Distinct Transcriptional Programs Underlie Sox9 Regulation of the Mammalian Chondrocyte

Cell Reports

Volumn 12, Issue 2, 2015, Pages 229-243

  Ohba, Shinsuke ^a   He, Xinjun ^b   Hojo, Hironori ^b   McMahon, Andrew P ^b  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR SOX9; RUNX2 PROTEIN, MOUSE; TRANSCRIPTION FACTOR RUNX2;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CARTILAGE CELL; CELL LINEAGE; CHROMATIN; CONTROLLED STUDY; DNA BINDING; ENHANCER REGION; GENE EXPRESSION; MESODERM; MOUSE; NEURAL CREST; NEWBORN; NONHUMAN; PRIORITY JOURNAL; TISSUE SPECIFICITY; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; ANIMAL; CELL CULTURE; CHONDROCYTE; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; TRANSCRIPTION INITIATION;

MAMMALIA;

ANIMALS; CELLS, CULTURED; CHONDROCYTES; CHROMATIN IMMUNOPRECIPITATION; CORE BINDING FACTOR ALPHA 1 SUBUNIT; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, INBRED ICR; SEQUENCE ANALYSIS, DNA; SOX9 TRANSCRIPTION FACTOR; TRANSCRIPTIONAL ACTIVATION;

EID: 84937521813     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.06.013     Document Type: Article

References (77)

1. Akiyama H., Lefebvre V. Unraveling the transcriptional regulatory machinery in chondrogenesis. J. Bone Miner. Metab. 2011, 29:390-395.
2. Akiyama H., Chaboissier M.C., Martin J.F., Schedl A., 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. 2002, 16:2813-2828.
3. Akiyama H., Kim J.E., Nakashima K., Balmes G., Iwai N., Deng J.M., Zhang Z., Martin J.F., Behringer R.R., Nakamura T., de Crombrugghe B. Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc. Natl. Acad. Sci. USA 2005, 102:14665-14670.
4. Arango N.A., Lovell-Badge R., Behringer R.R. Targeted mutagenesis of the endogenous mouse Mis gene promoter: in vivo definition of genetic pathways of vertebrate sexual development. Cell 1999, 99:409-419.
5. Bailey T.L., Boden M., Buske F.A., Frith M., Grant C.E., Clementi L., Ren J., Li W.W., Noble W.S. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009, 37:W202-W208.
6. Behrens A., Haigh J., Mechta-Grigoriou F., Nagy A., Yaniv M., Wagner E.F. Impaired intervertebral disc formation in the absence of Jun. Development 2003, 130:103-109.
7. Bell D.M., Leung K.K., Wheatley S.C., Ng L.J., Zhou S., Ling K.W., Sham M.H., Koopman P., Tam P.P., Cheah K.S. SOX9 directly regulates the type-II collagen gene. Nat. Genet. 1997, 16:174-178.
8. Bernard P., Tang P., Liu S., Dewing P., Harley V.R., Vilain E. Dimerization of SOX9 is required for chondrogenesis, but not for sex determination. Hum. Mol. Genet. 2003, 12:1755-1765.
9. Bessa J., Tena J.J., de la Calle-Mustienes E., Fernández-Miñán A., Naranjo S., Fernández A., Montoliu L., Akalin A., Lenhard B., Casares F., Gómez-Skarmeta J.L. Zebrafish enhancer detection (ZED) vector: a new tool to facilitate transgenesis and the functional analysis of cis-regulatory regions in zebrafish. Dev. Dyn. 2009, 238:2409-2417.
10. Bhandari R.K., Haque M.M., Skinner M.K. Global genome analysis of the downstream binding targets of testis determining factor SRY and SOX9. PLoS ONE 2012, 7:e43380.
11. Bi W., Deng J.M., Zhang Z., Behringer R.R., de Crombrugghe B. Sox9 is required for cartilage formation. Nat. Genet. 1999, 22:85-89.
