The mitochondrion: A perpetrator of acquired hearing loss

Hearing Research

Volumn 303, Issue , 2013, Pages 12-19

  Böttger, Erik C ^a   Schacht, Jochen ^b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; AMIKACIN; AMINOGLYCOSIDE ANTIBIOTIC AGENT; APRAMYCIN; ASCORBIC ACID; CARNITINE; GENTAMICIN; KANAMYCIN; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL DNA; NEOMYCIN; NETILMICIN; PLACEBO; REACTIVE OXYGEN METABOLITE; RETINOL; THIOCTIC ACID; TOBRAMYCIN;

AEROBIC METABOLISM; ANTIOXIDANT ACTIVITY; AUDIOGRAPHY; CELL DEATH; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY METABOLISM; HAIR CELL; HEARING ACUITY; HEARING IMPAIRMENT; HUMAN; MINIMUM INHIBITORY CONCENTRATION; MITOCHONDRIAL RESPIRATION; NOISE INJURY; NONHUMAN; OTOTOXICITY; OXIDATIVE STRESS; PRIORITY JOURNAL; RESPIRATORY CHAIN; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

MITOCHONDRIAL DNA; MTDNA; REACTIVE OXYGEN SPECIES; RIBOSOMAL RNA; ROS; RRNA; SOD; SUPEROXIDE DISMUTASE;

AMINOGLYCOSIDES; ANIMALS; CELL DEATH; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT; ENERGY METABOLISM; HAIR CELLS, AUDITORY; HEARING LOSS; HEARING LOSS, NOISE-INDUCED; HUMANS; MITOCHONDRIA; MUTATION; PRESBYCUSIS; REACTIVE OXYGEN SPECIES; RNA, RIBOSOMAL;

EID: 84880577813     PISSN: 03785955     EISSN: 18785891     Source Type: Journal    
DOI: 10.1016/j.heares.2013.01.006     Document Type: Review

References (89)

