Association of a citrate synthase missense mutation with age-related hearing loss in A/J mice

Neurobiology of Aging

Volumn 33, Issue 8, 2012, Pages 1720-1729

  Johnson, Kenneth R ^a   Gagnon, Leona H ^a   Longo Guess, Chantal ^a   Kane, Kelly L ^a  

^a JACKSON LABORATORY   (United States)

Author keywords

A J; Age related hearing loss; Ahl4; Citrate synthase; Genetics; Inbred strain; Mitochondria; Mouse; Oxidative stress

Indexed keywords

ADENOSINE TRIPHOSPHATE; FREE RADICAL;

AGING; AHL4 GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMOSOME 10; CITRATE SYNTHASE GENE; COCHLEA; CODON; CONTROLLED STUDY; DNA SEQUENCE; EXON; GENE; GENE LOCUS; GENE MAPPING; GENETIC LINKAGE; HAIR CELL; HEARING LOSS; MISSENSE MUTATION; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; STRAIN DIFFERENCE;

AGING; ANIMALS; CITRATE (SI)-SYNTHASE; GENETIC ASSOCIATION STUDIES; GENETIC LINKAGE; HEARING LOSS; MICE; MUTATION, MISSENSE; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84861910434     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.05.009     Document Type: Article

References (46)

