Remodelling of human osteoarthritic cartilage by FGF-2, alone or combined with Sox9 via rAAV gene transfer

Journal of Cellular and Molecular Medicine

Volumn 13, Issue 8 B, 2009, Pages 2476-2488

  Cucchiarini, Magali ^a   Terwilliger, Ernest F ^b   Kohn, Dieter ^a   Madry, Henning ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Articular cartilage; Combined gene transfer; FGF 2; Human osteoarthritis; RAAV; Sox9

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; SOX9 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX9;

ADENO ASSOCIATED VIRUS; ARTICLE; CARTILAGE; GENE THERAPY; GENE TRANSFER; GENE VECTOR; GENETICS; HUMAN; OSTEOARTHRITIS; PATHOPHYSIOLOGY;

CARTILAGE; DEPENDOVIRUS; FIBROBLAST GROWTH FACTOR 2; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; OSTEOARTHRITIS; SOX9 TRANSCRIPTION FACTOR;

ADENO-ASSOCIATED VIRUS; PARVOVIRUS;

EID: 72949105817     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2008.00474.x     Document Type: Article

References (62)

1. Poole AR. An introduction to the pathophysiology of osteoarthritis. Front Biosci. 1999 4 : D662 70.
2. Pelletier JP, DiBattista JA, Roughley P, et al. Cytokines and inflammation in cartilage degradation. Rheum Dis Clin North Am. 1993 19 : 545 568.
3. Baragi VM, Renkiewicz RR, Jordan H, et al. Transplantation of transduced chondrocytes protects articular cartilage from interleukin 1-induced extracellular matrix degradation. J Clin Invest. 1995 96 : 2454 2460.
4. Nixon AJ, Haupt JL, Frisbie DD, et al. Gene-mediated restoration of cartilage matrix by combination insulin-like growth factor-I(interleukin-1 receptor antagonist therapy. Gene Ther. 2005 12 : 177 186.
5. Pelletier JP, Caron JP, Evans C, et al. In vivo suppression of early experimental osteoarthritis by interleukin-1 receptor antagonist using gene therapy. Arthritis Rheum. 1997 40 : 1012 1019.
6. Frisbie DD, Ghivizzani SC, Robbins PD, et al. Treatment of experimental equine osteoarthritis by in vivo delivery of the equine interleukin-1 receptor antagonist gene. Gene Ther. 2002 9 : 12 20.
7. Madry H, Zurakowski D, Trippel SB. Overexpression of human insulin-like growth factor-I promotes new tissue formation in an ex vivo model of articular chondrocyte transplantation. Gene Ther. 2001 8 : 1443 1449.
8. Madry H, Emkey G, Zurakowski D, et al. Overexpression of human fibroblast growth factor 2 stimulates cell proliferation in an ex vivo model of articular chondrocyte transplantation. J Gene Med. 2004 6 : 238 245.
9. Inoue A, Takahashi KA, Arai Y, et al. The therapeutic effects of basic fibroblast growth factor contained in gelatin hydrogel microspheres on experimental osteoarthritis in the rabbit knee. Arthritis Rheum. 2006 54 : 264 270.
10. Hidaka C, Quitoriano M, Warren RF, et al. Enhanced matrix synthesis and in vitro formation of cartilage-like tissue by genetically modified chondrocytes expressing BMP-7. J Orthop Res. 2001 19 : 751 758.
11. Ulrich-Vinther M, Stengaard C, Schwarz EM, et al. Adeno-associated vector mediated gene transfer of transforming growth factor-beta1 to normal and osteoarthritic human chondrocytes stimulates cartilage anabolism. Eur Cell Mater. 2005 10 : 40 59.
12. Blaney Davidson EN, Vitters EL, Van Den Berg WB, et al. TGF beta-induced cartilage repair is maintained but fibrosis is blocked in the presence of Smad7. Arthritis Res Ther. 2006 8 : R65 72.
13. Venkatesan N, Barre L, Benani A, et al. Stimulation of proteoglycan synthesis by glucuronosyltransferase-I gene delivery: a strategy to promote cartilage repair. Proc Natl Acad Sci USA. 2004 101 : 18087 18092.
14. Aigner T, Vornehm SI, Zeiler G, et al. Suppression of cartilage matrix gene expression in upper zone chondrocytes of osteoarthritic cartilage. Arthritis Rheum. 1997 40 : 562 569.
15. Smith RL. Degradative enzymes in osteoarthritis. Front Biosci. 1999 4 : D704 12.
16. Aigner T, Gebhard PM, Schmid E, et al. SOX9 expression does not correlate with type II collagen expression in adult articular chondrocytes. Matrix Biol. 2003 22 : 363 372.
17. Bi W, Deng JM, Zhang Z, et al. SOX9 is required for cartilage formation. Nat Genet. 1999 22 : 85 9.
