Two of four alternatively spliced isoforms of RUNX2 control osteocalcin gene expression in human osteoblast cells

Gene

Volumn 413, Issue 1-2, 2008, Pages 8-17

  Makita, Naoyuki ^a   Suzuki, Mitsuhiro ^a   Asami, Shiori ^a   Takahata, Rintaroh ^a   Kohzaki, Daika ^a   Kobayashi, Sho ^a   Hakamazuka, Takashi ^b   Hozumi, Nobumichi ^a  

^a TOKYO UNIVERSITY OF SCIENCE   (Japan)

^b NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

Author keywords

Alternative splicing; Osteoblast; Osteocalcin; RUNX2; Transcriptional regulation

Indexed keywords

HISTONE ACETYLTRANSFERASE PCAF; HISTONE DEACETYLASE 3; ISOPROTEIN; OSTEOCALCIN; TRANSCRIPTION FACTOR RUNX2;

ALTERNATIVE RNA SPLICING; ARTICLE; CARTILAGE CELL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA BINDING; EXON; GENE EXPRESSION; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; OSTEOBLAST; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN VARIANT; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ALTERNATIVE SPLICING; BASE SEQUENCE; BINDING SITES; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL NUCLEUS; CELLS, CULTURED; CHONDROCYTES; CHONDROSARCOMA; CORE BINDING FACTOR ALPHA 1 SUBUNIT; CYTOSOL; DNA PRIMERS; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; HUMANS; MESENCHYMAL STEM CELLS; OSTEOBLASTS; OSTEOCALCIN; OSTEOSARCOMA; P300-CBP TRANSCRIPTION FACTORS; PROMOTER REGIONS (GENETICS); PROTEIN ISOFORMS; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFECTION;

EID: 41249084399     PISSN: 03781119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gene.2007.12.025     Document Type: Article

References (56)

