Twisted gastrulation and chordin inhibit differentiation and mineralization in MC3T3-E1 osteoblast-like cells

Bone

Volumn 36, Issue 4, 2005, Pages 617-626

  Petryk, Anna ^a,b   Shimmi, Osamu ^b   Jia, Xiaohong ^c   Carlson, Ann E ^d   Tervonen, Leah ^d   Jarcho, Michael P ^a   O'Connor, Michael B ^b   Gopalakrishnan, Rajaram ^d  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c RandD Systems Inc   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Bone morphogenetic protein; Chordin; Differentiation; MC3T3 E1; Mineralization; Osteoblast; Twisted gastrulation

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CHORDIN; OSTEOCALCIN; SMAD1 PROTEIN;

ANIMAL CELL; ARTICLE; CELL CLONE; CELL CLONING; CELL CULTURE; CELL DIFFERENTIATION; CULTURE MEDIUM; DOSE RESPONSE; ENZYME ACTIVITY; FEMALE; GASTRULATION; MINERALIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

EID: 18044395766     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2005.01.018     Document Type: Article

References (60)

1. H. Qi, D.J. Aguiar, S.M. Williams, A. La Pean, W. Pan, and C.M. Verfaillie Identification of genes responsible for osteoblast differentiation from human mesodermal progenitor cells Proc. Natl. Acad. Sci. U. S. A. 100 2003 3305 3310
2. M.F. Pittenger, A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, and J.D. Mosca Multilineage potential of adult human mesenchymal stem cells Science 284 1999 143 147
3. J.E. Dennis, A. Merriam, A. Awadallah, J.U. Yoo, B. Johnstone, and A.I. Caplan A quadripotential mesenchymal progenitor cell isolated from the marrow of an adult mouse J. Bone Miner. Res. 14 1999 700 709
4. A. Yamaguchi, T. Katagiri, T. Ikeda, J.M. Wozney, V. Rosen, and E.A. Wang Recombinant human bone morphogenetic protein-2 stimulates osteoblastic maturation and inhibits myogenic differentiation in vitro J. Cell. Biol. 113 1991 681 687
5. G. van der Horst, R.L. van Bezooijen, M.M. Deckers, J. Hoogendam, A. Visser, and C.W. Lowik Differentiation of murine preosteoblastic KS483 cells depends on autocrine bone morphogenetic protein signaling during all phases of osteoblast formation Bone 31 2002 661 669
6. J.M. Wozney, V. Rosen, A.J. Celeste, L.M. Mitsock, M.J. Whitters, and R.W. Kriz Novel regulators of bone formation: molecular clones and activities Science 242 1988 1528 1534
7. M. Suzawa, Y. Takeuchi, S. Fukumoto, S. Kato, N. Ueno, and K. Miyazono Extracellular matrix-associated bone morphogenetic proteins are essential for differentiation of murine osteoblastic cells in vitro Endocrinology 140 1999 2125 2133
8. A. Nohe, E. Keating, P. Knaus, and N.O. Petersen Signal transduction of bone morphogenetic protein receptors Cell Signal 16 2004 291 299
9. D. Chen, X. Ji, M.A. Harris, J.Q. Feng, G. Karsenty, and A.J. Celeste Differential roles for bone morphogenetic protein (BMP) receptor type IB and IA in differentiation and specification of mesenchymal precursor cells to osteoblast and adipocyte lineages J. Cell. Biol. 142 1998 295 305
10. L.B. Zimmerman, J.M. De Jesus-Escobar, and R.M. Harland The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4 Cell 86 1996 599 606
11. S. Piccolo, Y. Sasai, B. Lu, and E.M. De Robertis Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4 Cell 86 1996 589 598
12. M. Oelgeschlager, J. Larrain, D. Geissert, and E.M. De Robertis The evolutionarily conserved BMP-binding protein Twisted gastrulation promotes BMP signalling Nature 405 2000 757 763
