GDF5 coordinates bone and joint formation during digit development

Developmental Biology

Volumn 209, Issue 1, 1999, Pages 11-27

  Storm, Elaine E ^a   Kingsley, David M ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Brachypodism; Cartilage; GDF5; Joint; Skeletal development

Indexed keywords

BONE MORPHOGENETIC PROTEIN; GROWTH DIFFERENTIATION FACTOR 5; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CARTILAGE; CHICKEN; FINGER; GENE MUTATION; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; JOINT; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; REGULATORY MECHANISM; SYNDACTYLY;

ANIMALIA; GALLUS GALLUS; MAMMALIA; RODENTIA;

EID: 0033136001     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9241     Document Type: Article

References (66)

1. Amizuka N., Warshawsky H., Henderson J. E., Goltzman D., Karaplis A. C. Parathyroid hormone-related peptide-depleted mice show abnormal epiphyseal cartilage development and altered endochondral bone formation. J. Cell Biol. 126:1994;1611-1623.
2. Auerbach R., Kubai L., Knighton D., Folkman J. A simple procedure for the long-term cultivation of chicken embryos. Dev. Biol. 41:1974;391-394.
3. Bitgood M. J., McMahon A. P. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172:1995;126-138.
4. Blok L. J., Grossmann M. E., Perry J. E., Tindall D. J. Characterization of an early growth response gene, which encodes a zinc finger transcription factor, potentially involved in cell cycle regulation. Mol. Endocrinol. 9:1995;1610-1620.
5. Brunet L. J., McMahon J. A., McMahon A. P., Harland R. M. Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science. 280:1998;1455-1457.
6. Burkitt H. G., Young B., Heath J. W. Wheater's Functional Histology. 1993;Churchill Livingstone, London.
7. Cancedda R., Descalzi Cancedda F., Castagnola P. Chondrocyte differentiation. Int. Rev. Cytol. 159:1995;265-358.
8. Chang S. C., Hoang B., Thomas J. T., Vukicevic S., Luyten F. P., Ryba N. J., Kozak C. A., Reddi A. H., Moos M. Jr. Cartilage-derived morphogenetic proteins. New members of the transforming growth factor-beta superfamily predominantly expressed in long bones during human embryonic development. J. Biol. Chem. 269:1994;28227-28234.
9. Craig F. M., Bentley G., Archer C. W. The spatial and temporal pattern of collagens I and II and keratan sulphate in the developing chick metatarsophalangeal joint. Development. 99:1987;383-391.
10. Dalgleish A. E. Development of the Limbs of the Mouse. 1964;Stanford Univ. Press, Stanford.
11. Dosch R., Gawantka V., Delius H., Blumenstock C., Niehrs C. Bmp-4 acts as a morphogen in dorsoventral mesoderm patterning in Xenopus. Development. 124:1997;2325-2334.
12. Dudley A. T., Lyons K. M., Robertson E. J. A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev. 9:1995;2795-2807.
13. Ekanayake S., Hall B. K. The in vivo and in vitro effects of bone morphogenetic protein-2 on the development of the chick mandible. Int. J. Dev. Biol. 41:1997;67-81.
14. Erlacher L., McCartney J., Piek E., ten Dijke P., Yanagishita M., Oppermann H., Luyten F. P. Cartilage-derived morphogenetic proteins and osteogenic protein-1 differentially regulate osteogenesis. J. Bone Miner. Res. 13:1998;383-392.
15. Francis-West P. H., Richardson M. K., Bell E., Chen P., Luyten F., Adelfattah A., Barlow A. J., Brickell P. M., Wolpert L., Archer C. W. The effect of overexpression of BMPs and GDF-5 on the development of chick limb skeletal elements. Ann. N. Y. Acad. Sci. 785:1996;254-255.
16. Gañan Y., Macias D., Duterque-Coquillaud M., Ros M. A., Hurle J. M. Role of TGF betas and BMPs as signals controlling the position of the digits and the areas of interdigital cell death in the developing chick limb autopod. Development. 122:1996;2349-2357.
17. Graham A., Francis-West P., Brickell P., Lumsden A. The signalling molecule BMP4 mediates apoptosis in the rhombencephalic neural crest. Nature. 372:1994;684-686.
18. Grüneberg H., Lee A. J. The anatomy and development of brachypodism in the mouse. J. Embryol. Exp. Morphol. 30:1973;119-141.
