Transcription in the Osteoblast: Regulatory Mechanisms Utilized by Parathyroid Hormone and Transforming Growth Factor-Beta

Progress in Nucleic Acid Research and Molecular Biology

Volumn 80, Issue , 2005, Pages 287-321

  Boumah, Christine E ^a   Selvamurugan, Nagarajan ^a   Partridge, Nicola C ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGENASE; COLLAGENASE 3; CYCLIC AMP DEPENDENT PROTEIN KINASE; MMP13 PROTEIN, HUMAN; PARATHYROID HORMONE; PARATHYROID HORMONE RECEPTOR 1; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; BIOLOGICAL MODEL; DRUG EFFECT; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; OSTEOBLAST; OSTEOLYSIS; PROMOTER REGION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BONE RESORPTION; COLLAGENASES; CORE BINDING FACTOR ALPHA 1 SUBUNIT; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HUMANS; MATRIX METALLOPROTEINASE 13; MODELS, BIOLOGICAL; OSTEOBLASTS; PARATHYROID HORMONE; PROMOTER REGIONS (GENETICS); RECEPTOR, PARATHYROID HORMONE, TYPE 1; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 33644683683     PISSN: 00796603     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6603(05)80007-8     Document Type: Review

References (166)

1. Stein G.S., Lian J.B., and Owen T.A. Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation. FASEB J. 4 (1990) 3111-3123
2. Stein G.S., Lian J.B., Stein J.L., Van Wijnen A.J., and Montecino M. Transcriptional control of osteoblast growth and differentiation. Physiol. Rev. 76 (1996) 593-629
3. Shalhoub V., Conlon D., Tassinari M., Quinn C., Partridge N., Stein G.S., and Lian J.B. Glucocorticoids promote development of the osteoblast phenotype by selectively modulating expression of cell growth and differentiation associated genes. J. Cell Biochem. 50 (1992) 425-440
4. Owen T.A., Aronow M., Shalhoub V., Barone L.M., Wilming L., Tassinari M.S., Kennedy M.B., Pockwinse S., Lian J.B., and Stein G.S. Progressive development of the rat osteoblast phenotype in vitro: Reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J. Cell Physiol. 143 (1990) 420-430
5. Birnbaum R.S., Bowsher R.R., and Wiren K.M. Changes in IGF-I and -II expression and secretion during the proliferation and differentiation of normal rat osteoblasts. J. Endocrinol. 144 (1995) 251-259
6. Weinreb M., Shinar D., and Rodan G.A. Different pattern of alkaline phosphatase, osteopontin, and osteocalcin expression in developing rat bone visualized by in situ hybridization. J. Bone Miner. Res. 5 (1990) 831-842
7. Boskey A.L., Wright T.M., and Blank R.D. Collagen and bone strength. J. Bone Miner. Res. 14 (1999) 330-335
8. Dempster D.W., Cosman F., Parisien M., Shen V., and Lindsay R. Anabolic actions of parathyroid hormone on bone. Endocr. Rev. 14 (1993) 690-709
9. Swarthout J.T., D'Alonzo R.C., Selvamurugan N., and Partridge N.C. Parathyroid hormone-dependent signaling pathways regulating genes in bone cells. Gene 282 (2002) 1-17
10. Lian J.B., Stein G.S., Stein J.L., and van Wijnen A.J. Regulated expression of the bone-specific osteocalcin gene by vitamins and hormones. Vitam. Horm. 55 (1999) 443-509
11. Turner R.T., Riggs B.L., and Spelsberg T.C. Skeletal effects of estrogen. Endocr. Rev. 15 (1994) 275-300
12. Boyce B.F., Hughes D.E., Wright K.R., Xing L., and Dai A. Recent advances in bone biology provide insight into the pathogenesis of bone diseases. Lab. Invest. 79 (1999) 83-94
13. Delany A.M., Dong Y., and Canalis E. Mechanisms of glucocorticoid action in bone cells. J. Cell Biochem. 56 (1994) 295-302
14. Ishida Y., and Heersche J.N. Glucocorticoid-induced osteoporosis: Both in vivo and in vitro concentrations of glucocorticoids higher than physiological levels attenuate osteoblast differentiation. J. Bone Miner. Res. 13 (1998) 1822-1826
15. Bonewald L.F., and Mundy G.R. Role of transforming growth factor-beta in bone remodeling. Clin. Orthop. 26 (1990) 1-276
16. Breen E.C., Ignotz R.A., McCabe L., Stein J.L., Stein G.S., and Lian J.B. TGF beta alters growth and differentiation related gene expression in proliferating osteoblasts in vitro, preventing development of the mature bone phenotype. J. Cell Physiol. 160 (1994) 323-335
17. Tang K.T., Capparelli C., Stein J.L., Stein G.S., Lian J.B., Huber A.C., Braverman L.E., and DeVito W.J. Acidic fibroblast growth factor inhibits osteoblast differentiation in vitro: Altered expression of collagenase, cell growth-related, and mineralization-associated genes. J. Cell Biochem. 61 (1996) 152-166