1. Balaban R.S., Nemoto S., Finkel T. Mitochondria, oxidants, and aging. Cell 2005, 120:483-495.
2. Carelli V., Giordano C., d'Amati G. Pathogenic expression of homoplasmic mtDNA mutations needs a complex nuclear-mitochondrial interaction. Trends Genet 2003, 19:257-262.
3. Cheng T.L., Liao C.C., Tsai W.H., Lin C.C., Yeh C.W., Teng C.F., Chang W.T. Identification and characterization of the mitochondrial targeting sequence and mechanism in human citrate synthase. J. Cell. Biochem 2009, 107:1002-1015.
4. DeStefano A.L., Gates G.A., Heard-Costa N., Myers R.H., Baldwin C.T. Genomewide linkage analysis to presbycusis in the Framingham Heart Study. Arch. Otolaryngol. Head Neck Surg 2003, 129:285-289.
5. Dirks A.J., Hofer T., Marzetti E., Pahor M., Leeuwenburgh C. Mitochondrial DNA mutations, energy metabolism and apoptosis in aging muscle. Ageing Res. Rev 2006, 5:179-195.
6. Frazer K.A., Eskin E., Kang H.M., Bogue M.A., Hinds D.A., Beilharz E.J., Gupta R.V., Montgomery J., Morenzoni M.M., Nilsen G.B., Pethiyagoda C.L., Stuve L.L., Johnson F.M., Daly M.J., Wade C.M., Cox D.R. A sequence-based variation map of 8.27 million SNPs in inbred mouse strains. Nature 2007, 448:1050-1053.
7. Friedman R.A., Van Laer L., Huentelman M.J., Sheth S.S., Van Eyken E., Corneveaux J.J., Tembe W.D., Halperin R.F., Thorburn A.Q., Thys S., Bonneux S., Fransen E., Huyghe J., Pyykkö I., Cremers C.W., Kremer H., Dhooge I., Stephens D., Orzan E., Pfister M., Bille M., Parving A., Sorri M., Van de Heyning P.H., Makmura L., Ohmen J.D., Linthicum F.H., Fayad J.N., Pearson J.V., Craig D.W., Stephan D.A., Van Camp G. GRM7 variants confer susceptibility to age-related hearing impairment. Hum. Mol. Genet 2009, 18:785-796.
8. Gagnon L.H., Longo-Guess C.M., Berryman M., Shin J.B., Saylor K.W., Yu H., Gillespie P.G., Johnson K.R. The chloride intracellular channel protein CLIC5 is expressed at high levels in hair cell stereocilia and is essential for normal inner ear function. J. Neurosci 2006, 26:10188-10198.
9. Haramizu S., Nagasawa A., Ota N., Hase T., Tokimitsu I., Murase T. Different contribution of muscle and liver lipid metabolism to endurance capacity and obesity susceptibility of mice. J. Appl. Physiol 2009, 106:871-879.
10. Henry K.R. Age-related auditory loss and genetics: an electrocochleographic comparison of six inbred strains of mice. J. Gerontol 1982, 37:275-282.
11. Ho M., Post C.M., Donahue L.R., Lidov H.G., Bronson R.T., Goolsby H., Watkins S.C., Cox G.A., Brown R.H. Disruption of muscle membrane and phenotype divergence in two novel mouse models of dysferlin deficiency. Hum. Mol. Genet 2004, 13:1999-2010.
12. Hunter K.P., Willott J.F. Aging and the auditory brainstem response in mice with severe or minimal presbycusis. Hear. Res 1987, 30:207-218.
13. Huyghe J.R., Van Laer L., Hendrickx J.J., Fransen E., Demeester K., Topsakal V., Kunst S., Manninen M., Jensen M., Bonaconsa A., Mazzoli M., Baur M., Hannula S., Mäki-Torkko E., Espeso A., Van Eyken E., Flaquer A., Becker C., Stephens D., Sorri M., Orzan E., Bille M., Parving A., Pyykkö I., Cremers C.W., Kremer H., Van de Heyning P.H., Wienker T.F., Nürnberg P., Pfister M., Van Camp G. Genome-wide SNP-based linkage scan identifies a locus on 8q24 for an age-related hearing impairment trait. Am. J. Hum. Genet 2008, 83:401-407.
14. Jiang H., Talaska A.E., Schacht J., Sha S.H. Oxidative imbalance in the aging inner ear. Neurobiol. Aging 2007, 28:1605-1612.
15. Johnson K.R., Zheng Q.Y., Bykhovskaya Y., Spirina O., Fischel-Ghodsian N. A nuclear-mitochondrial DNA interaction affecting hearing impairment in mice. Nat. Genet 2001, 27:191-194.
16. Johnson K.R., Zheng Q.Y., Erway L.C. A major gene affecting age-related hearing loss is common to at least ten inbred strains of mice. Genomics 2000, 70:171-180.
17. Johnson K.R., Zheng Q.Y., Noben-Trauth K. Strain background effects and genetic modifiers of hearing in mice. Brain Res 2006, 1091:79-88.
18. Keithley E.M., Canto C., Zheng Q.Y., Wang X., Fischel-Ghodsian N., Johnson K.R. Cu/Zn superoxide dismutase and age-related hearing loss. Hear. Res 2005, 209:76-85.
19. Kokotas H., Petersen M.B., Willems P.J. Mitochondrial deafness. Clin. Genet 2007, 71:379-391.
20. 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.
21. Lee Y.J., Hoe K.L., Maeng P.J. Yeast cells lacking the CIT1-encoded mitochondrial citrate synthase are hypersusceptible to heat- or aging-induced apoptosis. Mol. Biol. Cell 2007, 18:3556-3567.
22. Lightfoot J.T., Turner M.J., Debate K.A., Kleeberger S.R. Interstrain variation in murine aerobic capacity. Med. Sci. Sports Exerc 2001, 33:2053-2057.
23. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
24. Manly K.F., Cudmore R.H., Meer J.M. Map Manager QTX, cross-platform software for genetic mapping. Mamm. Genome 2001, 12:930-932.
25. McFadden S.L., Ding D., Burkard R.F., Jiang H., Reaume A.G., Flood D.G., Salvi R.J. Cu/Zn SOD deficiency potentiates hearing loss and cochlear pathology in aged 129,CD-1 mice. J. Comp. Neurol 1999, 413:101-112.
26. Moreno-Loshuertos R., Acín-Pérez R., Fernández-Silva P., Movilla N., Pérez-Martos A., Rodriguez de Cordoba S., Gallardo M.E., Enríquez J.A. Differences in reactive oxygen species production explain the phenotypes associated with common mouse mitochondrial DNA variants. Nat. Genet 2006, 38:1261-1268.
27. Mulrow C.D., Aguilar C., Endicott J.E., Velez R., Tuley M.R., Charlip W.S., Hill J.A. Association between hearing impairment and the quality of life of elderly individuals. J. Am. Geriatr. Soc 1990, 38:45-50.
28. Nadeau J.H., Singer J.B., Matin A., Lander E.S. Analysing complex genetic traits with chromosome substitution strains. Nat. Genet 2000, 24:221-225.
29. Nesbitt M.N., Skamene E. Recombinant inbred mouse strains derived from A/J and C57BL/6J: a tool for the study of genetic mechanisms in host resistance to infection and malignancy. J. Leukoc. Biol 1984, 36:357-364.
30. Niu X., Trifunovic A., Larsson N.G., Canlon B. Somatic mtDNA mutations cause progressive hearing loss in the mouse. Exp. Cell Res 2007, 313:3924-3934.
31. Noben-Trauth K., Johnson K.R. Inheritance patterns of progressive hearing loss in laboratory strains of mice. Brain Res 2009, 1277:42-51.
32. Noben-Trauth K., Zheng Q.Y., Johnson K.R. Association of cadherin 23 with polygenic inheritance and genetic modification of sensorineural hearing loss. Nat. Genet 2003, 35:21-23.
33. Ohlemiller K.K. Contributions of mouse models to understanding of age- and noise-related hearing loss. Brain Res 2006, 1091:89-102.
34. Ohlemiller K.K., McFadden S.L., Ding D.L., Lear P.M., Ho Y.S. Targeted mutation of the gene for cellular glutathione peroxidase (Gpx1) increases noise-induced hearing loss in mice. J. Assoc. Res. Otolaryngol 2000, 1:243-254.
35. Petkov P.M., Ding Y., Cassell M.A., Zhang W., Wagner G., Sargent E.E., Asquith S., Crew V., Johnson K.A., Robinson P., Scott V.E., Wiles M.V. An efficient SNP system for mouse genome scanning and elucidating strain relationships. Genome Res 2004, 14:1806-1811.
36. Ratkevicius A., Carroll A.M., Kilikevicius A., Venckunas T., McDermott K.T., Gray S.R., Wackerhage H., Lionikas A. H55N polymorphism as a likely cause of variation in citrate synthase activity of mouse skeletal muscle. Physiol. Genomics 2010, 42A:96-102.
37. Shin J.B., Streijger F., Beynon A., Peters T., Gadzala L., McMillen D., Bystrom C., Van der Zee C.E., Wallimann T., Gillespie P.G. Hair bundles are specialized for ATP delivery via creatine kinase. Neuron 2007, 53:371-386.
38. Siemens J., Lillo C., Dumont R.A., Reynolds A., Williams D.S., Gillespie P.G., Müller U. Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature 2004, 428:950-955.
39. Someya S., Prolla T.A. Mitochondrial oxidative damage and apoptosis in age-related hearing loss. Mech. Ageing Dev 2010, 131:480-486.
40. Someya S., Yamasoba T., Kujoth G.C., Pugh T.D., Weindruch R., Tanokura M., Prolla T.A. The role of mtDNA mutations in the pathogenesis of age-related hearing loss in mice carrying a mutator DNA polymerase gamma. Neurobiol. Aging 2008, 29:1080-1092.
41. Soucek S., Michaels L., Frohlich A. Evidence for hair cell degeneration as the primary lesion in hearing loss of the elderly. J. Otolaryngol 1986, 15:175-183.
42. Spongr V.P., Flood D.G., Frisina R.D., Salvi R.J. Quantitative measures of hair cell loss in CBA and C57BL/6 mice throughout their life spans. J. Acoust. Soc. Am 1997, 101:3546-3553.
43. Staecker H., Zheng Q.Y., Van De Water T.R. Oxidative stress in aging in the C57B16/J mouse cochlea. Acta Otolaryngol 2001, 121:666-672.
44. Yamasoba T., Someya S., Yamada C., Weindruch R., Prolla T.A., Tanokura M. Role of mitochondrial dysfunction and mitochondrial DNA mutations in age-related hearing loss. Hear. Res 2007, 226:185-193.
45. Zheng Q.Y., Ding D., Yu H., Salvi R.J., Johnson K.R. A locus on distal chromosome 10 (ahl4) affecting age-related hearing loss in A/J mice. Neurobiol. Aging 2009, 30:1693-1705.
46. Zheng Q.Y., Johnson K.R., Erway L.C. Assessment of hearing in 80 inbred strains of mice by ABR threshold analyses. Hear. Res 1999, 130:94-107.