Abstract
Sphingosine-1-phosphate (S1P), which is generated from the sphingosine kinase-catalyzed phosphorylation of sphingosine, is now recognized as a critical regulator of many kinds of physiological and pathological processes, including cancer, cardiovascular function, and diabetes. It can also trigger a wide variety of biological effect, such as cell movement, differentiation, survival, inflammation, immunity, calcium homeostasis, and angiogenesis. As we know, a number of the biological effects of S1P are mediated by its binding to five specific G protein-coupled receptors located on the cell surface or intracellular targets. However, the synthesis and the secretion of S1P are regulated by various endogenetic or ectogenous stimuli and involve many kinds of enzymes and transporters. In this review, we discuss the regulation of S1P synthesis by many kinds of enzymes and mainly introduce the process of ceramide to S1P. Moreover, S1P deterioration is important balance in physiologic adjustment. We also describe the role of verified or potential transporters in S1P release in detail.
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Hla T, Lee MJ, Ancellin N, Paik JH, Kluk MJ (2001) Lysophospholipids–receptor revelations. Science 294:1875–1878
Anliker B, Chun J (2004) Lysophospholipid G protein-coupled receptors. J Biol Chem 279:20555–20558
Strub GM, Paillard M, Liang J, Gomez L, Allegood JC, Hait NC, Maceyka M, Price MM, Chen Q, Simpson DC, Kordula T, Milstien S, Lesnefsky EJ, Spiegel S (2011) Sphingosine-1-phosphate produced by sphingosine kinase 2 in mitochondria interacts with prohibitin 2 to regulate complex IV assembly and respiration. FASEB J 25:600–612
Alvarez SE, Harikumar KB, Hait NC, Allegood J, Strub GM, Kim EY, Maceyka M, Jiang H, Luo C, Kordula T, Milstien S, Spiegel S (2010) Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature 465:1084–1088
Hait NC, Allegood J, Maceyka M, Strub GM, Harikumar KB, Singh SK, Luo C, Marmorstein R, Kordula T, Milstien S, Spiegel S (2009) Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 325:1254–1257
Xia P, Wadham C (2011) Sphingosine 1-phosphate, a key mediator of the cytokine network: juxtacrine signaling. Cytokine Growth Factor Rev 22:45–53
Skoura A, Hla T (2009) Regulation of vascular physiology and pathology by the S1P2 receptor subtype. Cardiovasc Res 82:221–228
Saba JD, Hla T (2004) Point-counterpoint of sphingosine 1-phosphate metabolism. Circ Res 94:724–734
Phan VH, Herr DR, Panton D, Fyrst H, Saba JD, Harris GL (2007) Disruption of sphingolipid metabolism elicits apoptosis-associated reproductive defects in Drosophila. Dev Biol 309:329–341
Mendel J, Heinecke K, Fyrst H, Saba JD (2003) Sphingosine phosphate lyase expression is essential for normal development in Caenorhabditis elegans. J Biol Chem 278:22341–22349
Boujaoude LC, Bradshaw-Wilder C, Mao C, Cohn J, Ogretmen B, Hannun YA, Obeid LM (2001) Cystic fibrosis transmembrane regulator regulates uptake of sphingoid base phosphates and lysophosphatidic acid: modulation of cellular activity of sphingosine 1-phosphate. J Biol Chem 276:35258–35264
Hannun YA, Obeid LM (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9:139–150
Wojciak JM, Zhu N, Schuerenberg KT, Moreno K, Shestowsky WS, Hiraiwa M, Sabbadini R, Huxford T (2009) The crystal structure of sphingosine-1-phosphate in complex with a Fab fragment reveals metal bridging of an antibody and its antigen. Proc Natl Acad Sci USA 106:17717–17722
Xu R, Jin J, Hu W, Sun W, Bielawski J, Szulc Z, Taha T, Obeid LM, Mao C (2006) Golgi alkaline ceramidase regulates cell proliferation and survival by controlling levels of sphingosine and S1P. FASEB J 20:1813–1825
Bartke N, Hannun YA (2009) Bioactive sphingolipids: metabolism and function. J Lipid Res 50(Suppl):S91–S96
Le Stunff H, Peterson C, Liu H, Milstien S, Spiegel S (2002) Sphingosine-1-phosphate and lipid phosphohydrolases. Biochim Biophys Acta 1582:8–17
Pyne S, Lee SC, Long J, Pyne NJ (2009) Role of sphingosine kinases and lipid phosphate phosphatases in regulating spatial sphingosine 1-phosphate signalling in health and disease. Cell Signal 21:14–21
Kumar A, Saba JD (2009) Lyase to live by: sphingosine phosphate lyase as a therapeutic target. Expert Opin Ther Targets 13:1013–1025
