Cell-type-dependent up-regulation of in vitro mineralization after overexpression of the osteoblast-specific transcription factor Runx2/Cbfa1

Journal of Bone and Mineral Research

Volumn 17, Issue 11, 2002, Pages 1931-1944

  Byers, Benjamin A ^a   Pavlath, Grace K ^b   Murphy, T J ^b   Karsenty, Gerard ^b   García, Andrés J ^b  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cbfa1; Mineralization; Osteoblast; Osteoblast specific gene; Runx2; Transcription factor

Indexed keywords

COMPLEMENTARY DNA; RETROVIRUS VECTOR; RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BONE MATRIX; BONE MINERALIZATION; CELL STRAIN 3T3; CELL TYPE; CONTROLLED STUDY; ENZYME ACTIVITY; FIBROBLAST CULTURE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; GENETIC TRANSDUCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; POLYMERASE CHAIN REACTION; VIRAL GENE DELIVERY SYSTEM;

NON-PROGRAMMATIC;

3T3 CELLS; ALKALINE PHOSPHATASE; ANIMALS; CALCIFICATION, PHYSIOLOGIC; CELLS, CULTURED; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DEXAMETHASONE; EXTRACELLULAR MATRIX; FIBROBLASTS; GENE EXPRESSION REGULATION; MICE; NEOPLASM PROTEINS; OSTEOBLASTS; RETROVIRIDAE; SIALOGLYCOPROTEINS; SKIN; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 0036830322     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/jbmr.2002.17.11.1931     Document Type: Article

References (69)

