Gentamicin rapidly inhibits mitochondrial metabolism in high-frequency cochlear outer hair cells

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Jensen Smith, Heather C ^a   Hallworth, Richard ^a   Nichols, Michael G ^b  

^a CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CREIGHTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENTAMICIN; GLUCOSE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SUCCINATE DEHYDROGENASE; ANTIINFECTIVE AGENT; NICOTINAMIDE ADENINE DINUCLEOTIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CELL FATE; CELL FUNCTION; CELL METABOLISM; CELL STRUCTURE; CELL VIABILITY; COCHLEA; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG INHIBITION; DRUG SENSITIVITY; EAR INJURY; ENZYME ACTIVITY; ENZYME METABOLISM; GLUCOSE BLOOD LEVEL; HAIR CELL; HEARING LOSS; MITOCHONDRIAL RESPIRATION; MOUSE; NEWBORN; NOISE INJURY; NONHUMAN; OTOTOXICITY; PROTEIN FUNCTION; PROTEIN SYNTHESIS; TREATMENT RESPONSE; ANIMAL; METABOLISM; MITOCHONDRION; ORGAN CULTURE TECHNIQUE; PATHOLOGY;

ANIMALS; ANTI-BACTERIAL AGENTS; GENTAMICINS; HAIR CELLS, AUDITORY, OUTER; MICE; MITOCHONDRIA; NAD; ORGAN CULTURE TECHNIQUES;

EID: 84862006001     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038471     Document Type: Article

References (68)

