Impaired IL-17 signaling pathway contributes to the increased collagen expression in scleroderma fibroblasts

Journal of Immunology

Volumn 188, Issue 8, 2012, Pages 3573-3583

  Nakashima, Taiji ^a   Jinnin, Masatoshi ^a   Yamane, Keitaro ^a   Honda, Noritoshi ^a   Kajihara, Ikko ^a   Makino, Takamitsu ^a   Masuguchi, Shinichi ^a   Fukushima, Satoshi ^a   Okamoto, Yoshinobu ^b   Hasegawa, Minoru ^b   Fujimoto, Manabu ^b   Ihn, Hironobu ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b KANAZAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; COLLAGEN ALPHA1 CHAIN; CONNECTIVE TISSUE GROWTH FACTOR; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 17F; MICRORNA; MIR 129 5P; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ADULT; AGED; AMINO ACID SEQUENCE; ARTICLE; AUTOIMMUNE DISEASE; CELL TYPE; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EXTRACELLULAR MATRIX; FEMALE; FIBROBLAST; FIBROSIS; GENE CONTROL; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; NEGATIVE FEEDBACK; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; RECEPTOR DOWN REGULATION; SCLERODERMA; SEQUENCE HOMOLOGY; SERUM; SIGNAL TRANSDUCTION; SKIN; SYSTEMIC SCLEROSIS; UPREGULATION;

ADULT; AGED; AGED, 80 AND OVER; CELLS, CULTURED; COLLAGEN; CONNECTIVE TISSUE GROWTH FACTOR; EXTRACELLULAR MATRIX; FEMALE; FIBROBLASTS; FIBROSIS; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-17; MALE; MICRORNAS; MIDDLE AGED; RECEPTORS, INTERLEUKIN-17; SCLERODERMA, SYSTEMIC; SIGNAL TRANSDUCTION; SKIN; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84860330745     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100591     Document Type: Article

References (53)

1. Korn, J. H. 1989. Immunologic aspects of scleroderma. Curr. Opin. Rheumatol. 1: 479-484. (Pubitemid 20125933)
2. Mauch, C., and T. Kreig. 1990. Fibroblast-matrix interactions and their role in the pathogenesis of fibrosis. Rheum. Dis. Clin. North Am. 16: 93-107. (Pubitemid 20116147)
3. Mauch, C., E. Kozlowska, B. Eckes, and T. Krieg. 1992. Altered regulation of collagen metabolism in scleroderma fibroblasts grown within three-dimensional collagen gels. Exp. Dermatol. 1: 185-190.
4. Jelaska, A., M. Arakawa, G. Broketa, and J. H. Korn. 1996. Heterogeneity of collagen synthesis in normal and systemic sclerosis skin fibroblasts. Increased proportion of high collagen-producing cells in systemic sclerosis fibroblasts. Arthritis Rheum. 39: 1338-1346. (Pubitemid 26270093)
5. Massagué, J. 1990. The transforming growth factor-β family. Annu. Rev. Cell Biol. 6: 597-641.
6. Leroy, E. C., E. A. Smith, M. B. Kahaleh, M. Trojanowska, and R. M. Silver. 1989. A strategy for determining the pathogenesis of systemic sclerosis. Is transforming growth factor b the answer? Arthritis Rheum. 32: 817-825. (Pubitemid 19181003)
7. LeRoy, E. C. 1974. Increased collagen synthesis by scleroderma skin fibroblasts in vitro: a possible defect in the regulation or activation of the scleroderma fibroblast. J. Clin. Invest. 54: 880-889.
8. Jimenez, S. A., G. Feldman, R. I. Bashey, R. Bienkowski, and J. Rosenbloom. 1986. Co-ordinate increase in the expression of type I and type III collagen genes in progressive systemic sclerosis fibroblasts. Biochem. J. 237: 837-843. (Pubitemid 16003787)
9. Kikuchi, K., C. W. Hartl, E. A. Smith, E. C. LeRoy, and M. Trojanowska. 1992. Direct demonstration of transcriptional activation of collagen gene expression in systemic sclerosis fibroblasts: insensitivity to TGF beta 1 stimulation. Biochem. Biophys. Res. Commun. 187: 45-50.