Wu D, Ren Z, Pae M, Guo W, Cui X, Merrill AH, Meydani SN (2007) Aging up-regulates expression of inflammatory mediators in mouse adipose tissue. J Immunol 179:4829–4839
Zeidan YH, Hannun YA (2007) Translational aspects of sphingolipid metabolism. Trends Mol Med 13:327–336
Vilela RM, Lands LC, Meehan B, Kubow S (2006) Inhibition of IL-8 release from CFTR-deficient lung epithelial cells following pre-treatment with fenretinide. Int Immunopharmacol 6:1651–1664
Mari M, Caballero F, Colell A, Morales A, Caballeria J, Fernandez A, Enrich C, Fernandez-Checa JC, Garcia-Ruiz C (2006) Mitochondrial free cholesterol loading sensitizes to TNF- and Fas-mediated steatohepatitis. Cell Metab 4:185–198
Lang PA, Schenck M, Nicolay JP, Becker JU, Kempe DS, Lupescu A, Koka S, Eisele K, Klarl BA, Rubben H, Schmid KW, Mann K, Hildenbrand S, Hefter H, Huber SM, Wieder T, Erhardt A, Haussinger D, Gulbins E, Lang F (2007) Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide. Nat Med 13:164–170
Cutler RG, Kelly J, Storie K, Pedersen WA, Tammara A, Hatanpaa K, Troncoso JC, Mattson MP (2004) Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer’s disease. Proc Natl Acad Sci USA 101:2070–2075
Morales A, Lee H, Goni FM, Kolesnick R, Fernandez-Checa JC (2007) Sphingolipids and cell death. Apoptosis 12:923–939
Holland WL, Bikman BT, Wang LP, Yuguang G, Sargent KM, Bulchand S, Knotts TA, Shui G, Clegg DJ, Wenk MR, Pagliassotti MJ, Scherer PE, Summers SA (2011) Lipid-induced insulin resistance mediated by the proinflammatory receptor TLR4 requires saturated fatty acid-induced ceramide biosynthesis in mice. J Clin Invest 121:1858–1870
Fox TE, Houck KL, O’Neill SM, Nagarajan M, Stover TC, Pomianowski PT, Unal O, Yun JK, Naides SJ, Kester M (2007) Ceramide recruits and activates protein kinase C zeta (PKC zeta) within structured membrane microdomains. J Biol Chem 282:12450–12457
Yin X, Zafrullah M, Lee H, Haimovitz-Friedman A, Fuks Z, Kolesnick R (2009) A ceramide-binding C1 domain mediates kinase suppressor of ras membrane translocation. Cell Physiol Biochem 24:219–230
Kitatani K, Idkowiak-Baldys J, Hannun YA (2007) Mechanism of inhibition of sequestration of protein kinase C alpha/betaII by ceramide. Roles of ceramide-activated protein phosphatases and phosphorylation/dephosphorylation of protein kinase C alpha/betaII on threonine 638/641. J Biol Chem 282:20647–20656
Maula T, Urzelai B, Peter SJ (2011) The effects of N-acyl chain methylations on ceramide molecular properties in bilayer membranes. Eur Biophys J 40(7):857–863
Maltesen HR, Troelsen JT, Olsen J (2010) Identification of a functional hepatocyte nuclear factor 4 binding site in the neutral ceramidase promoter. J Cell Biochem 111:1330–1336
Lucki N, Sewer MB (2009) The cAMP-responsive element binding protein (CREB) regulates the expression of acid ceramidase (ASAH1) in H295R human adrenocortical cells. Biochim Biophys Acta 1791:706–713
O’Neill SM, Houck KL, Yun JK, Fox TE, Kester M (2011) AP-1 binding transcriptionally regulates human neutral ceramidase. Arch Biochem Biophys 511(1–2):31–39
Zhu Q, Shan X, Miao H, Lu Y, Xu J, You N, Liu C, Liao DF, Jin J (2009) Acute activation of acid ceramidase affects cytokine-induced cytotoxicity in rat islet beta-cells. FEBS Lett 583:2136–2141
Dube JJ, Amati F, Toledo FG, Stefanovic-Racic M, Rossi A, Coen P, Goodpaster BH (2011) Effects of weight loss and exercise on insulin resistance, and intramyocellular triacylglycerol, diacylglycerol and ceramide. Diabetologia 54:1147–1156
Inoue H, Someno T, Kato T, Kumagai H, Kawada M, Ikeda D (2009) Ceramidastin, a novel bacterial ceramidase inhibitor, produced by Penicillium sp. Mer-f17067. J Antibiot (Tokyo) 62:63–67
Proksch D, Klein JJ, Arenz C (2011) Potent inhibition of Acid ceramidase by novel B-13 analogues. J Lipids 2011:971618
Chun L, Junlin Z, Aimin W, Niansheng L, Benmei C, Minxiang L (2011) Inhibition of ceramide synthesis reverses endothelial dysfunction and atherosclerosis in streptozotocin-induced diabetic rats. Diabetes Res Clin Pract 93(1):77–85
Wang E, Norred WP, Bacon CW, Riley RT, Merrill AJ (1991) Inhibition of sphingolipid biosynthesis by fumonisins. Implications for diseases associated with Fusarium moniliforme. J Biol Chem 266:14486–14490