13. J.J. Ross, O. Shimmi, P. Vilmos, A. Petryk, H. Kim, and K. Gaudenz Twisted gastrulation is a conserved extracellular BMP antagonist Nature 410 2001 479 483
14. I.C. Scott, I.L. Blitz, W.N. Pappano, S.A. Maas, K.W. Cho, and D.S. Greenspan Homologues of Twisted gastrulation are extracellular cofactors in antagonism of BMP signalling Nature 410 2001 475 478
15. C. Chang, D.A. Holtzman, S. Chau, T. Chickering, E.A. Woolf, and L.M. Holmgren Twisted gastrulation can function as a BMP antagonist Nature 410 2001 483 487
16. A. Petryk, and M.B. O'Connor Introduction to TGFβ-related signaling C.J. Epstein R.P. Erickson A. Wynshaw-Boris Inborn errors of development: the molecular basis of clinical disorders of morphogenesis 2003 Oxford Univ. Press San Francisco, CA
17. J. Larrain, M. Oelgeschlager, N.I. Ketpura, B. Reversade, L. Zakin, and E.M. De Robertis Proteolytic cleavage of Chordin as a switch for the dual activities of twisted gastrulation in BMP signaling Development 128 2001 4439 4447
18. S.C. Little, and M.C. Mullins Twisted gastrulation promotes BMP signaling in zebrafish dorsal-ventral axial patterning Development 131 2004 5825 5835
19. M. Oelgeschlager, B. Reversade, J. Larrain, S. Little, M.C. Mullins, and E.M. De Robertis The pro-BMP activity of Twisted gastrulation is independent of BMP binding Development 130 2003 4047 4056
20. I.L. Blitz, K.W. Cho, and C. Chang Twisted gastrulation loss-of-function analyses support its role as a BMP inhibitor during early Xenopus embryogenesis Development 130 2003 4975 4988
21. G. Marques, M. Musacchio, M.J. Shimell, K. Wunnenberg-Stapleton, K.W. Cho, and M.B. O'Connor Production of a DPP activity gradient in the early Drosophila embryo through the opposing actions of the SOG and TLD proteins Cell 91 1997 417 426
22. S. Piccolo, E. Agius, B. Lu, S. Goodman, L. Dale, and E.M. De Robertis Cleavage of Chordin by Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity Cell 91 1997 407 416
23. J. Larrain, D. Bachiller, B. Lu, E. Agius, S. Piccolo, and E.M. De Robertis BMP-binding modules in chordin: a model for signalling regulation in the extracellular space Development 127 2000 821 830
24. S.D. Reynolds, D. Zhang, J.E. Puzas, R.J. O'Keefe, R.N. Rosier, and P.R. Reynolds Cloning of the chick BMP1/Tolloid cDNA and expression in skeletal tissues Gene 248 2000 233 243
25. A. Yamaguchi, T. Ishizuya, N. Kintou, Y. Wada, T. Katagiri, and J.M. Wozney Effects of BMP-2, BMP-4, and BMP-6 on osteoblastic differentiation of bone marrow-derived stromal cell lines, ST2 and MC3T3-G2/PA6 Biochem. Biophys. Res. Commun. 220 1996 366 371
26. G. Xiao, R. Gopalakrishnan, D. Jiang, E. Reith, M.D. Benson, and R.T. Franceschi Bone morphogenetic proteins, extracellular matrix, and mitogen-activated kinase signaling pathways are required for osteoblast-specific gene expression and differentiation in MC3T3-E1 cells J. Bone Miner. Res. 17 2002 101 110
27. D. Chen, M.A. Harris, G. Rossini, C.R. Dunstan, S.L. Dallas, and J.Q. Feng Bone morphogenetic protein 2 (BMP-2) enhances BMP-3, BMP-4, and bone cell differentiation marker gene expression during the induction of mineralized bone matrix formation in cultures of fetal rat calvarial osteoblasts Calcif. Tissue Int. 60 1997 283 290
