Mechanisms of rapid sensory hair-cell death following co-administration of gentamicin and ethacrynic acid

Hearing Research

Volumn 259, Issue 1-2, 2010, Pages 16-23

  Ding, Dalian ^a   Jiang, Haiyan ^a   Salvi, Richard J ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Apoptosis; Caspase 3; Caspase 8; Caspase 9; Cytochrome c; Ethacrynic acid; Gentamicin; Hair cells

Indexed keywords

CASPASE 3; CASPASE 8; CASPASE 9; CYTOCHROME C; ETACRYNIC ACID; GENTAMICIN; SUCCINATE DEHYDROGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL LOSS; CHINCHILLA; COCHLEAR NERVE; CONTROLLED STUDY; CUTICLE; CYTOSOL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME METABOLISM; ENZYME RELEASE; HAIR CELL; HISTOCHEMISTRY; LONG TERM EXPOSURE; MOLECULAR MECHANICS; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; STEREOCILIUM;

ANIMALS; ANTI-BACTERIAL AGENTS; APOPTOSIS; CASPASE 3; CASPASE 8; CASPASE 9; CELL DEATH; CHINCHILLA; CYTOCHROMES C; DRUG SYNERGISM; ETHACRYNIC ACID; GENTAMICINS; HAIR CELLS, AUDITORY; HAIR CELLS, AUDITORY, OUTER; MEMBRANE POTENTIAL, MITOCHONDRIAL; SIGNAL TRANSDUCTION; SUCCINATE DEHYDROGENASE;

EID: 73449135444     PISSN: 03785955     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.heares.2009.08.008     Document Type: Article

References (70)

