EBI3 downregulation contributes to type I collagen overexpression in scleroderma skin

Journal of Immunology

Volumn 195, Issue 8, 2015, Pages 3565-3573

  Kudo, Hideo ^a   Wang, Zhongzhi ^a   Jinnin, Masatoshi ^a   Nakayama, Wakana ^a   Inoue, Kuniko ^a   Honda, Noritoshi ^a   Nakashima, Taiji ^a   Kajihara, Ikko ^a   Makino, Katsunari ^a   Makino, Takamitsu ^a   Fukushima, Satoshi ^a   Ihn, Hironobu ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; EBI3 PROTEIN; GLYCOPROTEIN GP 130; INTERLEUKIN 35; MICRORNA; MICRORNA 4500; REGULATOR PROTEIN; UNCLASSIFIED DRUG; CYTOKINE RECEPTOR; EBI3 PROTEIN, HUMAN; EBI3 PROTEIN, MOUSE; IL6ST PROTEIN, MOUSE; INTERLEUKIN DERIVATIVE; MESSENGER RNA;

ADULT; AGED; ARTICLE; CELL SURFACE; CLINICAL ARTICLE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; CYTOLYSIS; DOWN REGULATION; EBI3 GENE; EPIDERMIS; EXTRACELLULAR MATRIX; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; MALE; PRIORITY JOURNAL; REGULATOR GENE; REGULATORY T LYMPHOCYTE; SCLERODERMA; SIGNAL TRANSDUCTION; SKIN FIBROBLAST; SKIN FIBROSIS; ANIMAL; DIFFUSE SCLERODERMA; GENETICS; IMMUNOLOGY; MIDDLE AGED; MOUSE; PATHOLOGY; RNA STABILITY; SKIN; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; COLLAGEN TYPE I; CYTOKINE RECEPTOR GP130; DOWN-REGULATION; FEMALE; HUMANS; INTERLEUKINS; MALE; MICE; MIDDLE AGED; RECEPTORS, CYTOKINE; RNA STABILITY; RNA, MESSENGER; SCLERODERMA, DIFFUSE; SKIN; T-LYMPHOCYTES, REGULATORY;

EID: 84943545805     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402362     Document Type: Article

References (45)

