Resveratrol reverses remodeling in hearts with large, old myocardial infarctions through enhanced autophagy-activating AMP kinase pathway

American Journal of Pathology

Volumn 182, Issue 3, 2013, Pages 701-713

  Kanamori, Hiromitsu ^a   Takemura, Genzou ^a   Goto, Kazuko ^a   Tsujimoto, Akiko ^a   Ogino, Atsushi ^a   Takeyama, Toshiaki ^a   Kawaguchi, Tomonori ^a   Watanabe, Takatomo ^a   Morishita, Kentaro ^a   Kawasaki, Masanori ^a   Mikami, Atsushi ^a   Fujiwara, Takako ^b   Fujiwara, Hisayoshi ^c   Seishima, Mitsuru ^a   Minatoguchi, Shinya ^a  

^a GIFU UNIVERSITY   (Japan)

^b KYOTO WOMEN'S UNIVERSITY   (Japan)

^c HYOGO PREFECTURAL AMAGASAKI GENERAL MEDICAL CENTER   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; CHLOROQUINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MANGANESE SUPEROXIDE DISMUTASE; MICROTUBULE ASSOCIATED PROTEIN 1; RESVERATROL; S6 KINASE; SILENT INFORMATION REGULATOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY LIGATION; ARTICLE; AUTOPHAGY; CELL VACUOLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HEART; HEART FAILURE; HEART FUNCTION; HEART INFARCTION; HEART MUSCLE CELL; IN VITRO STUDY; LEFT CORONARY ARTERY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TREATMENT DURATION; UPREGULATION;

ADENOSINE TRIPHOSPHATE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; AUTOPHAGY; CELLS, CULTURED; DENSITOMETRY; ENERGY METABOLISM; HEART FAILURE; HEART FUNCTION TESTS; MALE; MICE; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; SIRTUIN 1; STILBENES; SUPEROXIDE DISMUTASE; TOR SERINE-THREONINE KINASES; VACUOLES; VENTRICULAR REMODELING;

EID: 84874523611     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.11.009     Document Type: Article

References (45)