18. Silverberg S.J., Shane E., Jacobs T.P., Siris E., and Bilezikian J.P. A 10-year prospective study of primary hyperparathyroidism with or without parathyroid surgery. N. Engl. J. Med. 341 (1999) 1249-1255
19. Potts Jr. J.T., Gardella T.J., Juppner H., and Kronenberg H.M. Structure-based design of parathyroid hormone analogs. J. Endocrinol. 154 (1997) S15-S21
20. Rantakokko J., Aro H.T., Savontaus M., and Vuorio E. Mouse cathepsin K: cDNA cloning and predominant expression of the gene in osteoclasts, and in some hypertrophying chondrocytes during mouse development. FEBS Lett. 393 (1996) 307-313
21. Sato T., del Carmen Ovejero M., Hou P., Heegaard A.M., Kumegawa M., Foged N.T., and Delaisse J.M. Identification of the membrane-type matrix metalloproteinase MT1-MMP in osteoclasts. J. Cell Sci. 110 (1997) 589-596
22. Delaisse J.M., Eeckhout Y., Neff L., Francois-Gillet C., Henriet P., Su Y., Vaes G., and Baron R. (Pro)collagenase (matrix metalloproteinase-1) is present in rodent osteoclasts and in the underlying bone-resorbing compartment. J. Cell Sci. 106 (1993) 1071-1082
23. Chambers T.J., Darby J.A., and Fuller K. Mammalian collagenase predisposes bone surfaces to osteoclastic resorption. Cell Tissue Res. 421 (1985) 671-675
24. Yasuda H., Shima N., Nakagawa N., Yamaguchi K., Kinosaki M., Mochizuki S., Tomoyasu A., Yano K., Goto M., Murakami A., Tsuda E., Morinaga T., Higashio K., Udagawa N., Takahashi N., and Suda T. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc. Natl. Acad. Sci. USA 95 (1998) 3597-3602
25. Lacey D.L., Timms E., Tan H.L., Kelley M.J., Dunstan C.R., Burgess T., Elliott R., Colombero A., Elliott G., Scully S., Hsu H., Sullivan J., Hawkins N., Davy E., Capparelli C., Eli A., Qian Y.X., Kaufman S., Sarosi I., Shalhoub V., Senaldi G., Guo J., Delaney J., and Boyle W.J. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93 (1998) 165-176
26. Kong Y.Y., Yoshida H., Sarosi I., Tan H.L., Timms E., Capparelli C., Morony S., Oliveira-dos-Santos A.J., Van G., Itie A., Khoo W., Wakeham A., Dunstan C.R., Lacey D.L., Mak T.W., Boyle W.J., and Penninger J.M. OPGL is a key regulator of osteoclastogenesis, lymphocyte development, and lymph-node organogenesis. Nature 397 (1999) 315-323
27. Dietrich J.W., Canalis E.M., Maina D.M., and Raisz L.G. Hormonal control of bone collagen synthesis in vitro: Effects of parathyroid hormone and calcitonin. Endocrinology 98 (1976) 943-949
28. Partridge N.C., Dickson C.A., Kopp K., Teitelbaum S.L., Crouch E.C., and Kahn A.J. Parathyroid hormone inhibits collagen synthesis at both ribonucleic acid and protein levels in rat osteogenic sarcoma cells. Mol. Endocrinol. 3 (1989) 232-239
29. Delaisse J.M., Eeckhout Y., and Vaes G. Bone-resorbing agents affect the production and distribution of procollagenase as well as the activity of collagenase in bone tissue. Endocrinology 123 (1988) 264-276
30. Hamilton J.A., Lingelbach S., Partridge N.C., and Martin T.J. Regulation of plasminogen activator production by bone-resorbing hormones in normal and malignant osteoblasts. Endocrinology 116 (1985) 2186-2191
31. Wucherpfennig A.L., Li Y.P., Stetler-Stevenson W.G., Rosenberg A.E., and Stashenko P. Expression of 92 kD type IV collagenase/gelatinase B in human osteoclasts. J. Bone Miner. Res. 9 (1994) 549-556
32. Walker D.G., Lapiere C.M., and Gross J. A collagenolytic factor in rat bone promoted by parathyroid extract. Biochem. Biophys. Res. Commun. 15 (1964) 397-402
33. Rasmussen H., Arnaud C., and Hawker C. Actinomycin D and the response to parathyroid hormone. Science 144 (1964) 1019-1021
34. Tashjian Jr. A.H., Ontjes D.A., and Goodfriend T.L. Mechanism of parathyroid hormone action. Effects of actinomycin D on hormone-stimulated ion movement in vivo and in vitro. Biochem. Biophys. Res. Commun. 16 (1964) 209-215
35. Quinn C.O., Scott D.K., Brinckerhoff C.E., Matrisian L.M., Jeffrey J.J., and Partridge N.C. Rat collagenase. Cloning, amino acid sequence comparison, and parathyroid hormone regulation in osteoblastic cells. J. Biol. Chem. 265 (1990) 22342-22347
36. Partridge N.C., Jeffrey J.J., Ehlich L.S., Teitelbaum S.L., Fliszar C., Welgus H.G., and Kahn A.J. Hormonal regulation of the production of collagenase and a collagenase inhibitor activity by rat osteogenic sarcoma cells. Endocrinology 120 (1987) 1956-1962
