Involvement of bone morphogenetic protein-4 and bone morphogenetic protein-7 in the differentiation of the adrenergic phenotype in developing sympathetic neurons

Development

Volumn 122, Issue 7, 1996, Pages 2079-2088

  Reissmann, E ^a   Ernsberger, U ^a   Francis West, P H ^b   Rueger, D ^c   Brickell, P M ^b   Rohrer, H ^a  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c Creative BioMolecules   (United States)

Author keywords

Adrenergic; Bone morphogenetic protein 4; Bone morphogenetic protein 7; Dorsal aorta; Neural crest; Noradrenergic; Sympathetic

Indexed keywords

BONE MORPHOGENETIC PROTEIN; NEUROTRANSMITTER;

ADRENERGIC NERVE; ANIMAL CELL; AORTA; ARTICLE; CELL CULTURE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NONHUMAN; NOTOCHORD; PHENOTYPE; PRIORITY JOURNAL; SYMPATHETIC NERVE CELL;

ADRENERGIC FIBERS; ANIMALS; AORTA; BONE MORPHOGENETIC PROTEINS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CHICK EMBRYO; DOSE-RESPONSE RELATIONSHIP, DRUG; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NEURAL CREST; PHENOTYPE; PROTEINS; QUAIL; SYMPATHETIC NERVOUS SYSTEM; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTORS; TYROSINE 3-MONOOXYGENASE;

ANIMALIA;

