SOX9 determines RUNX2 transactivity by directing intracellular degradation

Journal of Bone and Mineral Research

Volumn 25, Issue 12, 2010, Pages 2680-2689

  Cheng, Aixin ^a   Genever, Paul G ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Lysosome; Proteasome; Protein Degradation; RUNX2; SOX9

Indexed keywords

BETA CATENIN; PROTEASOME; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9; UBIQUITIN; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CELL NUCLEUS MATRIX; HUMAN; HUMAN CELL; LYSOSOME; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 77958108690     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1002/jbmr.174     Document Type: Article

References (55)

1. Wright E, Hargrave MR, Christiansen J, et al. The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos. Nat Genet. 1995; 9: 15-20.
2. Wheatley S, Wright E, Jeske Y, MCCormack A, et al. Aetiology of the skeletal dysmorphology syndrome campomelic dysplasia: expression of the Sox9 gene during chondrogenesis in mouse embryos. Ann NY Acad Sci. 1996; 785: 350-352.
3. Bell DM, Leung KK, Wheatley SC, et al. SOX9 directly regulates the type II collagen gene. Nat Genet. 1997; 16: 174-178.
4. Lefebvre V, Huang W, Harley VR, et al. SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro-alpha1(II) collagen gene. Mol Cell Biol. 1997; 17: 2336-2346.
5. Ng LJ, Wheatley S, Muscat GE, et al. SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev Biol. 1997; 183: 108-121.
6. Bi W, Deng JM, Zhang Z, et al. Sox9 is required for cartilage formation. Nat Genet. 1999; 22: 85-89.
7. Sekiya I, Tsuji K, Koopman P, et al. 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.
8. Sock E, Pagon RA, Keymolen K, et al. Loss of DNA-dependent dimerization of the transcription factor SOX9 as a cause for campomelic dysplasia. Hum Mol Genet. 2003; 12: 1439-1447.
9. Giordano J, Prior HM, Bamforth JS, et al. Genetic study of SOX9 in a case of campomelic dysplasia. Am J Med Genet. 2001; 98: 176-181.
10. Ducy P, Zhang R, Geoffroy V, et al. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell. 1997; 89: 747-754.
11. Stein GS, Lian JB, van Wijnen AJ, et al. Runx2 control of organization, assembly and activity of the regulatory machinery for skeletal gene expression. Oncogene. 2004; 23: 4315-4329.
12. Li X, Huang M, Zheng H, et al. CHIP promotes Runx2 degradation and negatively regulates osteoblast differentiation. J Cell Biol. 2008; 181: 959-972.
13. Lou Y, Javed A, Hussain S, et al. A Runx2 threshold for the cleidocranial dysplasia phenotype. Hum Mol Genet. 2009; 18: 556-568.
14. Xuan D, Li S, Zhang X, et al. A novel RUNX2 mutation in cleidocranial dysplasia patients. Biochem Genet. 2008; 46: 702-707.
15. Xuan D, Li S, Zhang X, et al. Mutations in the RUNX2 gene in Chinese patients with cleidocranial dysplasia. Ann Clin Lab Sci. 2008; 38: 15-24. (Pubitemid 351323720)
16. Yoshida T, Kanegane H, Osato M, et al. Functional analysis of RUNX2 mutations in cleidocranial dysplasia: novel insights into genotype-phenotype correlations. Blood Cells Mol Dis. 2003; 30: 184-193.
17. Ito Y, Zhang YW., A RUNX2/PEBP2alphaA/CBFA1 mutation in cleidocranial dysplasia revealing the link between the gene and Smad. J Bone Miner Metab. 2001; 19: 188-194.
18. Zhang YW, Yasui N, Ito K, et al. A RUNX2/PEBP2alpha A/CBFA1 mutation displaying impaired transactivation and Smad interaction in cleidocranial dysplasia. Proc Natl Acad Sci U S A. 2000; 97: 10549-10554.
19. Morava E, Karteszi J, Weisenbach J, et al. Cleidocranial dysplasia with decreased bone density and biochemical findings of hypophosphatasia. Eur J Pediatr. 2002; 161: 619-622.
20. Komori T, Yagi H, Nomura S, 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.
21. Otto F, Thornell AP, Crompton T, et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell. 1997; 89: 765-771.
22. Shen R, Chen M, Wang YJ, et al. Smad6 interacts with Runx2 and mediates Smad ubiquitin regulatory factor 1-induced Runx2 degradation. J Biol Chem. 2006; 281: 3569-3576.
23. Shen R, Wang X, Drissi H, et al. Cyclin D1-cdk4 induce runx2 ubiquitination and degradation. J Biol Chem. 2006; 281: 16347-16353.
24. Bae SC, Lee YH., Phosphorylation, acetylation and ubiquitination: the molecular basis of RUNX regulation. Gene. 2006; 366: 58-66.
25. Zhao M, Qiao M, Oyajobi BO, et al. E3 ubiquitin ligase Smurf1 mediates core-binding factor alpha1/Runx2 degradation and plays a specific role in osteoblast differentiation. J Biol Chem. 2003; 278: 27939-27944.
26. Akiyama H, Kamitani T, Yang X, 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: 499-505.
