Transition of healthy to diseased synovial tissue in rheumatoid arthritis is associated with gain of mesenchymal/fibrotic characteristics

Arthritis Research and Therapy

Volumn 8, Issue 6, 2006, Pages

  Steenvoorden, Marjan M C ^a,b   Tolboom, Tanja C A ^a   van der Pluijm, Gabri ^a   Löwik, Clemens ^a   Visser, Cornelis P J ^c   DeGroot, Jeroen ^b   Gittenberger DeGroot, Adriana C ^a   DeRuiter, Marco C ^a   Wisse, Bert J ^a   Huizinga, Tom W J ^a   Toes, René E M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b TNO   (Netherlands)

^c RIJNLAND HOSPITAL   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BMP7 PROTEIN, HUMAN; BONE MORPHOGENETIC PROTEIN; CADHERIN; COLLAGEN TYPE 4; OSTEOGENIC PROTEIN 1; TRANSFORMING GROWTH FACTOR BETA;

BIOSYNTHESIS; CYTOLOGY; DISEASE COURSE; FIBROBLAST; FIBROSIS; HUMAN; IMMUNOHISTOCHEMISTRY; MESODERM; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHEUMATOID ARTHRITIS; SYNOVIUM;

ACTINS; ARTHRITIS, RHEUMATOID; BONE MORPHOGENETIC PROTEIN 7; BONE MORPHOGENETIC PROTEINS; CADHERINS; COLLAGEN TYPE IV; DISEASE PROGRESSION; FIBROBLASTS; FIBROSIS; HUMANS; IMMUNOHISTOCHEMISTRY; MESODERM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SYNOVIAL MEMBRANE; TRANSFORMING GROWTH FACTOR BETA;

EID: 34548391759     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar2073     Document Type: Article

References (46)

