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Review

Fibroblast abnormalities in the pathogenesis of systemic sclerosis

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Pages 491-498 | Published online: 10 Jan 2014

References

  • Silver RM. Clinical aspects of localized and systemic scleroderma. Curr. Opin. Rheumatol.3, 973–978 (1991).
  • LeRoy EC, Medsger TA Jr. Criteria for the classification of early systemic sclerosis. J. Rheumatol.28, 1573–1576 (2001).
  • Abraham DJ, Varga J. Scleroderma: from cell and molecular mechanisms to disease models. Trends Immunol.26, 587–595 (2005).
  • Steen VD, Medsger TA Jr. Severe organ involvement in systemic sclerosis with diffuse scleroderma. Arthritis Rheum.43, 2437–2444 (2000).
  • Arnett FC, Cho M, Chatterjee S, Aguilar MB, Reveille JD, Mayes MD. Familial occurrence frequencies and relative risks for systemic sclerosis (scleroderma) in three United States cohorts. Arthritis Rheum.44, 1359–1362 (2001).
  • Radstake TR, Gorlova O, Rueda B et al. Genome-wide association study of systemic sclerosis identifies CD247 as a new susceptibility locus. Nat. Genet.42, 426–429 (2010).
  • Dieudé P, Guedj M, Wipff J et al. The PTPN22 620W allele confers susceptibility to systemic sclerosis: findings of a large case-control study of European Caucasians and a meta-analysis. Arthritis Rheum.58, 2183–2188 (2008).
  • Rueda B, Broen J, Simeon C et al. The STAT4 gene influences the genetic predisposition to systemic sclerosis phenotype. Hum. Mol. Genet.18, 2071–2077 (2009).
  • Zhou X, Tan FK, Reveille JD et al. Association of novel polymorphisms with the expression of SPARC in normal fibroblasts and with susceptibility to scleroderma. Arthritis Rheum.46, 2990–2999 (2002).
  • Tan FK, Wang N, Kuwana M et al. Association of fibrillin 1 single-nucleotide polymorphism haplotypes with systemic sclerosis in Choctaw and Japanese populations. Arthritis Rheum.44, 893–901 (2001).
  • Fonseca C, Lindahl GE, Ponticos M et al. A polymorphism in the CTGF promoter region associated with systemic sclerosis. N. Engl. J. Med.357, 1210–1220 (2007).
  • Rueda B, Simeon C, Hesselstrand R et al. A large multicenter analysis of CTGF -945 promoter polymorphism does not confirm association with systemic sclerosis susceptibility or phenotype. Ann. Rheum. Dis.68, 1618–1620 (2009).
  • Rogai V, Lories RJ, Guiducci S, Luyten FP, Matucci Cerinic M. Animal models in systemic sclerosis. Clin. Exp. Rheumatol.26, 941–946 (2008).
  • LeRoy EC. 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 (1974).
  • Hitraya EG, Jiménez SA. Transcriptional activation of the α 1(I) procollagen gene in systemic sclerosis dermal fibroblasts. Role of intronic sequences. Arthritis Rheum.39, 1347–1354 (1996).
  • Jimenez SA, Hitraya E, Varga J. Pathogenesis of scleroderma. Collagen. Rheum. Dis. Clin. North Am.22, 647–674 (1996).
  • Leroy EC. Connective tissue synthesis by scleroderma skin fibroblasts in cell culture. J. Exp. Med.135, 1351–1362 (1972).
  • Botstein GR, Sherer GK, Leroy EC. Fibroblast selection in scleroderma. An alternative model of fibrosis. Arthritis Rheum.25, 189–195 (1982).
  • Jelaska A, Arakawa M, Broketa G, Korn JH. 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 (1996).
  • Jimenez SA, Saitta B. Alterations in the regulation of expression of the α 1(I) collagen gene (COL1A1) in systemic sclerosis (scleroderma). Springer Semin. Immunopathol.21, 397–414 (1999).
  • Jelaska A, Korn JH. Role of apoptosis and transforming growth factor β1 in fibroblast selection and activation in systemic sclerosis. Arthritis Rheum.43, 2230–2239 (2000).
  • Santiago B, Galindo M, Rivero M, Pablos JL. Decreased susceptibility to Fas induced apoptosis of systemic sclerosis dermal fibroblasts. Arthritis Rheum.44, 1667–1676 (2001).
  • Yamakage A, Kikuchi K, Smith EA, LeRoy EC, Trojanowska M. Selective upregulation of platelet-derived growth factor α receptors by transforming growth factor β in scleroderma fibroblasts. J. Exp. Med.175, 1227–1234 (1992).
