The expression of trkB and p75 and the role of BDNF in the developing neuromuscular system of the chick embryo

Development

Volumn 122, Issue 2, 1996, Pages 715-724

  McKay, S E ^a,c   Garner, A ^b   Caldero, J ^a,d   Tucker, R P ^a   Large, T ^b   Oppenheim, R W ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c YALE UNIVERSITY   (United States)

^d UNIVERSITY OF LLEIDA   (Spain)

Author keywords

Chick; Motoneurons; Neurotrophin receptors; Neurotrophins

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; COMPLEMENTARY RNA; DIGOXIGENIN; MESSENGER RNA; NERVE GROWTH FACTOR RECEPTOR; NEUROTROPHIN RECEPTOR; PROTEIN TYROSINE KINASE;

ANIMAL TISSUE; ARTICLE; CHICK EMBRYO; DEVELOPMENTAL GENETICS; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MOTONEURON; MUSCLE INNERVATION; NERVE CELL NECROSIS; NEUROMUSCULAR SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA PROBE; SPINAL CORD MOTONEURON; TISSUE SECTION; VENTRAL ROOT;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL SURVIVAL; CHICK EMBRYO; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LIMB BUD; MOTOR NEURONS; MUSCLE, SKELETAL; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; ORGAN SPECIFICITY; RECEPTOR, CILIARY NEUROTROPHIC FACTOR; RECEPTORS, NERVE GROWTH FACTOR; RNA, MESSENGER; SPINAL CORD;

EID: 0030038141     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (99)

1. Alderson, R. F., Alterman, A. L., Barde, Y. -A., and Lindsay, R. M. (1990). Brain-derived neurotrophic factor increases the survival and differentiated functions of rat septal cholinergic neurons in culture. Neuron 5, 297-306.
2. Arakawa, Y., Sendtner. M., and Thoenen, H. (1990). Survival effect of ciliary neurotrophic factor (CNTF) on chick embryonic motoneurons in culture: Comparison with other neurotrophic factors and cytokines. J. Neurosci. 10, 3507-3515.
3. Averbuch-Heller, L., Pruginin, M., Kahane, N., Tsoulfas, P., Parada, L., Rosenthal, A., and Kalcheim, C. (1994). Neurotrophin-3 stimulates the differentiation of motoneurons from avian neural tube progenitor cells. Proc. Natl. Acad. Sci. USA 91, 3247-3251.
4. Barbacid, M. (1993). Nerve growth factor: a tale of two receptors. Oncogene 8, 2033-2042.
5. Barde, Y.-A., Edgar, D., and Thoenen, H. (1982). Purification of a new neurotrophic factor from mammalian brain EMBO J. 5, 549-553.
6. Bhattacharyya, A., Oppenheim, R. W., Prevette, D., Moore, B. W., Brackenbury, R. and Ratner, N. (1992). S100 is present in developing chicken neurons and Schwann cells and promotes motor neuron survival in vivo. J. Neurobiol. 23, 451 -466.
7. Bloch-Gallego, E., Huchet, M., El M'Hamdi, H., Xie, F.-K., Tanaka, H. and Henderson, C. E. (1991). Survival in vitro of identified motoneurons purified by novel antibody-based methods is selectively enhanced by muscle-derived factors. Development 111, 221-232.
8. Bothwell, M. (1995). Functional interactions of neurotrophins and neurotrophin receptors. Ann. Rev. Neurosci. 18, 223-253.
9. Brenneman, D. E., Neale, E. A., Foster, G. A., d'Autremont, S. W., and Westbrook, G. L. (1987). Nonneuronal cells mediate neurotrophic action of vasoactive intestinal peptide J. Cell Biol. 104, 1603-1610.
10. Buchman, V. L. and Davies, A. M. (1993). Different neurotrophins are expressed and act in a developmental sequence to promote the survival of embryonic sensory neurons Development 118, 989-1001.
