The family of bone morphogenetic proteins

Kidney International

Volumn 57, Issue 6, 2000, Pages 2207-2214

  Ducy, Patricia ^a   Karsenty, Gerard ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Bone formation; Development; Gene mutation; Organogenesis; Skeleton; Transforming growth factor

Indexed keywords

BONE MORPHOGENETIC PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

BONE DEVELOPMENT; EPITHELIUM; HETEROTOPIC OSSIFICATION; HUMAN; MESENCHYME; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; REVIEW; SIGNAL TRANSDUCTION; SPONTANEOUS MUTATION; TISSUE INTERACTION;

EID: 0034128748     PISSN: 00852538     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1523-1755.2000.00081.x     Document Type: Article

References (94)

1. 1. URIST MR: Bone: Formation by autoinduction. Science 150:893-899, 1965
2. 2. URIST MR, IWATA H, CECCOTTI PL, DOREMAN RL, BOYD SD, MCDOWELI RM, CHIEN C: Bone morphogenesis in implants of insoluble bone gelatin. Proc Natl Acaid Sci USA 70:3511-3515, 1973
3. 3. URIST MR, MIKULSKI A, LIETZE A: Solubilized and insolubilized bone morphogenetic protein. Proc Natl Acad Sci USA 76:1828-1832, 1979
4. 4. REDDI AH: Regulation of cartilage and bone differentiation by bone morphogenetic proteins. Curr Opin Cell Biol 4:850-855,1992
5. 5. HORTON WA: Morphology of connective tissue: Cartilage, in Connective Tissue and Its Heritable Disorders, New York, Wiley-Liss, Inc., 1992, pp 73-84
6. 6. REDDI AH: Bone and cartilage differentiation. Curr Oppin Genet Dev 4:737-744, 1994
7. 7. WOZNEY JM, ROSEN V, CELESTE AJ, MITSOCK LM, WHITTERS MJ, KRIZ RW, HEWICK RM, WANG EA: Novel regulators of bone formation: Molecular clones and activities. Science 242:1528-1534, 1988
8. 8. SAMPATH TK, MUTHUKUMARAN N, REDDI AH: Isolation of osteogenin, an extracellular matrix-associated bone-inductive protein, by heparin affinity chromatography. Proc Natl Acad Sci USA 84:7109-7113, 1987
9. 9. WANG EA, ROSEN V, CORDES P, HEWICK RM, KRIZ MJ, LUXENBERG DP, SIBLEY BS, WOZNEY JM: Purification and characterization of other distinct bone-inducing factors. Proc Natl Acad Sci USA 85:9484-9488, 1988
10. 10. LUXENBERG DP, MCQUAID D, MOUSTATSOS IK, NOVE J, WOZNEY JM: Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci USA 87:2220-2224, 1990
11. 11. WANG EA, WOZNEY JM: Identification of transforming growth factor β family members present in bone-inductive protein purified from bovine bone. Proc Natl Acad Sci USA 87:9843-9847, 1990
12. 12. SAMPATH TK, MALIAKAL JC, HAUSCHKA PV, JONES WK, SASAK H, TUCKER RF, WHITE KH, COUGHLIN JE, TUCKER MM, PANG RH: 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, 1992
13. 13. WOZNEY JM: The bone morphogenetic protein family and osteogenesis. Mol Reprod Dev 32:160-167, 1992
14. 14. HARLAND RM: The transforming growth factor β family and induction of the vertebrate mesoderm: Bone morphogenetic proteins are ventral inducers. Proc Natl Acad Sci USA 91:10243-10246, 1994
15. 15. HOGAN BLM: Bone morphogenetic proteins: Multifunctional regulators of vertebrate development. Genes Dev 10:1580-1594, 1996
16. 16. REDDI AH: Bone morphogenetic proteins: An unconventional approach to isolation of first mammalian morphogens. Cytokine Growth Factor Rev 8:11-20, 1997
