Sirt3 protects cortical neurons against oxidative stress via regulating mitochondrial Ca2+ and mitochondrial biogenesis

International Journal of Molecular Sciences

Volumn 15, Issue 8, 2014, Pages 14591-14609

  Dai, Shu Hui ^a   Chen, Tao ^a,b   Wang, Yu Hai ^b   Zhu, Jie ^b   Luo, Peng ^a   Rao, Wei ^a   Yang, Yue Fan ^a   Fei, Zhou ^a   Jiang, Xiao Fan ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b Department of General Surgery   (China)

Author keywords

Mitochondria; Mitochondrial biogenesis; Oxidative stress; Sirt3

Indexed keywords

CALCIUM; HYDROGEN PEROXIDE; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; SIRTUIN 3;

ANIMAL; CELL LINE; DRUG EFFECTS; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; METABOLISM; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; NERVE CELL; OXIDATIVE STRESS; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; CALCIUM; CELL LINE; DNA, MITOCHONDRIAL; HUMANS; HYDROGEN PEROXIDE; IMMUNOHISTOCHEMISTRY; MITOCHONDRIA; MITOCHONDRIAL TURNOVER; NEURONS; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SIRTUIN 3;

EID: 84916632737     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms150814591     Document Type: Article

References (69)

1. Avery, S.V. Molecular targets of oxidative stress. Biochem. J. 2011, 434, 201-210
2. Luo, P.; Chen, T.; Zhao, Y.; Xu, H.; Huo, K.; Zhao, M.; Yang, Y.; Fei, Z. Protective effect of Homer 1a against hydrogen peroxide-induced oxidative stress in PC12 cells. Free Radic. Res. 2012, 46, 766-776
3. Krohn, K.; Maier, J.; Paschke, R. Mechanisms of disease: Hydrogen peroxide, DNA damage and mutagenesis in the development of thyroid tumors. Nat. Clin. Pract. Endocrinol. Metab. 2007, 3, 713-720
4. Stone, J.R. An assessment of proposed mechanisms for sensing hydrogen peroxide in mammalian systems. Arch. Biochem. Biophys. 2004, 422, 119-124
5. Halliwell, B.; Clement, M.V.; Long, L.H. Hydrogen peroxide in the human body. FEBS Lett. 2000, 486, 10-13
6. Armogida, M.; Nistico, R.; Mercuri, N.B. Therapeutic potential of targeting hydrogen peroxide metabolism in the treatment of brain ischaemia. Br. J. Pharmacol. 2012, 166, 1211-1224
7. Melo, A.; Monteiro, L.; Lima, R.M.; Oliveira, D.M.; Cerqueira, M.D.; El-Bacha, R.S. Oxidative stress in neurodegenerative diseases: Mechanisms and therapeutic perspectives. Oxid. Med. Cell. Longev. 2011, 2011, 467180
8. Cornelius, C.; Crupi, R.; Calabrese, V.; Graziano, A.; Milone, P.; Pennisi, G.; Radak, Z.; Calabrese, E.J.; Cuzzocrea, S. Traumatic brain injury: Oxidative stress and neuroprotection. Antioxid. Redox Signal. 2013, 19, 836-853
9. Brown, G.C.; Borutaite, V. Regulation of apoptosis by the redox state of cytochrome c. BBA Bioenerg. 2008, 1777, 877-881
10. Green, D.R. Apoptotic pathways: Ten minutes to dead. Cell 2005, 121, 671-674
11. Caroppi, P.; Sinibaldi, F.; Fiorucci, L.; Santucci, R. Apoptosis and human diseases: Mitochondrion damage and lethal role of released cytochrome c as proapoptotic protein. Curr. Med. Chem. 2009, 16, 4058-4065
12. Dias, T.R.; Rato, L.; Martins, A.D.; Simoes, V.L.; Jesus, T.T.; Alves, M.G.; Oliveira, P.F. Insulin deprivation decreases caspase-dependent apoptotic signaling in cultured rat sertoli cells. ISRN Urol. 2013, 2013, 970370
13. Simoes, V.L.; Alves, M.G.; Martins, A.D.; Dias, T.R.; Rato, L.; Socorro, S.; Oliveira, P.F. Regulation of apoptotic signaling pathways by 5α-dihydrotestosterone and 17β-estradiol in immature rat Sertoli cells. J. Steroid Biochem. Mol. Biol. 2013, 135, 15-23
14. Chan, P.H. Mitochondria and neuronal death/survival signaling pathways in cerebral ischemia. Neurochem. Res. 2004, 29, 1943-1949