11. Caroni, P. and Grandes, P. (1990). Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated levels of insulin-like growth factors. J. Cell Biol. 110, 1307-1317
12. Chao, M. V. (1992). Neurotrophin receptors: A window into neuronal differentiation. Neuron 9, 583-593.
13. Chao, M. V. (1994). The p75 neurotrophin receptor. J. Neurobiol. 25, 1373-1385.
14. Clark, P. G. H. and Oppenheim, R. W. (1995). Neuron death in vertebrate development: in vivo methods. In Methods in Cell Biology Cell Death vol. 46 (ed. Schwanz, L. M. and Osborn, B. A.), pp. 277-321. New York: Academic Press.
15. Conover, J.C., Erickson, J.T., Katz, D.M., Bianchi, L.M., Poveymirou, W .T., McClain, J., Pan, L., Helgren, M., Ip, N.Y., Boland, P., Friedman, B., Wiegand, S., Vejsada, R., Kato, A.C., DeChiara, T.M. and Yancopoulis, G.D., (1995). Neuronal deficits, not involving motor neurons in mice lacking BDNF and/or NT-4. Nature 375, 235-238.
16. Dahm, L. M. and Landmesser, L. T. (1988). The regulation of intramuscular nerve branching during normal development and following activity blockade. Dev. Biol. 130, 621 -644.
17. Dechant, G., Biffo, S., Okazawa, H., Kolbeck, R., Pottgiesser, J. and Barde, Y.-A. (1993). Expression and binding characteristics of the chick BDNF receptor trkB. Development 119, 545-558.
18. DiStefano, P. S., Friedman, B., Radziejewski, C., Alexander, C., Boland, P., Schick, C. M., Lindsay, R. M. and Wiegand, S. J. (1992). The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron 8, 983-993
19. Dohrmann, U., Edgar, D., Sendtner, M. and Thoenen, H. (1986). Muscle-derived factors that support survival and promote fiber outgrowth from embryonic chick spinal motor neurons in culture. Dev. Biol. 118, 209-221
20. Dohrmann, U., Edgar, D. and Thoenen, H. (1987). Distinct neurotrophic factors from skeletal muscle and the central nervous system interact synergistically to support the survival of cultured embryonic spinal motor neurons Dev Biol 124, 145-152
21. Dubrowsky, R. T., Werner, M. H., Castellino, A. M., Chao, M. V. and Hannum, Y. A. (1994). Activation of the sphingomyelin cycle pathway through the low-affinity neurotrophin receptor. Science 265, 1596-1599.
22. Eagleson, K. L., Raju, T. R., and Bennett, M. R. (1985). Motoneurone survival is induced by immatrue astrocytes from developing avian spinal cord. Dev. Brain Res 17, 95-104.
23. Ernfors, P., Hallböök, F., Ebeudal, T., Shooter, E.M., Radekc, M.J., Misko, T.P., and Persson, Håkan (1988). Developmental and regional expression of β-nerve growth factor receptor mRNA in the chick and rat. Neuron 1,983-996.
24. Ernfors, P., Lee, K.-F. and Jaenisch. R. (1994). Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368, 147-150.
25. Escandon, E., Soppet, D., Rosenthal, A., Mendoza-Ramirez, J.-L., Szonyi, E., Burton, L. E., Henderson, C. E., Parada, L. F. and Nikolics, K. (1994). Regulation of neurotrophin receptor expression during embryonic and postnatal development. J. Neurosci: 14, 2054-2068
26. Funakoshi, H., Bellvardo, N., Arenas, E., Yamamoto, Y., Casabona, A., Persson, H., and Ibáñez, C.F. (1995). Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons. Science 268, 1495-1499.
27. Gorin, P. D, and Johnson, E. M. (1979). Experimental autoimmune model of nerve growth factor deprivation: Effects on developing peripheral sympathetic and sensory neurons. Proc. Natl Acad. Sci. 76, 5382-5386.
28. Hallbook, F., Ibanez, C. F., Ebendal, T., and Persson, H. (1993), Cellular localization of brain-derived neurotrophic factor and neurotrophin-3 mRNA expression in the early chicken embryo. Eur J Neurosci. 5, 1-14.
