Why do hair cells and spiral ganglion neurons in the cochlea die during aging?

Aging and Disease

Volumn 2, Issue 3, 2011, Pages 231-241

  Perez, Philip ^a   Bao, Jianxin ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Cochlea; Hair cells; Hearing loss; Spiral ganglion neurons

Indexed keywords

EID: 84869761856     PISSN: None     EISSN: 21525250     Source Type: Journal    
DOI: None     Document Type: Review

References (106)

1. U.S. National Center for Health Statistics, 1994 National Health Interview Survey.
2. Gates GA, Mills J (2005). Presbycusis. Lancet, 366:1111-20.
3. Dalton DS, Cruickshanks KJ, Klein BE, Klein R, Wiley TL, Nondahl DM (2003). The impact of hearing loss on quality of life in older adults. Gerontologist, 43:661-8.
4. McFadden SL, Ding D, Reaume AG, Flood DG, Salvi RJ (1999). Age-related cochlear hair cell loss is enhanced in mice lacking copper/zinc superoxide dismutase. Neurobiol Aging, 20:1-8.
5. Frisina RD, Walton JP (2001). Aging of the mouse central auditory system. In: Willott JP, editor. Handbook of Mouse Auditory Research: From Behavior to Molecular Biology. New York: CRC Press, 243-77.
6. Keithley EM, Canto C, Zheng QY, Fischel-Ghodsian N, Johnson KR (2004). Age-related hearing loss and the ahl locus in mice. Hear Res, 188:21-8.
7. Keithley EM, Canto C, Zheng QY, Wang X, Fischel-Ghodsian N, Johnson KR (2005). Cu/Zn superoxide dismutase and age-related hearing loss. Hear Res, 209:76-85.
8. Ison JR, Allen PD, O'Neill WE (2007). Age-related hearing loss in C57BL/6J mice has both frequency-specific and non-frequency-specific components that produce a hyperacusis-like exaggeration of the acoustic startle reflex. J Assoc Res Otolaryngol, 8:539-50.
9. Bao J, Ohlemiller KK (2010). Age-related loss of spiral ganglion neurons. Hear Res, 264:93-7.
10. Hughes LF, Turner JG, Parrish JL, Caspary DM (2010). Processing of broadband stimuli across A1 layers in young and aged rats. Hear Res, 264:79-85.
11. Schuknecht HF, Igarashi M (1964). Pathology of slowly progressive sensori-neural deafness. Trans Am Acad Ophthalmol Otolaryngol. 68:222-42.
12. Schuknecht HF, Gacek MR (1993). Cochlear pathology in presbycusis. Ann Otol Rhinol Laryngol, 102:1-16.
13. Sun JC, Bohne BA, Harding GW (1994). Is the older ear more susceptible to noise damage?. Laryngoscope, 104:1251-8.
14. Miller JM, Dolan DF, Raphael Y, Altschuler RA (1998). Interactive effects of aging with noise induced hearing loss. Scan Audiol Suppl, 48:53-61.
15. Ohlemiller KK (2004). Age-related hearing loss: the status of Schuknecht's typology. Curr Opin Otolaryngol Head Neck Surg, 12:439-43.
16. Bielefeld EC, Tanaka C, Chen G, Henderson D (2010). Age-related hearing loss: Is it a preventable condition? Hear Res, 264:98-107.
17. Johnson KR, Yu H, Ding D, Jiang H, Gagnon LH, Salvi RJ (2010). Separate and combined effects of Sod1 and Cdh23 mutations on age-related hearing loss and cochlear pathology in C57BL/6J mice. Hear Res, 268:85-92.
18. Gates GA, Schmid P, Kujawa SG, Nam B, D'Agostino R (2000). Longitudinal threshold changes in older men with audiometric notches. Hear Res, 141:220-8.
19. Rosenhall U (2003). The influence of ageing on noise-induced hearing loss. Noise Health, 5:47-53.
20. Cruickshanks KJ, Nondahl DM, Tweed TS, Wiley TL, Klein BE, Klein R, Chappell R, Dalton DS, Nash SD (2010). Education, occupation, noise exposure history and the 10-yr cumulative incidence of hearing impairment in older adults. Hear Res, 264:3-9.
