Gene delivery of TGF-Β1 induces arthrofibrosis and chondrometaplasia of synovium in vivo

Laboratory Investigation

Volumn 90, Issue 11, 2010, Pages 1615-1627

  Watson, Rachael S ^a   Gouze, Elvire ^a   Levings, Padraic P ^a   Bush, Marsha L ^a   Kay, Jesse D ^a   Jorgensen, Marda S ^b   Dacanay, E Anthony ^a   Reith, John W ^a   Wright, Thomas W ^a   Ghivizzani, Steven C ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

adhesive capsulitis; arthrofibrosis; chondrometaplasia; differentiation; frozen shoulder; synovium; transforming growth factor beta 1

Indexed keywords

ADAMTS1 PROTEIN; ALPHA2 INTEGRIN; ALPHA3 INTEGRIN; COLLAGEN TYPE 1; COLLAGEN TYPE 2; COLLAGEN TYPE 3; COLLAGEN TYPE 4; COLLAGEN TYPE 5; COLLAGEN TYPE 6; COLLAGEN TYPE 8; COLLAGENASE 3; CONNECTIVE TISSUE GROWTH FACTOR; GELATINASE A; GELATINASE B; MACROPHAGE ELASTASE; MATRILYSIN; MATRIX METALLOPROTEINASE 16; NERVE CELL ADHESION MOLECULE; NEUTROPHIL COLLAGENASE; OSTEONECTIN; OSTEOPONTIN; P CADHERIN; SCLEROPROTEIN; STROMELYSIN 3; TENASCIN; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA1; UNINDEXED DRUG; UVOMORULIN; VERSICAN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTHROFIBROSIS; ARTHROPATHY; ARTICLE; ARTICULAR CARTILAGE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDROMETAPLASIA; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; FEMALE; FIBROSIS; GENE TARGETING; HISTOLOGY; IN VIVO STUDY; KNEE; KNEE FUNCTION; MALE; MYOFIBROBLAST; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNOVIUM;

EID: 78049327480     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2010.145     Document Type: Article

References (70)

