Time-dependence and cell-type specificity of synergistic neurotrophin actions on spiral ganglion neurons

Journal of Comparative Neurology

Volumn 402, Issue 1, 1998, Pages 129-139

  Mou, Kewa ^a   Adamson, Crista L ^a   Davis, Robin L ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

BDNF; Cochlea; Inner ear; NT 3; Primary auditory neuron

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; PERIPHERIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SPECIFICITY; CELL SURVIVAL; CONTROLLED STUDY; GERBIL; MOUSE; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SPIRAL GANGLION;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL SURVIVAL; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; GERBILLINAE; NERVE GROWTH FACTORS; NEURONS, AFFERENT; NEUROTROPHIN 3; SPIRAL GANGLION; TIME FACTORS;

EID: 0032495074     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19981207)402:1<129::AID-CNE9>3.0.CO;2-A     Document Type: Article

References (78)

1. Airaksinen, M.S., M. Koltzenburg, G.R. Lewin, Y. Masu, C. Helbig, E. Wolf, G. Brem, K.V. Toyka, H. Thoenen, and M. Meyer (1996) Specific subtypes of cutaneous mechanoreceptors require neurotrophin-3 following peripheral target innervation. Neuron 16:287-295.
2. Anniko, M., W. Arnold, T. Stigbrand, and A. Ström (1995) The human spiral ganglion. ORL 57:68-77.
3. Berglund, A.M. and D.K. Ryugo (1986) A monoclonal antibody labels type II neurons of the spiral ganglion. Brain Res. 353:327-332.
4. Berglund, A.M. and D.K. Ryugo (1987) Hair cell innervation by spiral ganglion neurons in the mouse. J. Comp. Neurol. 255:560-570.
5. Berglund, A.M. and D.K. Ryugo (1991) Neurofilament antibodies and spiral ganglion neurons of the mammalian cochlea. J. Comp. Neurol. 306:393-408.
6. Bernd, P., D. Zhang, L. Yao, and I. Rozenberg (1994) The potential role of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 in avian cochlear and vestibular ganglion development. Int. J. Dev. Neurosci. 12:709-723.
7. Bruchman, V.L. and A.M. Davies (1993) Different neurotrophins are expressed and act in a developmental sequence to promote the survival of embryonic sensory neurons. Development 118:989-1001.
8. Chalazonitis, A., J. Kalberg, D.R. Twardzik, R.S. Morrison, and J.A. Kessler (1992) Transforming growth factor beta has neurotrophic actions on sensory neurons in vitro and is synergistic with nerve growth factor. Dev. Biol. 152:121-132.
9. Chao, M.V. (1992) Neurotrophin receptors: A window into neuronal differentiation. Neuron 9:583-593.
10. Chiong, C.M., B.J. Burgess, and J.B. Nadol, Jr. (1993) Postnatal maturation of human spiral ganglion cells: Light and electron microscope observations. Hear. Res. 67:211-219.
11. Dau, J. and R.J. Wenthold (1985) Immunocytochemical localization of neurofilament subunits in the spiral ganglion of normal and neomycin-treated guinea pigs. Hear. Res. 42:253-264.
12. Després, G. and R. Romand (1994) Neurotrophins and the development of cochlear innervation. Life Sci. 18:1291-1297.
13. Després, G., G.-P. Leger, D. Dahl, and R. Romand. (1994) Distribution of cytoskeletal proteins (Neurofilaments, Peripherin and MAP-tau) in the cochlea of the human fetus. Acta Otolaryngol (Stockh) 114:377-381.
14. Echteler, S.M. (1992) Developmental segregation in the afferent projections to mammalian auditory hair cells. Proc. Natl. Acad. Sci. USA 89:6324-6327.
15. ElShamy, W.M. and P. Ernfors (1996) A local action of neurotrophin-3 prevents the death of proliferating sensory neuron precursor cells. Neuron 16:963-972.
16. Ernfors, P., J.-P. Merlio, and H. Persson (1992) Cells expressing mRNA for neurotrophins and their receptors during embryonic rat development. Eur. J. Neurosci. 4:1140-1158.
