. 2001;69:1109–19.

    PubMed  CAS  Google Scholar 

  282. Ying S, Seiffert BM, Hacker G, Fischer SF. Broad degradation of proapoptotic proteins with the conserved Bcl-2 homology domain 3 during infection with Chlamydia trachomatis. Infect Immun. 2005;73:1399–403.

    PubMed  CAS  Google Scholar 

  283. Mahida YR, Galvin A, Makh S, Hyde S, Sanfilippo L, Borriello SP, et al. Effect of Clostridium difficile toxin A on human colonic lamina propria cells: early loss of macrophages followed by T-cell apoptosis. Infect Immun. 1998;66:5462–9.

    PubMed  CAS  Google Scholar 

  284. Solomon K, Webb J, Ali N, Robins RA, Mahida YR. Highly sensitive to Clostridium difficile toxin A-induced apoptotic and nonapoptotic cell death. Infect Immun. 2005;73:1625–34.

    PubMed  CAS  Google Scholar 

  285. Brest P, Betis F, Cuburu N, Selva E, Herrant M, Servin A, et al. Increased rate of apoptosis and diminished phagocytic ability of human neutrophils infected with Afa/Dr diffusely adhering Escherichia coli strains. Infect Immun. 2004;72:5741–9.

    PubMed  CAS  Google Scholar 

  286. Fernandez-Prada C, Tall BD, Elliott SE, Hoover DL, Nataro JP, Venkatesan MM. Hemolysin-positive enteroaggregative and cell-detaching Escherichia coli strains cause oncosis of human monocyte-derived macrophages and poptosis of murine J774 cells. Infect Immun. 1998;66:3918–24.

    PubMed  CAS  Google Scholar 

  287. Hacker H, Furmann C, Wagner H, Hacker G. Caspase-9/-3 activation and apoptosis are induced in mouse macrophages upon ingestion and digestion of Escherichia coli bacteria. J Immunol. 2002;169:3172–9.

    PubMed  CAS  Google Scholar 

  288. Lai XH, Arencibia I, Johansson A, Wai SN, Oscarsson J, Kalfas S, et al. Cytocidal and apoptotic effects of the ClyA protein from Escherichia coli on primary and cultured monocytes and macrophages. Infect Immun. 2000;68:4363–7.

    PubMed  CAS  Google Scholar 

  289. Lai XH, Xu JG, Melgar S, Uhlin BE. An apoptotic response by J774 macrophage cells is common upon infection with diarrheagenic Escherichia coli. FEMS Microbiol Lett. 2006;172:29–34.

    Google Scholar 

  290. Rodrigues VS, Vidotto MC, Felipe I, Santos DS, Gaziri LC. Apoptosis of murine peritoneal macrophages induced by an avian pathogenic strain of Escherichia coli. FEMS Microbiol Lett. 1999;179:73–8.

    PubMed  CAS  Google Scholar 

  291. Stravodimos KG, Singhal PC, Sharma S, Reddy K, Smith AD. Escherichia coli promotes macrophage apoptosis. J Endourol. 1999;13:273–7.

    PubMed  CAS  Google Scholar 

  292. Yagi Y, Shiono H, Shibahara T, Chikayama Y, Makamura I, Ohnuma A. Increase in apoptotic polymorphonuclear neutrophils in peripheral blood after intramammary infusion of Escherichia coli lipopolysaccharide. Vet Immunol Immunopathol. 2002;89:115–25.

    PubMed  CAS  Google Scholar 

  293. Gille C, Leiber A, Spring B, Kempf VAJ, Loeffler J, Poets C, et al. Diminished phagocytosis-induced cell death (PICD) in neonatal monocytes upon infection with Escherichia coli. Pediatr Res. 2008;63:33–8.

    Article  PubMed  Google Scholar 

  294. Narayanan S, Stewart GC, Chengappa MM. Fusobacterium necrophorum leukotoxin induces activation and apoptosis of bovine leukocytes. Infect Immun. 2002;70:4609–20.

    PubMed  CAS  Google Scholar 

  295. Jewett A, Hume WR, Le H, Huynh TN, Han YW, Cheng G, et al. Induction of apoptotic cell death in peripheral blood mononuclear and polymorphonuclear cells by an oral bacterium, Fusobacterium nucleatum. Infect Immun. 2000;68:1893–8.

