Sox9 directly promotes Bapx1 gene expression to repress Runx2 in chondrocytes

Experimental Cell Research

Volumn 315, Issue 13, 2009, Pages 2231-2240

  Yamashita, Satoshi ^a   Andoh, Masataka ^b   Ueno Kudoh, Hiroe ^a   Sato, Tempei ^a,c   Miyaki, Shigeru ^d   Asahara, Hiroshi ^a,d  

^a NATIONAL RESEARCH INSTITUTE FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^b NEC CORPORATION   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Bapx1; Chondrocyte; Chondrogenesis; Runx2; shRNA; Sox9

Indexed keywords

BAPX1 PROTEIN; COLLAGEN; COLLAGEN TYPE 10 ALPHA 1; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CHONDROGENESIS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENCHONDRAL OSSIFICATION; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENE REPRESSION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION REGULATION;

VERTEBRATA;

EID: 67349120238     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.03.008     Document Type: Article

References (47)

1. Provot S., and Schipani E. Molecular mechanisms of endochondral bone development. Biochem. Biophys. Res. Commun. 328 (2005) 658-665
2. Lefebvre V., and Smits P. Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res. C. Embryo Today 75 (2005) 200-212
3. Goldring M.B., Tsuchimochi K., and Ijiri K. The control of chondrogenesis. J. Cell. Biochem. 97 (2006) 33-44
4. Lefebvre V., Huang W., Harley V.R., Goodfellow P.N., and de Crombrugghe B. SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol. Cell. Biol. 17 (1997) 2336-2346
5. Bridgewater L.C., Lefebvre V., and de Crombrugghe B. Chondrocyte-specific enhancer elements in the Col11a2 gene resemble the Col2a1 tissue-specific enhancer. J. Biol. Chem. 273 (1998) 14998-15006
6. Sekiya I., Tsuji K., Koopman P., Watanabe H., Yamada Y., Shinomiya K., Nifuji A., and Noda M. 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 (2000) 10738-10744
7. Bi W., Deng J.M., Zhang Z., Behringer R.R., and de Crombrugghe B. Sox9 is required for cartilage formation. Nat. Genet. 22 (1999) 85-89
8. Akiyama H., Chaboissier M.C., Martin J.F., Schedl A., and de Crombrugghe 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. 16 (2002) 2813-2828
9. Akiyama H., Lyons J.P., Mori-Akiyama Y., Yang X., Zhang R., Zhang Z., Deng J.M., Taketo M.M., Nakamura T., Behringer R.R., McCrea P.D., and de Crombrugghe B. Interactions between Sox9 and beta-catenin control chondrocyte differentiation. Genes Dev. 18 (2004) 1072-1087
10. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., Shimizu Y., Bronson R.T., Gao Y.H., Inada M., Sato M., Okamoto R., Kitamura Y., Yoshiki S., and Kishimoto T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89 (1997) 755-764
11. Inada M., Yasui T., Nomura S., Miyake S., Deguchi K., Himeno M., Sato M., Yamagiwa H., Kimura T., Yasui N., Ochi T., Endo N., Kitamura Y., Kishimoto T., and Komori T. Maturational disturbance of chondrocytes in Cbfa1-deficient mice. Dev. Dyn. 214 (1999) 279-290
12. Kim I.S., Otto F., Zabel B., and Mundlos S. Regulation of chondrocyte differentiation by Cbfa1. Mech. Dev. 80 (1999) 159-170
13. Takeda S., Bonnamy J.P., Owen M.J., Ducy P., and Karsenty G. Continuous expression of Cbfa1 in nonhypertrophic chondrocytes uncovers its ability to induce hypertrophic chondrocyte differentiation and partially rescues Cbfa1-deficient mice. Genes Dev. 15 (2001) 467-481
14. Ueta C., Iwamoto M., Kanatani N., Yoshida C., Liu Y., Enomoto-Iwamoto M., Ohmori T., Enomoto H., Nakata K., Takada K., Kurisu K., and Komori T. Skeletal malformations caused by overexpression of Cbfa1 or its dominant negative form in chondrocytes. J. Cell. Biol. 153 (2001) 87-100
