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Review Article

Control of chondrogenesis by the transcription factor Sox9

Pages 213-219 | Received 13 Dec 2007, Accepted 16 Jan 2008, Published online: 02 Jan 2014

References

  • Lefebvre V, Dumitriu B, Penzo-Mendez A, Han Y, Pallavi B. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell Biol. 2007;39(12):2195–214.
  • Akiyama H, Chaboissier MC, Martin JF, Schedl A, de Cromb-rugghe B. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev. 2002;16(21):2813–28.
  • Akiyama H, Chaboissier MC, Behringer RR, Rowitch DH, Schedl A, Epstein JA, et al. Essential role of Sox9 in the pathway that controls formation of cardiac valves and septa. Proc Natl Acad Sci USA. 2004;101(17):6502–7.
  • Chaboissier MC, Kobayashi A, Vidal VI, Lutzkendorf S, van de Kant HJ, Wegner M, et al. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development. 2004;131(9):1891–901.
  • Stolt CC, Lommes P, Sock E, Chaboissier MC, Schedl A, Wegner M. The Sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes Dev. 2003;17(13):1677–89.
  • Smits P, Li P, Mandel J, Zhang Z, Deng JM, Behringer RR, et al. The transcription factors L-Sox5 and Sox6 are essential for car-tilage formation. Dev Cell. 2001;1(2):277–90.
  • Stolt CC, Schlierf A, Lommes P, Hillgartner S, Werner T, Kosian T, et al. SoxD proteins influence multiple stages of oligoden-drocyte development and modulate SoxE protein function. Dev Cell. 2006;11(5):697–709.
  • Foster JW, Dominguez-Steglich MA, Guiofi S, Kowk G, Weller PA, Stevanovic M, et al. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature. 1994;372(6506):525–30.
  • Wagner T, Wirth J, Meyer J, Zabel B, Held M, Zimmer J, et al. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene 50X9. Cell. 1994;79(6):1111–20.
  • Epstein CJ, Erickson RP, Wynshaw-Boris A. Inborn errors of development. New York: Oxford University Press; 2004.
  • Ng LJ, Wheatley S, Muscat GE, Conway-Campbell J, Bowles J, Wright E, et al. 50X9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev Biol. 1997;183(1):108–21.
  • Zhao Q, Eberspaecher H, Lefebvre V, De Crombrugghe B. Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev Dyn. 1997;209(4):377–86.
  • Lefebvre V, Huang W, Harley VR, Goodfellow PN, de Cromb-rugghe B. 50X9 is a potent activator of the chondrocyte-specific enhancer of the pro alphal(II) collagen gene. Mol Cell Biol. 1997;17(4):2336–46.
  • Bernard P, Tang P, Liu S, Dewing P, Harley VR, Vilain E. Dimerization of 50X9 is required for chondrogenesis, but not for sex determination. Hum Mol Genet. 2003;12(14):1755–65.
  • Sock E, Pagon RA, Keymolen K, Lissens W, Wegner M, Scherer G. Loss of DNA-dependent dimerization of the transcription factor 50X9 as a cause for campomelic dysplasia. Hum Mol Genet. 2003;12(12):1439–47.
  • Jenkins E, Moss JB, Pace JM, Bridgewater LC. The new collagen gene COL27A1 contains 50X9-responsive enhancer elements. Matrix Biol. 2005;24(3):177–84.
  • Rentsendoij 0, Nagy A, Sinko I, Daraba A, Barta E, Kiss I. Highly conserved proximal promoter element harbouring paired Sox9-binding sites contributes to the tissue- and developmental stage-specific activity of the matrilin-1 gene. Biochem J. 2005;389\(Pt 3):705–16.
  • Genzer MA, Bridgewater LC. A Col9a1 enhancer element acti-vated by two interdependent 50X9 dimers. Nucleic Acids Res. 2007;35(4):1178–86.
  • Bi W, Huang W, Whitworth DJ, Deng JM, Zhang Z, Behringer RR, et al. Haploinsufficiency of Sox9 results in defective carti-lage primordia and premature skeletal mineralization. Proc Natl Acad Sci USA. 2001;98(12):6698–703.
  • Bi W, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B. Sox9 is required for cartilage formation. Nat Genet. 1999;22(1):85–9.
  • Akiyama H, Lyons JP, Mori-Akiyama Y, Yang X, Zhang R, Zhang Z, et al. Interactions between Sox9 and beta-catenin control chondrocyte differentiation. Genes Dev. 2004;18(9):1072–87.
  • Yun K, Wold B. Skeletal muscle determination and differentia-tion: story of a core regulatory network and its context. Curr Opin Cell Biol. 1996;8(6):877–89.
