BMP signalling in craniofacial development

International Journal of Developmental Biology

Volumn 50, Issue 6, 2006, Pages 511-521

  Nie, Xuguang ^a   Luukko, Keijo ^a   Kettunen, Paivi ^a  

^a UNIVERSITY OF BERGEN   (Norway)

Author keywords

Abnormality; Craniofacial development; Growth differentiation factor; Signalling

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXY 1 METHYLTETRALIN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 10; BONE MORPHOGENETIC PROTEIN 12; BONE MORPHOGENETIC PROTEIN 15; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 5; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN 8; BONE MORPHOGENETIC PROTEIN 9; GROWTH AND DIFFERENTIATION FACTOR 1; GROWTH DIFFERENTIATION FACTOR 10; GROWTH DIFFERENTIATION FACTOR 11; GROWTH DIFFERENTIATION FACTOR 3; GROWTH DIFFERENTIATION FACTOR 5; GROWTH DIFFERENTIATION FACTOR 6; GROWTH DIFFERENTIATION FACTOR 9; MYOSTATIN; OSTEOGENIC PROTEIN 1; OSTEOGENIN; PROTEIN ALK6; PROTEIN BMPRLL; PROTEIN LEFTY; PROTEIN NODAL; PROTIEN ALK2; UNCLASSIFIED DRUG;

APOPTOSIS; BONE DEVELOPMENT; BONE GROWTH; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CLEFT PALATE; CRANIOFACIAL DEVELOPMENT; DEVELOPMENTAL GENETICS; IN SITU HYBRIDIZATION; MUSCLE DEVELOPMENT; NEURAL CREST; NONHUMAN; ODONTOBLAST; PALATE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TOOTH DEVELOPMENT;

ANIMALS; BONE MORPHOGENETIC PROTEINS; FACIAL BONES; MICE; SIGNAL TRANSDUCTION; SKULL;

MAMMALIA; VERTEBRATA;

EID: 33746366789     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.052101xn     Document Type: Review

References (116)