    PubMed  CAS  Google Scholar 

  296. Yang YF, Sylte MJ, Czuprynski CJ. Apoptosis: a possible tactic of Haemophilus somnus for evasion of killing by bovine neutrophils? Microb Pathog. 1998;24:351–9.

    PubMed  CAS  Google Scholar 

  297. Betten A, Bylund J, Cristophe T, Boulay F, Romero A, Hellstrand K, et al. A proinflammatory peptide from Helicobacter pylori activates monocytes to induce lymphocyte dysfunction and apoptosis. J Clin Invest. 2001;108:1221–8.

    PubMed  CAS  Google Scholar 

  298. Das S, Suarez G, Beswick EJ, Sierra JC, Graham DY, Reyes VE. Expression of B7-H1 on Gastric epithelial cells: its potential role in regulating T cells during Helicobacter pylori Infection. J Immunol. 2006;176:3000–9.

    PubMed  CAS  Google Scholar 

  299. Gobert aP, Cheng Y, Wang JY, Boucher JL, Iyer RK, Cederbaum SD, et al. Helicobacter pylori induces macrophage apoptosis by activation of arginase II. J Immunol. 2002;168:4692–700.

    PubMed  CAS  Google Scholar 

  300. Kim JS, Kim JM, Jung HC, Song IS, Kim CY. Inhibition of apoptosis in human neutrophils by Helicobacter pylori water-soluble surface proteins. Scand J Gastroenterol. 2001;36:589–600.

    PubMed  CAS  Google Scholar 

  301. Barsig J, Kaufmann SH. The mechanism of cell death in Listeria monocytogenes-infected murine macrophages is distinct form apoptosis. Infect Immun. 1997;65:4075–81.

    PubMed  CAS  Google Scholar 

  302. Guzman CA, Domann E, Rohde M, Bruder D, Darji A, Weiss S, et al. Apoptosis of mouse dendritic cells is triggered by listeriolysin, the major virulence determinant of Listeria monocytogenes. Mol Microbiol. 1996;20:119–26.

    PubMed  CAS  Google Scholar 

  303. Vadyvaloo V, Arous S, Gravesen A, Hechard Y, Chauhan-Haubrock R, Hastings JW, et al. Cell-surface alteration in class IIa bacteriocin-resistant Listeria monocytogenes strains. Microbiology. 2004;150:3025–33.

    PubMed  CAS  Google Scholar 

  304. Warren SE, Mao DP, Rodriguez AE, Miao EA, Aderem A. Multiple Nod-like receptors activate caspase 1 during Listeria monocytogenes infection. J Immunol. 2008;180:7558–64.

    PubMed  CAS  Google Scholar 

  305. Zwaferink H, Stockinger S, Reipert S, Decker T. Stimulation of inducible nitric oxide synthase expression by beta interferon increases necrotic death of macrophages upon Listeria monocytogenes infection. Infect Immun. 2008;76:1649–56.

    PubMed  CAS  Google Scholar 

  306. Birmingham CL, Higgins DE, Brumell JH. Avoiding death by autophagy: interactions of listeria monocytogenes with the macrophage autophagy system. Autophagy. 2008;4:368–71.

    PubMed  Google Scholar 

  307. Cudd LA, Ownby CL, Clarke CR, Sun Y, Clinkenbeard KD. Effects of Mannheimia haemolytica leukotoxin on apoptosis and oncosis of bovine neutrophils. Am J Vet Res. 2001;62:136–41.

    PubMed  CAS  Google Scholar 

  308. Stevens PK, Czuprynski CJ. Pasteurella haemolytica leukotoxin induces bovine leukocytes to undergo morphologic changes consistent with apoptosis in vitro. Infect Immun. 1996;64:2687–94.

    PubMed  CAS  Google Scholar 

  309. Thumbikat P, Dileepan T, Kannan MS, Maheswaran SK. Mechanisms underlying Mannheimia haemolytica leukotoxin-induced oncosis and apoptosis of bovine alveolar macrophages. Microb Pathog. 2005;38:161–72.

    PubMed  CAS  Google Scholar 

  310. Ahmad A, Khan M, Raykundalia C, Catty D. Study of the mechanisms of killing of Mycobacterium bovis BCG by apoptosis in J774 murine macrophages. J Pak Med Assoc. 1999;49:273–8.

