Reinnervation of hair cells by auditory neurons after selective removal of spiral ganglion neurons

Journal of Neurobiology

Volumn 66, Issue 4, 2006, Pages 319-331

  Martinez Monedero, Rodrigo ^a,b   Corrales, C Eduardo ^a,b   Cuajungco, Math P ^a,b   Heller, Stefan ^a,b,c   Edge, Albert S B ^a,b,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Apoptosis; Beta bungarotoxin; Spiral ganglion; Transplantation

Indexed keywords

BETA BUNGAROTOXIN; CELL MARKER; SNAKE VENOM;

ACOUSTIC NERVE FIBER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL TYPE; COCHLEA; CONTROLLED STUDY; CORTI ORGAN; DEAFFERENTATION; EXPLANT; HAIR CELL; HEARING; HEARING LOSS; INNER EAR; MOUSE; NERVE CELL GROWTH; NERVE CELL LESION; NERVE DEGENERATION; NERVE GRAFT; NEWBORN; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; REINNERVATION; SPIRAL GANGLION; SYNAPSE VESICLE; SYNAPTOGENESIS;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BIOLOGICAL MARKERS; BUNGAROTOXINS; COCHLEAR NERVE; COCULTURE TECHNIQUES; DENERVATION; DISEASE MODELS, ANIMAL; GROWTH CONES; HAIR CELLS; HEARING LOSS, SENSORINEURAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE DEGENERATION; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NEUROTOXINS; SPIRAL GANGLION; SYNAPTIC VESICLES;

EID: 33344475790     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.20232     Document Type: Article

References (46)