15. Ye, R.; Yang, Q.; Kong, X.; Han, J.; Zhang, X.; Zhang, Y.; Li, P.; Liu, J.; Shi, M.; Xiong, L., et al. Ginsenoside Rd attenuates early oxidative damage and sequential inflammatory response after transient focal ischemia in rats. Neurochem. Int. 2011, 58, 391-398
16. Michan, S.; Sinclair, D. Sirtuins in mammals: Insights into their biological function. Biochem. J. 2007, 404, 1-13
17. Bause, A.S.; Haigis, M.C. Sirt3 regulation of mitochondrial oxidative stress. Exp. Gerontol. 2013, 48, 634-639
18. Pillai, V.B.; Sundaresan, N.R.; Kim, G.; Gupta, M.; Rajamohan, S.B.; Pillai, J.B.; Samant, S.; Ravindra, P.V.; Isbatan, A.; Gupta, M.P. Exogenous NAD blocks cardiac hypertrophic response via activation of the Sirt3-LKB1-AMP-activated kinase pathway. J. Biol. Chem. 2010, 285, 3133-3144
19. Lombard, D.B.; Alt, F.W.; Cheng, H.L.; Bunkenborg, J.; Streeper, R.S.; Mostoslavsky, R.; Kim, J.; Yancopoulos, G.; Valenzuela, D.; Murphy, A., et al. Mammalian Sir2 homolog Sirt3 regulates global mitochondrial lysine acetylation. Mol. Cell. Biol. 2007, 27, 8807-8814
20. Kim, S.H.; Lu, H.F.; Alano, C.C. Neuronal Sirt3 protects against excitotoxic injury in mouse cortical neuron culture. PLoS One 2011, 6, e14731
21. Tseng, A.H.; Shieh, S.S.; Wang, D.L. Sirt3 deacetylates FOXO3 to protect mitochondria against oxidative damage. Free Radic.Biol. Med. 2013, 63, 222-234
22. Haigis, M.C.; Guarente, L.P. Mammalian sirtuins-Emerging roles in physiology, aging, and calorie restriction. Genes Dev. 2006, 20, 2913-2921
23. Finkel, T.; Deng, C.X.; Mostoslavsky, R. Recent progress in the biology and physiology of sirtuins. Nature 2009, 460, 587-591
24. Kim, E.J.; Kho, J.H.; Kang, M.R.; Um, S.J. Active regulator of Sirt1 cooperates with Sirt1 and facilitates suppression of p53 activity. Mol. Cell 2007, 28, 277-290
25. Shindler, K.S.; Ventura, E.; Rex, T.S.; Elliott, P.; Rostami, A. Sirt1 activation confers neuroprotection in experimental optic neuritis. Investig. Ophthalmol. Vis. Sci. 2007, 48, 3602-3609
26. Sundaresan, N.R.; Gupta, M.; Kim, G.; Rajamohan, S.B.; Isbatan, A.; Gupta, M.P. Sirt3 blocks the cardiac hypertrophic response by augmenting FOXO3a-dependent antioxidant defense mechanisms in mice. J. Clin. Investig. 2009, 119, 2758-2771
27. Ahn, B.H.; Kim, H.S.; Song, S.; Lee, I.H.; Liu, J.; Vassilopoulos, A.; Deng, C.X.; Finkel, T. A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc. Natl. Acad. Sci. USA 2008, 105, 14447-14452
28. Park, S.H.; Ozden, O.; Jiang, H.; Cha, Y.I.; Pennington, J.D.; Aykin-Burns, N.; Spitz, D.R.; Gius, D.; Kim, H.S. Sirt3, Mitochondrial ROS, ageing, and carcinogenesis. Int. J. Mol. Sci. 2011, 12, 6226-6239
29. Verdin, E.; Hirschey, M.D.; Finley, L.W.; Haigis, M.C. Sirtuin regulation of mitochondria: Energy production, apoptosis, and signaling. Trends Biochem. Sci. 2010, 35, 669-675
30. Guarente, L. Mitochondria-A nexus for aging, calorie restriction, and sirtuins? Cell 2008, 132, 171-176
31. Smith, K.T.; Workman, J.L. Introducing the acetylome. Nat. biotechnol. 2009, 27, 917-919
32. Marfe, G.; Tafani, M.; Indelicato, M.; Sinibaldi-Salimei, P.; Reali, V.; Pucci, B.; Fini, M.; Russo, M.A. Kaempferol induces apoptosis in two different cell lines via Akt inactivation, Bax and Sirt3 activation, and mitochondrial dysfunction. J. Cell. Biochem. 2009, 106, 643-650
33. Allison, S.J.; Milner, J. Sirt3 is pro-apoptotic and participates in distinct basal apoptotic pathways. Cell Cycle 2007, 6, 2669-2677
34. Yang, H.; Yang, T.; Baur, J.A.; Perez, E.; Matsui, T.; Carmona, J.J.; Lamming, D.W.; Souza-Pinto, N.C.; Bohr, V.A.; Rosenzweig, A., et al. Nutrient-sensitive mitochondrial NAD+ levels dictate cell survival. Cell 2007, 130, 1095-1107