    PubMed  CAS  Google Scholar 

  311. Gutierrez-Pabello JA, McMurray DN, Adams LG. Upregulation of thymosin beta-10 by Mycobacterium bovis infection of bovine macrophages is associated with apoptosis. Infect Immun. 2002;70:2121–7.

    PubMed  CAS  Google Scholar 

  312. Kremer L, Estaquier J, Brandt E, Ameisen JC, Locht C. Mycobacterium bovis Bacillus Calmette Guerin infection prevents apoptosis of resting human monocytes. Eur J Immunol. 1997;27:2450–6.

    PubMed  CAS  Google Scholar 

  313. Suttmann H, Lehan N, Bohle A, Brandau S. Stimulation of neutrophil granulocytes with Mycobacterium bovis bacillus Calmette-Guerin induces changes in phenotype and gene expression and inhibits spontaneous apoptosis. Infect Immun. 2003;71:4647–56.

    PubMed  CAS  Google Scholar 

  314. Krzyzowska M, Schollenberger A, Pawlowski A, Hamasur B, Winnicka A, Augustynowicz-Kopec E, et al. Lipoarabinomannan as a regulator of the monocyte apoptotic response to Mycobacterium bovis BCG Danish strain 1331 infection. Pol J Microbiol. 2007;56:89–96.

    PubMed  CAS  Google Scholar 

  315. Vega-Manriquez X, Lopez-Vidal Y, Moran J, Adams LG, Gutierrez-Pabello JA. Apoptosis-inducing factor participation in bovine macrophage Mycobacterium bovis-induced caspase-independent cell death. Infect Immun. 2007;75:1223–8.

    PubMed  CAS  Google Scholar 

  316. Aleman M, Schierloh P, De La Barrera SS, Musella RM, Saab MA, Baldini M, et al. Mycobacterium tuberculosis triggers apoptosis in peripheral neutrophils involving toll-like receptor 2 and p38 mitogen protein kinase in tuberculosis patients. Infect Immun. 2004;72:5150–8.

    PubMed  CAS  Google Scholar 

  317. Ciaramella A, Martino A, Cicconi R, Colizzi V, Fraziano M. Mycobacterial 19-kDa lipoprotein mediates Mycobacterium tuberculosis-induced apoptosis in monocytes/macrophages at early stages of infection. Cell Death Diff. 2000;7:1270–2.

    CAS  Google Scholar 

  318. Ciaramella A, Cavone A, Santucci MB, Amicosante M, Martino A, Auricchio G, et al. Proinflammatory cytokines in the course of Mycobacterium tuberculosis-induced apoptosis in monocytes/macrophages. J Infect Dis. 2002;186:1277–82.

    PubMed  CAS  Google Scholar 

  319. Danelishvili L, McGarvey J, Li YJ, Bermudez LE. Mycobacterium tuberculosis infection causes different levels of apoptosis and necrosis in human macrophages and alveolar epithelial cells. Cell Microbiol. 2003;5:649–60.

    PubMed  CAS  Google Scholar 

  320. Duan L, Gan H, Arm J, Remold HG. Cytosolic phospholipase A2 participates with TNF-alpha in the induction of apoptosis of human macrophages infected with Mycobacterium tuberculosis H37Ra. J Immunol. 2001;166:7469–76.

    PubMed  CAS  Google Scholar 

  321. Duan L, Gan H, Golan DE, Remold HG. Critical role of mitochondrial damage in determining outcome of macrophage infection with Mycobacterium tuberculosis. J Immunol. 2002;169:5181–7.

    PubMed  Google Scholar 

  322. Durrbaum-Landmann I, Gercken J, Flad HD, Ernst M. Effect of in vitro infection of human monocytes with low numbers of Mycobacterium tuberculosis bacteria on monocytes apoptosis. Infect Immun. 1996;64:5384–9.

    PubMed  CAS  Google Scholar 

  323. Kasahara K, Sato I, Ogura K, Takeuchi H, Kobayashi K, Adachi M. Expression of chemokines and induction of rapid cell death in human blood neutrophils by Mycobacterium tuberculosis. J Infect Dis. 1998;178:127–37.

    PubMed  CAS  Google Scholar 

  324. Keane J, Balcewicz-Sablinska MK, Remold HG, Chupp GL, Meek BB, Fenton MJ, et al. Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect Immun. 1997;65:298–304.

