Schwann cells revert to non-myelinating phenotypes in the deafened rat cochlea

European Journal of Neuroscience

Volumn 26, Issue 7, 2007, Pages 1813-1821

  Hurley, Patricia A ^a   Crook, Jeremy M ^a,c   Shepherd, Robert K ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b BIONIC EAR INSTITUTE   (Australia)

^c ES Cell International   (Singapore)

Author keywords

Auditory nerve; Cochlear implant; Deafness; Myelin; Peripheral nerve; Schwann cell

Indexed keywords

BIOLOGICAL MARKER; FUROSEMIDE; GENTAMICIN; GLIAL FIBRILLARY ACIDIC PROTEIN; MYELIN BASIC PROTEIN; MYELIN PROTEIN; NERVE CELL ADHESION MOLECULE; PERIPHERAL MYELIN PROTEIN 22; PROTEIN S 100;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COCHLEA; CONTROL GROUP; DEMYELINATION; HEARING IMPAIRMENT; IMMUNOHISTOCHEMISTRY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; SCHWANN CELL; SPIRAL GANGLION; TISSUE SECTION;

ANIMALS; ANIMALS, NEWBORN; COCHLEA; DEAFNESS; DISEASE MODELS, ANIMAL; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; FUROSEMIDE; GENE EXPRESSION REGULATION; GENTAMICINS; GLIAL FIBRILLARY ACIDIC PROTEIN; MYELIN BASIC PROTEINS; MYELIN P0 PROTEIN; NEUROFILAMENT PROTEINS; NEURONS; RATS; RATS, WISTAR; S100 PROTEINS; SCHWANN CELLS; SPIRAL GANGLION; TIME FACTORS;

EID: 34848897792     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05811.x     Document Type: Article

References (61)

