Noggin regulation of bone morphogenetic protein (BMP) 2/7 heterodimer activity in vitro

Bone

Volumn 39, Issue 1, 2006, Pages 61-71

  Zhu, Wei ^a   Kim, Jaehon ^a   Cheng, Christina ^a   Rawlins, Bernard A ^a   Boachie Adjei, Oheneba ^a   Crystal, Ronald G ^b   Hidaka, Chisa ^a  

^a HOSPITAL FOR SPECIAL SURGERY   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Bone morphogenetic protein; Fusion gene; Homodimer and heterodimer; Noggin; Osteoblastic differentiation

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; HETERODIMER; NOGGIN; OSTEOCALCIN; OSTEOGENIC PROTEIN 1;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; FUSION GENE; GENE CONSTRUCT; GENE SYNTHESIS; GENETIC CODE; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; MYOBLAST; NONHUMAN; OSSIFICATION; OSTEOBLAST; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN SYNTHESIS INHIBITION; PROTEIN SYNTHESIS REGULATION; WESTERN BLOTTING;

ALKALINE PHOSPHATASE; ANIMALS; BIOLOGICAL MARKERS; BONE MORPHOGENETIC PROTEINS; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINE; DIMERIZATION; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE FUSION; HUMANS; MICE; OSTEOBLASTS; OSTEOCALCIN; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 33744785946     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2005.12.018     Document Type: Article

References (62)