  • Arnold HH, Winter B. Muscle differentiation: more complexity to the network of myogenic regulators. Curr Opin Genet Dev. 1998;8(5):539–44.
  • Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, et al. Targeted disruption of Cbfal results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell. 1997;89(5):755–64.
  • Otto F, Thorne11 AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, et al. Cbfal, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell. 1997;89(5):765–71.
  • Nakashima K, Thou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, et al. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone for-mation. Cell. 2002;108(1):17–29.
  • Ikeda T, Kamekura S, Mabuchi A, Kou I, Seki S, Takato T, et al. The combination of 50X5, 50X6, and 50X9 (the SOX trio) provides signals sufficient for induction of permanent cartilage. Arthritis Rheum. 2004;50(11):3561–73.
  • Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, et al. SOX9 directly regulates the type-II collagen gene. Nat Genet. 1997;16(2):174–8.
  • Zeng L, Kempf H, Murtaugh LC, Sato ME, Lassar AB. Shh establishes an Nkx3.2/Sox9 autoregulatory loop that is main-tained by BMP signals to induce somitic chondrogenesis. Genes Dev. 2002;16(15):1990–2005.
  • Kawakami Y, Tsuda M, Takahashi S, Taniguchi N, Esteban CR, Zemmyo M, et al. Transcriptional coactivator PGC- lalpha reg-ulates chondrogenesis via association with Sox9. Proc Natl Acad Sci USA. 2005;102(7):2414–9.
  • Akiyama H, Stadler HS, Martin JF, Ishii TM, Beachy PA, Nakamura T, et al. Misexpression of Sox9 in mouse limb bud mesenchyme induces polydactyly and rescues hypodactyly mice. Matrix Biol. 2006.
  • Murakami S, Kan M, McKeehan WL, de Crombrugghe B. Up-regulation of the chondrogenic Sox9 gene by fibroblast growth factors is mediated by the mitogen-activated protein kinase pathway. Proc Natl Acad Sci USA. 2000;97(3):1113–8.
  • Shakibaei M, Seifarth C, John T, Rahmanzadeh M, Mobasheri A. Igf-I extends the chondrogenic potential of human articular chondrocytes in vitro: molecular association between Sox9 and Erk1/2. Biochem Pharmacol. 2006;72(11):1382–95.
  • Jacques C, Recklies AD, Levy A, Berenbaum F. HC-gp39 con-tributes to chondrocyte differentiation by inducing SOX9 and type II collagen expressions. Osteoarthritis Cartilage. 2007;15(2):138–46.
  • Muramatsu S, Wakabayashi M, Ohno T, Amano K, Ooishi R, Sugahara T, et al. Functional gene screening system identified TRPV4 as a regulator of chondrogenic differentiation. J Biol Chem. 2007;282(44):32158–67.
  • Afonja 0, Raaka BM, Huang A, Das S, Zhao X, Helmer E, et al. RAR agonists stimulate SOX9 gene expression in breast cancer cell lines: evidence for a role in retinoid-mediated growth inhi-bition. Oncogene. 2002;21(51):7850–60.
  • Bursell L, Woods A, James CG, Pala D, Leask A, Beier F. Src kinase inhibition promotes the chondrocyte phenotype. Arthritis Res Ther. 2007;9(5):R105.
  • Colter DC, Piera-Velazquez S, Hawkins DF, Whitecavage MK, Jimenez SA, Stokes DG. Regulation of the human Sox9 promoter by the CCAAT-binding factor. Matrix Biol. 2005;24(3):185–97.
  • Piera-Velazquez S, Hawkins DF, Whitecavage MK, Colter DC, Stokes DG, Jimenez SA. Regulation of the human 50X9 pro-moter by Sp 1 and CREB. Exp Cell Res. 2007;313(6):1069–79.
  • Tavella S, Biticchi R, Schito A, Minina E, Di Martino D, Pagano A, et al. Targeted expression of SHH affects chondrocyte dif-ferentiation, growth plate organization, and Sox9 expression. J Bone Miner Res. 2004;19(10):1678–88.
  • Robins JC, Akeno N, Mukherjee A, Dalal RR, Aronow BJ, Koopman P, et al. Hypoxia induces chondrocyte-specific gene expression in mesenchymal cells in association with transcrip-tional activation of Sox9. Bone. 2005;37(3):313–22.
  • Amarilio R, Viukov SV, Sharir A, Eshkar-Oren I, Johnson RS, Zelzer E. HIF1 {alpha} regulation of Sox9 is necessary to main-tain differentiation of hypoxic prechondrogenic cells during early skeletogenesis. Development. 2007;134(21):3917–28.