29. Hamburger, V. (1934). The effects of wing bud extirpation on the development of the central nervous system in the chick embryo. J. Exp. Zool 68, 449-494.
30. Hamburger, V. (1975) Cell death in the development of the lateral motor column of the chick embryo J. Comp. Neurol. 160, 535-546.
31. Hamburger, V. and Oppenheim, R. W. (1982). Naturally occurring neuronal death in vertebrates. Neurosci. Comment. 1, 39-55.
32. Hefti, F. (1986). Nerve growth factor (NGF) promotes survival of septal cholinergic neurons after fimbrial transection. J. Neurosci. 6, 2155-2162.
33. Hempstead, B. L., Martin-Zanca. D., Kaplan. D. R., Parada, L. F. and Chao, M. V. (1991). High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor. Nature 350, 678-682.
34. Henderson, C. E., Camu, W., Mettling, C, Govin, A., Poulsen, K., Karihaloo, M., Rullamas, J., Evans, T., McMahon, S. B., Armanini,. M. P., Berkemeier, L., Phillips, H. S. and Rosenthal. A. (1993). Neurotrophins promote motor neuron survival and are present in the embryonic limb bud. Nature 331, 266-270.
35. Henderson, C. E., Phillips, H. S., Pollock, R. A., Davies, A. M., Lemeulle, C., Armanini, M., Simpson, L. C., Moffet, B., Vandlen, R. A., Koliatsos, V. E., and The Rosenthal, A. (1995). GDNF: A potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266, 1062-1064.
36. Heuer, J. G., Fatemie-Nainie, S., Wheeler, E. F. and Bothwell, M. (1990a). Structure and developmental expression of the chicken NGF receptor Dev. Biol. 137, 287-304.
37. Heuer, J. G., von Bartheld, C. S., Kinoshita, Y., Evers, P. C. and Bothwell, M. (1990b). Alternating phases of FGF receptor and NGF receptor expression in the developing chicken nervous system. Neuron 5, 283-296.
38. Hofer, M. M. and Barde, Y.-A. (1988). Brain-derived neurotrophic factor prevents neuronal death in vivo. Nature 331, 261-262.
39. Hollyday, M. and Hamburger, V. (1976). Reduction of the naturally-occurring motor neuron loss by enlargement of the periphery. J. Comp. Neurol. 170, 311-320.
40. trk mRNA marks NGF-responsive forebrain neurons: Evidence that trk gene expression is induced by NGF. Neuron 9, 465-478.
41. Houenou, L. J., Pincon-Raymond, M., Garcia, L., Harris, A. J., and Rieger, F. (1990) Neuromuscular development following tetrodotoxin-induced inactivity in mouse embryos J. Neurobiol. 21, 1249-1261.
42. Houenou, L. J., Haverkamp, L. J., McManaman, J. L., and Oppenhwim, R. W. (1991). The regulation of motoneuron survival and differentiation by putative muscle-derived neurotrophic agents: Neuromuscular activity and innervation. Development Supplement 2, 149-155.
43. Houenou, L. J., Li, L., Lo, A. C., Yan, Q., and Oppenheim, R. W. (1994). Programmed and axotomy-induced motoneuron death and their prevention by neurotrophic agents: A comparison between chick and mouse. Prog. Brain Res. 102, 217-226
44. Hughes, R. A., Sendtner, M., Thoenen, H. (1993). Members of several gene families influence survival of rat motoneurons in vitro and in vivo. J. Neurosci. Res. 36, 663-671.
45. Ibanez, C. F., Ernfors, P., Timmusk, T., Ip, N. Y., Arenas, E., Yancopoulos, G. D. and Persson, H. (1993). Neurotrophin-4 is a target-derived neurotrophic factor for neurons of the trigeminal ganglion. Development 117, 1345-1353.
46. Johnson, J. E., Barde, Y.-A., Schwab, M. and Thoenen, H. (1986). Brain-derived neurotrophic factor supports the survival of cultured rat retinal ganglion cells. J. Neurosci. 6, 3031-3038.
