Histone acetylation influences the activity of Sox9-related transcriptional complex

Acta Medica Okayama

Volumn 64, Issue 6, 2010, Pages 351-357

  Furumatsua, Takayuki ^a   Asahara, Hiroshi ^b  

^a OKAYAMA UNIVERSITY   (Japan)

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

Author keywords

Chondrogenesis; Coactivator p300; Scleraxis E47; Sox9; TGF Smad3

Indexed keywords

HISTONE; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA;

ACETYLATION; ANIMAL; CHONDROGENESIS; EPIGENETICS; HUMAN; METABOLISM; PHYSIOLOGY; REVIEW;

ACETYLATION; ANIMALS; CHONDROGENESIS; EPIGENOMICS; HISTONES; HUMANS; SOX9 TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA;

EID: 78650715737     PISSN: 0386300X     EISSN: 0386300X     Source Type: Journal    
DOI: None     Document Type: Review

References (70)

1. Akiyama H, Chaboissier MC, Martin JF, 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 (2002) 16: 2813-2828.
2. Strieker S, Fundele R, Vortkamp A and Mundlos S. Role of Runx genes in chondrocyte differentiation. Dev Biol (2002) 245: 95-108.
3. Shi Y and Massague J. Mechanisms of TGF-/3 signaling from cell membrane to the nucleus. Cell (2003) 113: 685-700.
4. Furumatsu T, Shukunami C, Amemiya-Kudo M, Shimano H and Ozaki T. Scleraxis and E47 cooperatively regulate the Sox9-dependent transcription. Int J Biochem Cell Biol (2010) 42: 148-156.
5. Kamachi Y, Uchikawa M and Kondoh H. Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet (2000) 16: 182-187.
6. Bernard P and Harley VR. Acquisition of SOX transcription factor specificity through protein-protein interaction, modulation of Wnt signalling and post-translational modification. Int J Biochem Cell Biol (2010)42: 400-410.
7. Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, Sham MH, Koopman P, Tam PP and Cheah KS. SOX9 directly regulates the type-ll collagen gene. Nat Genet (1997) 16: 174-178.
8. Bridgewater LC, Lefebvre V and de Crombrugghe B. Chondrocyte-specific enhancer elements in the Col11a2 gene resemble the Col2a1 tissue-specific enhancer. J Biol Chem (1998) 273: 14998-15006.
9. Xie WF, Zhang X, Sakano S, Lefebvre V and Sandell LJ. Transactivation of the mouse cartilage-derived retinoic acid-sensitive protein gene by Sox9. J Bone Miner Res (1999) 14: 757-763.
10. 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 (2000) 275: 10738-10744.
11. Zhang P, Jimenez SA and Stokes DG. Regulation of human COL9A1 gene expression. Activation of the proximal promoter region by SOX9. J Biol Chem (2003) 278: 117-123.
12. Kou I and Ikegawa S. SOX9-dependent and -independent transcriptional regulation of human cartilage link protein. J Biol Chem (2004) 279: 50942-50948.
13. Liu CJ, Zhang Y, Xu K, Parsons D, Alfonso D and Di Cesare PE. Transcriptional activation of cartilage oligomeric matrix protein by Sox9, Sox5, and Sox6 transcription factors and CBP/p300 coactivators. Front Biosci (2007) 12: 3899-3910.
14. Wagner T, Wirth J, Meyer J, Zabel B, Held M, Zimmer J, Pasantes J, Bricarelli FD, Keutel J, Hustert E, Wolf U, Tommerup N, Schempp W and Scherer G. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell (1994) 79: 1111-1120.
15. Bi W, Deng JM, Zhang Z, Behringer RR and de Crombrugghe B. Sox9 is required for cartilage formation. Nat Genet (1999) 22: 85-89.
16. Zhao Q, Eberspaecher H, Lefebvre V and de Crombrugghe B. Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev Dyn (1997) 209: 377-386.
17. Akiyama H, Lyons JP, Mori-Akiyama Y, Yang X, Zhang R, Zhang Z, Deng JM, Taketo MM, Nakamura T, Behringer RR, McCrea PD and de Crombrugghe B. Interactions between Sox9 and p -catenin control chondrocyte differentiation. Genes Dev (2004) 18: 1072-1087.
18. Akiyama H. Control of chondrogenesis by the transcription factor Sox9. Mod Rheumatol (2008) 18: 213-219.
19. Wegner M. All purpose Sox: The many roles of Sox proteins in gene expression. Int J Biochem Cell Biol (2010) 42: 381-390.
20. Huang W, Zhou X, Lefebvre V and de Crombrugghe B. Phosphorylation of SOX9 by cyclic AMP-dependent protein kinase A enhances SOX9's ability to transactivate a Col2a1 chondrocyte-specific enhancer. Mol Cell Biol (2000) 20: 4149-4158.
21. Oh HJ, Kido T and Lau YF. PIAS1 interacts with and represses SOX9 transactivation activity. Mol Reprod Dev (2007) 74: 1446-1455.
