Staying young at heart: Autophagy and adaptation to cardiac aging

Journal of Molecular and Cellular Cardiology

Volumn 95, Issue , 2016, Pages 78-85

  Leon, Leonardo J ^a   Gustafsson, Åsa B ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Aging; Autophagy; Heart; Mitochondria

Indexed keywords

AUTOPHAGY PROTEIN 5; LIPOFUSCIN; MAMMALIAN TARGET OF RAPAMYCIN; MITOCHONDRIAL DNA; PARKIN; PROTEIN PINK1; PROTEIN SERINE THREONINE KINASE; RAPAMYCIN; REACTIVE OXYGEN METABOLITE; RESVERATROL; UNCLASSIFIED DRUG;

ADAPTATION; AGING; AUTOPHAGY; CALORIC RESTRICTION; CARDIOMYOPATHY; CARDIOVASCULAR DISEASE; DISEASE COURSE; EXERCISE; HEART; HOMEOSTASIS; HUMAN; LIFESTYLE MODIFICATION; LONGEVITY; LOSS OF FUNCTION MUTATION; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MITOPHAGY; MUSCLE CELL; NONHUMAN; PREMATURE AGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SELECTIVE AUTOPHAGY; STRESS; ANIMAL; CARDIAC MUSCLE; CELL AGING; GENE EXPRESSION REGULATION; METABOLISM; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADAPTATION, PHYSIOLOGICAL; AGING; ANIMALS; AUTOPHAGY; CELL AGING; GENE EXPRESSION REGULATION; HEART; HUMANS; MYOCARDIUM; OXIDATION-REDUCTION; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

EID: 84955297109     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.11.006     Document Type: Review

References (113)

1. Go A.S., Mozaffarian D., Roger V.L., Benjamin E.J., Berry J.D., Borden W.B., et al. Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation 2013, 127:e6-e245.
2. Terman A., Brunk U.T. Autophagy in cardiac myocyte homeostasis, aging, and pathology. Cardiovasc. Res. 2005, 68:355-365.
3. Yang Z., Klionsky D.J. Eaten alive: a history of macroautophagy. Nat. Cell Biol. 2010, 12:814-822.
4. Simonsen A., Cumming R.C., Brech A., Isakson P., Schubert D.R., Finley K.D. Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila. Autophagy 2008, 4:176-184.
5. Morselli E., Maiuri M.C., Markaki M., Megalou E., Pasparaki A., Palikaras K., et al. Caloric restriction and resveratrol promote longevity through the Sirtuin-1-dependent induction of autophagy. Cell Death Dis. 2010, 1.
6. Bjedov I., Toivonen J.M., Kerr F., Slack C., Jacobson J., Foley A., et al. Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster. Cell Metab. 2010, 11:35-46.
7. Han X., Turdi S., Hu N., Guo R., Zhang Y., Ren J. Influence of long-term caloric restriction on myocardial and cardiomyocyte contractile function and autophagy in mice. J. Nutri. Biochem. 2012, 23:1592-1599.
8. Eisenberg T., Knauer H., Schauer A., Buttner S., Ruckenstuhl C., Carmona-Gutierrez D., et al. Induction of autophagy by spermidine promotes longevity. Nat. Cell Biol. 2009, 11:1305-1314.
9. Pyo J.O., Yoo S.M., Ahn H.H., Nah J., Hong S.H., Kam T.I., et al. Overexpression of Atg5 in mice activates autophagy and extends lifespan. Nat. Commun. 2013, 4:2300.
10. Toth M.L., Sigmond T., Borsos E., Barna J., Erdelyi P., Takacs-Vellai K., et al. Longevity pathways converge on autophagy genes to regulate life span in Caenorhabditis elegans. Autophagy 2008, 4:330-338.
11. Kwon J., Han E., Bui C.B., Shin W., Lee J., Lee S., et al. Assurance of mitochondrial integrity and mammalian longevity by the p62-Keap1-Nrf2-Nqo1 cascade. EMBO Rep. 2012, 13:150-156.
12. Taneike M., Yamaguchi O., Nakai A., Hikoso S., Takeda T., Mizote I., et al. Inhibition of autophagy in the heart induces age-related cardiomyopathy. Autophagy 2010, 6:600-606.
