Transient upregulation of CBFA1 in response to bone morphogenetic protein-2 and transforming growth factor β1 in C2C12 myogenic cells coincides with suppression of the myogenic phenotype but is not sufficient for osteoblast differentiation

Journal of Cellular Biochemistry

Volumn 73, Issue 1, 1999, Pages 114-125

  Lee, Mi Hye ^a   Javed, Amjad ^c   Kim, Hyun Jung ^a   Shin, Hong In ^a   Gutierrez, Soraya ^c   Choi, Je Yong ^c   Rosen, Vicky ^b   Stein, Janet L ^c   Van Wijnen, André J ^c   Stein, Gary S ^c   Lian, Jane B ^c   Ryoo, Hyun Mo ^a  

^a Kyungpook National University   (South Korea)

^b PFIZER INC   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Cbfa1; Msx 2; Osteocalcin promoter; Osteogenic commitment

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; COLLAGEN TYPE 1; HOMEODOMAIN PROTEIN; OSTEOCALCIN; OSTEOPONTIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; GENE EXPRESSION; GENETIC TRANSFECTION; MOUSE; MYOTUBE; NONHUMAN; OSSIFICATION; OSTEOBLAST; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION;

ANIMALS; BASE SEQUENCE; BIOLOGICAL MARKERS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL LINE; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DNA PRIMERS; ENHANCER ELEMENTS (GENETICS); GENES, REGULATOR; HUMANS; MICE; MUSCLES; NEOPLASM PROTEINS; OSTEOBLASTS; OSTEOCALCIN; PHENOTYPE; PROMOTER REGIONS (GENETICS); RECOMBINANT PROTEINS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA;

EID: 0033120916     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4644(19990401)73:1<114::AID-JCB13>3.0.CO;2-M     Document Type: Article

References (58)