47. Johnson, J. E. and Oppenheim, R. W. (1994). Keeping track of changing neurotrophic theory. Curr. Biol. 4, 662-665.
48. Jones, K. R., Fainas, I., Backer, C. and Reichardt, L. F. (1994). Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motoneuron development. Cell 76, 989-999.
49. Klein, R., Jing, S., Nanduri, V., O'Rourke, E., and Barbacid, M. (1991). The trk proto-oncogene encodes a receptor for nerve growth factor. Cell65, 189-197.
50. Klein, R., Smeyne, R. J., Wurst, W., Long, L. K., Auerbach, B. A., Joyner, A. L. and Barbacid, M. (1993). Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death. Cell 75, 113-122.
51. Koliatsos, V. E., Clatterbuck, R. E., Winslow, J. W., Cayouette, M. H. and Price, D. L. (1993). Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo. Neuron 10, 359-367.
52. Koliatsos, V. E., Cayouette, M. C., Berkemeir, L. R., Clatterbuck, R. E., Price, D. L. and Rosenthal, A. (1994). Neurotrophin 4/5 is a trophic factor for mammalian facial motor neurons. Proc. Nat. Acad. Sci. USA 91, 3304-3308
53. Landmesser, L. (1992). The relationship of intramuscular nerve branching and synaptogenesis to motoneuron survival. J. Neurobiol. 23, 1131-1139.
54. Landmesser, L. T. and O'Donovan, M. J. (1984). The activation patterns of embryonic chick hindlimb muscles recorded in ovo and in an isolated spinal cord preparation. J Physiol. 347, 189-204.
55. Landmesser, L., Dahm. L., Schultz, K.,. and Rutishauser, U. (1988). Distinct roles for adhesion molecules during innervation of embryonic chick muscle. Dev. Biol. 130, 645-670.
56. Landmesser, L, Dahm, L., Tang, J., and Rutishauser, U. (1990). Polysilaic acid as a regulator of intramuscular nerve branching during embryonic development. Neuron 4, 655-667.
57. Large, T. H., Weskamp, G., Helder, J. C., Radeke, M. J., Misko, T. P., Shooter, E. M. and Reichardt, L. F. (1989). Structure and developmental expression of the nerve growth factor receptor in the chicken central nervous system. Neuron 2, 1123-1134.
58. Larmet, Y., Dolphin, A. C. and Davies, A. M. (1992). Intracellular calcium regulates the survival of early sensory neurons before they become dependent on neurotrophic factors. Neuron 9, 563-574.
59. Lee, K.-F., Li, E., Huber, J., Landis, S. C., Sharpe. A. H., Chao, M. V. and Jaenisch, R. (1992). Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69, 737-749.
60. Levi-Montalcini, R. and Hamburger, V. (1953). A diffusable agent of mouse sarcoma producing hyperplasia of sympathetic ganglia and hyperneurotization of viscera in the chick embryo. J. Exp. Zool. 123, 233-287
61. Li, L., Oppenheim, R. W., Lei, M. and Houenou, L. (1994). Neurotrophic agents prevent motoneuron death following sciatic nerve section in the neonatal mouse. J. Neurobiol. 25, 759-766.
62. Liu, X., Ernfors, P., Wu, H. and Jaenisch, R. (1995). Sensory but not motor neuron deficits in mice lacking NT-4 and BDNF. Nature 375, 238-241.
63. Lindsay, R., Thoenen, H. and Barde, Y.-A. (1985). Placode and neural crest-derived sensory neurons are responsive at early developmental stages to brain-derived neurotrophic factor. Dev. Biol. 112, 319-328.
64. Lohof, A. M., Ip, N. Y. and Poo, M.-M. (1993). Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363. 350-353.
65. Maisonpiere, P. C., Belluscio, L., Squinto, S., Ip, N. Y., Furth, M. E., Lindsay, R. M., and Yancopoulis, G. D. (1990). Neurotrophin-3: A neurotrophic factor related to NGF and BDNF. Science 247, 1446-1451.
