SIRT3 mediates the antioxidant effect of hydrogen sulfide in endothelial cells

Antioxidants and Redox Signaling

Volumn 24, Issue 6, 2016, Pages 329-343

  Xie, Liping ^a   Feng, Haihua ^a   Li, Sha ^a   Meng, Guoliang ^a,b   Liu, Shangmin ^a   Tang, Xin ^a   Ma, Yan ^a   Han, Yi ^c   Xiao, Yujiao ^a   Gu, Yue ^a   Shao, Yongfeng ^a   Park, Chung Min ^d   Xian, Ming ^d   Huang, Yu ^e   Ferro, Albert ^f   Wang, Rui ^g   Moore, Philip K ^h   Wang, Hong ⁱ   Ji, Yong ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b NANTONG UNIVERSITY   (China)

^c Departments of Geriatrics   (China)

^d WASHINGTON STATE UNIVERSITY   (United States)

^e CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^f KING'S COLLEGE LONDON   (United Kingdom)

^g LAKEHEAD UNIVERSITY   (Canada)

^h NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

ⁱ Le University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CURCUMIN; CYTOPROTECTIVE AGENT; GYY 4173; HYDROGEN PEROXIDE; HYDROGEN SULFIDE; ISOCITRATE DEHYDROGENASE 2; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PARAQUAT; PROTEIN INHIBITOR; SIRTUIN 3; SR 11302; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG; ANTIOXIDANT; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BINDING AFFINITY; CELL DAMAGE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; GENETIC TRANSCRIPTION; MESENTERIC ARTERY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; VASODILATATION; ANIMAL; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; DRUG EFFECTS; GENETICS; METABOLISM; MUTANT MOUSE STRAIN; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; ANTIOXIDANTS; CELL LINE; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION; ENDOTHELIAL CELLS; HYDROGEN PEROXIDE; HYDROGEN SULFIDE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, MUTANT STRAINS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; SIRTUIN 3;

EID: 84958953105     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2015.6331     Document Type: Article

References (53)

