Identification of cadherin 11 as a mediator of dermal fibrosis and possible role in systemic sclerosis

Arthritis and Rheumatology

Volumn 66, Issue 4, 2014, Pages 1010-1021

  Wu, Minghua ^a   Pedroza, Mesias ^b   Lafyatis, Robert ^c   George, Anuh Teresa ^b   Mayes, Maureen D ^a   Assassi, Shervin ^a   Tan, Filemon K ^a   Brenner, Michael B ^d   Agarwal, Sandeep K ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN; CADHERIN; CADHERIN 11; MESSENGER RNA; MONOCLONAL ANTIBODY; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MOUSE; MYOFIBROBLAST; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SKIN BIOPSY; SKIN FIBROSIS; SKINFOLD THICKNESS; SYSTEMIC SCLEROSIS;

ADULT; ANIMALS; CADHERINS; CELL MOVEMENT; DISEASE MODELS, ANIMAL; FEMALE; FIBROBLASTS; FIBROSIS; HUMANS; MACROPHAGES; MALE; MICE; MICE, KNOCKOUT; SCLERODERMA, SYSTEMIC; SKIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84898658725     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.38275     Document Type: Article

References (48)

1. Charles C, Clements P, Furst DE,. Systemic sclerosis: hypothesis-driven treatment strategies. Lancet 2006; 367: 1683-91.
2. Abraham DJ, Varga J,. Scleroderma: from cell and molecular mechanisms to disease models. Trends Immunol 2005; 26: 587-95.
3. Lakos G, Takagawa S, Chen SJ, Ferreira AM, Han G, Masuda K, et al. Targeted disruption of TGF-β/Smad3 signaling modulates skin fibrosis in a mouse model of scleroderma. Am J Pathol 2004; 165: 203-17.
4. Tan FK, Zhou X, Mayes MD, Gourh P, Guo X, Marcum C, et al. Signatures of differentially regulated interferon gene expression and vasculotrophism in the peripheral blood cells of systemic sclerosis patients. Rheumatology (Oxford) 2006; 45: 694-702.
5. Agarwal SK, Wu M, Livingston CK, Parks DH, Mayes MD, Arnett FC, et al. Toll-like receptor 3 upregulation by type I interferon in healthy and scleroderma dermal fibroblasts. Arthritis Res Ther 2011; 13: R3.
6. Assassi S, Mayes MD, Arnett FC, Gourh P, Agarwal SK, McNearney TA, et al. Systemic sclerosis and lupus: points in an interferon-mediated continuum. Arthritis Rheum 2010; 62: 589-98.
7. York MR, Nagai T, Mangini AJ, Lemaire R, van Seventer JM, Lafyatis R,. A macrophage marker, Siglec-1, is increased on circulating monocytes in patients with systemic sclerosis and induced by type I interferons and Toll-like receptor agonists. Arthritis Rheum 2007; 56: 1010-20.
8. Farina GA, York MR, Di Marzio M, Collins CA, Meller S, Homey B, et al. Poly(I:C) drives type I IFN- and TGFβ-mediated inflammation and dermal fibrosis simulating altered gene expression in systemic sclerosis. J Invest Dermatol 2010; 130: 2583-93.
9. Wei J, Fang F, Lam AP, Sargent JL, Hamburg E, Hinchcliff ME, et al. Wnt/β-catenin signaling is hyperactivated in systemic sclerosis and induces Smad-dependent fibrotic responses in mesenchymal cells. Arthritis Rheum 2012; 64: 2734-45.
10. Wei J, Melichian D, Komura K, Hinchcliff M, Lam AP, Lafyatis R, et al. Canonical Wnt signaling induces skin fibrosis and subcutaneous lipoatrophy: a novel mouse model for scleroderma? Arthritis Rheum 2011; 63: 1707-17.
11. Bergmann C, Akhmetshina A, Dees C, Palumbo K, Zerr P, Beyer C, et al. Inhibition of glycogen synthase kinase 3β induces dermal fibrosis by activation of the canonical Wnt pathway. Ann Rheum Dis 2011; 70: 2191-8.