66. Marchetti, D., Haverkamp, L. J., Clark, R. C. and McManaman, J. L. (1991). Ontogeny of high- and low-affinity nerve growth factor receptors in the lumbar spinal cord of the developing chick embryo. Dev. Biol. 148, 306-313.
67. MeKay, S. E., Herzog, K.-H., Garner, A., Tucker, R. P., Large, T. and Oppenheim, R, W, (1993). Expression of BDNF and trkB in the developing neuromuscular system. Soc. Neurosci., Abst.
68. Meakin, S. O. and Shooter, E. M. (1992). The nerve growth factor family of receptors. Trends Neurosci. 15, 323-331.
69. Mettling, C., Gouin, A., Robinson, M., El M'Hamdi, H., Camu, W., Bloch-Gallego, E., Buisson, B., Tanaka, H., Davies, A. M. and Henderson, C. E. (1995). Survival of newly post-mitotic motoneurons is transiently independent of exogenous trophic support. J. Neurosci. 15, 3128-3137.
70. Neff, N. T., Prevette, D., Houenou, L. J., Lewis, M. E., Glicksman, M. A., Yin, Q. -W., and Oppenehim, R. W. (1993). Insulin-like growth factors. Putative muscle-derived trophic agents that promote motoneuron survival. J. Neuorbiol. 24, 1578-1588.
71. Newsome, A., Prevette, D., Johnson, J., Wang, S. and Oppenheim, R. W. (1994). Regulation of survival in developing non-dopaminergic neurons by ghal cell line-derived neurotrophic factor (GDNF). Soc. Neurosci. Abst.
72. Okado, N. and Oppenheim, R. W. (1984). Cell death of motoneurons in the chick embryo spinal cord IX. The loss of motoneuorns following removal of afferent inputs. Journal of Neuroscience 4, 1639-1652
73. Oppenheim, R. W. (1989). The neurotrophic theory and naturally occurring motoneuron death. Trends in Neuroscience 12, 252-255.
74. Oppenheim, R. W. and Reitzel, J. (1975). Ontogeny of behavioral sensitivity to strychnine in the chick embryo: Evidence for the early onset of CNS inhibition. Brain, Behavior. Evolution 11, 130-159.
75. Oppenheim, R. W., Haverkamp, L. J., Prevette, D., McManaman, J. L. and Appel, S. H. (1988) Reduction of naturally occurring motoneuron death in vivo by a target-derived neurotrophic factor. Science 240, 919-922.
76. Oppenheim, R. W., Prevette, D., Yin, Q.-W., Collins, F. and MacDonald, J. (1991). Control of embryonic motoneuron survival in vivo by ciliary neurotrophic factor. Science 251, 1616-1618.
77. Oppenheim, R. W., Yin, Q.-W., Prevette, D., and Yan, Q. (1992). Brain-derived neurtrophic factor rescues developing avian motoneurons from cell death. Nature 360, 755-757.
78. Oppenheim, R. W., Prevette, D., Haverkamp, L. J., Houenou, L., Yin, Q.-W. and McManaman, J. (1993a) Biological studies of a putative avian muscle-derived neurtrophic factor that prevents naturally occurring motoneuron death in vivo. J. Neurobiol. 24, 1065-1079.
79. Oppenheim, R. W., Prevette, D., McKay, S. and Cardwell, C. J. (1993b). Motoneuron survival in vivo after treatment with combinations of muscle-and CNS-derived trophic factors. Soc. Neurosci. Abst.
80. Oppenheim, R. W., Prevette, D., Houenou, L., Rohrer, H., Zackenfels, K., Caroni, P. and Zapf, J. (1994) The role of insulin-like growth factors in the differentiation and survival of developing avian motoneurons in vivo. Soc. Neurosci. Abst.
81. Oppenheim, R. W., Houenou, L. J., Johnson, J. E., Lin, L-f. H., Li, L., Lo, A. C., Newsome, A. L., Prevette, D. M. and Wang, S. (1995). Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature 373, 344-346.