1. Adam-Vizi V. Production of reactive oxygen species in brain mitochondria: contribution by electron transport chain and non-electron transport chain sources. Antioxid. Redox. Signal. 2005, 7:1140-1149.
2. Bagger-Sjöbäck D., Wersäll J. Gentamicin-induced mitochondrial damage in inner ear sensory cells of the lizard Calotes versicolor. Acta Otolaryngol. 1978, 86:35-51.
3. Bai U., Seidman M.D., Hinojosa R., Quirk W.S. Mitochondrial DNA deletions associated with aging and possibly presbycusis: a human archival temporal bone study. Am. J. Otol. 1997, 18:449-453.
4. Berrettini S., Forli F., Passetti S., Rocchi A., Pollina L., Cecchetti D., Mancuso M., Siciliano G. Mitochondrial non-syndromic sensorineural hearing loss: a clinical, audiological and pathological study from Italy, and revision of the literature. Biosci. Rep. 2008, 28:49-59.
5. Bielefeld E.C., Coling D., Chen G.D., Henderson D. Multiple dosing strategies with acetyl L-carnitine (ALCAR) fail to alter age-related hearing loss in the Fischer 344/NHsd rat. J.Negat Results Biomed. 2008, 7:4.
6. Bonneux S., Fransen E., Van Eyken E., Van Laer L., Huyghe J., Van de Heyning P., Voets A., Gerards M., Stassen A.P., Hendrickx A.T., Smeets H.J., Van Camp G. Inherited mitochondrial variants are not a major cause of age-related hearing impairment in the European population. Mitochondrion 2011, 11:729-734.
7. Bordone L., Guarente L. Calorie restriction, SIRT1 and metabolism: understanding longevity. Nat. Rev. Mol. Cell. Biol. 2005, 6:298-305.
8. Carter A.P., Clemons W.M., Brodersen D.E., Morgan-Warren R.J., Wimberly B.T., Ramakrishnan V. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 2000, 407:340-348.
9. Chen F.Q., Zheng H.W., Hill K., Sha S.H. Traumatic noise activates Rho-family GTPases through transient cellular energy depletion. J.Neurosci. 2012, 32:12421-12430.
10. Cline S.D. Mitochondrial DNA damage and its consequences for mitochondrial gene expression. Biochim. Biophys. Acta. 2012, 1819:979-991.
11. Dai P., Yang W., Jiang S., Gu R., Yuan H., Han D., Guo W., Cao J. Correlation of cochlear blood supply with mitochondrial DNA common deletion in presbyacusis. Acta Otolaryngol. 2004, 124:130-136.
12. Darrouzet J., Guilhaume A. Ototoxicité de la kanamycine au jour le jour. Étude expérimentale en microscopie électronique. Rev. Laryng (Bordeaux) 1974, 95:601-621.
13. Dehne N., Rauen U., de Groot H., Lautermann J. Involvement of the mitochondrial permeability transition in gentamicin ototoxicity. Hear. Res. 2002, 169:47-55.
14. Dröse S., Brandt U. Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv. Exp. Med. Biol. 2012, 748:145-169.
15. Finkel T. Signal transduction by mitochondrial oxidants. J.Biol. Chem. 2012, 287:4434-4440.
16. Fischel-Ghodsian N. Mitochondrial deafness. Ear Hear. 2003, 24:303-313.
17. Francois B., Russell R.J., Murray J.B., Aboul-ela F., Masquida B., Vicens Q., Westhof E. Crystal structures of complexes between aminoglycosides and decoding A site oligonucleotides: role of the number of rings and positive charges in the specific binding leading to miscoding. Nucleic Acids Res. 2005, 33:5677-5690.
18. 2+ concentrations and causes dynamic contractions of the hearing organ. Proc. Natl. Acad. Sci. U S A 1998, 95:7127-7132.
19. Gershon D. Evaluating evidence for aging. Science 2005, 310:441-443.
20. Guan M.X. Molecular pathogenetic mechanism of maternally inherited deafness. Ann. N. Y Acad. Sci. 2004, 1011:259-271.
21. Heinrich U.R., Maurer J., Mann W. Ultrastructural evidence for protection of the outer hair cells of the inner ear during intense noise exposure by application of the organic calcium channel blocker diltiazem. ORL J. Otorhinolaryngol. Relat. Spec. 1999, 61:321-327.