17. Ernfors, P., T. Van De Water, J. Loring, and R. Jaenisch (1995) Complementary roles of BDNF and NT-3 in vestibular and auditory development. Neuron 14:1153-1164.
18. Fariñas, I., K.R. Jones, C. Backus, X.-Y. Wang, and L.F. Reichardt (1994) Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369:658-661.
19. Fariñas, I., C.K. Yoshida, C. Backus, and L.F. Reichardt (1996) Lack of neurotrophin-3 results in death of spinal sensory neurons and premature differentiation of their precursors. Neuron 17:1065-1078.
20. Friedman, W.J., I.B. Black, H. Persson, and C.F. Ibáñez (1995) Synergistic trophic actions on rat basal forebrain neurons revealed by a synthetic NGF/BDNF chimaeric molecule. Eur. J. Neurosci. 7:656-662.
21. Fritzsch, B., I. Silos-Santiago, R. Smeyne, A.M. Fagan, and M. Barbacid (1995) Reduction and loss of inner ear innervation in trkB and trkC receptor knockout mice: A whole mount DiI and scanning electron microscope analysis. Audit. Neurosci. 1:401-417.
22. Fritzsch, B., I. Fariñas, and L.F. Reichardt (1997a) Lack of neurotrophin 3 causes losses of both classes of spiral ganglion neurons in the cochlea in a region-specific fashion. J. Neurosci. 17:6213-6225.
23. Fritzsch, B., I. Silos-Santiago, L.M. Bianchi, and I. Fariñas, (1997b) Effects of neurotrophin and neurotrophin receptor disruption on the afferent inner ear innervation. Cell Dev. Biol. 8:277-284.
24. Gaese, F., R. Kolbeck, and Y.-A. Barde (1994) Sensory ganglia require neurotrophin-3 early in development. Development 120:1613-1619.
25. Ghosh, A. and M.E. Greenberg (1995) Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron 15:89-103.
26. Ginzberg, R.D. and O.K. Morest (1983) A study of cochlear innervation in the young cat with the Golgi method. Hear. Res. 10:227-246.
27. Hafidi, A., G. Després, and R. Romand (1990) Cochlear innervation in the developing rat: An immunocytochemical study of neurofilament and spectrin proteins. J. Comp. Neurol. 300:153-161.
28. Hafidi, A., G. Després, and R. Romand (1993) Ontogenesis of type II spiral ganglion neurons during development: Peripherin immunohistochemistry. Int. J. Dev. Neurosci. 11:507-512.
29. i within a set range. J. Neurosci. 17:1959-1970.
30. Heidemann, S.R., H.C. Joshi, A. Schechter, J.R. Fletcher, and M. Bothwell (1985) Synergistic effects of cyclic AMP and nerve growth factor on neurite outgrowth and microtubule stability of PC12 cells. J. Cell Biol. 100:916-927.
31. Hossain, W.A., A. Rutledge, and D.K. Morest (1998) Interaction of NT3 with BDNF and FGF-2 in the development of the cochlear ganglion (CG) neurons in vitro. Abstracts of the Association of Research for Otolaryngology 21:648.
32. Ip, N.Y., T.N. Stitt, P. Tapley, R. Klein, D.J. Glass, J. Fandl, L.A. Greene, M. Barbacid, and G.D. Yancopoulos (1993) Similarities and differences in the way neurotrophins interact with the Trk receptors in neuronal and nonneuronal cells. Neuron 10:137-149.
33. Kaplan, D.R. and R.M. Stephens (1994) Neurotrophin signal transduction by the Trk receptor. J. Neurobiol. 25:1404-1417.
34. Kellerhals, B., H. Engstrom, and H.W. Ades (1967) Die Morphologie des Ganglion spirale Cochleae. Acta Otolaryngol. Suppl. 226:6-33.
35. Kiang, N.Y.-S., J.M. Rho, C.C. Northrop, M.C. Liberman, and D. Ryugo (1982) Hair-cell innervation by spiral ganglion cells in adult cat. Science 217:175-177.
36. Kikuchi, K. and D. Hilding (1965) The development of the organ of Corti in the mouse. Acta Otolaryngol. 60:207-222.
37. Lewin, G.R., Y.-A. Barde (1996) Physiology of the neurotrophins. Ann. Rev. Neurosci. 19:289-317.