Schwarz A, Futerman AH (1998) Inhibition of sphingolipid synthesis, but not degradation, alters the rate of dendrite growth in cultured hippocampal neurons. Brain Res Dev Brain Res 108:125–130
Mandala SM, Thornton RA, Frommer BR, Curotto JE, Rozdilsky W, Kurtz MB, Giacobbe RA, Bills GF, Cabello MA, Martin I, Et A (1995) The discovery of australifungin, a novel inhibitor of sphinganine N-acyltransferase from Sporormiella australis. Producing organism, fermentation, isolation, and biological activity. J Antibiot (Tokyo) 48:349–356
Kobayashi SD, Nagiec MM (2003) Ceramide/long-chain base phosphate rheostat in Saccharomyces cerevisiae: regulation of ceramide synthesis by Elo3p and Cka2p. Eukaryot Cell 2:284–294
Lahiri S, Park H, Laviad EL, Lu X, Bittman R, Futerman AH (2009) Ceramide synthesis is modulated by the sphingosine analog FTY720 via a mixture of uncompetitive and noncompetitive inhibition in an Acyl-CoA chain length-dependent manner. J Biol Chem 284:16090–16098
Friant S, Lombardi R, Schmelzle T, Hall MN, Riezman H (2001) Sphingoid base signaling via Pkh kinases is required for endocytosis in yeast. EMBO J 20:6783–6792
Gomez-Munoz A, Hamza EH, Brindley DN (1992) Effects of sphingosine, albumin and unsaturated fatty acids on the activation and translocation of phosphatidate phosphohydrolases in rat hepatocytes. Biochim Biophys Acta 1127:49–56
Natarajan V, Jayaram HN, Scribner WM, Garcia JG (1994) Activation of endothelial cell phospholipase D by sphingosine and sphingosine-1-phosphate. Am J Respir Cell Mol Biol 11:221–229
Yamada K, Sakane F, Imai S, Takemura H (1993) Sphingosine activates cellular diacylglycerol kinase in intact Jurkat cells, a human T-cell line. Biochim Biophys Acta 1169:217–224
Hait NC, Oskeritzian CA, Paugh SW, Milstien S, Spiegel S (2006) Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim Biophys Acta 1758:2016–2026
Mizugishi K, Yamashita T, Olivera A, Miller GF, Spiegel S, Proia RL (2005) Essential role for sphingosine kinases in neural and vascular development. Mol Cell Biol 25:11113–11121
Gillies L, Lee SC, Long JS, Ktistakis N, Pyne NJ, Pyne S (2009) The sphingosine 1-phosphate receptor 5 and sphingosine kinases 1 and 2 are localised in centrosomes: possible role in regulating cell division. Cell Signal 21:675–684
Hait NC, Sarkar S, Le Stunff H, Mikami A, Maceyka M, Milstien S, Spiegel S (2005) Role of sphingosine kinase 2 in cell migration toward epidermal growth factor. J Biol Chem 280:29462–29469
Shida D, Fang X, Kordula T, Takabe K, Lepine S, Alvarez SE, Milstien S, Spiegel S (2008) Cross-talk between LPA1 and epidermal growth factor receptors mediates up-regulation of sphingosine kinase 1 to promote gastric cancer cell motility and invasion. Cancer Res 68:6569–6577
Duan HF, Wu CT, Lu Y, Wang H, Liu HJ, Zhang QW, Jia XX, Lu ZZ, Wang LS (2004) Sphingosine kinase activation regulates hepatocyte growth factor induced migration of endothelial cells. Exp Cell Res 298:593–601
Hobson JP, Rosenfeldt HM, Barak LS, Olivera A, Poulton S, Caron MG, Milstien S, Spiegel S (2001) Role of the sphingosine-1-phosphate receptor EDG-1 in PDGF-induced cell motility. Science 291:1800–1803
Shu X, Wu W, Mosteller RD, Broek D (2002) Sphingosine kinase mediates vascular endothelial growth factor-induced activation of ras and mitogen-activated protein kinases. Mol Cell Biol 22:7758–7768
Bassi R, Anelli V, Giussani P, Tettamanti G, Viani P, Riboni L (2006) Sphingosine-1-phosphate is released by cerebellar astrocytes in response to bFGF and induces astrocyte proliferation through Gi-protein-coupled receptors. Glia 53:621–630
Xia P, Wang L, Moretti PA, Albanese N, Chai F, Pitson SM, D’Andrea RJ, Gamble JR, Vadas MA (2002) Sphingosine kinase interacts with TRAF2 and dissects tumor necrosis factor-alpha signaling. J Biol Chem 277:7996–8003
Pettus BJ, Bielawski J, Porcelli AM, Reames DL, Johnson KR, Morrow J, Chalfant CE, Obeid LM, Hannun YA (2003) The sphingosine kinase 1/sphingosine-1-phosphate pathway mediates COX-2 induction and PGE2 production in response to TNF-alpha. FASEB J 17:1411–1421
Sukocheva O, Wadham C, Holmes A, Albanese N, Verrier E, Feng F, Bernal A, Derian CK, Ullrich A, Vadas MA, Xia P (2006) Estrogen transactivates EGFR via the sphingosine 1-phosphate receptor Edg-3: the role of sphingosine kinase-1. J Cell Biol 173:301–310