15. Zhou G., Zheng Q., Engin F., Munivez E., Chen Y., Sebald E., Krakow D., and Lee B. Dominance of SOX9 function over RUNX2 during skeletogenesis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 19004-19009
16. Lettice L.A., Purdie L.A., Carlson G.J., Kilanowski F., Dorin J., and Hill R.E. The mouse bagpipe gene controls development of axial skeleton, skull, and spleen. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 9695-9700
17. Tribioli C., and Lufkin T. The murine Bapx1 homeobox gene plays a critical role in embryonic development of the axial skeleton and spleen. Development 126 (1999) 5699-5711
18. Akazawa H., Komuro I., Sugitani Y., Yazaki Y., Nagai R., and Noda T. Targeted disruption of the homeobox transcription factor Bapx1 results in lethal skeletal dysplasia with asplenia and gastroduodenal malformation. Genes Cells 5 (2000) 499-513
19. Lengner C.J., Hassan M.Q., Serra R.W., Lepper C., van Wijnen A.J., Stein J.L., Lian J.B., and Stein G.S. Nkx3.2-mediated repression of Runx2 promotes chondrogenic differentiation. J. Biol. Chem. 280 (2005) 15872-15879
20. Provot S., Kempf H., Murtaugh L.C., Chung U.I., Kim D.W., Chyung J., Kronenberg H.M., and Lassar A.B. Nkx3.2/Bapx1 acts as a negative regulator of chondrocyte maturation. Development 133 (2006) 651-662
21. Zeng L., Kempf H., Murtaugh L.C., Sato M.E., and Lassar A.B. Shh establishes an Nkx3.2/Sox9 autoregulatory loop that is maintained by BMP signals to induce somitic chondrogenesis. Genes Dev. 16 (2002) 1990-2005
22. Murtaugh L.C., Zeng L., Chyung J.H., and Lassar A.B. The chick transcriptional repressor Nkx3.2 acts downstream of Shh to promote BMP-dependent axial chondrogenesis. Dev. Cell 1 (2001) 411-422
23. Otto F., Thornell A.P., Crompton T., Denzel A., Gilmour K.C., Rosewell I.R., Stamp G.W., Beddington R.S., Mundlos S., Olsen B.R., Selby P.B., and Owen M.J. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89 (1997) 765-771
24. Denker A.E., Haas A.R., Nicoll S.B., and Tuan R.S. Chondrogenic differentiation of murine C3H10T1/2 multipotential mesenchymal cells: I. Stimulation by bone morphogenetic protein-2 in high-density micromass cultures. Diff. Res. Biol. Divers. 64 (1999) 67-76
25. Haas A.R., and Tuan R.S. Murine C3H10T1/2 multipotential cells as an in vitro model of mesenchymal chondrogenesis. Methods Mol. Biol. (Clifton N.J.) 137 (2000) 383-389
26. Zheng Q., Zhou G., Morello R., Chen Y., Garcia-Rojas X., and Lee B. Type X collagen gene regulation by Runx2 contributes directly to its hypertrophic chondrocyte-specific expression in vivo. J. Cell. Biol. 162 (2003) 833-842
27. Bernard P., Tang P., Liu S., Dewing P., Harley V.R., and Vilain E. Dimerization of SOX9 is required for chondrogenesis, but not for sex determination. Hum. Mol. Genet. 12 (2003) 1755-1765
28. Sock E., Pagon R.A., Keymolen K., Lissens W., Wegner M., and Scherer G. Loss of DNA-dependent dimerization of the transcription factor SOX9 as a cause for campomelic dysplasia. Hum. Mol. Genet. 12 (2003) 1439-1447
29. Bridgewater L.C., Walker M.D., Miller G.C., Ellison T.A., Holsinger L.D., Potter J.L., Jackson T.L., Chen R.K., Winkel V.L., Zhang Z., McKinney S., and de Crombrugghe B. Adjacent DNA sequences modulate Sox9 transcriptional activation at paired Sox sites in three chondrocyte-specific enhancer elements. Nucleic Acids Res. 31 (2003) 1541-1553
30. Genzer M.A., and Bridgewater L.C. A Col9a1 enhancer element activated by two interdependent SOX9 dimers. Nucleic Acids Res. 35 (2007) 1178-1186