12. Beyer C, Schramm A, Akhmetshina A, Dees C, Kireva T, Gelse K, et al. β-catenin is a central mediator of pro-fibrotic Wnt signaling in systemic sclerosis. Ann Rheum Dis 2012; 71: 761-7.
13. Schneider DJ, Wu M, Le TT, Cho SH, Brenner MB, Blackburn MR, et al. Cadherin-11 contributes to pulmonary fibrosis: potential role in TGF-β production and epithelial to mesenchymal transition. FASEB J 2012; 26: 503-12.
14. Wheelock MJ, Johnson KR,. Cadherin-mediated cellular signaling. Curr Opin Cell Biol 2003; 15: 509-14.
15. Wheelock MJ, Johnson KR,. Cadherins as modulators of cellular phenotype. Annu Rev Cell Dev Biol 2003; 19: 207-35.
16. Takeichi M,. Cadherins: a molecular family important in selective cell-cell adhesion. Annu Rev Biochem 1990; 59: 237-52.
17. Goodwin M, Yap AS,. Classical cadherin adhesion molecules: coordinating cell adhesion, signaling and the cytoskeleton. J Mol Histol 2004; 35: 839-44.
18. Perl AK, Wilgenbus P, Dahl U, Semb H, Christofori G,. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 1998; 392: 190-3.
19. Pishvaian MJ, Feltes CM, Thompson P, Bussemakers MJ, Schalken JA, Byers SW,. Cadherin-11 is expressed in invasive breast cancer cell lines. Cancer Res 1999; 59: 947-52.
20. Nieman MT, Prudoff RS, Johnson KR, Wheelock MJ,. N-cadherin promotes motility in human breast cancer cells regardless of their E-cadherin expression. J Cell Biol 1999; 147: 631-44.
21. Frixen UH, Behrens J, Sachs M, Eberle G, Voss B, Warda A, et al. E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol 1991; 113: 173-85.
22. Kim KK, Kugler MC, Wolters PJ, Robillard L, Galvez MG, Brumwell AN, et al. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci U S A 2006; 103: 13180-5.
23. Islam S, Carey TE, Wolf GT, Wheelock MJ, Johnson KR,. Expression of N-cadherin by human squamous carcinoma cells induces a scattered fibroblastic phenotype with disrupted cell-cell adhesion. J Cell Biol 1996; 135: 1643-54.
24. Okazaki M, Takeshita S, Kawai S, Kikuno R, Tsujimura A, Kudo A, et al. Molecular cloning and characterization of OB-cadherin, a new member of cadherin family expressed in osteoblasts. J Biol Chem 1994; 269: 12092-8.
25. Hoffmann I, Balling R,. Cloning and expression analysis of a novel mesodermally expressed cadherin. Dev Biol 1995; 169: 337-46.
26. Shibata T, Ochiai A, Gotoh M, Machinami R, Hirohashi S,. Simultaneous expression of cadherin-11 in signet-ring cell carcinoma and stromal cells of diffuse-type gastric cancer. Cancer Lett 1996; 99: 147-53.
27. Valencia X, Higgins JM, Kiener HP, Lee DM, Podrebarac TA, Dascher CC, et al. Cadherin-11 provides specific cellular adhesion between fibroblast-like synoviocytes. J Exp Med 2004; 200: 1673-9.
28. Lee DM, Kiener HP, Agarwal SK, Noss EH, Watts GF, Chisaka O, et al. Cadherin-11 in synovial lining formation and pathology in arthritis. Science 2007; 315: 1006-10.
29. Gardner H, Shearstone JR, Bandaru R, Crowell T, Lynes M, Trojanowska M, 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 2006; 54: 1961-73.
30. Whitfield ML, Finlay DR, Murray JI, Troyanskaya OG, Chi JT, Pergamenschikov A, et al. Systemic and cell type-specific gene expression patterns in scleroderma skin. Proc Natl Acad Sci U S A 2003; 100: 12319-24.
31. Subcommittee for Scleroderma Criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee. Preliminary criteria for the classification of systemic sclerosis (scleroderma). Arthritis Rheum 1980; 23: 581-90.