1. ABERG, T., WOZNEY, J. and THESLEFF, I. (1997). Expression patterns of bone morphogenetic proteins (bmps) in the developing mouse tooth suggest roles in morphogenesis and cell differentiation. Dev Dyn 210: 383-96.
2. ACAMPORA, D., MERLO, G.R., PALEARI, L., ZEREGA, B., POSTIGLIONE, M.P., MANTERO, S., BOBER, E., BARBIERI, O., SIMEONE, A. and LEVI, G. (1999). Craniofacial, vestibular and bone defects in mice lacking the distal-less-related gene dlx5. Development 126: 3795-809.
3. ANDL, T., AHN, K., KAIRO, A., CHU, E.Y., WINE-LEE, L., REDDY, S.T., CROFT, N.J., CEBRA-THOMAS, J.A., METZGER, D., CHAMBON, P. et al. (2004). Epithelial bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development. Development 131: 2257-68.
4. BAHAMONDE, M.E. and LYONS, K.M. (2001). Bmp3: To be or not to be a bmp. J Bone Joint Surg Am 83-A Suppl 1: S56-62.
5. BARLOW, A.J. and FRANCIS-WEST, P.H. (1997). Ectopic application of recombinant bmp-2 and bmp-4 can change patterning of developing chick facial primordia. Development 124: 391-8.
6. BENNETT, J.H., HUNT, P. and THOROGOOD, P. (1995). Bone morphogenetic protein-2 and -4 expression during murine orofacial development. Arch Oral Biol 40: 847-54.
7. BEPPU, H., KAWABATA, M., HAMAMOTO, T., CHYTIL, A., MINOWA, O., NODA, T. and MIYAZONO, K. (2000). Bmp type ii receptor is required for gastrulation and early development of mouse embryos. Dev Biol 221: 249-58.
8. BYRON, C.D., BORKE, J., YU, J., PASHLEY, D., WINGARD, C.J. and HAMRICK, M. (2004). Effects of increased muscle mass on mouse sagittal suture morphology and mechanics. Anat Rec A Discov Mol Cell Evol Biol 279: 676-84.
9. CARICASOLE, A.A., VAN SCHAIK, R.H., ZEINSTRA, L.M., WIERIKX, C.D., VAN GURP, R.J., VAN DEN POL, M., LOOIJENGA, L.H., OOSTERHUIS, J.W., PERA, M.F., WARD, A. et al. (1998). Human growth-differentiation factor 3 (hgdf3): Developmental regulation in human teratocarcinoma cell lines and expression in primary testicular germ cell tumours. Oncogens 16: 95-103.
10. CHANG, S.C., CHUANG, H., CHEN, Y.R., YANG, L.C., CHEN, J.K., MARDINI, S., CHUNG, H.Y., LU, Y.L., MA, W.C., LOU, J. et al. (2004). Cranial repair using bmp-2 gene engineered bone marrow stromal cells. J Surg Res 119: 85-91.
11. CHEN, D., ZHAO, M., HARRIS, S.E. and MI, Z. (2004). Signal transduction and biological functions of bone morphogenetic proteins. Front Biosci 9: 349-58.
12. DALUISKI, A., ENGSTRAND, T., BAHAMONDE, M.E., GAMER, L.W., AGIUS, E., STEVENSON, S.L., COX, K., ROSEN, V. and LYONS, K.M. (2001). Bone morphogenetic protein-3 is a negative regulator of bone density. Nat Genet 27: 84-8.
13. DELATTE, M., VON DEN HOFF, J.W., VAN RHEDEN, R.E. and KUIJPERS-JAGTMAN, A.M. (2004). Primary and secondary cartilages of the neonatal rat: The femoral head and the mandibular condyle. Eur J Oral Sci 112: 156-62.
14. DEPEW, M.J., LIU, J.K., LONG, J.E., PRESLEY, R., MENESES, J.J., PEDERSEN, R.A. and RUBENSTEIN, J.L. (1999). Dlx5 regulates regional development of the branchial arches and sensory capsules. Development 126: 3831-46.
15. DEWULF, N., VERSCHUEREN, K., LONNOY, O., MOREN, A., GRIMSBY, S., VANDE SPIEGLE, K., MIYAZONO, K., HUYLEBROECK, D. and TEN DIJKE, P. (1995). Distinct spatial and temporal expression patterns of two type i receptors for bone morphogenetic proteins during mouse embryogenesis. Endocrinology 136: 2652-63.
16. DILEONE, R.J., KING, J.A., STORM, E.E., COPELAND, N.G., JENKINS, N.A. and KINGSLEY, D.M. (1997). The bmp8 gene is expressed in developing skeletal tissue and maps near the achondroplasia locus on mouse chromosome 4. Genomics 40: 196-8.
17. DUBE, J.L., WANG, P., ELVIN, J., LYONS, K.M., CELESTE, A.J. and MATZUK, M.M. (1998). The bone morphogenetic protein 15 gene is x-linked and expressed in oocytes. Mol Endocrinol 12: 1809-17.
