Transient ischemia/hypoxia enhances gentamicin ototoxicity via caspase-dependent cell death pathway

Laboratory Investigation

Volumn 91, Issue 7, 2011, Pages 1092-1106

  Lin, Chia Der ^a,b   Kao, Ming Ching ^c,d   Tsai, Ming Hsui ^a,b   Lai, Chih Ho ^b   Wei, I Hua ^b   Tsai, Mang Hung ^b   Tang, Chih Hsin ^b   Lin, Cheng Wen ^b   Hsu, Chuan Jen ^e   Lin, Ching Yuang ^a,b  

^a CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^e NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

aminoglycoside; guinea pig; hypoxia; in vitro; ischemia; ototoxicity

Indexed keywords

CALCIUM; CALPAIN; CASPASE; GENTAMICIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUDITORY THRESHOLD SHIFT; CALCIUM TRANSPORT; CELL DEATH; CELL HYPOXIA; CELL INTERACTION; CELL LOSS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; GUINEA PIG; HAIR CELL; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; OTOTOXICITY; PRIORITY JOURNAL; REPERFUSION INJURY; SINGLE DRUG DOSE; SPIRAL GANGLION; TRANSIENT ISCHEMIC ATTACK;

ANIMALS; ANOXIA; ANTI-BACTERIAL AGENTS; APOPTOSIS; BLOTTING, WESTERN; CASPASES; CELL LINE; COCHLEA; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; GENTAMICINS; GUINEA PIGS; HEARING LOSS; ISCHEMIA;

EID: 79959751302     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2011.69     Document Type: Article

References (60)