10. Hitraya, E. G., and S. A. Jiménez. 1996. Transcriptional activation of the a 1(I) procollagen gene in systemic sclerosis dermal fibroblasts. Role of intronic sequences. Arthritis Rheum. 39: 1347-1354. (Pubitemid 26270094)
11. Ihn, H., K. Yamane, M. Kubo, and K. Tamaki. 2001. Blockade of endogenous transforming growth factor b signaling prevents up-regulated collagen synthesis in scleroderma fibroblasts: association with increased expression of transforming growth factor b receptors. Arthritis Rheum. 44: 474-480.
12. Asano, Y., H. Ihn, K. Yamane, M. Kubo, and K. Tamaki. 2004. Impaired Smad7Smurf-mediated negative regulation of TGF-β signaling in scleroderma fibroblasts. J. Clin. Invest. 113: 253-264. (Pubitemid 38544210)
13. Takehara, K. 2003. Hypothesis: pathogenesis of systemic sclerosis. J. Rheumatol. 30: 755-759.
14. Kawaguchi, Y. 1994. IL-1 a gene expression and protein production by fibroblasts from patients with systemic sclerosis. Clin. Exp. Immunol. 97: 445-450.
15. Feghali, C. A., K. L. Bost, D. W. Boulware, and L. S. Levy. 1992. Mechanisms of pathogenesis in scleroderma. I. Overproduction of interleukin 6 by fibroblasts cultured from affected skin sites of patients with scleroderma. J. Rheumatol. 19: 1207-1211.
16. Overbeek, M. J., A Boonstra, A. E. Voskuyl, M. C. Vonk, A. Vonk-Noordegraaf, M. P. van Berkel, W. J. Mooi, B. A. Dijkmans, L. S. Hondema, E. F. Smit, and K. Grünberg. 2011. Platelet-derived growth factor receptor-β and epidermal growth factor receptor in pulmonary vasculature of systemic sclerosis-associated pulmonary arterial hypertension versus idiopathic pulmonary arterial hypertension and pulmonary veno-occlusive disease: a case-control study. Arthritis Res. Ther. 13: R61.
17. Brissett, M., K. L. Veraldi, J. M. Pilewski, T. A. Medsger, Jr., and C. A. Feghali-Bostwick. 2011. Localized expression of tenascin in systemic sclerosis-associated lung fibrosis and its regulation by IGF binding protein (IGFBP)-3. Arthritis Rheum. 64: 272-280.
18. Aggarwal, S., N. Ghilardi, M. H. Xie, F. J. de Sauvage, and A. L. Gurney. 2003. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 278: 1910-1914. (Pubitemid 36801431)
19. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
20. Harrington, L. E., R. D. Hatton, P. R. Mangan, H. Turner, T. L. Murphy, K. M. Murphy, and C. T. Weaver. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132. (Pubitemid 41541790)