1. Acehan D., Jiang X., Morgan D.G., Heuser J.E., Wang X., and Akey C.W. Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol. Cell 9 (2002) 423-432
2. Akiyoshi M. Effect of loop-diuretics on hair cells of the cochlea in guinea pigs. Histological and histochemical study. Scand. Audiol. Suppl. 14 Suppl. (1981) 185-199
3. Babson J.R., Gavitt N.E., and Dougherty J.M. Chlorpromazine protection against Ca(2+)-dependent and oxidative cell injury. Limitations due to depressed mitochondrial function. Biochem. Pharmacol. 48 (1994) 1509-1517
4. Benbow U., Orndorff K.A., Brinckerhoff C.E., and Givan A.L. Confocal assay for invasion: use of propidium iodide fluorescence and laser reflectance to quantify the rate of migration of cells through a matrix. Cytometry 40 (2000) 253-259
5. Bosher S.K. The nature of the ototoxic actions of ethacrynic acid upon the mammalian endolymph system. I. Functional aspects. Acta Otolaryngol. 89 (1980) 407-418
6. Brummett R.E., Traynor J., Brown R., and Himes D. Cochlear damage resulting from kanamycin and furosemide. Acta Otolaryngol. 80 (1975) 86-92
7. Conlon B.J., McSwain S.D., and Smith D.W. Topical gentamicin and ethacrynic acid: effects on cochlear function. Laryngoscope 108 (1998) 1087-1089
8. Dai C.F., and Steyger P.S. A systemic gentamicin pathway across the stria vascularis. Hear. Res. 235 (2008) 114-124
9. Dai C.F., Mangiardi D., Cotanche D.A., and Steyger P.S. Uptake of fluorescent gentamicin by vertebrate sensory cells in vivo. Hear. Res. 213 (2006) 64-78
10. Dallos P., and Harris D. Properties of auditory nerve responses in absence of outer hair cells. J. Neurophysiol. 41 (1978) 365-383
11. de Groot J.C., Meeuwsen F., Ruizendaal W.E., and Veldman J.E. Ultrastructural localization of gentamicin in the cochlea. Hear. Res. 50 (1990) 35-42
12. Dehne N., Rauen U., de Groot H., and Lautermann J. Involvement of the mitochondrial permeability transition in gentamicin ototoxicity. Hear. Res. 169 (2002) 47-55
13. Ding D., Jin X., and Zhao J. Accumulation sites of kanamycin in cochlear basal membrane cells. Chin. J. Otolaryngol. 30 (1995) 323-325
14. Ding D., Jin X., and Zhao J. Different binding sites of kanamycin and streptomicin in the organ of Corti. J. Clin. Otorhinolarygol. 9 (1995) 346-347
15. Ding D., Jin X., and Zhao J. The changes of cochlear bioelectric potential on guinea pigs deafened with ethacrynic acid. Chin. J. Clin. Otorhinolaryngol. 10 (1996) 330-332
16. Ding D., Jin X., and Zhao J. Accumulative sites of kanamycin in the organ of Corti by microautoradiography. Chin. J. Otorhinolaryngol. 32 (1997) 348-349
17. Ding D., McFadden S., and Salvi R.J. Cochlear hair cell densities and inner ear staining techniques. In: Willott J. (Ed). The Auditory Psychobiology of the Mouse (2001), CRC Press, Boca Raton 189-204
18. Ding D., Stracher A., and Salvi R.J. Leupeptin protects cochlear and vestibular hair cells from gentamicin ototoxicity. Hear. Res. 164 (2002) 115-126
19. Ding D., Jin X., Wang J., and Hangfu M. Influence of ethacrynic acid on microcirculation of stria vascularis of cochlea in guinea pigs. Acta Univer. Med. Second Shanghai 8 (1988) 34-37
20. Ding D., Defeng L., Guo Y., and Musan H. Probe into ototoxic mechanism of aminoglycoside antibiotic. Chin. J. Otorhinolaryngol. 26 (1991) 154-155
21. Ding D., McFadden S.L., Woo J.M., and Salvi R.J. Ethacrynic acid rapidly and selectively abolishes blood flow in vessels supplying the lateral wall of the cochlea. Hear. Res. 173 (2002) 1-9
22. Ding D., McFadden S.L., Browne R.W., and Salvi R.J. Late dosing with ethacrynic acid can reduce gentamicin concentration in perilymph and protect cochlear hair cells. Hear. Res. 185 (2003) 90-96
23. Ding D., Jiang H., Wang P., and Salvi R. Cell death after co-administration of cisplatin and ethacrynic acid. Hear. Res. 226 (2007) 129-139
24. Ding D.L., Wang J., Salvi R., Henderson D., Hu B.H., McFadden S.L., and Mueller M. Selective loss of inner hair cells and type-I ganglion neurons in carboplatin-treated chinchillas. Mechanisms of damage and protection. Ann. N. Y. Acad. Sci. 884 (1999) 152-170
25. Dulon D., Zajic G., Aran J.M., and Schacht J. Aminoglycoside antibiotics impair calcium entry but not viability and motility in isolated cochlear outer hair cells. J. Neurosci. Res. 24 (1989) 338-346