13. Inoki K., Li Y., Zhu T., Wu J., Guan K.L. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 2002, 4:648-657.
14. Manning B.D., Tee A.R., Logsdon M.N., Blenis J., Cantley L.C. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol. Cell. 2002, 10:151-162.
15. Potter C.J., Pedraza L.G., Xu T. Akt regulates growth by directly phosphorylating Tsc2. Nat. Cell Biol. 2002, 4:658-665.
16. Vander Haar E., Lee S.I., Bandhakavi S., Griffin T.J., Kim D.H. Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40. Nat. Cell Biol. 2007, 9:316-323.
17. Wang L., Harris T.E., Roth R.A., Lawrence J.C. PRAS40 regulates mTORC1 kinase activity by functioning as a direct inhibitor of substrate binding. J. Biol. Chem. 2007, 282:20036-20044.
18. Kim J., Kundu M., Viollet B., Guan K.L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 2011, 13:132-141.
19. Yuan H.X., Russell R.C., Guan K.L. Regulation of PIK3C3/VPS34 complexes by MTOR in nutrient stress-induced autophagy. Autophagy 2013, 9:1983-1995.
20. Gwinn D.M., Shackelford D.B., Egan D.F., Mihaylova M.M., Mery A., Vasquez D.S., et al. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 2008, 30:214-226.
21. Inoki K., Zhu T., Guan K.L. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003, 115:577-590.
22. Kim J., Kim Y.C., Fang C., Russell R.C., Kim J.H., Fan W., et al. Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy. Cell 2013, 152:290-303.
23. Chan S.N., Tang B.L. Location and membrane sources for autophagosome formation - from ER-mitochondria contact sites to Golgi-endosome-derived carriers. Mol. Membr. Biol. 2013, 30:394-402.
24. Kang R., Zeh H.J., Lotze M.T., Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011, 18:571-580.
25. Mizushima N., Yoshimori T., Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 2011, 27:107-132.
26. Kabeya Y., Mizushima N., Yamamoto A., Oshitani-Okamoto S., Ohsumi Y., Yoshimori T. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J. Cell Sci. 2004, 117:2805-2812.
27. Pankiv S., Clausen T.H., Lamark T., Brech A., Bruun J.A., Outzen H., et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 2007, 282:24131-24145.
28. Hanna R.A., Quinsay M.N., Orogo A.M., Giang K., Rikka S., Gustafsson A.B. Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J. Biol. Chem. 2012, 287:19094-19104.
29. Narendra D., Tanaka A., Suen D.F., Youle R.J. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 2008, 183:795-803.
30. Iwata J., Ezaki J., Komatsu M., Yokota S., Ueno T., Tanida I., et al. Excess peroxisomes are degraded by autophagic machinery in mammals. J. Biol. Chem. 2006, 281:4035-4041.
31. Fujita N., Morita E., Itoh T., Tanaka A., Nakaoka M., Osada Y., et al. Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J. Cell Biol. 2013, 203:115-128.
32. Narendra D.P., Jin S.M., Tanaka A., Suen D.F., Gautier C.A., Shen J., et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010, 8.
33. Chen Y., Dorn G.W. PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science 2013, 340:471-475.
34. Koyano F., Okatsu K., Kosako H., Tamura Y., Go E., Kimura M., et al. Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature 2014, 510:162-166.
35. Kane L.A., Lazarou M., Fogel A.I., Li Y., Yamano K., Sarraf S.A., et al. PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J. Cell Biol. 2014, 205:143-153.
36. Kirkin V., Lamark T., Sou Y.S., Bjorkoy G., Nunn J.L., Bruun J.A., et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell 2009, 33:505-516.
37. Geisler S., Holmstrom K.M., Skujat D., Fiesel F.C., Rothfuss O.C., Kahle P.J., et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 2010, 12:119-131.
38. Lazarou M., Sliter D.A., Kane L.A., Sarraf S.A., Wang C., Burman J.L., et al. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature 2015, 524:309-314.
39. Narendra D., Kane L.A., Hauser D.N., Fearnley I.M., Youle R.J. p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy 2010, 6:1090-1106.