35. Sundaresan, N.R.; Samant, S.A.; Pillai, V.B.; Rajamohan, S.B.; Gupta, M.P. Sirt3 is a stress-responsive deacetylase in cardiomyocytes that protects cells from stress-mediated cell death by deacetylation of Ku70. Mol. Cell. Biol. 2008, 28, 6384-6401
36. Kincaid, B.; Bossy-Wetzel, E. Forever young: Sirt3 a shield against mitochondrial meltdown, aging, and neurodegeneration. Front. Aging Neurosci. 2013, 5, 48
37. Rato, L.; Duarte, A.I.; Tomas, G.D.; Santos, M.S.; Moreira, P.I.; Socorro, S.; Cavaco, J.E.; Alves, M.G.; Oliveira, P.F. Pre-diabetes alters testicular PGC1-α/Sirt3 axis modulating mitochondrial bioenergetics and oxidative stress. BBA Bioenerg. 2014, 1837, 335-344
38. Kong, X.; Wang, R.; Xue, Y.; Liu, X.; Zhang, H.; Chen, Y.; Fang, F.; Chang, Y. Sirtuin 3, a new target of PGC-1α, plays an important role in the suppression of ROS and mitochondrial biogenesis. PLoS One 2010, 5, e11707
39. Hafner, A.V.; Dai, J.; Gomes, A.P.; Xiao, C.Y.; Palmeira, C.M.; Rosenzweig, A.; Sinclair, D.A. Regulation of the mPTP by Sirt3-mediated deacetylation of CypD at lysine 166 suppresses age-related cardiac hypertrophy. Aging 2010, 2, 914-923
40. Shulga, N.; Wilson-Smith, R.; Pastorino, J.G. Sirtuin-3 deacetylation of cyclophilin D induces dissociation of hexokinase II from the mitochondria. J. Cell Sci. 2010, 123, 894-902
41. Schild, L.; Huppelsberg, J.; Kahlert, S.; Keilhoff, G.; Reiser, G. Brain mitochondria are primed by moderate Ca2+ rise upon hypoxia/reoxygenation for functional breakdown and morphological disintegration. J. Biol. Chem. 2003, 278, 25454-25460
42. Starkov, A.A.; Chinopoulos, C.; Fiskum, G. Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 2004, 36, 257-264
43. Brookes, P.S.; Yoon, Y.; Robotham, J.L.; Anders, M.W.; Sheu, S.S. Calcium, ATP, and ROS: A mitochondrial love-hate triangle. Am. J. Physiol. Cell Physiol. 2004, 287, C817-C833
44. Tanaka, K.; Iijima, T.; Mishima, T.; Suga, K.; Akagawa, K.; Iwao, Y. Ca2+ buffering capacity of mitochondria after oxygen-glucose deprivation in hippocampal neurons. Neurochem. Res. 2009, 34, 221-226
45. Martinez-Sanchez, M.; Striggow, F.; Schroder, U.H.; Kahlert, S.; Reymann, K.G.; Reiser, G. Na+ and Ca2+ homeostasis pathways, cell death and protection after oxygen-glucose-deprivation in organotypic hippocampal slice cultures. Neuroscience 2004, 128, 729-740
46. Peng, T.I.; Jou, M.J. Oxidative stress caused by mitochondrial calcium overload. Ann. N. Y. Acad. Sci. 2010, 1201, 183-188
47. Zong, W.X.; Li, C.; Hatzivassiliou, G.; Lindsten, T.; Yu, Q.C.; Yuan, J.; Thompson, C.B. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J. Cell Biol. 2003, 162, 59-69
48. Pinton, P.; Ferrari, D.; Rapizzi, E.; di Virgilio, F.; Pozzan, T.; Rizzuto, R. The Ca2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: Significance for the molecular mechanism of Bcl-2 action. EMBO J. 2001, 20, 2690-2701
49. Scorrano, L.; Korsmeyer, S.J. Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem. Biophys. Res. Commun. 2003, 304, 437-444
50. Nicholls, D.G.; Chalmers, S. The integration of mitochondrial calcium transport and storage. J. Bioenerg. Biomembr. 2004, 36, 277-281
51. Baughman, J.M.; Perocchi, F.; Girgis, H.S.; Plovanich, M.; Belcher-Timme, C.A.; Sancak, Y.; Bao, X.R.; Strittmatter, L.; Goldberger, O.; Bogorad, R.L., et al. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 2011, 476, 341-345
52. Fukumori, R.; Takarada, T.; Nakazato, R.; Fujikawa, K.; Kou, M.; Hinoi, E.; Yoneda, Y. Selective inhibition by ethanol of mitochondrial calcium influx mediated by uncoupling protein-2 in relation to N-methyl-D-aspartate cytotoxicity in cultured neurons. PLoS One 2013, 8, e69718