12. Bi W., Huang W., Whitworth D.J., Deng J.M., Zhang Z., Behringer R.R., de Crombrugghe B. Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc. Natl. Acad. Sci. USA 2001, 98:6698-6703.
13. Birney E., Stamatoyannopoulos J.A., Dutta A., Guigó R., Gingeras T.R., Margulies E.H., Weng Z., Snyder M., Dermitzakis E.T., Thurman R.E., et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007, 447:799-816. ENCODE Project Consortium, NISC Comparative Sequencing ProgramNISC Comparative Sequencing Program, Baylor College of Medicine Human Genome Sequencing CenterBaylor College of Medicine Human Genome Sequencing Center, Washington University Genome Sequencing CenterWashington University Genome Sequencing Center, Broad InstituteBroad Institute, Children's Hospital Oakland Research InstituteChildren's Hospital Oakland Research Institute.
14. Bridgewater L.C., Lefebvre V., de Crombrugghe B. Chondrocyte-specific enhancer elements in the Col11a2 gene resemble the Col2a1 tissue-specific enhancer. J. Biol. Chem. 1998, 273:14998-15006.
15. 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., et al. Adjacent DNA sequences modulate Sox9 transcriptional activation at paired Sox sites in three chondrocyte-specific enhancer elements. Nucleic Acids Res. 2003, 31:1541-1553.
16. Coustry F., Oh C.D., Hattori T., Maity S.N., de Crombrugghe B., Yasuda H. The dimerization domain of SOX9 is required for transcription activation of a chondrocyte-specific chromatin DNA template. Nucleic Acids Res. 2010, 38:6018-6028.
17. De Santa Barbara P., Bonneaud N., Boizet B., Desclozeaux M., Moniot B., Sudbeck P., Scherer G., Poulat F., Berta P. Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Müllerian hormone gene. Mol. Cell. Biol. 1998, 18:6653-6665.
18. Dy P., Wang W., Bhattaram P., Wang Q., Wang L., Ballock R.T., Lefebvre V. Sox9 directs hypertrophic maturation and blocks osteoblast differentiation of growth plate chondrocytes. Dev. Cell 2012, 22:597-609.
19. Foster J.W., Dominguez-Steglich M.A., Guioli S., Kwok C., Weller P.A., Stevanović M., Weissenbach J., Mansour S., Young I.D., Goodfellow P.N., et al. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 1994, 372:525-530.
20. Furumatsu T., Tsuda M., Yoshida K., Taniguchi N., Ito T., Hashimoto M., Ito T., Asahara H. Sox9 and p300 cooperatively regulate chromatin-mediated transcription. J. Biol. Chem. 2005, 280:35203-35208.
21. Genzer M.A., Bridgewater L.C. A Col9a1 enhancer element activated by two interdependent SOX9 dimers. Nucleic Acids Res. 2007, 35:1178-1186.
22. Gross S., Krause Y., Wuelling M., Vortkamp A. Hoxa11 and Hoxd11 regulate chondrocyte differentiation upstream of Runx2 and Shox2 in mice. PLoS ONE 2012, 7:e43553.
23. Han Y., Lefebvre V. L-Sox5 and Sox6 drive expression of the aggrecan gene in cartilage by securing binding of Sox9 to a far-upstream enhancer. Mol. Cell. Biol. 2008, 28:4999-5013.
24. He H.H., Meyer C.A., Shin H., Bailey S.T., Wei G., Wang Q., Zhang Y., Xu K., Ni M., Lupien M., et al. Nucleosome dynamics define transcriptional enhancers. Nat. Genet. 2010, 42:343-347.
25. Heintzman N.D., Stuart R.K., Hon G., Fu Y., Ching C.W., Hawkins R.D., Barrera L.O., Van Calcar S., Qu C., Ching K.A., et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 2007, 39:311-318.
26. Helms J.A., Schneider R.A. Cranial skeletal biology. Nature 2003, 423:326-331.
27. Hu G., Codina M., Fisher S. Multiple enhancers associated with ACAN suggest highly redundant transcriptional regulation in cartilage. Matrix Biol. 2012, 31:328-337.
