Interactive roles of fibroblast growth factor 2 and neurotrophin 3 in the sequence of migration, process outgrowth, and axonal differentiation of mouse cochlear ganglion cells

Journal of Neuroscience Research

Volumn 86, Issue 11, 2008, Pages 2376-2391

  Hossain, Waheeda A ^a   D'Sa, Chrystal ^a   Morest, D Kent ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Antagonism; BDNF; Immunostaining; Otocyst; Synaptic vesicle protein; Synergism; TrkC

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 2; GROWTH FACTOR; MEMBRANE PROTEIN; NEUROTROPHIN; NEUROTROPHIN 3; NEUROTROPHIN 3 RECEPTOR; SYNAPTIC VESICLE PROTEIN 2;

ANIMAL CELL; ARTICLE; AUDITORY SYSTEM; CELL COUNT; CELL MIGRATION; CELL NUCLEUS; CELL PROLIFERATION; CELL SURFACE; COCHLEAR NERVE; COCULTURE; CONTROLLED STUDY; CULTURE MEDIUM; CYTOPLASM; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; GENE OVEREXPRESSION; GROWTH CONE; HAIR CELL; HYPOTHESIS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVE GROWTH; NEUROBLAST; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; SYNAPSE VESICLE;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DIFFERENTIATION; CELL MOVEMENT; EMBRYO, MAMMALIAN; FIBROBLAST GROWTH FACTOR 2; IMMUNOHISTOCHEMISTRY; MICE; NEURONS; NEUROTROPHIN 3; RECEPTOR, TRKC; SPIRAL GANGLION; STEM CELLS;

EID: 49349118095     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21685     Document Type: Article

References (66)