17. 17. GRAFF JM: Embryonic patterning: To BMP or not to BMP, that is the question. Cell 89:171-174, 1997
18. 18. EBENDAL T, BENGTSSON H, SODERSTROM S: Bone morphogenetic proteins and their receptors: Potential functions in the brain. J Neurosci Res 51:139-146, 1998
19. 19. WOZNEY JM: The bone morphogenetic protein family: Multifunctional cellular regulators in the embryo and adult. Eur J Oral Sci 106:160-166, 1998
20. 20. WOLFMAN NM, HATTESLEY G, COX K, CELESTE AJ, NELSON R, YAMAJI N, DUBE JL, DIBLASIO-SMITH E, NOVE J, SONG JJ, WOZNEY JM, ROSEN V: Ectopic induction of tendon and ligament in rats by growth and differentiation factors 5, 6, and 7, members of the TGF-beta gene family. J Clin Invest 100:321-330, 1997
21. 21. HAMMONDS RG JR, SCHWALL R, DUDLEY A, BERKEMEIER L, LAI C, LEE J, CUNNINGHAM N, REDDI AH, WOOD WI, MASON AJ: Bone-inducing activity of mature BMP-2b produced from a hybrid BMP-2a/2b precursor. Mol Endocrinol 5:149-155, 1991
22. 22. COX K, HOLTROP M, D'ALESSANDRO JS, WANG EA, WOZNEY JM, ROSEN V: Histological and ultrastructural comparison of the in vivo activities of rhBMP-2 and rhBMP-5. J Bone Miner Res 6:S155, 1991
23. 23. D'ALESSANDRO JS, COX KA, ISRAEL DI: Purification, characterization and activities of recombinant bone morphogenetic protein 5. J Bone Miner Res 6:S153, 1991
24. 24. GITELMAN SE, KOBRIN MS, YE J-Q, LOPEZ AR, LEE A, DERYNCK R: Recombinant Bgr-1 BMP-6-expressing tumors induce fibrosis and endochondral bone formation in vivo. J Cell Biol 126:1595-1609, 1994
25. 25. RUTHERFORD RB, SAMPATH TK, RUEGER DC, TAYLOR TD: Use of bovine osteogenic protein to promote rapid osseointegration of endosseous dental implants, Int J Oral Maxillofac Implants 7:297-301, 1992
26. 26. KINGSLEY DM: The TGF-β superfamily: New members, new receptors, and genetic tests of function in different organisms. Genes Dev 8:133-146, 1994
27. 27. ISRAEL DI, NOVE J, KERNS KM, MOUTSATSOS IK, KAUFMAN RJ: Expression and characterization of bone morphogenetic protein-2 in Chinese hamster ovary cells. Growth Factors 7:139-150, 1992
28. 28. CUI Y, JEAN F, THOMAS G, CHRISTIAN JL: BMP-4 is proteolytically activated by furin and/or PC6 during vertebrate embryonic development. EMBO J 17:4735-4743, 1998
29. 29. CONSTAM DB, ROBERTSON EJ: Regulation of bone morphogenetic protein activity by pro domains and proprotein convertases. J Cell Biol 144:139-149, 1999
30. 30. SCHLUNEGGER MP, GRUTTFR MG: An unusual feature revealed by the crystal structure at 2.2: A resolution of human transforming growth factor-beta 2. Nature 358:430-434, 1992
31. 31. DAOPIN S, PIFZ KA, OGAWA Y, DAVIES DR: Crystal structure of transforming growth factor-beta 2: An unusual fold for the superfamily. Science 257:369-373, 1992
32. 32. GRIFFITH DL, KECK PC, SAMPATH TK, RUEGER DC, CARLSON WD: Three-dimensional structure of recombinant human osteogenic protein 1: Structural paradigm for the transforming growth factor beta superfamily. Proc Natl Acad Sci USA 93:878-883, 1996
33. 33. MCPHERRON AC, LEE SJ: GDF-3 and GDF-9: Two new members of the transforming growth factor-beta superfamily containing a novel pattern of cysteines. J Biol Chem 268:3444-3449, 1993
34. 34. MASSAGUE J, WEIS-GARCIA F: Serine/threonine kinase receptors: Mediators of transforming growth factor beta family signals. Cancer Surv 27:41-64, 1996