1. Aubin JE, Liu F 1996 The osteoblast lineage. In: Bilezikian JP, Raisz LG, Rodan GA (eds.) Principles of Bone Biology. Academic Press, New York, NY, USA, pp. 51-67.
2. Stein GS, Lian JB, Owen TA 1990 Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation. FASEB J 4:3111-3123.
3. Robey PG, Boskey A 1996 The biochemistry of bone. In: Marcus R, Feldman D, Kelsey JL (eds.) Osteoporosis. Academic Press, New York, NY, USA, pp. 95-182.
4. Moursi AM, Damsky CH, Lull J, Zimmerman D, Doty SB, Aota S, Globus RK 1996 Fibronectin regulates calvarial osteoblast differentiation. J Cell Sci 109:1369-1380.
5. Xiao G, Wang D, Benson MD, Karsenty G, Franceschi RT 1998 Role of the alpha2-integrin in osteoblast-specific gene expression and activation of the Osf2 transcription factor. J Biol Chem 273:32988-32994.
6. Lecanda F, Towler DA, Ziambaras K, Cheng SL, Koval M, Steinberg TH, Civitelli R 1998 Gap junctional communication modulates gene expression in osteoblastic cells. Mol Biol Cell 9:2249-2258.
7. Ogawa E, Maruyama M, Kagoshima H, Inuzuka M, Lu J, Satake M, Shigesada K, Ito Y 1993 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.
8. Levanon D, Negreanu V, Bernstein Y, Bar-Am I, Avivi L, Groner Y 1994 AML1, AML2, and AML3, the human members of the runt domain gene-family: cDNA structure, expression, and chromosomal localization. Genomics 23:425-432.
9. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G 1997 Osf2/Cbfa1: A transcriptional activator of osteoblast differentiation. Cell 89:747-754.
10. Ducy P, Karsenty G 1995 Two distinct osteoblast-specific cis-acting elements control expression of a mouse osteocalcin gene. Mol Cell Biol 15:1858-1869.
11. Geoffroy V, Ducy P, Karsenty G 1995 A PEBP2 alpha/AML1-related factor increases osteocalcin promoter activity through its binding to an osteoblast-specific cis-acting element. J Biol Chem 270:30973-30979.
12. 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.
13. Gergen JP, Wieschaus EF 1985 The localized requirements for a gene affecting segmentation in Drosophila: Analysis of larvae mosaic for runt. Dev Biol 109:321-335.
14. Daga A, Tighe JE, Calabi F 1992 Leukaemia/Drosophila homology. Nature 356:484 (letter).
15. Kagoshima H, Shigesada K, Satake M, Ito Y, Miyoshi H, Ohki M, Pepling M, Gergen P 1993 The Runt domain identifies a new family of heteromeric transcriptional regulators. Trends Genet 9:338-341 (letter).
16. Miyoshi H, Shimizu K, Kozu T, Maseki N, Kaneko Y, Ohki M 1991 t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1. Proc Natl Acad Sci USA 88:10431-10434.
17. Wang SW, Speck NA 1992 Purification of core-binding factor, a protein that binds the conserved core site in murine leukemia virus enhancers. Mol Cell Biol 12:89-102.
18. Bae SC, Yamaguchi-Iwai Y, Ogawa E, Maruyama M, Inuzuka M, Kagoshima H, Shigesada K, Satake M, Ito Y 1993 Isolation of PEBP2 alpha B cDNA representing the mouse homolog of human acute myeloid leukemia gene, AML1. Oncogene 8:809-814.
19. Bae SC, Takahashi E, Zhang YW, Ogawa E, Shigesada K, Namba Y, Satake M, Ito Y 1995 Cloning, mapping and expression of PEBP2 alpha C, a third gene encoding the mammalian Runt domain. Gene 159:245-248.
20. Wijmenga C, Speck NA, Dracopoli NC, Hofker MH, Liu P, Collins FS 1995 Identification of a new murine runt domain-containing gene. Cbfa3, and localization of the human homolog, CBFA3, to chromosome 1p35-pter. Genomics 26:611-614.
21. Meyers S, Lenny N, Hiebert SW 1995 The t(8;21) fusion protein interferes with AML-1B-dependent transcriptional activation. Mol Cell Biol 15:1974-1982.
22. Meyers S, Lenny N, Sun W, Hiebert SW 1996 AML-2 is a potential target for transcriptional regulation by the t(8;21) and t(12;21) fusion proteins in acute leukemia. Oncogene 13:303-312.
23. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, Stamp GW, Beddington RS, 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.
24. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, 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.
25. Mundlos S, Otto F, Mundlos C, Mulliken JB, Aylsworth AS, Albright S, Lindhout D, Cole WG, Henn W, Knoll JH, Owen MJ, Mertelsmann R, Zabel BU, Olsen BR 1997 Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89:773-779.
26. Kim IS, Otto F, Zabel B, Mundlos S 1999 Regulation of chondrocyte differentiation by Cbfa1. Mech Dev 80:159-170.