van Koppen CJ, Meyer ZHD, Alemany R, Jakobs KH (2001) Sphingosine kinase-mediated calcium signaling by muscarinic acetylcholine receptors. Life Sci 68:2535–2540
Delon C, Manifava M, Wood E, Thompson D, Krugmann S, Pyne S, Ktistakis NT (2004) Sphingosine kinase 1 is an intracellular effector of phosphatidic acid. J Biol Chem 279:44763–44774
Pappu R, Schwab SR, Cornelissen I, Pereira JP, Regard JB, Xu Y, Camerer E, Zheng YW, Huang Y, Cyster JG, Coughlin SR (2007) Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science 316:295–298
Niessen F, Schaffner F, Furlan-Freguia C, Pawlinski R, Bhattacharjee G, Chun J, Derian CK, Andrade-Gordon P, Rosen H, Ruf W (2008) Dendritic cell PAR1–S1P3 signalling couples coagulation and inflammation. Nature 452:654–658
Choi OH, Kim JH, Kinet JP (1996) Calcium mobilization via sphingosine kinase in signalling by the Fc epsilon RI antigen receptor. Nature 380:634–636
Schwalm S, Pfeilschifter J, Huwiler A (2010) Sphingosine kinase 1 is critically involved in nitric oxide-mediated human endothelial cell migration and tube formation. Br J Pharmacol 160:1641–1651
Meyer ZHD, Lass H, Kuchar I, Lipinski M, Alemany R, Rumenapp U, Jakobs KH (2001) Stimulation of intracellular sphingosine-1-phosphate production by G-protein-coupled sphingosine-1-phosphate receptors. Eur J Pharmacol 414:145–154
Leclercq TM, Moretti PA, Pitson SM (2011) Guanine nucleotides regulate sphingosine kinase 1 activation by eukaryotic elongation factor 1A and provide a mechanism for eEF1A-associated oncogenesis. Oncogene 30:372–378
Stahelin RV, Hwang JH, Kim JH, Park ZY, Johnson KR, Obeid LM, Cho W (2005) The mechanism of membrane targeting of human sphingosine kinase 1. J Biol Chem 280:43030–43038
Ancellin N, Colmont C, Su J, Li Q, Mittereder N, Chae SS, Stefansson S, Liau G, Hla T (2002) Extracellular export of sphingosine kinase-1 enzyme. Sphingosine 1-phosphate generation and the induction of angiogenic vascular maturation. J Biol Chem 277:6667–6675
Waters C, Sambi B, Kong KC, Thompson D, Pitson SM, Pyne S, Pyne NJ (2003) Sphingosine 1-phosphate and platelet-derived growth factor (PDGF) act via PDGF beta receptor-sphingosine 1-phosphate receptor complexes in airway smooth muscle cells. J Biol Chem 278:6282–6290
Hammad SM, Taha TA, Nareika A, Johnson KR, Lopes-Virella MF, Obeid LM (2006) Oxidized LDL immune complexes induce release of sphingosine kinase in human U937 monocytic cells. Prostaglandins Other Lipid Mediat 79:126–140
Venkataraman K, Thangada S, Michaud J, Oo ML, Ai Y, Lee YM, Wu M, Parikh NS, Khan F, Proia RL, Hla T (2006) Extracellular export of sphingosine kinase-1a contributes to the vascular S1P gradient. Biochem J 397:461–471
Hait NC, Bellamy A, Milstien S, Kordula T, Spiegel S (2007) Sphingosine kinase type 2 activation by ERK-mediated phosphorylation. J Biol Chem 282:12058–12065
Ding G, Sonoda H, Yu H, Kajimoto T, Goparaju SK, Jahangeer S, Okada T, Nakamura S (2007) Protein kinase D-mediated phosphorylation and nuclear export of sphingosine kinase 2. J Biol Chem 282:27493–27502
Riccio A (2010) New endogenous regulators of class I histone deacetylases. Sci Signal 3(103):pe1–pe1
Hannun YA, Luberto C, Argraves KM (2001) Enzymes of sphingolipid metabolism: from modular to integrative signaling. Biochemistry 40:4893–4903
Mandala SM, Thornton R, Galve-Roperh I, Poulton S, Peterson C, Olivera A, Bergstrom J, Kurtz MB, Spiegel S (2000) Molecular cloning and characterization of a lipid phosphohydrolase that degrades sphingosine-1-phosphate and induces cell death. Proc Natl Acad Sci USA 97:7859–7864
Ogawa C, Kihara A, Gokoh M, Igarashi Y (2003) Identification and characterization of a novel human sphingosine-1-phosphate phosphohydrolase, hSPP2. J Biol Chem 278:1268–1272
Le Stunff H, Galve-Roperh I, Peterson C, Milstien S, Spiegel S (2002) Sphingosine-1-phosphate phosphohydrolase in regulation of sphingolipid metabolism and apoptosis. J Cell Biol 158:1039–1049
Mandala SM (2001) Sphingosine-1-phosphate phosphatases. Prostaglandins Other Lipid Mediat 64:143–156
Renshaw D, Montero-Melendez T, Dalli J, Kamal A, Brancaleone V, D’Acquisto F, Cirino G, Perretti M (2010) Downstream gene activation of the receptor ALX by the agonist annexin A1. PLoS One 5:e12771
