Bone morphogenetic proteins: Neurotrophic roles for midbrain dopaminergic neurons and implications of astroglial cells

European Journal of Neuroscience

Volumn 9, Issue 8, 1997, Pages 1699-1710

  Jordan, Jens ^a   Böttner, Martina ^a   Schluesener, Hermann J ^a,b   Unsicker, Klaus ^a   Krieglstein, Kerstin ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Cell proliferation and differentiation; Embryonic rat mesencephalon; Glial fibrillary acidic protein; MPP+; Tyrosine hydroxylase

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 6; BROXURIDINE; FIBROBLAST GROWTH FACTOR 2; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; NEUROTRANSMITTER; NEUROTROPHIC FACTOR; TRANSFORMING GROWTH FACTOR BETA; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; DNA SYNTHESIS; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; DOSE RESPONSE; EMBRYO; EMBRYO DEVELOPMENT; IMMUNOCYTOCHEMISTRY; ISOTOPE LABELING; MESENCEPHALON; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; TISSUE GROWTH;

1-METHYL-4-PHENYLPYRIDINIUM; ANIMALS; ASTROCYTES; BONE MORPHOGENETIC PROTEINS; CELL AGING; CELL DIVISION; CELL SURVIVAL; CELLS, CULTURED; DOPAMINE; IMMUNOHISTOCHEMISTRY; MESENCEPHALON; NERVE GROWTH FACTORS; NEURONS; RATS; RATS, WISTAR;

EID: 0030875989     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.1997.tb01527.x     Document Type: Article

References (57)