27. Inada M, Yasui T, Nomura S, Miyake S, Deguchi K, Himeno M, Sato M, Yamagiwa H, Kimura T, Yasui N, Ochi T, Endo N, Kitamura Y, Kishimoto T, Komori T 1999 Maturational disturbance of chondrocytes in Cbfa1-deficient mice. Dev Dyn 214:279-290.
28. Enomoto H, Enomoto-Iwamoto M, Iwamoto M, Nomura S, Himeno M, Kitamura Y, Kishimoto T, Komori T 2000 Cbfa1 is a positive regulatory factor in chondrocyte maturation. J Biol Chem 275:8695-8702.
29. Takeda S, Bonnamy JP, Owen MJ, Ducy P, Karsenty G 2001 Continuous expression of Cbfa1 in nonhypertrophic chondrocytes uncovers its ability to induce hypertrophic chondrocyte differentiation and partially rescues Cbfa1-deficient mice. Genes Dev 15:467-481.
30. Ueta C, Iwamoto M, Kanatani N, Yoshida C, Liu Y, Enomoto-Iwamoto M, Ohmori T, Enomoto H, Nakata K, Takada K, Kurisu K, Komori T 2001 Skeletal malformations caused by overexpression of Cbfa1 or its dominant negative form in chondrocytes. J Cell Biol 153:87-100.
31. Kern B, Shen J, Starbuck M, Karsenty G 2001 Cbfa1 contributes to the osteoblast-specific expression of type I collagen genes. J Biol Chem 276:7101-7107.
32. Benson MD, Aubin JE, Xiao G, Thomas PE, Franceschi RT 1999 Cloning of a 2.5 kb murine bone sialoprotein promoter fragment and functional analysis of putative Osf2 binding sites. J Bone Miner Res 14:396-405.
33. Sato M, Morii E, Komori T, Kawahata H, Sugimoto M, Terai K, Shimizu H, Yasui T, Ogihara H, Yasui N, Ochi T, Kitamura Y, Ito Y, Nomura S 1998 Transcriptional regulation of osteopontin gene in vivo by PEBP2alphaA/CBFA1 and ETS1 in the skeletal tissues. Oncogene 17:1517-1525.
34. Ducy P, Starbuck M, Priemel M, Shen J, Pinero G, Geoffroy V, Amling M, Karsenty G 1999 A Cbfa1-dependent genetic pathway controls bone formation beyond embryonic development. Genes Dev 13:1025-1036.
35. 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.
36. Sudo H, Kodama HA, Amagai Y, Yamamoto S, Kasai S 1983 In vitro differentiation and calcification in a new clonal osteogenic cell line derived from newborn mouse calvaria. J Cell Biol 96:191-198.
37. Abbott KL, Loss JR, Robida AM, Murphy TJ 2000 Evidence that Galpha(q)-coupled receptor-induced interleukin-6 mRNA in vascular smooth muscle cells involves the nuclear factor of activated T cells. Mol Pharmacol 58:946-953.
38. 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 Cbfbeta. Mol Cell Biol 18:4197-4208.
39. Pear WS, Nolan GP, Scott ML, Baltimore D 1993 Production of high-titer helper-free retroviruses by transient transfection. Proc Natl Acad Sci USA 90:8392-8396.
40. Abbott KL, Friday BB, Thaloor D, Murphy TJ, Pavlath GK 1998 Activation and cellular localization of the cyclosporine A-sensitive transcription factor NF-AT in skeletal muscle cells. Mol Biol Cell 9:2905-2916.
41. Kotani H, Newton PB III, Zhang S, Chiang YL, Otto E, Weaver L, Blaese RM, Anderson WF, McGarrity GJ 1994 Improved methods of retroviral vector transduction and production for gene therapy. Hum Gene Ther 5:19-28.
42. Springer ML, Blau HM 1997 High-efficiency retroviral infection of primary myoblasts. Somat Cell Mol Genet 23:203-209.
43. 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.
44. Lee MH, Javed A, Kim HJ, Shin HI, Gutierrez S, Choi JY, Rosen V, Stein JL, van Wijnen AJ, Stein GS, Lian JB, Ryoo HM 1999 Transient upregulation of CBFA1 in response to bone morphogenetic protein-2 and transforming growth factor beta1 in C2C12 myogenic cells coincides with suppression of the myogenic phenotype but is not sufficient for osteoblast differentiation. J Cell Biochem 73:114-125.
45. Bellows CG, Aubin JE, Heersche JN 1987 Physiological concentrations of glucocorticoids stimulate formation of bone nodules from isolated rat calvaria cells in vitro. Endocrinology 121:1985-1992.
46. Galipeau J, Li H, Paquin A, Sicilia F, Karpati G, Nalbantoglu J 1999 Vesicular stomatitis virus G pseudotyped retrovector mediates effective in vivo suicide gene delivery in experimental brain cancer. Cancer Res 59:2384-2394.
47. Tintut Y, Parhami F, Le V, Karsenty G, Demer LL 1999 Inhibition of osteoblast-specific transcription factor Cbfa1 by the cAMP pathway in osteoblastic cells. Ubiquitin/proteasome-dependent regulation. J Biol Chem 274:28875-28879.