1. Anderson KA and Hirschey MD. Mitochondrial protein acetylation regulates metabolism. Essays Biochem 52: 23-35, 2012.
2. Bellizzi D, Covello G, Di Cianni F, Tong Q, De Benedictis G. Identification of GATA2 and AP-1 Activator elements within the enhancer VNTR occurring in intron 5 of the human SIRT3 gene. Mol Cells 28: 87-92, 2009.
3. Biswas G, Guha M, Avadhani NG. Mitochondria-tonucleus stress signaling in mammalian cells: nature of nuclear gene targets, transcription regulation, induced resistance to apoptosis. Gene 354: 132-139, 2005.
4. Calenic B, Yaegaki K, Ishkitiev N, Kumazawa Y, Imai T, Tanaka T. p53-Pathway activity and apoptosis in hydrogen sulfide-exposed stem cells separated from human gingival epithelium. J Periodontal Res 48: 322-330, 2013.
5. Chen Y, Nie YC, Luo YL, Lin F, Zheng YF, Cheng GH, Wu H, Zhang KJ, Su WW, Shen JG, Li PB. Protective effects of naringin against paraquat-induced acute lung injury and pulmonary fibrosis in mice. Food Chem Toxicol 58: 133-140, 2013.
6. Chen Y, Zhang J, Lin Y, Lei Q, Guan KL, Zhao S, Xiong Y. Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep 12: 534-541, 2011.
7. Chen ZF, Zhao B, Tang XY, Li W, Zhu LL, Tang CS, DU JB, Jin HF. Hydrogen sulfide regulates vascular endoplasmic reticulum stress in apolipoprotein E knockout mice. Chin Med J (Engl) 124: 3460-3467, 2011.
8. Gao Y, Yao X, Zhang Y, Li W, Kang K, Sun L, Sun X. The protective role of hydrogen sulfide in myocardial ischemia-reperfusion-induced injury in diabetic rats. Int J Cardiol 152: 177-183, 2011.
9. Hirschey MD, Shimazu T, Goetzman E, Jing E, Schwer B, Lombard DB, Grueter CA, Harris C, Biddinger S, Ilkayeva OR, Stevens RD, Li Y, Saha AK, Ruderman NB, Bain JR, Newgard CB, Farese RJ, Alt FW, Kahn CR, Verdin E. SIRT3 regulates mitochondrial fatty acid oxidation by reversible enzyme deacetylation. Nature 464: 121-125, 2010.
10. Hirschey MD, Shimazu T, Jing E, Grueter CA, Collins AM, Aouizerat B, Stancakova A, Goetzman E, Lam MM, Schwer B, Stevens RD, Muehlbauer MJ, Kakar S, Bass NM, Kuusisto J, Laakso M, Alt FW, Newgard CB, Farese R J, Kahn CR, Verdin E. SIRT3 deficiency and mitochondrial protein hyperacetylation accelerate the development of the metabolic syndrome. Mol Cell 44: 177-190, 2011.
11. Hu LF, Lu M, Wu ZY, Wong PT, Bian JS. Hydrogen sulfide inhibits rotenone-induced apoptosis via preservation of mitochondrial function. Mol Pharmacol 75: 27-34, 2009.
12. Hu Y, Li R, Yang H, Luo H, Chen Z. Sirtuin 6 is essential for sodium sulfide-mediated cytoprotective effect in ischemia/reperfusion-stimulated brain endothelial cells. J Stroke Cerebrovasc Dis 24: 601-609, 2015.
13. Jeney V, Komodi E, Nagy E, Zarjou A, Vercellotti GM, Eaton JW, Balla G, Balla J. Supression of heminmediated oxidation of low-density lipoprotein and subsequent endothelial reactions by hydrogen sulfide (H(2)S). Free Radic Biol Med 46: 616-623, 2009.
14. Jin L, Wei W, Jiang Y, Peng H, Cai J, Mao C, Dai H, Choy W, Bemis JE, Jirousek MR, Milne JC, Westphal CH, Perni RB. Crystal structures of human SIRT3 displaying substrate-induced conformational changes. J Biol Chem 284: 24394-24405, 2009.
15. Kong X, Wang R, Xue Y, Liu X, Zhang H, Chen Y, Fang F, Chang Y. Sirtuin 3, a new target of PGC-1alpha, plays an important role in the suppression of ROS and mitochondrial biogenesis. PLoS One 5: e11707, 2010.
16. Li L, Fox B, Keeble J, Salto-Tellez M, Winyard PG, Wood ME, Moore PK, Whiteman M. The complex effects of the slow-releasing hydrogen sulfide donor GYY4137 in a model of acute joint inflammation and in human cartilage cells. J Cell Mol Med 17: 365-376, 2013.
17. Li L, Whiteman M, Guan YY, Neo KL, Cheng Y, Lee SW, Zhao Y, Baskar R, Tan CH, Moore PK. Characterization of a novel, water soluble hydrogen sulfide-releasing molecule (GYY4137): new insights into the biology of hydrogen sulfide. Circulation 117: 2351-2360, 2008.