40. Wong Y.C., Holzbaur E.L. Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:E4439-E4448.
41. Novak I., Kirkin V., McEwan D.G., Zhang J., Wild P., Rozenknop A., et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010, 11:45-51.
42. Schwarten M., Mohrluder J., Ma P., Stoldt M., Thielmann Y., Stangler T., et al. Nix directly binds to GABARAP: a possible crosstalk between apoptosis and autophagy. Autophagy 2009, 5:690-698.
43. Chu C.T., Ji J., Dagda R.K., Jiang J.F., Tyurina Y.Y., Kapralov A.A., et al. Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells. Nat. Cell Biol. 2013, 15:1197-1205.
44. Liu L., Feng D., Chen G., Chen M., Zheng Q., Song P., et al. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat. Cell Biol. 2012, 14:177-185.
45. Murakawa T., Yamaguchi O., Hashimoto A., Hikoso S., Takeda T., Oka T., et al. Bcl-2-like protein 13 is a mammalian Atg32 homologue that mediates mitophagy and mitochondrial fragmentation. Nat. Commun. 2015, 6:7527.
46. Harrison D.E., Strong R., Sharp Z.D., Nelson J.F., Astle C.M., Flurkey K., et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 2009, 460:392-395.
47. Anisimov V.N., Zabezhinski M.A., Popovich I.G., Piskunova T.S., Semenchenko A.V., Tyndyk M.L., et al. Rapamycin increases lifespan and inhibits spontaneous tumorigenesis in inbred female mice. Cell Cycle 2011, 10:4230-4236.
48. Wu J.J., Liu J., Chen E.B., Wang J.J., Cao L., Narayan N., et al. Increased mammalian lifespan and a segmental and tissue-specific slowing of aging after genetic reduction of mTOR expression. Cell Rep. 2013, 4:913-920.
49. Hara T., Nakamura K., Matsui M., Yamamoto A., Nakahara Y., Suzuki-Migishima R., et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006, 441:885-889.
50. Komatsu M., Wang Q.J., Holstein G.R., Friedrich V.L., Iwata J., Kominami E., et al. Essential role for autophagy protein Atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:14489-14494.
51. Hsu H.C., Chen C.Y., Lee B.C., Chen M.F. High-fat diet induces cardiomyocyte apoptosis via the inhibition of autophagy. Eur. J. Nutr. 2015.
52. Wohlgemuth S.E., Julian D., Akin D.E., Fried J., Toscano K., Leeuwenburgh C., et al. Autophagy in the heart and liver during normal aging and calorie restriction. Rejuvenation Res. 2007, 10:281-292.
53. Shinmura K., Tamaki K., Sano M., Murata M., Yamakawa H., Ishida H., et al. Impact of long-term caloric restriction on cardiac senescence: caloric restriction ameliorates cardiac diastolic dysfunction associated with aging. J. Mol. Cell. Cardiol. 2011, 50:117-127.
54. Dai D.F., Karunadharma P.P., Chiao Y.A., Basisty N., Crispin D., Hsieh E.J., et al. Altered proteome turnover and remodeling by short-term caloric restriction or rapamycin rejuvenate the aging heart. Aging Cell 2014, 13:529-539.
55. Flynn J.M., O'Leary M.N., Zambataro C.A., Academia E.C., Presley M.P., Garrett B.J., et al. Late-life rapamycin treatment reverses age-related heart dysfunction. Aging Cell 2013, 12:851-862.
56. Bhuiyan M.S., Pattison J.S., Osinska H., James J., Gulick J., McLendon P.M., et al. Enhanced autophagy ameliorates cardiac proteinopathy. J. Clin. Invest. 2013, 123:5284-5297.
57. Yamaguchi O., Otsu K. Role of autophagy in aging. J. Cardiovasc. Pharmacol. 2012, 60:242-247.
58. Del Roso A., Vittorini S., Cavallini G., Donati A., Gori Z., Masini M., et al. Ageing-related changes in the in vivo function of rat liver macroautophagy and proteolysis. Exp. Gerontol. 2003, 38:519-527.