1. Uitto, J., and D. Kouba. 2000. Cytokine modulation of extracellular matrix gene expression: relevance to fibrotic skin diseases. J. Dermatol. Sci. 24(Suppl. 1):S60-S69.
2. Trojanowska, M., E. C. LeRoy, B. Eckes, and T. Krieg. 1998. Pathogenesis of fibrosis: type 1 collagen and the skin. J. Mol. Med. 76:266-274.
3. Varga, J., and D. Abraham. 2007. Systemic sclerosis: a prototypic multisystem fibrotic disorder. J. Clin. Invest. 117:557-567.
4. Gabrielli, A., E. V. Avvedimento, and T. Krieg. 2009. Scleroderma. N. Engl. J. Med. 360:1989-2003.
5. Ihn, H., K. Yamane, M. Kubo, and K. Tamaki. 2001. Blockade of endogenous transforming growth factor β signaling prevents up-regulated collagen synthesis in scleroderma fibroblasts: association with increased expression of transforming growth factor β receptors. Arthritis Rheum. 44:474-480.
6. Asano, Y., H. Ihn, K. Yamane, M. Kubo, and K. Tamaki. 2004. Impaired Smad7-Smurf-mediated negative regulation of TGF-β signaling in scleroderma fibroblasts. J. Clin. Invest. 113:253-264.
7. Takehara, K. 2003. Hypothesis: pathogenesis of systemic sclerosis. J. Rheumatol. 30:755-759.
8. 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-b 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.
9. Brissett, M., K. L. Veraldi, J. M. Pilewski, T. A. Medsger, Jr., and C. A. Feghali-Bostwick. 2012. Localized expression of tenascin in systemic sclerosisassociated pulmonary fibrosis and its regulation by insulin-like growth factor binding protein 3. Arthritis Rheum. 64:272-280.
10. Kawaguchi, Y. 1994. IL-1 a gene expression and protein production by fibroblasts from patients with systemic sclerosis. Clin. Exp. Immunol. 97:445-450.
11. 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.
12. Makino, T., S. Fukushima, S. Wakasugi, and H. Ihn. 2009. Decreased serum IL-7 levels in patients with systemic sclerosis. Clin. Exp. Rheumatol. 27(3 Suppl. 54):68-69.
13. 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.
14. Maricq, H. R., M. C. Weinrich, J. E. Keil, E. A. Smith, F. E. Harper, A. I. Nussbaum, E. C. LeRoy, A. R. McGregor, F. Diat, and E. J. Rosal. 1989. Prevalence of scleroderma spectrum disorders in the general population of South Carolina. Arthritis Rheum. 32:998-1006.
15. Maricq, H. R., A. R. McGregor, F. Diat, E. A. Smith, D. B. Maxwell, E. C. LeRoy, and M. C. Weinrich. 1990. Major clinical diagnoses found among patients with Raynaud phenomenon from the general population. J. Rheumatol. 17:1171-1176.
16. Ihn, H., S. Sato, T. Tamaki, Y. Soma, T. Tsuchida, Y. Ishibashi, and K. Takehara. 1992. Clinical evaluation of scleroderma spectrum disorders using a points system. Arch. Dermatol. Res. 284:391-395.
17. Higashi-Kuwata, N., M. Jinnin, T. Makino, S. Fukushima, Y. Inoue, F. C. Muchemwa, Y. Yonemura, Y. Komohara, M. Takeya, H. Mitsuya, and H. Ihn. 2010. Characterization of monocyte/macrophage subsets in the skin and peripheral blood derived from patients with systemic sclerosis. Arthritis Res. Ther. 12:R128.
18. Wang, R. X., C. R. Yu, I. M. Dambuza, R. M. Mahdi, M. B. Dolinska, Y. V. Sergeev, P. T. Wingfield, S. H. Kim, and C. E. Egwuagu. 2014. Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nat. Med. 20:633-641.
19. Honda, N., M. Jinnin, T. Kira-Etoh, K. Makino, I. Kajihara, T. Makino, S. Fukushima, Y. Inoue, Y. Okamoto, M. Hasegawa, et al. 2013. miR-150 downregulation contributes to the constitutive type I collagen overexpression in scleroderma dermal fibroblasts via the induction of integrin b3. Am. J. Pathol. 182:206-216.
20. Trappoliere, M., A. Caligiuri, M. Schmid, C. Bertolani, P. Failli, F. Vizzutti, E. Novo, C. di Manzano, F. Marra, C. Loguercio, and M. Pinzani. 2009. Silybin, a component of sylimarin, exerts anti-inflammatory and anti-fibrogenic effects on human hepatic stellate cells. J. Hepatol. 50:1102-1111.
21. Jinnin, M., T. Makino, I. Kajihara, N. Honda, K. Makino, A. Ogata, and H. Ihn. 2010. Serum levels of soluble vascular endothelial growth factor receptor-2 in patients with systemic sclerosis. Br. J. Dermatol. 162:751-758.
22. Ihn, H., K. Ohnishi, T. Tamaki, E. C. LeRoy, and M. Trojanowska. 1996. Transcriptional regulation of the human a2 (I) collagen gene. Combined action of upstream stimulatory and inhibitory cis-acting elements. J. Biol. Chem. 271:26717-26723.
23. Filippova, M., H. Song, J. L. Connolly, T. S. Dermody, and P. J. Duerksen-Hughes. 2002. The human papillomavirus 16 E6 protein binds to tumor necrosis factor (TNF) R1 and protects cells from TNF-induced apoptosis. J. Biol. Chem. 277:21730-21739.