35. 35. LIU F, VENTURA F, DOODY J, MASSAGUE J: Human type II receptor for bone morphogenic proteins (BMPs): Extension of the two-kinase receptor model to the BMPs. Mol Cell Biol 15:3479-3486, 1995
36. 36. RUBERTE E, MARTY T, NELLEN D, ATEOLTER M, BASLER K: An absolute requirement for both the type II and type I receptors, punt and thick veins, for dpp signaling in vivo. Cell 80:889-897, 1995
37. 37. HELDIN CH, MIYAZONO K, TEN DIJKE P: TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390: 465-471, 1997
38. 38. MASSAGUE J: TGF-beta signal transduction. Annu Rev Biochem 67:753-791, 1998
39. 39. LYONS KM, PELTON RW, HOGAN BL: Patterns of expression of murine Vgr-1 and BMP-2a RNA suggest that transforming growth factor-beta-like genes coordinately regulate aspects of embryonic development. Genes Dev 3:1657-1668, 1989
40. 40. LYONS KM, HOGAN BL, ROBERTSON EJ: Colocalization of BMP 7 and BMP 2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech Dev 50:71-83, 1995
41. 41. ZHANG H, BRADLEY A: Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122:2977-2986, 1996
42. 42. SCHULTHEISS TM, BURCH JBE, LASSAR AB: A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev 11:451-462, 1997
43. 43. DUDLEY AT, ROBERTSON EJ: Overlapping expression domains of bone morphogenetic protein family members potentially account for limited tissue defects in BMP7 deficient embryos. Dev Dyn 208:349-362, 1997
44. 44. LYONS KM, PELTON RW, HOGAN BL: Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for bone morphogenetic protein-2A (BMP-2A). Development 109: 833-844, 1990
45. 45. SOLLOWAY MJ, DUDLEY AT, BIKOFF EK, LYONS KM, HOGAN BL, ROBERTSON EJ: Mice lacking Bmp6 function. Dev Genet 22:321-339, 1998
46. 46. JONES CM, LYONS KM, HOGAN BL: Involvement of bone morphogenetic protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development 111:531-542, 1991
47. 47. JOHANSSON BM, WILES MV: Evidence for involvement of activin A and bone morphogenetic protein 4 in mammalian mesoderm and haematopoietic development. Mol Cell Biol 15:141-151, 1995
48. 48. WINNIER G, BLESSING M, LABOSKY PA, HOGAN BLM: Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 9:2105-2116, 1995
49. 49. OH SH, JOHNSON R, WU DK: Differential expression of bone morphogenetic proteins in the developing vestibular and auditory sensory organs. J Neurosci 16:6463-6475, 1996
50. 50. FURUTA Y, PISTON DW, HOGAN BL: Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124:2203-2212, 1997
51. 51. SOLLOWAY MJ, ROBERTSON EJ: Early embryonic lethality in Bmp5;Bmp7 double mutant mice suggests functional redundancy within the 60A subgroup. Development 126:1753-1768, 1999
52. 52. KING JA, MARKER PC, SEUNG KJ, KINGSLEY DM: BMP5 and the molecular, skeletal, and soft-tissue alterations in short ear mice. Dev Biol 166:112-122, 1994
53. 53. STORM EE, KINGSLEY DM: GDF5 coordinates bone and joint formation during digit development. Dev Biol 209:11-27, 1999
54. 54. FARRINGTON SM, BELAOUSSOFF M, BARON MH: Winged-helix, Hedgehog and BMP genes are differentially expressed in distinct cell layers of the murine yolk sac. Mech Dev 62:197-211, 1997
55. 55. IWASAKI M, LE AX, HELMS JA: Expression of Indian hedgehog, bone morphogenetic protein 6 and gli during skeletal morphogenesis. Mech Dev 69:197-202, 1997