59. Uddin M.N., Nishio N., Ito S., Suzuki H., Isobe K. Autophagic activity in thymus and liver during aging. Age (Dordr.) 2012, 34:75-85.
60. Rubinsztein D.C., Marino G., Kroemer G. Autophagy and aging. Cell 2011, 146:682-695.
61. Cuervo A.M. Autophagy and aging: keeping that old broom working. Trends Genet. 2008, 24:604-612.
62. Russ D.W., Boyd I.M., KM M.C., KW M.C. Muscle-specificity of age-related changes in markers of autophagy and sphingolipid metabolism. Biogerontology 2015.
63. Lipinski M.M., Zheng B., Lu T., Yan Z., Py B.F., Ng A., et al. Genome-wide analysis reveals mechanisms modulating autophagy in normal brain aging and in Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:14164-14169.
64. Inuzuka Y., Okuda J., Kawashima T., Kato T., Niizuma S., Tamaki Y., et al. Suppression of phosphoinositide 3-kinase prevents cardiac aging in mice. Circulation 2009, 120:1695-1703.
65. Boyle A.J., Shih H., Hwang J., Ye J., Lee B., Zhang Y., et al. Cardiomyopathy of aging in the mammalian heart is characterized by myocardial hypertrophy, fibrosis and a predisposition towards cardiomyocyte apoptosis and autophagy. Exp. Gerontol. 2011, 46:549-559.
66. Zhou J., Freeman T.A., Ahmad F., Shang X., Mangano E., Gao E., et al. GSK-3alpha is a central regulator of age-related pathologies in mice. J. Clin. Invest. 2013, 123:1821-1832.
67. Johnson S.C., Rabinovitch P.S., Kaeberlein M. mTOR is a key modulator of ageing and age-related disease. Nature 2013, 493:338-345.
68. Sciarretta S., Zhai P., Shao D., Maejima Y., Robbins J., Volpe M., et al. Rheb is a critical regulator of autophagy during myocardial ischemia: pathophysiological implications in obesity and metabolic syndrome. Circulation 2012, 125:1134-1146.
69. Terman A., Brunk U.T. The aging myocardium: roles of mitochondrial damage and lysosomal degradation. Heart Lung Circ. 2005, 14:107-114.
70. Scherz-Shouval R., Shvets E., Fass E., Shorer H., Gil L., Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J. 2007, 26:1749-1760.
71. Song M., Chen Y., Gong G., Murphy E., Rabinovitch P.S., Dorn G.W. Super-suppression of mitochondrial reactive oxygen species signaling impairs compensatory autophagy in primary mitophagic cardiomyopathy. Circ. Res. 2014, 115:348-353.
72. Sciarretta S., Zhai P., Shao D., Zablocki D., Nagarajan N., Terada L.S., et al. Activation of NADPH oxidase 4 in the endoplasmic reticulum promotes cardiomyocyte autophagy and survival during energy stress through the protein kinase RNA-activated-like endoplasmic reticulum kinase/eukaryotic initiation factor 2alpha/activating transcription factor 4 pathway. Circ. Res. 2013, 113:1253-1264.
73. Kubli D.A., Ycaza J.E., Gustafsson A.B. Bnip3 mediates mitochondrial dysfunction and cell death through Bax and Bak. Biochem. J. 2007, 405:407-415.
74. Hoshino A., Mita Y., Okawa Y., Ariyoshi M., Iwai-Kanai E., Ueyama T., et al. Cytosolic p53 inhibits Parkin-mediated mitophagy and promotes mitochondrial dysfunction in the mouse heart. Nat. Commun. 2013, 4:2308.
75. Dai D.F., Santana L.F., Vermulst M., Tomazela D.M., Emond M.J., MacCoss M.J., et al. Overexpression of catalase targeted to mitochondria attenuates murine cardiac aging. Circulation 2009, 119:2789-2797.
76. Corral-Debrinski M., Horton T., Lott M.T., Shoffner J.M., Beal M.F., Wallace D.C. Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Nat. Genet. 1992, 2:324-329.
77. Wanagat J., Wolff M.R., Aiken J.M. Age-associated changes in function, structure and mitochondrial genetic and enzymatic abnormalities in the Fischer 344 × Brown Norway F(1) hybrid rat heart. J. Mol. Cell. Cardiol. 2002, 34:17-28.