22. Henderson D., Bielefeld E.C., Harris K.C., Hu B.H. The role of oxidative stress in noise-induced hearing loss. Ear Hear. 2006, 27:1-19.
23. Henry K.R. Effects of dietary restriction on presbyacusis in the mouse. Audiology 1986, 25:329-337.
24. Hobbie S.N., Kalapala S.K., Akshay S., Bruell C.M., Dabow S., Vasella A., Sander P., Böttger E.C. Engineering the rRNA decoding site of eukaryotic cytosolic ribosomes in bacteria. Nucleic Acids Res. 2007, 35:6086-6093.
25. Hobbie S.N., Bruell C.M., Akshay S., Kalapala S.K., Shcherbakov D., Böttger E.C. Mitochondrial deafness alleles confer misreading of the genetic code. Proc. Natl. Acad. Sci. U S A 2008, 105:3244-3249.
26. Hobbie S.N., Akshay S., Kalapala S.K., Bruell C.M., Shcherbakov D., Böttger E.C. Genetic analysis of interactions with eukaryotic rRNA identify the mitoribosome as target in aminoglycoside ototoxicity. Proc. Natl. Acad. Sci. U S A 2008, 105:20888-20893.
27. Hong S.H., Park S.K., Cho Y.S., Lee H.S., Kim K.R., Kim M.G., Chung W.H. Gentamicin induced nitric oxide-related oxidative damages on vestibular afferents in the guinea pig. Hear. Res. 2006, 211:46-53.
28. Hughes D.E., Chou J.T.-Y. Respirometrie. Biochemie des Hörorgans 1964, 446-457. Georg Thieme, Stuttgart. S. Rauch (Ed.).
29. Huth M.E., Ricci A.J., Cheng A.G. Mechanisms of aminoglycoside ototoxicity and targets of prevention. Int. J. Otolaryngol. 2011, 937861. Epub 2011 Oct 25.
30. Hwang J.H., Liu K.S., Wu C.C., Liu T.C. Association of cadherin23 single nucleotide polymorphism with age-related hearing impairment in Han Chinese. Otolaryngol. Head Neck Surg. 2012, 147:531-534.
31. Jensen-Smith H.C., Hallworth R., Nichols M.G. Gentamicin rapidly inhibits mitochondrial metabolism in high-frequency cochlear outer hair cells. PLoS One 2012, 7(6):e38471.
32. Jiang H., Sha S.-H., Schacht J. The NF-κB pathway protects cochlear hair cells from aminoglycoside-induced ototoxicity. J.Neurosci. Res. 2005, 79:644-651.
33. Jiang H., Sha S.-H., Schacht J. Rac/Rho pathway regulates actin depolymerization induced by aminoglycoside antibiotics. J.Neurosci. Res. 2006, 83:1544-1551.
34. Jiang H., Talaska A.E., Schacht J., Sha S.-H. Oxidative imbalance in the aging inner ear. Neurobiol. Aging 2007, 28:1605-1612.
35. Kalinec G.M., Fernandez-Zapico M.E., Urrutia R., Esteban-Cruciani N., Chen S., Kalinec F. Pivotal role of Harakiri in the induction and prevention of gentamicin-induced hearing loss. Proc. Natl. Acad. Sci. U S A 2005, 102:16019-21604.
36. Kidd Iii A.R., Bao J. Recent advances in the study of age-related hearing loss: a mini-review. Gerontology 2012, Jun 15. [Epub ahead of print].
37. Kokotas H., Petersen M.B., Willems P.J. Mitochondrial deafness. Clin. Genet. 2007, 71:379-391.
38. Kotecha B., Richardson G.P. Ototoxicity invitro: effects of neomycin, gentamicin, dihydrostreptomycin, amikacin, spectinomycin, neamine, spermine and poly-L-lysine. Hear. Res. 1994, 73:173-184.
39. Kujoth G.C., Hiona A., Pugh T.D., Someya S., Panzer K., Wohlgemuth S.E., Hofer T., Seo A.Y., Sullivan R., Jobling W.A., Morrow J.D., Van Remmen H., Sedivy J.M., Yamasoba T., Tanokura M., Weindruch R., Leeuwenburgh C., Prolla T.A. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 2005, 309:481-484.
40. Lee H.C., Wei Y.H. Mitochondria and aging. Adv. Exp. Med. Biol. 2012, 942:311-327.
41. Lenaz G., Baracca A., Fato R., Genova M.L., Solaini G. New insights into structure and function of mitochondria and their role in aging and disease. Antioxid. Redox. Signal. 2006, 8:417-437.
42. Liu Y.M., Li X.D., Guo X., Liu B., Lin A.H., Ding Y.L., Rao S.Q. SOD2 V16A SNP in the mitochondrial targeting sequence is associated with noise induced hearing loss in Chinese workers. Dis. Markers 2010, 28:137-147.