26. Forge A. Ultrastructure in the stria vascularis of the guinea pig following intraperitoneal injection of ethacrynic acid. Acta Otolaryngol. 92 (1981) 439-457
27. Forge A., and Schacht J. Aminoglycoside antibiotics. Audiol. Neurootol. 5 (2000) 3-22
28. Hashino E., Shero M., and Salvi R.J. Lysosomal targeting and accumulation of aminoglycoside antibiotics in sensory hair cells. Brain Res. 777 (1997) 75-85
29. Hashino E., Shero M., and Salvi R.J. Lysosomal augmentation during aminoglycoside uptake in cochlear hair cells. Brain Res. 887 (2000) 90-97
30. Hayashida T., Hiel H., Dulon D., Erre J.P., Guilhaume A., and Aran J.M. Dynamic changes following combined treatment with gentamicin and ethacrynic acid with and without acoustic stimulation. Cellular uptake and functional correlates. Acta Otolaryngol. 108 (1989) 404-413
31. Hiel H., Schamel A., Erre J.P., Hayashida T., Dulon D., and Aran J.M. Cellular and subcellular localization of tritiated gentamicin in the guinea pig cochlea following combined treatment with ethacrynic acid. Hear. Res. 57 (1992) 157-165
32. Hiel H., Erre J., Aurousseau C., Bouali R., Dulon D., and Aran J. Gentamicin uptake by cochlear hair cells precedes hearing impairment during chronic treatment. Audiology 32 (1993) 78-87
33. Hu B.H., Henderson D., and Nicotera T.M. Involvement of apoptosis in progression of cochlear lesion following exposure to intense noise. Hear. Res. 166 (2002) 62-71
34. Ikeda K., and Takasaka T. Confocal laser-scanning microscopical image of the distribution of intracellular organelles in cochlear outer hair cells. Jpn. J. Physiol. 43 (1993) S171-S173
35. Izumikawa M., Minoda R., Kawamoto K., Abrashkin K.A., Swiderski D.L., Dolan D.F., Brough D.E., and Raphael Y. Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals. Nat. Med. 11 (2005) 271-276
36. Jiang H., Sha S.H., Forge A., and Schacht J. Caspase-independent pathways of hair cell death induced by kanamycin in vivo. Cell Death Differ. 13 (2006) 20-30
37. Kalinec G.M., Fernandez-Zapico M.E., Urrutia R., Esteban-Cruciani N., Chen S., and Kalinec F. Pivotal role of Harakiri in the induction and prevention of gentamicin-induced hearing loss. Proc. Natl. Acad. Sci. USA 102 (2005) 16019-16024
38. Kasajima K., Kaneko Y., and Ouchi J. Changes of the stria vascularis induced by ethacrynic acid. Auris Nasus Larynx 5 (1978) 1-16
39. Khadir A., Verreault J., and Averill D.A. Inhibition of antioxidants and hyperthermia enhance bleomycin-induced cytotoxicity and lipid peroxidation in Chinese hamster ovary cells. Arch. Biochem. Biophys. 370 (1999) 163-175
40. Kuzel R.A., Smith J.M., and Trennery P.N. Screening procedure for assessment of ototoxicity in the common marmoset. J. Pharmacol. Methods 24 (1990) 9-18
41. Lenaz G., Bovina C., Formiggini G., and Castelli G.P. Mitochondria, oxidative stress, and antioxidant defences. Acta Biochim. Pol. 46 (1999) 1-21
42. Lim D.J. Functional structure of the organ of Corti: a review. Hear. Res. 22 (1986) 117-146
43. Matsushima J.I., Shepherd R.K., Seldon H.L., Xu S.A., and Clark G.M. Electrical stimulation of the auditory nerve in deaf kittens: effects on cochlear nucleus morphology. Hear. Res. 56 (1991) 133-142
44. McFadden S.L., Ding D., Jiang H., and Salvi R.J. Time course of efferent fiber and spiral ganglion cell degeneration following complete hair cell loss in the chinchilla. Brain Res. 997 (2004) 40-51
45. McFadden S.L., Ding D., Jiang H., Woo J.M., and Salvi R.J. Chinchilla models of selective cochlear hair cell loss. Hear. Res. 174 (2002) 230-238
46. Mehta R., and Champney W.S. 30S ribosomal subunit assembly is a target for inhibition by aminoglycosides in Escherichia coli. Antimicrob. Agents Chemother. 46 (2002) 1546-1549
47. Michel-Briand Y. Mechanism of action of antibiotics: some examples. C. R. Seances Soc. Biol. Fil. 172 (1978) 609-627
48. Nagane M., Pan G., Weddle J.J., Dixit V.M., Cavenee W.K., and Huang H.J. Increased death receptor 5 expression by chemotherapeutic agents in human gliomas causes synergistic cytotoxicity with tumor necrosis factor-related apoptosis-inducing ligand in vitro and in vivo. Cancer Res. 60 (2000) 847-853