21. Kujawa SG, Liberman MC (2006). Acceleration of age-related hearing loss by early noise exposure: evidence of a misspent youth. J Neurosci, 26:2115-23.
22. Kujawa SG, Liberman MC (2009). Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss. J Neurosci, 29:14077-85.
23. Adams JC, Schulte BA (1997). Histopathologic observations of the aging gerbil cochlea. Hear Res, 104:101-11.
24. Bohne BA, Gruner MM, Harding GW (1990). Morphological correlates of aging in the chinchilla cochlea. Hear Res, 48:79-91.
25. Sha SH, Kanicki A, Dootz G, Talaska AE, Halsey K, Dolan D, Altschuler R, Schacht J (2008). Age-related auditory pathology in the CBA/J mouse. Hear Res, 243:87-94.
26. Shimada A, Ebisu M, Morita T, Takeuchi T, Umemura T (1998). Age-related changes in the cochlea and cochlear nuclei of dogs. J Vet Med Sci, 60:41-8.
27. Schacht J, Hawkins JE (2005). Sketches of otohistory Part 9: presby[a]cusis. Audiol Neurootol, 10:243-7.
28. Ohlemiller KK, Frisina, RD (2008). Clinical characterization of age-related hearing loss and its neural and molecular bases. In: Popper AN, Fay RR, Schacht J, editors. Springer Handbook of Auditory Research. New York: Springer, 145-94.
29. Ernfors P, Van De Water T, Loring J, Jaenisch R (1995). Complementary roles of BDNF and NT-3 in vestibular and auditory development. Neuron, 14:1153-64.
30. Fritzsch B, Fariñas I, Reichardt LF (1997). Lack of neurotrophin 3 causes losses of both classes of spiral ganglion neurons in the cochlea in a region-specific fashion. J Neurosci,17:6213-25.
31. Takeno S, Wake M, Mount RJ, Harrison RV (1998). Degeneration of spiral ganglion cells in the chinchilla after inner hair cell loss induced by carboplatin. Audiol Neurootol, 3:281-90.
32. Keithley EM, Feldman ML (1979). Spiral ganglion cell counts in an age-graded series of rat cochleas. J Comp Neurol, 188:429-42.
33. Keithley EM, Ryan AF, Woolf NK (1989). Spiral ganglion cell density in young and old gerbils. Hear Res, 38:125-33.
34. Linthicum FH Jr, Fayad JN (2009). Spiral ganglion cell loss is unrelated to segmental cochlear sensory system degeneration in humans. Otol Neurotol, 30:418-22.
35. Ryals BM, Westbrook EW (1988). Ganglion cell and hair cell loss in Coturnix quail associated with aging. Hear Res, 36:1-8.
36. Suzuka Y, Schuknecht HF (1988). Retrograde cochlear neuronal degeneration in human subjects. Acta Otolaryngol Suppl, 450:1-20.
37. White JA, Burgess BJ, Hall RD, Nadol JB (2000). Pattern of degeneration of the spiral ganglion cell and its processes in the C57BL/6J mouse. Hear Res, 141:12-8.
38. Hequembourg S, Liberman MC (2001). Spiral ligament pathology: a major aspect of age-related cochlear degeneration in C57BL/6 mice. J Assoc Res Otolaryngol, 2:118-29.
39. Stamacki S, Francis HW, Lehar M, May BJ, Ryugo DK (2006). Synaptic alternations at inner hair cells precede spiral ganglion cell loss in aging C57BL/6J mice. Hear Res, 221:104-18.
40. Bao J, Lin H, Ouyang Y, Lei D, Osman A, Kim TW, Mei L, Dai P, Ohlemiller KK, Ambron RT (2004). Activity-dependent transcription regulation of PSD-95 by neuregulin-1 and Eos. Nat Neurosci, 7:1250-8.
41. Jin D, Ohlemiller KK, Lei D, Dong E, Role L, Ryugo DK, Bao J (2010). Age-related neuronal loss in the cochlea is not delayed by synaptic modulation. Neurobiol Aging, [Epub ahead of print.]
42. Kim S, Frisina DR, Frisina RD (2002). Effects of age on contralateral suppression of distortion product otoacoustic emissions in human listeners with normal hearing. Audiol Neurootol, 7:348-57.
43. Jacobson M, Kim S, Romney J, Zhu X, Frisina RD (2003). Contralateral suppression of distortion-product otoacoustic emissions declines with age: a comparison of findings in CBA mice with human listeners. Laryngoscope, 113:1707-13.