    PubMed  CAS  Google Scholar 

  325. Keane J, Remold HG, Kornfeld H. Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol. 2000;164:2016–20.

    PubMed  CAS  Google Scholar 

  326. Keane J, Shurtleff B, Kornfeld H. TNF-dependent BALB/c murine macrophage apoptosis following Mycobacterium tuberculosis infection inhibits bacillary growth in an IFN-gamma independent manner. Tuberculosis. 2002;82:55–61.

    PubMed  CAS  Google Scholar 

  327. Lopez M, Sly LM, Luu Y, Young D, Cooper H, Reiner NE. The 19-kDa Mycobacterium tuberculosis protein induces macrophage apoptosis through Toll-like receptor-2. J Immunol. 2003;170:2409–16.

    PubMed  CAS  Google Scholar 

  328. Mustafa T, Phyu S, Nilsen R, Bjune G, Jonsson R. Increased expression of Fas ligand on Mycobacterium tuberculosis infected macrophages: a potential novel mechanism of immune evasion by Mycobacterium tuberculosis? Inflammation. 1999;23:507–21.

    PubMed  CAS  Google Scholar 

  329. Oddo M, Renno T, Attinger A, Bakker T, MacDonald HR, Meylan PR. Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis. J Immunol. 1998;160:5448–54.

    PubMed  CAS  Google Scholar 

  330. Placido R, Mancino G, Amendola A, Mariani F, Vendetti S, Piacentini M, et al. Apoptosis of human monocytes/macrophages in Mycobacterium tuberculosis infection. J Pathol. 1997;181:31–8.

    PubMed  CAS  Google Scholar 

  331. Rojas M, Barrera LF, Garcia LF. Induction of apoptosis in murine macrophages by Mycobacterium tuberculosis is reactive oxygen intermediates-independent. Biochem Biophys Res Commun. 1998;247:436–42.

    PubMed  CAS  Google Scholar 

  332. Rojas M, Olivier M, Gros P, Barrera LF, Garcia LF. TNF-alpha and IL-10 modulate the induction of apoptosis by virulent Mycobacterium tuberculosis in murine macrophages. J Immunol. 1999;162:6122–31.

    PubMed  CAS  Google Scholar 

  333. Rojas M, Garcia LF, Nigou J, Puzo G, Olivier M. Mannosylated lipoarabinomannan antagonizes Mycobacterium tuberculosis-induced macrophage apoptosis by altering Ca2+-dependent cell signalling. J Infect Dis. 2000;182:240–51.

    PubMed  CAS  Google Scholar 

  334. Santucci MB, Amicosante M, Cicconi R, Montesano C, Casarini M, Giosue S, et al. Mycobacterium tuberculosis-induced apoptosis in monocytes/macrophages: early membrane modifications and intracellular mycobacterial viability. J Infect Dis. 2000;181:1506–9.

    PubMed  CAS  Google Scholar 

  335. Sly LM, Hingley-Wilson SM, Reiner NE, McMaster WR. Survival of Mycobacterium tuberculosis in host macrophages involves resistance to apoptosis dependent upon induction of antiapoptotic Bcl-2 family member Mcl-1. J Immunol. 2003;170:430–7.

    PubMed  CAS  Google Scholar 

  336. Spira A, Carroll JD, Liu G, Aziz Z, Shah V, Kornfeld H, et al. Apoptosis genes in human alveolar macrophages infected with virulent or attenuated Mycobacterium tuberculosis: a pivotal role for tumor necrosis factor. Am J Respir Cell Mol Biol. 2003;29:545–51.

    PubMed  CAS  Google Scholar 

  337. Arcila ML, Sanchez MD, Ortiz B, Barrera LF, Garcia LF, Rojas M. Activation of apoptosis, but not necrosis, during Mycobacterium tuberculosis infection correlated with decreased bacterial growth: role of TNF-alpha, IL-10, caspases and phospholipase A2. Cell Immunol. 2007;249:80–93.

    PubMed  CAS  Google Scholar 

  338. do Vale A, Marques F, Silva MT. Apoptosis of sea bass (Dicentrarchus labrax L.) neutrophils and macrophages induced by experimental infection with Photobacterium damselae subsp. piscicida. Fish Shellfish Immunol. 2003;15:129–44.