31. Krebsbach P.H., Nakata K., Bernier S.M., Hatano O., Miyashita T., Rhodes C.S., and Yamada Y. Identification of a minimum enhancer sequence for the type II collagen gene reveals several core sequence motifs in common with the link protein gene. J. Biol. Chem. 271 (1996) 4298-4303
32. De Santa Barbara P., Bonneaud N., Boizet B., Desclozeaux M., Moniot B., Sudbeck P., Scherer G., Poulat F., and Berta P. Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene. Mol. Cell. Biol. 18 (1998) 6653-6665
33. Arango N.A., Lovell-Badge R., and Behringer R.R. Targeted mutagenesis of the endogenous mouse Mis gene promoter: in vivo definition of genetic pathways of vertebrate sexual development. Cell 99 (1999) 409-419
34. Rodrigo I., Hill R.E., Balling R., Munsterberg A., and Imai K. Pax1 and Pax9 activate Bapx1 to induce chondrogenic differentiation in the sclerotome. Development 130 (2003) 473-482
35. Rodrigo I., Bovolenta P., Mankoo B.S., and Imai K. Meox homeodomain proteins are required for Bapx1 expression in the sclerotome and activate its transcription by direct binding to its promoter. Mol. Cell. Biol. 24 (2004) 2757-2766
36. Deutsch U., Dressler G.R., and Gruss P. Pax 1, a member of a paired box homologous murine gene family, is expressed in segmented structures during development. Cell 53 (1988) 617-625
37. Peters H., Neubuser A., Kratochwil K., and Balling R. Pax9-deficient mice lack pharyngeal pouch derivatives and teeth and exhibit craniofacial and limb abnormalities. Genes Dev. 12 (1998) 2735-2747
38. Peters H., Wilm B., Sakai N., Imai K., Maas R., and Balling R. Pax1 and Pax9 synergistically regulate vertebral column development. Development 126 (1999) 5399-5408
39. Candia A.F., Hu J., Crosby J., Lalley P.A., Noden D., Nadeau J.H., and Wright C.V. Mox-1 and Mox-2 define a novel homeobox gene subfamily and are differentially expressed during early mesodermal patterning in mouse embryos. Development 116 (1992) 1123-1136
40. Candia A.F., and Wright C.V. Differential localization of Mox-1 and Mox-2 proteins indicates distinct roles during development. Int. J. Dev. Biol. 40 (1996) 1179-1184
41. Wright E., Hargrave M.R., Christiansen J., Cooper L., Kun J., Evans T., Gangadharan U., Greenfield A., and Koopman P. The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos. Nat. Genet. 9 (1995) 15-20
42. Ng L.J., Wheatley S., Muscat G.E., Conway-Campbell J., Bowles J., Wright E., Bell D.M., Tam P.P., Cheah K.S., and Koopman P. SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev. Biol. 183 (1997) 108-121
43. Zhao Q., Eberspaecher H., Lefebvre V., and De Crombrugghe B. Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev. Dyn. 209 (1997) 377-386
44. Tribioli C., Frasch M., and Lufkin T. Bapx1: an evolutionary conserved homologue of the Drosophila bagpipe homeobox gene is expressed in splanchnic mesoderm and the embryonic skeleton. Mech. Dev. 65 (1997) 145-162
45. Saito T., Ikeda T., Nakamura K., Chung U.I., and Kawaguchi H. S100A1 and S100B, transcriptional targets of SOX trio, inhibit terminal differentiation of chondrocytes. EMBO Rep. 8 (2007) 504-509
46. Wilhelm D., Hiramatsu R., Mizusaki H., Widjaja L., Combes A.N., Kanai Y., and Koopman P. SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development. J. Biol. Chem. 282 (2007) 10553-10560
47. Tribioli C., and Lufkin T. Bapx1 homeobox gene gain-of-function mice show preaxial polydactyly and activated Shh signaling in the developing limb. Dev. Dyn. 235 (2006) 2483-2492