Role of Sox9 in growth factor regulation of articular chondrocytes

Journal of Cellular Biochemistry

Volumn 116, Issue 7, 2015, Pages 1391-1400

  Shi, Shuiliang ^a   Wang, Congrong ^a   Acton, Anthony J ^a   Eckert, George J ^a   Trippel, Stephen B ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ARTICULAR CHONDROCYTES; GROWTH FACTORS; SMALL INHIBITORY RNA; sox9

Indexed keywords

AGGRECAN; BONE MORPHOGENETIC PROTEIN 2; COLLAGEN TYPE 1; COLLAGEN TYPE 2; DNA; FIBROBLAST GROWTH FACTOR 2; GLYCOSAMINOGLYCAN; OSTEOGENIC PROTEIN 1; SMALL INTERFERING RNA; SOMATOMEDIN C; TRANSCRIPTION FACTOR SOX9; SIGNAL PEPTIDE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARTILAGE CELL; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; DNA CONTENT; EXTRACELLULAR MATRIX; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; TRANSGENE; ANIMAL; ARTICULAR CARTILAGE; BOVINE; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

BOVINAE;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 7; CARTILAGE, ARTICULAR; CATTLE; CELL PROLIFERATION; CELLS, CULTURED; CHONDROCYTES; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION; INSULIN-LIKE GROWTH FACTOR I; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; SOX9 TRANSCRIPTION FACTOR;

EID: 84929118869     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.25099     Document Type: Article

References (50)