37. Scott D.K., Brakenhoff K.D., Clohisy J.C., Quinn C.O., and Partridge N.C. Parathyroid hormone induces transcription of collagenase in rat osteoblastic cells by a mechanism using cyclic adenosine 3′,5′-monophosphate and requiring protein synthesis. Mol. Endocrinol. 6 (1992) 2153-2159
38. Qin L., Qiu P., Wang L., Li X., Swarthout J.T., Soteropoulos P., Tolias P., and Partridge N.C. Gene expression profiles and transcription factors involved in parathyroid hormone signaling in osteoblasts revealed by microarray and bioinformatics. J. Biol. Chem. 278 (2003) 19723-19731
39. Juppner H. Receptors for parathyroid hormone and parathyroid hormone-related peptide: Exploration of their biological importance. Bone 25 (1999) 87-90
40. Civitelli R., Reid I.R., Westbrook S., Avioli L.V., and Hruska K.A. PTH elevates inositol polyphosphates and diacylglycerol in a rat osteoblast-like cell line. Am. J. Physiol. 255 (1988) E660-E667
41. Babich M., Choi H., Johnson R.M., King K.L., Alford G.E., and Nissenson R.A. Thrombin and parathyroid hormone mobilize intracellular calcium in rat osteosarcoma cells by distinct pathways. Endocrinology 129 (1991) 1463-1470
42. Takasu H., Guo J., and Bringhurst F.R. Dual signaling and ligand selectivity of the human PTH/PTHrP receptor. J. Bone Miner. Res. 14 (1999) 11-20
43. Chase L.R., and Aurbach G.D. The effect of parathyroid hormone on the concentration of adenosine 3′-5′-monophosphate in skeletal tissue in vitro. J. Biol. Chem. 245 (1970) 1520-1526
44. Yang R., Gotoh Y., Moore M.A., Rafidi K., and Gerstenfeld L.C. Characterization of an avian bone sialoprotein (BSP) cDNA: Comparisons to mammalian BSP and identification of conserved structural domains. J. Bone Miner. Res. 10 (1995) 632-640
45. Yang R., and Gerstenfeld L.C. Signal transduction pathways mediating parathyroid hormone stimulation of bone sialoprotein gene expression in osteoblasts. J. Biol. Chem. 271 (1996) 29839-29846
46. Woessner Jr. J.F. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 5 (1991) 2145-2154
47. Matrisian L.M. The matrix-degrading metalloproteinases. Bioessays 14 (1992) 455-463
48. Roswit W.T., Halme J., and Jeffrey J.J. Purification and properties of rat uterine procollagenase. Arch. Biochem. Biophys. 225 (1983) 285-295
49. Mattot V., Raes M.B., Henriet P., Eeckhout Y., Stehelin D., Vandenbunder B., and Desbiens X. Expression of interstitial collagenase is restricted to skeletal tissue during mouse embryogenesis. J. Cell Sci. 108 (1995) 529-535
50. Meikle M.C., Bord S., Hembry R.M., Compston J., Croucher P.I., and Reynolds J.J. Human osteoblasts in culture synthesize collagenase and other matrix metalloproteinases in response to osteotropic hormones and cytokines. J. Cell Sci. 103 (1992) 1093-1099
51. Gack S., Vallon R., Schmidt J., Grigoriadis A., Tuckermann J., Schenkel J., Weiher H., Wagner E.F., and Angel P. Expression of interstitial collagenase during skeletal development of the mouse is restricted to osteoblast-like cells and hypertrophic chondrocytes. Cell Growth Differ. 6 (1995) 759-767
52. Zhao W., Byrne M.H., Boyce B.F., and Krane S.M. Bone resorption induced by parathyroid hormone is strikingly diminished in collagenase-resistant mutant mice. J. Clin. Invest. 103 (1999) 517-524
53. Delany A.M., Rydziel S., and Canalis E. Autocrine down-regulation of collagenase-3 in rat bone cell cultures by insulin-like growth factors. Endocrinology 137 (1996) 4665-4670
54. Varghese S., and Canalis E. Regulation of collagenase-3 by bone morphogenetic protein-2 in bone cell cultures. Endocrinology 138 (1997) 1035-1040
55. Gazzerro E., Rydziel S., and Canalis E. Skeletal bone morphogenetic proteins suppress the expression of collagenase-3 by rat osteoblasts. Endocrinology 140 (1999) 562-567
56. Aznavoorian S., Murphy A.N., Stetler-Stevenson W.G., and Liotta L.A. Molecular aspects of tumor cell invasion and metastasis. Cancer 71 (1993) 1368-1383
57. Billinghurst R.C., Dahlberg L., Ionescu M., Reiner A., Bourne R., Rorabeck C., Mitchell P., Hambor J., Diekmann O., Tschesche H., Chen J., Van Wart H., and Poole A.R. Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J. Clin. Invest. 99 (1997) 1534-1545
58. Mitchell P.G., Magna H.A., Reeves L.M., Lopresti-Morrow L.L., Yocum S.A., Rosner P.J., Geoghegan K.F., and Hambor J.E. Cloning, expression, and type II collagenolytic activity of matrix metalloproteinase-13 from human osteoarthritic cartilage. J. Clin. Invest. 97 (1996) 761-768