28. Huang B.L., Brugger S.M., Lyons K.M. Stage-specific control of connective tissue growth factor (CTGF/CCN2) expression in chondrocytes by Sox9 and beta-catenin. J. Biol. Chem. 2010, 285:27702-27712.
29. Ikeda T., Kamekura S., Mabuchi A., Kou I., Seki S., Takato T., Nakamura K., Kawaguchi H., Ikegawa S., Chung U.I. The combination of SOX5, SOX6, and SOX9 (the SOX trio) provides signals sufficient for induction of permanent cartilage. Arthritis Rheum. 2004, 50:3561-3573.
30. Jenkins E., Moss J.B., Pace J.M., Bridgewater L.C. The new collagen gene COL27A1 contains SOX9-responsive enhancer elements. Matrix Biol. 2005, 24:177-184.
31. Ji H., Jiang H., Ma W., Johnson D.S., Myers R.M., Wong W.H. An integrated software system for analyzing ChIP-chip and ChIP-seq data. Nat. Biotechnol. 2008, 26:1293-1300.
32. Kan A., Ikeda T., Saito T., Yano F., Fukai A., Hojo H., Ogasawara T., Ogata N., Nakamura K., Chung U.I., Kawaguchi H. Screening of chondrogenic factors with a real-time fluorescence-monitoring cell line ATDC5-C2ER: identification of sorting nexin 19 as a novel factor. Arthritis Rheum. 2009, 60:3314-3323.
33. Karreth F., Hoebertz A., Scheuch H., Eferl R., Wagner E.F. The AP1 transcription factor Fra2 is required for efficient cartilage development. Development 2004, 131:5717-5725.
34. Kim T.K., Hemberg M., Gray J.M., Costa A.M., Bear D.M., Wu J., Harmin D.A., Laptewicz M., Barbara-Haley K., Kuersten S., et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 2010, 465:182-187.
35. Kimura A., Inose H., Yano F., Fujita K., Ikeda T., Sato S., Iwasaki M., Jinno T., Ae K., Fukumoto S., et al. Runx1 and Runx2 cooperate during sternal morphogenesis. Development 2010, 137:1159-1167.
36. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., Shimizu Y., Bronson R.T., Gao Y.H., Inada M., et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997, 89:755-764.
37. Kou I., Ikegawa S. SOX9-dependent and -independent transcriptional regulation of human cartilage link protein. J. Biol. Chem. 2004, 279:50942-50948.
38. Kronenberg H.M. Developmental regulation of the growth plate. Nature 2003, 423:332-336.
39. Lefebvre V. The SoxD transcription factors-Sox5, Sox6, and Sox13-are key cell fate modulators. Int. J. Biochem. Cell Biol. 2010, 42:429-432.
40. Lefebvre V., Zhou G., Mukhopadhyay K., Smith C.N., Zhang Z., Eberspaecher H., Zhou X., Sinha S., Maity S.N., de Crombrugghe B. An 18-base-pair sequence in the mouse proalpha1(II) collagen gene is sufficient for expression in cartilage and binds nuclear proteins that are selectively expressed in chondrocytes. Mol. Cell. Biol. 1996, 16:4512-4523.
41. 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, 17:5718-5733.
42. Lefebvre V., Dumitriu B., Penzo-Méndez 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, 39:2195-2214.
43. Leung K.K., Ng L.J., Ho K.K., Tam P.P., Cheah K.S. Different cis-regulatory DNA elements mediate developmental stage- and tissue-specific expression of the human COL2A1 gene in transgenic mice. J. Cell Biol. 1998, 141:1291-1300.
44. Leung V.Y., Gao B., Leung K.K., Melhado I.G., Wynn S.L., Au T.Y., Dung N.W., Lau J.Y., Mak A.C., Chan D., Cheah K.S. SOX9 governs differentiation stage-specific gene expression in growth plate chondrocytes via direct concomitant transactivation and repression. PLoS Genet. 2011, 7:e1002356.