1. Aigner T, Gebhard PM, Schmid E, Bau B, Harley V, Poschl E,. 2003. SOX9 expression does not correlate with type II collagen expression in adult articular chondrocytes. Matrix Biol 22: 363-372.
2. Akiyama H, Lefebvre V,. 2011. Unraveling the transcriptional regulatory machinery in chondrogenesis. J Bone Miner Metab 29: 390-395.
3. Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, Sham MH, Koopman P, Tam PP, Cheah KS,. 1997. SOX9 directly regulates the type-II collagen gene. Nat Genet 16: 174-178.
4. Bi W, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B,. 1999. Sox9 is required for cartilage formation. Nat Genet 22: 85-89.
5. Bradham DM, der Wiesche B, Precht P, Balakir R, Horton W,. 1994. Transrepression of type II collagen by TGF-beta and FGF is protein kinase C dependent and is mediated through regulatory sequences in the promoter and first intron. J Cell Physiol 158: 61-68.
6. Buckwalter JA, Mankin HJ,. 1998. Articular cartilage repair and transplantation. Arthritis Rheum 41: 1331-1342.
7. Chen D, Zhao M, Mundy GR,. 2004. Bone morphogenetic proteins. Growth Factors 22: 233-241.
8. Chubinskaya S, Hurting M, Rueger DC,. 2007. OP-1/BMP-7 in cartilage repair. Int Orthop 31: 773-781.
9. Cucchiarini M, Orth P, Madry H,. 2013. Direct rAAV SOX9 administration for durable articular cartilage repair with delayed terminal differentiation and hypertrophy in vivo. J Mol Med (Berl) 91: 625-636.
10. Cucchiarini M, Terwilliger EF, Kohn D, Madry H,. 2009. Remodelling of human osteoarthritic cartilage by FGF-2, alone or combined with Sox9 via rAAV gene transfer. J Cell Mol Med 13: 2476-2488.
11. Cucchiarini M, Thurn T, Weimer A, Kohn D, Terwilliger EF, Madry H,. 2007. Restoration of the extracellular matrix in human osteoarthritic articular cartilage by overexpression of the transcription factor SOX9. Arthritis Rheum 56: 158-167.
12. Davies SR, Sakano S, Zhu Y, Sandell LJ., 2002. Distribution of the transcription factors Sox9, AP-2, and [delta]EF1 in adult murine articular and meniscal cartilage and growth plate. J Histochem Cytochem 50: 1059-1065.
13. de Crombrugghe B, Lefebvre V, Behringer RR, Bi W, Murakami S, Huang W,. 2000. Transcriptional mechanisms of chondrocyte differentiation. Matrix Biol 19: 389-394.
14. Ellman MB, Yan D, Ahmadinia K, Chen D, An HS, Im HJ,. 2013. Fibroblast growth factor control of cartilage homeostasis. J Cell Biochem 114: 735-742.
15. Eyre D,. 2002. Collagen of articular cartilage. Arthritis Res 4: 30-35.
16. Flechtenmacher J, Huch K, Thonar EJ, Mollenhauer JA, Davies SR, Schmid TM, Puhl W, Sampath TK, Aydelotte MB, Kuettner KE,. 1996. Recombinant human osteogenic protein 1 is a potent stimulator of the synthesis of cartilage proteoglycans and collagens by human articular chondrocytes. Arthritis Rheum 39: 1896-1904.
17. Fortier LA, Mohammed HO, Lust G, Nixon AJ., 2002. Insulin-like growth factor-I enhances cell-based repair of articular cartilage. J Bone Joint Surg Br 84: 276-288.
18. Fujimoto E, Ochi M, Kato Y, Mochizuki Y, Sumen Y, Ikuta Y,. 1999. Beneficial effect of basic fibroblast growth factor on the repair of full-thickness defects in rabbit articular cartilage. Arch Orthop Trauma Surg 119: 139-145.
19. Goodrich LR, Hidaka C, Robbins PD, Evans CH, Nixon AJ,. 2007. Genetic modification of chondrocytes with insulin-like growth factor-1 enhances cartilage healing in an equine model. J Bone Joint Surg Br 89: 672-685.
20. Grunder T, Gaissmaier C, Fritz J, Stoop R, Hortschansky P, Mollenhauer J, Aicher WK,. 2004. Bone morphogenetic protein (BMP)-2 enhances the expression of type II collagen and aggrecan in chondrocytes embedded in alginate beads. Osteoarthritis Cartilage 12: 559-567.
21. Henry SP, Liang S, Akdemir KC, de Crombrugghe B,. 2012. The postnatal role of Sox9 in cartilage. J Bone Miner Res 27: 2511-2525.
22. Henson FM, Bowe EA, Davies ME,. 2005. Promotion of the intrinsic damage-repair response in articular cartilage by fibroblastic growth factor-2. Osteoarthritis Cartilage 13: 537-544.
23. Im H-J, Muddasani P, Natarajan V, Schmid TM, Block JA, Davis F, van Wijnen AJ, Loeser RF,. 2007. Basic fibroblast growth factor stimulates matrix metalloproteinase-13 via the molecular cross-talk between the mitogen-activated protein kinases and protein kinase Cdelta pathways in human adult articular chondrocytes. J Biol Chem 282: 11110-11121.
24. Kypriotou M, Fossard-Demoor M, Chadjichristos C, Ghayor C, de Crombrugghe B, Pujol J, Galera P,. 2003. SOX9 exerts a bifunctional effect on type II collagen gene (COL2A1) expression in chondrocytes depending on the differentiation state. DNA Cell Biol 22: 119-129.
25. Lefebvre V, Smits P,. 2005. Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res C 75: 200-212.
26. Loeser RF, Pacione CA, Chubinskaya S,. 2003. The combination of insulin-like growth factor 1 and osteogenic protein 1 promotes increased survival of and matrix synthesis by normal and osteoarthritic human articular chondrocytes. Arthritis Rheum 48: 2188-2196.
27. Luyten FP, Hascall VC, Nissley SP, Morales TI, Reddi AH,. 1988. Insulin-like growth factors maintain steady-state metabolism of proteoglycans in bovine articular cartilage explants. Arch Biochem Biophys 267: 416-425.