1. Gholve PA, Voellmicke KV, Guven M, et al. Arthrofibrosis of the knee after tibial spine fracture in children: a report of two complicated cases. Hss J 2008;4:14-19.
2. Lee SK, Gargano F, Hausman MR. Wrist arthrofibrosis. Hand Clin 2006;22:529-538; abstract vii.
3. Schiavone Panni A, Cerciello S, Vasso M, et al. Stiffness in total knee arthroplasty. J Orthop Traumatol 2009;10:111-118.
4. Boldt JG, Munzinger UK, Zanetti M, et al. Arthrofibrosis associated with total knee arthroplasty: gray-scale and power Doppler sonographic findings. AJR Am J Roentgenol 2004;182:337-340.
5. Neviaser RJ, Neviaser TJ. The frozen shoulder. Diagnosis and management. Clin Orthop Relat Res 1987;223:59-64.
6. Dias R, Cutts S, Massoud S. Frozen shoulder. Br Med J 2005;331: 1453-1456.
7. Hannafin JA, Chiaia TA. Adhesive capsulitis. A treatment approach. Clin Orthop Relat Res 2000;372:95-109.
8. Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol 2008;214:199-210.
9. Pohlers D, Brenmoehl J, Loffler I, et al. TGF-beta and fibrosis in different organs\-molecular pathway imprints. Biochim Biophys Acta 2009;1792:746-756.
10. Gressner OA, Rizk MS, Kovalenko E, et al. Changing the pathogenetic roadmap of liver fibrosis? Where did it start; where will it go? J Gastroenterol Hepatol 2008;23:1024-1035.
11. Border WA, Noble NA. Transforming growth factor beta in tissue fibrosis. N Engl J Med 1994;331:1286-1292.
12. Rahimi RA, Leof EB. TGF-beta signaling: a tale of two responses. J Cell Biochem 2007;102:593-608.
13. Leivonen SK, Kahari VM. Transforming growth factor-beta signaling in cancer invasion and metastasis. Int J Cancer 2007;121:2119-2124.
14. Ihn H. Pathogenesis of fibrosis: role of TGF-beta and CTGF. Curr Opin Rheumatol 2002;14:681-685.
15. Bonniaud P, Margetts PJ, Ask K, et al. TGF-beta and Smad3 signaling link inflammation to chronic fibrogenesis. J Immunol 2005;175: 5390-5395.
16. Takagawa S, Lakos G, Mori Y, et al. Sustained activation of fibroblast transforming growth factor-beta/Smad signaling in a murine model of scleroderma. J Invest Dermatol 2003;121:41-50.
17. Verrecchia F, Chu ML, Mauviel A. Identification of novel TGF-beta/ Smad gene targets in dermal fibroblasts using a combined cDNA microarray/promoter transactivation approach. J Biol Chem 2001;276: 17058-17062.
18. Verrecchia F, Mauviel A. Transforming growth factor-beta signaling through the Smad pathway: role in extracellular matrix gene expression and regulation. J Invest Dermatol 2002;118:211-215.
19. Holmes A, Abraham DJ, Sa S, et al. CTGF and SMADs, maintenance of scleroderma phenotype is independent of SMAD signaling. J Biol Chem 2001;276:10594-10601.
20. Rodeo SA, Hannafin JA, Tom J, et al. Immunolocalization of cytokines and their receptors in adhesive capsulitis of the shoulder. J Orthop Res 1997;15:427-436.
21. Ryu JD, Kirpalani PA, Kim JM, et al. Expression of vascular endothelial growth factor and angiogenesis in the diabetic frozen shoulder. J Shoulder Elbow Surg 2006;15:679-685.
22. Hardy S, Kitamura M, Harris-Stansil T, et al. Construction of adenovirus vectors through Cre-lox recombination. J Virol 1997;71:1842-1849.
23. Ng P, Graham FL. Construction of first-generation adenoviral vectors. Methods Mol Med 2002;69:389-414.
24. Gouze E, Gouze JN, Palmer GD, et al. Transgene persistence and cell turnover in the diarthrodial joint: implications for gene therapy of chronic joint diseases. Mol Ther 2007;15:1114-1120.
25. Spessotto P, Cervi M, Mucignat MT, et al. Beta 1 integrin-dependent cell adhesion to EMILIN-1 is mediated by the gC1q domain. J Biol Chem 2003;278:6160-6167.
26. Zhang HY, Gharaee-Kermani M, Zhang K, et al. Lung fibroblast alpha-smooth muscle actin expression and contractile phenotype in bleomycin-induced pulmonary fibrosis. Am J Pathol 1996;148: 527-537.
27. Gouze E, Pawliuk R, Pilapil C, et al. In vivo gene delivery to synovium by lentiviral vectors. Mol Ther 2002;5:397-404.