1. Aronson BD, Fisher AL, Blechman K, Caudy M, Gergen JP. 1997. Groucho-dependent and -independent repression activities of Runt domain proteins. Mol Cell Biol 17:5581-5587.
2. Aslam F, Shalhoub V, van Wijnen AJ, Banerjee C, Bortell R, Shakoori AR, Litwack G, Stein JL, Stein GS, Lian JB. 1995. Contributions of distal and proximal promoter elements to glucocorticoid regulation of osteocalcin gene transcription. Mol Endocrinol 9:679-690.
3. Banerjee C, Hiebert SW, Stein JL, Lian JB, Stein GS. 1996. An AML-1 consensus sequence binds an osteoblast-specific complex and transcriptionally activates the osteocalcin gene. Proc Natl Acad Sci USA 93:4968-4973.
4. Banerjee C, McCabe LR, Choi J-Y, Hiebert SW, Stein JL, Stein GS, Lian JB. 1997. Runt homology domain proteins in osteoblast differentiation: AML-3/CBFA1 is a major component of a bone specific complex. J Cell Biochem 66:1-8.
5. Catron KM, Wang H, Hu G, Shen MM, Abate-Shen C. 1996. Comparison of MSX-1 and MSX-2 suggests a molecular basis for functional redundancy. Mech Dev 55:185-199.
6. Celeste AJ, Ross JL, Yamaji N, Wozney JM. 1995. The molecular cloning of human bone morphogenetic proteins-10, -11, and -12, three new members of the transforming growth factor-β superfamily. J Bone Miner Res 10:S336.
7. Centrella M, Horowitz MC, Wozney JM, McCarthy TL. 1994. Transforming growth factor-β gene family members and bone. Endocr Rev 15:27-39.
8. Chen X, Rubock MJ, Whitman M. 1996. A transcriptional partner for MAD proteins in TGF-beta signalling. Nature 383:691-696.
9. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
10. Chu ML, Myers JC, Bernard MP, Ding JF, Ramirez F. 1982. Cloning and characterization of five overlapping cDNAs specific for the human pro alpha 1(I) collagen chain. Nucleic Acids Res 10:5925-5934.
11. Dube JL, Celeste AJ. 1995. Human bone morphogenetic protein-13, a molecule which is highly related to human bone morphogenetic-12. J Bone Miner Res 10:S336.
12. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. 1997. Osf2/Cbfa1: A transcriptional activator of osteoblast differentiation. Cell 89:747-754.
13. Erlebacher A, Filvaroff EH, Gitelman SE, Derynck R. 1995. Toward a molecular understanding of skeletal development. Cell 80:371-378.
14. Feinberg AP, Vogelstein B. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to a high specific activity. Anal Biochem 132:6-13.
15. Ferrari D, Sumoy L, Gannon J, Sun H, Brown AM, Upholt WB, Kosher RA. 1995. The expression pattern of the Distal-less homeobox-containing gene Dlx-5 in the developing chick limb bud suggests its involvement in apical ectodermal ridge activity, pattern formation, and cartilage differentiation. Mech Dev 52:257-264.
16. Frenkel B, Montecino M, Green J, Aslam F, Desai R, Banerjee C, Stein JL, Lian JB, Stein GS. 1996. Basal and vitamin D-responsive activity of the rat osteocalcin promoter in stably transfected osteosarcoma cells: Requirement of upstream sequences for control by the proximal regulatory domain. Endocrinology 137:1080-1088.
17. Goto K, Heymont JL, Klein-Nulend J, Kronenberg HM, Demay MB. 1996. Identification of an osteoblastic silencer element in the first intron of the rat osteocalcin gene. Biochemistry 35:11005-11011.
18. Heldin CH. 1997. Simultaneous induction of stimulatory and inhibitory signals by PDGF. FEBS Lett 410:17-21.
19. Hoffmann HM, Catron KM, van Wijnen AJ, McCabe LR, Lian JB, Stein GS, Stein JL. 1994. Transcriptional control of the tissue-specific, developmentally regulated osteocalcin gene requires a binding motif for the Msx family of homeodomain proteins. Proc Natl Acad Sci USA 91:12887-12891.
20. Hoffmann HM, Beumer TL, Rahman S, McCabe LR, Banerjee C, Aslam F, Tiro JA, van Wijnen AJ, Stein JL, Stein GS, Lian JB. 1996. Bone tissue-specific transcription of the osteocalcin gene: Role of an activator osteoblast-specific complex and suppressor hox proteins that bind the OC box. J Cell Biochem 61:310-324.