45. Liu Y., Li H., Tanaka K., Tsumaki N., Yamada Y. Identification of an enhancer sequence within the first intron required for cartilage-specific transcription of the alpha2(XI) collagen gene. J. Biol. Chem. 2000, 275:12712-12718.
46. Maher B. ENCODE: The human encyclopaedia. Nature 2012, 489:46-48.
47. McLean C.Y., Bristor D., Hiller M., Clarke S.L., Schaar B.T., Lowe C.B., Wenger A.M., Bejerano G. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 2010, 28:495-501.
48. Mead T.J., Wang Q., Bhattaram P., Dy P., Afelik S., Jensen J., Lefebvre V. A far-upstream (-70 kb) enhancer mediates Sox9 auto-regulation in somatic tissues during development and adult regeneration. Nucleic Acids Res. 2013, 41:4459-4469.
49. Nagy A., Kénesi E., Rentsendorj O., Molnár A., Szénási T., Sinkó I., Zvara A., Oommen S.T., Barta E., Puskás L.G., et al. Evolutionarily conserved, growth plate zone-specific regulation of the matrilin-1 promoter: L-Sox5/Sox6 and Nfi factors bound near TATA finely tune activation by Sox9. Mol. Cell. Biol. 2011, 31:686-699.
50. Nakashima K., Zhou X., Kunkel G., Zhang Z., Deng J.M., Behringer R.R., de Crombrugghe B. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 2002, 108:17-29.
51. Nifuji A., Miura N., Kato N., Kellermann O., Noda M. Bone morphogenetic protein regulation of forkhead/winged helix transcription factor Foxc2 (Mfh1) in a murine mesodermal cell line C1 and in skeletal precursor cells. J. Bone Miner. Res. 2001, 16:1765-1771.
52. Odom D.T., Zizlsperger N., Gordon D.B., Bell G.W., Rinaldi N.J., Murray H.L., Volkert T.L., Schreiber J., Rolfe P.A., Gifford D.K., et al. Control of pancreas and liver gene expression by HNF transcription factors. Science 2004, 303:1378-1381.
53. Oh C.D., Maity S.N., Lu J.F., Zhang J., Liang S., Coustry F., de Crombrugghe B., Yasuda H. Identification of SOX9 interaction sites in the genome of chondrocytes. PLoS ONE 2010, 5:e10113.
54. Oh C.D., Lu Y., Liang S., Mori-Akiyama Y., Chen D., de Crombrugghe B., Yasuda H. SOX9 regulates multiple genes in chondrocytes, including genes encoding ECM proteins, ECM modification enzymes, receptors, and transporters. PLoS ONE 2014, 9:e107577.
55. Olsen B.R., Reginato A.M., Wang W. Bone development. Annu. Rev. Cell Dev. Biol. 2000, 16:191-220.
56. Rada-Iglesias A., Bajpai R., Swigut T., Brugmann S.A., Flynn R.A., Wysocka J. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 2011, 470:279-283.
57. Rentsendorj O., Nagy A., Sinkó 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, 389:705-716.
58. Rodova M., Lu Q., Li Y., Woodbury B.G., Crist J.D., Gardner B.M., Yost J.G., Zhong X.B., Anderson H.C., Wang J. Nfat1 regulates adult articular chondrocyte function through its age-dependent expression mediated by epigenetic histone methylation. J. Bone Miner. Res. 2011, 26:1974-1986.
59. Rosenbloom K.R., Dreszer T.R., Pheasant M., Barber G.P., Meyer L.R., Pohl A., Raney B.J., Wang T., Hinrichs A.S., Zweig A.S., et al. ENCODE whole-genome data in the UCSC Genome Browser. Nucleic Acids Res. 2010, 38:D620-D625.
60. Schafer A.J., Foster J.W., Kwok C., Weller P.A., Guioli S., Goodfellow P.N. Campomelic dysplasia with XY sex reversal: diverse phenotypes resulting from mutations in a single gene. Ann. N Y Acad. Sci. 1996, 785:137-149.