49. Naito H., and Watanabe K. Alteration in capillary permeability of horseradish peroxidase in the stria vascularis and movement of leaked horseradish peroxidase after administration of furosemide. ORL J. Otorhinolaryngol. Relat. Spec. 59 (1997) 248-257
50. Nakagawa T., Yamane H., Takayama M., Sunami K., and Nakai Y. Apoptosis of guinea pig cochlear hair cells following chronic aminoglycoside treatment. Eur. Arch. Otorhinolaryngol. 255 (1998) 127-131
51. Nourski K.V., Miller C.A., Hu N., and Abbas P.J. Co-administration of kanamycin and ethacrynic acid as a deafening method for acute animal experiments. Hear. Res. 187 (2004) 131-133
52. Prazma J., Browder J.P., and Fischer N.D. Ethacrynic acid ototoxicity potentiation by kanamycin. Ann. Otol. Rhinol. Laryngol. 83 (1974) 111-118
53. Russell N.J., Fox K.E., and Brummett R.E. Ototoxic effects of the interaction between kanamycin and ethacrynic acid. Cochlear ultrastructure correlated with cochlear potentials and kanamycin levels. Acta Otolaryngol. 88 (1979) 369-381
54. Rybak L.P. Furosemide ototoxicity: clinical and experimental aspects. Laryngoscope 95 (1985) 1-14
55. Samali A., Zhivotovsky B., Jones D., Nagata S., and Orrenius S. Apoptosis: cell death defined by caspase activation. Cell Death Differ. 6 (1999) 495-496
56. Schmiedt R.A., Zwislocki J.J., and Hamernik R.P. Effects of hair cell lesions on responses of cochlear nerve fibers. I. Lesions, tuning curves, two-tone inhibition, and responses to trapezoidal-wave patterns. J. Neurophysiol. 43 (1980) 1367-1389
57. Sha S.H., Taylor R., Forge A., and Schacht J. Differential vulnerability of basal and apical hair cells is based on intrinsic susceptibility to free radicals. Hear. Res. 155 (2001) 1-8
58. Shepherd R.K., Xu S.A., and Clark G.M. Partial hearing loss in the macaque following the co-administration of kanamycin and ethacrynic acid. Hear. Res. 72 (1994) 89-98
59. Syka J., and Melichar I. Comparison of the effects of furosemide and ethacrynic acid upon the cochlear function in the guinea pig. Scand. Audiol. Suppl. 14 (1981) 63-69
60. Tabuchi K., Pak K., Chavez E., and Ryan A.F. Role of inhibitor of apoptosis protein in gentamicin-induced cochlear hair cell damage. Neuroscience 149 (2007) 213-222
61. Tran Ba Huy P., Bernard P., and Schacht J. Kinetics of gentamicin uptake and release in the rat. Comparison of inner ear tissues and fluids with other organs. J. Clin. Invest. 77 (1986) 1492-1500
62. Tran Ba Huy P., Manuel C., Meulemans A., Sterkers O., Wassef M., and Amiel C. Ethacrynic acid facilitates gentamicin entry into endolymph of the rat. Hear. Res. 11 (1983) 191-202
63. Trautwein P.G., Hashino E., and Salvi R.J. Regenerated hair cells become functional during continuous administration of kanamycin. Audiol. Neurootol. 3 (1998) 229-239
64. Tsuruya K., Tokumoto M., Ninomiya T., Hirakawa M., Masutani K., Taniguchi M., Fukuda K., Kanai H., Hirakata H., and Iida M. Antioxidant ameliorates cisplatin-induced renal tubular cell death through inhibition of death receptor-mediated pathways. Am. J. Physiol. Renal Physiol. 285 (2003) F208-F218
65. Voldrich L. The kinetics of streptomycin, kanamycin and neomycin in the inner ear. Acta Otolaryngol. 60 (1965) 243-248
66. Wang R., Li C., Song D., Zhao G., Zhao L., and Jing Y. Ethacrynic acid butyl-ester induces apoptosis in leukemia cells through a hydrogen peroxide mediated pathway independent of glutathione S-transferase P1-1 inhibition. Cancer Res. 67 (2007) 7856-7864
67. Xu S.A., Shepherd R.K., Chen Y., and Clark G.M. Profound hearing loss in the cat following the single co-administration of kanamycin and ethacrynic acid. Hear. Res. 70 (1993) 205-215
68. Ylikoski J., Xing-Qun L., Virkkala J., and Pirvola U. Blockade of c-Jun N-terminal kinase pathway attenuates gentamicin-induced cochlear and vestibular hair cell death. Hear. Res. 166 (2002) 33-43
69. Zhang M., Liu W., Ding D., and Salvi R. Pifithrin-alpha suppresses p53 and protects cochlear and vestibular hair cells from cisplatin-induced apoptosis. Neuroscience 120 (2003) 191-205
70. Zhu Q., Liu G., and Ding D. Accumulation of gentamicin in perilymph of guinea pigs. Acad. J. Second Mil Med. Univ. 114 (1993) 568-571