Topographic and quantitative evaluation of gentamicin-induced damage to peripheral innervation of mouse cochleae

NeuroToxicology

Volumn 40, Issue , 2014, Pages 86-96

  Ruan, Qingwei ^a,b   Ao, Huafei ^a   He, Jingchun ^a   Chen, Zhengnong ^a   Yu, Zhuowei ^b   Zhang, Ruxin ^b   Wang, Jian ^a,c   Yin, Shankai ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Afferent dendrites; Efferent axons; Hair cells; Mouse; Spiral ganglion neurons; Tetramethyl rhodamine dextran

Indexed keywords

FUROSEMIDE; GENTAMICIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; COCHLEA INJURY; CONTROLLED STUDY; DENDRITE; DISEASE SEVERITY; DOSE RESPONSE; DRUG INDUCED DISEASE; EFFERENT NERVE; EXPERIMENTAL MOUSE; FEMALE; HABENULA; HAIR CELL; IMMUNOHISTOCHEMISTRY; INNERVATION; MALE; MOUSE; NERVE CELL LESION; NERVE FIBER; NONHUMAN; OTOTOXICITY; PRIORITY JOURNAL; QUANTITATIVE STUDY; SURVIVAL TIME;

4′,6-DIAMIDINO-2-PHENYLINDOLE; A; AFFERENT DENDRITES; APEX SEGMENT; B; BASAL SEGMENT; DAPI; EFFERENT AXONS; HABENULAR PERFORATE; HAIR CELL; HAIR CELLS; HC; HP; IHC; INNER HAIR CELL; LATERAL OLIVARY COMPLEX; LOC; M; MEDIAL OLIVARY COMPLEX; MIDDLE SEGMENT; MOC; MOUSE; OHC; OSL; OSSEOUS SPIRAL LAMINA; OUTER HAIR CELL; SGNS; SPIRAL GANGLION NEURONS; TETRAMETHYL RHODAMINE DEXTRAN; TETRAMETHYLRHODAMINE-CONJUGATED DEXTRAN; TMRD;

ANIMALS; ANTI-BACTERIAL AGENTS; COCHLEA; FEMALE; GENTAMICINS; HAIR CELLS, AUDITORY, OUTER; MALE; MICE; MICE, INBRED C57BL; NEURAL PATHWAYS; OLIVARY NUCLEUS; SPIRAL GANGLION;

EID: 84891121773     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2013.11.002     Document Type: Article

References (56)