1. Urist M.R. Bone: formation by autoinduction. Science 150 (1965) S893-S899
2. Celeste A.J., Iannazzi J.A., Taylor R.C., Hewick R.M., Rosen V., Wang E.A., et al. Identification of transforming growth factor beta family members present in bone-inductive protein purified from bovine bone. Proc. Natl. Acad. Sci. U. S. A. 87 24 (1990) 9843-9847
3. Helder M.N., Ozkaynak E., Sampath K.T., Luyten F.P., Latin V., Oppermann H., et al. Expression pattern of osteogenic protein-1 (bone morphogenetic protein-7) in human and mouse development. J. Histochem. Cytochem. 43 10 (1995) 1035-1044
4. Reddi A.H. Role of morphogenetic proteins in skeletal tissue engineering and regeneration. Nat. Biotechnol. 16 3 (1998) 247-252
5. Reddi A.H. Interplay between bone morphogenetic proteins and cognate binding proteins in bone and cartilage development: noggin, chordin and DAN. Arthritis Res. 3 1 (2001) 1-5
6. Sampath T.K., Coughlin J.E., Whetstone R.M., Banach D., Corbett C., Ridge R.J., et al. Bovine osteogenic protein is composed of dimers of OP-1 and BMP-2A, two members of the transforming growth factor-beta superfamily. J. Biol. Chem. 265 22 (1990) 13198-131205
7. Sampath T.K., Maliakal J.C., Hauschka P.V., Jones W.K., Sasak H., Tucker R.F., et al. 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 28 (1992) 20352-20362
8. Schmitt J.M., Hwang K., Winn S.R., and Hollinger J.O. Bone morphogenetic proteins: an update on basic biology and clinical relevance. J. Orthop. Res. 17 2 (1999) 269-278
9. Wozney J.M. Overview of bone morphogenetic proteins. Spine 27 16 Suppl. 1 (2002) S2-S8
10. Wozney J.M., and Rosen V. Bone morphogenetic protein and bone morphogenetic protein gene family in bone formation and repair. Clin. Orthop. 346 (1998) 26-37
11. Higuchi C., Myoui A., Hashimoto N., Kuriyama K., Yoshioka K., Yoshikawa H., et al. Continuous inhibition of MAPK signaling promotes the early osteoblastic differentiation and mineralization of the extracellular matrix. J. Bone Miner. Res. 17 10 (2002) 1785-1794
12. Kawabata M., Imamura T., and Miyazono K. Signal transduction by bone morphogenetic proteins. Cytokine Growth Factor Rev. 9 (1998) 49-61
13. Kawabata M., and Miyazono K. Bone morphogenetic proteins. In: Canalis E. (Ed). Skeletal Growth Factors (2000), Lippincott, Williams and Wilkins, Philadelphia 269-290
14. Kretzschmar M., and Massague J. Smads: mediators and regulators of TGF-beta signaling. Curr. Opin. Genet. Dev. 8 (1998) 103-111
15. Miyazono K. Signal transduction by bone morphogenetic protein receptors: functional roles of Smads proteins. Bone 25 (1999) 91-93
16. Nohe A., Hassel S., Enrlich M., Neubauer F., Sebald W., Henis Y.I., et al. The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP2 signaling pathways. J. Biol. Chem. 277 (2002) 5330-5338
17. Gazzerro E., Gangji V., and Canalis E. Bone morphogenetic proteins induce the expression of noggin, which limits their activity in cultured rat osteoblasts. J. Clin. Invest. 102 12 (1998) 2106-2114
18. Abe E., Yamamoto M., Taguchi Y., Lecka-Czernik B., O'Brien C.A., Economides A.N., et al. 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 4 (2000) 663-673
19. Hanaoka E., Ozaki T., Nakamura Y., Moriya H., Nakagawara A., and Sakiyama S. Overexpression of DAN causes a growth suppression in p53-deficient SAOS-2 cells. Biochem. Biophys. Res. Commun. 278 1 (2000) 20-26
20. Pereira R.C., Economides A.N., and Canalis E. Bone morphogenetic proteins induce gremlin, a protein that limits their activity in osteoblasts. Endocrinology 141 12 (2000) 4558-4563
21. Balemans W., and Van Hul W. Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol. 250 2 (2002) 231-250
22. Winkler D.G., Yu C., Geoghegan J.C., Ojala E.W., Skonier J.E., Shpektor D., et al. Noggin and sclerostin bone morphogenetic protein antagonists form a mutually inhibitory complex. J. Biol. Chem. 279 35 (2004) 36293-36298