38. Lim, D.J. and M. Anniko (1985) Developmental morphology of the mouse inner ear. Acta Otolaryngol. Suppl. 422:5-69.
39. Liu, Y., R. Dyck, and M. Cynader (1994) The correlation between cortical neuron maturation and neurofilament phosphorylation: A developmental study of phosphorylated 200 kDa neurofilament protein in cat visual cortex. Brain Res. Dev. Brain Res. 81:151-161.
40. McMahon, S.B., M.P. Armanini, L.H. Ling, and H.S. Phillips (1994) Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12:1161-1171.
41. Memberg, S.P. and A.K. Hall (1995) Proliferation, differentiation, and survival of rat sensory neuron precursors in vitro require specific trophic factors. Mol. Cell. Neurosci. 6:323-335.
42. Minichello, L., F. Piehl, E. Vazquez, T. Schimmang, T. Hökfelt, J. Represa, and R. Klein (1995) Differential effects of combined trk receptor mutations on dorsal root ganglian and inner ear sensory neurons. Development 121:4067-4075.
43. Morrison, C.F., J. McAllister, V. Lyons, K. Chapman, and J.P. Quinn (1994) The rat preprotachykinin-A promoter is regulated in PC12 cells by the synergistic action of multiple stimuli. Neurosci. Lett. 181:117-120.
44. Mou, K., C.L. Hunsberger, J.M. Cleary, and R.L. Davis (1997) Synergistic effects of BDNF and NT-3 on postnatal spiral ganglion neurons. J. Comp. Neurol. 386:529-539.
45. Mulderry, P.K. (1993) Synergistic regulation of vasoactive intestinal polypeptide expression by cyclic AMP and calcium in newborn but not adult rat sensory neurons in culture. Neuroscience 53:229-238.
46. Nakai, Y. and D. Hilding (1968) Cochlear development. Acta Otolaryngol. 66:369-385.
47. Nishimura, T., I. Kon, S. Awataguchi, M. Ishida, and Y. Yamamoto (1965) Submicroscopic studies on the spiral ganglion in guinea pigs: 1. The fine structure of the normal spiral ganglion. Hirosaki Med. J. 17:1-19.
48. Perkins, R.E. and D.K. Morest (1975) A study of cochlear innervation patterns in cats and rats with the Golgi method and Normarski optics. J. Comp. Neurol. 163:129-158.
49. Pirvola, U., E. Lehtonen, and J. Ylikoski (1991) Spatiotemporal development of cochlear innervation and hair cell differentiation in the rat. Hear. Res. 52:345-355.
50. Pirvola, U., J. Ylikoski, J. Palgi, E. Lehtonen, U. Arumar, and M. Saarma (1992) Brain-derived neurotrophic factor and neurotrophin 3 mRNAs in the peripheral target fields of developing inner ear ganglia. Proc. Natl. Acad. Sci. USA 89:9915-9919.
51. Romand, R., H. Sobkowicz, M. Emmerling, D. Whitlon, and D. Dahl (1990) Patterns of neurofilament stain in the spiral ganglion of the developing and adult mouse. Hear. Res. 49:119-126.
52. Roth, B. and V. Bruns (1992a) Postnatal development of the rat organ of Corti: I. General morphology, basilar membrane, tectorial membrane and border cells. Anat. Embryol. 185:559-569.
53. Roth, B. and V. Bruns (1992b) Postnatal development of the rat organ of Corti II. Hair cell receptors and their supporting elements. Anat. Embryol. 155:571-581.
54. Rubel, E.W. (1978) Ontogeny of structure and function in the vertebrate auditory system. In A. Autrum, R. Jung, W.R. Loewenstein, D.M. McKay, and H.L. Teuber (eds): Handbook of Sensory Physiology. Berlin: Springer-Verlag, pp. 135-237.
55. Ruben, R. J. (1967) Development of the inner ear of the mouse: A radioautographic study of terminal mitosis. Acta. Otolayngol. Suppl. 220:5-44.
56. Ryan, A. (1976) Hearing sensitivity of the mongolian gerbil, Meriones unguiculatus. J. Acoust. Soc. Am. 59:1222-1226.
57. Ryugo, D.K. (1992) The auditory nerve: Peripheral innervation, cell body morphology, and central projections. In, D.W. Webster, A.N. Popper, and R.R. Fay (eds): The Mammalian Auditory Pathway: Neuroanatomy. New York: Springer-Verlag, pp. 23-65.