1. Rizzi MD, Hirose K, (2007) Aminoglycoside ototoxicity. Curr Opin Otolaryngol Head Neck Surg 15: 352-357.
2. Rybak LP, Ramkumar V, (2007) Ototoxicity. Kidney Int 72: 931-935.
3. Forge A, Li L, (2000) Apoptotic death of hair cells in mammalian vestibular sensory epithelia. Hear Res 139: 97-115.
4. Cheng AG, Cunningham LL, Rubel EW, (2003) Hair cell death in the avian basilar papilla: characterization of the in vitro model and caspase activation. J Assoc Res Otolaryngol 4: 91-105.
5. Cunningham LL, Cheng AG, Rubel EW, (2002) Caspase activation in hair cells of the mouse utricle exposed to neomycin. J Neurosci 22: 8532-8540.
6. Matsui JI, Gale JE, Warchol ME, (2004) Critical signaling events during the aminoglycoside-induced death of sensory hair cells in vitro. J Neurobiol 61: 250-266.
7. Abi-Hachem RN, Zine A, Van De Water TR, (2010) The injured cochlea as a target for inflammatory processes, initiation of cell death pathways and application of related otoprotectives strategies. Recent Pat CNS Drug Discov 5: 147-163.
8. Ohlemiller KK, Wright JS, Dugan LL, (1999) Early elevation of cochlear reactive oxygen species following noise exposure. Audiol Neurootol 4: 229-236.
9. Nicotera TM, Hu BH, Henderson D, (2003) The caspase pathway in noise-induced apoptosis of the chinchilla cochlea. J Assoc Res Otolaryngol 4: 466-477.
10. Someya S, Prolla TA, (2010) Mitochondrial oxidative damage and apoptosis in age-related hearing loss. Mech Ageing Dev 131: 480-486.
11. Marcotti W, van Netten SM, Kros CJ, (2005) The aminoglycoside antibiotic dihydrostreptomycin rapidly enters mouse outer hair cells through the mechano-electrical transducer channels. J Physiol 567: 505-521.
12. Hashino E, Shero M, (1995) Endocytosis of aminoglycoside antibiotics in sensory hair cells. Brain Res 704: 135-140.
13. Alharazneh A, Luk L, Huth M, Monfared A, Steyger PS, et al. (2011) Functional hair cell mechanotransducer channels are required for aminoglycoside ototoxicity. PLoS ONE 6: e22347.
14. Hobbie SN, Akshay S, Kalapala SK, Bruell CM, Shcherbakov D, et al. (2008) Genetic analysis of interactions with eukaryotic rRNA identify the mitoribosome as target in aminoglycoside ototoxicity. Proc Natl Acad Sci U S A 105: 20888-20893.
15. Wirmer J, Westhof E, (2006) Molecular contacts between antibiotics and the 30 S ribosomal particle. Methods Enzymol 415: 180-202.
16. Dehne N, Rauen U, de Groot H, Lautermann J, (2002) Involvement of the mitochondrial permeability transition in gentamicin ototoxicity. Hear Res 169: 47-55.
17. Hobbie SN, Bruell CM, Akshay S, Kalapala SK, Shcherbakov D, et al. (2008) Mitochondrial deafness alleles confer misreading of the genetic code. Proc Natl Acad Sci U S A 105: 3244-3249.
18. Fischel-Ghodsian N, (1999) Mitochondrial deafness mutations reviewed. Hum Mutat 13: 261-270.
19. Prezant TR, Agapian JV, Bohlman MC, Bu X, Oztas S, et al. (1993) Mitochondrial ribosomal RNA mutation associated with both antibiotic-induced and non-syndromic deafness. Nat Genet 4: 289-294.
20. Shadel GS, (2004) Coupling the mitochondrial transcription machinery to human disease. Trends Genet 20: 513-519.
21. Bottger EC, (2010) Mutant A1555G mitochondrial 12 S rRNA and aminoglycoside susceptibility. Antimicrob Agents Chemother 54: 3073-3074; author reply 3074-3075.
22. Pandya A, (1993) Nonsyndromic Hearing Loss and Deafness, Mitochondrial. In: Pagon RA, Bird TD, Dolan CR, Stephens K, editors. GeneReviews Seattle (WA).
23. Qian Y, Guan MX, (2009) Interaction of aminoglycosides with human mitochondrial 12 S rRNA carrying the deafness-associated mutation. Antimicrob Agents Chemother 53: 4612-4618.
24. Bindu LH, Reddy PP, (2008) Genetics of aminoglycoside-induced and prelingual non-syndromic mitochondrial hearing impairment: a review. Int J Audiol 47: 702-707.
25. Nicotera P, Leist M, Ferrando-May E, (1998) Intracellular ATP, a switch in the decision between apoptosis and necrosis. Toxicol Lett 102-103: 139-142.
26. Eguchi Y, Shimizu S, Tsujimoto Y, (1997) Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res 57: 1835-1840.
27. Sokolova IM, Evans S, Hughes FM, (2004) Cadmium-induced apoptosis in oyster hemocytes involves disturbance of cellular energy balance but no mitochondrial permeability transition. J Exp Biol 207: 3369-3380.
28. Yang WP, Hu BH, Sun JH, Zhai SQ, Henderson D, (2010) Death mode-dependent reduction in succinate dehydrogenase activity in hair cells of aging rat cochleae. Chin Med J (Engl) 123: 1633-1638.
29. Ding DL, Wang J, Salvi R, Henderson D, Hu BH, et al. (1999) 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: 152-170.
30. Fredelius L, Viberg A, Canlon B, (2001) Succinic dehydrogenase histochemistry as an early marker for hair cell pathology. ORL J Otorhinolaryngol Relat Spec 63: 12-18.
31. Ding D, McFadden S, Salvi RJ, (2001) Cochlear hair cell densities and inner ear staining techniques. In: Willott JF, editors. Handbook of mouse auditory research: from behavior to molecular biology Boca Raton: CRC Press pp. 189-204.
32. Heikal AA, (2010) Intracellular coenzymes as natural biomarkers for metabolic activities and mitochondrial anomalies. Biomark Med 4: 241-263.
33. Mayevsky A, Rogatsky GG, (2007) Mitochondrial function in vivo evaluated by NADH fluorescence: from animal models to human studies. Am J Physiol Cell Physiol 292: C615-640.
34. Tiede L, Steyger PS, Nichols MG, Hallworth R, (2009) Metabolic imaging of the organ of corti-a window on cochlea bioenergetics. Brain Res 1277: 37-41.