1. Alharazneh A., Luk L., Huth M., Monfared A., Steyger P.S., Cheng A.G., et al. Functional hair cell mechanotransducer channels are required for aminoglycoside ototoxicity. PLoS ONE 2011, 6:e22347.
2. Bae W.Y., Kim L.S., Hur D.Y., Jeong S.W., Kim J.R. Secondary apoptosis of spiral ganglion cells induced by aminoglycoside: Fas-Fas ligand signaling pathway. Laryngoscope 2008, 118:1659-1668.
3. Bao J., Lei D., Du Y., Ohlemiller K.K., Beaudet A.L., Role L.W. Requirement of nicotinic acetylcholine receptor subunit b2 in the maintenance of spiral ganglion neurons during aging. J Neurosci 2005, 25:3041-3045.
4. Basile A.S., Huang J.M., Xie C., Webster D., Berlin C., Skolnick P. N-Methyl-d-aspartate antagonists limit aminoglycoside antibiotic-induced hearing loss. Nat Med 1996, 2:1338-1343.
5. Boyer S., Ruel J., Puel J.L., Chabbert C. A procedure to label inner ear afferent nerve endings for calcium imaging. Brain Res Brain Res Protoc 2004, 13:91-98.
6. Chen Z., Peppi M., Kujawa S.G., Sewell W.F. Regulated expression of surface AMPA receptors reduces excitotoxicity in auditory neurons. J Neurophysiol 2009, 102:1152-1159.
7. Ding D., Jiang H., Salvi R.J. Mechanisms of rapid sensory hair-cell death following co-administration of gentamicin and ethacrynic acid. Hear Res 2010, 259:16-23.
8. Darrow K.N., Maison S.F., Liberman M.C. Selective removal of lateral olivocochlear effects increase vulnerability to acute acoustic injury. J Neurophysiol 2007, 97:1775-1785.
9. Dodson H.C., Mohuiddin A. Response of spiral ganglion neurons to cochlear hair cell destruction in the guinea pig. J Neurocytol 2000, 29:525-537.
10. Duan M., Agerman K., Ernfors P., Canlon B. Complementary roles of neurotrophin 3 and a N-methyl-d-aspartate antagonist in the protection of noise and aminoglycoside-induced ototoxicity. PNAS 2000, 97:7597-7602.
11. Dupont J., Guilhaume A., Aran J.M. Neuronal degeneration of primary cochlear and vestibular innervations after local injection of sisomicin in the guinea pig. Hear Res 1993, 68:217-228.
12. Edson R.S., Terrell C.L. The aminoglycosides. Mayo Clin Proc 1999, 74:519-528.
13. Fritzsch B. Fast axonal diffusion of 3000 molecular weight dextran amines. J Neurosci Methods 1993, 50:95-103.
14. Glowatzki E., Fuchs P.A. Cholinergic synaptic inhibition of inner hair cells in the neonatal mammalian cochlea. Science 2000, 288:2366-2368.
15. Hafidi A. Peripherin-like immunoreactivity in type II spiral ganglion cell body and projections. Brain Res 1998, 805:181-190.
16. Harvey S.C., Skolnick P. Polyamine-like actions of aminoglycosides at recombinant N-methyl-d-aspartate receptors. J Pharmacol Exp Ther 1999, 291:285-291.
17. Heydt J.L., Cunningham L.L., Rubel E.W., Coltrera M.D. Round window gentamicin application: an inner ear hair cell damage protocol for the mouse. Hear Res 2004, 192(1-2):65-74.
18. Hinojosa R., Lerner S.A. Cochlear neural degeneration without hair cell loss in two patients with aminoglycoside ototoxicity. J Infect Dis 1987, 156:449-455.
19. Hong S.H., Park S.K., Cho Y.S., Lee H.S., Kim K.R., Kim M.G., et al. Gentamicin induced nitric oxide-related oxidative damages on vestibular afferents in the guinea pig. Hear Res 2006, 211:46-53.
20. Huang L., Thorne P., Houseley G., Montgometry J. Spatiotemporal definition of neurite outgrowth, refinement and retraction in the developing mouse cochlea. Development 2007, 134:2925-2933.
21. Keithley E.M., Ryan A.F., Woolf N.K. Spiral ganglion cell density in young and old gerbils. Hear Res 1989, 38:125-133.
22. Kiang N.Y.S., Liberman M.C., Levine R.A. Auditory-nerve activity in cats exposed to ototoxic drugs and high-intensity sounds. Ann Otol Rhinol Laryngol 1976, 85:752-768.
23. Kujawa S.G., Liberman M.C. Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss. J Neurosci 2009, 29:14077-14085.
24. Kusakari J., Ise I., Comegys T.H., Thalmann I., Thalmann R. Effect of ethacrynic acid, furosemide, and ouabain upon the endolymphatic potential and upon high energy phosphates of the stria vascularis. Laryngoscope 1978, 88:12-37.
25. Le Prell C.G., Yagi M., Kawamoto K., Beyer L.A., Atkin G., Raphael Y., et al. Chronic excitotoxicity in the guinea pig cochlea induces temporary functional deficits without disrupting otoacoustic emissions. J Acoust Soc Am 2004, 116:1044-1056.
26. Liberman M.C., Kiang N.Y. Acoustic trauma in cats. Cochlear pathology and auditory-nerve activity. Acta Otolaryngol [Suppl] 1978, 358:1-63.
27. McFadden S.L., Ding D., Jiang H., Salvi R.J. Time course of efferent fiber and spiral ganglion cell degeneration following complete hair cell loss in the chinchilla. Brain Res 2004, 997:40-51.
28. McFadden S.L., Ding D., Jiang H., Woo J.M., Salvi R.J. Chinchilla models of selective cochlear hair cell loss. Hear Res 2002, 174:230-238.
29. Mulheran M., Harpur E.S. The effect of gentamicin and furosemide given in combination on cochlear potentials in the guinea pig. Br J Audiol 1998, 32:47-56.