48. Sodek J, Berkman FA 1987 Bone cell cultures. Methods Enzymol 145:303-324.
49. Boskey AL, Guidon P, Doty SB, Stiner D, Leboy P, Binderman I 1996 The mechanism of beta-glycerophosphate action in mineralizing chick limb-bud mesenchymal cell cultures. J Bone Miner Res 11:1694-1702.
50. Sokal RR, Rohlf FJ 1980 Assumptions of analysis of variance. In: Wilson C, Cotter (eds.) Biometry. W.H. Freeman & Co., New York, NY, USA, pp. 400-453.
51. Weinreb M, Shinar D, Rodan GA 1990 Different pattern of alkaline phosphatase, osteopontin, and osteocalcin expression in developing rat bone visualized by in situ hybridization. J Bone Miner Res 5:831-842.
52. Hauschka PV, Lian JB, Cole DE, Gundberg CM 1989 Osteocalcin and matrix Gla protein: Vitamin K-dependent proteins in bone. Physiol Rev 69:990-1047.
53. Harada H, Tagashira S, Fujiwara M, Ogawa S, Katsumata T, Yamaguchi A, Komori T, Nakatsuka M 1999 Cbfa1 isoforms exert functional differences in osteoblast differentiation. J Biol Chem 274:6972-6978.
54. Xiao ZS, Thomas R, Hinson TK, Quarles LD 1998 Genomic structure and isoform expression of the mouse, rat and human Cbfa1/Osf2 transcription factor. Gene 214:187-197.
55. Ogata T, Wozney JM, Benezra R, Noda M 1993 Bone morphogenetic protein 2 transiently enhances expression of a gene, Id (inhibitor of differentiation), encoding a helix-loop-helix molecule in osteoblast-like cells. Proc Natl Acad Sci USA 90:9219-9222.
56. Locklin RM, Riggs BL, Hicok KC, Horton HF, Byrne MC, Khosla S 2001 Assessment of gene regulation by bone morphogenetic protein 2 in human marrow stromal cells using gene array technology. J Bone Miner Res 16:2192-2204.
57. Bellows CG, Aubin JE, Heersche JN 1987 Physiological concentrations of glucocorticoids stimulate formation of bone nodules from isolated rat calvaria cells in vitro. Endocrinology 121:1985-1992.
58. Leboy PS, Beresford JN, Devlin C, Owen ME 1991 Dexamethasone induction of osteoblast mRNAs in rat marrow stromal cell cultures. J Cell Physiol 146:370-378.
59. Mendelsohn R, Hassankhani A, DiCarlo E, Boskey A 1989 FT-IR microscopy of endochondral ossification at 20 mu spatial resolution. Calcif Tissue Int 44:20-24.
60. Xiao ZS, Hinson TK, Quarles LD 1999 Cbfa1 isoform overexpression upregulates osteocalcin gene expression in non-osteoblastic and pre-osteoblastic cells. J Cell Biochem 74:596-605.
61. Marsh ME, Munne AM, Vogel JJ, Cui Y, Franceschi RT 1995 Mineralization of bone-like extracellular matrix in the absence of functional osteoblasts. J Bone Miner Res 10:1635-1643.
62. Choi JY, Lee BH, Song KB, Park RW, Kim IS, Sohn KY, Jo JS, Ryoo HM 1996 Expression patterns of bone-related proteins during osteoblastic differentiation in MC3T3-E1 cells. J Cell Biochem 61:609-618.
63. Hunter GK, Hauschka PV, Poole AR, Rosenberg LC, Goldberg HA 1996 Nucleation and inhibition of hydroxyapatite formation by mineralized tissue proteins. Biochem J 317:59-64.
64. Wennberg C, Hessle L, Lundberg P, Mauro S, Narisawa S, Lerner UH, Millan JL 2000 Functional characterization of osteoblasts and osteoclasts from alkaline phosphatase knockout mice. J Bone Miner Res 15:1879-1888.
65. Liu W, Toyosawa S, Furuichi T, Kanatani N, Yoshida C, Liu Y, Himeno M, Narai S, Yamaguchi A, Komori T 2001 Overexpression of Cbfa1 in osteoblasts inhibits osteoblast maturation and causes osteopenia with multiple fractures. J Cell Biol 155:157-166.
66. McLarren KW, Lo R, Grbavec D, Thirunavukkarasu K, Karsenty G, Stifani S 2000 The mammalian basic helix loop helix protein HES-1 binds to and modulates the transactivating function of the runt-related factor Cbfa1. J Biol Chem 275:530-538.
67. Hess J, Porte D, Munz C, Angel P 2001 AP-1 and Cbfa/Runt physically interact and regulate parathyroid hormone-dependent MMP13 expression in osteoblasts through a new osteoblast-specific element 2/AP-1 composite element. J Biol Chem 276:20029-20038.
68. Gutierrez S, Javed A, Tennant DK, van Rees M, Montecino M, Stein GS, Stein JL, Lian JB 2002 CCAAT/enhancer-binding proteins (C/EBP) beta and delta activate osteocalcin gene transcription and synergize with Runx2 at the C/EBP element to regulate bone-specific expression. J Biol Chem 277:1316-1323.
69. Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Bebringer RR, de Crombrugghe B 2002 The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108:17-29.