Mast cell CD30 ligand is upregulated in cutaneous inflammation and mediates degranulation-independent chemokine secretion

J Clin Invest. 2006 Oct;116(10):2748-56. doi: 10.1172/JCI24274. Epub 2006 Sep 7.

Abstract

Mast cells are involved in many disorders where the triggering mechanism that leads to degranulation and/or cytokine secretion has not been defined. Several chronic inflammatory diseases are associated with increased mast cell numbers and upregulation of the TNF receptor family member CD30, but the role of elevated CD30 expression is poorly understood. Here we report what we believe to be a novel way to activate mast cells with CD30 that leads to degranulation-independent secretion of chemokines. CD30 induced a de novo synthesis and secretion of the chemokines IL-8, macrophage inflammatory protein-1alpha (MIP-1alpha), and MIP-1beta, a process involving the MAPK/ERK pathway. Mast cells were found to be the predominant CD30 ligand-positive (CD30L-positive) cell in the chronic inflammatory skin diseases psoriasis and atopic dermatitis, and both CD30 and CD30L expression were upregulated in lesional skin in these conditions. Furthermore, the number of IL-8-positive mast cells was elevated both in psoriatic and atopic dermatitis lesional skin as well as in ex vivo CD30-treated healthy skin organ cultures. In summary, characterization of CD30 activation of mast cells has uncovered an IgE-independent pathway that is of importance in understanding the entirety of the role of mast cells in diseases associated with mast cells and CD30 expression. These diseases include Hodgkin lymphoma, atopic dermatitis, and psoriasis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • CD30 Ligand / metabolism*
  • CD30 Ligand / pharmacology
  • Cell Degranulation / drug effects
  • Cell Degranulation / physiology*
  • Cells, Cultured
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / metabolism
  • Chemokine CCL3
  • Chemokine CCL4
  • Chemokines / metabolism*
  • Cytokines / genetics
  • Cytokines / metabolism
  • Dermatitis, Atopic / metabolism
  • Dermatitis, Atopic / pathology
  • Female
  • Fetal Blood / cytology
  • Gene Expression / drug effects
  • Gene Expression / genetics
  • Histamine Release / drug effects
  • Humans
  • Interleukin-8 / genetics
  • Interleukin-8 / metabolism
  • Ki-1 Antigen / metabolism
  • Leukotrienes / biosynthesis
  • MAP Kinase Signaling System / drug effects
  • MAP Kinase Signaling System / physiology
  • Macrophage Inflammatory Proteins / genetics
  • Macrophage Inflammatory Proteins / metabolism
  • Male
  • Mast Cells / drug effects
  • Mast Cells / metabolism*
  • Mast Cells / physiology
  • Middle Aged
  • Psoriasis / metabolism
  • Psoriasis / pathology
  • Skin Diseases / metabolism*
  • Skin Diseases / pathology
  • Tryptases / metabolism
  • Up-Regulation

Substances

  • CCL2 protein, human
  • CD30 Ligand
  • Chemokine CCL2
  • Chemokine CCL3
  • Chemokine CCL4
  • Chemokines
  • Cytokines
  • Interleukin-8
  • Ki-1 Antigen
  • Leukotrienes
  • Macrophage Inflammatory Proteins
  • Tryptases