30. Oesterle E.C., Campbell S., Taylor R., Forge A., Hume A.C. SOX2 and Jagged 1 expression in normal and drug-damaged adult mouse inner ear. JARO 2008, 9:65-89.
31. Puel J.L., Pujol R., Tribillac F., Ladrech S., Eybalin M. Excitatory amino acid antagonists protect cochlear auditory neurons from excitotoxicity. J Comp Neurol 1994, 341:241-256.
32. Robertson C.M., Tyebkhan J.M., Peliowski A., Etches P.C., Cheung P.Y. Ototoxic drugs and sensorineural hearing loss following severe neonatal respiratory failure. Acta Paediatr 2006, 95:214-223.
33. Ruel J., Wang J., Rebillard G., Eybalin M., Lloyd R., Pujol R., et al. Physiology, pharmacology and plasticity at the inner hair cell synaptic complex. Hear Res 2007, 227:19-27.
34. Rubel E.W., Fritzsch B. Auditory system development: primary auditory neurons and their targets. Annu Rev Neurosci 2002, 5:51-101.
35. Ryals B.M., Westbrook E.W. Ganglion cell and hair cell loss in Coturnix quail associated with aging. Hear Res 1988, 36:1-8.
36. Schimmang T.J., Tan M., Muller U., Zimmermann K., Rohbock I., Kopschall A., et al. Lack of Bdnf and TrkB signalling in the postnatal cochlea leads to a spatial reshaping of innervation along the tonotopic axis and hearing loss. Development 2000, 130:4741-4750.
37. Segal J.A., Skolnick P. Polyamine-like actions of aminoglycosides and aminoglycoside derivatives at NMDA receptors. Eur J Pharmacol 1998, 347:311-317.
38. Segal J.A., Harris B.D., Kustova Y., Basile A., Skolnick P. Aminoglycoside neurotoxicity involves NMDA receptor activation. Brain Res 1999, 815:270-277.
39. Sweileh W.M. A prospective comparative study of gentamicin- and amikacin-induced nephrotoxicity in patients with normal baseline renal function. Fundam Clin Pharmacol 2009, 23(4):515-520.
40. Sobkowicz H.M., Emmerling M.R. Development of acetylcholinesterase-positive neuronal pathways in the cochlea of the mouse. J Neurocytol 1989, 18:209-224.
41. Sone M., Schachern P.A., Paparella M.M. Loss of spiral ganglion cells as primary manifestation of aminoglycoside ototoxicity. Hear Res 1998, 115:217-223.
42. Song B., Li Y., Han D. Delayed electrical stimulation and BDNF application following induced deafness in rats. Acta Oto-Laryngol 2009, 129:142-154.
43. Stepanyan R.S., Indzhykulian A.A., Vélez-ortega A.C., Boger E.T., Steyger P.S., Friedman T.B., et al. TRPA1-mediated accumulation of aminoglycosides in mouse cochlear outer hair cells. J Assoc Res Otolaryngol 2011, 12:729-740.
44. Tadros S.F., D'Souza M., Zettel M.L., Zhu X., Waxmonsky N.C., Frisina R.D. Glutamate-related gene expression changes with age in the mouse auditory midbrain. Brain Res 2007, 1127:1-9.
45. Takeno S., Wake M., Mount R.J., Harrison R.V. Degeneration of spiral ganglion cells in the chinchilla after inner hair cell loss induced by carboplatin. Audiol Neurootol 1998, 3:281-290.
46. Taylor R.R., Nevill G., Forge A. Rapid hair cell loss: a mouse model for auditory lesions. JARO 2008, 9:44-64.
47. Thiers F.A., Nado J.R.J.B., Liberman M.C. Reciprocal synapses between outer hair cells and their afferent terminals: evidence for a local neural network in mammalian cochlea. JARO 2008, 9:477-489.
48. Tran Ba Huy P., Manuel C., Meulemans A., Sterkers O., Wassef M., Amie C. Ethacrynic acid facilitates gentamicin entry into endolymph of the rat. Hear Res 1983, 11:191-202.
49. Usami S., Matsubara A., Fujita S., Shinkawa H., Hayashi M. NMDA (NMDAR1) and AMPA-type (GluR2/3) receptor subunits are expressed in the inner ear. Neuroreport 1995, 6:1161-1164.
50. Viberg A., Canlon B. The guide to plotting a cochleogram. Hear Res 2004, 197:1-10.
51. Wang J., Menchenton T., Yin S., Yu Z., Bance M., Morris D.P., et al. Over-expression of X-linked inhibitor of apoptosis protein slows presbycusis in C57BL/6J mice. Neurobiol Aging 2010, 31:1238-1249.
52. Weisz C., Glowatzki E., Fuchs P.A. The postsynaptic function of type II cochlear afferents. Nature 2009, 461:1027-1162.
53. Wu W.J., Sha S.H., Mclaren J.D., Kawamoto K., Raphael Y., Schacht J. Aminoglycoside ototoxicity in adult CBA, C57BL and BALB mice and the Sprague-Dawley rat. Hear Res 2001, 158:165-178.
54. Yukihara M., Ito K., Tanoue O., Goto K., Matsushita T., Matsumoto Y., et al. Effective drug delivery system for Duchenne muscular dystrophy using hybrid liposomes including gentamicin along with reduced toxicity. Bio Pharm Bull 2011, 34:712-716.
55. Zeron M.M., Fernandes H.B., Krebs C., Shehadeh J., Wellington C.L., Leavit B.R., et al. Potentiation of NMDA receptor-mediated excitotoxicity linked with intrinsic apoptotic pathway in YAC transgenic mouse model of Huntington's disease. Mol Cell Neurosci 2004, 25:469-479.
56. Zilberstein Y., Liberman M.C., Corfas G. Inner hair cells are not required for survival of spiral ganglion neurons in the adult cochlea. J Neurosci 2012, 32:405-410.