1. Bao J, Lei D, Du Y, Ohlemiller KK, Beaudet AL, Role LW. 2005. Requirement of nicotinic acetylcholine receptor subunit beta2 in the maintenance of spiral ganglion neurons during aging. J Neurosci 25:3041-3045.
2. Berglund AM, Ryugo DK. 1987. Hair cell innervation by spiral ganglion neurons in the mouse. J Comp Neurol 255:560-570.
3. Bok J, Zha XM, Cho YS, Green SH. 2003. An extranuclear locus of cAMP-dependent protein kinase action is necessary and sufficient for promotion of spiral ganglion neuronal survival by cAMP. J Neurosci 23:777-787.
4. Carnicero E, Knipper M, Tan J, Alonso MT, Schimmang T. 2002. Herpes simplex virus type 1-mediated transfer of neurotrophin-3 stimulates survival of chicken auditory sensory neurons. Neurosci Lett 321:149-152.
5. Ding DL, Wang J, Salvi R, Henderson D, Hu BH, McFadden SL, Mueller M. 1999. Selective loss of inner hair cells and type-I ganglion neurons in carboplatin-treated chinchillas. Mechanisms of damage and protection. Ann NY Acad Sci 884:152-170.
6. 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.
7. Farinas I, Jones KR, Backus C, Wang XY, Reichardt LF. 1994. Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369:658-661.
8. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, et al. 2000. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
9. Fritzsch B, Farinas I, Reichardt LF. 1997. 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.
10. Goslin K, Banker G. 1989. Experimental observations on the development of polarity by hippocampal neurons in culture. J Cell Biol 108:1507-1516.
11. Hamada M, Kimura RS. 1999. Morphological changes induced by administration of a Na+, K+-ATPase inhibitor in normal and hydropic inner ears of the guinea pig. Acta Otolaryngol 119:778-786.
12. Herkert M, Shakhman O, Schweins E, Becker CM. 2001. Beta-bungarotoxin is a potent inducer of apoptosis in cultured rat neurons by receptor-mediated internalization. Eur J Neurosci 14:821-828.
13. Hirokawa N. 1977. Disappearance of afferent and efferent nerve terminals in the inner ear of the chick embryo after chronic treatment with beta-bungarotoxin. J Cell Biol 73:27-46.
14. 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.
15. Hu Z, Ulfendahl M, Olivius MP. 2005a. NGF stimulates extensive neurite outgrowth from implanted dorsal root ganglion neurons following transplantation into the adult rat inner ear. Neurobiol Dis 18:184-192.
16. Hu Z, Wei D, Johansson CB, Holmstrom N, Duan M, Frisen J, Ulfendahl M. 2005b. Survival and neural differentiation of adult neural stem cells transplanted into the mature inner ear. Exp Cell Res 302:40-47.
17. Huang EJ, Liu W, Fritzsch B, Bianchi LM, Reichardt LF, Xiang M. 2001. Brn3a is a transcriptional regulator of soma size, target field innervation and axon pathfinding of inner ear sensory neurons. Development 128:2421-2432.
18. Jiang H, Guo W, Liang X, Rao Y. 2005. Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 120:123-135.
19. Keithley EM, Croskrey KL. 1990. Spiral ganglion cell endings in the cochlear nucleus of young and old rats. Hear Res 49:169-177.
20. Keithley EM, Feldman ML. 1979. Spiral ganglion cell counts in an age-graded series of rat cochleas. J Comp Neurol 188:429-442.
21. Kim WY, Fritzsch B, Serls A, Bakel LA, Huang EJ, Reichardt LF, Barth DS, et al. 2001. NeuroD-null mice are deaf due to a severe loss of the inner ear sensory neurons during development. Development 128:417-426.
22. Kros CJ, Ruppersberg JP, Rusch A. 1998. Expression of a potassium current in inner hair cells during development of hearing in mice. Nature 394:281-284.
23. Lang H, Schulte BA, Schmiedt RA. 2005. Ouabain Induces Apoptotic Cell Death in Type I Spiral Ganglion Neurons, but not Type II Neurons. J Assoc Res Otolaryngol 6:63-74.
24. Lee JE, Nakagawa T, Kim TS, Iguchi F, Endo T, Dong Y, Yuki K, et al. 2003. A novel model for rapid induction of apoptosis in spiral ganglions of mice. Laryngoscope 113:994-999.
25. Liberman MC, Kiang NY. 1978. Acoustic trauma in cats. Cochlear pathology and auditory-nerve activity. Acta Otolaryngol Suppl 358:1-63.
26. Lumpkin EA, Collisson T, Parab P, Omer-Abdalla A, Haeberle H, Chen P, Doetzlhofer A, et al. 2003. Math1-driven GFP expression in the developing nervous system of transgenic mice. Gene Expr Patterns 3:389-395.
27. Ma Q, Anderson DJ, Fritzsch B. 2000. Neurogenin 1 null mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. J Assoc Res Otolaryngol 1:129-143.
28. McFadden SL, Ding D, Jiang H, Salvi RJ. 2004. Time course of efferent fiber and spiral ganglion cell degeneration following complete hair cell loss in the chinchilla. Brain Res 997:40-51.
29. Montecucco C, Rossetto O. 2000. How do presynaptic PLA2 neurotoxins block nerve terminals? Trends Biochem Sci 25:266-270.
30. Nadol JB, Jr. 1997. Patterns of neural degeneration in the human cochlea and auditory nerve: implications for cochlear implantation. Otolaryngol Head Neck Surg 117:220-228.
31. Noben-Trauth K, Zheng QY, Johnson KR. 2003. Association of cadherin 23 with polygenic inheritance and genetic modification of sensorineural hearing loss. Nat Genet 35:21-23.
32. Fuel JL, d'Aldin C, Ruel J, Ladrech S, Pujol R. 1997. Synaptic repair mechanisms responsible for functional recovery in various cochlear pathologies. Acta Otolaryngol 117:214-218.
33. Scarfone E, Dememes D, Sans A. 1991. Synapsin I and Synaptophysin expression during ontogenesis of the mouse peripheral vestibular system. J Neurosci 11:1173-1181.
34. Schimmang T, Minichiello L, Vazquez E, San Jose I, Giraldez F, Klein R, Represa J. 1995. Developing inner ear sensory neurons require TrkB and TrkC receptors for innervation of their peripheral targets. Development 121:3381-3391.
35. Schmiedt RA, Okamura HO, Lang H, Schulte BA. 2002. Ouabain application to the round window of the gerbil cochlea: a model of auditory neuropathy and apoptosis. J Assoc Res Otolaryngol 3:223-233.
36. Schwamborn JC, Puschel AW. 2004. The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat Neurosci 7:923-929.
37. Sekiya T, Shimamura N, Yagihashi A, Suzuki S. 2003. Effect of topically applied basic fibroblast growth factor on injured cochlear nerve. Neurosurgery 52:900-907.
38. Shakhman O, Herkert M, Rose C, Humeny A, Becker CM. 2003. Induction by beta-bungarotoxin of apoptosis in cultured hippocampal neurons is mediated by Ca(2+)-dependent formation of reactive oxygen species. J Neurochem 87:598-608.
39. Sobkowicz HM, Bereman B, Rose JE. 1975. Organotypic development of the organ of Corti in culture. J Neurocytol 4:543-572.
40. Stankovic K, Rio C, Xia A, Sugawara M, Adams JC, Liberman MC, Corfas G. 2004. Survival of adult spiral ganglion neurons requires erbB receptor signaling in the inner ear. J Neurosci 24:8651-8661.
41. Starr A, Sininger YS, Pratt H. 2000. The varieties of auditory neuropathy. J Basic Clin Physiol Pharmacol 11:215-230.
42. Suzuka Y, Schuknecht HF. 1988. Retrograde cochlear neuronal degeneration in human subjects. Acta Otolaryngol Suppl 450:1-20.
43. Tseng WP, Lin-Shiau SY. 2003. Activation of NMDA receptor partly involved in beta-bungarotoxin-induced neurotoxicity in cultured primary neurons. Neurochem Int 42:333-344.
44. White JA, Burgess BJ, Hall RD, Nadol JB. 2000. Pattern of degeneration of the spiral ganglion cell and its processes in the C57BL/6J mouse. Hear Res 141:12-18.
45. Xiang M, Can L, Li D, Chen ZY, Zhou L, O'Malley BW Jr., Klein W, et al. 1997. Essential role of POU-domain factor Brn-3c in auditory and vestibular hair cell development. Proc Natl Acad Sci USA 94:9445-9450.
46. Zheng JL, Gao WQ. 1996. Differential damage to auditory neurons and hair cells by ototoxins and neuroprotection by specific neurotrophins in rat cochlear organotypic cultures. Eur J Neurosci 8:1897-1905.