58. Schecterson, L.C. and M. Bothwell (1992) Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron 9:449-463.
59. Schecterson, L.C. and M. Bothwell (1994) Neurotrophin and neurotrophin receptor mRNA expression in developing inner ear. Hear. Res. 73:92-100.
60. Schlessinger, J. and A. Ullrich (1992) Growth factor signaling by receptor tyrosine kinases. Neuron 9:383-391.
61. Schwartz, M.L., P.S. Shneidman, J. Bruce, and W.W. Schlaepfer (1994) Stabilization of neurofilament transcripts during postnatal development. Brain Res. Mol. Brain Res. 27:215-220.
62. Sher, A.E. (1971) The embryonic and postnatal development of the inner ear of the mouse. Acta Otolaryngol. Suppl. 285:5-76.
63. Shnerson, A. and R. Pujol (1983) Development: Anatomy, electrophysiology and behavior. In J.F. Willot (ed): The Auditory Psychobiology of the Mouse. Springfield IL: C.C. Thomas, pp. 395-425.
64. Snider, W.D. (1994) Functions of the neurotrophins during nervous system development: What the knockouts are teaching us. Cell 77:627-638.
65. Sobkowicz, H.M. and J.E. Rose (1983) Innervation of the organ of Corti of the fetal mouse in culture. In R. Romand (ed): Development of Auditory and Vestibular Systems. New York: Academic Press, pp. 27-45.
66. Souter, M., G. Nevill, and A. Forge (1997) Postnatal maturation of the organ of Corti in gerbils: Morphology and physiological responses. J. Comp. Neurol. 386:635-651.
67. Spoendlin, H. (1973) The innervation of the cochlea receptor. In A.R. Møiler (ed): Mechanisms in Hearing. New York: Academic Press, pp. 185-229.
68. Stoop, R. and M,-m. Poo (1996) Synaptic modulation by neurotrophic factors: Differential and synergistic effects of brain-derived neurotrophic factor and ciliary neurotrophic factor. J. Neurosci. 16:3256-3264.
69. Thoenen, H. (1995) Neurotrophins and neuronal plasticity. Science 270:953-598.
70. Thomsen, E. (1966) Ultrastructure of the spiral ganglion of the guinea pig. Acta Otolaryngol. Suppl. 224:442-448.
71. Valenzuela, D.M., P.C. Maisonpierre, D.J. Glass, E. Rojas, L. Nuñez, Y. Kong, D.R. Gies, T.N. Stitt, N.Y. Ip, and G.D. Yancopoulos (1993) Alternative forms of rat TrkC with different functional capabilities. Neuron 10:963-974.
72. Van De Water, T.R., P. Heywood, and R.J. Ruben (1973) Development of sensory structures in organ cultures of the twelfth and thirteenth gestation day mouse embryo inner ears. Ann. Otol. Rhinol. Laryngol. Suppl. 4:2-18.
73. Walsh, E.J. and R. Romand (1992) Functional development of the cochlea and the cochlear nerve. In R. Romand (ed): Development of Auditory and Vestibular Systems 2. New York: Elsevier, 161-219.
74. Wheeler, E.F., M. Bothwell, L.C. Schecterson, and C.S. von Bartheld (1994) Expression of BDNF and NT-3 mRNAin hair cells of the organ of Corti: Quantitative analysis in developing rats. Hear. Res. 73:46-56.
75. Wong, V., R. Arriaga, N.Y. Ip, and R.M. Lindsay (1993) The neurotrophins BDNF, NT-3 and NT-4/5, but not NGF, up-regulate the cholinergic phenotype of developing motor neurons. Eur. J. Neurosci. 5:466-474.
76. Wright, E.M., K.S. Vogel, and A.M. Davies (1992) Neurotrophic factors promote the maturation of developing sensory neurons before they become dependent on these factors for survival. Neuron 9:139-150.
77. Ylikoski, J., U. Pirvola, M. Moshnyakov, J. Palgi, U. Arumäe, and M. Saarma (1993) Expression patterns of neurotrophin and their receptor mRNAs in the rat inner ear. Hear. Res. 65:69-78.
78. Zheng, J.L., R.R. Stewart, and W.-Q. Gao (1995) Neurotrophin-4/5 enhances survival of cultured spiral ganglion neurons and protects them from cisplatin neurotoxicity. J. Neurosci. 15:5079-5087.