19. Haines R. W. The development of joints. J. Anat. 81:1947;33-55.
20. Hamburger V., Hamilton H. L. A series of normal stages in the development of the chick embryo. J. Morphol. 88:1951;49-92.
21. Heldin C. H., Miyazono K., ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature. 390:1997;465-471.
22. Hinchliffe J. R., Johnson D. R. The Development of the Vertebrate Limb. 1980;Clarendon Press, Oxford.
23. Hogan B. L. Bone morphogenetic proteins in development. Curr. Opin. Genet. Dev. 6:1996;432-438.
24. Hötten G. C., Matsumoto T., Kimura M., Bechtold R. F., Kron R., Ohara T., Tanaka H., Satoh Y., Okazaki M., Shirai T., Pan H., Kawai S., Pohl J. S., Kudo A. Recombinant human growth/differentiation factor 5 stimulates mesenchyme aggregation and chondrogenesis responsible for the skeletal development of limbs. Growth Factors. 13:1996;65-74.
25. Hui C. C., Joyner A. L. A mouse model of Greig cephalopolysyndactyly syndrome: The extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat. Genet. 3:1993;241-246.
26. Hui C. C., Slusarski D., Platt K. A., Holmgren R., Joyner A. L. Expression of three mouse homologs of theDrosophila. Dev. Biol. 162:1994;402-413.
27. Karaplis A. C., Luz A., Glowacki J., Bronson R. T., Tybulewicz V. L., Kronenberg H. M., Mulligan R. C. Lethal skeletal dysplasia from targeted disruption of the parathyroid hormone-related peptide gene. Genes Dev. 8:1994;277-289.
28. Kingsley D. M. The TGF-beta superfamily: New members, new receptors, and new genetic tests of function in different organisms. Genes Dev. 8:1994a;133-146.
29. Kingsley D. M. What do BMPs do in mammals? Clues from the mouse short ear mutation. Trends Genet. 10:1994b;16-21.
30. Krieglstein K., Suter-Crazzolara C., Hötten G., Pohl J., Unsicker K. Trophic and protective effects of growth/differentiation factor 5, a member of the transforming growth factor-beta superfamily, on midbrain dopaminergic neurons. J. Neurosci. Res. 42:1995;724-732.
31. Landauer W. Brachypodism: A recessive mutation of house-mice. J. Hered. 43:1952;293-298.
32. Luo G., Hofmann C., Bronckers A. L., 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. 9:1995;2808-2820.
33. Macias D., Gañan Y., Sampath T. K., Piedra M. E., Ros M. A., Hurle J. M. Role of BMP-2 and OP-1 (BMP-7) in programmed cell death and skeletogenesis during chick limb development. Development. 124:1997;1109-1117.
34. Massague J. TGFbeta signaling: Receptors, transducers, and Mad proteins. Cell. 85:1996;947-950.
35. Mishina Y., Suzuki A., Ueno N., Behringer R. R. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev. 9:1995;3027-3037.
36. Mitrovic D. Development of the diarthrodial joints in the rat embryo. Am. J. Anat. 151:1978;475-486.
37. Monsoro-Burq A. H., Duprez D., Watanabe Y., Bontoux M., Vincent C., Brickell P., Le Douarin N. The role of bone morphogenetic proteins in vertebral development. Development. 122:1996;3607-3616.
38. Nakamura K., Hirosawa K., Hama K., Oda S. Defects in the growth plate of brachypodism in mice - Light and electron microscopic findings and cell proliferation by the method of tritiated thymidine autoradiography. Nippon Seikeigeka Gakkai Zasshi. 58:1984;835-845.
39. Otto F., Thornell A. P., Crompton T., Denzel A., Gilmour K. C., Rosewell I. R., Stamp G. W., Beddington R. S., Mundlos S., Olsen B. R., Selby P. B., Owen M. J. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell. 89:1997;765-771.
40. Owens E. M., Solursh M. Cell-cell interaction by mouse limb cells duringin vitro. Dev. Biol. 91:1982;376-388.
41. Piccolo S., Sasai Y., Lu B., De Robertis E. M. Dorsoventral patterning in Xenopus: Inhibition of ventral signals by direct binding of chordin to BMP-4. Cell. 86:1996;589-598.
42. Polinkovsky A., Robin N. H., Thomas J. T., Irons M., Lynn A., Goodman F. R., Reardon W., Kant S. G., Brunner H. G., van der Burgt I., Chitayat D., McGaughran J., Donnai D., Luyten F. P., Warman M. L. Mutations in CDMP1 cause autosomal dominant brachydactyly type C. Nat. Genet. 17:1997;18-19.
