Role of BMP-2 and OP-1 (BMP-7) in programmed cell death and skeletogenesis during chick limb development

Development

Volumn 124, Issue 6, 1997, Pages 1109-1117

  Macias, D ^a   Ganan Y ^a   Sampath, T K ^b   Piedra, M E ^c   Ros, M A ^c   Hurle, J M ^c  

^a UNIVERSITY OF EXTREMADURA   (Spain)

^b CURIS INC   (United States)

^c UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

Apoptosis; Cartilage growth; Chondrogenesis; Indian hedgehog; Joint formation

Indexed keywords

BONE MORPHOGENETIC PROTEIN; HEPARIN; OSTEOGENIC PROTEIN 1; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE DEVELOPMENT; CARTILAGE; CHICKEN; CHONDROGENESIS; DEVELOPMENTAL GENETICS; DIFFERENTIATION; EMBRYO; EMBRYO DEVELOPMENT; FINGER; IN SITU HYBRIDIZATION; JOINT; LIMB DEVELOPMENT; NONHUMAN; PERICHONDRIUM; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; BONE MORPHOGENETIC PROTEINS; CARTILAGE; CHICK EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMERUS; IN SITU HYBRIDIZATION; JOINTS; LIMB BUD; MESODERM; OSTEOGENESIS; RADIUS; TRANSFORMING GROWTH FACTOR BETA; ULNA;

ANIMALIA; ERINACEIDAE; GALLUS GALLUS;

EID: 1842405367     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (46)