18. DUDAS, M., SRIDURONGRIT, S., NAGY, A., OKAZAKI, K. and KAARTINEN, V. (2004). Craniofacial defects in mice lacking bmp type i receptor alk2 in neural crest cells. Mech Dev 121: 173-82.
19. DUDLEY, A.T., LYONS, K.M. and ROBERTSON, E.J. (1995). A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev 9: 2795-807.
20. DUDLEY, A.T. and ROBERTSON, E.J. (1997). Overlapping expression domains of bone morphogenetic protein family members potentially account for limited tissue defects in bmp7 deficient embryos. Dev Dyn 208: 349-62.
21. DUPREZ, D., BELL, E.J., RICHARDSON, M.K., ARCHER, C.W., WOLPERT, L., BRICKELL, P.M. and FRANCIS-WEST, P.H. (1996a). Overexpression of bmp-2 and bmp-4 alters the size and shape of developing skeletal elements in the chick limb. Mech Dev 57: 145-57.
22. DUPREZ, D.M., COLTEY, M., AMTHOR, H., BRICKELL, P.M. and TICKLE, C. (1996b). Bone morphogenetic protein-2 (bmp-2) inhibits muscle development and promotes cartilage formation in chick limb bud cultures. Dev Biol 174: 448-52.
23. EAMES, B.F. and HELMS, J.A. (2004). Conserved molecular program regulating cranial and appendicular skeletogenesis. Dev Dyn 231: 4-13.
24. FRANCIS-WEST, P., LADHER, R., BARLOW, A. and GRAVESON, A. (1998). Signalling interactions during facial development. Mech Dev 75: 3-28.
25. FRANCIS-WEST, P.H., TATLA, T. and BRICKELL, P.M. (1994). Expression patterns of the bone morphogenetic protein genes bmp-4 and bmp-2 in the developing chickface suggest a role in outgrowth of the primordia. Dev Dyn 201: 168-78.
26. GATO, A., MARTINEZ, M.L., TUDELA, C., ALONSO, I., MORO, J.A., FORMOSO, M.A., FERGUSON, M.W. and MARTINEZ-ALVAREZ, C. (2002). Tgf-beta(3)-induced chondroitin sulphate proteoglycan mediates palatal shelf adhesion. Dev Biol 250: 393-405.
27. GONG, S.G. and GUO, C. (2003). Bmp4 gene is expressed at the putative site of fusion in the midfacial region. Differentiation 71: 228-36.
28. GRAHAM, A., FRANCIS-WEST, P., BRICKELL, P. and LUMSDEN, A. (1994). The signalling molecule bmp4 mediates apoptosis in the rhombencephalic neural crest. Nature 372: 684-6.
29. GU, Z., REYNOLDS, E.M., SONG, J., LEI, H., FEIJEN, A., YU, L., HE, W., MACLAUGHLIN, D.T., VAN DEN EIJNDEN-VAN RAAIJ, J., DONAHOE, P.K. et al. (1999). The type i serine/threonine kinase receptor actria (alk2) is required for gastrulation of the mouse embryo. Development 126: 2551-61.
30. GUHA, U., GOMES, W.A., KOBAYASHI, T., PESTELL, R.G. and KESSLER, J.A. (2002). In vivo evidence that bmp signaling is necessary for apoptosis in the mouse limb. Dev Biol 249: 108-20.
31. HAN, B., PERELMAN, N., TANG, B., HALL, F., SHORS, E.C. and NIMNI, M.E. (2002). Collagen-targeted bmp3 fusion proteins arrayed on collagen matrices or porous ceramics impregnated with type i collagen enhance osteogenesis in a rat cranial defect model. J Orthop Res 20: 747-55.
32. HELMS, J.A. and SCHNEIDER, R.A. (2003). Cranial skeletal biology. Nature 423: 326-31.
33. HOLLEVILLE, N., QUILHAC, A., BONTOUX, M. and MONSORO-BURQ, A.H. (2003). Bmp signals regulate dlx5 during early avian skull development. Dev Biol 257: 177-89.
34. HUANG, R., LANG, E.R., OTTO, W.R., CHRIST, B. and PATEL, K. (2001). Molecular and cellular analysis of embryonic avian tongue development. Anat Embryol (Berl) 204: 179-87.
35. INADA, M., KATAGIRI, T., AKIYAMA, S., NAMIKA, M., KOMAKI, M., YAMAGUCHI, A., KAMOI, K., ROSEN, V. and SUDA, T. (1996). Bone morphogenetic protein-12 and -13 inhibit terminal differentiation of myoblasts, but do not induce their differentiation into osteoblasts. Biochem Biophys Res Commun 222: 317-22.