78. Khaidakov M., Heflich R.H., Manjanatha M.G., Myers M.B., Aidoo A. Accumulation of point mutations in mitochondrial DNA of aging mice. Mutat. Res. 2003, 526:1-7.
79. Bratic A., Larsson N.G. The role of mitochondria in aging. J. Clin. Invest. 2013, 123:951-957.
80. Khrapko K., Bodyak N., Thilly W.G., van Orsouw N.J., Zhang X., Coller H.A., et al. Cell-by-cell scanning of whole mitochondrial genomes in aged human heart reveals a significant fraction of myocytes with clonally expanded deletions. Nucleic Acids Res. 1999, 27:2434-2441.
81. Kujoth G.C., Hiona A., Pugh T.D., Someya S., Panzer K., Wohlgemuth S.E., et al. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 2005, 309:481-484.
82. Trifunovic A., Wredenberg A., Falkenberg M., Spelbrink J.N., Rovio A.T., Bruder C.E., et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 2004, 429:417-423.
83. Dai D.F., Chen T., Wanagat J., Laflamme M., Marcinek D.J., Emond M.J., et al. Age-dependent cardiomyopathy in mitochondrial mutator mice is attenuated by overexpression of catalase targeted to mitochondria. Aging Cell 2010, 9:536-544.
84. Li-Harms X., Milasta S., Lynch J., Wright C., Joshi A., Iyengar R., et al. Mito-protective autophagy is impaired in erythroid cells of aged mtDNA-mutator mice. Blood 2015, 125:162-174.
85. Porta E.A. Advances in age pigment research. Arch. Gerontol. Geriatr. 1991, 12:303-320.
86. Jolly R.D., Douglas B.V., Davey P.M., Roiri J.E. Lipofuscin in bovine muscle and brain: a model for studying age pigment. Gerontology 1995, 41(Suppl. 2):283-295.
87. Brunk U.T., Terman A. Lipofuscin: mechanisms of age-related accumulation and influence on cell function. Free Radic. Biol. Med. 2002, 33:611-619.
88. Brunk U.T., Jones C.B., Sohal R.S. A novel hypothesis of lipofuscinogenesis and cellular aging based on interactions between oxidative stress and autophagocytosis. Mutat. Res. 1992, 275:395-403.
89. Brunk U.T., Terman A. The mitochondrial-lysosomal axis theory of aging: accumulation of damaged mitochondria as a result of imperfect autophagocytosis. Eur. J. Biochem./FEBS. 2002, 269:1996-2002.
90. He C., Bassik M.C., Moresi V., Sun K., Wei Y., Zou Z., et al. Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature 2012, 481:511-515.
91. Wilson M.G., Ellison G.M., Cable N.T. Basic science behind the cardiovascular benefits of exercise. Heart 2015, 101:758-765.
92. Giannuzzi P., Temporelli P.L., Corra U., Tavazzi L., Group E.-C.S. Antiremodeling effect of long-term exercise training in patients with stable chronic heart failure: results of the Exercise in Left Ventricular Dysfunction and Chronic Heart Failure (ELVD-CHF) Trial. Circulation 2003, 108:554-559.
93. Maloyan A., Gulick J., Glabe C.G., Kayed R., Robbins J. Exercise reverses preamyloid oligomer and prolongs survival in alphaB-crystallin-based desmin-related cardiomyopathy. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:5995-6000.
94. Fiuza-Luces C., Delmiro A., Soares-Miranda L., Gonzalez-Murillo A., Martinez-Palacios J., Ramirez M., et al. Exercise training can induce cardiac autophagy at end-stage chronic conditions: insights from a graft-versus-host-disease mouse model. Brain Behav. Immun. 2014, 39:56-60.
95. Colman R.J., Anderson R.M., Johnson S.C., Kastman E.K., Kosmatka K.J., Beasley T.M., et al. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 2009, 325:201-204.
96. Liao C.Y., Rikke B.A., Johnson T.E., Diaz V., Nelson J.F. Genetic variation in the murine lifespan response to dietary restriction: from life extension to life shortening. Aging Cell 2010, 9:92-95.