53. Vassalle, M.; Lin, C.I. Calcium overload and cardiac function. J. Biomed. Sci. 2004, 11, 542-565
54. Tian, Y.; Li, B.; Shi, W.Z.; Chang, M.Z.; Zhang, G.J.; Di, Z.L.; Liu, Y. Dynamin-related protein 1 inhibitors protect against ischemic toxicity through attenuating mitochondrial Ca2+ uptake from endoplasmic reticulum store in PC12 cells. Int. J. Mol. Sci. 2014, 15, 3172-3185
55. Cheng, A.; Hou, Y.; Mattson, M.P. Mitochondria and neuroplasticity. ASN Neuro 2010, 2, e00045
56. Seo, A.Y.; Joseph, A.M.; Dutta, D.; Hwang, J.C.; Aris, J.P.; Leeuwenburgh, C. New insights into the role of mitochondria in aging: mitochondrial dynamics and more. J. Cell Sci. 2010, 123, 2533-2542
57. McLeod, C.J.; Pagel, I.; Sack, M.N. The mitochondrial biogenesis regulatory program in cardiac adaptation to ischemia-A putative target for therapeutic intervention. Trends Cardiovasc. Med. 2005, 15, 118-123
58. Ljubicic, V.; Joseph, A.M.; Saleem, A.; Uguccioni, G.; Collu-Marchese, M.; Lai, R.Y.; Nguyen, L.M.; Hood, D.A. Transcriptional and post-transcriptional regulation of mitochondrial biogenesis in skeletal muscle: Effects of exercise and aging. BBA Gen. Subj. 2010, 1800, 223-234
59. Vina, J.; Gomez-Cabrera, M.C.; Borras, C.; Froio, T.; Sanchis-Gomar, F.; Martinez-Bello, V.E.; Pallardo, F.V. Mitochondrial biogenesis in exercise and in ageing. Adv. Drug Deliv. Rev. 2009, 61, 1369-1374
60. Nisoli, E.; Carruba, M.O. Nitric oxide and mitochondrial biogenesis. J. Cell Sci. 2006, 119, 2855-2862
61. Weir, H.J.; Murray, T.K.; Kehoe, P.G.; Love, S.; Verdin, E.M.; O'Neill, M.J.; Lane, J.D.; Balthasar, N. CNS Sirt3 expression is altered by reactive oxygen species and in Alzheimer's disease. PLoS One 2012, 7, e48225
62. Sano, R.; Annunziata, I.; Patterson, A.; Moshiach, S.; Gomero, E.; Opferman, J.; Forte, M.; d'Azzo, A. GM1-ganglioside accumulation at the mitochondria-associated ER membranes links ER stress to Ca2+-dependent mitochondrial apoptosis. Mol. Cell 2009, 36, 500-511
63. Kaufman, R.J.; Malhotra, J.D. Calcium trafficking integrates endoplasmic reticulum function with mitochondrial bioenergetics. BBA Mol. Cell Res. 2014, 1843, 2233-2239
64. Baumeister, P.; Dong, D.; Fu, Y.; Lee, A.S. Transcriptional induction of GRP78/BiP by histone deacetylase inhibitors and resistance to histone deacetylase inhibitor-induced apoptosis. Mol. Cancer Ther. 2009, 8, 1086-1094
65. Ageberg, M.; Rydstrom, K.; Relander, T.; Drott, K. The histone deacetylase inhibitor valproic acid sensitizes diffuse large B-cell lymphoma cell lines to CHOP-induced cell death. Am. J. Transl. Res. 2013, 5, 170-183
66. Redmond, L.; Kashani, A.H.; Ghosh, A. Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 2002, 34, 999-1010
67. Chen, T.; Yang, Y.F.; Luo, P.; Liu, W.; Dai, S.H.; Zheng, X.R.; Fei, Z.; Jiang, X.F. Homer1 knockdown protects dopamine neurons through regulating calcium homeostasis in an in vitro model of Parkinson's disease. Cell. Signal. 2013, 25, 2863-2870
68. Chen, H.; Hu, C.J.; He, Y.Y.; Yang, D.I.; Xu, J.; Hsu, C.Y. Reduction and restoration of mitochondrial dna content after focal cerebral ischemia/reperfusion. Stroke 2001, 32, 2382-2387
69. Parone, P.A.; Da Cruz, S.; Han, J.S.; McAlonis-Downes, M.; Vetto, A.P.; Lee, S.K.; Tseng, E.; Cleveland, D.W. Enhancing mitochondrial calcium buffering capacity reduces aggregation of misfolded SOD1 and motor neuron cell death without extending survival in mouse models of inherited amyotrophic lateral sclerosis. J. Neurosci. 2013, 33, 4657-4671.