36. IOHARA, K., NAKASHIMA, M., ITO, M., ISHIKAWA, M., NAKASIMA, A. and AKAMINE, A. (2004). Dentin regeneration by dental pulp stem cell therapy with recombinant human bone morphogenetic protein 2. J Dent Res 83: 590-5.
37. JENA, N., MARTIN-SEISDEDOS, C., MCCUE, P. and CROCE, C.M. (1997). Bmp7 null mutation in mice: Developmental defects in skeleton, kidney and eye. Exp Cell Res 230: 28-37.
38. KAN, L., HU, M., GOMES, W.A. and KESSLER, J.A. (2004). Transgenic mice overexpressing bmp4 develop a fibrodysplasia ossificans progressiva (fop)-like phenotype. Am J Pathol 165: 1107-15.
39. KANZLER, B., FOREMAN, R.K., LABOSKY, P.A. and MALLO, M. (2000). Bmp signaling is essential for development of skeletogenic and neurogenic cranial neural crest. Development 127: 1095-104.
40. KARSENTY, G. (1999). The genetic transformation of bone biology. Genes Dev 13: 3037-51.
41. KARSENTY, G. (2003). The complexities of skeletal biology. Nature 423: 316-8.
42. KIM, H.J., RICE, D.P., KETTUNEN, P.J. and THESLEFF, I. (1998). Fgf-, bmp- and shh-mediated signalling pathways in the regulation of cranial suture morphogenesis and calvarial bone development. Development 125: 1241-51.
43. KING, J.A., MARKER, P.C., SEUNG, K.J. and KINGSLEY, D.M. (1994). Bmp5 and the molecular, skeletal and soft-tissue alterations in short ear mice. Dev Biol 166: 112-22.
44. KINGSLEY, D.M., BLAND, A.E., GRUBBER, J.M., MARKER, P.C., RUSSELL, L.B., COPELAND, N.G. and JENKINS, N.A. (1992). 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.
45. KISHIGAMI, S. and MISHINA, Y. (2005). Bmp signaling and early embryonic patterning. Cytokine Growth Factor Rev 16: 265-78.
46. KNECHT, A.K. and BRONNER-FRASER, M. (2002). Induction of the neural crest: A multigene process. Nat Rev Genet 3: 453-61.
47. KULESA, P., ELLIES, D.L. and TRAINOR, P.A. (2004). Comparative analysis of neural crest cell death, migration and function during vertebrate embryogenesis. Dev Dyn 229: 14-29.
48. LEE, K.J., MENDELSOHN, M. and JESSELL, T.M. (1998). 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: 3394-407.
49. LIEBERMAN, J.R., DALUISKI, A., STEVENSON, S., WU, L., MCALLISTER, P., LEE, Y.P., KABO, J.M., FINERMAN, G.A., BERK, A.J. and WITTE, O.N. (1999). The effect of regional gene therapy with bone morphogenetic protein-2-producing bone-marrow cells on the repair of segmental femoral defects in rats. J Bone Joint Surg Am 81: 905-17.
50. LIEBERMAN, J.R., LE, L.Q., WU, L., FINERMAN, G.A., BERK, A., WITTE, O.N. and STEVENSON, S. (1998). Regional gene therapy with a bmp-2-producing murine stromal cell line induces heterotopic and orthotopic bone formation in rodents. J Orthop Res 16: 330-9.
51. LIEM, K.F., JR., TREMML, G., ROELINK, H. and JESSELL, T.M. (1995). Dorsal differentiation of neural plate cells induced by bmp-mediated signals from epidermal ectoderm. Cell 82: 969-79.
52. LIU, W., SUN, X., BRAUT, A., MISHINA, Y., BEHRINGER, R.R., MINA, M. and MARTIN, J.F. (2005). Distinct functions for bmp signaling in lip and palate fusion in mice. Development 132: 1453-61.
53. LOPEZ-COVIELLA, I., BERSE, B., KRAUSS, R., THIES, R.S. and BLUSZTAJN, J.K. (2000). Induction and maintenance of the neuronal cholinergic phenotype in the central nervous system by bmp-9. Science 289: 313-6.
54. LU, H., JIN, Y. and TIPOE, G.L. (2000). Alteration in the expression of bone morphogenetic protein-2,3,4,5 mrna during pathogenesis of cleft palate in balb/c mice. Arch Oral Biol 45: 133-40.
55. LUO, G., HOFMANN, C., BRONCKERS, A.L., SOHOCKI, M., BRADLEY, A. and KARSENTY, G. (1995). Bmp-7 is an inducer of nephrogenesis and is also required for eye development and skeletal patterning. Genes Dev 9: 2808-20.
56. MACIAS, D., GANAN, Y., SAMPATH, T.K., PIEDRA, M.E., ROS, M.A. and HURLE, J.M. (1997). Role of bmp-2 and op-1 (bmp-7) in programmed cell death and skeletogenesis during chick limb development. Development 124: 1109-17.