18. Ikeda T, Kamekura S, Mabuchi A, et al. The combination of SOX5, SOX6, and SOX9 (the SOX trio) provides signals sufficient for induction of permanent cartilage. Arthritis Rheum. 2004 50 : 3561 3573.
19. Salminen H, Vuorio E, Saamanen AM. Expression of SOX9 and type IIA procollagen during attempted repair of articular cartilage damage in a transgenic mouse model of osteoarthritis. Arthritis Rheum. 2001 44 : 947 955.
20. Tew SR, Li Y, Pothacharoen P, et al. Retroviral transduction with SOX9 enhances re-expression of the chondrocyte phenotype in passaged osteoarthritic human articular chondrocytes. Osteoarthritis Cartilage. 2005 13 : 80 9.
21. Li Y, Tew SR, Russell AM, et al. Transduction of passaged human articular chondrocytes with adenoviral, retroviral, and lentiviral vectors and the effects of enhanced expression of SOX9. Tissue Eng. 2004 10 : 575 584.
22. Cucchiarini M, Thurn T, Weimer A, et al. Restoration of the extracellular matrix in human osteoarthritic articular cartilage by overexpression of the transcription factor SOX9. Arthritis Rheum. 2007 56 : 158 167.
23. Loeser RF, Pacione CA, Chubinskaya S. The combination of insulin-like growth factor 1 and osteogenic protein 1 promotes increased survival of matrix synthesis by normal and osteoarthritic human articular chondrocytes. Arthritis Rheum. 2003 48 : 2188 2196.
24. Kypriotou M, Fossard-Demoor M, Chadjichristos C, et al. SOX9 exerts a bifunctional effect on type II collagen gene (COL2A1) expression in chondrocytes depending on the differentiation state. DNA Cell Biol. 2003 22 : 119 129.
25. Posever J, Phillips FM, Pottenger LA. Effects of basic fibroblast growth factor, transforming growth factor-beta 1, insulin-like growth factor-1, and insulin on human osteoarthritic articular cartilage explants. J Orthop Res. 1995 13 : 832 837.
26. Loeser RF, Chubinskaya S, Pacione C, et al. Basic fibroblast growth factor inhibits the anabolic activity of insulin-like growth factor 1 and osteogenic protein 1 in adult human articular chondrocytes. Arthritis Rheum. 2005 52 : 3910 3917.
27. Arai Y, Kubo T, Fushiki S, et al. Gene delivery to human chondrocytes by an adeno associated virus vector. J Rheumatol. 2000 27 : 979 982.
28. Madry H, Cucchiarini M, Terwilliger EF, et al. Recombinant adeno-associated virus vectors efficiently and persistently transduce chondrocytes in normal and osteoarthritic human articular cartilage. Hum Gene Ther. 2003 14 : 393 402.
29. Cucchiarini M, Madry H, Ma C, et al. Improved tissue repair in articular cartilage defects in vivo by rAAV-mediated overexpression of human fibroblast growth factor 2. Mol Ther. 2005 12 : 229 238. (Pubitemid 41025092)
30. Rendahl KG, Leff SE, Otten GR, et al. Regulation of gene expression in vivo following transduction by two separate rAAV vectors. Nat Biotechnol. 1998 16 : 757 761.
31. Muramatsu S, Fujimoto K, Ikeguchi K, et al. Behavioral recovery in a primate model of Parkinson's disease by triple transduction of striatal cells with adeno-associated viral vectors expressing dopamine-synthesizing enzymes. Hum Gene Ther. 2002 13 : 345 354.
32. Xiao X, Li J, Samulski RJ. Efficient long-term gene transfer into muscle tissue of immunocompetent mice by adeno-associated virus vector. J Virol. 1996 70 : 8098 8108. (Pubitemid 26339120)
33. Mason JM, Grande DA, Barcia M, et al. Expression of human bone morphogenic protein 7 in primary rabbit periosteal cells: potential utility in gene therapy for osteochondral repair. Gene Ther. 1998 5 : 1098 1104.
34. Mi Z, Ghivizzani SC, Lechman ER, et al. Adenovirus-mediated gene transfer of insulin-like growth factor 1 stimulates proteoglycan synthesis in rabbit joints. Arthritis Rheum. 2000 43 : 2563 2570.
35. Mankin HJ, Dorfman H, Lippiello L, et al. Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J Bone Joint Surg Am. 1971 53 : 523 537.
36. Samulski RJ, Chang LS, Shenk T. Helper-free stocks of recombinant adeno-associated viruses: normal integration does not require viral gene expression. J Virol. 1989 63 : 3822 3828.
37. Cucchiarini M, Ren XL, Perides G, et al. Selective gene expression in brain microglia mediated via adeno-associated virus type 2 and type 5 vectors. Gene Ther. 2003 10 : 657 667.
38. Seno M, Masago A, Nishimura A, et al. BALB(c 3T3 cells co-expressing FGF-2 and soluble FGF receptor acquire tumorigenicity. Cytokine. 1998 10 : 290 294.