1. Agerman K, Hjerling-Leffler J, Blanchard MP, Scarfone E, Canlon B, Nosrat C, Ernfors P. 2003. BDNF gene replacement reveals multiple mechanisms for establishing neurotrophin specificity during sensory nervous system development. Development 130:1479-1491.
2. Ard MD, Morest DK, Hauger SH. 1985. Trophic interactions between the cochleovestibular ganglion of the chick embryo and its synaptic targets in culture. Neuroscience 16:151-170.
3. Brumwell CL, Hossain WA, Morest DK, Wolf B. 2005. Biotinidase reveals the morphogenetic sequence in cochlea and cochlear nucleus of mice. Hear Res 209:104-121.
4. Cavanagh JF, Mione MC, Pappas IS, Parnavelas JG. 1997. Basic fibroblast growth factor prolongs the proliferation of rat cortical progenitor cells in vitro without altering their cell cycle parameters. Cereb Cortex 7:293-302.
5. Coffin JD, Florkiewicz RZ, Neumann J, Mort-Hopkins T, Dorn GW 2nd, Lightfoot P, German R, Howles PN, Kier A, O'Toole BA, Sasse J, Gonzalez AM, Baird A, Doetschman T. 1995. Abnormal bone growth and selective translational regulation in basic fibroblast growth factor (FGF-2) transgenic mice. Mol Biol Cell 6:1861-1873.
6. Dazert S, Kim D, Luo L, Aletsee C, Garfunkel S, Maciag T, Baird A, Ryan AF. 1998. Focal delivery of fibroblast growth factor-1 by transfected cells induces spiral ganglion neurite targeting in vitro. J Cell Physiol 177:123-129.
7. Després G, Jalenques I, Romand R. 1991. Basic FGF-like protein in the lower stato-acoustic system of the neonatal and adult rat. Neuroreport 2:639-642.
8. Dono R, Texido G, Dussel R, Ehmke H, Zeller R. 1998. Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice. EMBO J 17:4213-4225.
9. D'Sa C, Gross J, Francone VP, Morest DK. 2007. Plasticity of synaptic endings in the cochlear nucleus following noise-induced hearing loss is facilitated in the adult FGF2 overexpressor mouse. Eur J Neurosci 26: 666-680.
10. ElShamy WM, Linnarsson S, Lee KF, Jaenisch R, Ernfors P. 1996. Prenatal and postnatal requirements of NT-3 for sympathetic neuroblast survival and innervation of specific targets. Development 122:491-500.
11. Ernfors P, Lonnerberg P, Ayer-LeLievre C, Persson H. 1990. Developmental and regional expression of basic fibroblast growth factor mRNA in the rat central nervous system. J Neurosci Res 27:10-15.
12. Ernfors P, Merlio JP, Persson H. 1992. Cells expressing mRNA for neurotrophins and their receptors during embryonic rat development. Eur J Neurosci 4:1140-1158.
13. Ernfors P, Van De Water T, Loring J, Jaenisch R. 1995. Complementary roles of BDNF and NT-3 in vestibular and auditory development. Neuron 14:1153-1164.
14. Fariñas I, Jones KR, Tessarollo L, Vigers AJ, Huang E, Kirstein M, de Caprona DC, Coppola V, Backus C, Reichardt LF, Fritzsch B. 2001. Spatial shaping of cochlear innervation by temporally regulated neurotrophin expression. J Neurosci 21:6170-6180.
15. Fritzsch B, Silos-Santiago I, Smeyne R, Fagan A, Barbacid M. 1995. Reduction and loss of inner ear innervation in trkB and trkC receptor knockout mice: a whole mount Dil and scanning electron microscopic analysis. Aud Neurosci 1:401-417.
16. Fritzsch B, Farinas I, Reichardt LF. 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.
17. Fritzsch B, Silos-Santiago I, Bianchi LM, Farinas I. 1997b. The role of neurotrophic factors in regulating the development of inner ear innervation. Trends Neurosci 20:159-164.
18. Gibbs RB, Pfaff DW. 1994. In situ hybridization detection of trkA mRNA in brain: distribution, colocalization. with p75NGFR and upregulation by nerve growth factor. J Comp Neurol 341:324-339.
19. Gomez-Pinilla F, Lee JW, Cotman CW. 1994. Distribution of basic fibroblast growth factor in the developing rat brain. Neuroscience 61:911-923.
20. Gospodarowicz D. 1987. Isolation and characterization of acidic and basic fibroblast growth factor. Methods Enzymol 147:106-119.
21. Gospodarowicz D, Neufeld G, Schweigerer L. 1986. Fibroblast growth factor. Mol Cell Endocrinol 46:187-204.
22. Hafidi A. 1999. Distribution of BDNF, NT-3 and NT-4 in the developing auditory brainstem. Int J Dev Neurosci 17:285-294.