43. Lu J., Li Z., Zhu Y., Yang A., Li R., Zheng J., Cai Q., Peng G., Zheng W., Tang X., Chen B., Chen J., Liao Z., Yang L., Li Y., You J., Ding Y., Yu H., Wang J., Sun D., Zhao J., Xue L., Wang J., Guan M.X. Mitochondrial 12S rRNA variants in 1642 Han Chinese pediatric subjects with aminoglycoside-induced and nonsyndromic hearing loss. Mitochondrion 2010, 10(4):380-390.
44. Lundquist P.-G., Wersäll J. Kanamycin-induced changes in cochlear hair cells of the guinea pig. Z.Zellforsch Mikrosk Anat. 1966, 72:543-561.
45. Majumder P., Duchen M., Gale J. Investigating free radical production in the cochlea during ototoxicity. Abstr. Inner Ear Biol. 2012, 49:169.
46. Marcus D.C., Thalmann R., Marcus N.Y. Respiratory rate and ATP content of stria vascularis of guinea pig invitro. Laryngoscope 1978, 88:1825-1835.
47. Markaryan A., Nelson E.G., Hinojosa R. Detection of mitochondrial DNA deletions in the cochlea and its structural elements from archival human temporal bone tissue. Mutat. Res. 2008, 640:38-45.
48. Markaryan A., Nelson E.G., Hinojosa R. Quantification of the mitochondrial DNA common deletion in presbycusis. Laryngoscope 2009, 119:1184-1189.
49. Martin L.J. Biology of mitochondria in neurodegenerative diseases. Prog. Mol. Biol. Transl Sci. 2012, 107:355-415.
50. Matt T., Ng C.L., Lang K., Sha S.H., Akbergenov R., Shcherbakov D., Meyer M., Duscha S., Xie J., Dubbaka S.R., Perez-Fernandez D., Vasella A., Ramakrishnan V., Schacht J., Böttger E.C. Dissociation of antibacterial activity and aminoglycoside ototoxicity in the 4-monosubstituted 2-deoxystreptamine apramycin. Proc. Natl. Acad. Sci. U S A 2012, 109:10984-10989.
51. Miller R.A. Evaluating evidence for aging. Science 2005, 310:441-443.
52. Miller R.A., Burke D., Nadon N. Announcement: four-way cross mouse stocks: a new, genetically heterogeneous resource for aging research. J.Gerontol. A Biol. Sci. Med. Sci. 1999, 54A:B358.
53. Minami S.B., Yamashita D., Schacht J., Miller J.M. Calcineurin activation contributes to noise-induced hearing loss. J.Neurosci. Res. 2004, 78:383-392.
54. Nakai Y., Hilding D. Oxidative enzymes in the cochlea. Acta Oto-laryngol 1968, 65:459-467.
55. Ohinata Y., Miller J.M., Altschuler R.A., Schacht J. Intense noise induces formation of vasoactive lipid peroxidation products in the cochlea. Brain Res. 2000, 878:163-173.
56. Ohlemiller K.K. Contributions of mouse models to understanding of age- and noise-related hearing loss. Brain Res. 2006, 1091:89-102.
57. Ohlemiller K.K., Wright J.S., Dugan L.L. Early elevation of cochlear reactive oxygen species following noise exposure. Audiol. Neurootol. 1999, 4:229-236.
58. Oishi N., Schacht J. Emerging treatments for noise-induced hearing loss. Expert Opin. Emerg. Drugs 2011, 16:235-245.
59. Op de Beeck K., Schacht J., Van Camp G. Apoptosis in acquired and genetic hearing impairment: the programmed death of the hair cell. Hear. Res. 2011, 281:18-27.
60. Park J.C., Cook K.C., Verde E.A. Dietary restriction slows the abnormally rapid loss of spiral ganglion neurons in C57BL/6 mice. Hear. Res. 1990, 48:275-279.
61. Peng T.I., Jou M.J. Oxidative stress caused by mitochondrial calcium overload. Ann. N. Y Acad. Sci. 2010, 1201:183-188.
62. Poirrier A.L., Pincemail J., Van Den Ackerveken P., Lefebvre P.P., Malgrange B. Oxidative stress in the cochlea: an update. Curr. Med. Chem. 2010, 17:3591-3604.
63. Priuska E., Schacht J. Formation of free radicals by gentamicin and iron and evidence for an iron/gentamicin complex. Biochem. Pharmacol. 1995, 50:1749-1752.
64. Puschner B., Schacht J. Energy metabolism in cochlear outer hair cells invitro. Hear. Res. 1997, 114:102-106.
65. Ray P.D., Huang B.W., Tsuji Y. Cell. Signal. 2012, 24:981-990.
66. Reeve A.K., Krishnan K.J., Turnbull D. Mitochondrial DNA mutations in disease, aging, and neurodegeneration. Ann. N. Y Acad. Sci. 2008, 1147:21-29.