1. Akiyama H., Kanno T., Ito H., Terry A., Neil J., Ito Y., and Nakamura T. Positive and negative regulation of chondrogenesis by splice variants of PEBP2alphaA/CBFalpha1 in clonal mouse EC cells, ATDC5. J. Cell Physiol. 181 (1999) 169-178
2. 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
3. Atsumi T., Miwa Y., Kimata K., and Ikawa Y. A chondrogenic cell line derived from a differentiating culture of AT805 teratocarcinoma cells. Cell Differ. Dev. 30 (1990) 109-116
4. Bangsow C., et al. The RUNX3 gene-sequence, structure and regulated expression. Gene 279 (2001) 221-232
5. Billiau A., et al. Human interferon: mass production in a newly established cell line, MG-63. Antimicrob. Agents Chemother. 12 (1977) 11-15
6. Choi J.Y., et al. Subnuclear targeting of Runx/Cbfa/AML factors is essential for tissue-specific differentiation during embryonic development. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 8650-8655
7. de Crombrugghe B., Lefebvre V., and Nakashima K. Regulatory mechanisms in the pathways of cartilage and bone formation. Curr. Opin. Cell Biol. 13 (2001) 721-727
8. Ducy P., Zhang R., Geoffroy V., Ridall A.L., and Karsenty G. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89 (1997) 747-754
9. Enomoto H., et al. Cbfa1 is a positive regulatory factor in chondrocyte maturation. J. Biol. Chem. 275 (2000) 8695-8702
10. Foster J.W., et al. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372 (1994) 525-530
11. Frendo J.L., Xiao G., Fuchs S., Franceschi R.T., Karsenty G., and Ducy P. Functional hierarchy between two OSE2 elements in the control of osteocalcin gene expression in vivo. J. Biol. Chem. 273 (1998) 30509-30516
12. Geoffroy V., Corral D.A., Zhou L., Lee B., and Karsenty G. Genomic organization, expression of the human CBFA1 gene, and evidence for an alternative splicing event affecting protein function. Mamm. Genome 9 (1998) 54-57
13. Harada H., et al. Cbfa1 isoforms exert functional differences in osteoblast differentiation. J. Biol. Chem. 274 (1999) 6972-6978
14. Hassan M.Q., et al. Dlx3 transcriptional regulation of osteoblast differentiation: temporal recruitment of Msx2, Dlx3, and Dlx5 homeodomain proteins to chromatin of the osteocalcin gene. Mol. Cell Biol. 24 (2004) 9248-9261
15. Javed A., et al. Multiple Cbfa/AML sites in the rat osteocalcin promoter are required for basal and vitamin D-responsive transcription and contribute to chromatin organization. Mol. Cell Biol. 19 (1999) 7491-7500
16. Javed A., et al. Groucho/TLE/R-esp proteins associate with the nuclear matrix and repress RUNX CBFa/AML/PRBP2a dependent activation of tissue-specific gene transcription. J. Cell Sci. 113 (2000) 2221-2231
17. Karsenty G. Genetics of skeletogenesis. Dev. Genet. 22 (1998) 301-313
18. Karsenty G., and Wagner E.F. Reaching a genetic and molecular understanding of skeletal development. Dev. Cell 2 (2002) 389-406
19. Komori T. Runx2, a multifunctional transcription factor in skeletal development. J. Cell Biochem. 87 (2002) 1-8
20. Komori T., et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89 (1997) 755-764
21. Lee B., et al. Missense mutations abolishing DNA binding of the osteoblast-specific transcription factor OSF2/CBFA1 in cleidocranial dysplasia. Nat. Genet. 16 (1997) 307-310
22. Lian J.B., et al. Contributions of nuclear architecture and chromatin to vitamin D-dependent transcriptional control of the rat osteocalcin gene. Steroids 66 (2001) 159-170
23. Miyoshi H., et al. Alternative splicing and genomic structure of the AML1 gene involved in acute myeloid leukemia. Nucleic Acids Res. 23 (1995) 2762-2769
24. Montecino M., Lian J., Stein G., and Stein J. Changes in chromatin structure support constitutive and developmentally regulated transcription of the bone-specific osteocalcin gene in osteoblastic cells. Biochemistry 35 (1996) 5093-5102
25. Mundlos S., et al. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89 (1997) 773-779
26. Nakashima K., and de Crombrugghe B. Transcriptional mechanisms in osteoblast differentiation and bone formation. Trends Genet. 19 (2003) 458-466
27. Ogawa E., et al. PEBP2/PEA2 represents a family of transcription factors homologous to the products of the Drosophila runt gene and the human AML1 gene. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 6859-6863
28. Ogawa S., Harada H., Fujiwara M., Tagashira S., Katsumata T., and Takada H. Cbfa1, an essential transcription factor for bone formation, is expressed in testis from the same promoter used in bone. DNA Res. 7 (2000) 181-185
29. Otto F., et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89 (1997) 765-771