56. 56. DUDLEY A, LYONS K, ROBERTSON EJ: A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev 9:2795-2807, 1995
57. 57. LUO G, HOFMANN C, BRONCKERS ALJ, SOHOCKI M, BRADLEY A, KARSENTY G: BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev 9:2808-2820, 1995
58. 58. MCGRATH SA, ESQUELA AF, LEE SJ: Oocyte-specific expression of growth/differentiation factor-9. Mol Endocrinol 9:131-136, 1995
59. 59. DONG J, ALBERTINI DF, NISHIMORI K, KUMAR TR, LU N, MATZUK MM: Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383:531-535, 1996
60. 60. FITZPATRICK SL, SINDONI DM, SHUGHRUE PJ, LANE MV, MERCHENTHALER U, FRAIL DE: Expression of growth differentiation factor-9 messenger ribonucleic acid in ovarian and nonovarian rodent and human tissues. Endocrinology 139:2571-2578, 1998
61. 61. MCPHERRON AC, LAWLER AM, LEE SJ: Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387:83-90, 1997
62. 62. NEUHAUS H, ROSEN V, THIES RS: Heart specific expression of mouse BMP-10 a novel member of the TGF-beta superfamily. Mech Dev 80:181-184, 1999
63. 63. LEE SJ: Expression of growth/differentiation factor 1 in the nervous system: Conservation of a bicistronic structure. Proc Natl Acad Sci USA 88:4250-4254, 1991
64. 64. LEE KJ, MENDELSOHN M, JESSELL TM: Neuronal patterning by BMPs: A requirement for GDF7 in the generation of a discrete class of commissural interneurons in the mouse spinal cord. Genes Dev 12:3394-3407, 1998
65. 65. NAKASHIMA M, TOYONO T, AKAMINE A, JOYNER A: Expression of growth/differentiation factor 11, a new member of the BMP/TGFβ superfamily during mouse embryogenesis. Mech Dev 80:185-189, 1999
66. 66. LYNCH CJ: Short ears, an autosomal mutation in the house mouse. Am Nat 55:421-426, 1921
67. 67. GREEN EL, GREEN MC: The development of three manifestations of the short ear gene in the mouse. J Morphol 70:1-19, 1942
68. 68. GREEN EL, GREEN MC: Effect of the short ear gene on number of ribs and presacral vertebrae in the house mouse. Am Nat 80:619-625, 1946
69. 69. GREEN MC: Further morphological effects of the short ear gene in the house mouse. J Morphol 88:1-22, 1951
70. 70. GREEN MC: Effects of the short ear gene in the mouse on cartilage formation in healing bone fractures. J Exp Zool 137:75-88, 1958
71. 71. GREEN MC: Mechanism of the pleiotropic effects of the short ear mutant gene in the mouse. J Exp Zool 167:129-150, 1968
72. 72. KINGSLEY DM, BLAND AE, GRUBBER JM, MARKER PC, RUSSELL LB, COPELAND NG, JENKINS NA: The mouse short ear skeletal morphogenesis locus is associated with defects in a bone morphogenetic member of the TGF beta superfamily. Cell 71:399-410, 1992
73. 73. MIKIC B, VAN DER MEULEN MC, KINGSLEY DM, CARTER DR: Mechanical and geometric changes in the growing femora of BMP-5 deficient mice. Bone 18:601-617, 1996
74. 74. LANDAUER W: Brachypodism, a recessive mutation of house mice. J Hered 43:293-298, 1952
75. 75. GRUNEBERG H, LEE AJ: The anatomy and development of brachypodism in the mouse. J Embryol Exp Morphol 30:119-141, 1973
76. 76. MALININA NA, KINDIAKOV BN, KONIUKHOV BV: Mutant gene expression in mouse aggregation chimeras. 3. Barachypodism-H gene. Ontogenes 15:514-521, 1984
77. 77. OWENS EM, SOLURSH M: Cell-cell interaction by mouse limb cells during in vitro chondrogenesis: Analysis of the brachypod mutation. Dev Biol 91:376-388, 1982