  • Whitfield ML, Finlay DR, Murray JI et al. Systemic and cell type-specific gene expression patterns in scleroderma skin. Proc. Natl Acad. Sci. USA100, 12319–12324 (2003).
  • Gardner H, Shearstone JR, Bandaru R et al. Gene profiling of scleroderma skin reveals robust signatures of disease that are imperfectly reflected in the transcript profiles of explanted fibroblasts. Arthritis Rheum.54, 1961–1973 (2006).
  • Kissin EY, Merkel PA, Lafyatis R. Myofibroblasts and hyalinized collagen as markers of skin disease in systemic sclerosis. Arthritis Rheum.54, 3655–3660 (2006).
  • Rajkumar VS, Howell K, Csiszar K, Denton CP, Black CM, Abraham DJ. Shared expression of phenotypic markers in systemic sclerosis indicates a convergence of pericytes and fibroblasts to a myofibroblast lineage in fibrosis. Arthritis Res. Ther.7, R1113–R1123 (2005).
  • Farina G, Lemaire R, Pancari P, Bayle J, Widom RL, Lafyatis R. Cartilage oligomeric matrix protein expression in systemic sclerosis reveals heterogeneity of dermal fibroblast responses to transforming growth factor β. Ann. Rheum. Dis.68, 435–441 (2009).
  • Desmoulière A, Chaponnier C, Gabbiani G. Tissue repair, contraction, and the myofibroblast. Wound Repair Regen.13, 7–12 (2005).
  • Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The myofibroblast: one function, multiple origins. Am. J. Pathol.170, 1807–1816 (2007).
  • Hu B, Gharaee-Kermani M, Wu Z, Phan SH. Epigenetic regulation of myofibroblast differentiation by DNA methylation. Am. J. Pathol.177, 21–28 (2010).
  • Chesney J, Bacher M, Bender A, Bucala R. The peripheral blood fibrocyte is a potent antigen-presenting cell capable of priming naive T cells in situ. Proc. Natl Acad. Sci. USA94, 6307–6312 (1997).
  • Abe R, Donnelly SC, Peng T, Bucala R, Metz CN. Peripheral blood fibrocytes: differentiation pathway and migration to wound sites. J. Immunol.166, 7556–7562 (2001).
  • Shao DD, Suresh R, Vakil V, Gomer RH, Pilling D. Pivotal advance: Th-1 cytokines inhibit, and Th-2 cytokines promote fibrocyte differentiation. J. Leukoc. Biol.83, 1323–1333 (2008)
  • Pilling D, Buckley CD, Salmon M, Gomer RH. Inhibition of fibrocyte differentiation by serum amyloid P. J. Immunol.171, 5537–5546 (2003).
  • Phillips RJ, Burdick MD, Hong K et al. Circulating fibrocytes traffic to the lungs in response to CXCL12 and mediate fibrosis. J. Clin. Invest.114, 438–446 (2004).
  • Schmidt M, Sun G, Stacey MA, Mori L, Mattoli S. Identification of circulating fibrocytes as precursors of bronchial myofibroblasts in asthma. J. Immunol.171, 380–389 (2003).
  • Ortonne N, Lipsker D, Chantrel F, Boehm N, Grosshans E, Cribier B. Presence of CD45RO+ CD34+ cells with collagen syntesis activity in nephrogenic fibrosing dermopathy: a new pathogenic hyphotesis. Br. J. Dermatol.150, 1050–1052 (2004).
  • Aiba S, Tabata N, Ohtani H, Tagami H. CD34+ spindle-shaped cells selectively disappear from the skin lesion of scleroderma. Arch. Dermatol.130, 593–597 (1994).
  • Kuwana M, Okazaki Y, Kodama H et al. Human circulating CD14+ monocytes as a source of progenitors that exhibit mesenchymal cell differentiation. J. Leukoc. Biol.74, 833–845 (2003).
  • Postlethwaite AE, Shigemitsu H, Kanangat S. Cellular origins of fibroblasts: possible implications for organ fibrosis in systemic sclerosis. Curr. Opin. Rheumatol.16, 733–738 (2004).
  • Boban I, Barisic-Dujmovic T, Clark SH. Parabiosis and transplantation models show no evidence of circulating dermal fibroblast progenitors in bleomycin-induced skin fibrosis. J. Cell Physiol.214, 230–237 (2008).
  • Ishii G, Sangai T, Sugiyama K et al.In vivo characterization of bone marrow-derived fibroblasts recruited into fibrotic lesions. Stem Cells23, 699–706 (2005).