30. Otto F., Lubbert M., and Stock M. Upstream and downstream targets of RUNX proteins. J. Cell. Biochem. 89 (2003) 9-18
31. Paredes R., et al. The Runx2 transcription factor plays a key role in the 1alpha,25-dihydroxy Vitamin D3-dependent upregulation of the rat osteocalcin (OC) gene expression in osteoblastic cells. J. Steroid. Biochem. Mol. Biol. 89-90 (2004) 269-271
32. Pittenger M.F., et al. Multilineage potential of adult human mesenchymal stem cells. Science 284 (1999) 143-147
33. Schroeder T.M., Kahler R.A., Li X., and Westendorf J.J. Histone deacetylase 3 interacts with runx2 to repress the osteocalcin promoter and regulate osteoblast differentiation. J. Biol. Chem. 279 (2004) 41998-42007
34. Shen R., et al. Smad6 interacts with Runx2 and mediates Smad ubiquitin regulatory factor1-induced Runx2 degradation. J. Biol. Chem. 281 (2006) 3569-3576
35. Shukunami C., Shigeno C., Atsumi T., Ishizeki K., Suzuki F., and Hiraki Y. Chondrogenic differentiation of clonal mouse embryonic cell line ATDC5 in vitro: differentiation-dependent gene expression of parathyroid hormone (PTH)/PTH-related peptide receptor. J. Cell Biol. 133 (1996) 457-468
36. Sierra J., et al. Regulation of the bone-specific osteocalcin gene by p300 requires Runx2/Cbfa1 and the vitamin D3 receptor but not p300 intrinsic histone acetyltransferase activity. Mol. Cell Biol. 23 (2003) 3339-3351
37. Spencer Jr. V.D. Role of covalent modifications of histones in regulating gene expression. Gene 240 (1999) 1-12
38. Stein G.S., et al. Runx2 control of organization, assembly and activity of the regulatory machinery for skeletal gene expression. Oncogene 23 (2004) 4315-4329
39. Stewart M., et al. Proviral insertions induce the expression of bone-specific isoforms of PEBP2alphaA (CBFA1): evidence for a new myc collaborating oncogene. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 8646-8651
40. Strahl B.D., and Allis C.D. The language of covalent histone modifications. Nature 403 (2000) 41-45
41. Sun L., Vitolo M.I., Qiao M., Anglin I.E., and Passaniti A. Regulation of TGFbeta1-mediated growth inhibition and apoptosis by RUNX2 isoforms in endothelial cells. Oncogene 23 (2004) 4722-4734
42. Suzuki M., et al. Site-specific DNA methylation by a complex of PU.1 and Dnmt3a/b. Oncogene 25 (2006) 2477-2488
43. Takeda Y., et al. Can the life span of human marrow stromal cells be prolonged by bmi-1, E6, E7, and/or telomerase without affecting cardiomyogenic differentiation?. J. Gene Med. 6 (2004) 833-845
44. Terry A., et al. Conservation and expression of an alternative 3′ exon of Runx2 encoding a novel proline-rich C-terminal domain. Gene 336 (2004) 115-125
45. Thirunavukkarasu K.M.M., McLarren K.W., Stifani S., and Karsenty G. Two domains unique to osteoblast-specific transcription factor Osf2/Cbfa1 contribute to its transactivation function and its inability to heterodimerize with Cbfbeta. Mol. Cell Biol. 7 (1998) 4192-4208
46. 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. 278 (2003) 27224-27229
47. Vega R.B., et al. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 119 (2004) 555-566
48. Villagra A., et al. Chromatin remodeling and transcriptional activity of the bone-specific osteocalcin gene require CCAAT/enhancer-binding protein beta-dependent recruitment of SWI/SNF activity. J. Biol. Chem. 281 (2006) 22695-22706
49. Wagner T., et al. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79 (1994) 1111-1120
50. Westendorf J.J. Transcriptional co-repressors of Runx2. J. Cell Biochem. 98 (2006) 54-64
51. Westendorf J.J., et al. Runx2 (Cbfa1, AML-3) interacts with histone deacetylase 6 and represses the p21 (CIP1/WAF1) promoter. Mol. Cell Biol. 22 (2002) 7982-7992
52. Xiao Z.S., Thomas R., Hinson T.K., and Quarles L.D. Genomic structure and isoform expression of the mouse, rat and human Cbfa1/Osf2 transcription factor. Gene 214 (1998) 187-197
53. Xiao Z.S., Hinson T.K., and Quarles L.D. Cbfa1 isoform overexpression upregulates osteocalcin gene expression in non-osteoblastic and pre-osteoblastic cells. J. Cell Biochem. 74 (1999) 596-605
54. Xiao Z.S., Liu S.G., Hinson T.K., and Quarles L.D. Characterization of the upstream mouse Cbfa1/Runx2 promoter. J. Cell Biochem. 82 (2001) 647-659
55. Yang X.O., Ax V.V., Nishikawa J., Howard B.H., and Nakatani Y. A p300/CBP-associated factor that competes with the adenoviral oncoprotein E1A. Nature 382 (1996) 319-324
56. Zhao M., Qiao M., Oyajobi B., Mundy G., and Chen D. E3 ubiquitin ligase Smurf1 mediates core-binding factor alpha1/Runx2 degradation and plays a specific role in osteoblast differentiation. J. Biol. Chem. 278 (2003) 27939-27944