59. Wernicke D., Seyfert C., Hinzmann B., and Gromnica-Ihle E. Cloning of collagenase 3 from the synovial membrane and its expression in rheumatoid arthritis and osteoarthritis. J. Rheumatol. 23 (1996) 590-595
60. Rajakumar R.A., and Quinn C.O. Parathyroid hormone induction of rat interstitial collagenase mRNA in osteosarcoma cells is mediated through an AP-1-binding site. Mol. Endocrinol. 10 (1996) 867-878
61. Selvamurugan N., Chou W.Y., Pearman A.T., Pulumati M.R., and Partridge N.C. Parathyroid hormone regulates the rat collagenase-3 promoter in osteoblastic cells through the cooperative interaction of the activator protein-1 site and the runt domain binding sequence. J. Biol. Chem. 273 (1998) 10647-10657
62. Porte D., Tuckermann J., Becker M., Baumann B., Teurich S., Higgins T., Owen M.J., Schorpp-Kistner M., and Angel P. Both AP-1 and Cbfa1-like factors are required for the induction of interstitial collagenase by parathyroid hormone. Oncogene 18 (1999) 667-678
63. Pendas A.M., Balbin M., Llano E., Jimenez M.G., and Lopez-Otin C. Structural analysis and promoter characterization of the human collagenase-3 gene (MMP13). Genomics 40 (1997) 222-233
64. Karsenty G. Role of Cbfa1 in osteoblast differentiation and function. Semin. Cell. Dev. Biol. 11 (2000) 343-346
65. Thunyakitpisal P., Alvarez M., Tokunaga K., Onyia J.E., Hock J., Ohashi N., Feister H., Rhodes S.J., and Bidwell J.P. Cloning and functional analysis of a family of nuclear matrix transcription factors (NP/NMP4) that regulate type I collagen expression in osteoblasts. J. Bone Miner. Res. 16 (2001) 10-23
66. Shah R., Alvarez M., Jones D.R., Torrungruang K., Watt A.J., Selvamurugan N., Partridge N.C., Quinn C.O., Pavalko F.M., Rhodes S.J., and Bidwell J.P. Nmp4/CIZ regulation of matrix metalloproteinase 13 (MMP-13) response to parathyroid hormone in osteoblasts. Am. J. Physiol. Endocrinol. Metab. 287 (2004) E289-E296
67. Janknecht R., Cahill M.A., and Nordheim A. Signal integration at the c-fos promoter. Carcinogenesis 16 (1995) 443-450
68. Pearman A.T., Chou W.Y., Bergman K.D., Pulumati M.R., and Partridge N.C. Parathyroid hormone induces c-fos promoter activity in osteoblastic cells through phosphorylated cAMP response element (CRE)-binding protein binding to the major CRE. J. Biol. Chem. 271 (1996) 25715-25721
69. Angel P., and Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim. Biophys. Acta 1072 (1991) 129-157
70. Zhou X.F., Shen X.Q., and Shemshedini L. Ligand-activated retinoic acid receptor inhibits AP-1 transactivation by disrupting c-Jun/c-Fos dimerization. Mol. Endocrinol. 13 (1999) 276-285
71. Franceschi R.T. The developmental control of osteoblast-specific gene expression: Role of specific transcription factors and the extracellular matrix environment. Crit. Rev. Oral Bio. Med. 10 (1999) 40-57
72. Rajaram N., and Kerppola T.K. DNA bending by Fos-Jun and the orientation of heterodimer binding depend on the sequence of the AP-1 site. EMBO J. 16 (1997) 2917-2925
73. Ruther U., Komitowski D., Schubert F.R., and Wagner E.F. c-fos expression induces bone tumors in transgenic mice. Oncogene 4 (1989) 861-865
74. Wang Z.Q., Ovitt C., Grigoriadis A.E., Mohle-Steinlein U., Ruther U., and Wagner E.F. Bone and hematopoietic defects in mice lacking c-fos. Nature 360 (1992) 741-745
75. Clohisy J.C., Scott D.K., Brakenhoff K.D., Quinn C.O., and Partridge N.C. Parathyroid hormone induces c-fos and c-jun messenger RNA in rat osteoblastic cells. Mol. Endocrinol. 6 (1992) 1834-1842
76. Tyson D.R., Swarthout J.T., and Partridge N.C. Increased osteoblastic c-fos expression by parathyroid hormone requires protein kinase A phosphorylation of the cyclic adenosine 3′,5′-monophosphate response element-binding protein at serine 133. Endocrinology 140 (1999) 1255-1261
77. Tyson D.R., Swarthout J.T., Jefcoat S.C., and Partridge N.C. PTH induction of transcriptional activity of the cAMP response element-binding protein requires the serine 129 site and glycogen synthase kinase-3 activity, but not casein kinase II sites. Endocrinology 143 (2002) 674-682
78. Daga A., Karlovich C.A., Dumstrei K., and Banerjee U. Patterning of cells in the Drosophila eye by Lozenge, which shares homologous domains with AML1. Genes Dev. 10 (1996) 1194-1205
79. Bae S.C., Takahashi E., Zhang Y.W., Ogawa E., Shigesada K., Namba Y., Satake M., and Ito Y. Cloning, mapping and expression of PEBP2 alpha C, a third gene encoding the mammalian Runt domain. Gene 159 (1995) 245-248