18. Li X, Zhang KY, Zhang P, Chen L X, Wang L, Xie M, Wang CY, Tang XQ. Hydrogen sulfide inhibits formaldehyde-induced endoplasmic reticulum stress in PC12 cells by upregulation of SIRT-1. PLoS One 9: e89856, 2014.
19. Liu YH, Lu M, Hu LF, Wong PT, Webb GD, Bian JS. Hydrogen sulfide in the mammalian cardiovascular system. Antioxid Redox Signal 17: 141-185, 2012.
20. Liu Z, Han Y, Li L, Lu H, Meng G, Li X, Shirhan M, Peh MT, Xie L, Zhou S, Wang X, Chen Q, Dai W, Tan CH, Pan S, Moore PK, Ji Y. The hydrogen sulfide donor, GYY4137, exhibits anti-atherosclerotic activity in high fat fed apolipoprotein E(-/-) mice. Br J Pharmacol 169: 1795-1809, 2013.
21. Migliaccio E, Giorgio M, Mele S, Pelicci G, Reboldi P, Pandolfi PP, Lanfrancone L, Pelicci PG. The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature 402: 309-313, 1999.
22. Mortuza R, Chen S, Feng B, Sen S, Chakrabarti S. High glucose induced alteration of SIRTs in endothelial cells causes rapid aging in a p300 and FOXO regulated pathway. PLoS One 8: e54514, 2013.
23. Olmos Y, Valle I, Borniquel S, Tierrez A, Soria E, Lamas S, Monsalve M. Mutual dependence of Foxo3a and PGC-1alpha in the induction of oxidative stress genes. J Biol Chem 284: 14476-14484, 2009.
24. Papapetropoulos A, Pyriochou A, Altaany Z, Yang G, Marazioti A, Zhou Z, Jeschke MG, Branski LK, Herndon DN, Wang R, Szabo C. Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc Natl Acad Sci USA 106: 21972-21977, 2009.
25. Peek CB, Affinati AH, Ramsey KM, Kuo HY, Yu W, Sena LA, Ilkayeva O, Marcheva B, Kobayashi Y, Omura C, Levine DC, Bacsik DJ, Gius D, Newgard CB, Goetzman E, Chandel NS, Denu JM, Mrksich M, Bass J. Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science 342: 1243417, 2013.
26. Porter AG and Janicke RU. Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6: 99-104, 1999.
27. Purwantini E and Mukhopadhyay B. Conversion of NO2 to NO by reduced coenzyme F420 protects mycobacteria from nitrosative damage. Proc Natl Acad Sci USA 106: 6333-6338, 2009.
28. Qiu X, Brown K, Hirschey MD, Verdin E, Chen D. Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab 12: 662-667, 2010.
29. Rajendran P, Rengarajan T, Thangavel J, Nishigaki Y, Sakthisekaran D, Sethi G, Nishigaki I. The vascular endothelium and human diseases. Int J Biol Sci 9: 1057-1069, 2013.
30. Rinaldi L, Gobbi G, Pambianco M, Micheloni C, Mirandola P, Vitale M. Hydrogen sulfide prevents apoptosis of human PMN via inhibition of p38 and caspase 3. Lab Invest 86: 391-397, 2006.
31. Rocha M, Apostolova N, Hernandez-Mijares A, Herance R, Victor VM. Oxidative stress and endothelial dysfunction in cardiovascular disease: mitochondriatargeted therapeutics. Curr Med Chem 17: 3827-3841, 2010.
32. Shen Y, Guo W, Wang Z, Zhang Y, Zhong L, Zhu Y. Protective effects of hydrogen sulfide in hypoxic human umbilical vein endothelial cells: a possible mitochondriadependent pathway. Int J Mol Sci 14: 13093-13108, 2013.
33. Shrotriya S, Kundu JK, Na HK, Surh YJ. Diallyl trisulfide inhibits phorbol ester induced tumor promotion, activation of AP-1, expression of COX-2 in mouse skin by blocking JNK and Akt signaling. Cancer Res 70: 1932-1940, 2010.
34. Someya S, Yu W, Hallows WC, Xu J, Vann JM, Leeuwenburgh C, Tanokura M, Denu JM, Prolla TA. Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 143: 802-812, 2010.
35. Sundaresan NR, Gupta M, Kim G, Rajamohan SB, Isbatan A, Gupta MP. Sirt3 blocks the cardiac hypertrophic response by augmenting Foxo3a-dependent antioxidant defense mechanisms in mice. J Clin Invest 119: 2758-2771, 2009.
36. Suo R, Zhao ZZ, Tang ZH, Ren Z, Liu X, Liu LS, Wang Z, Tang CK, Wei DH, Jiang Z S. Hydrogen sulfide prevents H(2)O(2)-induced senescence in human umbilical vein endothelial cells through SIRT1 activation. Mol Med Rep 7: 1865-1870, 2013.