Venkataraman K, Lee YM, Michaud J, Thangada S, Ai Y, Bonkovsky HL, Parikh NS, Habrukowich C, Hla T (2008) Vascular endothelium as a contributor of plasma sphingosine 1-phosphate. Circ Res 102:669–676
Lepine S, Allegood JC, Park M, Dent P, Milstien S, Spiegel S (2011) Sphingosine-1-phosphate phosphohydrolase-1 regulates ER stress-induced autophagy. Cell Death Differ 18:350–361
Peter BF, Lidington D, Harada A, Bolz HJ, Vogel L, Heximer S, Spiegel S, Pohl U, Bolz SS (2008) Role of sphingosine-1-phosphate phosphohydrolase 1 in the regulation of resistance artery tone. Circ Res 103:315–324
Johnson KR, Johnson KY, Becker KP, Bielawski J, Mao C, Obeid LM (2003) Role of human sphingosine-1-phosphate phosphatase 1 in the regulation of intra- and extracellular sphingosine-1-phosphate levels and cell viability. J Biol Chem 278:34541–34547
Giussani P, Maceyka M, Le Stunff H, Mikami A, Lepine S, Wang E, Kelly S, Merrill AJ, Milstien S, Spiegel S (2006) Sphingosine-1-phosphate phosphohydrolase regulates endoplasmic reticulum-to-golgi trafficking of ceramide. Mol Cell Biol 26:5055–5069
Saddoughi SA, Song P, Ogretmen B (2008) Roles of bioactive sphingolipids in cancer biology and therapeutics. Subcell Biochem 49:413–440
Weber C, Krueger A, Munk A, Bode C, Van Veldhoven PP, Graler MH (2009) Discontinued postnatal thymocyte development in sphingosine 1-phosphate-lyase-deficient mice. J Immunol 183:4292–4301
Pyne NJ, Pyne S (2010) Sphingosine 1-phosphate and cancer. Nat Rev Cancer 10:489–503
Oskouian B, Sooriyakumaran P, Borowsky AD, Crans A, Dillard-Telm L, Tam YY, Bandhuvula P, Saba JD (2006) Sphingosine-1-phosphate lyase potentiates apoptosis via p53- and p38-dependent pathways and is down-regulated in colon cancer. Proc Natl Acad Sci USA 103:17384–17389
Merrill AJ (2002) De novo sphingolipid biosynthesis: a necessary, but dangerous, pathway. J Biol Chem 277:25843–25846
Katsel P, Li C, Haroutunian V (2007) Gene expression alterations in the sphingolipid metabolism pathways during progression of dementia and Alzheimer’s disease: a shift toward ceramide accumulation at the earliest recognizable stages of Alzheimer’s disease? Neurochem Res 32:845–856
Morgan AR, Turic D, Jehu L, Hamilton G, Hollingworth P, Moskvina V, Jones L, Lovestone S, Brayne C, Rubinsztein DC, Lawlor B, Gill M, O’Donovan MC, Owen MJ, Williams J (2007) Association studies of 23 positional/functional candidate genes on chromosome 10 in late-onset Alzheimer’s disease. Am J Med Genet B Neuropsychiatr Genet 144B:762–770
Seo EY, Park GT, Lee KM, Kim JA, Lee JH, Yang JM (2006) Identification of the target genes of atopic dermatitis by real-time PCR. J Invest Dermatol 126:1187–1189
Wood SH, Clements DN, Ollier WE, Nuttall T, McEwan NA, Carter SD (2009) Gene expression in canine atopic dermatitis and correlation with clinical severity scores. J Dermatol Sci 55:27–33
Holleran WM, Takagi Y, Uchida Y (2006) Epidermal sphingolipids: metabolism, function, and roles in skin disorders. FEBS Lett 580:5456–5466
Schwab SR, Pereira JP, Matloubian M, Xu Y, Huang Y, Cyster JG (2005) Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 309:1735–1739
Allende ML, Bektas M, Lee BG, Bonifacino E, Kang J, Tuymetova G, Chen W, Saba JD, Proia RL (2011) Sphingosine-1-phosphate lyase deficiency produces a pro-inflammatory response while impairing neutrophil trafficking. J Biol Chem 286:7348–7358
Vogel P, Donoviel MS, Read R, Hansen GM, Hazlewood J, Anderson SJ, Sun W, Swaffield J, Oravecz T (2009) Incomplete inhibition of sphingosine 1-phosphate lyase modulates immune system function yet prevents early lethality and non-lymphoid lesions. PLoS One 4:e4112
Claas RF, ter Braak M, Hegen B, Hardel V, Angioni C, Schmidt H, Jakobs KH, Van Veldhoven PP, Zu HD (2010) Enhanced Ca2 + storage in sphingosine-1-phosphate lyase-deficient fibroblasts. Cell Signal 22:476–483
Colie S, Van Veldhoven PP, Kedjouar B, Bedia C, Albinet V, Sorli SC, Garcia V, Djavaheri-Mergny M, Bauvy C, Codogno P, Levade T, Andrieu-Abadie N (2009) Disruption of sphingosine 1-phosphate lyase confers resistance to chemotherapy and promotes oncogenesis through Bcl-2/Bcl-xL upregulation. Cancer Res 69:9346–9353
