Age-related decrease in the mitochondrial sirtuin deacetylase sirt3 expression associated with ROS accumulation in the auditory cortex of the mimetic aging rat model

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Zeng, Lingling ^a   Yang, Yang ^a   Hu, Yujuan ^a   Sun, Yu ^a   Du, Zhengde ^b   Xie, Zhen ^a   Zhou, Tao ^a   Kong, Weijia ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b GUANGDONG MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GALACTOSE; MALONALDEHYDE; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; SIRTUIN 3;

ACETYLATION; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUDITORY CORTEX; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME REGULATION; GENE DELETION; GENOME SIZE; HISTOPATHOLOGY; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRESBYACUSIS; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION;

ACETYLATION; AGING; ANIMALS; APOPTOSIS; AUDITORY CORTEX; DISEASE MODELS, ANIMAL; DNA, MITOCHONDRIAL; GALACTOSE; GENE EXPRESSION; MALONDIALDEHYDE; MITOCHONDRIA; OXIDATIVE STRESS; PRESBYCUSIS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SIRTUIN 3; SUPEROXIDE DISMUTASE;

EID: 84895089601     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088019     Document Type: Article

References (64)

1. Fetoni AR, Picciotti PM, Paludetti G, Troiani D (2011) Pathogenesis of presbycusis in animal models: a review. Exp Gerontol 46: 413-425.
2. Humes LE, Dubno JR, Gordon-Salant S, Lister JJ, Cacace AT, et al. (2012) Central presbycusis: a review and evaluation of the evidence. J Am Acad Audiol 23: 635-666.
3. King AJ, Bajo VM, Bizley JK, Campbell RA, Nodal FR, et al. (2007) Physiological and behavioral studies of spatial coding in the auditory cortex. Hear Res 229: 106-115. (Pubitemid 46920880)
4. Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120: 483-495. (Pubitemid 40269763)
5. Mao P, Reddy PH (2011) Aging and amyloid beta-induced oxidative DNA damage and mitochondrial dysfunction in Alzheimer's disease: implications for early intervention and therapeutics. Biochim Biophys Acta 1812: 1359-1370.
6. Bohr VA, Anson RM (1995) DNA damage, mutation and fine structure DNA repair in aging. Mutat Res 338: 25-34.
7. Warner HR (1994) Superoxide dismutase, aging, and degenerative disease. Free Radic Biol Med 17: 249-258.
8. Levine RL, Stadtman ER (2001) Oxidative modification of proteins during aging. Exp Gerontol 36: 1495-1502. (Pubitemid 32768727)
9. Radak Z, Zhao Z, Goto S, Koltai E (2011) Age-associated neurodegeneration and oxidative damage to lipids, proteins and DNA. Mol Aspects Med 32: 305-315.
10. Richter C, Park JW, Ames BN (1988) Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc Natl Acad Sci U S A 85: 6465-6467.
11. Mao P, Gallagher P, Nedungadi S, Manczak M, Shirendeb UP, et al. (2012) Mitochondrial DNA deletions and differential mitochondrial DNA content in Rhesus monkeys: implications for aging. Biochim Biophys Acta 1822: 111-119.
12. Meissner C, Bruse P, Mohamed SA, Schulz A, Warnk H, et al. (2008) The 4977 bp deletion of mitochondrial DNA in human skeletal muscle, heart and different areas of the brain: a useful biomarker or more? Exp Gerontol 43: 645-652.
13. Markaryan A, Nelson EG, Hinojosa R (2009) Quantification of the mitochondrial DNA common deletion in presbycusis. Laryngoscope 119: 1184-1189.
14. Ross OA, Hyland P, Curran MD, McIlhatton BP, Wikby A, et al. (2002) Mitochondrial DNA damage in lymphocytes: a role in immunosenescence? Exp Gerontol 37: 329-340. (Pubitemid 34073551)
15. Chen B, Zhong Y, Peng W, Sun Y, Hu YJ, et al. (2011) Increased mitochondrial DNA damage and decreased base excision repair in the auditory cortex of D-galactose-induced aging rats. Mol Biol Rep 38: 3635-3642.
16. Dumont M, Beal MF (2011) Neuroprotective strategies involving ROS in Alzheimer disease. Free Radic Biol Med 51: 1014-1026.
17. Tretter L, Sipos I, Adam-Vizi V (2004) Initiation of neuronal damage by complex I deficiency and oxidative stress in Parkinson's disease. Neurochem Res 29: 569-577. (Pubitemid 38295007)