21. Hogan BL. 1996. Bone morphogenetic proteins: Multifunctional regulators of vertebrate development. Genes Dev 10:1580-1594.
22. Hu PP, Datto MB, Wang XF. 1998. Molecular mechanisms of transforming growth factor-beta signalling. Endocr Rev 19:349-363.
23. Ji C, Casinghino S, Chang DJ, Chen Y, Javed A, Ito Y, Hiebert SW, Lian JB, Stein GS, McCarthy TL, Centrella M. 1998. CBFa(AML/PEBP2)-related elements in the TGF-beta type I receptor promoter and expression with osteoblast differentiation. J Cell Biochem 69:353-363.
24. Katagiri T, Yamaguchi A, Ikeda T, Yoshiki S, Wozney JM, Rosen V, Wang EA, Tanaka H, Omura S, Suda T. 1990. The non-osteogenic mouse pluripotent cell line, C3H10T1/2, is induced to differentiate into osteoblastic cells by recombinant human bone morphogenetic protein-2. Biochem Biophys Res Commun 172:295-299.
25. Katagiri T, Yamaguchi A, Komaki M, Abe E, Takahashi N, Ikeda T, Rosen V, Wozney JM, Fujisawa-Sehara A, Suda T. 1994. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J Cell Biol 127:1755-1766.
26. Katagiri T, Akiyama S, Namiki M, Komaki M, Yamaguchi A, Rosen V, Wozney JM, Fujisawa-Sehara A, Suda T. 1997. Bone morphogenetic protein-2 inhibits terminal differentiation of myogenic cells by suppressing the transcriptional activity of MyoD and myogenin. Exp Cell Res 230:342-351.
27. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao Y-H, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755-764.
28. Kornblihtt AR, Vibe-Pedersen K, Baralle FE. 1983. Isolation and characterization of cDNA clones for human and bovine fibronectins. Proc Natl Acad Sci USA 80:3218-3222.
29. Kretzschmar M, Doody J, Massague J. 1997a. Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1. Nature 389:618-622.
30. Kretzschmar M, Liu F, Hata A, Doody J, Massague J. 1997b. The TGF-beta family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev 11:984-995.
31. Lagna G, Hata A, Hemmati-Brivanlou A, Massague J. 1996. Partnership between DPC4 and SMAD proteins in TGF-beta signalling pathways. Nature 383:832-836.
32. Lian J, Stewart C, Puchacz E, Mackowiak S, Shalhoub V, Collart D, Zambetti G, Stein G. 1989. Structure of the rat osteocalcin gene and regulation of vitamin D-dependent expression. Proc Natl Acad Sci USA 86:1143-1147.
33. Liu F, Hata A, Baker JC, Doody J, Carcamo J, Harland RM, Massague J. 1996. A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381: 620-623.
34. Luo G, D'Souza R, Hogue D, Karsenty G. 1995. The matrix Gla protein gene is a marker of the chondrogenesis cell lineage during mouse development. J Bone Miner Res 10:325-334.
35. Merriman HL, van Wijnen AJ, Hiebert S, Bidwell JP, Fey E, Lian J, Stein J, Stein GS. 1995. The tissue-specific nuclear matrix protein, NMP-2, is a member of the AML/CBF/ PEBP2/runt domain transcription factor family: Interactions with the osteocalcin gene promoter. Biochemistry 34:13125-13132.
36. Mundlos S, Otto F, Mundlos C, Mulliken JB, Aylsworth AS, Albright S, Lindhout D, Cole WG, Henn W, Knoll JHM, Owen MJ, Mertelsmann R, Zabel BU, Olsen BR. 1997. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89:773-779.
37. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, Tamaki K, Hanai J, Heldin CH, Miyazono K, ten Dijke P. 1997. TGFβ receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J 16:5353-5362.
38. Namiki M, Akiyama S, Katagiri T, Suzuki A, Ueno N, Yamaji N, Rosen V, Wozney JM, Suda T. 1997. A kinase domain-truncated type I receptor blocks bone morphogenetic protein-2-induced signal transduction in C2C12 myoblasts. J Biol Chem 272:22046-22052.
39. Nishimura R, Kato Y, Chen D, Harris SE, Mundy GR, Yoneda T. 1998. Smad5 and DPC4 are key molecules in mediating BMP-2-induced osteoblastic differentiation of the pluripotent mesenchymal precursor cell line C2C12. J Biol Chem 273:1872-1879.
40. Noda M, Rodan GA. 1986. Type-beta transforming growth factor inhibits proliferation and expression of alkaline phosphatase in murine osteoblast-like cells. Biochem Biophys Res Commun 140:56-65.