  • Ortiz LA, Gambelli F, McBride C et al. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc. Natl Acad. Sci. USA100, 8407–8411 (2003).
  • Ninichuk V, Gross O, Segerer S et al. Multipotent mesenchymal stem cells reduce interstitial fibrosis but do not delay progression of chronic kidney disease in collagen4A3-deficient mice. Kidney Int.70, 121–129 (2006).
  • Cheng Z, Ou L, Zhou X et al. Targeted migration of mesenchymal stem cells modified with CXCR4 gene to infarcted myocardium improves cardiac performance. Mol. Ther.16, 571–579 (2008).
  • Pasha Z, Wang Y, Sheikh R, Zhang D, Zhao T, Ashraf M. Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarcted myocardium. Cardiovasc. Res.77, 134–142 (2008).
  • Willis BC, Liebler JM, Luby-Phelps K et al. Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-β1: potential role in idiopathic pulmonary fibrosis. Am. J. Pathol.166, 1321–1332 (2005).
  • Kim KK, Kugler MC, Wolters PJ et al. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc. Natl Acad. Sci. USA103, 13180–13185 (2006).
  • Kalluri R, Neilson EG. Epithelial–mesenchymal transition and its implications for fibrosis. J. Clin. Invest.112, 1776–1784 (2003).
  • Zeisberg EM, Tarnavski O, Zeisberg M et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat. Med.13, 952–961 (2007).
  • Rajkumar VS, Sundberg C, Abraham DJ, Rubin K, Black CM. Activation of microvascular pericytes in autoimmune Raynaud’s phenomenon and systemic sclerosis. Arthritis Rheum.42, 930–941 (1999).
  • Rajkumar VS, Shiwen X, Bostrom M et al. Platelet-derived growth factor-β receptor activation is essential for fibroblast and pericyte recruitment during cutaneous wound healing. Am. J. Pathol.169, 2254–2265 (2006).
  • Gay S, Jones RE Jr, Huang GQ, Gay RE. Immunohistologic demonstration of platelet-derived growth factor (PDGF) and sis-oncogene expression in scleroderma. J. Invest. Dermatol.92, 301–303 (1989).
  • Zheng XY, Zhang JZ, Tu P, Ma SQ. Expression of platelet-derived growth factor B-chain and platelet-derived growth factor β-receptor in fibroblasts of scleroderma. J. Dermatol. Sci.18, 90–97 (1998).
  • Varga J, Abraham D. Systemic sclerosis: a prototypic multisystem fibrotic disorder. J. Clin. Invest.117, 557–567 (2007).
  • Wynn TA. Fibrotic disease and the T(h)1/T(h)2 paradigm. Nat. Rev. Immunol.4, 583–594 (2004).
  • Distler JH, Jüngel A, Pileckyte M et al. Hypoxia-induced increase in the production of extracellular matrix proteins in systemic sclerosis. Arthritis Rheum.56, 4203–4215 (2007).
  • Varga J, Pasche B. Transforming growth factor β as a therapeutic target in systemic sclerosis. Nat. Rev. Rheumatol.5, 200–206 (2009).
  • Roberts AB, Sporn MB, Assoian RK et al. Transforming growth factor type β: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc. Natl Acad. Sci. USA83, 4167–4171 (1986).
  • Blobe GC, Schiemann WP, Lodish HF. Role of transforming growth factor β in human disease. N. Engl. J. Med.342, 1350–1358 (2000).
  • Desmoulière A, Geinoz A, Gabbiani F, Gabbiani G. Transforming growth factor-β induces α smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J. Cell. Biol.122, 103–111 (1993).
  • Kawakami T, Ihn H, Xu W, Smith E, LeRoy C, Trojanowska M. Increased expression of TGF-β receptors by scleroderma fibroblasts: evidence for contribution of autocrine TGF-β signalling to scleroderma phenotype. J. Invest. Dermatol.110, 47–51 (1998).
  • Asano Y, Ihn H, Yamane K, Jinnin M, Mimura Y, Tamaki K. Involvement of αvβ5 integrin-mediated activation of latent transforming growth factor β1 in autocrine transforming growth factor β signalling in systemic sclerosis fibroblasts. Arthritis Rheum.52, 2897–2905 (2005).
  • Kubo M, Ihn H, Yamane K, Tamaki K. Upregulated expression of transforming growth factor-β receptors in dermal fibroblasts of skin sections from patients with systemic sclerosis. J. Rheumatol.29, 2558–2564 (2002).
  • Mori Y, Chen SJ, Varga J. Expression and regulation of intracellular SMAD signalling in scleroderma skin fibroblasts. Arthritis Rheum.48, 1964–1978 (2003).