61. Sekido R., Lovell-Badge R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 2008, 453:930-934.
62. Sock E., Pagon R.A., Keymolen K., Lissens W., Wegner M., Scherer G. Loss of DNA-dependent dimerization of the transcription factor SOX9 as a cause for campomelic dysplasia. Hum. Mol. Genet. 2003, 12:1439-1447.
63. Tang Q., Chen Y., Meyer C., Geistlinger T., Lupien M., Wang Q., Liu T., Zhang Y., Brown M., Liu X.S. A comprehensive view of nuclear receptor cancer cistromes. Cancer Res. 2011, 71:6940-6947.
64. Tsuda M., Takahashi S., Takahashi Y., Asahara H. Transcriptional co-activators CREB-binding protein and p300 regulate chondrocyte-specific gene expression via association with Sox9. J. Biol. Chem. 2003, 278:27224-27229.
65. Visel A., Blow M.J., Li Z., Zhang T., Akiyama J.A., Holt A., Plajzer-Frick I., Shoukry M., Wright C., Chen F., et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858.
66. Vokes S.A., Ji H., McCuine S., Tenzen T., Giles S., Zhong S., Longabaugh W.J.R., Davidson E.H., Wong W.H., McMahon A.P. Genomic characterization of Gli-activator targets in sonic hedgehog-mediated neural patterning. Development 2007, 134:1977-1989.
67. Wagner T., Wirth J., Meyer J., Zabel B., Held M., Zimmer J., Pasantes J., Bricarelli F.D., Keutel J., Hustert E., et al. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 1994, 79:1111-1120.
68. Wainwright E.N., Jorgensen J.S., Kim Y., Truong V., Bagheri-Fam S., Davidson T., Svingen T., Fernandez-Valverde S.L., McClelland K.S., Taft R.J., et al. SOX9 regulates microRNA miR-202-5p/3p expression during mouse testis differentiation. Biol. Reprod. 2013, 89:34.
69. Wang J., Gardner B.M., Lu Q., Rodova M., Woodbury B.G., Yost J.G., Roby K.F., Pinson D.M., Tawfik O., Anderson H.C. Transcription factor Nfat1 deficiency causes osteoarthritis through dysfunction of adult articular chondrocytes. J. Pathol. 2009, 219:163-172.
70. Whyte W.A., Orlando D.A., Hnisz D., Abraham B.J., Lin C.Y., Kagey M.H., Rahl P.B., Lee T.I., Young R.A. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 2013, 153:307-319.
71. Wright E., Hargrave M.R., Christiansen J., Cooper L., Kun J., Evans T., Gangadharan U., Greenfield A., Koopman P. The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos. Nat. Genet. 1995, 9:15-20.
72. Yoshida C.A., Yamamoto H., Fujita T., Furuichi T., Ito K., Inoue K., Yamana K., Zanma A., Takada K., Ito Y., Komori T. Runx2 and Runx3 are essential for chondrocyte maturation, and Runx2 regulates limb growth through induction of Indian hedgehog. Genes Dev. 2004, 18:952-963.
73. Yueh Y.G., Gardner D.P., Kappen C. Evidence for regulation of cartilage differentiation by the homeobox gene Hoxc-8. Proc. Natl. Acad. Sci. USA 1998, 95:9956-9961.
74. Zentner G.E., Tesar P.J., Scacheri P.C. Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res. 2011, 21:1273-1283.
75. Zhang P., Jimenez S.A., Stokes D.G. Regulation of human COL9A1 gene expression. Activation of the proximal promoter region by SOX9. J. Biol. Chem. 2003, 278:117-123.
76. Zhou G., Lefebvre V., Zhang Z., Eberspaecher H., de Crombrugghe B. 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. 1998, 273:14989-14997.
77. Zhou V.W., Goren A., Bernstein B.E. Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet. 2011, 12:7-18.