24. Ma, J., and L. Z. Xie. 2013. [Eukaryotic expression and biological activity of human interleukin-35]. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 35:618-622.
25. Jinnin, M., D. Medici, L. Park, N. Limaye, Y. Liu, E. Boscolo, J. Bischoff, M. Vikkula, E. Boye, and B. R. Olsen. 2008. Suppressed NFAT-dependent VEGFR1 expression and constitutive VEGFR2 signaling in infantile hemangioma. Nat. Med. 14:1236-1246.
26. 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.
27. Yamamoto, T., M. Kuroda, and K. Nishioka. 2000. Animal model of sclerotic skin. III: Histopathological comparison of bleomycin-induced scleroderma in various mice strains. Arch. Dermatol. Res. 292:535-541.
28. Oi, M., T. Yamamoto, and K. Nishioka. 2004. Increased expression of TGFbeta1 in the sclerotic skin in bleomycin-'susceptible' mouse strains. J. Med. Dent. Sci. 51:7-17.
29. 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.
30. Probert, P. M. E., M. R. Ebrahimkhani, F. Oakley, M. Mann, A. D. Burt, and D. A. Mann, and M. C. Wright. 2014. A reversible model for periportal fibrosis and a refined alternative to bile duct ligation. Toxicol. Res. 3:98-109.
31. Marotta, M., and G. Martino. 1985. Sensitive spectrophotometric method for the quantitative estimation of collagen. Anal. Biochem. 150:86-90.
32. Antiga, E., P. Quaglino, S. Bellandi, W. Volpi, E. Del Bianco, A. Comessatti, S. Osella-Abate, C. De Simone, A. Marzano, M. G. Bernengo, et al. 2010. Regulatory T cells in the skin lesions and blood of patients with systemic sclerosis and morphoea. Br. J. Dermatol. 162:1056-1063.
33. Klein, S., C. C. Kretz, V. Ruland, C. Stumpf, M. Haust, W. Hartschuh, M. Hartmann, A. Enk, E. Suri-Payer, N. Oberle, et al. 2011. Reduction of regulatory T cells in skin lesions but not in peripheral blood of patients with systemic scleroderma. Ann. Rheum. Dis. 70:1475-1481.
34. Neurath, M. F. 2008. IL-12 family members in experimental colitis. Mucosal Immunol. 1(Suppl. 1):S28-S30.
35. Seyerl, M., S. Kirchberger, O. Majdic, J. Seipelt, C. Jindra, C. Schrauf, and J. Stöckl. 2010. Human rhinoviruses induce IL-35-producing Treg via induction of B7-H1 (CD274) and sialoadhesin (CD169) on DC. Eur. J. Immunol. 40:321-329.
36. Maaser, C., L. J. Egan, M. P. Birkenbach, L. Eckmann, and M. F. Kagnoff. 2004. Expression of Epstein-Barr virus-induced gene 3 and other interleukin-12-related molecules by human intestinal epithelium. Immunology 112:437-445.
37. Kempe, S., P. Heinz, E. Kokai, O. Devergne, N. Marx, and T. Wirth. 2009. Epstein-barr virus-induced gene-3 is expressed in human atheroma plaques. Am. J. Pathol. 175:440-447.
38. Niedbala, W., X. Q. Wei, B. Cai, A. J. Hueber, B. P. Leung, I. B. McInnes, and F. Y. Liew. 2007. IL-35 is a novel cytokine with therapeutic effects against collagen-induced arthritis through the expansion of regulatory T cells and suppression of Th17 cells. Eur. J. Immunol. 37:3021-3029.
39. Nakashima, T., M. Jinnin, K. Yamane, N. Honda, I. Kajihara, T. Makino, S. Masuguchi, S. Fukushima, Y. Okamoto, M. Hasegawa, et al. 2012. Impaired IL-17 signaling pathway contributes to the increased collagen expression in scleroderma fibroblasts. J. Immunol. 188:3573-3583.
40. Apras, S., I. Ertenli, Z. Ozbalkan, S. Kiraz, M. A. Ozturk, I. C. Haznedaroglu, V. Cobankara, S. Pay, and M. Calguneri. 2003. Effects of oral cyclophosphamide and prednisolone therapy on the endothelial functions and clinical findings in patients with early diffuse systemic sclerosis. Arthritis Rheum. 48:2256-2261.
41. Pope, J. E., N. Bellamy, J. R. Seibold, M. Baron, M. Ellman, S. Carette, C. D. Smith, I. M. Chalmers, P. Hong, D. O'Hanlon, et al. 2001. A randomized, controlled trial of methotrexate versus placebo in early diffuse scleroderma. Arthritis Rheum. 44:1351-1358.
42. Haustein, U. F. 2002. Systemic sclerosis-scleroderma. Dermatol. Online J. 8:3.
43. Yamamoto, T., S. Takagawa, M. Kuroda, and K. Nishioka. 2000. Effect of interferon-gamma on experimental scleroderma induced by bleomycin. Arch. Dermatol. Res. 292:362-365.
44. Koca, S. S., A. Isik, I. H. Ozercan, B. Ustundag, B. Evren, and K. Metin. 2008. Effectiveness of etanercept in bleomycin-induced experimental scleroderma. Rheumatology (Oxford) 47:172-175.
45. Arai, M., Y. Ikawa, S. Chujo, Y. Hamaguchi, W. Ishida, F. Shirasaki, M. Hasegawa, N. Mukaida, M. Fujimoto, and K. Takehara. 2013. Chemokine receptors CCR2 and CX3CR1 regulate skin fibrosis in the mouse model of cytokine-induced systemic sclerosis. J. Dermatol. Sci. 69:250-258.