  • Lefebvre V, Smits P. Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res C Embryo Today. 2005;75(3):200–12.
  • Velagaleti GV, Bien-Willner GA, Northup JK, Lockhart LH, Hawkins JC, Jalal SM, et al. Position effects due to chromosome breakpoints that map approximately 900 Kb upstream and approximately 1.3 Mb downstream of 50X9 in two patients with campomelic dysplasia. Am J Hum Genet. 2005;76(4):652–62.
  • Leipoldt M, Erdel M, Bien-Willner G, Smyk M, Theurl M, Yatsenko S, et al. Two novel translocation breakpoints upstream of 50X9 define borders of the proximal and distal breakpoint cluster region in campomelic dysplasia. Clin Genet. 2007;71(1):67–75.
  • Wunderle VM, Critcher R, Hastie N, Goodfellow PN, Schedl A. Deletion of long-range regulatory elements upstream of 50X9 causes campomelic dysplasia. Proc Natl Acad Sci USA. 1998;95(18):10649–54.
  • Huang W, Zhou X, Lefebvre V, de Crombrugghe B. Phosphor-ylation of 50X9 by cyclic AMP-dependent protein kinase A enhances 50X9's ability to transactivate a Col2a1 chondrocyte-specific enhancer. Mol Cell Biol. 2000;20(11):4149–58.
  • Huang W, Chung UI, Kronenberg HM, de Crombrugghe B. The chondrogenic transcription factor Sox9 is a target of signaling by the parathyroid hormone-related peptide in the growth plate of endochondral bones. Proc Natl Acad Sci USA. 2001;98(1):160–5.
  • Argentaro A, Sim H, Kelly S, Preiss S, Clayton A, Jans DA, et al. A 50X9 defect of calmodulin-dependent nuclear import in campomelic dysplasia/autosomal sex reversal. J Biol Chem. 2003;278(36):33839–47.
  • Chikuda H, Kugimiya F, Hoshi K, Ikeda T, Ogasawara T, Shimoaka T, et al. Cyclic GMP-dependent protein kinase II is a molecular switch from proliferation to hypertrophic differentia-tion of chondrocytes. Genes Dev. 2004;18(19):2418–29.
  • Taylor KM, Labonne C. SoxE factors function equivalently during neural crest and inner ear development and their activity is regulated by SUMOylation. Dev Cell. 2005;9(5):593–603.
  • Komatsu T, Mizusaki H, Mukai T, Ogawa H, Baba D, Shirakawa M, et al. Small ubiquitin-like modifier 1 (SUMO-1) modification of the synergy control motif of Ad4 binding protein/steroidogenic factor 1 (Ad4BP/SF-1) regulates synergistic transcription between Ad4BP/SF-1 and Sox9. Mol Endocrinol. 2004;18(10):2451–62.
  • Oh HJ, Kido T, Lau YF. PIAS1 interacts with and represses 50X9 transactivation activity. Mol Reprod Dev. 2007;74(11):1446–55.
  • Akiyama H, Kamitani T, Yang X, Kandyil R, Bridgewater LC, Fellous M, et al. The transcription factor Sox9 is degraded by the ubiquitin-proteasome system and stabilized by a mutation in a ubiquitin-target site. Matrix Biol. 2005;23(8):499–505.
  • Lefebvre V, Li P, de Crombrugghe B. A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene. EMBO J. 1998;17(19):5718–33.
  • Lefebvre V, Behringer RR, de Crombrugghe B. L-Sox5, Sox6 and Sox9 control essential steps of the chondrocyte differentia-tion pathway. Osteoarthritis Cartilage. 2001;9(Suppl A):569–75.
  • Huang W, Lu N, Eberspaecher H, De Crombrugghe B. A new long form of c-Maf cooperates with Sox9 to activate the type II collagen gene. J Biol Chem. 2002;277(52):50668–75.
  • Meech R, Edelman DB, Jones FS, Makarenkova HP. The homeobox transcription factor Barx2 regulates chondrogenesis during limb development. Development. 2005;132(9):2135–46.
  • Tsuda M, Takahashi S, Takahashi Y, Asahara H. Transcriptional co-activators CREB-binding protein and p300 regulate chondro-cyte-specific gene expression via association with Sox9. J Biol Chem. 2003;278(29):27224–9.
  • Furumatsu T, Tsuda M, Taniguchi N, Tajima Y, Asahara H. Smad3 induces chondrogenesis through the activation of 50X9 via CREB-binding protein/p300 recruitment. J Biol Chem. 2005;280(9):8343–50.
  • Zhou R, Bonneaud N, Yuan CX, de Santa Barbara P, Boizet B, Schomber T, et al. 50X9 interacts with a component of the human thyroid hormone receptor-associated protein complex. Nucleic Acids Res. 2002;30(14):3245–52.