1. Ahrens, P. B., Solursh, M. and Reitter, R. (1977). Stage-related capacity for limb chondrogenesis in cell cultures. Dev. Biol. 60, 69-82.
2. Alles, A. J. and Sulik, K. K. (1989). Retinoic-acid-induced limb-reduction defects: Perturbation of zone of programmed cell death as a pathogenetic mechanism. Teratology 40, 163-171.
3. Aulthouse, A. L. and Solursh, M. (1987). The detection of a precartilage, blastema-specific marker. Dev. Biol. 120, 377-384.
4. Carrington, J. L., Chen, P., Yanagishita, M. and Reddi, A. H. (1991). Osteogenin (bone morphogenetic protein-3) stimulates cartilage formation by chick limb bud cells in vitro. Dev. Biol. 146, 406-415.
5. Chang, S. C., Hoang, B., Thomas, J. T., Vukicevic, S., Luyten, F. P., Ryba, N. J. P., Kozak, C. A., Reddi, A. H. and Moos, M. Jr. (1994). Cartilagederived morphogenetic proteins. New members of the transforming growth factor-β superfamily predominantly expressed in long bones during human embryonic development. J. Biol. Chem. 269, 28227-28234.
6. Chen, P., Carrington, J. L., Hammonds, R. G. and Reddi, A. H. (1991). Stimulation of chondrogenesis in limb bud cells by recombinant human bone morphogenetic protein 2B (BMP-2B) and modulation by transforming growth factor β1 and β2. Exp. Cell. Res. 195, 509-515.
7. Coelho, C. N. D., Sumoy, L., Rodgers, B. J., Davidson, D. R., Hill, R., Upholt, W. B. and Kosher, R. A. (1991). Expression of chicken homeobox-containing gene GHox-8 during embryonic chick limb development. Mech. Dev. 34, 143-154.
8. Duprez, D. M., Bell, E. J., Richardson, M., 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, 145-157.
9. 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, 448-452.
10. Duprez, D. M., Kostakopoulou, K., Francis-West, P., Tickle, C. and Brickell, P. M. (1996c). Activation of Fgf-4 and HoxD gene expression by BMP-2 expressing cells in the developing chick limb. Development 122, 1821-1828.
11. Francis, P., H., Richardson, M. K., Brickell, P. M. and Tickle, C. (1994). Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb. Development 120, 209-218.
12. 3) limb buds: their relationships in the signalling cascade involved in limb patterning. Dev. Dyn. 203, 187-197.
13. Gañan, Y., Macias, D., Duterque-Coquillaud, M., Ros, M. A. and Hurle, J. M. (1996). Role of TGF-βs and BMPs as signals controlling the position of the digits and the areas of cell death in the developing chick limb autopod. Development 122, 2349-2357
14. Hamburger, V. and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morph. 88, 49-92.
15. Hazama, M., Aono, A., Veno, N. and Fujisawa, Y. (1995). Efficient expression of a heterodimer of bone morphogenetic protein subunits using a baculovirus expression system. Biochem. Biophys. Res. Comm. 209, 859-866.
16. Helder, M. N., Ozkaynak, E., Sampath, K. T., Luyten, F. P., Latin, V., Oppermann, H. and Vukicevic, S. (1995). Expression pattern of osteogenic protein-1 (Bone morphogenetic protein-7) in human and mouse development. J. Histochem. Cytochem. 43, 1035-1044.
17. Hinchliffe, J. R. (1982). Cell death in vertebrate limb morphogenesis. In Progress in Anatomy. Vol. 2 (ed. R. J. Harrison and V. Navaratnam V. eds.) pp. 113-126. Cambridge: Cambridge University Press.
18. Hofmann, C., Luo, G., Balling, R. and Karsenty, G. (1996). Analysis of limb patterning in BMP-7-deficient mice. Dev. Gen. 19, 43-50.
19. Hogan, B. L. M. (1996). Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Gen. Dev. 10, 1580-1594.
20. Höten, 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. and Kudo, A. (1996). Recombinant human growth/differentiation factor 5′ stimulates mesenchyme aggregation and chondrogenesis responsible for the skeletal development of limbs. Growth Factors 13, 65-74.
21. Hurle, J. M., Gañan, Y. and Macias, D. (1989). Experimental analysis of the in vivo chondrogenic potential of the interdigital mesenchyme of the chick leg bud subjected to local ectodermal removal. Dev. Biol. 132, 368-374.
22. Hurle, J. M., Ros, M. A., Garcia-Martinez, V., Macias, D. and Gañan, Y. (1995). Cell death in the embryonic developing limb. Scan. Microsc. 9, 519-534.
23. Hurle, J. M., Ros, M. A., Climent, V. and Garcia-Martinez, V. (1996). Morphology and significance of programmed cell death in the developing limb bud of the vertebrate embryo. Microsc. Res. Tech. 34, 236-246.
24. Jones, C. M., Lyons, K. M. and Hogan, B. L. M. (1991). Involvement of bone morphogenetic protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development 111, 531-542.
25. Kingsley, D. (1994). What do BMPs do in mammals? Clues from the mouse short-ear mutation. Trends Genet. 10, 16-21.
26. Kochhar, D. M. and Agnish, N. D. (1977). 'Chemical surgery' as an aproach to study morphogenetic events in embryonic mouse limb. Dev. Biol. 61, 388-394.
27. Lanske, B., Karaplis, A. C., Lee, K., Luz, A., Vortkamp, A., Pirro, A., Karperien, M., Defize, L. H. K., Ho, C., Mulligan, R. C., Abou-Samra, A-B., Juppner, H., Segre, G. V. and Kronenberg, H. M. (1996). PTH/PTHrP receptor in early development and indian hedgehog-regulated bone growth. Science 273, 663-666.
28. Liu, F., Ventura, F., Doody, J. and Massague, J. (1995). Human type II receptor for bone morphogenetic proteins (BMPs): extension of the two-kinase receptor model to the BMPs. Mol. Cell biol. 15, 3479-3486.
29. Luo, G., Hofmann, C., Bronckers, A. L. J. J., 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. Gen. Develop. 9, 2808-2820.
30. Lyons, K. M., Hogan, B. L. M. and Robertson, E. J. (1995). Colocalization of BMP 7 and BMP 2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech. Dev. 50, 71-83.
31. Lyons, K. M., Pelton, R. W. and Hogan, B. L. M. (1989). Patterns of expression of murine Vgr-1 and BMP-2a RNA suggest that transforming growth factor-β-like genes coordinately regulate aspects of embryonic development. Gen. Develop. 3, 1657-1668.
32. Lyons, K. M., Pelton, R. W. and Hogan, B. L. M. (1990). Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for bone morphogenetic protein-2A (BMP-2A). Development 109, 833-844.
33. Macias, D., Gañan, Y., Ros, M. A. and Hurle, J. M. (1996). In vivo inhibition of programmed cell death by local administration of FGF-2 and FGF-4 in the interdigital areas of the embryonic leg bud. Anat. Embryol. 193, 533-541.
34. Niswander, L. and Martin, G. R. (1993). FGF-4 and BMP-2 have opposite effects on limb outgrowth. Nature 361, 68-71.
35. Oliver, G., Wehr, R., Jenkins, N. A., Copeland, N. G., Cheyette, B. N. R., Hartenstein, V., Zipursky, S. L. and Gruss, P. (1995). Homeobox genes and connective tissue patterning. Development 121, 693-705.
36. Patel, K., Nittenberg, R., D'Souza, D., Irving, C., Burt, D., Wilkinson, D. G. and Tickle, C. (1996). Expression and regulation of Cek-8, a cell to cell signalling receptor in tdeveloping chick limb buds. Development 122, 1147-1155.
37. Roark, E. F. and Greer, K. (1994). Transforming growth factor-β and bone morphogenetic protein-2 act by distinct mechanisms to rpomote chick limb cartilage differentiation in vitro. Dev. Dyn. 200, 103-116.
38. Ros, M. A., Macias, D., Fallen, J. F. and Hurle, J. M. (1994). Formation of extra digits in the interdigital spaces of the chick leg bud is not preceded by changes in the expression of Msx and Hoxd genes. Anal. Embryol. 190, 375-382.
39. Sampath, T. K. and Reddi, A. H. (1981). Dissociative extraction and reconstitution of extracellular matrix components involved in local bone differentiation. Proc. Natl. Acad. Sci. USA 78, 7599-7602.
40. Sampath, T. K., Coughlin, J. E., Whetstone, R. M., Banach, D., Corbett, C., Ridge, R. J. and Ozkaynak, E. (1990). Bovine osteogenic protein is composed of dimers of OP-1 and BMP-2A, two members of the transforming growth factor-β superfamily. J. Biol. Chem. 265, 13198-13205.
41. 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-β superfamily. Nature 368, 639-643.
42. Urist, M. R., Mikulski, A. and Lietze, A. (1979). Solubilized and insolubilized bone morphogenetic protein. Proc. Natl. Acad. Sci. USA. 76, 1828-1832.
43. Vortkamp, A., Lee, K., Lanske, B., Segre, G. V., Kronenberg, H. M. and Tabin, C. J. (1996). Regulation of rayte of certilage differentiation by indian hedgeho and PTH-related protein. Science 273, 613-622
44. Wozney, J. M., Rosen, V., Cleste, 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, 1528-1534.
45. Wozney, J. M., Capparella, J. and Rosen, V. (1993). The bone morphogenetic proteins in cartilage and bone development. In Molecular Basis of Morphogenesis (ed. M. Bernfield) pp. 221-230. New York: Wiley-Liss Inc.
46. Zou, H. and Niswander, L. (1996). Requirement for BMP signaling in interdigital apoptosis and scale formation. Science 272, 738-741.