Interleukin-17 enhances tumor necrosis factor alpha-induced synthesis of interleukins 1,6, and 8 in skin and synovial fibroblasts: a possible role as a "fine-tuning cytokine" in inflammation processes

Arthritis Rheum. 2001 Sep;44(9):2176-84. doi: 10.1002/1529-0131(200109)44:9<2176::aid-art371>3.0.co;2-4.

Abstract

Objective: To compare the singular and combined effects of tumor necrosis factor alpha (TNFalpha), interleukin-1beta (IL-1beta), and IL-17 on messenger RNA (mRNA) expression, translation, and secretion of IL-6, IL-8, and IL-1beta in fibroblasts.

Methods: Fibroblasts were stimulated with the relevant cytokine(s), pulse labeled with 35S-methionine, and the newly synthesized proteins were immunoprecipitated and subjected to sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Gene expression was determined by Northern blot analysis. Secreted proteins were detected by enzyme-linked immunosorbent assay (ELISA).

Results: IL-17 alone was a weaker stimulator of the transcription, translation, and secretion of other interleukins than was TNFalpha or IL-1beta. IL-17 (10 ng/ml) stimulated the expression of IL-6 mRNA by 1.3-fold, while TNFalpha (1 ng/ml) increased it by 3.7-fold, and IL-1beta (0.1 ng/ml) increased it by >30-fold. Unlike TNFalpha and IL-1beta, IL-17 hardly affected the expression of IL-8 and IL-1beta mRNA. Translation of IL-6 was 6.2 times greater with IL-17, but TNFalpha and IL-1beta stimulated it 28.9- and 174-fold, respectively. ELISA-measured secretion of IL-6 and IL-8 increased by 6.7 and 5.8 times, respectively, with IL-17, compared with 52 and 269 times with TNFalpha stimulation and 1,356 and 1,084 times with IL-1beta stimulation. Yet, when IL-17 was combined with other cytokines, these activities were stimulated much beyond the sum of the individual effects. The combination of IL-17 and TNFalpha induced the expression of IL-6 or IL-1beta mRNA 7 times more than their additive stimulation, and that of IL-8 mRNA 3.8 times more. Likewise, the secretion of IL-6 and IL-8 was 20 times and 5 times higher, respectively, than expected. This synergism started after 4 hours of combined treatment, and decayed after 24-48 hours regardless of cytokine presence. It could be blocked with anti-IL-17 but not with anti-IL-1.

Conclusion: Our findings suggest that the primary role of IL-17 is to synergize with TNFalpha and to fine-tune the inflammation process. Therefore, IL-17 may be a potential target for therapeutic intervention.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • Drug Synergism
  • Enzyme-Linked Immunosorbent Assay
  • Fibroblasts / cytology
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Gene Expression / drug effects
  • Gene Expression / immunology
  • Humans
  • Inflammation / drug therapy
  • Inflammation / immunology
  • Inflammation / metabolism
  • Interleukin-1 / genetics*
  • Interleukin-1 / metabolism
  • Interleukin-17 / pharmacology*
  • Interleukin-6 / genetics
  • Interleukin-6 / metabolism
  • Interleukin-8 / genetics
  • Interleukin-8 / metabolism
  • RNA, Messenger / analysis
  • Skin / cytology
  • Synovial Membrane / cytology*
  • Tumor Necrosis Factor-alpha / pharmacology*

Substances

  • Interleukin-1
  • Interleukin-17
  • Interleukin-6
  • Interleukin-8
  • RNA, Messenger
  • Tumor Necrosis Factor-alpha