1. Iwanaga T, Shikichi M, Kitamura H, Yanase H, Nozawa-Inoue K: Morphology and functional roles of synoviocytes in the joint. Arch Histol Cytol 2000, 63:17-31.
2. Burgel PR, Nadel JA: Roles of epidermal growth factor receptor activation in epithelial cell repair and mucin production in airway epithelium. Thorax 2004, 59:992-996.
3. Edwards JC: Fibroblast biology. Development and differentiation of synovial fibroblasts in arthritis. Arthritis Res 2000, 2 344-347.
4. Kraan MC, Versendaal H, Jonker M, Bresnihan B, Post WJ, Hart BA, Breedveld FC, Tak PP: Asymptomatic synovitis precedes clinically manifest arthritis. Arthritis Rheum 1998, 41:1481-1488.
5. Qu Z, Garcia CH, O'Rourke LM, Planck SR, Kohli M, Rosenbaum JT: Local proliferation of fibroblast-like synoviocytes contributes to synovial hyperplasia. Results of proliferating cell nuclear antigen/cyclin, c-myc, and nucleolar organizer region staining. Arthritis Rheum 1994, 37:212-220.
6. Aupperle KR, Boyle DL, Hendrix M, Seftor EA, Zvaifler NJ, Barbosa M, Firestein GS: Regulation of synoviocyte proliferation, apoptosis, and invasion by the p53 tumor suppressor gene. Am J Pathol 1998, 152:1091-1098.
7. Muller-Ladner U, Kriegsmann J, Franklin BN, Matsumoto S, Geiler T, Gay RE, Gay S: Synovial fibroblasts of patients with rheumatoid arthritis attach to and invade normal human cartilage when engrafted into SCID mice. Am J Pathol 1996, 149:1607-1615.
8. Firestein GS: Invasive fibroblast-like synoviocytes in rheumatoid arthritis. Passive responders or transformed aggressors? Arthritis Rheum 1996, 39:1781-1790.
9. Sun Y, Cheung HS: p53, proto-oncogene and rheumatoid arthritis. Semin Arthritis Rheum 2002, 31:299-310.
10. Inazuka M, Tahira T, Horiuchi T, Harashima S, Sawabe T, Kondo M, Miyahara H, Hayashi K: Analysis of p53 tumour suppressor gene somatic mutations in rheumatoid arthritis synovium. Rheumatology (Oxford 2000, 39:262-266.
11. Firestein GS, Echeverri F, Yeo M, Zvaifler NJ, Green DR: Somatic mutations in the p53 tumor suppressor gene in rheumatoid arthritis synovium. Proc Natl Acad Sci USA 1997, 94:10895-10900.
12. Tak PP, Smeets TJ, Boyle DL, Kraan MC, Shi Y, Zhuang S, Breedveld FC, Firestein GS: p53 overexpression in synovial tissue from patients with early and longstanding rheumatoid arthritis compared with patients with reactive arthritis and osteoarthritis. Arthritis Rheum 1999, 42:948-953.
13. Yanez-Mo M, Lara-Pezzi E, Selgas R, Ramirez-Huesca M, Dominguez-Jimenez C, Jimenez-Heffernan JA, Aguilera A, Sanchez-Tomero JA, Bajo MA, Alvarez V, Castro MA, del Peso G, Cirujeda A, Gamallo C, Sanchez-Madrid F, Lopez-Cabrera M: Peritoneal dialysis and epithelial-to-mesenchymal transition of mesothelial cells. N Engl J Med 2003, 348 403-413.
14. Bissell DM: Chronic liver injury, TGF-beta, and cancer. Exp Mol Med 2001, 33:179-190.
15. Desmouliere A, Redard M, Darby I, Gabbiani G: Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. Am J Pathol 1995, 146:56-66.
16. Vittal R, Horowitz JC, Moore BB, Zhang H, Martinez FJ, Toews GB, Standiford TJ, Thannickal VJ: Modulation of prosurvival signaling in fibroblasts by a protein kinase inhibitor protects against fibrotic tissue injury. Am J Pathol 2005, 166:367-375.
17. Frixen UH, Behrens J, Sachs M, Eberle G, Voss B, Warda A, Lochner D, Birchmeier W: E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol 1991, 113 173-185.
18. Hay ED: The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev Dyn 2005, 233:706-720.
19. Zeisberg M, Kalluri R: The role of epithelial-to-mesenchymal transition in renal fibrosis. J Mol Med 2004, 82:175-181.
20. Foell D, Kane D, Bresnihan B, Vogl T, Nacken W, Sorg C, FitzGerald O, Roth J: Expression of the pro-inflammatory protein S100A12 (EN-RAGE) in rheumatoid and psoriatic arthritis. Rheumatology (Oxford) 2003, 42:1383-1389.
21. Kalluri R, Neilson EG: Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 2003, 112 1776-1784.
22. Li JH, Wang W, Huang XR, Oldfield M, Schmidt AM, Cooper ME, Lan HY: Advanced glycation end products induce tubular epithelial- myofibroblast transition through the RAGE-ERK1/2 MAP kinase signaling pathway. Am J Pathol 2004, 164:1389-1397.
23. Oldfield MD, Bach LA, Forbes JM, Nikolic-Paterson D, McRobert A, Thallas V, Atkins RC, Osicka T, Jerums G, Cooper ME: Advanced glycation end products cause epithelial-myofibroblast transdifferentiation via the receptor for advanced glycation end products (RAGE). J Clin Invest 2001, 108:1853-1863.
24. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, Strutz F, Kalluri R: BMP-7 counteracts TGF-beta1-induced epithelialto- mesenchymal transition and reverses chronic renal injury. Nat Med 2003, 9:964-968.
25. Brennan FM, Chantry D, Turner M, Foxwell B, Maini R, Feldmann M: Detection of transforming growth factor-beta in rheumatoid arthritis synovial tissue: Lack of effect on spontaneous cytokine production in joint cell cultures. Clin Exp Immunol 1990, 81:278-285.
26. Zvaifler NJ: Relevance of the stroma and epithelial-mesenchymal transition (EMT) for the rheumatic diseases. Arthritis Res Ther 2006, 8:210.