1. Alexi, T. and Hefti, F. (1993) Trophic actions of transforming growth-factor-alpha on mesencephalic dopaminergic neurons developing in culture. Neuroscience, 55, 903-918.
2. Beck, K. D., Valverde, J., Alexi, T., Poulsen, K., Moffat, B., Vandlen, R. A., Rosenthal, A. and Hefti, F. (1995) Mesencephalic dopaminergic neurons protected by GDNF from axotomy-induced degeneration in the adult brain. Nature, 373, 339-341.
3. Bottenstein, J., Skaper, S., Varon, S. and Sato, G. (1980) Selective survival of neurons in chick sensory ganglionic cultures utilizing serum-free supplement medium. Exp. Cell Res., 125, 183-190.
4. Canalis, E. and Gabbitas, B. (1994) Bone morphogenetic protein 2 increases insulin-like growth factor I and II transcripts and polypeptide levels in bone cell cultures. J. Bone Miner. Res., 9, 1999-2005.
5. Constam, D. B., Schmid, P., Aguzzi, A., Schachner, M. and Fontana, A. (1994) Transient production of TGF-α2 by postnatal cerebellar neurons and its effect on neuroblast proliferation. Eur. J. Neurosci., 6, 766-778.
6. D'Alessandro, J. S. and Wang, E. A. (1994) Bone morphogenetic proteins inhibit proliferation, induce reversible differentiation and prevent cell death in astrocyte lineage cells. Growth Factors, 11, 45-52.
7. Eddleston, M. and Mucke, L. (1993) Molecular profile of reactive astrocytes - implications for their role in neurologic disease. Neuroscience, 54, 15-36.
8. Engele, J. and Bohn, M. C. (1991) The neurotrophic effects of fibroblast growth factors on dopaminergic neurons in vitro are mediated by mesencephalic glia. J. Neurosci., 11, 3070-3078. [Published erratum appears in J. Neurosci., 1992, 12, 685].
9. Fann, M.-J. and Patterson, P. H. (1994) Depolarization differentially regulates the effects of bone morphogenetic protein (BMP)-2, BMP-6, and activin A on sympathetic neuronal phenotype. J. Neurochem., 63, 2074-2079.
10. Flanders, K. C., Ludecke, G., Engels, S., Cissel, D. S., Roberts, A. B., Kondaiah, P., Lafyatis, R., Sporn, M. B. and Unsicker, K. (1991) Localization and actions of transforming growth factor-beta-s in the embryonic nervous system. Development, 113, 183-191.
11. Flanders, K. C., Ludecke, G., Renzing, J., Hamm, C., Cissel, D. S. and Unsicker, K. (1993) Effects of TGF-beta-s and bFGF on astroglial cell growth and gene expression in vitro. Mol. Cell. Neurosci., 4, 406-417.
12. Forno, L. S., Delanney, L. E., Irwin, I. and Langston, J. W. (1993) Similarities and differences between MPTP-induced parkinsonism and Parkinson's disease-neuropathologic considerations. Adv. Neurol., 60, 600-608.
13. 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, 210, 209-218.
14. Graham, A., Francis-West, P., Brickell, P. and Lumsden, A. (1994) The signalling molecule BMP 4 mediates apoptosis in the rhombencephalic neural crest. Nature, 372, 684-686.
15. Grossi, R. E., Mehler, M. F., Mabie, P. C., Zang, Z., Santschi, L. and Kessler, J. A. (1996) Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron, 17, 595-606.
16. Hoffer, B. J., Hoffman, A., Bowenkamp, K., Huettl, P., Hudson, J., Martin, D., Lin, L.-F. H. and Gerhardt, G. A. (1994) Glial cell line-derived neurotrophic factor reverses toxin-induced injury to midbrain dopaminergic neurons in vivo. Neurosci. Lett., 182, 107-111.
17. Johansson, B. M. and Wiles, M. V. (1995) Evidence for involvement of activin A and bone morphogenetic protein 4 in mammalian mesoderm and hematopoietic development. Mol. Cell. Biol., 15, 141-151.
18. Jones, C. M., Lyons, K. M. and Hogan, B. L. (1991) Involvement of bone morphogenetic protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development, 111, 531-542.
19. Jones, C. M., Lyons, K. M., Lapan, P. M., Wright, C. V. and Hogan, B. L. (1992) DVR-4 (bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction. Development, 115, 639-647.
20. 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, 112-122.
21. Kingsley, D. M. (1994a) The TGF-beta superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev., 8, 133-146.
22. Kingsley, D. M. (1994b) What do BMPs do in mammals? Clues from the mouse short-ear mutation. Trends Genet., 10, 16-21.
23. Kopin, I. J. and Markey, S. P. (1988) MPTP toxicity: implications for research in Parkinson's disease. Annu. Rev. Neurosci., 11, 81-96.
24. Krieglstein, K. and Unsicker, K. (1994) Transforming growth factor-β promotes survival of midbrain dopaminergic neurons and protects them against N-methyl-4-phenylpyridinium ion toxicity. Neuroscience, 63, 1189-1196.
25. Krieglstein, K., Rufer, M., Suter-Crazzolara, C. and Unsicker, K. (1995a) Neural functions of the transforming growth factors β. Int. J. Dev. Neurosci., 13, 301-315.
26. + toxicity. EMBO J., 14, 736-742.
27. Krieglstein, K., Maysinger, D. and Unsicker, K. (1996) The survival of mesencephalic dopaminergic neurons to the neurotrophins BDNF and NT-4 requires priming with serum: comparison with members of the TGF-β superfamily and characterization of the serum-free culture system. J Neural Trans., Suppl., 47, 247-258.
28. Lin, L. F. H., Doherty, D. H., Lile, J. D., Bektesh, S. and Collins, F. (1993) GDNF - a glial cell line derived neurotrophic factor for midbrain dopaminergic neurons. Science, 260, 1130-1132.
29. Lyons, K. M., Jones, C. M. and Hogan, B. L. M. (1991) The DVR gene family in embryonic development. Trends Genet., 7, 408-412.
