Excessive interleukin-15 transpresentation endows NKG2D+CD4+ T cells with innate-like capacity to lyse vascular endothelium in granulomatosis with polyangiitis (Wegener's)

Arthritis Rheum. 2011 Jul;63(7):2116-26. doi: 10.1002/art.30355.

Abstract

Objective: Granulomatosis with polyangiitis (Wegener's) (GPA) is a rare systemic vasculitis of unknown etiology. Contribution of T cell-mediated immunity is suggested by the presence of granulomatous inflammation and T cell infiltrates in different tissues. We undertook this study to determine whether CD4+ T cells aberrantly expressing the NKG2D activating receptor might participate in the pathophysiology of the disease.

Methods: We performed a detailed phenotype and functional analysis of CD4+ T cells in a cohort of 90 GPA patients (37 with localized GPA and 53 with generalized GPA) in comparison with 39 age-matched controls.

Results: We observed circulating innate-like CD4+ T cells expressing an assortment of activating natural killer (NK) cell receptors (NKG2D, 2B4, DNAX-associated molecule 1, and some killer cell Ig-like receptors) and their signaling partners. Expansions of NKG2D+CD4+ T cells greater than a critical threshold of 3% yielded 100% specificity for generalized vasculitis versus localized granulomatosis, suggesting their participation in endothelium damage. Excessive interleukin-15 (IL-15) transpresentation through increased expression of IL-15 receptor α (IL-15Rα), together with abnormal expression of major histocompatibility complex (MHC) class I chain-related A protein on monocyte/macrophages, induced abnormal expansion of NKG2D+CD4+ T cells. These cells were primed in vivo to exert direct, MHC-independent cytotoxicity toward microvascular endothelial cells expressing the cognate ligands of NK cell receptors.

Conclusion: Our results suggest that NK cell-like CD4+ T cells might be the driving force of the vasculitis in GPA, and point to IL-15 as an important mediator in the progression of GPA toward generalized vasculitis. IL-15/IL-15Rα antagonists may thus become novel therapeutic tools to decrease the pool of NK cell receptor-positive CD4+ T cells in selected GPA patients.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Aged, 80 and over
  • Antibodies, Antineutrophil Cytoplasmic / immunology
  • Antibodies, Antineutrophil Cytoplasmic / metabolism
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / metabolism
  • CD4-Positive T-Lymphocytes / pathology
  • Cytotoxicity, Immunologic*
  • Endothelium, Vascular / immunology*
  • Endothelium, Vascular / metabolism
  • Endothelium, Vascular / pathology
  • Female
  • Flow Cytometry
  • Granulomatosis with Polyangiitis / immunology*
  • Granulomatosis with Polyangiitis / metabolism
  • Granulomatosis with Polyangiitis / pathology
  • Humans
  • Immunity, Cellular
  • Immunohistochemistry
  • Interleukin-15 / pharmacology*
  • Male
  • Middle Aged
  • NK Cell Lectin-Like Receptor Subfamily K / metabolism*
  • Receptors, Interleukin-15 / metabolism

Substances

  • Antibodies, Antineutrophil Cytoplasmic
  • Interleukin-15
  • KLRK1 protein, human
  • NK Cell Lectin-Like Receptor Subfamily K
  • Receptors, Interleukin-15