Bektas M, Allende ML, Lee BG, Chen W, Amar MJ, Remaley AT, Saba JD, Proia RL (2010) Sphingosine 1-phosphate lyase deficiency disrupts lipid homeostasis in liver. J Biol Chem 285:10880–10889
Oskouian B, Mendel J, Shocron E, Lee MJ, Fyrst H, Saba JD (2005) Regulation of sphingosine-1-phosphate lyase gene expression by members of the GATA family of transcription factors. J Biol Chem 280:18403–18410
Dannenberg JH, David G, Zhong S, van der Torre J, Wong WH, Depinho RA (2005) mSin3A corepressor regulates diverse transcriptional networks governing normal and neoplastic growth and survival. Genes Dev 19:1581–1595
Reiss U, Oskouian B, Zhou J, Gupta V, Sooriyakumaran P, Kelly S, Wang E, Merrill AJ, Saba JD (2004) Sphingosine-phosphate lyase enhances stress-induced ceramide generation and apoptosis. J Biol Chem 279:1281–1290
Ikeda M, Kihara A, Igarashi Y (2004) Sphingosine-1-phosphate lyase SPL is an endoplasmic reticulum-resident, integral membrane protein with the pyridoxal 5′-phosphate binding domain exposed to the cytosol. Biochem Biophys Res Commun 325:338–343
Lee YM, Venkataraman K, Hwang SI, Han DK, Hla T (2007) A novel method to quantify sphingosine 1-phosphate by immobilized metal affinity chromatography (IMAC). Prostaglandins Other Lipid Mediat 84:154–162
Kobayashi N, Nishi T, Hirata T, Kihara A, Sano T, Igarashi Y, Yamaguchi A (2006) Sphingosine 1-phosphate is released from the cytosol of rat platelets in a carrier-mediated manner. J Lipid Res 47:614–621
Rea PA, Li ZS, Lu YP, Drozdowicz YM, Martinoia E (1998) From vacuolar GS-X pumps to multispecific ABC transporters. Annu Rev Plant Physiol Plant Mol Biol 49:727–760
Kobayashi N, Kobayashi N, Yamaguchi A, Nishi T (2009) Characterization of the ATP-dependent sphingosine 1-phosphate transporter in rat erythrocytes. J Biol Chem 284:21192–21200
Murata N, Sato K, Kon J, Tomura H, Yanagita M, Kuwabara A, Ui M, Okajima F (2000) Interaction of sphingosine 1-phosphate with plasma components, including lipoproteins, regulates the lipid receptor-mediated actions. Biochem J 352(Pt 3):809–815
Argraves KM, Argraves WS (2007) HDL serves as a S1P signaling platform mediating a multitude of cardiovascular effects. J Lipid Res 48:2325–2333
Kimura T, Sato K, Kuwabara A, Tomura H, Ishiwara M, Kobayashi I, Ui M, Okajima F (2001) Sphingosine 1-phosphate may be a major component of plasma lipoproteins responsible for the cytoprotective actions in human umbilical vein endothelial cells. J Biol Chem 276:31780–31785
Christoffersen C, Jauhiainen M, Moser M, Porse B, Ehnholm C, Boesl M, Dahlback B, Nielsen LB (2008) Effect of apolipoprotein M on high density lipoprotein metabolism and atherosclerosis in low density lipoprotein receptor knock-out mice. J Biol Chem 283:1839–1847
Wolfrum C, Poy MN, Stoffel M (2005) Apolipoprotein M is required for prebeta-HDL formation and cholesterol efflux to HDL and protects against atherosclerosis. Nat Med 11:418–422
Nielsen LB, Christoffersen C, Ahnstrom J, Dahlback B (2009) ApoM: gene regulation and effects on HDL metabolism. Trends Endocrinol Metab 20:66–71
Sevvana M, Ahnstrom J, Egerer-Sieber C, Lange HA, Dahlback B, Muller YA (2009) Serendipitous fatty acid binding reveals the structural determinants for ligand recognition in apolipoprotein M. J Mol Biol 393:920–936
Christoffersen C, Obinata H, Kumaraswamy SB, Galvani S, Ahnstrom J, Sevvana M, Egerer-Sieber C, Muller YA, Hla T, Nielsen LB, Dahlback B (2011) Endothelium-protective sphingosine-1-phosphate provided by HDL-associated apolipoprotein M. Proc Natl Acad Sci USA 108:9613–9618
Sato K, Malchinkhuu E, Horiuchi Y, Mogi C, Tomura H, Tosaka M, Yoshimoto Y, Kuwabara A, Okajima F (2007) Critical role of ABCA1 transporter in sphingosine 1-phosphate release from astrocytes. J Neurochem 103:2610–2619
Liang Y, Lin S, Beyer TP, Zhang Y, Wu X, Bales KR, DeMattos RB, May PC, Li SD, Jiang XC, Eacho PI, Cao G, Paul SM (2004) A liver X receptor and retinoid X receptor heterodimer mediates apolipoprotein E expression, secretion and cholesterol homeostasis in astrocytes. J Neurochem 88:623–634
Lorenzi I, von Eckardstein A, Radosavljevic S, Rohrer L (2008) Lipidation of apolipoprotein A-I by ATP-binding cassette transporter (ABC) A1 generates an interaction partner for ABCG1 but not for scavenger receptor BI. Biochim Biophys Acta 1781:306–313