43. Reddi A. H. Cell biology and biochemistry of endochondral bone development. Collagen Relat. Res. 1:1981;209-226.
44. Reddi A. H., Huggins C. Biochemical sequences in the transformation of normal fibroblasts in adolescent rats. Proc. Natl. Acad. Sci. USA. 69:1972;1601-1605.
45. Rosen V., Thies R. S., Lyons K. Signaling pathways in skeletal formation: A role for BMP receptors. Ann. N. Y. Acad. Sci. 785:1996;59-69.
46. Ruiz i Altaba A. Catching a Gli-mpse of Hedgehog. Cell. 90:1997;193-196.
47. Sandell L. J. In situ expression of collagen and proteoglycan genes in notochord and during skeletal development and growth. Microsc. Res. Tech. 28:1994;470-482.
48. Storm E. E., Huynh T. V., Copeland N. G., Jenkins N. A., Kingsley D. M., Lee S. Limb alterations inbrachypodism. Nature. 368:1994;639-643.
49. Storm E. E., Kingsley D. M. Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (BMP) family. Development. 122:1996;3969-3979.
50. Thomas J. T., Kilpatrick M. W., Lin K., Erlacher L., Lembessis P., Costa T., Tsipouras P., Luyten F. P. Disruption of human limb morphogenesis by a dominant negative mutation in CDMP1. Nat. Genet. 17:1997;58-64.
51. Thomas J. T., Lin K., Nandedkar M., Camargo M., Cervenka J., Luyten F. P. A human chondrodysplasia due to a mutation in a TGF-beta superfamily member. Nat. Genet. 12:1996;315-317.
52. Tonegawa A., Funayama N., Ueno N., Takahashi Y. Mesodermal subdivision along the mediolateral axis in chicken controlled by different concentrations of BMP-4. Development. 124:1997;1975-1984.
53. Urist M. R. Bone formation by autoinduction. Science. 150:1965;893-899.
54. Vainio S., Karavanova I., Jowett A., Thesleff I. Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell. 75:1993;45-58.
55. Vortkamp A., Lee K., Lanske B., Segre G. V., Kronenberg H. M., Tabin C. J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science. 273:1996;613-622.
56. Weir E. C., Philbrick W. M., Amling M., Neff L. A., Baron R., Broadus A. E. Targeted overexpression of parathyroid hormone-related peptide in chondrocytes causes chondrodysplasia and delayed endochondral bone formation. Proc. Natl. Acad. Sci. USA. 93:1996;10240-10245.
57. Wolfman N. M., Hattersley G., Cox K., Celeste A. J., Nelson R., Yamaji N., Dube J. L., DiBlasio-Smith E., Nove J., Song J. J., Wozney J. M., 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. 100:1997;321-330.
58. Yamaji N., Celeste A. J., Thies R. S., Song J. J., Bernier S. M., Goltzman D., Lyons K. M., Nove J., Rosen V., Wozney J. M. A mammalian serine/threonine kinase receptor specifically binds BMP-2 and BMP-4. Biochem. Biophys. Res. Commun. 205:1994;1944-1951.
59. Yamashita H., Shimizu A., Kato M., Nishitoh H., Ichijo H., Hanyu A., Morita I., Kimura M., Makishima F., Miyazono K. Growth/differentiation factor-5 induces angiogenesis in vivo. Exp. Cell Res. 235:1997;218-226.
60. Yokouchi Y., Sakiyama J., Kameda T., Iba H., Suzuki A., Ueno N., Kuroiwa A. BMP-2/-4 mediate programmed cell death in chicken limb buds. Development. 122:1996;3725-3734.
61. Zhang H., Bradley A. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development. 122:1996;2977-2986.
62. Zhao G. Q., Deng K., Labosky P. A., Liaw L., Hogan B. L. The gene encoding bone morphogenetic protein 8B is required for the initiation and maintenance of spermatogenesis in the mouse. Genes Dev. 10:1996a;1657-1669.
63. Zhao G. Q., Hogan B. L. Evidence that mouse Bmp8a (Op2) and Bmp8b are duplicated genes that play a role in spermatogenesis and placental development. Mech. Dev. 57:1996b;159-168.
64. Zimmerman L. B., De Jesus-Escobar J. M., Harland R. M. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell. 86:1996;599-606.
65. Zou H., Niswander L. Requirement for BMP signaling in interdigital apoptosis and scale formation. Science. 272:1996;738-741.
66. Zou H., Wieser R., Massague J., Niswander L. Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev. 11:1997;2191-2203.