80. Kanno T., Kanno Y., Chen L.F., Ogawa E., Kim W.Y., and Ito Y. Intrinsic transcriptional activation-inhibition domains of the polyomavirus enhancer binding protein 2/core binding factor alpha subunit revealed in the presence of the beta subunit. Mol. Cell. Biol. 18 (1998) 2444-2454
81. Wang S., Wang Q., Crute B.E., Melnikova I.N., Keller S.R., and Speck N.A. Cloning and characterization of subunits of the T-cell receptor and murine leukemia virus enhancer core-binding factor. Mol. Cell. Biol. 13 (1993) 3324-3339
82. Golling G., Li L., Pepling M., Stebbins M., and Gergen J.P. Drosophila homologs of the proto-oncogene product PEBP2/CBF beta regulate the DNA-binding properties of Runt. Mol. Cell. Biol. 16 (1996) 932-942
83. 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
84. Thirunavukkarasu K., Mahajan 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. 18 (1998) 4197-4208
85. Tintut Y., Parhami F., Le V., Karsenty G., and Demer L.L. Inhibition of osteoblast-specific transcription factor Cbfa1 by the cAMP pathway in osteoblastic cells. Ubiquitin/proteasome-dependent regulation. J. Biol. Chem. 274 (1999) 28875-28879
86. Selvamurugan N., Pulumati M.R., Tyson D.R., and Partridge N.C. Parathyroid hormone regulation of the rat collagenase-3 promoter by protein kinase A-dependent transactivation of core binding factor alpha1. J. Biol. Chem. 275 (2000) 5037-5042
87. Xiao G., Wang D., Benson M.D., Karsenty G., and Franceschi R.T. Role of the alpha2-integrin in osteoblast-specific gene expression and activation of the Osf2 transcription factor. J. Biol. Chem. 273 (1998) 32988-32994
88. Fujiwara M., Tagashira S., Harada H., Ogawa S., Katsumata T., Nakatsuka M., Komori T., and Takada H. Isolation and characterization of the distal promoter region of mouse Cbfa1. Biochim. Biophys. Acta 1446 (1999) 265-272
89. Tsuji K., Ito Y., and Noda M. Expression of the PEBP2alphaA/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 (1998) 87-92
90. Li J., Tsuji K., Komori T., Miyazono K., Wrana J.L., Ito Y., Nifuji A., and Noda M. Smad2 overexpression enhances Smad4 gene expression and suppresses CBFA1 gene expression in osteoblastic osteosarcoma ROS17/2.8 cells and primary rat calvaria cells. J. Biol. Chem. 273 (1998) 31009-31015
91. Ducy P., Starbuck M., Priemel M., Shen J., Pinero G., Geoffroy V., Amling M., and Karsenty G. A Cbfa1-dependent genetic pathway controls bone formation beyond embryonic development. Genes Dev. 13 (1999) 1025-1036
92. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., Shimizu Y., Bronson R.T., Gao Y.H., Inada M., Sato M., Okamoto R., Kitamura Y., Yoshiki S., and Kishimoto T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89 (1997) 755-764
93. Lee B., Thirunavukkarasu K., Zhou L., Pastore L., Baldini A., Hecht J., Geoffroy V., Ducy P., and Karsenty G. Missense mutations abolishing DNA binding of the osteoblast-specific transcription factor OSF2/CBFA1 in cleidocranial dysplasia. Nat. Genet. 16 (1997) 307-310
94. Gutman A., and Wasylyk B. Nuclear targets for transcription regulation by oncogenes. Trends Genet. 7 (1991) 49-54
95. Fry C.J., and Farnham P.J. Context-dependent transcriptional regulation. J. Biol. Chem. 274 (1999) 29583-29586
96. Ning Y.M., and Robins D.M. AML3/CBFalpha1 is required for androgen-specific activation of the enhancer of the mouse sex-limited protein (Slp) gene. J. Biol. Chem. 274 (1999) 30624-30630
97. McLarren K.W., Lo R., Grbavec D., Thirunavukkarasu K., Karsenty G., and Stifani S. 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 (2000) 530-538
98. Westendorf J.J., Zaidi S.K., Cascino J.E., Kahler R., van Wijnen A.J., Lian J.B., Yoshida M., Stein G.S., and Li X. Runx2 (Cbfa1, AML-3) interacts with histone deacetylase 6 and represses the p21(CIP1/WAF1) promoter. Mol. Cell. Biol. 22 (2002) 7982-7992
99. Cui C.B., Cooper L.F., Yang X., Karsenty G., and Aukhil I. Transcriptional coactivation of bone-specific transcription factor Cbfa1 by TAZ. Mol. Cell. Biol. 23 (2003) 1004-1013
100. Chen L., Glover J.N., Hogan P.G., Rao A., and Harrison S.C. Structure of the DNA-binding domains from NFAT, Fos and Jun bound specifically to DNA. Nature 392 (1998) 42-48
101. Bannister A.J., and Kouzarides T. CBP-induced stimulation of c-Fos activity is abrogated by E1A. EMBO J. 14 (1995) 4758-4762
102. Kamei Y., Xu L., Heinzel T., Torchia J., Kurokawa R., Gloss B., Lin S.C., Heyman R.A., Rose D.W., Glass C.K., and Rosenfeld M.G. A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors. Cell 85 (1996) 403-414