97. Schleit J., Johnson S.C., Bennett C.F., Simko M., Trongtham N., Castanza A., et al. Molecular mechanisms underlying genotype-dependent responses to dietary restriction. Aging Cell 2013, 12:1050-1061.
98. Kume S., Uzu T., Horiike K., Chin-Kanasaki M., Isshiki K., Araki S., et al. Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J. Clin. Invest. 2010, 120:1043-1055.
99. Howitz K.T., Bitterman K.J., Cohen H.Y., Lamming D.W., Lavu S., Wood J.G., et al. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 2003, 425:191-196.
100. Wood J.G., Rogina B., Lavu S., Howitz K., Helfand S.L., Tatar M., et al. Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature 2004, 430:686-689.
101. Pearson K.J., Baur J.A., Lewis K.N., Peshkin L., Price N.L., Labinskyy N., et al. Resveratrol delays age-related deterioration and mimics transcriptional aspects of dietary restriction without extending life span. Cell Metab. 2008, 8:157-168.
102. Baur J.A., Pearson K.J., Price N.L., Jamieson H.A., Lerin C., Kalra A., et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 2006, 444:337-342.
103. Gu X.S., Wang Z.B., Ye Z., Lei J.P., Li L., Su D.F., et al. Resveratrol, an activator of SIRT1, upregulates AMPK and improves cardiac function in heart failure. Genet. Mol. Res.: GMR 2014, 13:323-335.
104. Sung M.M., Das S.K., Levasseur J., Byrne N.J., Fung D., Kim T.T., et al. Resveratrol treatment of mice with pressure-overload-induced heart failure improves diastolic function and cardiac energy metabolism. Circ. Heart Fail. 2015, 8:128-137.
105. Danz E.D., Skramsted J., Henry N., Bennett J.A., Keller R.S. Resveratrol prevents doxorubicin cardiotoxicity through mitochondrial stabilization and the Sirt1 pathway. Free Radic. Biol. Med. 2009, 46:1589-1597.
106. Gurusamy N., Lekli I., Mukherjee S., Ray D., Ahsan M.K., Gherghiceanu M., et al. Cardioprotection by resveratrol: a novel mechanism via autophagy involving the mTORC2 pathway. Cardiovasc. Res. 2010, 86:103-112.
107. Baarine M., Thandapilly S.J., Louis X.L., Mazue F., Yu L., Delmas D., et al. Pro-apoptotic versus anti-apoptotic properties of dietary resveratrol on tumoral and normal cardiac cells. Genes Nutri. 2011, 6:161-169.
108. Wilkinson J.E., Burmeister L., Brooks S.V., Chan C.C., Friedline S., Harrison D.E., et al. Rapamycin slows aging in mice. Aging Cell 2012, 11:675-682.
109. Miller R.A., Harrison D.E., Astle C.M., Baur J.A., Boyd A.R., de Cabo R., et al. Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J. Gerontol. A Biol. Sci. Med. Sci. 2011, 66:191-201.
110. Anisimov V.N., Zabezhinski M.A., Popovich I.G., Piskunova T.S., Semenchenko A.V., Tyndyk M.L., et al. Rapamycin extends maximal lifespan in cancer-prone mice. Am. J. Pathol. 2010, 176:2092-2097.
111. Chang G.R., Wu Y.Y., Chiu Y.S., Chen W.Y., Liao J.W., Hsu H.M., et al. Long-term administration of rapamycin reduces adiposity, but impairs glucose tolerance in high-fat diet-fed KK/HlJ mice. Basic Clin. Pharmacol. Toxicol. 2009, 105:188-198.
112. Houde V.P., Brule S., Festuccia W.T., Blanchard P.G., Bellmann K., Deshaies Y., et al. Chronic rapamycin treatment causes glucose intolerance and hyperlipidemia by upregulating hepatic gluconeogenesis and impairing lipid deposition in adipose tissue. Diabetes 2010, 59:1338-1348.
113. Subramani S., Malhotra V. Non-autophagic roles of autophagy-related proteins. EMBO Rep. 2013, 14:143-151.