21. Iwakura, Y., and H. Ishigame. 2006. The IL-23/IL-17 axis in inflammation. J. Clin. Invest. 116: 1218-1222.
22. Hymowitz, S. G., E. H. Filvaroff, J. P. Yin, J. Lee, L. Cai, P. Risser, M. Maruoka, W. Mao, J. Foster, R. F. Kelley, et al. 2001. IL-17s adopt a cystine knot fold: structure and activity of a novel cytokine, IL-17F, and implications for receptor binding. EMBO J. 20: 5332-5341. (Pubitemid 32959452)
23. Yao, Z., M. K. Spriggs, J. M. Derry, L. Strockbine, L. S. Park, T. VandenBos, J. D. Zappone, S. L. Painter, and R. J. Armitage. 1997. Molecular characterization of the human interleukin (IL)-17 receptor. Cytokine 9: 794-800. (Pubitemid 27494143)
24. Ye, P., F. H. Rodriguez, S. Kanaly, K. L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, et al. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colonystimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194: 519-527. (Pubitemid 32835046)
25. Yao, Z., W. C. Fanslow, M. F. Seldin, A. M. Rousseau, S. L. Painter, M. R. Comeau, J. I. Cohen, and M. K. Spriggs. 1995. Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 3: 811-821. (Pubitemid 26091152)
26. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201: 233-240. (Pubitemid 40189432)
27. Park, H., Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6: 1133-1141. (Pubitemid 41541791)
28. Arican, O., M. Aral, S. Sasmaz, and P. Ciragil. 2005. Serum levels of TNF-α, IFN-γ, IL-6, IL-8, IL-12, IL-17, and IL-18 in patients with active psoriasis and correlation with disease severity. Mediators Inflamm. 2005: 273-279. (Pubitemid 41577417)
29. Bessis, N., and M. C. Boissier. 2001. Novel pro-inflammatory interleukins: potential therapeutic targets in rheumatoid arthritis. Joint Bone Spine 68: 477-481. (Pubitemid 34037276)
30. Fujino, S., A. Andoh, S. Bamba, A. Ogawa, K. Hata, Y. Araki, T. Bamba, and Y. Fujiyama. 2003. Increased expression of interleukin 17 in inflammatory bowel disease. Gut 52: 65-70. (Pubitemid 36020767)
31. Kawaguchi, M., L. F. Onuchic, X. D. Li, D. M. Essayan, J. Schroeder, H. Q. Xiao, M. C. Liu, G. Krishnaswamy, G. Germino, and S. K. Huang. 2001. Identification of a novel cytokine, ML-1, and its expression in subjects with asthma. J. Immunol. 167: 4430-4435. (Pubitemid 32954320)
32. Lubberts, E., L. A. Joosten, M. Chabaud, L. van Den Bersselaar, B. Oppers, C. J. Coenen-De Roo, C. D. Richards, P. Miossec, and W. B. van Den Berg. 2000. IL-4 gene therapy for collagen arthritis suppresses synovial IL-17 and osteoprotegerin ligand and prevents bone erosion. J. Clin. Invest. 105: 1697-1710. (Pubitemid 30421751)
33. Murata, M., M. Fujimoto, T. Matsushita, Y. Hamaguchi, M. Hasegawa, K. Takehara, K. Komura, and S. Sato. 2008. Clinical association of serum interleukin-17 levels in systemic sclerosis: is systemic sclerosis a Th17 disease? J. Dermatol. Sci. 50: 240-242.
34. Kurasawa, K., K. Hirose, H. Sano, H. Endo, H. Shinkai, Y. Nawata, K. Takabayashi, and I. Iwamoto. 2000. Increased interleukin-17 production in patients with systemic sclerosis. Arthritis Rheum. 43: 2455-2463.
35. Gourh, P., F. C. Arnett, S. Assassi, F. K. Tan, M. Huang, L. Diekman, M. D. Mayes, J. D. Reveille, and S. K. Agarwal. 2009. Plasma cytokine profiles in systemic sclerosis: associations with autoantibody subsets and clinical manifestations. Arthritis Res. Ther. 11: R147.
36. LeRoy, E. C., C. Black, R. Fleischmajer, S. Jablonska, T. Krieg, T. A. J. Medsger, Jr., N. Rowell, and F. Wollheim. 1988. Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J. Rheumatol. 15: 202-205. (Pubitemid 18073738)
37. Subcommittee for scleroderma criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee. 1980. Preliminary criteria for the classification of systemic sclerosis (scleroderma). Arthritis Rheum. 23: 581-590.