18. Patten DA, Germain M, Kelly MA, Slack RS (2010) Reactive oxygen species: stuck in the middle of neurodegeneration. J Alzheimers Dis 20 Suppl 2: S357-367.
19. Jacono AA, Hu B, Kopke RD, Henderson D, Van De Water TR, et al. (1998) Changes in cochlear antioxidant enzyme activity after sound conditioning and noise exposure in the chinchilla. Hear Res 117: 31-38. (Pubitemid 28157428)
20. 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. (Pubitemid 29352358)
21. Fortunato G, Marciano E, Zarrilli F, Mazzaccara C, Intrieri M, et al. (2004) Paraoxonase and superoxide dismutase gene polymorphisms and noise-induced hearing loss. Clin Chem 50: 2012-2018. (Pubitemid 39425837)
22. Jiang H, Talaska AE, Schacht J, Sha SH (2007) Oxidative imbalance in the aging inner ear. Neurobiol Aging 28: 1605-1612. (Pubitemid 47238531)
23. Kong WJ, Wang Y, Wang Q, Hu YJ, Han YC, et al. (2006) The relation between D-galactose injection and mitochondrial DNA 4834 bp deletion mutation. Exp Gerontol 41: 628-634. (Pubitemid 43867227)
24. Kong WJ, Hu YJ, Wang Q, Wang Y, Han YC, et al. (2006) The effect of the mtDNA4834 deletion on hearing. Biochem Biophys Res Commun 344: 425-430.
25. Imai S, Johnson FB, Marciniak RA, McVey M, Park PU, et al. (2000) Sir2: an NAD-dependent histone deacetylase that connects chromatin silencing, metabolism, and aging. Cold Spring Harb Symp Quant Biol 65: 297-302. (Pubitemid 32611950)
26. Dali-Youcef N, Lagouge M, Froelich S, Koehl C, Schoonjans K, et al. (2007) Sirtuins: the 'magnificent seven', function, metabolism and longevity. Ann Med 39: 335-345.
27. Michishita E, Park JY, Burneskis JM, Barrett JC, Horikawa I (2005) Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol Biol Cell 16: 4623-4635. (Pubitemid 41416446)
28. Pellegrini L, Pucci B, Villanova L, Marino ML, Marfe G, et al. (2012) SIRT3 protects from hypoxia and staurosporine-mediated cell death by maintaining mitochondrial membrane potential and intracellular pH. Cell Death Differ 19: 1815-1825.
29. Lombard DB, Alt FW, Cheng HL, Bunkenborg J, Streeper RS, et al. (2007) Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol Cell Biol 27: 8807-8814.
30. Buler M, Aatsinki SM, Izzi V, Hakkola J (2012) Metformin reduces hepatic expression of SIRT3, the mitochondrial deacetylase controlling energy metabolism. PLoS One 7: e49863.
31. Kong X, Wang R, Xue Y, Liu X, Zhang H, et al. (2010) Sirtuin 3, a new target of PGC-1alpha, plays an important role in the suppression of ROS and mitochondrial biogenesis. PLoS One 5: e11707.
32. Sack MN, Finkel T (2012) Mitochondrial metabolism, sirtuins, and aging. Cold Spring Harb Perspect Biol 4.
33. D'Aquila P, Rose G, Panno ML, Passarino G, Bellizzi D (2012) SIRT3 gene expression: a link between inherited mitochondrial DNA variants and oxidative stress. Gene 497: 323-329.
34. Ahn BH, Kim HS, Song S, Lee IH, Liu J, et al. (2008) A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc Natl Acad Sci U S A 105: 14447-14452.
35. Hirschey MD, Shimazu T, Goetzman E, Jing E, Schwer B, et al. (2010) SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464: 121-125.
36. Shimazu T, Hirschey MD, Hua L, Dittenhafer-Reed KE, Schwer B, et al. (2010) SIRT3 deacetylates mitochondrial 3-hydroxy-3-methylglutaryl CoA synthase 2 and regulates ketone body production. Cell Metab 12: 654-661.
37. He W, Newman JC, Wang MZ, Ho L, Verdin E (2012) Mitochondrial sirtuins: regulators of protein acylation and metabolism. Trends Endocrinol Metab 23: 467-476.
38. Alhazzazi TY, Kamarajan P, Verdin E, Kapila YL (2011) SIRT3 and cancer: tumor promoter or suppressor? Biochim Biophys Acta 1816: 80-88.
39. Finley LW, Haas W, Desquiret-Dumas V, Wallace DC, Procaccio V, et al. (2011) Succinate dehydrogenase is a direct target of sirtuin 3 deacetylase activity. PLoS One 6: e23295.
40. Qiu X, Brown K, Hirschey MD, Verdin E, Chen D (2010) Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab 12: 662-667.