23. Hafidi A, Moore T, Sanes DH. 1996. Regional distribution of neurotrophin receptors in the developing auditory brainstem. J Comp Neurol 367:454-464.
24. Hartnick CJ, Staecker H, Malgrange B, Lefebvre PP, Liu W, Moonen G, Van de Water TR. 1996. Neurotrophic effects of BDNF and CNTF, alone and in combination, on postnatal day 5 rat acoustic ganglion neurons. J Neurobiol 30:246-254.
25. Hegarty JL, Kay AR, Green SH. 1997. Trophic support of cultured spiral ganglion neurons by depolarization exceeds and is additive with that by neurotrophins or cAMP and requires elevation of [Ca2+]i within a set range. J Neurosci 17:1959-1970.
26. Hossain WA, Morest DK. 2000. Fibroblast growth factors (FGF-1, FGF-2) promote migration and neurite growth of mouse cochlear ganglion cells in vitro: immunohistochemistry and antibody perturbation. J Neurosci Res 62:40-55.
27. Hossain WA, Zhou X, Rutledge A, Baier C, Morest DK. 1996. Basic fibroblast growth factor affects neuronal migration and differentiation in normotypic cell cultures from the cochleovestibular ganglion of the chick embryo. Exp Neurol 138:121-143.
28. Hossain WA, Rutledge A, Morest DK. 1997. Critical periods of basic fibroblast growth factor and brain-derived neurotrophic factor in the development of the chicken cochleovestibular ganglion in vitro. Exp Neurol 147:437-451.
29. Hossain WA, Pang J, Morest DK. 2001. Expression of fibroblast growth factor receptor FGFR 1 and 2 during early development of mouse cochlear nucleus and ganglion. Assoc Res Otolaryngol Abs 21329.
30. Hossain WA, Brumwell CL, Morest DK. 2002. Sequential interactions of fibroblast growth factor-2, brain-derived neurotrophic factor, neurotrophin-3, and their receptors define critical periods in the development of cochlear ganglion cells. Exp Neurol 175:138-151.
31. Hossain WA, D'Sa C, Morest DK. 2006. Site-specific interactions of neurotrophin-3 and fibroblast growth factor (FGF2) in the embryonic development of the mouse cochlear nucleus. J Neurobiol 66:897-915.
32. Jeffery ND, Fitzgerald M. 2001. Effects of red nucleus ablation and exogenous neurotrophin-3 on corticospinal axon terminal distribution in the adult rat. Neuroscience 104:513-521.
33. Kalcheim C, Carmeli C, Rosenthal A. 1992. Neurotrophin 3 is a mitogen for cultured neural crest cells. Proc Natl Acad Sci U S A 89:1661-1665.
34. Ladher RK, Wright TJ, Moon AM, Mansour SL, Schoenwolf GC. 2005. FGF8 initiates inner ear induction in chick and mouse. Genes Dev 19:603-613.
35. Lefebvre PP, Malgrange B, Staecker H, Moghadass M, Van de Water TR, Moonen G. 1994. Neurotrophins affect survival and neuritogenesis by adult injured auditory neurons in vitro. Neuroreport 5:865-868.
36. Lewin GR, Barde YA. 1996. Physiology of the neurotrophins. Annu Rev Neurosci 19:289-317.
37. Li CW, Van De Water TR, Ruben RJ. 1976. In vitro study of fate mapping of the mouse otocyst. Trans Sect Otolaryngol Am Acad Ophthalmol Otolaryngol 82:273-280.
38. Li CW, Van De Water TR, Ruben RJ. 1978. The fate mapping of the eleventh and twelfth day mouse otocyst: an in vitro study of the sites of origin of the embryonic inner ear sensory structures. J Morphol 157:249-267.
39. Li R, Bernd P. 1999. Neurotrophin-3 increases neurite outgrowth and apoptosis in explants of the chicken neural plate. Dev Neurosci 21:12-21.
40. Logan A, Ahmed Z, Baird A, Gonzalez AM, Berry M. 2006. Neurotrophic factor synergy is required for neuronal survival and disinhibited axon regeneration after CNS injury. Brain 129:490-502.
41. Low W, Dazert S, Baird A, Ryan AF. 1996. Basic fibroblast growth factor (FGF-2) protects rat cochlear hair cells in organotypical culture from aminoglycoside injury. J Cell Physiol 167:443-450.
42. Luo L, Koutnouyan H, Baird A, Ryan AF. 1993. Acidic and basic FGF mRNA expression in the adult and developing rat cochlea. Hear Res 69:182-193.
43. Luo L, Moore JK, Baird A, Ryan AF. 1995. Expression of acidic FGF mRNA in rat auditory brainstem during postnatal maturation. Brain Res Dev Brain Res 86:24-34.
44. Marzella PL, Gillespie LN, Clark GM, Bartlett PF, Kilpatrick TJ. 1999. The neurotrophins act synergistically with LIF and members of the TGF-beta superfamily to promote the survival of spiral ganglia neurons in vitro. Hear Res 138:73-80.