  • Dong C, Zhu S, Wang T et al. Deficient Smad7 expression: a putative molecular defect in scleroderma. Proc. Natl Acad. Sci. USA99, 3908–3913 (2002).
  • Jinnin M, Ihn H, Mimura Y, Asano Y, Tamaki K. Involvement of the constitutive complex formation of c-Ski/SnoN with Smads in the impaired negative feedback regulation of transforming growth factor β signalling in scleroderma fibroblasts. Arthritis Rheum.56, 1694–1705 (2007).
  • Ishida W, Mori Y, Lakos G et al. Intracellular TGF-β receptor blockade abrogates Smad-dependent fibroblast activation in vitro and in vivo. J. Invest. Dermatol.126, 1733–1744 (2006).
  • Del Galdo F, Sotgia F, de Almeida CJ et al. Decreased expression of caveolin 1 in patients with systemic sclerosis: crucial role in the pathogenesis of tissue fibrosis. Arthritis Rheum.58, 2854–2865 (2008).
  • Tan FK, Hildebrand BA, Lester MS et al. Classification analysis of the transcriptosome of nonlesional cultured dermal fibroblasts from systemic sclerosis patients with early disease. Arthritis Rheum.52, 865–876 (2005).
  • Massague J. TGF-β signal transduction. Annu. Rev. Biochem.67, 753–791 (1998).
  • Moustakas A, Heldin CH. Non-Smad TGF-β signals. J. Cell. Sci.118, 3573–3584 (2005).
  • Chung L, Fiorentino DF, Benbarak MJ et al. Molecular framework for response to imatinib mesylate in systemic sclerosis. Arthritis Rheum.60, 584–591 (2009).
  • Distler JH, Jüngel A, Huber LC et al. Imatinib mesylate reduces production of extracellular matrix and prevents development of experimental dermal fibrosis. Arthritis Rheum.56, 311–322 (2007).
  • Akhmetshina A, Dees C, Pileckyte M et al. Dual inhibition of c-abl and PDGF receptor signalling by dasatinib and nilotinib for the treatment of dermal fibrosis. FASEB J.22, 2214–2222 (2008).
  • Pannu J, Asano Y, Nakerakanti S et al. Smad1 pathway is activated in systemic sclerosis fibroblasts and is targeted by imatinib mesylate. Arthritis Rheum.58, 2528–2537 (2008).
  • Mimura Y, Ihn H, Jinnin M, Asano Y, Yamane K, Tamaki K. Constitutive phosphorylation of focal adhesion kinase is involved in the myofibroblast differentiation of scleroderma fibroblasts. J. Invest. Dermatol.124, 886–892 (2005).
  • Jun JB, Kuechle M, Min J et al. Scleroderma fibroblasts demonstrate enhanced activation of Akt (protein kinase B) in situ. J. Invest. Dermatol.124, 298–303 (2005).
  • Ihn H, Yamane K, Tamaki K. Increased phosphorylation and activation of mitogen-activated protein kinase p38 in scleroderma fibroblasts. J. Invest. Dermatol.125, 247–255 (2005).
  • Sato M, Shegogue D, Gore EA, Smith EA, McDermott PJ, Trojanowska M. Role of p38 MAPK in transforming growth factor β stimulation of collagen production by scleroderma and healthy dermal fibroblasts. J. Invest. Dermatol.118, 704–711 (2002).
  • Wu M, Melichian DS, de la Garza M et al. Essential roles for early growth response transcription factor Egr-1 in tissue fibrosis and wound healing. Am. J. Pathol.175, 1041–1055 (2009).
  • Bhattacharyya S, Wei J, Melichian DS, Milbrandt J, Takehara K, Varga J. The transcriptional cofactor Nab2 is induced by TGF-β and suppresses fibroblast activation: physiological roles and impaired expression in scleroderma. PLoS ONE26(4), e7620 (2009).
  • Abraham D, Distler O. How does endothelial cell injury start? The role of endothelin in systemic sclerosis. Arthritis Res. Ther.9(Suppl. 2), S2 (2007).
  • Shi-wen X, Kennedy L, Renzoni EA et al. Endothelin is a downstream mediator of pro-fibrotic responses to transforming growth factor β in human lung fibroblasts. Arthritis Rheum.56, 4189–4194 (2007).
  • Denton CP, Abraham DJ. Transforming growth factor-β and connective tissue growth factor: key cytokines in scleroderma pathogenesis. Curr. Opin. Rheumatol.13, 505–511 (2001).
  • Stratton R, Shiwen X, Martini G et al. Iloprost suppresses connective tissue growth factor production in fibroblasts and in the skin of scleroderma patients. J. Clin. Invest.108, 241–250 (2001).