1. M.A. Pfefer Left ventricular remodeling after acute infarction Annu Rev Med 46 1995 455 456
2. K.A. Reimer, R.S. Vander Heide, and V.J. Richard Reperfusion in acute myocardial infarction: effect of timing and modulating factors in experimental models Am J Cardiol 72 1993 13G 21G
3. K. Shan, K. Kurrelmeyer, Y. Seta, F. Wang, Z. Dibbs, A. Deswal, D. Lee-Jackson, and D.L. Mann The role of cytokines in disease progression in heart failure Curr Opin Cardiol 12 1997 218 223
4. H.F. Weisman, D.E. Bush, J.A. Mannisi, M.L. Weisfeldt, and B. Healy Cellular mechanisms of myocardial infarct expansion Circulation 78 1988 186 201
5. M.W. Knaapen, M.J. Davies, M. De Bie, A.J. Haven, W. Martinet, and M.M. Kockx Apoptotic versus autophagic cell death in heart failure Cardiovasc Res 51 2001 304 312
6. H. Shimomura, F. Terasaki, T. Hayashi, Y. Kitaura, T. Isomura, and H. Suma Autophagic degeneration as a possible mechanism of myocardial cell death in dilated cardiomyopathy Jpn Circ J 65 2001 965 968
7. G. Takemura, S. Miyata, Y. Kawase, H. Okada, R. Maruyama, and H. Fujiwara Autophagic degeneration and death of cardiomyocytes in heart failure Autophagy 2 2006 212 214
8. S. Hein, E. Arnon, S. Kostin, M. Schönburg, A. Elsässer, V. Polyakova, E.P. Bauer, W.P. Klövekorn, and J. Schaper Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: structural deterioration and compensatory mechanisms Circulation 107 2003 984 991
9. A. Nakai, O. Yamaguchi, T. Takeda, Y. Higuchi, S. Hikoso, M. Taniike, S. Omiya, I. Mizote, Y. Matsumura, M. Asahi, K. Nishida, M. Hori, N. Mizushima, and K. Otsu The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress Nat Med 13 2007 619 624
10. L. Yan, D.E. Vatner, S.J. Kim, H. Ge, M. Masurekar, W.H. Massover, G. Yang, Y. Matsui, J. Sadoshima, and S.F. Vatner Autophagy in chronically ischemic myocardium Proc Natl Acad Sci U S A 102 2005 13807 13812
11. K. Shinmura, K. Tamaki, M. Sano, M. Murata, H. Yamakawa, H. Ishida, and K. Fukuda Impact of long-term caloric restriction on cardiac senescence: caloric restriction ameliorates cardiac diastolic dysfunction associated with aging J Mol Cell Cardiol 50 2011 117 127
12. H. Kanamori, G. Takemura, K. Goto, R. Maruyama, A. Tsujimoto, A. Ogino, T. Takeyama, T. Kawaguchi, T. Watanabe, T. Fujiwara, H. Fujiwara, M. Seishima, and S. Minatoguchi The role of autophagy emerging in post infarction cardiac remodeling Cardiovasc Res 91 2011 330 339
13. J.A. Baur, and D.A. Sinclair Therapeutic potential of resveratrol: the in vivo evidence Nat Rev Drug Discov 5 2006 493 506
14. F. Brisdelli, G. D'Andrea, and A. Bozzi Resveratrol: a natural polyphenol with multiple chemopreventive properties Curr Drug Metab 10 2009 530 546
15. E. Morselli, G. Mariño, M.V. Bennetzen, T. Eisenberg, E. Megalou, S. Schroeder, S. Cabrera, P. Bénit, P. Rustin, A. Criollo, O. Kepp, L. Galluzzi, S. Shen, S.A. Malik, M.C. Maiuri, Y. Horio, C. López- Otín, J.S. Andersen, N. Tavernarakis, F. Madeo, and G. Kroemer Spermidine and resveratrol induce autophagy by distinct pathways converging on the acetylproteome J Cell Biol 192 2011 615 629
16. V.W. Dolinsky, and J.R. Dyck Calorie restriction and resveratrol in cardiovascular health and disease Biochim Biophys Acta 1812 2011 1477 1489
17. E. Iwai-Kanai, H. Yuan, C. Huang, M.R. Sayen, C.N. Perry-Garza, L. Kim, and R.A. Gottlieb A method to measure cardiac autophagic flux in vivo Autophagy 4 2008 322 329
18. H. Kanamori, G. Takemura, R. Maruyama, K. Goto, A. Tsujimoto, A. Ogino, L. Li, I. Kawamura, T. Takeyama, T. Kawaguchi, K. Nagashima, T. Fujiwara, H. Fujiwara, M. Seishima, and S. Minatiguchi Functional significance and morphological characterization of starvation-induced autophagy in the adult heart Am J Pathol 174 2009 1705 1714
19. L. Wang, Z.P. Feng, C.S. Kondo, R.S. Sheldon, and H.J. Duff Developmental changes in the delayed rectifier K+ channels in mouse heart Circ Res 79 1996 79 85
20. M. Lee, J.T. Hwang, H.J. Lee, S.N. Jung, I. Kang, S.G. Chi, S.S. Kim, and J. Ha AMP-activated protein kinase activity is critical for hypoxia-inducible factor-1 transcriptional activity and its target gene expression under hypoxic conditions in DU145 cells J Biol Chem 278 2003 3965-3961
21. Y. Kabeya, N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi, and T. Yoshimori LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing EMBO J 19 2000 5720 5728
22. M. Komatsu, S. Waguri, M. Koike, Y.S. Sou, T. Ueno, T. Hara, N. Mizushima, J. Iwata, J. Ezaki, S. Murata, J. Hamazaki, Y. Nishito, S. Iemura, T. Natume, T. Yanagawa, J. Uwayama, E. Warabi, H. Yoshida, T. Ishii, A. Kobayashi, M. Yamamoto, Z. Yue, Y. Uchiyama, E. Kominami, and K. Tanaka Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice Cell 131 2007 1149 1163
23. S. Kovacic, C.L. Soltys, A.J. Barr, I. Shiojima, K. Walsh, and J.R. Dyck Akt activity negatively regulates phosphorylation of AMP-activated protein kinase in the heart J Biol Chem 278 2003 39422 39427
24. A.Y. Chan, V.W. Dolinsky, C.L. Soltys, B. Viollet, S. Baksh, P.E. Light, and J.R. Dyck Resveratrol inhibits cardiac hypertrophy via AMP-activated protein kinase and Akt J Biol Chem 283 2008 24194 24201