45. Matsuyama A, Iwata H, Okumura N, Yoshida S, Imaizumi K, Lee Y, Shiraishi S, Shiosaka S. 1992. Localization of basic fibroblast growth factor-like immunoreactivity in the rat brain. Brain Res 587:49-65.
46. Mitsumoto H, Ikeda K, Klinkosz B, Cedarbaum JM, Wong V, Lindsay RM. 1994. Arrest of motor neuron disease in wobbler mice cotreated with CNTF and BDNF. Science 265:1107-1110.
47. Mou K, Hunsberger CL, Cleary JM, Davis RL. 1997. Synergistic effects of BDNF and NT-3 on postnatal spiral ganglion neurons. J Comp Neurol 386:529-539.
48. Nishio T, Akiguchi I, Furukawa S. 1992. Detailed distribution of nerve growth factor in rat brain determined by a highly sensitive enzyme immunoassay. Exp Neurol 116:76-84.
49. Pickles JO, Harter C, Rebillard G. 1998. Fibroblast growth factor receptor expression in outer hair cells of rat cochlea. NeuroReport 9:4093-4095.
50. Pirvola U, Ylikoski J, Palgi J, Lehtonen E, Arumae U, Saarma M. 1992. Brain-derived neurotrophic factor and neurotrophin 3 mRNAs in the peripheral target fields of developing inner ear ganglia. Proc Natl Acad Sci U S A 89:9915-9919.
51. Pirvola U, Arumae U, Moshnyakov M, Palgi J, Saarma M, Ylikoski J. 1994. Coordinated expression and function of neurotrophins and their receptors in the rat inner ear during target innervation. Hear Res 75:131-144.
52. Pirvola U, Cao Y, Oellig C, Suoqiang Z, Pettersson RF, Ylikoski J. 1995. The site of action of neuronal acidic fibroblast growth factor is the organ of Corti of the rat cochlea. Proc Natl Acad Sci U S A 92:9269-9273.
53. Pirvola U, Ylikoski J, Trokovic R, Hebert JM, McConnell SK, Partanen J. 2002. FGFR1 is required for the development of the auditory sensory epithelium. Neuron 35:671-680.
54. Raivich G, Kreutzberg GW. 1987. The localization and distribution of high affinity beta-nerve growth factor binding sites in the central nervous system of the adult rat. A light microscopic autoradiographic study using [125I]beta-nerve growth factor. Neuroscience 20:23-36.
55. Represa J, Avila MA, Romero G, Mato JM, Giraldez F, Varela-Nieto I. 1993. Brain-derived neurotrophic factor and neurotrophin-3 induce cell proliferation in the cochleovestibular ganglion through a glycosyl-phosphatidylinositol signaling system. Dev Biol 159:257-265.
56. Riedel B, Friauf E, Grothe C, Unsicker K. 1995. Fibroblast growth factor-2-like immunoreactivity in auditory brainstem nuclei of the developing and adult rat: correlation with onset and loss of hearing. J Comp Neurol 354:353-360.
57. Ruben RJ. 1967. Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol:Suppl 220:221-244.
58. Schecterson LC, Bothwell M. 1994. Neurotrophin and neurotrophin receptor mRNA expression in developing inner ear. Hear Res 73:92-100.
59. Sieber-Blum M. 1998. Growth factor synergism and antagonism in early neural crest development. Biochem Cell Biol 76:1039-1050.
60. Sugawara M, Murtie JC, Stankovic KM, Liberman MC, Corfas G. 2007. Dynamic patterns of neurotrophin 3 expression in the postnatal mouse inner ear. J Comp Neurol 501:30-37.
61. Temple S, Qian X. 1995. bFGF, neurotrophins, and the control of cortical neurogenesis. Neuron 15:249-252.
62. Tierney TS, T PD, Xia G, Moore DR. 2001. Development of brain-derived neurotrophic factor and neurotrophin-3 immunoreactivity in the lower auditory brainstem of the postnatal gerbil. Eur J Neurosci 14:785-793.
63. Vescovi AL, Reynolds BA, Fraser DD, Weiss S. 1993. bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/ astroglial) EGF-generated CNS progenitor cells. Neuron 11:951-966.
64. Wheeler EF, Bothwell M, Schecterson LC, von Bartheld CS. 1994. Expression of BDNF and NT-3 mRNA in hair cells of the organ of Corti: quantitative analysis in developing rats. Hear Res 73:46-56.
65. Ylikoski J, Pirvola U, Moshnyakov M, Palgi J, Arumae U, Saarma M. 1993. Expression patterns of neurotrophin and their receptor mRNAs in the rat inner ear. Hear Res 65:69-78.
66. Zhou L, Shine HD. 2003. Neurotrophic factors expressed in both cortex and spinal cord induce axonal plasticity after spinal cord injury. J Neurosci Res 74:221-226.