57. MARAZZI, G., WANG, Y. and SASSOON, D. (1997). Msx2 is a transcriptional regulator in the bmp4-mediated programmed cell death pathway. Dev Biol 186: 127-38.
58. MCPHERRON, A.C., LAWLER, A.M. and LEE, S.J. (1997). Regulation of skeletal muscle mass in mice by a new tgf-beta superfamily member. Nature 387:83-90.
59. MCPHERRON, A.C., LAWLER, A.M. and LEE, S.J. (1999). Regulation of anterior/posterior patterning of the axial skeleton by growth/differentiation factor 11. Nat Genet 22: 260-4.
60. MILLER, A.F., HARVEY, S.A., THIES, R.S. and OLSON, M.S. (2000). Bone morphogenetic protein-9. An autocrine/paracrine cytokine in the liver. J Biol Chem 275: 17937-45.
61. MININA, E., KRESCHEL, C., NASKI, M.C., ORNITZ, D.M. and VORTKAMP, A. (2002). Interaction of fgf, ihh/pthlh and bmp signaling integrates chondrocyte proliferation and hypertrophic differentiation. Dev Cell 3: 439-49.
62. MININA, E., WENZEL, H.M., KRESCHEL, C., KARP, S., GAFFIELD, W., MCMAHON, A.P. and VORTKAMP, A. (2001). Bmp and ihh/pthrp signaling interact to coordinate chondrocyte proliferation and differentiation. Development 128: 4523-34.
63. MISHINA, Y., CROMBIE, R., BRADLEY, A. and BEHRINGER, R.R. (1999). Multiple roles for activin-like kinase-2 signaling during mouse embryogenesis. Dev Biol 213: 314-26.
64. MISHINA, Y., SUZUKI, A., UENO, N. and BEHRINGER, R.R. (1995). Bmpr encodes a type i bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev 9: 3027-37.
65. MUSGRAVE, D.S., PRUCHNIC, R., WRIGHT, V., BOSCH, P., GHIVIZZANI, S.C., ROBBINS, P.D. and HUARD, J. (2001). The effect of bone morphogenetic protein-2 expression on the early fate of skeletal muscle-derived cells. Bone 28: 499-506.
66. NAKASHIMA, M. (1994). Induction of dentin formation on canine amputated pulp by recombinant human bone morphogenetic proteins (bmp)-2 and -4. J Dent Res 73: 1515-22.
67. NAKASHIMA, M. and REDDI, A.H. (2003). The application of bone morphogenetic proteins to dental tissue engineering. Nat Biotechnol 21: 1025-32.
68. NAKASHIMA, M., TOYONO, T., AKAMINE, A. and JOYNER, A. (1999). Expression of growth/differentiation factor 11, a new member of the bmp/tgfbeta superfamily during mouse embryogenesis. Mech Dev 80: 185-9.
69. NAKASHIMA, M., TOYONO, T., MURAKAMI, T. and AKAMINE, A. (1998). Transforming growth factor-beta superfamily members expressed in rat incisor pulp. Arch Oral Biol 43: 745-51.
70. NASKI, M.C., COLVIN, J.S., COFFIN, J.D. and ORNITZ, D.M. (1998). Repression of hedgehog signaling and bmp4 expression in growth plate cartilage by fibroblast growth factor receptor 3. Development 125: 4977-88.
71. NEUHAUS, H., ROSEN, V. and THIES, R.S. (1999). Heart specific expression of mouse bmp-10 a novel member of the tgf-beta superfamily. Mech Dev 80: 181-4.
72. NIE, X. (2005a). Apoptosis, proliferation and gene expression patterns in mouse developing tongue. Anat Embryol (Berl) 210: 125-32.
73. NIE, X. (2005b). Cranial base in craniofacial development: Developmental features, influence on facial growth, anomaly and molecular basis. Acta Odontol Scand 63: 127-35.
74. NIE, X.G. (2005c). [differential expression of bmp2, bmp4 and bmp3 in embryonic development of mouse anterior and posterior palate.]. Chin Med J (Engl) 118: 1710-6.
75. NODEN, D.M. (1983). The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. Am J Anat 168: 257-76.
76. NODEN, D.M. (1988). Interactions and fates of avian craniofacial mesenchyme. Development 103 Suppl: 121-40.
77. NOHE, A., KEATING, E., KNAUS, P. and PETERSEN, N.O. (2004). Signal transduction of bone morphogenetic protein receptors. Cell Signal 16: 291-9.