30. Martinou, J. C., Le Van Thai, A., Valette, A. and Weber, M. J. (1990) Transforming growth factor beta 1 is a potent survival factor for rat embryo motoneurons in culture. Dev. Brain Res., 52, 175-181.
31. Mehler, M. F., Marmur, R., Gross, R., Mabie, P. C., Zang, Z., Papavasiliou, A. and Kessler, J. A. (1995) Cytokines regulate the cellular phenotype of developing neural lineage species. Int. J. Dev. Neurosci., 13, 213-240.
32. Müller, H. W., Junghans, U. and Kappler, J. (1995) Astroglial neurotrophic and neurite-promoting factors. Phramacol. Ther., 65, 1-18.
33. Niswander, L. and Martin, G. R. (1993) FGF-4 and BMP-2 have opposite effects on limb growth. Nature, 361, 68-71.
34. Okano, H., Yoshikawa, S., Suzuki, A., Ueno, N., Kaizu, M., Okabe, M., Takahashi, T., Matsumoto, M., Sawamoto, K. and Mikoshiba, K. (1994) Cloning of a Drosophila melanogaster homologue of the mouse type-I bone morphogenetic protein-2/-4 receptor: a potential decapentaplegic receptor. Gene, 148, 203-209.
35. O'Malley, E. K., Sieber, B.-A., Morrison, R. S., Black, I. B. and Dreyfus, C. F. (1994) Nigral type I astrocytes release a soluble factor that increases dopaminergic neuron survival through mechanisms distinct from basic fibroblast growth factor. Brain Res., 647, 83-90.
36. + - specificity and impact of culture conditions, non-dopaminergic neurons, and astroglial cells. J. Neurosci. Res., 34, 382-393.
37. Paralkar, V. M., Weeks, B. S., Yu, Y. M., Kleinmann, H. K. and Reddi, A. H. (1992) Recombinant human bone morphogenetic protein 2B stimulates PC12 cell differentiation: potentiation and binding to type IV collagen. J. Cell Biol., 119, 1721-1728.
38. Poulsen, K. T., Armanini, M. P., Klein, R. D., Hynes, M. A., Phillips, H. S. and Rosenthal, A. (1994) TGFβ2 and TGFβ3 are potent survival factors for midbrain dopaminergic neurons. Neuron, 13, 1245-1252.
39. Reisert, I., Schuster, R., Zienecker, R. and Pilgrim, C. (1990) Prenatal development of mesencephalic and diencephalic dopaminergic systems in the male and female rat. Dev. Brain Res., 53, 222-229.
40. Reissmann, E., Ernsberger, U., Francis-West, P. H., Rueger, D., Brickell, P. M. and Rohrer, H. (1996) Involvement of bone morphogenetic protein-4 and bone morphogenetic protein-7 in the differentiation of the adrenergic phenotype in developing sympathetic neurons. Development, 122, 2079-2088.
41. Roberts, A. B. and Sporn, M. B. (1990) The transforming growth factor-βs. In Sporn, M. B. and Roberts, A. B. (eds), Peptide Growth Factors And Their Receptors I. Springer-Verlag, New York, pp. 419-472.
42. Rosen, V. and Thies, R. S. (1992) The BMP proteins in bone formation and repair. Trends Genet., 8, 97-102.
43. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
44. Sauermann, U., Meyermann, R. and Schluesener, H. J. (1992) Cloning of a novel TGF-beta related cytokine, the vgr, from rat brain - cloning of and comparison with homologous human cytokines. J. Neurosci. Res., 33, 142-147.
45. Schluesener, H. J. and Meyermann, R. (1994) Expression of BMP-6, a TGF-β related morphogenetic cytokine, in rat radial glial cells. Glia, 12, 161-164.
46. Schluesener, H. J., Meyermann, R. and Jung, S. (1995) Immunolocalization of vgr (BMP-6, DVR-6), a TGF-beta related cytokine, to Schwann cells of the rat peripheral nervous system: expression patterns are not modulated by autoimmune disease. Glia, 13, 75-78.
47. Shimoda, K., Sauve, Y., Marini, A., Schwartz, J. P. and Commisiong, J. W. (1992) A high percentage yield of tyrosine hydroxylase-positive cells from rat E14 mesencephalic cell culture. Brain Res., 586, 319-331.
48. Ten Dijke, P., Ichijo, H., Franzen, P., Schulz, P., Saras, J., Toyoshima, H., Heldin, C.-H. and Miyazono, K. (1993) Activin receptor-like kinases: a novel subclass of cell-surface receptors with predicted serine/threonine kinase activity. Oncogene, 8, 2879-2887.
49. Tomac, A., Lindqvist, E., Lin, L.-F. H., Ögren, S. O., Young, D., Hoffer, B. J. and Olson, L. (1995) Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature, 373, 335-339.
50. Tomizawa, K., Matsui, H., Kondo, E., Miyamoto, K., Tokuda, M., Itano, T., Nagahata, S., Akagi, T. and Hatase, O. (1995) Developmental alteration and neuron-specific expression of bone morphogenetic protein-6 (BMP-6) mRNA in rodent brain. Mol. Brain Res., 28, 122-128.
51. Unsicker, K., Flanders, K. C., Cissel, D. S., Lafyatis, R. and Sporn, M. B. (1991) Transforming growth factor beta isoforms in the adult rat central and peripheral nervous system. Neuroscience, 44, 613-625.
52. Unsicker, K., Suter-Crazzolara, C. and Krieglstein, K. (1995) Functions of growth factors in the development and maintenance of midbrain dopaminergic neurons: concepts, facts, and prospects of the transforming growth factor-β. CIBA Found. Symp., 196, 70-84.
53. 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.
54. Wall, N. A., Blessing, M., Wright, C. V. E. and Hogan, B. L. M. (1993) Biosynthesis and in vivo localization of the decapentaplegic-Vg-related protein, DVR-6 (bone morphogenetic protein 6). J. Cell Biol., 120, 493-502.
55. Wolf, N., Bieger, S., Unsicker, K. and Krieglstein, K. (1994) Does TGF-β regulate chromaffin cell proliferation? Soc. Neurosci. Abstr., 20, 1689.
56. 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, 1528-1534.
57. Zang, Z., Mehler, M. F., Marmur, R., Wozney, J. M. and Kessler, J. A. (1994) Bone morphogenetic proteins are expressed in developing mouse brain and are neurotrophic in vitro. Soc. Neurosci. Abstr., 20, 1307.