103. Metz R., Bannister A.J., Sutherland J.A., Hagemeier C., O'Rourke E.C., Cook A., Bravo R., and Kouzarides T. c-Fos-induced activation of a TATA-box-containing promoter involves direct contact with TATA-box-binding protein. Mol. Cell. Biol. 14 (1994) 6021-6029
104. Martin M.L., Lieberman P.M., and Curran T. Fos-Jun dimerization promotes interaction of the basic region with TFIIE-34 and TFIIF. Mol. Cell. Biol. 16 (1996) 2110-2118
105. D'Alonzo R.C., Selvamurugan N., Karsenty G., and Partridge N.C. Physical interaction of the activator protein-1 factors c-Fos and c-Jun with Cbfa1 for collagenase-3 promoter activation. J. Biol. Chem. 277 (2002) 816-822
106. John S., and Workman J.L. Just the facts of chromatin transcription. Science 282 (1998) 1836-1837
107. Boumah C.E., Selvamurugan N., and Partridge N.C. Transcriptional activation of collagenase-3 by PTH: Changes in chromatin structure in the proximal promoter region. J. Bone Min. Res. 19 (2004) S218
108. Kurdistani S.K., Tavazoie S., and Grunstein M. Mapping global histone acetylation patterns to gene expression. Cell 117 (2004) 721-733
109. Lian J.B., Javed A., Zaidi S.K., Lengner C., Montecino M., van Wijnen A.J., Stein J.L., and Stein G.S. Regulatory controls for osteoblast growth and differentiation: Role of Runx/Cbfa/AML factors. Crit. Rev. Eukaryotic Gene Exp. 14 (2004) 1-41
110. Horner A., Kemp P., Summers C., Bord S., Bishop N.J., Kelsall A.W., Coleman N., and Compston J.E. Expression and distribution of transforming growth factor-beta isoforms and their signaling receptors in growing human bone. Bone 23 (1998) 95-102
111. Hartsough M.T., and Mulder K.M. Transforming growth factor-beta signaling in epithelial cells. Pharmacol. Therapeutics 75 (1997) 21-41
112. Centrella M., and Canalis E. Transforming and nontransforming growth factors are present in medium conditioned by fetal rat calvariae. Proc. Natl. Acad. Sci. USA 82 (1985) 7335-7339
113. Oursler M.J. Osteoclast synthesis and secretion and activation of latent transforming growth factor beta. J. Bone Min. Res. 9 (1994) 443-452
114. Oreffo R.O., Mundy G.R., Seyedin S.M., and Bonewald L.F. Activation of the bone-derived latent TGF beta complex by isolated osteoclasts. Biochem. Biophys. Res. Comm. 158 (1989) 817-823
115. Bonewald L.F., Wakefield L., Oreffo R.O., Escobedo A., Twardzik D.R., and Mundy G.R. Latent forms of transforming growth factor-beta (TGF beta) derived from bone cultures: Identification of a naturally occurring 100-kDa complex with similarity to recombinant latent TGF beta. Mol. Endocrin. 5 (1991) 741-751
116. Bonewald L.F., and Dallas S.L. Role of active and latent transforming growth factor beta in bone formation. J. Cell. Biochem. 55 (1994) 350-357
117. Pfeilschifter J., and Mundy G.R. Modulation of type beta transforming growth factor activity in bone cultures by osteotropic hormones. Proc. Natl. Acad. Sci. USA 84 (1987) 2024-2028
118. Centrella M., Horowitz M.C., Wozney J.M., and McCarthy T.L. Transforming growth factor-beta gene family members and bone. Endocrine Reviews 15 (1994) 27-39
119. Noda M., and Camilliere J.J. In vivo stimulation of bone formation by transforming growth factor-beta. Endocrinology 124 (1989) 2991-2994
120. Garcia C., Boyce B.F., Gilles J., Dallas M., Qiao M., Mundy G.R., and Bonewald L.F. Leukotriene B4 stimulates osteoclastic bone resorption both in vitro and in vivo. J. Bone Min. Res. 11 (1996) 1619-1627
121. Rosier R.N., O'Keefe R.J., and Hicks D.G. The potential role of transforming growth factor beta in fracture healing. Clin. Orthopaedics Related Res. (1998) S294-S300
122. Geiser A.G., Zeng Q.Q., Sato M., Helvering L.M., Hirano T., and Turner C.H. Decreased bone mass and bone elasticity in mice lacking the transforming growth factor-beta1 gene. Bone 23 (1998) 87-93
123. Filvaroff E., Erlebacher A., Ye J., Gitelman S.E., Lotz J., Heillman M., and Derynck R. Inhibition of TGF-beta receptor signaling in osteoblasts leads to decreased bone remodeling and increased trabecular bone mass. Development 126 (1999) 4267-4279
124. Rydziel S., Varghese S., and Canalis E. Transforming growth factor beta1 inhibits collagenase 3 expression by transcriptional and post-transcriptional mechanisms in osteoblast cultures. J. Cell. Physiol. 170 (1997) 145-152, [erratum appears in J. Cell. Physiol. 1997, May; 171(2):234].