23. Avsian-Kretchmer O., and Hsueh A.J. Comparative genomic analysis of the eight-membered ring cystine knot-containing bone morphogenetic protein antagonists. Mol. Endocrinol. 18 1 (2004) 1-12
24. Groppe J., Greenwald J., Wiater E., Rodriguez-Leon J., Economides A.N., Kwiatkowski W., et al. Structural basis of BMP signalling inhibition by the cystine knot protein Noggin. Nature 420 6916 (2002) 636-642
25. Groppe J., Greenwald J., Wiater E., Rodriguez-Leon J., Economides A.N., Kwiatkowski W., et al. Structural basis of BMP signaling inhibition by Noggin, a novel twelve-membered cystine knot protein. J. Bone Jt. Surg., Am. 85-A Suppl. 3 (2003) 52-58
26. Katagiri T., Yamaguchi A., Komaki M., Abe E., Takahashi N., Ikeda T., et al. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J. Cell Biol. 127 6 Pt. 1 (1994) 1755-1766
27. Yeh L.C., Tsai A.D., and Lee J.C. Osteogenic protein-1 (OP-1, BMP-7) induces osteoblastic cell differentiation of the pluripotent mesenchymal cell line C2C12. J. Cell Biochem. 87 (2002) 292-304
28. Zlotolow D.A., Vaccaro A.R., and Salamon M.L. The role of human bone morphogenetic proteins in spinal fusion. J. Am. Acad. Orthop. Surg. 8 (2000) 3-9
29. Cook S.D. Preclinical and clinical evaluation of osteogenic protein-1 (BMP-7) in bony sites. Orthopedics 22 7 (1999) 669-671
30. Boden S.D., Hair G.A., Viggeswarapu M., Liu Y., and Titus L. Gene therapy for spine fusion. Clin. Orthop. 379 (2000) S225-S233 (Suppl.)
31. Boden S.D., Kang J., Sandhu H., and Heller J.G. 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 23 (2002) 2662-2673
32. Khan S.N., Hidaka C., Sandhu H.S., Girardi F.P., Cammisa Jr. F.P., and Diwan A.D. Gene therapy for spine fusion. Orthop. Clin. North Am. 31 3 (2000) 473-484
33. Khan S.N., Sandhu H.S., Lane J.M., Cammisa Jr. F.P., and Girardi F.P. Bone morphogenetic proteins: relevance in spine surgery. Orthop. Clin. North Am. 33 2 (2002) 447-463
34. Vaccaro A.R., Anderson D.G., and Toth C.A. Recombinant human osteogenic protein-1 (bone morphogenetic protein-7) as an osteoinductive agent in spinal fusion. Spine 27 16 Suppl. 1 (2002) S59-S65
35. Kanatani M., Sugimoto T., Kaji H., Kobayashi T., Nishiyama K., Fukase M., et al. Stimulatory effect of bone morphogenetic protein-2 on osteoclast-like cell formation and bone-resorping activity. J. Bone Miner. Res. 10 11 (1995) 1681-1690
36. Kaneko H., Arakawa T., Mano H., Kaneda T., Ogasawara A., Nakagawa M., et al. Direct stimulation of osteoclastic bone resorption by bone morphogenetic protein (BMP)-2 and expression of BMP receptors in mature osteoclasts. Bone 27 4 (2002) 479-486
37. Paramore C.G., Lauryssen C., Rauzzino M.J., Wadlington V.R., Palmer C.A., Brix A., et al. The safety of OP-1 for lumbar fusion with decompression - A canine study. Neurosurgery 44 5 (1999) 1151-1155
38. Panchision D.M., Pickel J.M., Studer L., Lee S.H., Turner P.A., Hazel T.G., et al. Sequential actions of BMP receptors control neural precursor cell production and fate. Genes Dev. 15 16 (2001) 2094-2110
39. Yabe T., Samuels I., and Schwartz J.P. Bone morphogenetic proteins BMP-6 and BMP-7 have differential effects on survival and neurite outgrowth of cerebellar granule cell neurons. J. Neurosci. Res. 68 2 (2002) 161-168
40. Yanagisawa M., Takizawa T., Ochiai W., Uemura A., Nakashima K., et al. Fate alteration of neuroepithelial cells from neurogenesis to astrocytogenesis by bone morphogenetic proteins. Neurosci. Res. 41 4 (2001) 391-396
41. Israel D.I., Nove J., Kerns K.M., Kaufman R.J., Rosen V., Cox K.A., et al. Heterodimeric bone morphogenetic proteins show enhanced activity in vitro and in vivo. Growth Factors 13 3-4 (1996) 291-300
42. Aono A., Hazama M., Notoya K., Taketomi S., Yamasaki H., Tsukuda R., et al. Potent ectopic bone-inducing activity of bone morphogenetic protein-4/7 heterodimer. Biochem. Biophys. Res. Commun. 210 3 (1995) 670-677
43. Hazama M., Aono A., Ueno N., and Fujisawa Y. Efficient expression of a heterodimer of bone morphogenetic protein subunits using a baculovirus expression system. Biochem. Biophys. Res. Commun. 209 3 (1995) 859-866