1. Gupta R, Kim JY, Espinal MA, et al. Public health. Responding to market failures in tuberculosis control. Science 2001;293:1049-1051. (Pubitemid 32758067)
2. Forge A, Schacht J. Aminoglycoside antibiotics. Audiol Neurootol 2000;5:3-22. (Pubitemid 30093591)
3. Contopoulos-Ioannidis DG, Giotis ND, Baliatsa DV, et al. Extendedinterval aminoglycoside administration for children: a meta-analysis. Pediatrics 2004;114:e111-e118.
4. Bernard PA. Freedom from ototoxicity in aminoglycoside treated neonates: a mistaken notion. Laryngoscope 1981;91:1985-1994. (Pubitemid 12205815)
5. Ensink RJ, Camp GV, Cremers CW. Mitochondrial inherited hearing loss. Clin Otolaryngol Allied Sci 1998;23:3-8. (Pubitemid 28344929)
6. Guan MX, Fischel-Ghodsian N, Attardi G. A biochemical basis for the inherited susceptibility to aminoglycoside ototoxicity. Hum Mol Genet 2000;9:1787-1793. (Pubitemid 30608612)
7. Fischel-Ghodsian N. Mitochondrial deafness mutations reviewed. Hum Mutat 1999;13:261-270. (Pubitemid 29307069)
8. Johnson RF, Cohen AP, Guo Y, et al. Genetic mutations and aminoglycoside-induced ototoxicity in neonates. Otolaryngol Head Neck Surg 2010;142:704-707.
9. Tran Ba Huy P, Manuel C, Meulemans A, et al. Ethacrynic acid facilitates gentamicin entry into endolymph of the rat. Hear Res 1983;11:191-202. (Pubitemid 13034056)
10. Bates DE, Beaumont SJ, Baylis BW. Ototoxicity induced by gentamicin and furosemide. Ann Pharmacother 2002;36:446-451. (Pubitemid 34205320)
11. Guthrie OW. Aminoglycoside induced ototoxicity. Toxicology 2008;249:91-96.
12. Li H, Steyger PS. Synergistic ototoxicity due to noise exposure and aminoglycoside antibiotics. Noise Health 2009;11:26-32.
13. Salamy A, Eldredge L, Tooley WH. Neonatal status and hearing loss in high-risk infants. J Pediatr 1989;114:847-852. (Pubitemid 19122987)
14. Aust G. Vestibulotoxicity and ototoxicity of gentamicin in newborns at risk. Int Tinnitus J 2001;7:27-29. (Pubitemid 34056608)
15. Chayasirisobhon S, Yu L, Griggs L, et al. Recording of brainstem evoked potentials and their association with gentamicin in neonates. Pediatr Neurol 1996;14:277-280. (Pubitemid 26198942)
16. Axelsson A, Nuttall AL, Miller JM. Observations of cochlear microcirculation using intravital microscopy. Acta Otolaryngol (Stockh) 1990;109:263-270. (Pubitemid 20083684)
17. Pirodda A, Saggese D, Giausa G, et al. Can hypotension episodes cause cochlear damage in young subjects? Med Hypotheses 1997;48: 195-196. (Pubitemid 27165592)
18. Chao TK. Sudden sensorineural hearing loss after rapid reduction of blood pressure in malignant hypertension. Ann Otol Rhinol Laryngol 2004;113:73-75.
19. Seidman MD, Ahmad N, Bai U. Molecular mechanisms of age-related hearing loss. Ageing Res Rev 2002;1:331-343. (Pubitemid 38340328)
20. Henderson D, Bielefeld EC, Harris KC, et al. The role of oxidative stress in noise-induced hearing loss. Ear Hear 2006;27:1-19. (Pubitemid 44378662)
21. Thorne PR, Nuttall AL. Laser Doppler measurements of cochlear blood flow during loud sound exposure in the guinea pig. Hear Res 1987;27:1-10. (Pubitemid 17061871)
22. Wu WJ, Sha SH, McLaren JD, et al. Aminoglycoside ototoxicity in adult CBA, C57BL and BALB mice and the Sprague-Dawley rat. Hear Res 2001;158:165-178. (Pubitemid 32739289)
23. Boettcher FA, Henderson D, Gratton MA, et al. Synergistic interactions of noise and other ototraumatic agents. Ear Hear 1987;8:192-212.
24. Lin CD, Wei IH, Tsai MH, et al. Changes in guinea pig cochlea after transient cochlear ischemia. NeuroReport 2010;21:968-975.
25. Perlman HB, Kimura R, Fernandez C. Experiments on temporary obstruction of the internal auditory artery. Laryngoscope 1959;69: 591-613.
26. Steyger PS, Peters SL, Rehling J, et al. Uptake of gentamicin by bullfrog saccular hair cells in vitro. J Assoc Res Otolaryngol 2003;4:565-578. (Pubitemid 38112638)
27. Wang Q, Steyger PS. Trafficking of systemic fluorescent gentamicin into the cochlea and hair cells. J Assoc Res Otolaryngol 2009;10: 205-219.
28. Tang CH, Chiu YC, Huang CF, et al. Arsenic induces cell apoptosis in cultured osteoblasts through endoplasmic reticulum stress. Toxicol Appl Pharmacol 2009;241:173-181.
29. Jin X, Jin X, Sheng X. Methylcobalamin as antagonist to transient ototoxic action of gentamicin. Acta Otolaryngol (Stockh) 2001;121: 351-354. (Pubitemid 32472989)
30. Leake PA, Hradek GT. Cochlear pathology of long term neomycin induced deafness in cats. Hear Res 1988;33:11-33.
31. Hayashida T, Nomura Y, Iwamori M, et al. Distribution of gentamicin by immunofluorescence in the guinea pig inner ear. Arch Otorhinolaryngol 1985;242:257-264. (Pubitemid 16235318)
32. Mizukoshi O, Daly JF. Oxygen consumption in normal and kanamycin damaged cochleae. Acta Otolaryngol 1967;64:45-54.