28. Madry H, Emkey G, Zurakowski D, Trippel SB,. 2004. Overexpression of human fibroblast growth factor 2 stimulates cell proliferation in an ex vivo model of articular chondrocyte transplantation. J Gene Med 6: 238-245.
29. Madry H, Kaul G, Cucchiarini M, Stein U, Zurakowski D, Remberger K, Menger MD, Kohn D, Trippel SB,. 2005. Enhanced repair of articular cartilage defects in vivo by transplanted chondrocytes overexpressing insulin-like growth factor I (IGF-I). Gene Ther 12: 1171-1179.
30. Madry H, Zurakowski D, Trippel SB,. 2001. Overexpression of human insulin-like growth factor-I promotes new tissue formation in an ex vivo model of articular chondrocyte transplantation. Gene Ther 8: 1443-1449.
31. Mandl EW, Jahr H, Koevoet JLM, van Leeuwen JPTM, Weinans H, Verhaar JAN, van Osch GJVM,. 2004. Fibroblast growth factor-2 in serum-free medium is a potent mitogen and reduces dedifferentiation of human ear chondrocytes in monolayer culture. Matrix Biol 23: 231-241.
32. Montaseri A, Busch F, Mobasheri A, Buhrmann C, Aldinger C, Rad JS, Shakibaei M,. 2011. IGF-1 and PDGF-bb suppress IL-1beta-induced cartilage degradation through down-regulation of NF-B signaling: Involvement of Src/PI-3K/AKT pathway. PLoS ONE 6: e28663.
33. Murakami S, Kan M, McKeehan WL, de Crombrugghe B,. 2000. Up-regulation of the chondrogenic Sox9 gene by fibroblast growth factors is mediated by the mitogen-activated protein kinase pathway. Proc Natl Acad Sci U S A 97: 1113-1118.
34. Pan Q, Yu Y, Chen Q, Li C, Wu H, Wan Y, Ma J, Sun F,. 2008. Sox9, a key transcription factor of bone morphogenetic protein-2-induced chondrogenesis, is activated through BMP pathway and a CCAAT box in the proximal promoter. J Cell Physiol 217: 228-241.
35. Renard E, Poree B, Chadjichristos C, Kypriotou M, Maneix L, Bigot N, Legendre F, Ollitrault D, De Crombrugghe B, Mallein-Gerin F, Moslemi S, Demoor M, Boumediene K, Galera P,. 2012. Sox9/Sox6 and Sp1 are involved in the insulin-like growth factor-I-mediated upregulation of human type II collagen gene expression in articular chondrocytes. J Mol Med 90: 649-666.
36. Sah RL, Chen AC, Grodzinsky AJ, Trippel SB,. 1994. Differential effects of bFGF and IGF-I on matrix metabolism in calf and adult bovine cartilage explants. Arch Biochem Biophys 308: 137-147.
37. Sailor LZ, Hewick Rm, Morris EA,. 1996. Recombinant human bone morphogenetic protein-2 maintains the articular chondrocyte phenotype in long-term culture. J Orthop Res 14: 937-945.
38. Salminen H, Vuorio E, Saamanen AM,. 2001. Expression of Sox9 and type IIA procollagen during attempted repair of articular cartilage damage in a transgenic mouse model of osteoarthritis. Arthritis Rheum 44: 947-955.
39. Sekiya I, Tsuji K, Koopman P, Watanabe H, Yamada Y, Shinomiya K, Nifuji A, Noda M,. 2000. SOX9 enhances aggrecan gene promoter/enhancer activity and is up-regulated by retinoic acid in a cartilage-derived cell line, TC6. J Biol Chem 275: 10738-10744.
40. Shakibaei M, Seifarth C, John T, Rahmanzadeh M, Mobasheri A,. 2006. Igf-I extends the chondrogenic potential of human articular chondrocytes in vitro: Molecular association between Sox9 and Erk1/2. Biochem Pharmacol 72: 1382-1395.
41. Shi S, Mercer S, Eckert GJ, Trippel SB,. 2012. Regulation of articular chondrocyte aggrecan and collagen gene expression by multiple growth factor gene transfer. J Orthop Res 30: 1026-1031.
42. Shi S, Mercer S, Eckert GJ, Trippel SB,. 2013. Growth factor transgenes interactively regulate articular chondrocytes. J Cell Biochem 114: 908-919.
43. Tew SR, Pothacharoen P, Katopodi T, Hardingham TE,. 2008. SOX9 transduction increases chondroitin sulfate synthesis in cultured human articular chondrocytes without altering glycosyltransferase and sulfotransferase transcription. Biochem J 414: 231-236.
44. Trippel SB,. 1995. Growth factor actions on articular cartilage. J Rheumatol Suppl 43: 129-132.
45. von der Mark K, Gauss V, von der Mark H, Muller P,. 1977. Relationship between cell shape and type of collagen synthesised as chondrocytes lose their cartilage phenotype in culture. Nature 267: 531-532.
46. Werner H, Weinstein D, Bentov I,. 2008. Similarities and differences between insulin and IGF-I: structures, receptors, and signalling pathways. Arch Physiol Biochem 114: 17-22.
47. Wright E, Hargrave MR, Christiansen J, Cooper L, Kun J, Evans T, Gangadharan U, Greenfield A, Koopman P,. 1995. The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos. Nat Genet 9: 15-20.
48. Yagi R, McBurney D, Laverty D, Weiner S, Horton WE Jr,. 2005. Intrajoint comparisons of gene expression patterns in human osteoarthritis suggest a change in chondrocyte phenotype. J Orthop Res 23: 1128-1138.
49. Yokoo N, Saito T, Uesugi M, Kobayashi N, Xin KQ, Okuda K, Mizukami H, Ozawa K, Koshino T,. 2005. Repair of articular cartilage defect by autologous transplantation of basic fibroblast growth factor gene-transduced chondrocytes with adeno-associated virus vector. Arthritis Rheum 52: 164-170.
50. Zhou G, Lefebvre V, Zhang Z, Eberspaecher H, de Crombrugghe B,. 1998. Three high mobility group-like sequences within a 48-base pair enhancer of the Col2a1 gene are required for cartilage-specific expression in vivo. J Biol Chem 273: 14989-14997.