44. Varghese GI, Zhu X, Frisina RD (2005). Age-related declines in distortion product otoacoustic emissions utilizing pure tone contralateral stimulation in CBA/CaJ mice. Hear Res, 209:60-7.
45. Fu B, Le Prell C, Simmons D, Lei D, Schrader A, Chen AB, Bao J (2010). Age-related synaptic loss of the medial olivocochlear efferent innervation. Mol Neurodegener, 5:53.
46. Seidman MD (2000). Effects of dietary restriction and antioxidants on presbyacusis. Laryngoscope, 110:727-38.
47. Someya S, Xu J, Kondo K, Ding D, Salvi RJ, Yamasoba T, Rabinovitch PS, Weindruch R, Leeuwenburgh C, Tanokura M, Prolla TA (2009). Age-related hearing loss in C57BL/6J mice is mediated by Bak-dependent mitochondrial apoptosis. Proc Natl Acad Sci USA, 106:19432-7.
48. Bared A, Ouyang X, Angeli S, Du LL, Hoang K, Yan D, Liu XZ (2010). Antioxidant enzymes, presbycusis, and ethnic variability. Otolaryngol Head Neck Surg, 143:263-8.
49. Rhee SG (2006). Cell signaling H2O2, a necessary evil for cell signaling. Science, 312:1882-3.
50. Ohlemiller KK, McFadden SL, Ding DL, Lear PM, Ho YS (2000). Targeted mutation of the gene for cellular glutathione peroxidase (Gpx1) increases noise-induced hearing loss in mice. J Assoc Res Otolaryngol, 1:243-54.
51. Coling DE, Yu KC, Somand D, Satar B, Bai U, Huang TT, Seidman MD, Epstein CJ, Mhatre AN, Lalwani AK (2003). Effect of SOD1 overexpression on age- and noise-related hearing loss. Free Radic Biol Med, 34:873-80.
52. Le T, Keithley EM (2007). Effects of antioxidants on the aging inner ear. Hear Res, 226:194-202.
53. Staecker H, Zheng QY, Van De Water TR (2001). Oxidative stress in aging in the C57B16/J mouse cochlea. Acta Otolaryngol, 121:666-72.
54. Davis RR, Kuo MW, Stanton SG, Canlon B, Krieg E, Alagramam KN (2007). N-Acetyl L-cysteine does not protect against premature age-related hearing loss in C57BL/6J mice: a pilot study. Hear Res, 226:203-8.
55. Bielefeld EC, Coling D, Chen GD, Li M, Tanaka C, Hu BH, Henderson D (2008). Age-related hearing loss in the Fischer 344/NHsd rat substrain. Hear Res, 241:26-33.
56. Bielefeld EC, Coling D, Chen GD, Henderson D (2008). 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, 7:4.
57. Pickles JO (2004). Mutation in mitochondrial DNA as a cause of presbyacusis. Audiol Neurootol, 9:23-33.
58. Bai U, Seidman MD, Hinojosa R, Quirk WS (1997). Mitochondrial DNA deletions associated with aging and possibly presbycusis: a human archival temporal bone study. Am J Otol, 18:449-53.
59. Niu X, Trifunovic A, Larsson NG, Canlon B (2007). Somatic mtDNA mutations cause progressive hearing loss in the mouse. Exp Cell Res, 313:3924-34.
60. Yamasoba T, Someya S, Yamada C, Weindruch R, Prolla TA, Tanokura M (2007). Role of mitochondrial dysfunction and mitochondrial DNA mutations in age-related hearing loss. Hear Res, 226:185-93.
61. Feuers RJ (1998). The effects of dietary restriction on mitochondrial dysfunction in aging. Ann N Y Acad Sci, 854:192-201.
62. Someya S, Yamasoba T, Weindruch R, Prolla TA, Tanokura M (2007). Caloric restriction suppresses apoptotic cell death in the mammalian cochlea and leads to prevention of presbycusis. Neurobiol Aging, 28:1613-22.
63. Landfield PW (1996). Aging-related increase in hippocampal calcium channels. Life Sci, 59:399-404.
64. Pottorf WJ, Duckles SP, Buchholz JN (2002). Aging and calcium buffering in adrenergic neurons. Auton Neurosci, 96:2-7.