27. van der Slot AJ, Zuurmond AM, Bardoel AF, Wijmenga C, Pruijs HE, Sillence DO, Brinckmann J, Abraham DJ, Black CM, Verzijl N, DeGroot J, Hanemaaijer R, TeKoppele JM, Huizinga TW, Bank RA: Identification of PLOD2 as telopeptide lysyl hydroxylase, an important enzyme in fibrosis J Biol Chem 2003, 278:40967-40972.
28. Lettesjo H, Nordstrom E, Strom H, Nilsson B, Glinghammar B, Dahlstedt L, Moller E: Synovial fluid cytokines in patients with rheumatoid arthritis or other arthritic lesions. Scand J Immunol 1998, 48:286-292.
29. Valencia X, Higgins JM, Kiener HP, Lee DM, Podrebarac TA, Dascher CC, Watts GF, Mizoguchi E, Simmons B, Patel DD, Bahn AK, Brenner MB: Cadherin-11 provides specific cellular adhesion between fibroblast-like synoviocytes. J Exp Med 2004, 200:1673-1679.
30. Trollmo C, Nilsson IM, Sollerman C, Tarkowski A: Expression of the mucosal lymphocyte integrin alpha E beta 7 and its ligand E-cadherin in the synovium of patients with rheumatoid arthritis. Scand J Immunol 1996, 44:293-298.
31. Pollock LE, Lalor P, Revell PA: Type IV collagen and laminin in the synovial intimal layer: An immunohistochemical study. Rheumatol Int 1990, 9:277-280.
32. Xue C, Takahashi M, Hasunuma T, Aono H, Yamamoto K, Yoshino S, Sumida T, Nishioka K: Characterisation of fibroblast-like cells in pannus lesions of patients with rheumatoid arthritis sharing properties of fibroblasts and chondrocytes. Ann Rheum Dis 1997, 56 262-267.
33. Rinaldi N, Willhauck M, Weis D, Brado B, Kern P, Lukoschek M, Schwarz-Eywill M, Barth TF: Loss of collagen type IV in rheumatoid synovia and cytokine effect on the collagen type-IV gene expression in fibroblast-like synoviocytes from rheumatoid arthritis. Virchows Arch 2001, 439:675-682.
34. Tolboom TC, van der Helm-Van Mil AH, Nelissen RG, Breedveld FC, Toes RE, Huizinga TW: Invasiveness of fibroblast-like synoviocytes is an individual patient characteristic associated with the rate of joint destruction in patients with rheumatoid arthritis. Arthritis Rheum 2005, 52:1999-2002.
35. Aidinis V, Carninci P, Armaka M, Witke W, Harokopos V, Pavelka N, Koczan D, Argyropoulos C, Thwin MM, Moller S, Kazunori W, Gopalakrishnakone P, Ricciardi-Castagnoli P, Thiesen HJ, Hayashizaki Y, Kollias G: Cytoskeletal rearrangements in synovial fibroblasts as a novel pathophysiological determinant of modeled rheumatoid arthritis. PLoS Genet 2005, 1:e48.
36. Mattey DL, Dawes PT, Nixon NB, Slater H: Transforming growth factor beta 1 and interleukin 4 induced alpha smooth muscle actin expression and myofibroblast-like differentiation in human synovial fibroblasts in vitro: Modulation by basic fibroblast growth factor. Ann Rheum Dis 1997, 56:426-431.
37. Gabbiani G: The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 2003, 200:500-503.
38. Kriegsmann J, Berndt A, Hansen T, Borsi L, Zardi L, Brauer R, Petrow PK, Otto M, Kirkpatrick CJ, Gay S, Kosmehl H: Expression of fibronectin splice variants and oncofetal glycosylated fibronectin in the synovial membranes of patients with rheumatoid arthritis and osteoarthritis. Rheumatol Int 2004, 24:25-33.
39. Chen JR, Takahashi M, Suzuki M, Kushida K, Miyamoto S, Inoue T: Pentosidine in synovial fluid in osteoarthritis and rheumatoid arthritis: Relationship with disease activity in rheumatoid arthritis J Rheumatol 1998, 25:2440-2444.
40. Chen JR, Takahashi M, Suzuki M, Kushida K, Miyamoto S, Inoue T: Comparison of the concentrations of pentosidine in the synovial fluid, serum and urine of patients with rheumatoid arthritis and osteoarthritis Rheumatology (Oxford) 1999, 38:1275-1278.
41. Drinda S, Franke S, Canet CC, Petrow P, Brauer R, Huttich C, Stein G, Hein G: Identification of the advanced glycation end products N(epsilon)-carboxymethyllysine in the synovial tissue of patients with rheumatoid arthritis. Ann Rheum Dis 2002, 61:488-492.
42. Kokkola R, Sundberg E, Ulfgren AK, Palmblad K, Li J, Wang H, Ulloa L, Yang H, Yan XJ, Furie R, Chiorazzi N, Tracey KJ, Andersson U, Harris HE: High mobility group box chromosomal protein 1: A novel proinflammatory mediator in synovitis. Arthritis Rheum 2002, 46:2598-2603.
43. Rodriguez-Garcia J, Requena JR, Rodriguez-Segade S: Increased concentrations of serum pentosidine in rheumatoid arthritis. Clin Chem 1998, 44:250-255.
44. Taniguchi N, Kawahara K, Yone K, Hashiguchi T, Yamakuchi M, Goto M, Inoue K, Yamada S, Ijiri K, Matsunaga S, Nakajima T, Komiya S, Maruyama I: High mobility group box chromosomal protein 1 plays a role in the pathogenesis of rheumatoid arthritis as a novel cytokine. Arthritis Rheum 2003, 48:971-981.
45. Bobacz K, Gruber R, Soleiman A, Graninger WB, Luyten FP, Erlacher L: Cartilage-derived morphogenetic protein-1 and -2 are endogenously expressed in healthy and osteoarthritic human articular chondrocytes and stimulate matrix synthesis. Osteoarthritis Cartilage 2002, 10:394-401.
46. Markwald R, Eisenberg C, Eisenberg L, Trusk T, Sugi Y: Epithelial- mesenchymal transformations in early avian heart development. Acta Anat (Basel) 1996, 156:173-186.