78. OMI, M., SATO-MAEDA, M. and IDE, H. (2000). Role of chondrogenic tissue in programmed cell death and bmp expression in chick limb buds. Int J Dev Biol 44: 381-8.
79. OZKAYNAK, E., SCHNEGELSBERG, P.N., JIN, D.F., CLIFFORD, G.M., WARREN, F.D., DRIER, E.A. and OPPERMANN, H. (1992). Osteogenic protein-2. A new member of the transforming growth factor-beta superfamily expressed early in embryogenesis. J Biol Chem 267: 25220-7.
80. RANKIN, C.T., BUNTON, T., LAWLER, A.M. and LEE, S.J. (2000). Regulation of left-right patterning in mice by growth/differentiation factor-1. Nat Genet 24: 262-5.
81. SATOKATA, I. and MAAS, R. (1994). Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat Genet 6: 348-56.
82. SCHUELKE, M., WAGNER, K.R., STOLZ, L.E., HUBNER, C., RIEBEL, T., KOMEN, W., BRAUN, T., TOBIN, J.F. and LEE, S.J. (2004). Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med 350: 2682-8.
83. SENA, K., MOROTOME, Y., BABA, O., TERASHIMA, T., TAKANO, Y. and ISHIKAWA, I. (2003). Gene expression of growth differentiation factors in the developing periodontium of rat molars. J Dent Res 82: 166-71.
84. SETTLE, S., MARKER, P., GURLEY, K., SINHA, A., THACKER, A., WANG, Y., HIGGINS, K., CUNHA, G. and KINGSLEY, D.M. (2001). The bmp family member gdf7 is required for seminal vesicle growth, branching morphogenesis and cytodifferentiation. Dev Biol 234: 138-50.
85. SETTLE, S.H., JR., ROUNTREE, R.B., SINHA, A., THACKER, A., HIGGINS, K. and KINGSLEY, D.M. (2003). Multiple joint and skeletal patterning defects caused by single and double mutations in the mouse gdf6 and gdf5 genes. Dev Biol 254: 116-30.
86. SHIBATA, S., SUZUKI, S., TENGAN, T., ISHII, M. and KURODA, T. (1996). A histological study of the developing condylar cartilage of the fetal mouse mandible using coronal sections. Arch Oral Biol 41: 47-54.
87. SHUM, L., WANG, X., KANE, A.A. and NUCKOLLS, G.H. (2003). Bmp4 promotes chondrocyte proliferation and hypertrophy in the endochondral cranial base. Int J Dev Biol 47: 423-31.
88. SOLLOWAY, M.J., DUDLEY, A.T., BIKOFF, E.K., LYONS, K.M., HOGAN, B.L. and ROBERTSON, E.J. (1998). Mice lacking bmp6 function. Dev Genet 22: 321-39.
89. SOLLOWAY, M.J. and ROBERTSON, E.J. (1999). Early embryonic lethality in bmp5;bmp7 double mutant mice suggests functional redundancy within the 60a subgroup. Development 126: 1753-68.
90. STORM, E.E., HUYNH, T.V., COPELAND, N.G., JENKINS, N.A., KINGSLEY, D.M. and LEE, S.J. (1994). Limb alterations in brachypodism mice due to mutations in a new member of the tgf beta-superfamily. Nature 368: 639-43.
91. STORM, E.E. and KINGSLEY, D.M. (1996). Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (bmp) family. Development 122: 3969-79.
92. SUZUKI, T., BESSHO, K., FUJIMURA, K., OKUBO, Y., SEGAMI, N. and IIZUKA, T. (2002). Regeneration of defects in the articular cartilage in rabbit temporomandibular joints by bone morphogenetic protein-2. Br J Oral Maxillofac Surg 40: 201-6.
93. TAKAHASHI, K., NUCKOLLS, G.H., TANAKA, O., SEMBA, I., TAKAHASHI, I., DASHNER, R., SHUM, L. and SLAVKIN, H.C. (1998). Adenovirus-mediated ectopic expression of msx2 in even-numbered rhombomeres induces apoptotic elimination of cranial neural crest cells in ovo. Development 125: 1627-35.
94. TEIXEIRA FILHO, F.L., BARACAT, E.G., LEE, T.H., SUH, C.S., MATSUI, M., CHANG, R.J., SHIMASAKI, S. and ERICKSON, G.F. (2002). Aberrant expression of growth differentiation factor-9 in oocytes of women with polycystic ovary syndrome. J Clin Endocrinol Metab 87: 1337-44.
95. TRAINOR, P.A., MELTON, K.R. and MANZANARES, M. (2003). Origins and plasticity of neural crest cells and their roles in jaw and craniofacial evolution. Int J Dev Biol 47: 541-53.
96. TRIBULO, C., AYBAR, M.J., NGUYEN, V.H., MULLINS, M.C. and MAYOR, R. (2003). Regulation of msx genes by a bmp gradient is essential for neural crest specification. Development 130: 6441-52.