67. Rybak L.P., Ramkumar V. Ototoxicity. Kidney Int. 2007, 72:931-935.
68. Schacht J., Altschuler R.A., Burke D.T., Chen S., Dolan D., Galecki A.T., Kohrman D., Miller R.A. Alleles that modulate late life hearing in genetically heterogeneous mice. Neurobiol. Aging 2012, 33:1842.e15-1842.e29.
69. Schuknecht H.F., Gacek M.R. Cochlear pathology in presbycusis. Ann. Otol. Rhinol. Laryngol. 1993, 102:1-16.
70. Seidman M.D. Effects of dietary restriction and antioxidants on presbyacusis. Laryngoscope 2000, 110:727-738.
71. Seidman M.D., Ahmad N., Joshi D., Seidman J., Thawani S., Quirk W.S. Age-related hearing loss and its association with reactive oxygen species and mitochondrial DNA damage. Acta Otolaryngol. Suppl. 2004, 552:16-24.
72. Sha S.-H., Kanicki A., Halsey K., Wearne K.A., Schacht J. Antioxidant-enriched diet does not delay the progression of age-related hearing loss. Neurobiol. Aging 2012, 33:1010.e15-1010.e16.
73. Sha S.-H., Taylor R., Forge A., Schacht J. Differential vulnerability of basal and apical hair cells is based on intrinsic susceptibility to free radicals. Hear. Res. 2001, 155:1-8.
74. Shen H., Zhang B., Shin J.H., Lei D., Du Y., Gao X., Wang Q., Ohlemiller K.K., Piccirillo J., Bao J. Prophylactic and therapeutic functions of T-type calcium blockers against noise-induced hearing loss. Hear. Res. 2007, 226:52-60.
75. Sipos I., Tretter L., Adam-Vizi V. Quantitative relationship between inhibition of respiratory complexes and formation of reactive oxygen species in isolated nerve terminals. J.Neurochem. 2003, 84:112-118.
76. Spoendlin H. Primary structural changes in the organ of Corti after acoustic overstimulation. Acta Otolaryngol. 1971, 71:166-176.
77. Spicer S.S., Schulte B.A. Spiral ligament pathology in quiet-aged gerbils. Hear. Res. 2002, 172:172-185.
78. Sweet R.J., Price J.M., Henry K.R. Dietary restriction and presbyacusis: periods of restriction and auditory threshold losses in the CBA/J mouse. Audiology 1988, 27:305-312.
79. Thorne P.R., Nuttall A.L. Laser Doppler measurements of cochlear blood flow during loud sound exposure in the guinea pig. Hear. Res. 1987, 27:1-10.
80. Tretter L., Adam-Vizi V. Generation of reactive oxygen species in the reaction catalyzed by alpha-ketoglutarate dehydrogenase. J.Neurosci. 2004, 24:7771-7778.
81. Vicente-Torres M.A., Schacht J. ABAD link to mitochondrial cell death in the cochlea of mice with noise-induced hearing loss. J.Neurosci. Res. 2006, 83:1564-1572.
82. Warchol M.E. Cellular mechanisms of aminoglycoside ototoxicity. Curr. Opin. Otolaryngol. Head Neck Surg. 2010, 18:454-458.
83. Willott J.F., Erway L.C., Archer J.R., Harrison D. Genetics of age related hearing loss in mice: II. Strain differences and effects of caloric restriction on cochlear pathology and evoked response thresholds. Hear. Res. 1995, 88:143-155.
84. Wilson D.N. The A-Z of bacterial translation inhibitors. Crit. Rev. Biochem. Mol. Biol. 2009, 44:393-433.
85. Xie J., Talaska A.E., Schacht J. New developments in aminoglycoside therapy and ototoxicity. Hear. Res. 2011, 281:28-37.
86. Yamane H., Nakai Y., Takayama M., Iguchi H., Nakagawa T., Kojima A. Appearance of free radicals in the guinea pig inner ear after noise-induced acoustic trauma. Eur. Arch. Otorhinolaryngol. 1995, 252:504-508.
87. Yamashita D., Jiang H.-Y., Schacht J., Miller J.M. Delayed production of free radicals following noise exposure. Brain Res. 2004, 1019:201-209.
88. Yao Y.G., Salas A., Bravi C.M., Bandelt H.J. Areappraisal of complete mtDNA variation in East Asian families with hearing impairment. Hum. Genet. 2006, 119:505-515.
89. Zuo H., Cui B., She X., Wu M. Changes in Guinea pig cochlear hair cells after sound conditioning and noise exposure. J.Occup. Health 2005, 50:373-379.