  • Baroni SS, Santillo M, Bevilacqua F et al. Stimulatory autoantibodies to the PDGF receptor in systemic sclerosis. N. Engl. J. Med.354, 2667–2676 (2006).
  • Classen JF, Henrohn D, Rorsman F et al. Lack of evidence of stimulatory autoantibodies to platelet-derived growth factor receptor in patients with systemic sclerosis. Arthritis Rheum.60, 1137–1144 (2009).
  • Loizos N, Lariccia L, Weiner J et al. Lack of detection of agonist activity by antibodies to platelet-derived growth factor receptor α in a subset of normal and systemic sclerosis patient sera. Arthritis Rheum.60, 1145–1151 (2009).
  • Hogaboam CM, Bone-Larson CL, Lipinski S et al. Differential monocyte chemoattractant protein-1 and chemokine receptor 2 expression by murine lung fibroblasts derived from Th1- and Th2-type pulmonary granuloma models. J. Immunol.163, 2193–2201 (1999).
  • Chizzolini C, Parel Y, Scheja A, Dayer JM. Polarized subsets of human T-helper cells induce distinct patterns of chemokine production by normal and systemic sclerosis dermal fibroblasts. Arthritis Res. Ther.8, R10 (2006).
  • Galindo M, Santiago B, Rivero M, Rullas J, Alcami J, Pablos JL. Chemokine expression by systemic sclerosis fibroblasts: abnormal regulation of monocyte chemoattractant protein 1 expression. Arthritis Rheum.44, 1382–1386 (2001).
  • Distler JH, Jüngel A, Caretto D et al. Monocyte chemoattractant protein 1 released from glycosaminoglycans mediates its pro-fibrotic effects in systemic sclerosis via the release of interleukin-4 from T cells. Arthritis Rheum.54, 214–225 (2006).
  • Granstein RD, Flotte TJ, Amento EP. Interferons and collagen production. J. Invest. Dermatol.95, 75S–80S (1990).
  • Desmoulière A, Rubbia-Brandt L, Abdiu A, Walz T, Macieira-Coelho A, Gabbiani G. A-smooth muscle actin is expressed in a subpopulation of cultured and cloned fibroblasts and is modulated by γ-interferon. Exp. Cell. Res.201, 64–73 (1992).
  • Santiago B, Galindo M, Palao G, Pablos JL. Intracellular regulation of Fas-induced apoptosis in human fibroblasts by extracellular factors and cycloheximide. J. Immunol.172, 560–566 (2004).
  • Lemaire R, Farina G, Bayle J et al. Antagonistic effect of the matricellular signalling protein CCN3 on TGF-β- and Wnt-mediated fibrillinogenesis in systemic sclerosis and Marfan syndrome. J. Invest. Dermatol.130, 1514–1523 (2010).
  • Castelino FV, Seiders J, Bain G et al. Genetic deletion or pharmacologic antagonism of LPA(1) ameliorates dermal fibrosis in a scleroderma mouse model. Arthritis Rheum.63(5), 1405–1415 (2011).
  • Oga T, Matsuoka T, Yao C et al. Prostaglandin F(2α) receptor signalling facilitates bleomycin-induced pulmonary fibrosis independently of transforming growth factor-β. Nat. Med.15, 1426–1430 (2009).
  • Shi-wen X, Eastwood M, Stratton RJ, Denton CP, Leask A, Abraham DJ. Rosiglitazone alleviates the persistent fibrotic phenotype of lesional skin scleroderma fibroblasts. Rheumatology (Oxford).49, 259–263 (2010).
  • Wu M, Melichian DS, Chang E, Warner-Blankenship M, Ghosh AK, Varga J. Rosiglitazone abrogates bleomycin-induced scleroderma and blocks pro-fibrotic responses through peroxisome proliferator-activated receptor-γ. Am. J. Pathol.174, 519–533 (2009).
  • Maurer B, Stanczyk J, Jüngel A et al. MicroRNA-29, a key regulator of collagen expression in systemic sclerosis. Arthritis Rheum.62, 1733–1743 (2010).
  • Wang Y, Fan PS, Kahaleh B. Association between enhanced type I collagen expression and epigenetic repression of the FLI1 gene in scleroderma fibroblasts. Arthritis Rheum.54, 2271–2279 (2006).
  • Kubo M, Czuwara-Ladykowska J, Moussa O et al. Persistent down-regulation of Fli1, a suppressor of collagen transcription, in fibrotic scleroderma skin. Am. J. Pathol.163, 571–578 (2003).

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