Elevated production of interleukin-6 is associated with a lower incidence of disease-related ischemic events in patients with giant-cell arteritis: angiogenic activity of interleukin-6 as a potential protective mechanism

Circulation. 2003 May 20;107(19):2428-34. doi: 10.1161/01.CIR.0000066907.83923.32. Epub 2003 May 12.

Abstract

Background: Patients with giant-cell arteritis (GCA) who develop a strong acute-phase response are at low risk of disease-related ischemic events.

Methods and results: To assess the potential protective role of proinflammatory cytokines in the development of ischemic events in GCA, we measured tissue expression (66 individuals) and/or circulating levels (80 individuals) of interleukin (IL)-1beta, tumor necrosis factor-alpha (TNF-alpha), and IL-6 in patients with biopsy-proven GCA. Tissue expression was determined by quantitative real-time polymerase chain reaction and immunohistochemistry. Circulating cytokines were determined by enzyme-linked immunoassay. We found that patients with disease-related ischemic events had lower IL-6 mRNA levels (5.9+/-2.1 versus 27.6+/-7.8 relative units, P=0.013), lower IL-6 immunohistochemical expression scores (1.5+/-0.9 versus 2.7+/-1, P=0.001), and lower circulating levels of IL-6 (13.6+/-2.1 versus 24+/-2.4 pg/mL, P=0.002) than patients without ischemic complications. No significant differences were found for either IL-1beta or TNF-alpha. We subsequently investigated direct effects of IL-6 on vessel wall components. We found that IL-6 stimulates endothelial cell proliferation and differentiation into capillary-like structures and induces full angiogenic activity in both ex vivo (aortic ring) and in vivo (chick chorioallantoic membrane) assays.

Conclusions: GCA patients with ischemic complications have lower tissue expression and circulating levels of IL-6 than patients with no ischemic events. IL-6 has relevant direct effects on vascular wall components that might be protective: IL-6 activates a functional program related to angiogenesis that may compensate for ischemia in patients with GCA.

Publication types

  • Clinical Trial
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute-Phase Reaction
  • Aged
  • Aged, 80 and over
  • Animals
  • Biopsy
  • Cell Differentiation / drug effects
  • Cell Division / drug effects
  • Cells, Cultured
  • Chick Embryo
  • Endothelium, Vascular / cytology
  • Endothelium, Vascular / drug effects
  • Female
  • Giant Cell Arteritis / immunology
  • Giant Cell Arteritis / metabolism*
  • Giant Cell Arteritis / pathology
  • Humans
  • Immunohistochemistry
  • In Vitro Techniques
  • Interleukin-1 / genetics
  • Interleukin-1 / metabolism
  • Interleukin-6 / genetics
  • Interleukin-6 / metabolism*
  • Interleukin-6 / pharmacology
  • Ischemia
  • Male
  • Middle Aged
  • Neovascularization, Physiologic / drug effects
  • Prospective Studies
  • RNA, Messenger / analysis
  • RNA, Messenger / metabolism
  • Receptors, Interleukin
  • Receptors, Interleukin-6
  • Recombinant Fusion Proteins / pharmacology
  • Temporal Arteries / metabolism
  • Temporal Arteries / pathology
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Interleukin-1
  • Interleukin-6
  • RNA, Messenger
  • Receptors, Interleukin
  • Receptors, Interleukin-6
  • Recombinant Fusion Proteins
  • Tumor Necrosis Factor-alpha
  • interleukin 6-interleukin 6 receptor fusion protein, recombinant