32. Takagawa S, Lakos G, Mori Y, Yamamoto T, Nishioka K, Varga J,. Sustained activation of fibroblast transforming growth factor-β/Smad signaling in a murine model of scleroderma. J Invest Dermatol 2003; 121: 41-50.
33. Wu M, Schneider DJ, Mayes MD, Assassi S, Arnett FC, Tan FK, et al. Osteopontin in systemic sclerosis and its role in dermal fibrosis. J Invest Dermatol 2012; 132: 1605-14.
34. Wu M, Melichian DS, Chang E, Warner-Blankenship M, Ghosh AK, Varga J,. Rosiglitazone abrogates bleomycin-induced scleroderma and blocks profibrotic responses through peroxisome proliferator-activated receptor-γ. Am J Pathol 2009; 174: 519-33.
35. Yamamoto T,. Animal model of sclerotic skin induced by bleomycin: a clue to the pathogenesis of and therapy for scleroderma? Clin Immunol 2002; 102: 209-16.
36. Yamamoto T, Nishioka K,. Animal model of sclerotic skin. V. Increased expression of α-smooth muscle actin in fibroblastic cells in bleomycin-induced scleroderma. Clin Immunol 2002; 102: 77-83.
37. Yamamoto T, Nishioka K,. Cellular and molecular mechanisms of bleomycin-induced murine scleroderma: current update and future perspective. Exp Dermatol 2005; 14: 81-95.
38. Yamamoto T, Takagawa S, Katayama I, Yamazaki K, Hamazaki Y, Shinkai H, et al. Animal model of sclerotic skin. I. Local injections of bleomycin induce sclerotic skin mimicking scleroderma. J Invest Dermatol 1999; 112: 456-62.
39. Farina G, Lafyatis D, Lemaire R, Lafyatis R,. A four-gene biomarker predicts skin disease in patients with diffuse cutaneous systemic sclerosis. Arthritis Rheum 2010; 62: 580-8.
40. Kovacs EJ,. Fibrogenic cytokines: the role of immune mediators in the development of scar tissue. Immunol Today 1991; 12: 17-23.
41. Wu M, Melichian DS, de la Garza M, Gruner K, Bhattacharyya S, Barr L, et al. Essential roles for early growth response transcription factor Egr-1 in tissue fibrosis and wound healing. Am J Pathol 2009; 175: 1041-55.
42. Chen SJ, Ning H, Ishida W, Sodin-Semrl S, Takagawa S, Mori Y, et al. The early-immediate gene EGR-1 is induced by transforming growth factor-β and mediates stimulation of collagen gene expression. J Biol Chem 2006; 281: 21183-97.
43. Lam AP, Flozak AS, Russell S, Wei J, Jain M, Mutlu GM, et al. Nuclear β-catenin is increased in systemic sclerosis pulmonary fibrosis and promotes lung fibroblast migration and proliferation. Am J Respir Cell Mol Biol 2011; 45: 915-22.
44. Yamamoto T, Eckes B, Krieg T,. High expression and autoinduction of monocyte chemoattractant protein-1 in scleroderma fibroblasts. Eur J Immunol 2001; 31: 2936-41.
45. Yamamoto T, Nishioka K,. Role of monocyte chemoattractant protein-1 and its receptor, CCR-2, in the pathogenesis of bleomycin-induced scleroderma. J Invest Dermatol 2003; 121: 510-6.
46. Wynn TA,. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest 2007; 117: 524-9.
47. Querfeld C, Eckes B, Huerkamp C, Krieg T, Sollberg S,. Expression of TGF-β1, -β2 and -β3 in localized and systemic scleroderma. J Dermatol Sci 1999; 21: 13-22.
48. Chang SK, Noss EH, Chen M, Gu Z, Townsend K, Grenha R, et al. Cadherin-11 regulates fibroblast inflammation. Proc Natl Acad Sci U S A 2011; 108: 8402-7. Musculoskeletal and Skin Diseases and Skin Diseases and Skin Diseases and Skin Diseases and Skin Diseases and Skin Diseases Musculoskeletal and Skin Diseases and Skin Diseases