EID: 0030018314     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Allan, I. J. and Newgreen, D. F. (1977). Catecholamine accumulation in neural crest cells and the primary sympathetic chain. Am. J. Anat. 149, 413-421.
2. Anderson, D. J. (1993). Molecular control of cell fate in the neural crest: The sympathoadrenal lineage. Annu. Rev. Neurosci. 16, 129-158.
3. Attisano, L., Wrana, J. L., Lopez-Casillas, F. and Massagué, J. (1994). TGF-β receptors and actions. Biochem. Biophys. Acta 1222, 71-80.
4. Baroffio, A., Dupin, E. and Le Douarin, N. M. (1988). Clone-forming ability and differentiation potential of migratory neural crest cells. Proc. Natl. Acad. Sci. USA 85, 5325-5329.
5. Bitgood, M. J. and McMahon, A. P. (1995). Hedgehog and BMP genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172, 126-138.
6. Cohen, A. M. (1972). Factors directing the expression of sympathetic nerve trails in cells of neural crest origin. J. Exp. Zool. 179, 167-182.
7. Duprez, D., de H. Bell, E. J., Richardson, M. K., Archer, C. W., Wolpert, L., Brickell, P. M. and Francis-West, P. H. (1996) Overexpression of BMP-2 and BMP-4 alters the size and shape of developing skeletal elements in the chick limb. Mech. of Development, in press
8. Enemar, A., Falck, B. and Hakanson, R. (1965). Observations on the appearance of norepinephrine in the sympathetic nervous system of the chick embryo. Dev. Biol. 11, 268-283.
9. Ernsberger, U., Sendtner, M. and Rohrer, H. (1989). Proliferation and differentiation of embryonic chick sympathetic neurons: effects of ciliary neurotrophic factor. Neuron 2, 1275-1284.
10. Ernsberger, U., Patzke, H., Tissier-Seta, J. P., Reh, T., Goridis, C. and Rohrer, H. (1995). The expression of tyrosine hydroxylase and the transcription factors cPhox-2 and Cash-1: Evidence for distinct inductive steps in the differentiation of chick sympathetic precursor cells. Mech. Dev. 52, 125-136.
11. Fan, C.-M. and Tessier-Lavigne, M. (1994). Patterning of mammalian somites by surface ectoderm and notochord: Evidence for sclerotome induction by a hedgehog homolog. Cell 79, 1175-1186.
12. Fauquet, M., Smith, J., Ziller, C. and LeDouarin, N. M. (1981). Differentiation of autonomic neuron precursors in vitro: cholinergic and adrenergic traits in cultured crest cells. J. Neurosci. 1, 478-492.
13. Ferguson, E. L. and Anderson, K. V. (1992). Decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71, 451-561.
14. 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.
15. Fukada, K. (1985). Purification and partial characterization of a cholinergic neuronal differentiation factor. Proc. Natl Acad. Sci. USA 82, 8795-8799.
16. Green, J. B. A. and Smith, J. C. (1990). Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature 347, 391-394.
17. Groves, A. K., George, K. M., Tissier-Seta, J.-P., Engel, J. D., Brunet, J.-F. and Anderson, D. J. (1995). Differential regulation of transcription factor gene expression and phenotypic markers in developing sympathetic neurons. Development 121, 887-901.
18. Gurdon, J. B., Harger, P., Mitchell, A. and Lemaire, P. (1994). Activin signalling and response to a morphogen gradient. Nature 371, 487-492.
19. Hamburger, V. and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
20. Hogan, B. L. M., Blessing, M., Winnier, G. K., Suzuki, N. and Jones, C. M. (1994). Growth factors in development: the role of TGF-β related polypeptide signalling molecules in embryogenesis. Development Supplement, 53-60.
21. Houston, B., Thorp, B. H. and Burt, D. H. (1994). Molecular cloning and expression of bone morphogenetic protein-7 in the chick epiphyseal growth plate. J. Mol. Endocrinol. 13, 289-301.
22. Howard, M. J. and Bronner-Fraser, M. (1985). The influence of neural tube-derived factors on differentiation of neural crest cells in vitro I Histochemical study on the appearance of adrenergic cells. J. Neurosci. 5, 3302-3309.
23. Howard, M. J. and Bronner-Fraser, M. (1986). Neural tube-derived factors influence differentiation of neural crest cells in vitro: effects on activity of neurotransmitter biosynthetic enzymes. Dev. Biol. 117, 45-54.
24. Hughes, S. H., Greenhouse, J. J., Petropoulos, C. J. and Sutrave, P. (1987). Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. J. Virol. 61, 3004-3012.
25. Hynes, M., Porter, J. A., Chiang, C., Chang, D., Tessier-Lavigne, M., Beachy, P. A. and Rosenthal, A. (1995). Induction of midbrain dopaminergic neurons by sonic hedgehog. Neuron 15, 35-44.
26. Johnson, R. L., Laufer, E., Riddle, R. D. and Tabin, C. (1994). Ectopic expression of Sonic hedgehog alters dorsal-ventral patterning of somites. Cell 79, 1165-1173.
27. 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.
28. Kingsley, D. M. (1994). The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev. 8, 133-146.
29. Kirby, M. L. and Gilmore, S. A. (1976). A correlative histofluorescence and light microscopic study of the formation of the sympathetic trunks in chick embryos. Anat. Rec. 186, 437-450.
30. Koenig, B. B., Cook, J. S., Wolsing, D. H., Ting, J., Tiesman, J. P., Correa, P. E., Olson, C. A., Pecquet, A. L., Ventura, F., Grant, R. A., Chen, G.-X., Wrana, J. L., Massagué, J. and Rosenbaum, J. S. (1994). Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells. Mol. Cell. Biol. 14, 5961-5974.
31. Laufer, E., Nelson, C. E., Johnson, R. L., Morgan, B. A. and Tabin, C. (1994). Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell 79, 993-1003.
32. LeLievre, C. S., Schweizer, G. G., Ziller, C. M. and LeDouarin, N. M. (1980). Restrictions of developmental capabilities in neural crest cell derivatives as tested by in vivo transplantation experiments. Dev. Biol. 77, 362-378.
33. Liem, K. F., 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, 969-979.
34. Liu, F., Ventura, F., Doody, J. and Massagué, 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.