33. Thalmann R, Miyoshi T, Thalmann I. The influence of ischemia upon the energy reserves of inner ear tissues. Laryngoscope 1972;82: 2249-2272.
34. Sha SH, Taylor R, Forge A, et al. Differential vulnerability of basal and apical hair cells is based on intrinsic susceptibility to free radicals. Hear Res 2001;155:1-8. (Pubitemid 32401586)
35. Jiang H, Sha SH, Forge A, et al. Caspase-independent pathways of hair cell death induced by kanamycin in vivo. Cell Death Differ 2006;13:20-30.
36. McDowell B. Patterns of cochlear degeneration following gentamicin administration in both old and young guinea pigs. Br J Audiol 1982;16:123-129. (Pubitemid 12122767)
37. Suzuki M, Yagi M, Brown JN, et al. Effect of transgenic GDNF expression on gentamicin-induced cochlear and vestibular toxicity. Gene Ther 2000;7:1046-1054. (Pubitemid 30398354)
38. Tabuchi K, Tsuji S, Fujihira K, et al. Outer hair cells functionally and structurally deteriorate during reperfusion. Hear Res 2002;173:153-163.
39. Suzuki M, Ushio M, Yamasoba T. Time course of apoptotic cell death in guinea pig cochlea following intratympanic gentamicin application. Acta Otolaryngol (Stockh) 2008;128:724-731. (Pubitemid 351882534)
40. Bae WY, Kim LS, Hur DY, et al. Secondary apoptosis of spiral ganglion cells induced by aminoglycoside: Fas-Fas ligand signaling pathway. Laryngoscope 2008;118:1659-1668.
41. Steinbach S, Lutz J. Glutamate induces apoptosis in cultured spiral ganglion explants. Biochem Biophys Res Commun 2007;357:14-19. (Pubitemid 46574493)
42. Kalkandelen S, Selimoglu E, Erdogan F, et al. Comparative cochlear toxicities of streptomycin, gentamicin, amikacin and netilmicin in guinea-pigs. J Int Med Res 2002;30:406-412. (Pubitemid 34993565)
43. Hashino E, Shero M. Endocytosis of aminoglycoside antibiotics in sensory hair cells. Brain Res 1995;704:135-140.
44. Marcotti W, van Netten SM, Kros CJ. The aminoglycoside antibiotic dihydrostreptomycin rapidly enters mouse outer hair cells through the mechano-electrical transducer channels. J Physiol (Lond) 2005;567: 505-521. (Pubitemid 41301048)
45. Dai CF, Steyger PS. A systemic gentamicin pathway across the stria vascularis. Hear Res 2008;235:114-124. (Pubitemid 50016732)
46. Laurell G, Viberg A, Teixeira M, et al. Blood-perilymph barrier and ototoxicity: an in vivo study in the rat. Acta Otolaryngol (Stockh) 2000;120:796-803. (Pubitemid 32511248)
47. Spatz M. Past and recent BBB studies with particular emphasis on changes in ischemic brain edema. Acta Neurochir Suppl 2010; 106:21-27.
48. Jahnke K. The blood-perilymph barrier. Arch Otorhinolaryngol 1980;228:29-34. (Pubitemid 10063259)
49. Zhang X, Wang J. Effects of microcirculatory disorders of inner ear on blood-labyrinth barrier permeability in guinea pigs. Chin J Otorhinolaryngol 2000;35:339-341.
50. Kastenbauer S, Klein M, Koedel U, et al. Reactive nitrogen species contribute to blood-labyrinth barrier disruption in suppurative labyrinthitis complicating experimental pneumococcal meningitis in the rat. Brain Res 2001;904:208-217. (Pubitemid 32537644)
51. Lesniak W, Pecoraro VL, Schacht J. Ternary complexes of gentamicin with iron and lipid catalyze formation of reactive oxygen species. Chem Res Toxicol 2005;18:357-364. (Pubitemid 40256257)
52. Tabuchi K, Tsuji S, Asaka Y, et al. Ischemia-reperfusion injury of the cochlea: effects of an iron chelator and nitric oxide synthase inhibitors. Hear Res 2001;160:31-36. (Pubitemid 32936610)
53. Ylikoski J, Xing-Qun L, Virkkala J, et al. Blockade of c-Jun N-terminal kinase pathway attenuates gentamicin-induced cochlear and vestibular hair cell death. Hear Res 2002;166:33-43. (Pubitemid 34626457)
54. Rybak LP, Kelly T. Ototoxicity: bioprotective mechanisms. Curr Opin Otolaryngol HN Surg 2003;11:328-333. (Pubitemid 37176002)
55. Bodmer D, Brors D, Pak K, et al. Gentamicin-induced hair cell death is not dependent on the apoptosis receptor Fas. Laryngoscope 2003;113:452-455. (Pubitemid 36297023)
56. Guan MX. Molecular pathogenetic mechanism of maternally inherited deafness. Ann NY Acad Sci 2004;1011:259-271.
57. Walker PD, Barri Y, Shah SV. Oxidant mechanisms in gentamicin nephrotoxicity. Ren Fail 1999;21:433-442. (Pubitemid 29318213)
58. Lin CD, Oshima T, Oda K, et al. Ototoxic interaction of kanamycin and 3-nitropropionic acid. Acta Otolaryngol (Stockh) 2008;128:1280-1285.
59. Hirose K, Westrum LE, Stone JS, et al. Dynamic studies of ototoxicity in mature avian auditory epithelium. Ann NY Acad Sci 1999;884:389-409.
60. Ding D, Stracher A, Salvi RJ. Leupeptin protects cochlear and vestibular hair cells from gentamicin ototoxicity. Hear Res 2002;164:115-126. (Pubitemid 34285584)