Activation of SIRT3 by resveratrol ameliorates cardiac fibrosis and improves cardiac function via the TGF-β/smad3 pathway

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 308, Issue 5, 2015, Pages H424-H434

  Chen, Tongshuai ^a,b   Li, Jingyuan ^a,b   Liu, Junni ^b   Li, Na ^a,b   Wang, Shujian ^a,b   Liu, Hui ^a,b   Zeng, Mei ^a,b   Zhang, Yun ^a,b   Bu, Peili ^a,b  

^a SHANDONG UNIVERSITY   (China)

^b SHANDONG UNIVERSITY   (China)

Author keywords

Cardiac function; Fibrosis; Mothers against decapentaplegic homolog 3; Resveratrol; Sirtuin 3; Transforming growth factor

Indexed keywords

COLLAGEN; RESVERATROL; SIRTUIN 3; SMAD3 PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TRANSFORMING GROWTH FACTOR BETA; SIRT3 PROTEIN, MOUSE; SMAD3 PROTEIN, MOUSE; STILBENE DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HEART FIBROBLAST; HEART FUNCTION; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CARDIOMEGALY; CELL CULTURE; DRUG EFFECTS; FIBROSIS; HEART; HEART MUSCLE; HEART MUSCLE CELL; MALE; METABOLISM; MYOFIBROBLAST; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CARDIOMEGALY; CELLS, CULTURED; COLLAGEN; FIBROSIS; HEART; MALE; MICE; MYOCARDIUM; MYOCYTES, CARDIAC; MYOFIBROBLASTS; SIRTUIN 3; SMAD3 PROTEIN; STILBENES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84928635872     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00454.2014     Document Type: Article

References (43)