44. Zhu W., Rawlins B.A., Boachie-Adjei O., Myers E.J., Arimizu J., Choi E., et al. Combined bone morphogenetic protein-2 and -7 gene transfer enhances osteoblastic differentiation and spine fusion in a rodent model. J. Bone Miner. Res. 19 12 (2004) 2021-2032
45. Qin Y.L., Yu D.Y., and Wei Q. Function and structure of recombinant single chain calcineurin. Biochem. Biophys. Res. Commun. 308 1 (2003) 87-93
46. Zimmerman L.B., De Jesus-Escobar J.M., and Harland R.M. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86 4 (1996) 599-606
47. Israel D.I., Nove J., Kerns K.M., Moutsatsos I.K., and Kaufman R.J. Expression and characterization of bone morphogenetic protein-2 in Chinese hamster ovary cells. Growth Factors 7 2 (1992) 139-150
48. Wang E.A., Rosen V., D'Alessandro J.S., Bauduy M., Cordes P., Harada T., et al. Recombinant human bone morphogenetic protein induces bone formation. Proc. Natl. Acad. Sci. U. S. A. 87 6 (1990) 2220-2224
49. Jones W.K., Richmond E.A., White K., Sasak H., Kusmik W., Smart J., et al. Osteogenic protein-1 (OP-1) expression and processing in Chinese hamster ovary cells: isolation of a soluble complex containing the mature and pro-domains of OP-1. Growth Factors 11 3 (1994) 215-225
50. Griffith D.L., Keck P.C., Sampath T.K., Rueger D.C., and Carlson W.D. Three-dimensional structure of recombinant human osteogenic protein1: structural paradigm for the transforming growth factor beta superfamily. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 878-883
51. Scheufler C., Sebald W., and Hulsmeyer M. Crystal structure of human bone morphogenetic protein-2 at 2.7A resolution. J. Mol. Biol. 287 (1999) 103-115
52. Ahn J., Serrano de la Pena L., Shore E.M., and Kaplan F.S. Paresis of a bone morphogenetic protein-antagonist response in a genetic disorder of heterotopic skeletogenesis. J. Bone Jt. Surg., Am. 85-A 4 (2003) 667-674
53. Glaser D.L., Economides A.N., Wang L., Liu X., Kimble R.D., Fandl J.P., et al. In vivo somatic cell gene transfer of an engineered Noggin mutein prevents BMP4-induced heterotopic ossification. J. Bone Jt. Surg., Am. 85-A 12 (2003) 2332-2342
54. Weber F.E., Schmokel H., Oelgeschlager M., Nickel J., Maly F.E., Hortschansky P., et al. Deletion mutants of BMP folding variants act as BMP antagonists and are efficient inhibitors for heterotopic ossification. J. Bone Miner. Res. 18 12 (2003) 2142-2151
55. Wozney J.M., Rosen V., Celeste A.J., Mitsock L.M., Whitters M.J., Kriz R.W., et al. Novel regulators of bone formation: molecular clones and activities. Science 242 (1998) 1528-1534
56. Lyons K.M., Hogan B.L., and Robertson E.J. Colocalization of BMP 7 and BMP 2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech. Dev. 50 (1995) 71-83
57. Katagiri T., Boorla S., Frendo J.L., Hogan B.L., and Karsenty G. Skeletal abnormalities in doubly heterozygous Bmp4 and Bmp7 mice. Dev. Genet. 22 (1998) 340-348
58. Solloway M.J., and Robertson E.J. Early embryonic lethality in BmpBmp7 double mutant mice suggests functional redundancy within the 60A subgroup. Development 126 5 (1999) 1753-1768
59. Ohyama Y., Nifuji A., Maeda Y., Amagasa T., and Noda M. Spatiotemporal association and BMP regulation of SOST and Osterix expression during embryonic osteogenesis. Endocrinology 145 10 (2004) 4685-4692
60. Van Bezooijen R.L., Roelen B.A., Visser A., Van Der Wee-Pals L., De Wilt E., Karperien M., et al. Sclerostin is an osteocyte-expressed negative regulator of bone formation, but not a classical BMP antagonist. J. Exp. Med. 199 6 (2004) 805-814
61. Winkler D.G., Sutherland M.K., Geoghegan J.C., Yu C., Hayes T., Skonier J.E., et al. Osteocyte control of bone formation via sclerostin, a novel BMP antagonist. EMBO J. 22 23 (2003) 6267-6276
62. Nickel J., Dreyer M.K., Kirsch T., and Sebald W. The crystal structure of the BMP-2: BMPR-IA complex and the generation of BMP-2 antagonists. J. Bone Jt. Surg., Am. 83-A Suppl. 1 (Pt. 1) (2001) S7-S14