39. Sudbeck P, Schmitz ML, Baeuerle PA, et al. Sex reversal by loss of the C-terminal transactivation domain of human SOX9. Nat Genet. 1996 13 : 230 232.
40. Madry H, Cucchiarini M, Stein U, et al. Sustained transgene expression in cartilage defects in vivo after transplantation of articular chondrocytes modified by lipid-mediated gene transfer in a gel suspension delivery system. J Gene Med. 2003 5 : 502 509.
41. Uusitalo H, Hiltunen A, Ahonen M, et al. Accelerated up-regulation of L-Sox5, Sox6, and Sox9 by BMP-2 gene transfer during murine fracture healing. J Bone Miner Res. 2001 16 : 1837 1845.
42. Iwasaki M, Nakahara H, Nakata K, et al. Regulation of proliferation and osteochondrogenic differentiation of periosteum-derived cells by transforming growth factor-beta and basic fibroblast growth factor. J Bone Joint Surg Am. 1995 77 : 543 554.
43. Ogawa T, Shimokawa H, Fukada K, et al. Localization and inhibitory effect of basic fibroblast growth factor on chondrogenesis in cultured mouse mandibular condyle. J Bone Miner Metab. 2003 21 : 145 153.
44. Trippel SB, Wroblewski J, Makower AM, et al. Regulation of growth-plate chondrocytes by insulin-like growth-factor I and basic fibroblast growth factor. J Bone Joint Surg Am. 1993 75 : 177 189.
45. Panda DK, Miao D, Lefebvre V, et al. The transcription factor SOX9 regulates cell cycle and differentiation genes in chondrocytic CFK2 cells. J Biol Chem. 2001 276 : 41229 41236.
46. Drivdahl R, Haugh KH, Sprenger CC, et al. Suppression of growth and tumorigenicity in the prostate tumor cell line M12 by overexpression of the transcription factor SOX9. Oncogene. 2004 23 : 4584 4593.
47. Bell DM, Leung KK, Wheatley SC, et al. SOX9 directly regulates the type-II collagen gene. Nat Genet. 1997 16 : 174 178.
48. Lefebvre V, Huang W, Harley VR, et al. SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol Cell Biol. 1997 17 : 2336 2346.
49. Ng LJ, Wheatley S, Muscat GE, et al. SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev Biol. 1997 183 : 108 121.
50. Goater J, Müller R, Kollias G, et al. Empirical advantages of adeno associated viral vectors for in vivo gene therapy for arthritis. J. Rheumatol. 2000 27 : 983 989.
51. Doherty PJ, Zhang H, Tremblay L, et al. Resurfacing of articular cartilage explants with genetically-modified human chondrocytes in vitro. Osteoarthritis Cartilage. 1998 6 : 153 159.
52. Schmal H, Zwingmann J, Fehrenbach M, et al. bFGF influences human articular chondrocyte differentiation. Cytotherapy. 2007 9 : 184 193.
53. Hoyland JA, Thomas JT, Donn R, et al. Distribution of type X collagen mRNA in normal and osteoarthritic human cartilage. Bone Miner. 1991 15 : 151 163.
54. von der Mark K, Kirsch T, Nerlich A, et al. Type X collagen synthesis in human osteoarthritic cartilage. Indication of chondrocyte hypertrophy. Arthritis Rheum. 1992 35 : 806 811.
55. Kirsch T, Swoboda B, Nah H. Activation of annexin II and V expression, terminal differentiation, mineralization and apoptosis in human osteoarthritic cartilage. Osteoarthritis Cartilage. 2000 8 : 294 302.
56. Tsuchiya H, Kitoh H, Sugiura F, et al. Chondrogenesis enhanced by overexpression of sox9 gene in mouse bone marrow-derived mesenchymal stem cells. Biochem Biophys Res Comm. 2003 301 : 338 343.
57. Hardingham TE, Oldershaw RA, Tew SR. Cartilage, SOX9 and Notch signals in chondrogenesis. J Anat. 2006 209 : 469 480.
58. Vincent T, Hermansson M, Bolton M, et al. Basic FGF mediates an immediate response of articular cartilage to mechanical injury. Proc Natl Acad Sci USA. 2002 99 : 8259 8264.
59. Vincent TL, Hermansson MA, Hansen UN, et al. Basic fibroblast growth factor mediates transduction of mechanical signals when articular cartilage is loaded. Arthritis Rheum. 2004 50 : 526 533.
60. Wang X, Manner PA, Horner A, et al. Regulation of MMP-13 expression by RUNX2 and FGF2 in osteoarthritic cartilage. Osteoarthritis Cartilage. 2004 12 : 963 973.
61. Smits P, Li P, Mandel J, et al. The transcription factors L-SOX5 and SOX6 are essential for cartilage formation. Dev Cell. 2001 1 : 277 290.
62. Cucchiarini M, Madry H. Gene therapy for cartilage defects. J Gene Med. 2005 7 : 1495 1509.