37. Tampo Y, Kotamraju S, Chitambar CR, Kalivendi SV, Keszler A, Joseph J, Kalyanaraman B. Oxidative stress-induced iron signaling is responsible for peroxidedependent oxidation of dichlorodihydrofluorescein in endothelial cells: role of transferrin receptor dependent iron uptake in apoptosis. Circ Res 92: 56-63, 2003.
38. Tao R, Coleman MC, Pennington JD, Ozden O, Park SH, Jiang H, Kim HS, Flynn CR, Hill S, Hayes MW, Olivier AK, Spitz DR, Gius D. Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol Cell 40: 893-904, 2010.
39. Tian G, Sawashita J, Kubo H, Nishio S Y, Hashimoto S, Suzuki N, Yoshimura H, Tsuruoka M, Wang Y, Liu Y, Luo H, Xu Z, Mori M, Kitano M, Hosoe K, Takeda T, Usami S, Higuchi K. Ubiquinol-10 supplementation activates mitochondria functions to decelerate senescence in senescence-accelerated mice. Antioxid Redox Signal 20: 2606-2620, 2014.
40. Tseng AH, Shieh SS, Wang DL. SIRT3 deacetylates FOXO3 to protect mitochondria against oxidative damage. Free Radic Biol Med 63: 222-234, 2013.
41. Vadivel A, Alphonse RS, Ionescu L, Machado DS, O'Reilly M, Eaton F, Haromy A, Michelakis ED, Thebaud B. Exogenous hydrogen sulfide (H2S) protects alveolar growth in experimental O2-induced neonatal lung injury. PLoS One 9: e90965, 2014.
42. Wang T, Wang L, Zaidi SR, Sammani S, Siegler J, Moreno-Vinasco L, Mathew B, Natarajan V, Garcia JG. Hydrogen sulfide attenuates particulate matter induced human lung endothelial barrier disruption via combined reactive oxygen species scavenging and Akt activation. Am J Respir Cell Mol Biol 47: 491-496, 2012.
43. Waypa GB, Osborne SW, Marks JD, Berkelhamer SK, Kondapalli J, Schumacker PT. Sirtuin 3 deficiency does not augment hypoxia-induced pulmonary hypertension. Am J Respir Cell Mol Biol 49: 885-891, 2013.
44. Wen YD, Wang H, Kho SH, Rinkiko S, Sheng X, Shen HM, Zhu YZ. Hydrogen sulfide protects HUVECs against hydrogen peroxide induced mitochondrial dysfunction and oxidative stress. PLoS One 8: e53147, 2013.
45. Winnik S, Auwerx J, Sinclair DA, Matter CM. Protective effects of sirtuins in cardiovascular diseases: from bench to bedside. Eur Heart J, 2015 [Epub ahead of print]; DOI: http://dx.doi.org/10.1093/eurheart/ehv290.
46. Xiao D, Li M, Herman-Antosiewicz A, Antosiewicz J, Xiao H, Lew KL, Zeng Y, Marynowski SW, Singh SV. Diallyl trisulfide inhibits angiogenic features of human umbilical vein endothelial cells by causing Akt inactivation and down-regulation of VEGF and VEGF-R2. Nutr Cancer 55: 94-107, 2006.
47. Xie L, Liu Z, Lu H, ZhangW, Mi Q, Li X, Tang Y, Chen Q, Ferro A, Ji Y. Pyridoxine inhibits endothelial NOS uncoupling induced by oxidized low-density lipoprotein via the PKCalpha signalling pathway in human umbilical vein endothelial cells. Br J Pharmacol 165: 754-764, 2012.
48. Xu ZS, Wang XY, Xiao DM, Hu L F, Lu M, Wu ZY, Bian JS. Hydrogen sulfide protects MC3T3-E1 osteoblastic cells against H2O2-induced oxidative damage-implications for the treatment of osteoporosis. Free Radic Biol Med 50: 1314-1323, 2011.
49. Yang G, Wu L, Bryan S, Khaper N, Mani S, Wang R. Cystathionine gamma-lyase deficiency and overproliferation of smooth muscle cells. Cardiovasc Res 86: 487-495, 2010.
50. Zhang LJ, Tao BB, Wang MJ, Jin HM, Zhu YC. PI3K p110alpha isoform-dependent Rho GTPase Rac1 activation mediates H2S-promoted endothelial cell migration via actin cytoskeleton reorganization. PLoS One 7: e44590, 2012.
51. Zhao D, Liu TZ, Chan EC, Fein H, Zhang X. A novel enzymatic method for determination of homocysteine using electrochemical hydrogen sulfide sensor. Front Biosci 12: 3774-3780, 2007.
52. Zhao W, Zhang J, Lu Y, Wang R. The vasorelaxant effect of H(2)S as a novel endogenous gaseous K(ATP) channel opener. EMBO J 20: 6008-6016, 2001.
53. Zheng M, Qiao W, Cui J, Liu L, Liu H, Wang Z, Yan C. Hydrogen sulfide delays nicotinamide-induced premature senescence via upregulation of SIRT1 in human umbilical vein endothelial cells. Mol Cell Biochem 393: 59-67, 2014.