    PubMed  CAS  Google Scholar 

  339. Ozaki K, Hanazawa S. Porphyromonas ginigivalis fimbraie inhibit caspase-3-mediated apoptosis of monocytic THP-1 cells under growth factor deprivation via extracellular signal-regulated kinase-dependent expression of p21 Cip/WAF1. Infect Immun. 2001;69:4944–50.

    PubMed  CAS  Google Scholar 

  340. Preshaw PM, Schifferle RE, Walters JD. Porphyromonas gingivalis lipopolysaccharide delays human polymorphonuclear leukocyte apoptosis in vitro. J Periodontal Res. 1999;34:197–202.

    PubMed  CAS  Google Scholar 

  341. Dacheux D, Goure J, Chabert J, Usson Y, Attree I. Pore-forming activity of type III system-secreted proteins leads to oncosis of Pseudomonas aeruginosa-infected macrophages. Mol Microbiol. 2001;40:76–85.

    PubMed  CAS  Google Scholar 

  342. Dacheux D, Attree I, Schneider C, Toussaint B. Cell death of human polymorphonuclear neutrophils induced by a Pseudomonas aeruginosa cystic fibrosis isolate requires a functional type III secretion system. Infect Immun. 1999;67:6164–7.

    PubMed  CAS  Google Scholar 

  343. Hauser aR, Engel JN. Pseudomonas aeruginosa induces type-III-secretion-mediated apoptosis of macrophages and epithelial cells. Infect Immun. 1999;67:5530–7.

    PubMed  CAS  Google Scholar 

  344. Yt Huang, Jeng CR, Cheng CH, Chueh LL, Liu JJ, Pang VF. Morphological and immunological evidence of a unique selective production and endoplasmic reticular accumulation of interleukin-1alpha in rat peritoneal macrophages induced by Pseudomonas aeruginosa exotoxin A. Cell Immunol. 2003;221:143–56.

    Google Scholar 

  345. Tateda K, Ishii Y, Horikawa M, Matsumoto T, Miyairi S, Pechere JC, et al. The Pseudomonas aeruginosa autoinducer N-3-oxododecanoyl homoserine lactone accelerates apoptosis in macrophages and neutrophils. Infect Immun. 2003;71:5785–93.

    PubMed  CAS  Google Scholar 

  346. Usher LR, Lawson RA, Geary I, Taylor CJ, Bingle CD, Taylor GW, et al. Induction of neutrophil apoptosis by the Pseudomonas aeruginosa exotoxin pyocyanin: a potential mechanism of persistent infection. J Immunol. 2002;168:1861–8.

    PubMed  CAS  Google Scholar 

  347. Worgall S, Martushova K, Busch A, Lande L, Crystal RG. Apoptosis induced by Pseudomonas aeruginosa in antigen presenting cells is diminished by genetic modification with CD40 ligand. Pediatr Res. 2002;52:636–44.

    PubMed  CAS  Google Scholar 

  348. Zaborina O, Dhiman N, Ling Chen M, Kostal J, Holder IA, Chakrabarty AM. Secreted products of a nonmucoid Pseudomonas aeruginosa strain induce two modes of macrophage killing: external-ATP-dependent, P2Z-receptor-mediated necrosis and ATP-independent, caspase-mediated apoptosis. Microbiology. 2000;146:2521–30.

    PubMed  CAS  Google Scholar 

  349. Zhang J, Takayama H, Matsuba T, Jiang R, Tanaka Y. Induction of apoptosis in macrophage cell line, J774, by the cell-free supernatant from Pseudomonas aeruginosa. Microbiol Immunol. 2003;47:199–206.

    PubMed  CAS  Google Scholar 

  350. Raqib R, Ekberg C, Sharkar P, Bardhan PK, Zychlinsky A, Sansonetti PJ, et al. Apoptosis in acute shigellosis is associated with increased production of Fas/Fas ligand, perforin, caspase-1, and caspase-3 but reduced production of Bcl-2 and interleukin-2. Infect Immun. 2002;70:3199–207.

    PubMed  CAS  Google Scholar 

  351. Lee S-Y, Lee M-S, Cherla RP, Tesh VL. Shiga toxin1 induces apoptosis through the endoplasmic reticulum stress response in human monocytic cells. Cell Microbiol. 2008;10:770–80.