1. Ahn BH, Kim HS, Song S, Lee IH, Liu J, Vassilopoulos A, Deng CX, Finkel T. A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc Natl Acad Sci USA 105: 14447–14452, 2008.
2. Banks AS, Kon N, Knight C, Matsumoto M, Gutierrez-Juarez R, Rossetti L, Gu W, Accili D. Sirt1 gain of function increases energy efficiency and prevents diabetes in mice. Cell Metab 8: 333–341, 2008.
3. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, Ramaswamy S, Fishbein KW, Spencer RG, Lakatta EG, Le Couteur D, Shaw RJ, Navas P, Puigserver P, Ingram DK, de Cabo R, Sinclair DA. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444: 337–342, 2006.
4. Bellizzi D, Rose G, Cavalcante P, Covello G, Dato S, De Rango F, Greco V, Maggiolini M, Feraco E, Mari V, Franceschi C, Passarino G, De Benedictis G. A novel VNTR enhancer within the SIRT3 gene, a human homologue of SIR2, is associated with survival at oldest ages. Genomics 85: 258–263, 2005.
5. Bordone L, Cohen D, Robinson A, Motta MC, van Veen E, Czopik A, Steele AD, Crowe H, Marmor S, Luo J, Gu W, Guarente L. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 6: 759–767, 2007.
6. Burstein B, Nattel S. Atrial fibrosis: mechanisms and clinical relevance in atrial fibrillation. J Am Coll Cardiol 51: 802–809, 2008.
7. Canto C, Jiang LQ, Deshmukh AS, Mataki C, Coste A, Lagouge M, Zierath JR, Auwerx J. Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab 11: 213–219, 2010.
8. Dolinsky VW, Chakrabarti S, Pereira TJ, Oka T, Levasseur J, Beker D, Zordoky BN, Morton JS, Nagendran J, Lopaschuk GD, Davidge ST, Dyck JR. Resveratrol prevents hypertension and cardiac hypertrophy in hypertensive rats and mice. Biochim Biophys Acta 1832: 1723–1733, 2013.
9. Donmez G, Wang D, Cohen DE, Guarente L. SIRT1 suppresses _-amyloid production by activating the alpha-secretase gene ADAM10. Cell 142: 320–332, 2010.
10. Fang Z, Tang Y, Jiao W, Xing Z, Guo Z, Wang W, Xu Z, Liu Z. Nitidine chloride induces apoptosis and inhibits tumor cell proliferation via suppressing ERK signaling pathway in renal cancer. Food Chem Toxicol 66: 210–216, 2014.
11. Fulco M, Cen Y, Zhao P, Hoffman EP, McBurney MW, Sauve AA, Sartorelli V. Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev Cell 14: 661–673, 2008.
12. Gao S, Ho D, Vatner DE, Vatner SF. Echocardiography in mice. Curr Protoc Mouse Biol 1: 71–83, 2011.
13. Gertz M, Nguyen GT, Fischer F, Suenkel B, Schlicker C, Franzel B, Tomaschewski J, Aladini F, Becker C, Wolters D, Steegborn C. A molecular mechanism for direct sirtuin activation by resveratrol. PLos One 7: e49761, 2012.
14. Guarente L. Sirtuins as potential targets for metabolic syndrome. Nature 444: 868–874, 2006.
15. Gustafsson AB, Brunton LL. β-Adrenergic stimulation of rat cardiac fibroblasts enhances induction of nitric-oxide synthase by interleukin-1β via message stabilization. Mol Pharmacol 58: 1470–1478, 2000.
16. Heilbronn LK, de Jonge L, Frisard MI, DeLany JP, Larson-Meyer DE, Rood J, Nguyen T, Martin CK, Volaufova J, Most MM, Greenway FL, Smith SR, Deutsch WA, Williamson DA, Ravussin E, Pennington CT. Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals: a randomized controlled trial. JAMA 295: 1539–1548, 2006.
17. Herranz D, Munoz-Martin M, Canamero M, Mulero F, Martinez- Pastor B, Fernandez-Capetillo O, Serrano M. Sirt1 improves healthy ageing and protects from metabolic syndrome-associated cancer. Nat Commun 1: 3, 2010.
18. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, Zipkin RE, Chung P, Kisielewski A, Zhang LL, Scherer B, Sinclair DA. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425: 191–196, 2003.
19. Khan R, Sheppard R. Fibrosis in heart disease: understanding the role of transforming growth factor-beta in cardiomyopathy, valvular disease and arrhythmia. Immunology 118: 10–24, 2006.
20. Koubova J, Guarente L. How does calorie restriction work? Genes Dev 17: 313–321, 2003.
21. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P, Auwerx J. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α. Cell 127: 1109–1122, 2006.
22. Lanza IR, Short DK, Short KR, Raghavakaimal S, Basu R, Joyner MJ, McConnell JP, Nair KS. Endurance exercise as a countermeasure for aging. Diabetes 57: 2933–2942, 2008.
23. Li B, Comai L. Functional interaction between Ku and the werner syndrome protein in DNA end processing. J Biol Chem 275: 28349–28352, 2000.
24. Lin SJ, Defossez PA, Guarente L. Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 289: 2126–2128, 2000.
25. Masoro EJ. Caloric restriction and aging: an update. Exp Gerontol 35: 299–305, 2000.
26. Meguro T, Hong C, Asai K, Takagi G, McKinsey TA, Olson EN, Vatner SF. Cyclosporine attenuates pressure-overload hypertrophy in mice while enhancing susceptibility to decompensation and heart failure. Circ Res 84: 735–740, 1999.
27. Pearson KJ, Baur JA, Lewis KN, Peshkin L, Price NL, Labinskyy N, Swindell WR, Kamara D, Minor RK, Perez E, Jamieson HA, Zhang Y, Dunn SR, Sharma K, Pleshko N, Woollett LA, Csiszar A, Ikeno Y, Le Couteur D, Elliott PJ, Becker KG, Navas P, Ingram DK, Wolf NS, Ungvari Z, Sinclair DA, de Cabo R. Resveratrol delays age-related deterioration and mimics transcriptional aspects of dietary restriction without extending life span. Cell Metab 8: 157–168, 2008.
28. Pfluger PT, Herranz D, Velasco-Miguel S, Serrano M, Tschop MH. Sirt1 protects against high-fat diet-induced metabolic damage. Proc Natl Acad Sci USA 105: 9793–9798, 2008.
29. Pugh TD, Klopp RG, Weindruch R. Controlling caloric consumption: protocols for rodents and rhesus monkeys. Neurobiol Aging 20: 157–165, 1999.
30. 1. Am J Physiol Heart Circ Physiol 283: H1253–H1262, 2002.
31. Sohal RS, Weindruch R. Oxidative stress, caloric restriction, and aging. Science 273: 59–63, 1996.
32. 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.
33. Suchankova G, Nelson LE, Gerhart-Hines Z, Kelly M, Gauthier MS, Saha AK, Ido Y, Puigserver P, Ruderman NB. Concurrent regulation of AMP-activated protein kinase and SIRT1 in mammalian cells. Biochem Biophys Res Commun 378: 836–841, 2009.
34. Sulaiman M, Matta MJ, Sunderesan NR, Gupta MP, Periasamy M, Gupta M. Resveratrol, an activator of SIRT1, upregulates sarcoplasmic calcium ATPase and improves cardiac function in diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 298: H833–H843, 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. Sundaresan NR, Samant SA, Pillai VB, Rajamohan SB, Gupta MP. SIRT3 is a stress-responsive deacetylase in cardiomyocytes that protects cells from stress-mediated cell death by deacetylation of Ku70. Mol Cell Biol 28: 6384–6401, 2008.
37. Um JH, Park SJ, Kang H, Yang S, Foretz M, McBurney MW, Kim MK, Viollet B, Chung JH. AMP-activated protein kinase-deficient mice are resistant to the metabolic effects of resveratrol. Diabetes 59: 554–563, 2010.
38. Weiss EP, Fontana L. Caloric restriction: powerful protection for the aging heart and vasculature. Am J Physiol Heart Circ Physiol 301: H1205–H1219, 2011.
39. Woessner JF Jr. Role of matrix proteases in processing enamel proteins. Connect Tissue Res 39: 69–73 and 141–149, 1998.
40. Wood JG, Rogina B, Lavu S, Howitz K, Helfand SL, Tatar M, Sinclair D. Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature 430: 686–689, 2004.
41. Yang M, Zheng J, Miao Y, Wang Y, Cui W, Guo J, Qiu S, Han Y, Jia L, Li H, Cheng J, Du J. Serum-glucocorticoid regulated kinase 1 regulates alternatively activated macrophage polarization contributing to angiotensin II-induced inflammation and cardiac fibrosis. Arterioscler Thromb Vasc Biol 32: 1675–1686, 2012.
42. Yang YC, Piek E, Zavadil J, Liang D, Xie D, Heyer J, Pavlidis P, Kucherlapati R, Roberts AB, Bottinger EP. Hierarchical model of gene regulation by transforming growth factor beta. Proc Natl Acad Sci USA 100: 10269–10274, 2003.
43. Zeglinski MR, Hnatowich M, Jassal DS, Dixon IM. SnoN as a novel negative regulator of TGF-β/Smad signaling: a target for tailoring organ fibrosis. Am J Physiol Heart Circ Physiol 308: H75–H82, 2015.