28. Gouze E, Pawliuk R, Gouze JN, et al. Lentiviral-mediated gene delivery to synovium: potent intra-articular expression with amplification by inflammation. Mol Ther 2003;7:460-466.
29. Magit D, Wolff A, Sutton K, et al. Arthrofibrosis of the knee. J Am Acad Orthop Surg 2007;15:682-694.
30. Murphey MD, Vidal JA, Fanburg-Smith JC, et al. Imaging of synovial chondromatosis with radiologic-pathologic correlation. Radiographics 2007;27:1465-1488.
31. Vargas-Gonzalez R, Sanchez-Sosa S. Fibrocartilaginous dysplasia (fibrous dysplasia with extensive cartilaginous differentiation). Pathol Oncol Res 2006;12:111-114.
32. Zoricic S, Maric I, Bobinac D, et al. Expression of bone morphogenetic proteins and cartilage-derived morphogenetic proteins during osteophyte formation in humans. J Anat 2003;202:269-277.
33. Matsui Y, Hasegawa T, Kubo T, et al. Intrapatellar tendon lipoma with chondro-osseous differentiation: detection of HMGA2-LPP fusion gene transcript. J Clin Pathol 2006;59:434-436.
34. Wirrig EE, Snarr BS, Chintalapudi MR, et al. Cartilage link protein 1 (Crtl1), an extracellular matrix component playing an important role in heart development. Dev Biol 2007;310:291-303.
35. Gueders MM, Foidart JM, Noel A, et al. Matrix metalloproteinases (MMPs) and tissue inhibitors of MMPs in the respiratory tract: potential implications in asthma and other lung diseases. Eur J Pharmacol 2006;533:133-144.
36. Hemmann S, Graf J, Roderfeld M, et al. Expression of MMPs and TIMPs in liver fibrosis a systematic review with special emphasis on anti-fibrotic strategies. J Hepatol 2007;46:955-975.
37. English JL, Kassiri Z, Koskivirta I, et al. Individual Timp deficiencies differentially impact pro-MMP-2 activation. J Biol Chem 2006;281: 10337-10346.
38. Pardo A, Selman M. Matrix metalloproteases in aberrant fibrotic tissue remodeling. Proc Am Thorac Soc 2006;3:383-388.
39. Bornstein P, Sage EH. Matricellular proteins: extracellular modulators of cell function. Curr Opin Cell Biol 2002;14:608-616.
40. Alford AI, Hankenson KD. Matricellular proteins: extracellular modulators of bone development, remodeling, and regeneration. Bone 2006;38:749-757.
41. Mo FE, Lau LF. The matricellular protein CCN1 is essential for cardiac development. Circ Res 2006;99:961-969.
42. Moura R, Tjwa M, Vandervoort P, et al. Thrombospondin-1 activates medial smooth muscle cells and triggers neointima formation upon mouse carotid artery ligation. Arterioscler Thromb Vasc Biol 2007;27:2163-2169.
43. Bradshaw AD, Sage EH. SPARC, a matricellular protein that functions in cellular differentiation and tissue response to injury. J Clin Invest 2001; 107:1049-1054.
44. Bornstein P. Matricellular proteins: an overview. Matrix Biol 2000;19:555-556.
45. Agnihotri R, Crawford HC, Haro H, et al. Osteopontin, a novel substrate for matrix metalloproteinase-3 (stromelysin-1) and matrix meta-lloproteinase-7 (matrilysin). J Biol Chem 2001;276:28261-28267.
46. Pardo A, Gibson K, Cisneros J, et al. Up-regulation and profibrotic role of osteopontin in human idiopathic pulmonary fibrosis. PLoS Med 2005;2:e251.
47. Castellano G, Malaponte G, Mazzarino MC, et al. Activation of the osteopontin/matrix metalloproteinase-9 pathway correlates with prostate cancer progression. Clin Cancer Res 2008;14:7470-7480.
48. Gao YA, Agnihotri R, Vary CP, et al. Expression and characterization of recombinant osteopontin peptides representing matrix meta-lloproteinase proteolytic fragments. Matrix Biol 2004;23:457-466.
49. Kobayashi T, Inoue T, Okada H, et al. Connective tissue growth factor mediates the profibrotic effects of transforming growth factor-beta produced by tubular epithelial cells in response to high glucose. Clin Exp Nephrol 2005;9:114-121.
50. Leask A, Parapuram SK, Shi-Wen X, et al. Connective tissue growth factor (CTGF, CCN2) gene regulation: a potent clinical bio-marker of fibroproliferative disease? J Cell Commun Signal 2009;3:89-94.