78. 78. STORM EE, HUYNH TV, COPELAND NG, JENKINS NA, KINGSLEY DM, LEE S-J: Limb alterations in brachypodism mice due to mutations in a new member of the TGFβ-superfamily. Nature 368:639-643, 1994
79. 79. MERINO R, MACIAS D, GANAN Y, ECONOMIDES AN, WANG X, WU Q, STAHL N, SAMPATH KT, VARONA P, HURLE JM: Expression and function of Gdf-5 during digit skeletogenesis in the embryonic chick leg bud. Dev Biol 206:33-45, 1999
80. 80. LANGER LO JR, CERVENKA J, CAMARGO M: A severe autosomal recessive acromesomelic dysplasia, the Hunter-Thompson type, and comparison with the Grebe type. Hum Genet 81:323-328, 1989
81. 81. THOMAS JT, LIN K, NANDEDKAR M, CAMARGO M, CERVENKA J, LUYTEN FP: A human chondrodysplasia due to a mutation in a TGF-beta superfamily member. Nat Genet 12:315-317, 1996
82. 82. THOMAS JT, KILPATRICK MW, LIN K, ERLACHER L, LEMBESSIS P, COSTA T, TSIPOURAS P, LUYTEN FP: Disruption of human limb morphogenesis by a dominant negative mutation in DCMP1. Nat Genet 17:58-64, 1997
83. 83. POLINKOVSKY A, ROBIN NH, THOMAS JT, IRONS M, LYNN A, GOODMAN FR, REARDON W, KANT SG, BRUNNER HG, VAN DER BURGT I, CHITAYAT D, MCCAUGHRAN J, DONNAI D, LUYTEN FP, WARMAN ML: Mutations in CDMP1 cause autosomal dominant brachydactyly type C. Nat Genet 17:18-19, 1997
84. 84. FRANCIS-WEST PH, ABDELFATTAH A, CHEN P, ALLEN C, PARISH J, LADHER R, ALLEN S, MACPHERSON S, LUYTEN FP, ARCHER CW: Mechanisms of GDF-5 action during skeletal development. Development 126:1305-1315, 1999
85. 85. BRUNET LJ, MCMAHON JA, MCMAHON AP, HARLAND RM: Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science 280:1455-1457, 1998
86. 86. GONG Y, KRAKOW D, MARCELINO J, WILKIN D, CHITAYAT D, BABULHIRJI R, HUDGINS L, CREMERS CW, CREMERS FP, BRUNNER HG, REINKER K, RIMOIN DL, COHN DH, GOODMAN FR, RFARDON W, PATION M, FRANCOMANO CA, WARMAN ML: Heterozygous mutations in the gene encoding noggin affect human joint morphogenesis. Nat Genet 21:302-304, 1999
87. 87. STORM EE, KINGSLEY DM: Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (BMP) family. Development 122:3969-3979, 1996
88. 88. TAKENOBU K, BOORLA S, FREWNDO J-L, HOGAN BLM, KARSENTY G: Skeletal abnormalities in doubly heterozygous Bmp4 and Bmp7 mice. Dev Genet 22:340-348, 1998
89. 89. FURUTA Y, HOGAN BLM: BMP4 is essential for lens induction in the mouse embryo. Genes Dev 12:3764-3775, 1998
90. 90. LAWSON KA, DUNN NR, ROELEN BA, ZEINSTRA LM, DAVIS AN, WRIGHT CV, KORVING JP, HOGAN L: Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 13:424-436, 1999
91. 91. KAMBADUR R, SHARMA M, SMITH TP, BASS JJ: Mutations in myostatin (GDF8) in double-muscled Belgian blue and piedmontese cattle. Genome Res 7:910-916, 1997
92. 92. ZHAO GQ, LIAW L, HOGAN BL: Bone morphogenetic protein 8A plays a role in the maintenance of spermatogenesis and the integrity of the epididymis. Development 125:1103-1112, 1998
93. 93. ZHAO GQ, DENG K, LABOSKY PA, LIAW L, HOGAN BL: The gene encoding bone morphogenetic protein 8B is required for the initiation and maintenance of spermatogenesis in the mouse. Genes Dev 10:1657-1669, 1996
94. 94. CARABATSOS MJ, ELVIN J, MATZUK MM, ALBERTINI DF: Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev Biol 204:373-384, 1998