125. Zhang Y., Feng X., We R., and Derynck R. Receptor-associated Mad homologues synergize as effectors of the TGF-beta response. Nature 383 (1996) 168-172
126. Engel M.E., McDonnell M.A., Law B.K., and Moses H.L. Interdependent SMAD and JNK signaling in transforming growth factor-beta-mediated transcription. J. Biol. Chem. 274 (1999) 37413-37420
127. de Caestecker M.P., Hemmati P., Larisch-Bloch S., Ajmera R., Roberts A.B., and Lechleider R.J. Characterization of functional domains within Smad4/DPC4. J. Biol. Chem. 272 (1997) 13690-13696
128. Liu F., Pouponnot C., and Massague J. Dual role of the Smad4/DPC4 tumor suppressor in TGFbeta-inducible transcriptional complexes. Genes Devel. 11 (1997) 3157-3167
129. de Caestecker M.P., Yahata T., Wang D., Parks W.T., Huang S., Hill C.S., Shioda T., Roberts A.B., and Lechleider R.J. The Smad4 activation domain (SAD) is a proline-rich, p300-dependent transcriptional activation domain. J. Biol. Chem. 275 (2000) 2115-2122
130. Miyazawa K., Shinozaki M., Hara T., Furuya T., and Miyazono K. Two major Smad pathways in TGF-beta superfamily signalling. Genes Cells 7 (2002) 1191-1204
131. Shi Y., Wang Y.F., Jayaraman L., Yang H., Massague J., and Pavletich N.P. Crystal structure of a Smad MH1 domain bound to DNA: Insights on DNA binding in TGF-beta signaling. Cell 94 (1998) 585-594
132. Pardali E., Xie X.Q., Tsapogas P., Itoh S., Arvanitidis K., Heldin C.H., ten Dijke P., Grundstrom T., and Sideras P. Smad and AML proteins synergistically confer transforming growth factor beta1 responsiveness to human germ-line IgA genes. J. Biol. Chem. 275 (2000) 3552-3560
133. Moustakas A., and Kardassis D. Regulation of the human p21/WAF1/Cip1 promoter in hepatic cells by functional interactions between Sp1 and Smad family members. Proc. Natl. Acad. Sci. USA 95 (1998) 6733-6738
134. Attisano L., Silvestri C., Izzi L., and Labbe E. The transcriptional role of Smads and FAST (FoxH1) in TGFbeta and activin signalling. Mol. Cell Endocrin. 180 (2001) 3-11
135. Chen C.R., Kang Y., and Massague J. Defective repression of c-myc in breast cancer cells: A loss at the core of the transforming growth factor beta growth arrest program. Proc. Natl. Acad. Sci. USA 98 (2001) 992-999
136. Verrecchia F., Chu M.L., and Mauviel A. Identification of novel TGF-beta/Smad gene targets in dermal fibroblasts using a combined cDNA microarray/promoter transactivation approach. J. Biol. Chem. 276 (2001) 17058-17062
137. Zavadil J., Bitzer M., Liang D., Yang Y.C., Massimi A., Kneitz S., Piek E., and Bottinger E.P. Genetic programs of epithelial cell plasticity directed by transforming growth factor-beta. Proc. Natl. Acad. Sci. USA 98 (2001) 6686-6691
138. Kang Y., Chen C.R., and Massague J. A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol. Cell 11 (2003) 915-926
139. Hannon G.J., and Beach D. p15INK4B is a potential effector of TGF-beta-induced cell cycle arrest. [see comment]. Nature 371 (1994) 257-261
140. Reynisdottir I., Polyak K., Iavarone A., and Massague J. Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Devel. 9 (1995) 1831-1845
141. Datto M.B., Yu Y., and Wang X.F. Functional analysis of the transforming growth factor beta responsive elements in the WAF1/Cip1/p21 promoter. J. Biol. Chem. 270 (1995) 28623-28628
142. Hill C.S. The Smads. Int. J. Biochem. Cell Bio. 31 (1999) 1249-1254
143. Qian S.W., Burmester J.K., Sun P.D., Huang A., Ohlsen D.J., Suardet L., Flanders K.C., Davies D., Roberts A.B., and Sporn M.B. Characterization of mutated transforming growth factor-betas which possess unique biological properties. Biochemistry 33 (1994) 12298-12304
144. Massague J. TGF-beta signal transduction. Ann. Rev. Biochem. 67 (1998) 753-791
145. Derynck R., Akhurst R.J., and Balmain A. TGF-beta signaling in tumor suppression and cancer progression. Nat. Genet. 29 (2001) 117-129, [erratum appears in Nat. Genet. 2001, Nov; 29(3), 351].