1. Andrew, J. (2003) Rehabilitation of the deafened auditory nerve with Schwann cell transplantation. Honours Dissertation, Department of Otolaryngology, University of Melbourne, Melbourne.
2. Bunge, R.P. (1993) Expanding roles for the Schwann cell: ensheathment, myelination, trophism and regeneration. Curr. Opin. Neurobiol., 3, 805 809.
3. Coppens, A.G., Kiss, R., Heizmann, C.W., Schafer, B.W. Poncelet, L. (2001) Immunolocalization of the calcium binding S100A1, S100A5 and S100A6 proteins in the dog cochlea during postnatal development. Brain Res. Dev. Brain Res., 126, 191 199.
4. Dau, J. Wenthold, R.J. (1989) Immunocytochemical localization of neurofilament subunits in the spiral ganglion of normal and neomycin-treated guinea pigs. Hear. Res., 42, 253 263.
5. Demerens, C., Stankoff, B., Logak, M., Anglade, P., Allinquant, B., Couraud, F., Zalc, B. Lubetzki, C. (1996) Induction of myelination in the central nervous system by electrical activity. Proc. Natl Acad. Sci. USA, 93, 9887 9892.
6. Despres, G., Leger, G.P., Dahl, D. Romand, R. (1994) Distribution of cytoskeletal proteins (neurofilaments, peripherin and MAP-tau) in the cochlea of the human fetus. Acta Otolaryngol., 114, 377 381.
7. Dodson, H.C. (1997) Loss and survival of spiral ganglion neurons in the guinea pig after intracochlear perfusion with aminoglycosides. J. Neurocytol., 26, 541 556.
8. Dodson, H.C. Mohuiddin, A. (2000) Response of spiral ganglion neurones to cochlear hair cell destruction in the guinea pig. J. Neurocytol., 29, 525 537.
9. Ernfors, P., Duan, M.L., EIShamy, W.M. Canlon, B. (1996) Protection of auditory neurons from aminoglycoside toxicity by neurotrophin-3. Nat. Med., 2, 463 467.
10. Felix, H. Hoffmann, V. (1985) Light and electron microscopic investigation of cochlear nerve specimens from profoundly deaf patients. Acta Otolaryngol. Suppl., 423, 67 72.
11. Foster, J.D., Drescher, M.J., Hatfield, J.S. Drescher, D.G. (1994) Immunohistochemical localization of S-100 protein in auditory and vestibular end organs of the mouse and hamster. Hear. Res., 74, 67 76.
12. Fraher, J.P. (1992) The CNS-PNS transitional zone of the rat. Morphometric studies at cranial and spinal levels. Prog. Neurobiol., 38, 261 316.
13. Fraher, J.P. (2000) The transitional zone and CNS regeneration. J. Anat., 196, 137 158.
14. Fraher, J.P. Delanty, F.J. (1987) The development of the central-peripheral transitional zone of the rat cochlear nerve. A light microscopic study. J. Anat., 155, 109 118.
15. Geal-Dor, M., Freeman, S., Li, G. Sohmer, H. (1993) Development of hearing in neonatal rats: air and bone conducted ABR thresholds. Hear. Res., 69, 236 242.
16. Gillespie, L.N., Clark, G.M., Bartlett, P.F. Marzella, P.L. (2003) BDNF-induced survival of auditory neurons in vivo: cessation of treatment leads to an accelerated loss of survival effects. J. Neurosci. Res., 71, 785 790.
17. Gillespie, L.N., Clark, G.M. Marzella, P.L. (2004) Delayed neurotrophin treatment supports auditory neuron survival in deaf guinea pigs. Neuroreport, 15, 1121 1125.
18. Glueckert, R., Pfaller, K., Kinnefors, A., Rask-Andersen, H. Schrott-Fischer, A. (2005) The human spiral ganglion: new insights into ultrastructure, survival rate and implications for cochlear implants. Audiol. Neurootol., 10, 258 273.
19. Hafidi, A., Despres, G. Romand, R. (1990) Cochlear innervation in the developing rat: an immunocytochemical study of neurofilament and spectrin proteins. J. Comp. Neurol., 300, 153 161.
20. Hardie, N.A. Shepherd, R.K. (1999) Sensorineural hearing loss during development: morphological and physiological response of the cochlea and auditory brainstem. Hear. Res., 128, 147 165.
21. Heid, S., Hartmann, R. Klinke, R. (1998) A model for prelingual deafness, the congenitally deaf white cat - population statistics and degenerative changes. Hear. Res., 115, 101 112.
22. Heizmann, C.W., Fritz, G. Schafer, B.W. (2002) S100 proteins: structure, functions and pathology. Front. Biosci., 7, d1356 1368.
23. Hilding, D.A. Ginzberg, R.D. (1977) Pigmentation of the stria vascularis. The contribution of neural crest melanocytes. Acta Otolaryngol., 84, 24 37.
24. Hoeffding, V. Feldman, M.L. (1988) Degeneration in the cochlear nerve of the rat following cochlear lesions. Brain Res., 449, 104 115.
25. Hurley, P.A. (2005) Molecular changes to the auditory nerve following sensorineural hearing loss. PhD Dissertation. Department of Otolaryngology, University of Melbourne, Melbourne.
26. Hurley, P.A., Clarke, M., Crook, J.M., Wise, A. Shepherd, R.K. (2003) Cochlear immunochemistry - a new technique based on gelatin embedding. J. Neurosci. Meth., 129, 81 86.
27. Imamura, S.I. Adams, J.C. (2003) Changes in cytochemistry of sensory and nonsensory cells in gentamicin-treated cochleas. J. Assoc. Res. Otolaryngol., 4, 196 218.
28. Ishibashi, T., Dakin, K.A., Stevens, B., Lee, P.R., Kozlov, S.V., Stewart, C.L. Fields, R.D. (2006) Astrocytes promote myelination in response to electrical impulses. Neuron, 49, 823 832.
29. Jessen, K.R. Mirsky, R. (1999) Schwann cells and their precursors emerge as major regulators of nerve development. Trends Neurosci., 22, 402 410.
30. Jessen, K.R. Mirsky, R. (2002) Signals that determine Schwann cell identity. J. Anat., 200, 367 376.
31. Johnsson, L.G. (1974) Sequence of degeneration of Corti's organ and its first-order neurons. Ann. Otol. Rhinol. Laryngol., 83, 294 303.