65. Toescu EC, Verkhratsky A, Landfield PW (2004). Ca2+ regulation and gene expression in normal brain aging. Trends Neurosci, 27:614-20.
66. Niedzielski AS, Safieddine S, Wenthold RJ (1997). Molecular analysis of excitatory amino acid receptor expression in the cochlea. Audiol Neurootol, 2:79-91.
67. Parks TN (2000). The AMPA receptors of auditory neurons. Hear Res, 147:77-91.
68. Puyal J, Sage C, Dememes D, Dechesne CJ (2002). Distribution of alpha-amino-3-hydroxy-5-methyl-4 isoazolepropionic acid and N-methyl-D-aspartate receptor subunits in the vestibular and spiral ganglia of the mouse during early development. Brain Res Dev Brain Res, 139:51-7.
69. Morley BJ, Li HS, Hiel H, Drescher DG, Elgoyhen AB (1998). Identification of the subunits of the nicotinic cholinergic receptors in the rat cochlea using RT-PCR and in situ hybridization. Brain Res Mol Brain Res, 53:78-87.
70. Bao J, Lei D, Du Y, Ohlemiller KK, Beaudet AL, Role LW (2005). Requirement of nicotinic acetylcholine receptor subunit beta2 in the maintenance of spiral ganglion neurons during aging. J Neurosci, 25:3041-5.
71. Lopez I, Ishiyama G, Acuna D, Ishiyama A, Baloh RW (2003). Immunolocalization of voltage-gated calcium channel alpha1 subunits in the chinchilla cochlea. Cell Tissue Res, 313:177-86.
72. Shen H, Zhang B, Shin JH, Lei D, Du Y, Gao X, Wang Q, Ohlemiller KK, Piccirillo J, Bao J (2007). Prophylactic and therapeutic functions of T-type calcium blockers against noise-induced hearing loss. Hear Res, 226:52-60.
73. Nie L, Zhu J, Gratton MA, Liao A, Mu KJ, Nonner W, Richardson GP, Yamoah EN (2008). Molecular identity and functional properties of a novel T-type Ca2+ channel cloned from the sensory epithelia of the mouse inner ear. J Neurophysiol, 100:2287-99.
74. Mills JH, Matthews LJ, Lee FS, Dubno JR, Schulte BA, Weber PC (1999). Gender-specific effects of drugs on hearing levels of older persons. Ann N Y Acad Sci, 884:381-8.
75. Wildburger N, Lin-Ye A, Baird M, Lei D, Bao J (2009). Neuroprotective effects of blockers for T-type calcium channels. Molecular Neurodegeneration, 4:44.
76. Lang H, Schulte BA, Zhou D, Smythe N, Spicer SS, Schmiedt RA (2006). Nuclear factor kappaB deficiency is associated with auditory nerve degeneration and increased noise-induced hearing loss. J Neurosci, 26:3541-50.
77. Zoli M, Picciotto MR, Ferrari R, Cocchi D, Changeux JP (1999). Increased neurodegeneration during ageing in mice lacking high-affinity nicotine receptors. EMBO J, 18:1235-44.
78. Shen H, Matsui JI, Lei D, Han L, Ohlemiller KK, Bao J (2010). No dramatic age-related loss of hair cells and spiral ganglion neurons in Bcl-2 over-expression mice or Bax null mice. Mol Neurodegener, 5:28.
79. Jin DX, Lin Z, Lei D, Bao J (2009). The role of glucocorticoids for spiral ganglion neuron survival. Brain Res, 1277:3-11.
80. Nelson RF, Glenn KA, Zhang Y, Wen H, Knutson T, Gouvion CM, Robinson BK, Zhou Z, Yang B, Smith RJ, Paulson HL (2007). Selective cochlear degeneration in mice lacking the F-box protein, Fbx2, a glycoprotein-specific ubiquitin ligase subunit. J Neurosci, 27:5163-71.
81. Kerr JF, Wyllie AH, Currie AR (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer, 26:239-57.
82. Bohne BA, Harding GW, Lee SC (2007). Death pathways in noise-damaged outer hair cells. Hear Res, 223:61-70.
83. Choi DW (1996). Ischemia-induced neuronal apoptosis. Curr Opin Neurobiol, 6:667-72.
84. Wood KA, Dipasquale B, Youle RJ (1993). In situ labeling of granule cells for apoptosis-associated DNA fragmentation reveals different mechanisms of cell loss in developing cerebellum. Neuron, 11:621-32.