27. Malki S, Nef S, Notarnicola C, et al. Prostaglandin D2 induces nuclear import of the sex-determining factor SOX9 via its cAMP-PKA phosphorylation. EMBO J. 2005; 24: 1798-1809.
28. Huang W, Zhou X, Lefebvre V, et al. 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.
29. Pan Q, Wu Y, Lin T, et al. Bone morphogenetic protein-2 induces chromatin remodeling and modification at the proximal promoter of Sox9 gene. Biochem Biophys Res Commun. 2009; 379: 356-361.
30. Liu S, Cheng H, Kwan W, et al. Histone deacetylase inhibitors induce growth arrest, apoptosis, and differentiation in clear cell sarcoma models. Mol Cancer Ther. 2008; 7: 1751-1761.
31. Smith N, Dong Y, Lian JB, et al. Overlapping expression of Runx1(Cbfa2) and Runx2(Cbfa1) transcription factors supports cooperative induction of skeletal development. J Cell Physiol. 2005; 203: 133-143.
32. Zhou G, Zheng Q, Engin F, et al. Dominance of SOX9 function over RUNX2 during skeletogenesis. Proc Natl Acad Sci U S A. 2006; 103: 19004-19009.
33. Enomoto H, Enomoto-Iwamoto M, Iwamoto M, et al. Cbfa1 is a positive regulatory factor in chondrocyte maturation. J Biol Chem. 2000; 275: 8695-8702.
34. Wang Y, Belflower RM, Dong YF, et al. Runx1/AML1/Cbfa2 mediates onset of mesenchymal cell differentiation toward chondrogenesis. J Bone Miner Res. 2005; 20: 1624-1636.
35. Dong YF, Soung do, Schwarz Y, et al. Wnt induction of chondrocyte hypertrophy through the Runx2 transcription factor. J Cell Physiol. 2006; 208: 77-86.
36. Blache P, van de Wetering M, Duluc I, et al. SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes. J Cell Biol. 2004; 166: 37-47.
37. Zheng L, Iohara K, Ishikawa M, et al. Runx3 negatively regulates Osterix expression in dental pulp cells. Biochem J. 2007; 405: 69-75.
38. Muramatsu S, Wakabayashi M, Ohno T, et al. Functional gene screening system identified TRPV4 as a regulator of chondrogenic differentiation. J Biol Chem. 2007; 282: 32158-32167.
39. Woods A, Wang G, Beier F., RhoA/ROCK signaling regulates Sox9 expression and actin organization during chondrogenesis. J Biol Chem. 2005; 280: 11626-11634.
40. Guimont P, Grondin F, Dubois CM., Sox9-dependent transcriptional regulation of the proprotein convertase furin. Am J Physiol Cell Physiol. 2007; 293: C172-83.
41. Tintut Y, Parhami F, Le V, et al. Inhibition of osteoblast-specific transcription factor Cbfa1 by the cAMP pathway in osteoblastic cells. Ubiquitin/proteasome-dependent regulation. J Biol Chem. 1999; 274: 28875-28879.
42. Lee DH, Goldberg AL., Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 1998; 8: 397-403.
43. Stelter P, Ulrich HD., Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature. 2003; 425: 188-191.
44. Xue Y, Zhou F, Fu C, et al. SUMOsp: a web server for sumoylation site prediction. Nucleic Acids Res 34(Web Server issue). 2006; W254-7.
45. Tanaka RD, Li AC, Fogelman AM, et al. Inhibition of lysosomal protein degradation inhibits the basal degradation of 3-hydroxy-3-methylglutaryl coenzyme A reductase. J Lipid Res. 1986; 27: 261-273.
46. Aberle H, Bauer A, Stappert J, et al. beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 1997; 16: 3797-3804.
47. Akiyama H, Kim JE, Nakashima K, et al. Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc Natl Acad Sci U S A. 2005; 102: 14665-14670.
48. Wee HJ, Huang G, Shigesada K, et al. Serine phosphorylation of RUNX2 with novel potential functions as negative regulatory mechanisms. EMBO Rep. 2002; 3: 967-974.
49. Dai P, Akimaru H, Ishii S., A hedgehog-responsive region in the Drosophila wing disc is defined by debra-mediated ubiquitination and lysosomal degradation of Ci. Dev Cell. 2003; 4: 917-928.
50. Orford K, Crockett C, Jensen JP, et al. Serine phosphorylation-regulated ubiquitination and degradation of beta-catenin. J Biol Chem. 1997; 272: 24735-24738.
51. Hino S, Tanji C, Nakayama KI, et al. Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase stabilizes beta-catenin through inhibition of its ubiquitination. Mol Cell Biol. 2005; 25: 9063-9072.
52. Topol L, Chen W, Song H, et al. Sox9 inhibits Wnt signaling by promoting beta-catenin phosphorylation in the nucleus. J Biol Chem. 2009; 284: 3323-3333.
53. Akiyama H, Lyons JP, Mori-Akiyama Y, et al. Interactions between Sox9 and beta-catenin control chondrocyte differentiation. Genes Dev. 2004; 18: 1072-1087.
54. Jia L, Yu G, Zhang Y, et al. Lysosome-dependent degradation of Notch3. Int J Biochem Cell Biol. 2009; 41: 2594-2598.
55. Yamashita S, Andoh M, Ueno-Kudoh H, et al. Sox9 directly promotes Bapx1 gene expression to repress Runx2 in chondrocytes. Exp Cell Res. 2009; 315: 2231-2240.