25. A. Vaquero, M. Scher, D. Lee, H. Erdjument-Bromage, P. Tempst, and D. Reinberg Human Sirt1 interacts with histone H1 and promotes formation of facultative heterochromatin Mol Cell 16 2004 93 105
26. P. Boya, R.A. Gonzalez-Polo, N. Casares, J.L. Perfettini, P. Dessen, N. Larochette, D. Métivier, D. Meley, S. Souquere, T. Yoshimori, G. Pierron, P. Codogno, and G. Kroemer Inhibition of macroautophagy triggers apoptosis Mol Cell Biol 25 2005 1025 1040
27. H. Kanamori, G. Takemura, K. Goto, R. Maruyama, Ono, K. Nagano, A. Tsujimoto, A. Ogino, T. Takeyama, T. Kawaguchi, T. Watanabe, M. Kawasaki, T. Fujiwara, H. Fujiwara, M. Seishima, and S. MInatoguchi Autophagy limits acute myocardial infarction induced by permanent coronary occlusion Am J Physiol Heart Circ Physiol 300 2011 H2261 H2271
28. K. Inoki, T. Zhu, and K.L. Guan TSC2 mediates cellular energy response to control cell growth and survival Cell 115 2003 577 590
29. H.R. Samari, and P.O. Seglen Inhibition of hepatocytic autophagy by adenosine, aminoimidazole-4-carboxamide riboside, and N6-mercaptopurine riboside. Evidence for involvement of AMP-activated protein kinase J Biol Chem 273 1998 23758 23763
30. Y. Ikeda, K. Sato, D.R. Pimentel, F. Sam, R.J. Shaw, J.R. Dyck, and K. Walsh Cardiac-specific deletion of LKB1 leads to hypertrophy and dysfunction J Biol Chem 284 2009 35839 35849
31. V.W. Dolinsky, A.Y. Chan, I. Robillard Frayne, P.E. Light, C. Des Rosiers, and J.R. Dyck Resveratrol prevents the prohypertrophic effects of oxidative stress on LKB-1 Circulation 119 2009 1643 1652
32. J.A. Baur, K.J. Pearson, N.L. Price, H.A. Jamieson, C. Lerin, A. Kalra, V.V. Prabhu, J.S. Allard, G. Lopez-Lluch, K. Lewis, P.J. Pistell, S. Poosala, K.G. Becker, O. Boss, D. Gwinn, M. Wang, S. Ramaswamy, K.W. Fishbein, R.G. Spencer, E.G. Lakatta, D. Le Couteur, R.J. Shaw, P. Navas, P. Puigserver, D.K. Ingram, R. de Cabo, and D.A. Sinclair Resveratrol improves health and survival of mice on a high-calorie diet Nature 444 2006 337 342
33. J.H. Um, S.J. Park, H. Kang, S. Yang, M. Foretz, M.W. McBurney, M.K. Kim, B. Viollet, and J.H. Chung AMP-activated protein kinase-deficient mice are resistant to the metabolic effects of resveratrol Diabetes 59 2010 554 563
34. R.J. Shaw LKB1 and AMP-activated protein kinase control of mTOR signaling and growth Acta Physiol (Oxf) 196 2009 65 80
35. S.J. Buss, S. Muenz, J.H. Riffel, P. Malekar, M. Hagenmueller, C.S. Weiss, F. Bea, R. Bekeredjian, M. Schinke-Braun, S. Izumo, H.A. Katus, and S.E. Hardt Beneficial effects of Mammalian target of rapamycin inhibition on left ventricular remodeling after myocardial infarction J Am Coll Cardiol 54 2009 2435 2446
36. M. Tanno, A. Kuno, T. Yano, T. Miura, S. Hisahara, S. Ishikawa, K. Shimamoto, and Y. Horio Induction of manganese superoxide dismutase by nuclear translocation and activation of SIRT1 promotes cell survival in chronic heart failure J Biol Chem 285 2010 8375 8382
37. S.M. Nadtochiy, H. Yao, M.W. McBurney, W. Gu, L. Guarente, I. Raham, and P.S. Brookes SIRT1-mediated acute cardioprotection Am J Physiol Heart Circ Physiol 301 2011 H1506 H1512
38. T. Kawashima, Y. Inuzuka, J. Okuda, T. Kato, S. Niizuma, Y. Tamaki, Y. Iwanaga, A. Kawamoto, M. Narazaki, T. Matsuda, S. Adachi, G. Takemura, T. Kita, T. Kimura, and T. Shioi Constitutive SIRT1 overexpression impairs mitochondria and reduces cardiac function in mice J Mol Cell Cardiol 51 2011 1026 1036
39. A. Baldi, A. Abbate, R. Bussani, G. Patti, R. Melfi, Angelini, A. Dobrina, R. Rossiello, F. Silvestri, F. Baldi, and G. Di Sciascio Apoptosis and post-infarction left ventricular remodeling J Mol Cell Cardiol 34 2002 165 174
40. K.C. Wollert, J. Heineke, J. Westermann, M. Ludde, B. Fiedler, W. Zierhut, D. Laurent, M.K. Bauer, K. Schulze-Osthoff, and H. Drexler The cardiac Fas (APO-1/CD95) Receptor/Fas ligand system: relation to diastolic wall stress in volume-overload hypertrophy in vivo and activation of the transcription factor AP-1 in cardiac myocytes Circulation 101 2000 1172 1178
41. K. Hayakawa, G. Takemura, M. Koda, Y. Kawase, R. Maruyama, Y. Li, S. Minatoguchi, T. Fujiwara, and H. Fujiwara Sensitivity to apoptosis signal, clearance rate, and ultrastructure of Fas ligand-induced apoptosis in in vivo adult cardiac cells Circulation 105 2002 3039 3045
42. A. Kawai, H. Uchiyama, S. Takano, N. Nakamura, and S. Ohkuma Autophagosome-lysosome fusion depends on the pH in acidic compartments in CHO cells Autophagy 3 2007 154 157
43. A. Yamamoto, Y. Tagawa, T. Yoshimori, Y. Moriyama, R. Masaki, and Y. Tashiro Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line H-4-II-E cells Cell Struct Funct 23 1998 33 42
44. C. Centeno-Baez, P. Dallaire, and A. Marette Resveratrol inhibition of inducible nitric oxide synthase in skeletal muscle involves AMPK but not SIRT1 Am J Physiol Endocrinol Metab 301 2011 E922 E930
45. Y. Nishida, S. Arakawa, K. Fujitani, H. Yamaguchi, T. Mizuta, T. Kanaseki, M. Komatsu, K. Otsu, Y. Tsujimoto, and S. Shimizu Discovery of Atg5/Atg7-independent alternative macroautophagy Nature 461 2009 654 658