51. Woods A, Wang G, Beier F. Regulation of chondrocyte differentiation by the actin cytoskeleton and adhesive interactions. J Cell Physiol 2007;213:1-8.
52. Lehembre F, Yilmaz M, Wicki A, et al. NCAM-induced focal adhesion assembly: a functional switch upon loss of E-cadherin. Embo J 2008;27:2603-2615.
53. Frame MC, Inman GJ. NCAM is at the heart of reciprocal regulation of E-cadherin-and integrin-mediated adhesions via signaling modulation. Dev Cell 2008;15:494-496.
54. Bartok B, Firestein GS. Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev 2010;233:233-255.
55. Chu CQ, Field M, Abney E, et al. Transforming growth factor-beta 1 in rheumatoid synovial membrane and cartilage/pannus junction. Clin Exp Immunol 1991;86:380-386.
56. Szekanecz Z, Haines GK, Harlow LA, et al. Increased synovial expression of transforming growth factor (TGF)-beta receptor endoglin and TGF-beta 1 in rheumatoid arthritis: possible interactions in the patho-genesis of the disease. Clin Immunol Immunopathol 1995;76:187-194.
57. Taketazu F, Kato M, Gobl A, et al. Enhanced expression of transforming growth factor-beta s and transforming growth factor-beta type II receptor in the synovial tissues of patients with rheumatoid arthritis. Lab Invest 1994;70:620-630.
58. Goddard DH, Grossman SL, Williams WV, et al. Regulation of synovial cell growth. Coexpression of transforming growth factor beta and basic fibroblast growth factor by cultured synovial cells. Arthritis Rheum 1992;35:1296-1303.
59. Fava R, Olsen N, Keski-Oja J, et al. Active and latent forms of transforming growth factor beta activity in synovial effusions. J Exp Med 1989;169:291-296.
60. Kasperkovitz PV, Timmer TC, Smeets TJ, et al. Fibroblast-like synoviocytes derived from patients with rheumatoid arthritis show the imprint of synovial tissue heterogeneity: evidence of a link between an increased myofibroblast-like phenotype and high-inflammation synovitis. Arthritis Rheum 2005;52:430-441.
61. Shintani N, Hunziker EB. Chondrogenic differentiation of bovine synovium: bone morphogenetic proteins 2 and 7 and transforming growth factor beta1 induce the formation of different types of cartilaginous tissue. Arthritis Rheum 2007;56:1869-1879.
62. Fiorito S, Magrini L, Adrey J, et al. Inflammatory status and cartilage regenerative potential of synovial fibroblasts from patients with osteo-arthritis and chondropathy. Rheumatology (Oxford) 2005;44:164-171.
63. Mochizuki T, Muneta T, Sakaguchi Y, et al. Higher chondrogenic potential of fibrous synovium-and adipose synovium-derived cells compared with subcutaneous fat-derived cells: distinguishing properties of mesenchymal stem cells in humans. Arthritis Rheum 2006;54:843-853.
64. Shirasawa S, Sekiya I, Sakaguchi Y, et al. In vitro chondrogenesis of human synovium-derived mesenchymal stem cells: optimal condition and comparison with bone marrow-derived cells. J Cell Biochem 2006;97:84-97.
65. Jiang X, Cui P, Chen W, et al. [Study on the directed inducing process of cartilage cells differentiated from human marrow mesenchymal stem cells]. Zhonghua Er Bi Yan Hou Ke Za Zhi 2002;37: 137-139.
66. De Bari C, Dell'Accio F, Tylzanowski P, et al. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 2001;44:1928-1942.
67. Karystinou A, Dell'Accio F, Kurth TB, et al. Distinct mesenchymal progenitor cell subsets in the adult human synovium. Rheumatology (Oxford) 2009;48:1057-1064.
68. Crawford A, Frazer A, Lippitt JM, et al. A case of chondromatosis indicates a synovial stem cell aetiology. Rheumatology (Oxford) 2006;45:1529-1533.
69. Krampera M, Pizzolo G, Aprili G, et al. Mesenchymal stem cells for bone, cartilage, tendon and skeletal muscle repair. Bone 2006;39: 678-683.
70. Ahmed N, Stanford WL, Kandel RA. Mesenchymal stem and progenitor cells for cartilage repair. Skeletal Radiol 2007;36:909-912.