82. Phillips, H. S., Hains, J. M., Laramee, G. R., Rosenthal, A. and Winslow, J. W. (1990). Widespread expression of BDNF but not NT-3 by target areas of basal forebrain cholinergic neurons. Science 250, 290-294.
83. Pittman, R. and Oppenheim, R. W. (1979). Cell death of motoneurons in the chick embryo spinal cord: IV. Evidence that a functional neuromuscular teraction Is involved in the regulation of naturally occurring cell death and the stabilization of synapses. J. Comp. Neurol. 187, 425-446.
84. Pollack, E. D., Muhiach, W. L. and Liebig, V. (1981). Neurotropic influence of mesenchymal limb target tissue on spinal cord neurite outgrowth in vitro. J. Comp. Neural. 200, 393-405.
85. Prevette, D., Caldero, J., D'Costa, A., Mei, X. and Oppenheim, R. W. (1994). Survival and death of developing sensory and motor neurons in vivo following target deletion: Effects of neurotrophic agents. Soc. Neurosci. Abst.
86. Provine, R. R. (1971). Embryonic spinal cord- Synchrony and spatial distribution of polyneuronal burst discharges. Brain Res. 29, 155-158.
87. Rabizadeh, S., Oh, J., Zhong, L.-T., Yang, J., Bitler, C. M., Butcher, L. L. and Bredesen. D. E. (1993). Induction of apoptosis by the low-affinity NGF receptor. Science 261, 345-348.
88. Radeke, M. J. and Feinstein, S. C. (1991). Analytical purification of the slow, high affinity NGF receptor: Identification of a novel 135 kd polypeptide. Neuron 7, 141-150.
89. Ripley, K. L. and Provine, R. R. (1972). Neural correlates of embryonic motility in the chick. Brain Res 45, 127-134.
90. Schaeren-Wiemers, N. and Gerfin-Moser, A. (1993). A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labeled cRNA probes. Histochem. 100, 431-440.
91. Sendtner, M., Holtmann, B., Kolbeck, R., Thoenen, H., and Barde, Y.-A. (1992). Brain-derived neurotrophic factor and neurotrophin-3 prevent the death of motoneurons in newborn rats after nerve section. Nature 360, 757-759.
92. Snider, W. D. (1994). Functions of the neurotrophins during nervous system development: What the knockouts are teaching us. Cell 77, 627-638.
93. Sofroniew, M. V., Galletly. N. P., Isacson, O. and Svendsen. C. N. (1990). Survival of adult basal forebrain cholinergic neurons after loss of target neurons. Science 24, 338-342.
94. Verge, V. M. K., Merlio, J.-P., Grondin, J., Ernfors, P., Persson, H., Riopelle, R. J., Hokfelt, T. and Richardson, P. M. (1992). Colocalization of NGF binding sites, trk mRNA, and low-affinity NGF receptor mRN'A in primary sensory neurons: Responses to injury and infusion of NGF J. Neurosci. 12, 4011-4022.
95. vonBartheld, C.S., Schober, A., Kinoshita, Y., Williams, R., Ebendal, T. and Bothwell, M. (1995). Noradrenergic neurons in the locus coerulius of birds express TrkA. transport NGF. and respond to NGF. J Neurosci. 15, 2225-2239.
96. Wang, T., Xic, K. and Lu, B. (1995). Neurotrophins promote maturation of developing neuromuscular synapses. J. Neurosci. 15, 4796-4805.
97. Weskamp, G, and Reichardt, L. F. (1991). Evidence that biological activity of NGF is mediated through a novel subclass of high affinity receptors. Neuron 6, 649-663.
98. Wright, E. M., Vogel, K. S., and Davies, A. M. (1992). Neurotrophic factors promote the maturation of developing sensory neurons before they become dependent on these factors for survival. Neuron 9, 139-150.
99. Yan, Q., Elliot, J. L. and Snider, W. D. (1992). Brain-derived neurotrophic factor rescues spinal cord motor neurons from axotomy-induced cell death. Nature 360, 753-755.