  • Rau MJ, Fischer S, Neumann CJ. Zebrafish Trap230/Med12 is required as a coactivator for Sox9-dependent neural crest, carti-lage and ear development. Dev Biol. 2006;296(1):83–93.
  • Tew SR, Clegg PD, Brew CJ, Redmond CM, Hardingham TE. SOX9 transduction of a human chondrocytic cell line identifies novel genes regulated in primary human chondrocytes and in osteoarthritis. Arthritis Res Ther. 2007;9(5):R107.
  • Takahashi I, Nuckolls GH, Takahashi K, Tanaka 0, Semba I, Dashner R, et al. Compressive force promotes sox9, type II collagen and aggrecan and inhibits IL- lbeta expression resulting in chondrogenesis in mouse embryonic limb bud mesenchymal cells. J Cell Sci. 1998;111 ( Pt 14):2067–76.
  • Tsuchiya H, Kitoh H, Sugiura F, Ishiguro N. Chondrogenesis enhanced by overexpression of sox9 gene in mouse bone marrow-derived mesenchymal stem cells. Biochem Biophys Res Commun. 2003 ;301 (2) : 338–43.
  • Li Y, Tew SR, Russell AM, Gonzalez KR, Hardingham TE, Hawkins RE. Transduction of passaged human articular chon-drocytes with adenoviral, retroviral, and lentiviral vectors and the effects of enhanced expression of SOX9. Tissue Eng. 2004;10(3-4):575–84.
  • Tew SR, Li Y, Pothacharoen P, Tweats LM, Hawkins RE, Hardingham TE. Retroviral transduction with SOX9 enhances re-expression of the chondrocyte phenotype in passaged osteo-arthritic human articular chondrocytes. Osteoarthritis Cartilage. 2005;13(1):80–9.
  • Cucchiarini M, Thum T, Weimer A, Kohn D, Terwilliger EF, Madry H. Restoration of the extracellular matrix in human osteoarthritic articular cartilage by overexpression of the tran-scription factor SOX9. Arthritis Rheum. 2007;56(1):158–67.
  • Gruber HE, Norton H.T, Ingram JA, Hanley EN Jr The SOX9 transcription factor in the human disc: decreased immunolocali-zation with age and disc degeneration. Spine. 2005;30(6):625–30.
  • Paul R, Haydon RC, Cheng H, Ishikawa A, Nenadovich N, Jiang W, et al. Potential use of Sox9 gene therapy for intervertebral degenerative disc disease. Spine. 2003;28(8):755–63.
  • Zhang Y, Anderson DG, Phillips FM, Thonar RI, He TC, Pietryla D, et al. Comparative effects of bone morphogenetic proteins and Sox9 overexpression on matrix accumulation by bovine anulus fibrosus cells: implications for anular repair. Spine. 2007;32(23):2515–20.
  • Malki S, Nef S, Notarnicola C, Thevenet L, Gasca S, Mejean C, et al. Prostaglandin D2 induces nuclear import of the sex-deter-mining factor 50X9 via its cAMP-PKA phosphorylation. EMBO J. 2005;24(10):1798–809.
  • Murakami S, Lefebvre V, de Crombrugghe B. Potent inhibition of the master chondrogenic factor Sox9 gene by interleukin-1 and tumor necrosis factor-alpha. J Biol Chem. 2000;275(5):3687–92.
  • Legendre F, Dudhia J, Pujol JP, Bogdanowicz P. JAK/STAT but not ERK1/ERK2 pathway mediates interleukin (IL)-6/soluble IL-6R down-regulation of Type II collagen, aggrecan core, and link protein transcription in articular chondrocytes. Association with a down-regulation of 50X9 expression. J Biol Chem. 2003;278(5):2903–12.
  • Schaefer JF, Millham ML, de Crombrugghe B, Buckbinder L. FGF signaling antagonizes cytokine-mediated repression of Sox9 in SW1353 chondrosarcoma cells. Osteoarthritis Cartilage. 2003;11(4):233–41.
  • Shealy DJ, Wooley PH, Emmell E, Volk A, Rosenberg A, Treacy G, et al. Anti-TNF-alpha antibody allows healing of joint damage in polyarthritic transgenic mice. Arthritis Res. 2002;4(5):R7.
  • Klareskog L, van der Heijde D, de Jager JP, Gough A, Kalden J, Malaise M, et al. Therapeutic effect of the combination of eta-nercept and methotrexate compared with each treatment alone in patients with rheumatoid arthritis: double-blind randomised controlled trial. Lancet. 2004;363(9410):675–81.

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