85. Cohen GM, Sun XM, Snowden RT, Dinsdale D, Skilleter DN (1992). Key morphological features of apoptosis may occur in the absence of internucleosomal DNA fragmentation. Biochem J, 286:331-4.
86. Yuan J, Lipinski M, Degterev A (2003). Diversity in the mechanisms of neuronal cell death. Neuron, 40:401-13.
87. Mattson MP (2007). Calcium and neurodegeneration. Aging Cell, 6:337-50.
88. Pollack M, Leeuwenburgh C (2001). Apoptosis and aging: role of the mitochondria. J Gerontol A Biol Sci Med Sci, 56:B475-82.
89. Alam SA, Oshima T, Suzuki M, Kawase T, Takasaka T, Ikeda K (2001). The expression of apoptosis-related proteins in the aged cochlea of Mongolian gerbils. Laryngoscope, 111:528-34.
90. Nevado J, Sanz R, Casqueiro JC, Ayala A, García-Berrocal JR, Ramírez-Camacho R (2006). Ageing evokes an intrinsic pro-apoptotic signalling pathway in rat cochlea. Acta Otolaryngol, 126:1134-9.
91. Hengartner MO, Horvitz HR (1994). C elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell, 76:665-76.
92. Metzstein MM, Stanfield GM, Horvitz HR (1998). Genetics of programmed cell death in C elegans: past, present and future. Trends Genet, 14:410-6.
93. Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR (1993). The C elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell, 75:641-52.
94. Yuan J, Horvitz HR (2004). A first insight into the molecular mechanisms of apoptosis. Cell, 116 (2 Suppl):S53-6, 1 p following S59.
95. Cunningham LL, Matsui JI, Warchol ME, Rubel EW (2004). Overexpression of Bcl-2 prevents neomycin-induced hair cell death and caspase-9 activation in the adult mouse utricle in vitro. J Neurobiol, 60:89-100.
96. Mostafapour SP, Del Puerto NM, Rubel EW (2002). Bcl-2 overexpression eliminates deprivation-induced cell death of brainstem auditory neurons. J Neurosci, 22:4670-4.
97. Deckwerth TL, Elliott JL, Knudson CM, Johnson EM Jr, Snider WD, Korsmeyer SJ (1996). BAX is required for neuronal death after trophic factor deprivation and during development. Neuron, 17:401-11.
98. Sun W, Oppenheim RW (2003). Response of motoneurons to neonatal sciatic nerve axotomy in Bax-knockout mice. Mol Cell Neurosci, 24:875-86.
99. White FA, Keller-Peck CR, Knudson CM, Korsmeyer SJ, Snider WD (1998). Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J Neurosci, 18:1428-39.
100. Sastry PS, Rao KS (2000). Apoptosis and the nervous system. J Neurochem, 74:1-20.
101. Dazert S, Feldman ML, Keithley EM (1996). Cochlear spiral ganglion cell degeneration in wild-caught mice as a function of age. Hear Res, 100:101-6.
102. Jókay I, Soós G, Répássy G, Dezsõ B (1998). Apoptosis in the human inner ear detection by in situ end-labeling of fragmented DNA and correlation with other markers. Hear Res, 117:131-9.
103. Usami S, Takumi Y, Fujita S, Shinkawa H, Hosokawa M (1997). Cell death in the inner ear associated with aging is apoptosis?. Brain Res, 747:147-50.
104. Kressel M, Groscurth P (1994). Distinction of apoptotic and necrotic cell death by in situ labelling of fragmented DNA. Cell Tissue Res, 278:549-56.
105. Nishizaki K, Yoshino T, Orita Y, Nomiya S, Masuda Y (1999). TUNEL staining of inner ear structures may reflect autolysis, not apoptosis. Hear Res, 130:131-6.
106. Takahashi K, Kamiya K, Urase K, Suga M, Takizawa T, Mori H, Yoshikawa Y, Ichimura K, Kuida K, Momoi T (2001). Caspase-3-deficiency induces hyperplasia of supporting cells and degeneration of sensory cells resulting in the hearing loss. Brain Res, 894:359-67.