41. Chen Y, Zhang J, Lin Y, Lei Q, Guan KL, et al. (2011) Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep 12: 534-541.
42. Tao R, Coleman MC, Pennington JD, Ozden O, Park SH, et al. (2010) Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol Cell 40: 893-904.
43. Shi T, Wang F, Stieren E, Tong Q (2005) SIRT3, a mitochondrial sirtuin deacetylase, regulates mitochondrial function and thermogenesis in brown adipocytes. J Biol Chem 280: 13560-13567. (Pubitemid 40517248)
44. Miao L, St Clair DK (2009) Regulation of superoxide dismutase genes: implications in disease. Free Radic Biol Med 47: 344-356.
45. Chetty C, Lakka SS, Bhoopathi P, Kunigal S, Geiss R, et al. (2008) Tissue inhibitor of metalloproteinase 3 suppresses tumor angiogenesis in matrix metalloproteinase 2-down-regulated lung cancer. Cancer Res 68: 4736-4745.
46. Someya S, Prolla TA (2010) Mitochondrial oxidative damage and apoptosis in age-related hearing loss. Mech Ageing Dev 131: 480-486.
47. Seidman MD (2000) Effects of dietary restriction and antioxidants on presbyacusis. Laryngoscope 110: 727-738.
48. Weir HJ, Murray TK, Kehoe PG, Love S, Verdin EM, et al. (2012) CNS SIRT3 expression is altered by reactive oxygen species and in Alzheimer's disease. PLoS One 7: e48225.
49. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11: 298-300.
50. Reddy PH (2009) Role of mitochondria in neurodegenerative diseases: mitochondria as a therapeutic target in Alzheimer's disease. CNS Spectr 14: 8-13; discussion 16-18.
51. Cuatrecasas P, Segal S (1966) Galactose conversion to D-xylulose: an alternate route of galactose metabolism. Science 153: 549-551.
52. Jordens RG, Berry MD, Gillott C, Boulton AA (1999) Prolongation of life in an experimental model of aging in Drosophila melanogaster. Neurochem Res 24: 227-233. (Pubitemid 29067964)
53. Cui X, Wang L, Zuo P, Han Z, Fang Z, et al. (2004) D-galactose-caused life shortening in Drosophila melanogaster and Musca domestica is associated with oxidative stress. Biogerontology 5: 317-325. (Pubitemid 41449159)
54. Wei H, Li L, Song Q, Ai H, Chu J, et al. (2005) Behavioural study of the D-galactose induced aging model in C57BL/6J mice. Behav Brain Res 157: 245-251. (Pubitemid 40082567)
55. Zhang Q, Li X, Cui X, Zuo P (2005) D-galactose injured neurogenesis in the hippocampus of adult mice. Neurol Res 27: 552-556. (Pubitemid 41040845)
56. Ho SC, Liu JH, Wu RY (2003) Establishment of the mimetic aging effect in mice caused by D-galactose. Biogerontology 4: 15-18.
57. Lei H, Wang B, Li WP, Yang Y, Zhou AW, et al. (2003) Anti-aging effect of astragalosides and its mechanism of action. Acta Pharmacol Sin 24: 230-234. (Pubitemid 36286009)
58. Tian J, Ishibashi K, Ishibashi K, Reiser K, Grebe R, et al. (2005) Advanced glycation endproduct-induced aging of the retinal pigment epithelium and choroid: a comprehensive transcriptional response. Proc Natl Acad Sci U S A 102: 11846-11851. (Pubitemid 41170813)
59. Engle JR, Recanzone GH (2012) Characterizing spatial tuning functions of neurons in the auditory cortex of young and aged monkeys: a new perspective on old data. Front Aging Neurosci 4: 36.
60. Giralt A, Villarroya F (2012) SIRT3, a pivotal actor in mitochondrial functions: metabolism, cell death and aging. Biochem J 444: 1-10.
61. Brown K, Xie S, Qiu X, Mohrin M, Shin J, et al. (2013) SIRT3 reverses aging-associated degeneration. Cell Rep 3: 319-327.
62. Choudhury M, Jonscher KR, Friedman JE (2011) Reduced mitochondrial function in obesity-associated fatty liver: SIRT3 takes on the fat. Aging (Albany NY) 3: 175-178.
63. Wu YT, Lee HC, Liao CC, Wei YH (2013) Regulation of mitochondrial F(o)F(1)ATPase activity by Sirt3-catalyzed deacetylation and its deficiency in human cells harboring 4977bp deletion of mitochondrial DNA. Biochim Biophys Acta 1832: 216-227.
64. Jing E, Emanuelli B, Hirschey MD, Boucher J, Lee KY, et al. (2011) Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc Natl Acad Sci U S A 108: 14608-14613.