22. Akiyama H, Kamitani T, Yang X, Kandyil R, Bridgewater LC, Fellous M, Mori-Akiyama Y and de Crombrugghe B. 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: 499-505.
23. Ikeda T, Kawaguchi H, Kamekura S, Ogata N, Mori Y, Nakamura K, Ikegawa S and Chung Ul. Distinct roles of Sox5, Sox6, and Sox9 in different stages of chondrogenic differentiation. J Bone Miner Metab (2005) 23: 337-340.
24. Smits P, Li P, Mandel J, Zhang Z, Deng JM, Behringer RR, de Crombrugghe B and Lefebvre V. The transcription factors L-Sox5 and Sox6 are essential for cartilage formation. Dev Cell (2001) 1: 277-290.
25. Brent AE, Braun T and Tabin CJ. Genetic analysis of interactions between the somitic muscle, cartilage and tendon cell lineages during mouse development. Development (2005) 132: 515-528.
26. Hattori T, Coustry F, Stephens S, Eberspaecher H, Takigawa M, Yasuda H and de Crombrugghe B. Transcriptional regulation of chondrogenesis by coactivator Tip60 via chromatin association with Sox9 and Sox5. Nucleic Acids Res (2008) 36: 3011-3024.
27. Han Y and 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.
28. Liu F. Receptor-regulated Smads in TGF-/3 signaling. Front Biosci (2003)8: s1280-1303.
29. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S and Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science (1999) 284: 143-147.
30. Ferguson CM, Schwarz EM, Reynolds PR, Puzas JE, Rosier RN and O'Keefe RJ. Smad2 and 3 mediate transforming growth factor-β1-induced inhibition of chondrocyte maturation. Endocrinology (2000) 141: 4728-4735.
31. HanafusaH, Ninomiya-Tsuji J, Masuyama N, NishitaM, Fujisawa J, Shibuya H, Matsumoto K and Nishida E. Involvement of the p38 mitogen-activated protein kinase pathway in transforming growth factor-β-induced gene expression. J Biol Chem (1999) 274: 27161-27167.
32. Furumatsu T, Tsuda M, Taniguchi N, Tajima Y and Asahara H. Smad3 induces chondrogenesis through the activation of SOX9 via CREB-binding protein/p300 recruitment. J Biol Chem (2005) 280: 8343-8350.
33. Alliston T, Choy L, Ducy P, Karsenty G and Derynck R. TGF-β-induced repression of CBFA1 by Smad3 decreases cbfal and osteocalcin expression and inhibits osteoblast differentiation. EMBO J (2001)20: 2254-2272.
34. Liu D, Black BL and Derynck R. TGF-β inhibits muscle differentia tion through functional repression of myogenic transcription factors by Smad3. Genes Dev (2001) 15: 2950-2966.
35. Nishihara A, Hanai Jl, Okamoto N, Yanagisawa J, Kato S, Miyazono K and Kawabata M. Role of p300, a transcriptional coactivator, in signalling of TGF-β. Genes Cells (1998) 3: 613-623.
36. Murakami S, Kan M, McKeehan WL and de Crombrugghe B. Up-regulation of the chondrogenic Sox9 gene by fibroblast growth fac tors is mediated by the mitogen-activated protein kinase pathway. Proc Natl Acad Sci USA (2000) 97: 1113-1118.
37. Tuli R, Tuli S, Nandi S, Huang X, Manner PA, Hozack WJ, Danielson KG, Hall DJ and Tuan RS. Transforming growth factor-beta-mediated chondrogenesis of human mesenchymal progenitor cells involves N-cadherin and mitogen-activated protein kinase and Wnt signaling cross-talk. J Biol Chem (2003) 278: 41227-41236.
38. Stanton LA, Underhill TM and Beier F. MAP kinases in chondro cyte differentiation. Dev Biol (2003) 263: 165-175.
39. Watanabe H, de Caestecker MP and Yamada Y. Transcriptional cross-talk between Smad, ERK1/2, and p38 mitogen-activated protein kinase pathways regulates transforming growth factor-beta-induced aggrecan gene expression in chondrogenic ATDC5 cells. J Biol Chem (2001) 276: 14466-14473.
40. Quina AS, Buschbeck M and Di Croce L. Chromatin structure and epigenetics. Biochem Pharmacol (2006) 72: 1563-1569.
41. Strahl BD and All is CD. The language of covalent histone modifi cations. Nature (2000) 403: 41-45.
42. Jenuwein T and Allis CD. Translating the histone code. Science (2001) 293: 1074-1080.
43. Roth SY, Denu JM and Allis CD. Histone acetyltransferases. Annu Rev Biochem (2001) 70: 81-120.
44. Tavella S, Biticchi R, Schito A, Minina E, Di Martino D, Pagano A, Vortkamp A, Horton WA, Cancedda R and Garofalo S. Targeted expression of SHH affects chondrocyte differentiation, growth plate organization, and Sox9 expression. J Bone Miner Res (2004) 19: 1678-1688.