Gelissen IC, Harris M, Rye KA, Quinn C, Brown AJ, Kockx M, Cartland S, Packianathan M, Kritharides L, Jessup W (2006) ABCA1 and ABCG1 synergize to mediate cholesterol export to apoA-I. Arterioscler Thromb Vasc Biol 26:534–540
Vaughan AM, Oram JF (2006) ABCA1 and ABCG1 or ABCG4 act sequentially to remove cellular cholesterol and generate cholesterol-rich HDL. J Lipid Res 47:2433–2443
Thuahnai ST, Lund-Katz S, Williams DL, Phillips MC (2001) Scavenger receptor class B, type I-mediated uptake of various lipids into cells. Influence of the nature of the donor particle interaction with the receptor. J Biol Chem 276:43801–43808
Rhode S, Breuer A, Hesse J, Sonnleitner M, Pagler TA, Doringer M, Schutz GJ, Stangl H (2004) Visualization of the uptake of individual HDL particles in living cells via the scavenger receptor class B type I. Cell Biochem Biophys 41:343–356
Swarnakar S, Temel RE, Connelly MA, Azhar S, Williams DL (1999) Scavenger receptor class B, type I, mediates selective uptake of low density lipoprotein cholesteryl ester. J Biol Chem 274:29733–29739
Kobayashi A, Takanezawa Y, Hirata T, Shimizu Y, Misasa K, Kioka N, Arai H, Ueda K, Matsuo M (2006) Efflux of sphingomyelin, cholesterol, and phosphatidylcholine by ABCG1. J Lipid Res 47:1791–1802
Mitra P, Oskeritzian CA, Payne SG, Beaven MA, Milstien S, Spiegel S (2006) Role of ABCC1 in export of sphingosine-1-phosphate from mast cells. Proc Natl Acad Sci USA 103:16394–16399
Jolly PS, Bektas M, Olivera A, Gonzalez-Espinosa C, Proia RL, Rivera J, Milstien S, Spiegel S (2004) Transactivation of sphingosine-1-phosphate receptors by FcepsilonRI triggering is required for normal mast cell degranulation and chemotaxis. J Exp Med 199:959–970
Rivera J, Olivera A (2008) A current understanding of Fc epsilon RI-dependent mast cell activation. Curr Allergy Asthma Rep 8:14–20
Takabe K, Kim RH, Allegood JC, Mitra P, Ramachandran S, Nagahashi M, Harikumar KB, Hait NC, Milstien S, Spiegel S (2010) Estradiol induces export of sphingosine 1-phosphate from breast cancer cells via ABCC1 and ABCG2. J Biol Chem 285:10477–10486
Spencer ES, Minch J, Lahmers KK, Haldorson GJ, Mealey KL (2010) Canine ABCB4: Tissue expression and cDNA structure. Res Vet Sci 89:65–71
Sugawara T, Kinoshita M, Ohnishi M, Tsuzuki T, Miyazawa T, Nagata J, Hirata T, Saito M (2004) Efflux of sphingoid bases by P-glycoprotein in human intestinal Caco-2 cells. Biosci Biotechnol Biochem 68:2541–2546
Frijters CM, Tuijn CJ, Ottenhoff R, Zegers BN, Groen AK, Elferink RP (1999) The role of different P-glycoproteins in hepatobiliary secretion of fluorescently labeled short-chain phospholipids. J Lipid Res 40:1950–1958
Raggers RJ, van Helvoort A, Evers R, van Meer G (1999) The human multidrug resistance protein MRP1 translocates sphingolipid analogs across the plasma membrane. J Cell Sci 112(Pt 3):415–422
Bosch I, Dunussi-Joannopoulos K, Wu RL, Furlong ST, Croop J (1997) Phosphatidylcholine and phosphatidylethanolamine behave as substrates of the human MDR1 P-glycoprotein. Biochemistry 36:5685–5694
Ernest S, Bello-Reuss E (1999) Secretion of platelet-activating factor is mediated by MDR1 P-glycoprotein in cultured human mesangial cells. J Am Soc Nephrol 10:2306–2313
Honig SM, Fu S, Mao X, Yopp A, Gunn MD, Randolph GJ, Bromberg JS (2003) FTY720 stimulates multidrug transporter- and cysteinyl leukotriene-dependent T cell chemotaxis to lymph nodes. J Clin Invest 111:627–637
Pohl A, Lage H, Muller P, Pomorski T, Herrmann A (2002) Transport of phosphatidylserine via MDR1 (multidrug resistance 1)P-glycoprotein in a human gastric carcinoma cell line. Biochem J 365:259–268
Hinrichs JW, Klappe K, Hummel I, Kok JW (2004) ATP-binding cassette transporters are enriched in non-caveolar detergent-insoluble glycosphingolipid-enriched membrane domains (DIGs) in human multidrug-resistant cancer cells. J Biol Chem 279:5734–5738
Nagelin MH, Srinivasan S, Lee J, Nadler JL, Hedrick CC (2008) 12/15-Lipoxygenase activity increases the degradation of macrophage ATP-binding cassette transporter G1. Arterioscler Thromb Vasc Biol 28:1811–1819
Radeva G, Perabo J, Sharom FJ (2005) P-Glycoprotein is localized in intermediate-density membrane microdomains distinct from classical lipid rafts and caveolar domains. FEBS J 272:4924–4937