146. Kusano K., Miyaura C., Inada M., Tamura T., Ito A., Nagase H., Kamoi K., and Suda T. Regulation of matrix metalloproteinases (MMP-2, -3, -9, and -13) by interleukin-1 and interleukin-6 in mouse calvaria: Association of MMP induction with bone resorption. Endocrinology 139 (1998) 1338-1345
147. Varghese S., Delany A.M., Liang L., Gabbitas B., Jeffrey J.J., and Canalis E. Transcriptional and posttranscriptional regulation of interstitial collagenase by platelet-derived growth factor BB in bone cell cultures. Endocrinology 137 (1996) 431-437
148. Varghese S., Ramsby M.L., Jeffrey J.J., and Canalis E. Basic fibroblast growth factor stimulates expression of interstitial collagenase and inhibitors of metalloproteinases in rat bone cells. Endocrinology 136 (1995) 2156-2162
149. Varghese S., Rydziel S., and Canalis E. Basic fibroblast growth factor stimulates collagenase-3 promoter activity in osteoblasts through an activator protein-1-binding site. Endocrinology 141 (2000) 2185-2191
150. Zhao W., Byrne M.H., Wang Y., and Krane S.M. Osteocyte and osteoblast apoptosis and excessive bone deposition accompany failure of collagenase cleavage of collagen. J. Clin. Invest. 106 (2000) 941-949
151. Selvamurugan N., Kwok S., Alliston T., Reiss M., and Partridge N.C. Transforming growth factor-beta 1 regulation of collagenase-3 expression in osteoblastic cells by cross-talk between the Smad and MAPK signaling pathways and their components, Smad2 and Runx2. J. Biol. Chem. 279 (2004) 19327-19334
152. Uria J.A., Jimenez M.G., Balbin M., Freije J.M., and Lopez-Otin C. Differential effects of transforming growth factor-beta on the expression of collagenase-1and collagenase-3 in human fibroblasts. J. Biol. Chem. 273 (1998) 9769-9777
153. Zhang Y., and Derynck R. Transcriptional regulation of the transforming growth factor-beta-inducible mouse germ line Ig alpha constant region gene by functional cooperation of Smad, CREB, and AML family members. J. Biol. Chem. 275 (2000) 16979-16985
154. Leivonen S.K., Chantry A., Hakkinen L., Han J., and Kahari V.M. Smad3 mediates transforming growth factor-beta-induced collagenase-3 (matrix metalloproteinase-13) expression in human gingival fibroblasts. Evidence for cross-talk between Smad3 and p38 signaling pathways. J. Biol. Chem. 277 (2002) 46338-46346
155. Tardif G., Reboul P., Dupuis M., Geng C., Duval N., Pelletier J.P., and Martel-Pelletier J. Transforming growth factor-beta induced collagenase-3 production in human osteoarthritic chondrocytes is triggered by Smad proteins: Cooperation between activator protein-1 and PEA-3 binding sites. J. Rheum. 28 (2001) 1631-1639
156. Johansson N., Ala-aho R., Uitto V., Grenman R., Fusenig N.E., Lopez-Otin C., and Kahari V.M. Expression of collagenase-3 (MMP-13) and collagenase-1 (MMP-1) by transformed keratinocytes is dependent on the activity of p38 mitogen-activated protein kinase. J. Cell Sci. 2 (2000) 227-235
157. Franceschi R.T., Xiao G., Jiang D., Gopalakrishnan R., Yang S., and Reith E. Multiple signaling pathways converge on the Cbfa1/Runx2 transcription factor to regulate osteoblast differentiation. Conn. Tiss. Res. 44 (2003) 109-116
158. Xiao G., Jiang D., Gopalakrishnan R., and Franceschi R.T. Fibroblast growth factor 2 induction of the osteocalcin gene requires MAPK activity and phosphorylation of the osteoblast transcription factor, Cbfa1/Runx2. J. Biol. Chem. 277 (2002) 36181-36187
159. Choi J.Y., Pratap J., Javed A., Zaidi S.K., Xing L., Balint E., Dalamangas S., Boyce B., van Wijnen A.J., Lian J.B., Stein J.L., Jones S.N., and Stein G.S. Subnuclear targeting of Runx/Cbfa/AML factors is essential for tissue-specific differentiation during embryonic development. Proc. Natl. Acad. Sci. USA 98 (2001) 8650-8655
160. Uchiyama-Tanaka Y., Matsubara H., Mori Y., Kosaki A., Kishimoto N., Amano K., Higashiyama S., and Iwasaka T. Involvement of HB-EGF and EGF receptor transactivation in TGF-beta-mediated fibronectin expression in mesangial cells. Kidney International 62 (2002) 799-808
161. Lee K.S., Hong S.H., and Bae S.C. Both the Smad and p38 MAPK pathways play a crucial role in Runx2 expression following induction by transforming growth factor-beta and bone morphogenetic protein. Oncogene 21 (2002) 7156-7163
162. Mengshol J.A., Vincenti M.P., and Brinckerhoff C.E. IL-1 induces collagenase-3 (MMP-13) promoter activity in stably transfected chondrocytic cells: Requirement for Runx-2 and activation by p38 MAPK and JNK pathways. Nucleic Acids Res. 29 (2001) 4361-4372
163. Pouponnot C., Jayaraman L., and Massague J. Physical and functional interaction of SMADs and p300/CBP. J. Biol. Chem. 273 (1998) 22865-22868
164. Feng X.H., Zhang Y., Wu R.Y., and Derynck R. The tumor suppressor Smad4/DPC4 and transcriptional adaptor CBP/p300 are coactivators for smad3 in TGF-beta-induced transcriptional activation. Genes Devel. 12 (1998) 2153-2163
165. Ulloa L., Doody J., and Massague J. Inhibition of transforming growth factor-beta/SMAD signalling by the interferon-gamma/STAT pathway. Nature 397 (1999) 710-713
166. Kim S., Koga T., Isobe M., Kern B.E., Yokochi T., Chin Y.E., Karsenty G., Taniguchi T., and Takayanagi H. Stat1 functions as a cytoplasmic attenuator of Runx2 in the transcriptional program of osteoblast differentiation. Genes Devel. 17 (2003) 1979-1991