35. 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.
36. Lyons, K. M., Hogan, B. L. M. and Robertson, E. J. (1995). Colocalization of BMP 7 and BMP 2 RNAs suggest that these factors cooperatively mediate tissue interactions during murine development. Mech. Dev. 50, 71-83.
37. Marti, E., Bumcrot, D. A., Takada, R. and McMahon, A. P. (1995). Requirement of 19k sonic hedgehog for induction of distinct ventral cell types in CNS explants. Nature 375, 322-325.
38. Masu, Y., Wolf, E., Holtmann, B., Sendtner, M., Brem, G. and Thoenen, H. (1993). Disruption of the CNTF gene results in motor neuron degeneration. Nature 365, 27-32.
39. Norr, S. C. (1973). In vitro analysis of sympathetic neuron differentiation from chick neural crest cells. Dev. Biol. 34, 16-38.
40. O'Farrell, P. H. (1994). Unanimity waits in the wings. Nature 368, 188-189.
41. Perrimon, N. (1995). Hedgehog and beyond. Cell 80, 517-529.
42. Placzek, M., Jessell, T. M. and Dodd, J. (1993). Induction of floor plate differentiation by contact-dependent, homeogenetic signals. Development 117, 205-218.
43. Rao, M. S., Sun, Y., Escary, J. L., Perreau, J., Tresser, S., Patterson, P. H., Zigmond, R. E., Brulet, P. and Landis, S. C. (1993). Leukemia inhibitory factor mediates an injury response but not a target-directed developmental transmitter switch in sympathetic neurons. Neuron 11, 1175-1185.
44. Roelink, H., Augsburger, A., Heemskerk, J., Korzh, V., Norlin, S., Ruiz i Altaba, A., Tanabe, Y., Placzek, M., Edlund, T., Jessell, T. M. and Dodd, J. (1994). Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76, 761-775.
45. Rohrer, H., Acheson, A. L., Thibault, J. and Thoenen, H. (1986). Developmental potential of quail dorsal root ganglion cells analyzed in vitro and in vivo. J. Neurosci. 6, 2616-2624.
46. Rohrer, H. and Thoenen, H. (1987). Relationship between differentiation and terminal mitosis: chick sensory and ciliary neurons differentiate after terminal mitosis of precursor cells whereas sympathetic neurons continue to divide after differentiation. J. Neurosci. 7, 3739-3748.
47. Rosenzweig, B. L, Imamura, T., Okadome, T., Cox, G. N., Yamashita, H., ten Dijke, P., Heldin, C.-H. and Miyazono, K. (1995) Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc. Natl. Acad. Sci. USA 92, 7632-7636.
48. Rothman, T. P., Gershon, M. D. and Holtzer, H. (1978). The relationship of cell division to the acquisition of adrenergic characteristics by developing sympathetic ganglion cell precursors. Dev. Biol. 65, 321-341.
49. Saadat, S., Sendtner, M. and Rohrer, H. (1989). Ciliary neurotrophic factor induces cholinergic differentiation of rat sympathetic neurons in culture. J. Cell Biol. 108, 1807-1816.
50. Sampath, T. K., Maliakal, J. C., Hauschka, P. V., Jones, W. K., Sasak, H., Tucker, R. F., White, K. H., Coughlin, J. E., Tucker, M. M., Pang, R. H. L., Corbett, C., Özkaynak, E., Oppermann, H. and Rueger, D. C. (1992). Recombinanat 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.
51. Schaeren-Wiemers, N. and Gerfin-Moser, A. (1993). A single proptocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100, 431-440.
52. Selleck, M. A. J., Scherson, T. Y. and Bronner-Fraser, M. (1993). Origins of neural crest cell diversity. Dev. Biol. 159, 1-11.
53. Stern, C. D., Artinger, K. B. and Bronner-Fraser, M. (1991). Tissue interactions affecting the migration and differentiation of neural crest cells in the chick embryo. Development 113, 207-216.
54. Teiltet, M.-A. and LeDouarin, N. M. (1983). Consequences of neural tube and notochord excision on the development of the peripheral nervous system in the chick embryo. Dev. Biol. 98, 192-211.
55. Ten Dijke, P., Yamashita, H., Sampath, T. K., Reddi, A. H., Estevez, M., Riddle, D. L., Ichijo, H., Heldin, C.-H. and Miyazono, K. (1994). Identification of Type I Receptors for Osteogenic Protein-1 and Bone Morphogenetic Protein-4. J. Biol. Chem. 269, 16985-16988.
56. Tucker, G. C., Aoyama, H., Lipinski, M., Tursz, T. and Thiery, J. P. (1984). Identical reactivity of monoclonal antibodies HNK-1 and NC-1:conservation in vertebrates on cells derived from the neural primordium and on some leukocytes. Cell Different. 14, 223-230.
57. Varley, J. E., Wehby, R. G., Rueger, D. C. and Maxwell, G. D. (1995). Number of adrenergic and Islet-1 immunoreactive cells is increased in avian trunk neural crest cultures in the presence of human recombinant osteogenic protein-1. Develop. Dynamics 203, 434-447.
58. Wehby, R. G., Varley, J. E. and Maxwell, G. D. (1993). Recombinant human osteogenic protein-1 (OP-1) increases adrenergic cell number in avian neural crest cultures. Neuroscl. Abstr. 19, 711-7. (Abstract)
59. Weston, J. A. and Butler, S. L. (1966). Temporal factors affecting localization of neural crest cells in the chicken embryo. Dev. Biol. 14, 246-266.
60. Wilkinson, D. G. (1993). Whole mount in situ hybridization of vertebrate embryos. In In situ Hybridization. (ed. D. G. Wilkinson). pp. 75-83. Oxford: Oxford University Press.
61. Xue, Z. G., Smith, J. and LeDouarin, N. M. (1985). Differentiation of catecholaminergic cells in cultures of embryonic avian sensory ganglia. Proc. Natl. Acad. Sci. USA 82, 8800-8804.
62. Yamada, T., Pfaff, S. L., Edlund, T. and Jessell, T. M. (1993). Control of cell pattern in the neural tube: Motor neuron induction by diffusible factors from notochord and floor plate. Cell 73, 673-686.
63. Yamamori, T., Fukada, K., Aebersold, R., Korsching, S., Fann, M.-J. and Patterson, P. H. (1989). The cholinergic neuronal differentiation factor from heart cells is identical to leukemia inhibitory factor. Science 246, 1412-1416.
64. Yang, Y. and Niswander, L. (1995). Interaction between the signaling molecules WNT7a and SHH during vertebrate limb development: Dorsal signals regulates anteroposterior patterning. Cell 80, 939-947.