Rosmorduc O, Poupon R (2007) Low phospholipid associated cholelithiasis: association with mutation in the MDR3/ABCB4 gene. Orphanet J Rare Dis 2:29
Zhou Y, Gottesman MM, Pastan I (1999) Domain exchangeability between the multidrug transporter (MDR1) and phosphatidylcholine flippase (MDR2). Mol Pharmacol 56:997–1004
Abulrob AG, Gumbleton M (1999) Transport of phosphatidylcholine in MDR3-negative epithelial cell lines via drug-induced MDR1 P-glycoprotein. Biochem Biophys Res Commun 262:121–126
Elferink RP, Ottenhoff R, Fricker G, Seward DJ, Ballatori N, Boyer J (2004) Lack of biliary lipid excretion in the little skate, Raja erinacea, indicates the absence of functional Mdr2, Abcg5, and Abcg8 transporters. Am J Physiol Gastrointest Liver Physiol 286:G762–G768
Kawahara A, Nishi T, Hisano Y, Fukui H, Yamaguchi A, Mochizuki N (2009) The sphingolipid transporter spns2 functions in migration of zebrafish myocardial precursors. Science 323:524–527
Hisano Y, Kobayashi N, Kawahara A, Yamaguchi A, Nishi T (2011) The sphingosine 1-phosphate transporter, SPNS2, functions as a transporter of the phosphorylated form of the immunomodulating agent FTY720. J Biol Chem 286:1758–1766
Nofer JR, Bot M, Brodde M, Taylor PJ, Salm P, Brinkmann V, van Berkel T, Assmann G, Biessen EA (2007) FTY720, a synthetic sphingosine 1 phosphate analogue, inhibits development of atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation 115:501–508
Keul P, Tolle M, Lucke S, von Wnuck LK, Heusch G, Schuchardt M, van der Giet M, Levkau B (2007) The sphingosine-1-phosphate analogue FTY720 reduces atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 27:607–613
Morales CR, Marat AL, Ni X, Yu Y, Oko R, Smith BT, Argraves WS (2008) ATP-binding cassette transporters ABCA1, ABCA7, and ABCG1 in mouse spermatozoa. Biochem Biophys Res Commun 376:472–477
Choudhuri S, Klaassen CD (2006) Structure, function, expression, genomic organization, and single nucleotide polymorphisms of human ABCB1 (MDR1), ABCC (MRP), and ABCG2 (BCRP) efflux transporters. Int J Toxicol 25:231–259
Olivera A, Urtz N, Mizugishi K, Yamashita Y, Gilfillan AM, Furumoto Y, Gu H, Proia RL, Baumruker T, Rivera J (2006) IgE-dependent activation of sphingosine kinases 1 and 2 and secretion of sphingosine 1-phosphate requires Fyn kinase and contributes to mast cell responses. J Biol Chem 281:2515–2525
Vaughan AM, Oram JF (2005) ABCG1 redistributes cell cholesterol to domains removable by high density lipoprotein but not by lipid-depleted apolipoproteins. J Biol Chem 280:30150–30157
Wang N, Yvan-Charvet L, Lutjohann D, Mulder M, Vanmierlo T, Kim TW, Tall AR (2008) ATP-binding cassette transporters G1 and G4 mediate cholesterol and desmosterol efflux to HDL and regulate sterol accumulation in the brain. FASEB J 22:1073–1082
Visentin B, Vekich JA, Sibbald BJ, Cavalli AL, Moreno KM, Matteo RG, Garland WA, Lu Y, Yu S, Hall HS, Kundra V, Mills GB, Sabbadini RA (2006) Validation of an anti-sphingosine-1-phosphate antibody as a potential therapeutic in reducing growth, invasion, and angiogenesis in multiple tumor lineages. Cancer Cell 9:225–238
Maceyka M, Harikumar KB, Milstien S and Spiegel S (2011) Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol (in press)
Fox TE, Bewley MC, Unrath KA, Pedersen MM, Anderson RE, Jung DY, Jefferson LS, Kim JK, Bronson SK, Flanagan JM, Kester M (2011) Circulating sphingolipid biomarkers in models of type 1 diabetes. J Lipid Res 52:509–517
Sattler KJ, Elbasan S, Keul P, Elter-Schulz M, Bode C, Graler MH, Brocker-Preuss M, Budde T, Erbel R, Heusch G, Levkau B (2010) Sphingosine 1-phosphate levels in plasma and HDL are altered in coronary artery disease. Basic Res Cardiol 105:821–832
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The authors gratefully acknowledge the financial support from the National Natural Sciences Foundation of China (30570958), Funds of The Hunan Provincial College Research Project (Accented Term 09A078).
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Liu, X., Zhang, QH. & Yi, GH. Regulation of metabolism and transport of sphingosine-1-phosphate in mammalian cells. Mol Cell Biochem 363, 21–33 (2012). https://doi.org/10.1007/s11010-011-1154-1
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DOI: https://doi.org/10.1007/s11010-011-1154-1