    PubMed  CAS  Google Scholar 

  352. Nilsdotter-Augustinsson ASA, Wilsson ASA, Larsson JENN, Stendahl OLLE, Ohman LENA, Lundqvist-Gustafsson HELE. Staphylococcus aureus, but not Staphylococcus epidermidis, modulates the oxidative response and induces apoptosis in human neutrophils. APMIS. 2004;112:109–18.

    PubMed  Google Scholar 

  353. Schnaith A, Kashkar H, Leggio SA, Addicks K, Kronke M, Krut O. Staphylococcus aureus subvert autophagy for induction of caspase-independent host cell death. J Biol Chem. 2007;282:2695–706.

    PubMed  CAS  Google Scholar 

  354. Kubica M, Guzik K, Koziel J, Zarebski M, Richter W, Gajkowska B, et al. A potential new pathway for Staphylococcus aureus dissemination: the silent survival of S. aureus phagocytosed by human monocyte-derived macrophages. PLoS ONE. 2008;3:e1409.

  355. Dockrell DH, Whyte MKB. Regulation of phagocyte lifespan in the lung during bacterial infection. J Leukoc Biol. 2006;79:904–8.

    PubMed  CAS  Google Scholar 

  356. Ali F, Lee ME, Iannelli F, Pozzi G, Mitchell TJ, Read RC, et al. Streptococcus pneumoniae-associated human macrophage apoptosis after bacterial internalization via complement and Fcgamma receptors correlates with intracellular bacterial load. J Infect Dis. 2003;188:1119–31.

    PubMed  CAS  Google Scholar 

  357. Dockrell DH, Lee M, Lynch DH, Read RC. Immune-mediated phagocytosis and killing of Streptococcus pneumoniae are associated with direct and bystander macrophage apoptosis. J Infect Dis. 2001;184:713–22.

    PubMed  CAS  Google Scholar 

  358. Kirby AC, Raynes JG, Kaye PM. The role played by tumor necrosis factor during localized systemic infection with Streptococcus pneumoniae. J Infect Dis. 2005;191:1538–47.

    PubMed  CAS  Google Scholar 

  359. Marriott HM, Dockrell DH. Streptococcus pneumoniae: the role of apoptosis in host defense and pathogenesis. Int J Biochem Cell Biol. 2006;38:1848–54.

    PubMed  CAS  Google Scholar 

  360. Marriott HM, Hellewell PG, Cross SS, Ince PG, Whyte MKB, Dockrell DH. Decreased alveolar macrophage apoptosis is associated with increased pulmonary inflammation in a murine model of pneumococcal pneumonia. J Immunol. 2006;177:6480–8.

    PubMed  CAS  Google Scholar 

  361. Farnworth SL, Henderson NC, MacKinnon AC, Atkinson KM, Wilkinson T, Dhaliwal K, et al. Galectin-3 reduces the severity of pneumococcal pneumonia by augmenting neutrophil function. Am J Pathol. 2008;172:395–405.

    PubMed  CAS  Google Scholar 

  362. Srivastava A, Henneke P, Visintin A, Morse SC, Martin V, Watkins C, et al. The apoptotic response to pneumolysin is toll-like receptor 4 dependent and protects against pneumococcal disease. Infect Immun. 2005;73:6479–87.

    PubMed  CAS  Google Scholar 

  363. Staali L, Bauer S, Morgelin M, Bjorck L, Tapper H. Streptococcus pyogenes bacteria modulate membrane traffic in human neutrophils and selectively inhibit azurophilic granule fusion with phagosomes. Microbiology. 2006;8:690–703.

    CAS  Google Scholar 

  364. Medina E, Goldmann O, Toppel AW, Chhatwal GS. Survival of Streptococcus pyogenes within host phagocytic cells: a pathogenic mechanism for persistence and systemic invasion. J Infect Dis. 2003;187:597–603.

    PubMed  Google Scholar 

  365. Gozuacik D, Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene. 2004;23:2891–906.

    PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the Intramural Research Program of the National Institute of Allergy and Infectious Diseases, National Institutes of Health.

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Correspondence to Frank R. DeLeo.

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Kennedy, A.D., DeLeo, F.R. Neutrophil apoptosis and the resolution of infection. Immunol Res 43, 25–61 (2009). https://doi.org/10.1007/s12026-008-8049-6

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