38. Ihn, H., E. C. LeRoy, and M. Trojanowska. 1997. Oncostatin M stimulates transcription of the human a2(I) collagen gene via the Sp1/Sp3-binding site. J. Biol. Chem. 272: 24666-24672. (Pubitemid 27418684)
39. Yamamoto, T., S. Takagawa, I. Katayama, K. Yamazaki, Y. Hamazaki, H. Shinkai, and K. Nishioka. 1999. Animal model of sclerotic skin. I: Local injections of bleomycin induce sclerotic skin mimicking scleroderma. J. Invest. Dermatol. 112: 456-462. (Pubitemid 29171935)
40. Tanaka, C., M. Fujimoto, Y. Hamaguchi, S. Sato, K. Takehara, and M. Hasegawa. 2010. Inducible costimulator ligand regulates bleomycin-induced lung and skin fibrosis in a mouse model independently of the inducible costimulator/inducible costimulator ligand pathway. Arthritis Rheum. 62: 1723-1732.
41. Johansen, C., P. A. Usher, R. B. Kjellerup, D. Lundsgaard, L. Iversen, and K. Kragballe. 2009. Characterization of the interleukin-17 isoforms and receptors in lesional psoriatic skin. Br. J. Dermatol. 160: 319-324.
42. Arai, K. Y., and T. Nishiyama. 2007. Developmental changes in extracellular matrix messenger RNAs in the mouse placenta during the second half of pregnancy: possible factors involved in the regulation of placental extracellular matrix expression. Biol. Reprod. 77: 923-933. (Pubitemid 350197969)
43. Jinnin, M., H. Ihn, Y. Asano, K. Yamane, M. Trojanowska, and K. Tamaki. 2004. Tenascin-C upregulation by transforming growth factor-beta in human dermal fibroblasts involves Smad3, Sp1, and Ets1. Oncogene 23: 1656-1667. (Pubitemid 38445158)
44. Yuan, W., and J. Varga. 2001. Transforming growth factor-β repression of matrix metalloproteinase-1 in dermal fibroblasts involves Smad3. J. Biol. Chem. 276: 38502-38510.
45. Lewis, B. P., C. B. Burge, and D. P. Bartel. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20. (Pubitemid 40094598)
46. Long, J. M., and D. K. Lahiri. 2011. MicroRNA-101 downregulates Alzheimer's amyloid-β precursor protein levels in human cell cultures and is differentially expressed. Biochem. Biophys. Res. Commun. 404: 889-895.
47. Kuehbacher, A., C. Urbich, and S. Dimmeler. 2008. Targeting microRNA expression to regulate angiogenesis. Trends Pharmacol. Sci. 29: 12-15.
48. Chen, Y., and D. H. Gorski. 2008. Regulation of angiogenesis through a microRNA (miR-130a) that down-regulates antiangiogenic homeobox genes GAX and HOXA5. Blood 111: 1217-1226. (Pubitemid 351213403)
49. Furer, V., J. D. Greenberg, M. Attur, S. B. Abramson, and M. H. Pillinger. 2010. The role of microRNA in rheumatoid arthritis and other autoimmune diseases. Clin. Immunol. 136: 1-15.
50. Lu, L. F., and A. Liston. 2009. MicroRNA in the immune system, microRNA as an immune system. Immunology 127: 291-298.
51. Davidson-Moncada, J., F. N. Papavasiliou, and W. Tam. 2010. MicroRNAs of the immune system: roles in inflammation and cancer. Ann. N. Y. Acad. Sci. 1183: 183-194.
52. Hymowitz, S. G., E. H. Filvaroff, J. P. Yin, J. Lee, L. Cai, P. Risser, M. Maruoka, W. Mao, J. Foster, R. F. Kelley, et al. 2001. IL-17s adopt a cystine knot fold: structure and activity of a novel cytokine, IL-17F, and implications for receptor binding. EMBO J. 20: 5332-5341. (Pubitemid 32959452)
53. Kuestner, R. E., D. W. Taft, A. Haran, C. S. Brandt, T. Brender, K. Lum, B. Harder, S. Okada, C. D. Ostrander, J. L. Kreindler, et al. 2007. Identification of the IL-17 receptor related molecule IL-17RC as the receptor for IL-17F. J. Immunol. 179: 5462-5473.