35. Tiede LM, Rocha-Sanchez SM, Hallworth R, Nichols MG, Beisel K, (2007) Determination of hair cell metabolic state in isolated cochlear preparations by two-photon microscopy. J Biomed Opt 12: 021004.
36. Zhao LD, Guo WW, Lin C, Li LX, Sun JH, et al. (2011) Effects of DAPT and Atoh1 overexpression on hair cell production and hair bundle orientation in cultured Organ of Corti from neonatal rats. PLoS ONE 6: e23729.
37. Lancaster CR, (2002) Succinate:quinone oxidoreductases: an overview. Biochim Biophys Acta 1553: 1-6.
38. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P, (1997) Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 185: 1481-1486.
39. Shulman A, (1999) The cochleovestibular system/ototoxicity/clinical issues. Ann N Y Acad Sci 884: 433-436.
40. Rybak LP, Whitworth CA, (2005) Ototoxicity: therapeutic opportunities. Drug Discov Today 10: 1313-1321.
41. Rybak LP, (2005) Neurochemistry of the peripheral and central auditory system after ototoxic drug exposure: implications for tinnitus. Int Tinnitus J 11: 23-30.
42. Op de Beeck K, Schacht J, Van Camp G, (2011) Apoptosis in acquired and genetic hearing impairment: the programmed death of the hair cell. Hear Res 281: 18-27.
43. Jiang H, Sha SH, Forge A, Schacht J, (2006) Caspase-independent pathways of hair cell death induced by kanamycin in vivo. Cell Death Differ 13: 20-30.
44. Chance B, Sies H, Boveris A, (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59: 527-605.
45. Ralph SJ, Moreno-Sanchez R, Neuzil J, Rodriguez-Enriquez S, (2011) Inhibitors of succinate: quinone reductase/Complex II regulate production of mitochondrial reactive oxygen species and protect normal cells from ischemic damage but induce specific cancer cell death. Pharm Res 28: 2695-2730.
46. Forkink M, Smeitink JA, Brock R, Willems PH, Koopman WJ, (2010) Detection and manipulation of mitochondrial reactive oxygen species in mammalian cells. Biochim Biophys Acta 1797: 1034-1044.
47. Koopman WJ, Nijtmans LG, Dieteren CE, Roestenberg P, Valsecchi F, et al. (2010) Mammalian mitochondrial complex I: biogenesis, regulation, and reactive oxygen species generation. Antioxid Redox Signal 12: 1431-1470.
48. Ding D, Jiang H, Salvi RJ, (2010) Mechanisms of rapid sensory hair-cell death following co-administration of gentamicin and ethacrynic acid. Hear Res 259: 16-23.
49. Gropper SS, Smith JL, Groff JL, (2008) Advanced nutrition and human metabolism: Wadsworth Cengage Learning.
50. Huth ME, Ricci AJ, Cheng AG, (2011) Mechanisms of aminoglycoside ototoxicity and targets of hair cell protection. Int J Otolaryngol 2011 937861.
51. Yorgason JG, Luxford W, Kalinec F, (2011) In vitro and in vivo models of drug ototoxicity: studying the mechanisms of a clinical problem. Expert Opin Drug Metab Toxicol 7: 1521-1534.
52. Xie J, Talaska AE, Schacht J, (2011) New developments in aminoglycoside therapy and ototoxicity. Hear Res 281: 28-37.
53. Warchol ME, (2010) Cellular mechanisms of aminoglycoside ototoxicity. Curr Opin Otolaryngol Head Neck Surg 18: 454-458.
54. Ziegler M, (2000) New functions of a long-known molecule. Emerging roles of NAD in cellular signaling. Eur J Biochem 267: 1550-1564.
55. Tabuchi K, Nishimura B, Nakamagoe M, Hayashi K, Nakayama M, et al. (2011) Ototoxicity: Mechanisms of Cochlear Impairment and its Prevention. Curr Med Chem.
56. Poirrier AL, Pincemail J, Van Den Ackerveken P, Lefebvre PP, Malgrange B, (2010) Oxidative stress in the cochlea: an update. Curr Med Chem 17: 3591-3604.
57. Wu WJ, Sha SH, Schacht J, (2002) Recent advances in understanding aminoglycoside ototoxicity and its prevention. Audiol Neurootol 7: 171-174.
58. Kim HJ, Lee JH, Kim SJ, Oh GS, Moon HD, et al. (2010) Roles of NADPH oxidases in cisplatin-induced reactive oxygen species generation and ototoxicity. J Neurosci 30: 3933-3946.
59. Banfi B, Malgrange B, Knisz J, Steger K, Dubois-Dauphin M, et al. (2004) NOX3, a superoxide-generating NADPH oxidase of the inner ear. J Biol Chem 279: 46065-46072.
60. Jiang H, Sha SH, Schacht J, (2006) Rac/Rho pathway regulates actin depolymerization induced by aminoglycoside antibiotics. J Neurosci Res 83: 1544-1551.
61. Mukherjea D, Jajoo S, Whitworth C, Bunch JR, Turner JG, et al. (2008) Short interfering RNA against transient receptor potential vanilloid 1 attenuates cisplatin-induced hearing loss in the rat. J Neurosci 28: 13056-13065.
62. Chen GD, McWilliams ML, Fechter LD, (2000) Succinate dehydrogenase (SDH) activity in hair cells: a correlate for permanent threshold elevations. Hear Res 145: 91-100.
63. Horn KL, Langley LR, Gates GA, (1978) Early effects of ethacrynic acid on cochlear histochemistry. Arch Otolaryngol 104: 42-46.
64. Hu BH, Henderson D, Yang WP, (2008) The impact of mitochondrial energetic dysfunction on apoptosis in outer hair cells of the cochlea following exposure to intense noise. Hear Res 236: 11-21.
65. Karnes HE, Scaletty PN, Durham D, (2010) Histochemical and fluorescent analyses of mitochondrial integrity in chick auditory neurons following deafferentation. J Am Acad Audiol 21: 204-218.
66. Yang FS, Han JS, (1991) Gentamicin-induced alterations of succinic dehydrogenase activity in the organ of Corti as revealed by non-decalcified frozen sections of the guinea pig's cochlea. Eur Arch Otorhinolaryngol 248: 195-201.
67. 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.
68. Abramoff M, Magelhaes PJ, Ram SJ, (2004) Image Processing with Image J. Biophotonics International 11: 36-42.