28. E. Abe, M. Yamamoto, Y. Taguchi, B. Lecka-Czernik, C.A. O'Brien, and A.N. Economides Essential requirement of BMPs-2/4 for both osteoblast and osteoclast formation in murine bone marrow cultures from adult mice: antagonism by noggin J. Bone Miner. Res. 15 2000 663 673
29. H. Sudo, H.A. Kodama, Y. Amagai, S. Yamamoto, and S. Kasai In vitro differentiation and calcification in a new clonal osteogenic cell line derived from newborn mouse calvaria J. Cell. Biol. 96 1883 191 198
30. L.D. Quarles, D.A. Yohay, L.W. Lever, R. Caton, and R.J. Wenstrup Distinct proliferative and differentiated stages of murine MC3T3-E1 cells in culture: an in vitro model of osteoblast development J. Bone Miner. Res. 7 1992 683 692
31. R.T. Franceschi, and B.S. Iyer Relationship between collagen synthesis and expression of the osteoblast phenotype in MC3T3-E1 cells J. Bone Miner. Res. 7 1992 235 246
32. D. Wang, K. Christensen, K. Chawla, G. Xiao, P.H. Krebsbach, and R.T. Franceschi Isolation and characterization of MC3T3-E1 preosteoblast subclones with distinct in vitro and in vivo differentiation/mineralization potential J. Bone Miner. Res. 14 1999 893 903
33. G. Xiao, Y. Cui, P. Ducy, G. Karsenty, and R.T. Franceschi Ascorbic acid-dependent activation of the osteocalcin promoter in MC3T3-E1 preosteoblasts: requirement for collagen matrix synthesis and the presence of an intact OSE2 sequence Mol. Endocrinol. 11 1997 1103 1113
34. R. Gopalakrishnan, H. Ouyang, M.J. Somerman, L.K. McCauley, and R.T. Franceschi Matrix gamma-carboxyglutamic acid protein is a key regulator of PTH-mediated inhibition of mineralization in MC3T3-E1 osteoblast-like cells Endocrinology 142 2001 4379 4388
35. P.S. Thomas Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose Proc. Natl. Acad. Sci. U. S. A. 77 1980 5201 5205
36. A.J. Celeste, V. Rosen, J.L. Buecker, R. Kriz, E.A. Wang, and J.M. Wozney Isolation of the human gene for bone gla protein utilizing mouse and rat cDNA clones EMBO J. 5 1986 1885 1890
37. M.F. Young, K. Ibaraki, J.M. Kerr, M.S. Lyu, and C.A. Kozak Murine bone sialoprotein (BSP): cDNA cloning, mRNA expression, and genetic mapping Mamm. Genome 5 1994 108 111
38. M.E. Marsh, A.M. Munne, J.J. Vogel, Y. Cui, and R.T. Franceschi Mineralization of bone-like extracellular matrix in the absence of functional osteoblasts J. Bone Miner. Res. 10 1995 1635 1643
39. R.T. Franceschi, W.M. James, and G. Zerlauth 1,25-Dihydroxyvitamin D3 specific regulation of growth, morphology, and fibronectin in a human osteosarcoma cell line J. Cell. Physiol. 123 1985 401 409
40. E. Gazzerro, V. Gangji, and E. Canalis Bone morphogenetic proteins induce the expression of noggin, which limits their activity in cultured rat osteoblasts J. Clin. Invest. 102 1998 2106 2114
41. M.R. Urist Bone: formation by autoinduction Science 150 1965 893 899
42. S.D. Boden, J. Kang, H. Sandhu, and J.G. Heller Use of recombinant human bone morphogenetic protein-2 to achieve posterolateral lumbar spine fusion in humans: a prospective, randomized clinical pilot trial: 2002 Volvo Award in clinical studies Spine 27 2002 2662 2673
43. M. Kos, K. Luczak, M. Matusiewicz, M. Krzystek-Korpacka, and M. Rapala Perspectives of clinical application of bone morphogenetic proteins in children Eur. J. Pediatr. Surg. 12 2002 272 277