97. TZAHOR, E., KEMPF, H., MOOTOOSAMY, R.C., POON, A.C., ABZHANOV, A., TABIN, C.J., DIETRICH, S. and LASSAR, A.B. (2003). Antagonists of wnt and bmp signaling promote the formation of vertebrate head muscle. Genes Dev 17: 3087-99.
98. URIST, M.R. (1965). Bone: Formation by autoinduction. Science 150: 893-9.
99. VAINIO, S., KARAVANOVA, I., JOWETT, A. and THESLEFF, I. (1993). Identification of bmp-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 75: 45-58.
100. WALL, N.A., CRAIG, E.J., LABOSKY, P.A. and KESSLER, D.S. (2000). Mesendoderm induction and reversal of left-right pattern by mouse gdf1, a vg1-related gene. Dev Biol 227: 495-509.
101. WILSON, J. and TUCKER, A.S. (2004). Fgf and bmp signals repress the expression of bapx1 in the mandibular mesenchyme and control the position of the developing jaw joint. Dev Biol 266: 138-50.
102. WINNIER, G., BLESSING, M., LABOSKY, P.A. and HOGAN, B.L. (1995). Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 9: 2105-16.
103. WOZNEY, J.M., ROSEN, V., CELESTE, A.J., MITSOCK, L.M., WHITTERS, M.J., KRIZ, R.W., HEWICK, R.M. and WANG, E.A. (1988). Novel regulators of bone formation: Molecular clones and activities. Science 242: 1528-34.
104. YAMASHIRO, T., TUMMERS, M. and THESLEFF, I. (2003). Expression of bone morphogenetic proteins and msx genes during root formation. J Dent Res 82: 172-6.
105. YI, S.E., DALUISKI, A., PEDERSON, R., ROSEN, V. and LYONS, K.M. (2000). The type i bmp receptor bmprib is required for chondrogenesis in the mouse limb. Development 127: 621-30.
106. YOKOUCHI, Y., SAKIYAMA, J., KAMEDA, T., IBA, H., SUZUKI, A., UENO, N. and KUROIWA, A. (1996). Bmp-2/-4 mediate programmed cell death in chicken limb buds. Development 122: 3725-34.
107. YOON, B.S. and LYONS, K.M. (2004). Multiple functions of bmps in chondrogenesis. J Cell Biochem 93: 93-103.
108. ZHANG, H. and BRADLEY, A. (1996). Mice deficient for bmp2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122: 2977-86.
109. ZHANG, Y., ZHANG, Z., ZHAO, X., YU, X., HU, Y., GERONIMO, B., FROMM, S.H. and CHEN, Y.P. (2000). A new function of bmp4: Dual role for bmp4 in regulation of sonic hedgehog expression in the mouse tooth germ. Development 127: 1431-43.
110. ZHANG, Z., SONG, Y., ZHANG, X., TANG, J., CHEN, J. and CHEN, Y. (2003). Msx1/bmp4 genetic pathway regulates mammalian alveolar bone formation via induction of dlx5 and cbfa1. Mech Dev 120: 1469-79.
111. ZHANG, Z., SONG, Y., ZHAO, X., ZHANG, X., FERMIN, C. and CHEN, Y. (2002). Rescue of cleft palate in msxl-deficient mice by transgenic bmp4 reveals a network of bmp and shh signaling in the regulation of mammalian palatogenesis. Development 129: 4135-46.
112. ZHAO, G.Q., LIAW, L. and HOGAN, B.L. (1998). Bone morphogenetic protein 8a plays a role in the maintenance of spermatogenesis and the integrity of the epididymis. Development 125: 1103-12.
113. ZHAO, M., HARRIS, S.E., HORN, D., GENG, Z., NISHIMURA, R., MUNDY, G.R. and CHEN, D. (2002). Bone morphogenetic protein receptor signaling is necessary for normal murine postnatal bone formation. J Cell Biol 157: 1049-60.
114. ZHAO, P. and HOFFMAN, E.P. (2004). Embryonic myogenesis pathways in muscle regeneration. Dev Dyn 229: 380-92.
115. ZHAO, R., LAWLER, A.M. and LEE, S.J. (1999). Characterization of gdf-10 expression patterns and null mice. Dev Biol 212: 68-79.
116. ZHAO, X., ZHANG, Z., SONG, Y., ZHANG, X., ZHANG, Y., HU, Y., FROMM, S.H. and CHEN, Y. (2000). Transgenically ectopic expression of bmp4 to the msx1 mutant dental mesenchyme restores downstream gene expression but represses shh and bmp2 in the enamel knot of wild type tooth germ. Mech Dev 99: 29-38.