45. Piera-Velazquez S, Hawkins DF, Whitecavage MK, Colter DC, Stokes DG and Jimenez SA. Regulation of the human SOX9 pro moter by Sp1 and CREB. Exp Cell Res (2007) 313: 1069-1079.
46. Amarilio R, Viukov SV, Sharir A, Eshkar-Oren I, Johnson RS and Zelzer E. HIF1« regulation of Sox9 is necessary to maintain differ entiation of hypoxic prechondrogenic cells during early skeletogenesis. Development (2007) 134: 3917-3928.
47. Shakibaei M, Seifarth C, John T, Rahmanzadeh M and 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: 1382-1395.
48. Hanley KP, Oakley F, Sugden S, Wilson DI, Mann DA and Hanley NA. Ectopic SOX9 mediates extracellular matrix deposition characteristic of organ fibrosis. J Biol Chem (2008) 283: 14063-14071.
49. Murakamis, Lefebvre V and 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: 3687-3692.
50. Lorda-Diez Cl, Montero JA, Martinez-Cue C, Garcia-Porrero JA and Hurle JM. Transforming growth factors beta coordinate carti lage and tendon differentiation in the developing limb mesenchyme. J Biol Chem (2009) 284: 29988-29996.
51. Pan Q, Wu Y, Lin T, Yao H, Yang Z, Gao G, Song E and Shen H. Bone morphogenetic protein-2 induces chromatin remodeling and modification at the proximal promoter of Sox9 gene. Biochem Biophys Res Commun (2009) 379: 356-361.
52. Lincoln J, Lange AW and Yutzey KE. Hearts and bones: shared regulatory mechanisms in heart valve, cartilage, tendon, and bone development. Dev Biol (2006) 294: 292-302.
53. Furumatsu T, Hachioji M, Saiga K, Takata N, Yokoyama Y and Ozaki T. Anterior cruciate ligament-derived cells have high chon drogenic potential. Biochem Biophys Res Commun (2010) 391: 1142-1147.
54. Chan HM and La Thangue NB. p300/CBP proteins: HATs for transcriptional bridges and scaffolds. J Cell Sci (2001) 114: 2363-2373.
55. Tsuda M, Takahashi S, Takahashi Y and 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.
56. Furumatsu T, Tsuda M, Yoshida K, Taniguchi N, Ito T, Hashimoto M, Ito T and Asahara H. Sox9 and p300 cooperatively regulate chromatin-mediated transcription. J Biol Chem (2005) 280: 35203-35208.
57. Furumatsu T, Ozaki T and Asahara H. Smad3 activates the Sox9-dependent transcription on chromatin. Int J Biochem Cell Biol (2009)41: 1198-1204.
58. Zhou R, Bonneaud N, Yuan CX, de Santa Barbara P, Boizet B, SchomberT, Scherer G, Roeder RG, Poulat F and Berta P. SOX9 interacts with a component of the human thyroid hormone receptor-associated protein complex. Nucleic Acids Res (2002) 30: 3245-3252.
59. Kawakami Y, Tsuda M, Takahashi S, Taniguchi N, Rodriguez Esteban C, Zemmyo M, Furumatsu T, Lotz M, Izpisua Belmonte JC and Asahara H. Transcriptional coactivator Pgc-1α regulates chondrogenesis via association with Sox9. Proc Natl Acad Sci USA (2005) 102: 2414-2419.
60. Meech R, Edelman DB, Jones FS and Makarenkova HP. The homeobox transcription factor Barx2 regulates chondrogenesis dur ing limb development. Development (2005) 132: 2135-2146.
61. Furumatsu T. Sox9-dependent transcription in chondrogenesis. J Joint Surg (2008) 27: 146-147 (in Japanese).
62. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet (2002) 3: 662-673.
63. Jaenisch R and Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet (2003) 33: Suppl. 245-254.
64. Felsenfeld G and Groudine M. Controlling the double helix. Nature (2003) 421: 448-453.
65. Sterner DE and Berger SL. Acetylation of histones and transcrip tion-related factors. Microbiol Mol Biol Rev (2000) 64: 435-459.
66. Shahbazian MD and Grunstein M. Functions of site-specific his tone acetylation and deacetylation. Annu Rev Biochem (2007) 76: 75-100.
67. Furumatsu T and Ozaki T. Epigenetic regulation in chondrogene sis. Acta Med Okayama (2010) 64: 155-161.
68. Furumatsu T, Ozaki T and Asahara H. TGF-β-Smad3 pathway activates the Sox9-dependent chondrogenesis. Okayama Igakkai Zasshi (J Okayama Med Assoc) (2010) 122: 95-99 (in Japanese).
69. Furumatsu T. Sox9-related epigenetic regulation. Orthop Surg Trauma (2009) 52: 1040-1041 (in Japanese).
70. Bayly R, Chuen L, Currie RA, Hyndman BD, Casselman R, Blobel GA and LeBrun DP. E2A-PBX1 interacts directly with the KIX domain of CBP/p300 in the induction of proliferation in primary hematopoietic cells. J Biol Chem (2004) 279: 55362-55371.