44. G.N. King, and D.L. Cochran Factors that modulate the effects of bone morphogenetic protein-induced periodontal regeneration: a critical review J. Periodontol. 73 2002 925 936
45. N. Abe, Y.P. Lee, M. Sato, X. Zhang, J. Wu, and K. Mitani Enhancement of bone repair with a helper-dependent adenoviral transfer of bone morphogenetic protein-2 Biochem. Biophys. Res. Commun. 297 2002 523 527
46. A.B. Shafritz, E.M. Shore, F.H. Gannon, M.A. Zasloff, R. Taub, and M. Muenke Overexpression of an osteogenic morphogen in fibrodysplasia ossificans progressiva N. Engl. J. Med. 335 1996 555 561
47. F.S. Kaplan, D.L. Glaser, N. Hebela, and E.M. Shore Heterotopic ossification J. Am. Acad. Orthop. Surg. 12 2004 116 125
48. R.C. Pereira, A.N. Economides, and E. Canalis Bone morphogenetic proteins induce gremlin, a protein that limits their activity in osteoblasts Endocrinology 141 2000 4558 4563
49. R.D. Devlin, Z. Du, R.C. Pereira, R.B. Kimble, A.N. Economides, and V. Jorgetti Skeletal overexpression of noggin results in osteopenia and reduced bone formation Endocrinology 144 2003 1972 1978
50. E. Gazzerro, Z. Du, R.D. Devlin, S. Rydziel, L. Priest, and A.N. Economides Noggin arrests stromal cell differentiation in vitro Bone 32 2003 111 119
51. L.J. Brunet, J.A. McMahon, A.P. McMahon, and R.M. Harland Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton Science 280 1998 1455 1457
52. I. Kalajzic, Z. Kalajzic, M.M. Hurley, A.C. Lichtler, and D.W. Rowe Stage specific inhibition of osteoblast lineage differentiation by FGF2 and noggin J. Cell. Biochem. 88 2003 1168 1176
53. A. Petryk, R.M. Anderson, M.P. Jarcho, I. Leaf, C.S. Carlson, and J. Klingensmith The mammalian twisted gastrulation gene functions in foregut and craniofacial development Dev. Biol. 267 2004 374 386
54. T. Nosaka, S. Morita, H. Kitamura, H. Nakajima, F. Shibata, and Y. Morikawa Mammalian twisted gastrulation is essential for skeleto-lymphogenesis Mol. Cell. Biol. 23 2003 2969 2980
55. L. Zakin, and E.M. De Robertis Inactivation of mouse Twisted gastrulation reveals its role in promoting Bmp4 activity during forebrain development Development 131 2004 413 424
56. K. Yu, S. Srinivasan, O. Shimmi, B. Biehs, K.E. Rashka, and D. Kimelman Processing of the Drosophila Sog protein creates a novel BMP inhibitory activity Development 127 2000 2143 2154
57. I.C. Scott, I.L. Blitz, W.N. Pappano, Y. Imamura, T.G. Clark, and B.M. Steiglitz Mammalian BMP-1/Tolloid-related metalloproteinases, including novel family member mammalian Tolloid-like 2, have differential enzymatic activities and distributions of expression relevant to patterning and skeletogenesis Dev. Biol. 213 1999 283 300
58. K. Takahara, G.E. Lyons, and D.S. Greenspan Bone morphogenetic protein-1 and a mammalian tolloid homologue (mTld) are encoded by alternatively spliced transcripts which are differentially expressed in some tissues J. Biol. Chem. 269 1994 32572 32578
59. K. Takahara, R. Brevard, G.G. Hoffman, N. Suzuki, and D.S. Greenspan Characterization of a novel gene product (mammalian tolloid-like) with high sequence similarity to mammalian tolloid/bone morphogenetic protein-1 Genomics 34 1996 157 165
60. O. Shimmi, and M.B. O'Connor Physical properties of Tld, Sog, Tsg and Dpp protein interactions are predicted to help create a sharp boundary in Bmp signals during dorsoventral patterning of the Drosophila embryo Development 130 2003 4673 4682