32. Knipper, M., Bandtlow, C., Gestwa, L., Kopschall, I., Rohbock, K., Wiechers, B., Zenner, H.P. Zimmermann, U. (1998) Thyroid hormone affects Schwann cell and oligodendrocyte gene expression at the glial transition zone of the VIIIth nerve prior to cochlea function. Development, 125, 3709 3718.
33. Koles, Z.J. Rasminsky, M. (1972) A computer simulation of conduction in demyelinated nerve fibres. J. Physiol., 227, 351 364.
34. Leake, P.A. Hradek, G.T. (1988) Cochlear pathology of long term neomycin induced deafness in cats. Hear. Res., 33, 11 33.
35. Martini, R. (1994) Myelin-associated glycoprotein is not detectable in perikaryal myelin of spiral ganglion neurons of adult mice. Glia, 10, 311 314.
36. Martini, R., Zielasek, J., Toyka, K.V., Giese, K.P. Schachner, M. (1995) Protein zero (P0)-deficient mice show myelin degeneration in peripheral nerves characteristic of inherited human neuropathies. Nat. Genet., 11, 281 286.
37. McGuinness, S.L. Shepherd, R.K. (2005) Exogenous BDNF rescues rat spiral ganglion neurons in vivo. Otol. Neurotol., 26, 1064 1072.
38. Miller, J.M., Chi, D.H., O'Keeffe, L.J., Kruszka, P., Raphael, Y. Altschuler, R.A. (1997) Neurotrophins can enhance spiral ganglion cell survival after inner hair cell loss. Int. J. Dev. Neurosci., 15, 631 643.
39. Mirsky, R. Jessen, K.R. (1996) Schwann cell development, differentiation and myelination. Curr. Opin. Neurobiol., 6, 89 96.
40. Mirsky, R. Jessen, K.R. (1999) The neurobiology of Schwann cells. Brain Pathol., 9, 293 311.
41. O'Leary, S.J. Moore, D.R. (1998) Development of cochlear sensitivity to aminoglycoside antibiotics. Ann. Otol. Rhinol. Laryngol., 107, 220 226.
42. Quarles, R.H. (2002) Myelin sheaths: glycoproteins involved in their formation, maintenance and degeneration. Cell. Mol. Life Sci., 59, 1851 1871.
43. Romand, R., Sobkowicz, H., Emmerling, M., Whitlon, D. Dahl, D. (1990) Patterns of neurofilament stain in the spiral ganglion of the developing and adult mouse. Hear. Res., 49, 119 125.
44. Shepherd, R.K., Coco, A., Epp, S.B. Crook, J.M. (2005) Chronic depolarization enhances the trophic effects of brain-derived neurotrophic factor in rescuing auditory neurons following a sensorineural hearing loss. J. Comp. Neurol., 486, 145 158.
45. Shepherd, R.K. Hardie, N.A. (2001) Deafness induced changes in the auditory pathway: implications for cochlear implants. Audiol. Neurootol., 6, 305 318.
46. Shepherd, R.K. Javel, E. (1997) Electrical stimulation of the auditory nerve. I. Correlation of physiological responses with cochlear status. Hear. Res., 108, 112 144.
47. Shepherd, R.K., Roberts, L.A. Paolini, A.G. (2004) Long-term sensorineural hearing loss induces functional changes in the rat auditory nerve. Eur. J. Neurosci., 20, 3131 3140.
48. Smith, K.J. McDonald, W.I. (1999) The pathophysiology of multiple sclerosis: the mechanisms underlying the production of symptoms and the natural history of the disease. Philos. Trans. R. Soc. Lond. B Biol. Sci., 354, 1649 1673.
49. Spoendlin, H. (1984) Factors inducing retrograde degeneration of the cochlear nerve. Ann. Otol. Rhinol. Laryngol. Suppl., 112, 76 82.
50. Staecker, H., Kopke, R., Malgrange, B., Lefebvre, P. Van de Water, T.R. (1996) NT-3 and/or BDNF therapy prevents loss of auditory neurons following loss of hair cells. Neuroreport, 7, 889 894.
51. Stevens, B. Fields, R.D. (2000) Response of Schwann cells to action potentials in development. Science, 287, 2267 2271.
52. Tachibana, M. (1999) Sound needs sound melanocytes to be heard. Pigment Cell Res., 12, 344 354.
53. Tasaki, I. (1955) New measurements of the capacity and the resistance of the myelin sheath and the nodal membrane of the isolated frog nerve fiber. Am. J. Physiol., 181, 639 650.
54. Terayama, Y., Kaneko, Y., Kawamoto, K. Sakai, N. (1977) Ultrastructural changes of the nerve elements following disruption of the organ of Corti. I. Nerve elements in the organ of Corti. Acta Otolaryngol., 83, 291 302.
55. Terayama, Y., Kaneko, K., Tanaka, K. Kawamoto, K. (1979) Ultrastructural changes of the nerve elements following disruption of the organ of Corti. II. Nerve elements outside the organ of Corti. Acta Otolaryngol., 88, 27 36.
56. Toesca, A. (1996) Central and peripheral myelin in the rat cochlear and vestibular nerves. Neurosci. Lett., 221, 21 24.
57. Whitlon, D.S., Ketels, K.V., Coulson, M.T., Williams, T., Grover, M., Edpao, W. Richter, C.P. (2006) Survival and morphology of auditory neurons in dissociated cultures of newborn mouse spiral ganglion. Neuroscience, 138, 653 662.
58. Wise, A.K., Richardson, R., Hardman, J., Clark, G. O'Leary, S. (2005) Resprouting and survival of guinea pig cochlear neurons in response to the administration of the neurotrophins brain-derived neurotrophic factor and neurotrophin-3. J. Comp. Neurol., 487, 147 165.
59. World Health Organization (2006) Deafness and hearing impairment. World Health Organization, Fact Sheet no. 300.
60. Zhou, R., Abbas, P.J. Assouline, J.G. (1995a) Electrically evoked auditory brainstem response in peripherally myelin-deficient mice. Hear. Res., 88, 98 106.
61. Zhou, R., Assouline, J.G., Abbas, P.J., Messing, A. Gantz, B.J. (1995b) Anatomical and physiological measures of auditory system in mice with peripheral myelin deficiency. Hear. Res., 88, 87 97.