41. Ogawa E, Inuzuka M, Maruyama M, Satake M, Naito-Fujimoto M, Ito Y, Shigesada K. 1993a. Molecular cloning and characterization of PEBP2β, the heterodimeric partner of a novel Drosophila runt-related DNA binding protein PEBP2α. Virology 194:314-331.
42. Ogawa E, Maruyama M, Kagoshima H, Inuzuka M, Lu J, Satake M, Shigesada K, Ito Y. 1993b. 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 USA 90:6859-6863.
43. Oldberg A, Franze A, Heinegard D. 1986. Cloning and sequence analysis of rat bone scialoprotein (osteopontin) cDNA reveals an Arg-Gly-Asp cell-binding sequence. Proc Natl Acad Sci USA 83:8819-8823.
44. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, Stamp GWH, Beddington RSP, Mundlos S, Olsen BR, Selby PB, Owen MJ. 1997. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89:765-771.
45. Ryoo H-M, Hoffmann HM, Beumer TL, Frenkel B, Towler DA, Stein GS, Stein JL, van Wijnen AJ, Lian JB. 1997. Stage-specific expression of Dlx-5 during osteoblast differentiation: Involvement in regulation of osteocalcin gene expression. Mol Endocrinol 11:1681-1694.
46. Sampath TK, Maliakal JC, Hauschka PV, Jones WK, Sasak H, Tucker RF, White KH, Coughlin JE, Tucker MM, Pang RH. 1992. Recombinant human osteogenic protein-1 (hOP-1) induces new bone formation in vivo with a specific activity comparable with natural bovine osteogenic protein and stimulates osteoblast proliferation and differentiation in vitro. J Biol Chem 267:20352-20362.
47. Schmidt CJ, Sladek TE. 1993. A rat homolog of the Drosophila enhancer of split (groucho) locus lacking WD-40 repeats. J Biol Chem 268:25681-25686.
48. Stewart M, Terry A, Hu M, O'Hara M, Blyth K, Baxter E, Cameron E, Onions DE, Neil JC. 1997. Proviral insertions induce the expression of bone-specific isoforms of PEBP2alphaA (CBFA1): Evidence for a new myc collaborating oncogene. Proc Natl Acad Sci USA 94:8646-8651.
49. Stifani S, Blaumueller CM, Redhead NJ, Hill RE, Artavanis-Tsakonas S. 1992. Human homologs of a Drosophila Enhancer of split gene product define a novel family of nuclear proteins. Nat Genet 2:119-127.
50. Thies RS, Bauduy M, Ashton BA, Kurtzberg L, Wozney JM, Rosen V. 1992. Recombinant human bone morphogenetic protein-2 induces osteoblastic differentiation in W-20-17 stromal cells. Endocrinology 130:1318-1324.
51. Thirunavukkarasu K, Mahajan M, McLarren KW, Stifani S, Karsenty G. 1998. Two domains unique to osteoblast-specific transcription factor Osf2/Cbfa1 contribute to its transactivation function and its inability to heterodimerize with Cbf beta. Mol Cell Biol 18:4197-4208.
52. Towler DA, Rutledge SJ, Rodan GA. 1994. Msx-2/Hox 8.1: A transcriptional regulator of the rat osteocalcin promoter. Mol Endocrinol 8:1484-1493.
53. Tsuji K, Ito Y, Noda M. 1998. Expression of the PEBP2αA/ AML3/CBFA1 gene is regulated by BMP4/7 heterodimer and its overexpression suppresses type I collagen and osteocalcin gene expression in osteoblastic and nonosteoblastic mesenchymal cells. Bone 22:87-92.
54. Urist MR. 1965. Bone: Formation by autoinduction. Science 150:893-899.
55. Wang EA, Rosen V, D'Alessandro JS, Bauduy M, Cordes P, Harada T, Israel DI, Hewick RM, Kerns KM, LaPan P, Luxenberg DP, McQuaid D, Moutsatsos IK, Nove J, Wozney JM. 1990. Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci USA 87:2220-2224.
56. Yamaguchi A, Katagiri T, Ikeda T, Wozney J, Rosen V, Wang E, Kahn A, Suda T, Yoshiki S. 1991. Recombinant human bone morphogenetic protein-2 stimulates osteoblastic maturation and inhibits myogenic differentiation in vitro. J Cell Biol 113:681-687.
57. Yamamoto N, Akiyama S, Katagiri T, Namiki M, Kurokawa T, Suda T. 1997. Smad1 and smad5 act downstream of intracellular signallings of BMP-2 that inhibits myogenic differentiation and induces osteoblast differentiation in C2C12 myoblasts. Biochem Biophys Res Commun 238: 574-580.
58. Zhang H, Hu G, Wang H, Sciavolino P, Iler N, Shen MM, Abate-Shen C. 1997. Heterodimerization of Msx and Dlx homeoproteins results in functional antagonism. Mol Cell Biol 17:2920-2932.