Upregulated autophagy protects cardiomyocytes from oxidative stress-induced toxicity

Autophagy

Volumn 9, Issue 3, 2013, Pages 328-344

  Dutta, Debapriya ^a,b   Xu, Jinze ^a   Kim, Jae Sung ^b   Dunn, William A ^a   Leeuwenburgh, Christiaan ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Autophagy; Cardiomyocytes; Mitochondrial Dysfunction; MTOR; Mtoroxidative Stress; Oxidative Stress; Rapamycin

Indexed keywords

ANTIMYCIN A1; CELL NUCLEUS DNA; RAPAMYCIN; SUPEROXIDE;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL DEATH; CELL PROTECTION; CELL RESPIRATION; CELL STRESS; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; HEART MUSCLE CELL; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MITOPHAGY; MOUSE; NONHUMAN; OXIDATION; OXIDATIVE STRESS;

EID: 84877342029     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.22971     Document Type: Article

References (77)

1. Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell 2005; 120:483-95; PMID:15734681; http://dx.doi.org/10.1016/j. cell.2005.02.001
2. Judge S, Jang YM, Smith A, Hagen T, Leeuwenburgh C. Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: Implications for the mitochondrial theory of aging. FASEB J 2005; 19:419-21; PMID:15642720
3. Grivennikova VG, Kareyeva AV, Vinogradov AD. What are the sources of hydrogen peroxide production by heart mitochondria? Biochim Biophys Acta 2010; 1797:939-44; PMID:20170624; http://dx.doi.org/10.1016/j.bbabio.2010.02.013
4. Starkov AA. The role of mitochondria in reactive oxygen species metabolism and signaling. Ann N Y Acad Sci 2008; 1147:37-52; PMID:19076429; http://dx.doi.org/10.1196/annals.1427.015
5. Brand MD. The sites and topology of mitochondrial superoxide production. Exp Gerontol 2010; 45:466-72; PMID:20064600; http://dx.doi.org/10.1016/j. exger.2010.01.003
6. Finkel T. Signal transduction by mitochondrial oxidants. J Biol Chem 2012; 287:4434-40; PMID:21832045; http://dx.doi.org/10.1074/jbc.R111.271999
7. Lin MT, Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006; 443:787-95; PMID:17051205; http://dx.doi.org/10.1038/nature05292
8. Judge S, Leeuwenburgh C. Cardiac mitochondrial bioenergetics, oxidative stress, and aging. Am J Physiol Cell Physiol 2007; 292:C1983-92; PMID:17344313; http://dx.doi.org/10.1152/ajpcell.00285.2006
9. Yakes FM, Van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci U S A 1997; 94:514-9; PMID:9012815; http://dx.doi.org/10.1073/pnas.94.2.514
10. Sohal RS, Ku HH, Agarwal S, Forster MJ, Lal H. Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction in the mouse. Mech Ageing Dev 1994; 74:121-33; PMID:7934203; http://dx.doi.org/10.1016/0047-6374(94)90104-X
11. Barja G, Herrero A. Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J 2000; 14:312-8; PMID:10657987
12. Abel ED, Doenst T. Mitochondrial adaptations to physiological vs. pathological cardiac hypertrophy. Cardiovasc Res 2011; 90:234-42; PMID:21257612; http://dx.doi.org/10.1093/cvr/cvr015
13. Lesnefsky EJ, Moghaddas S, Tandler B, Kerner J, Hoppel CL. Mitochondrial dysfunction in cardiac disease: Ischemia-reperfusion, aging, and heart failure. J Mol Cell Cardiol 2001; 33:1065-89; PMID:11444914; http://dx.doi.org/10.1006/ jmcc.2001.1378
14. Dai DF, Santana LF, Vermulst M, Tomazela DM, Emond MJ, MacCoss MJ, et al. Overexpression of catalase targeted to mitochondria attenuates murine cardiac aging. Circulation 2009; 119:2789-97; PMID:19451351; http://dx.doi.org/10.1161/ CIRCULATIONAHA.108.822403
15. Mizushima N, Levine B. Autophagy in mammalian development and differentiation. Nat Cell Biol 2010; 12:823-30; PMID:20811354; http://dx.doi.org/10.1038/ncb0910-823
16. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67-93; PMID:19653858; http://dx.doi.org/10. 1146/annurev-genet-102808-114910
17. Tait SW, Green DR. Mitochondria and cell death: Outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 2010; 11:621-32; PMID:20683470; http://dx.doi.org/10.1038/nrm2952
18. Cuervo AM, Bergamini E, Brunk UT, Dröge W, Ffrench M, Terman A. Autophagy and aging: The importance of maintaining "clean" cells. Autophagy 2005; 1:131-40; PMID:16874025; http://dx.doi.org/10.4161/auto.1.3.2017
19. 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; 26:1749-60; PMID:17347651; http://dx.doi.org/10. 1038/sj.emboj.7601623
20. Dewaele M, Maes H, Agostinis P. ROS-mediated mechanisms of autophagy stimulation and their relevance in cancer therapy. Autophagy 2010; 6:838-54; PMID:20505317; http://dx.doi.org/10.4161/auto.6.7.12113
21. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 2004; 36:585-95; PMID:15146184; http://dx.doi.org/10.1038/ng1362
22. Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 2009; 20:1992-2003; PMID:19225151; http://dx.doi.org/10.1091/mbc.E08-12-1249
23. Khan S, Salloum F, Das A, Xi L, Vetrovec GW, Kukreja RC. Rapamycin confers preconditioning-like protection against ischemia-reperfusion injury in isolated mouse heart and cardiomyocytes. J Mol Cell Cardiol 2006; 41:256-64; PMID:16769083; http://dx.doi.org/10.1016/j.yjmcc.2006.04.014
24. McMullen JR, Sherwood MC, Tarnavski O, Zhang L, Dorfman AL, Shioi T, et al. Inhibition of mTOR signaling with rapamycin regresses established cardiac hypertrophy induced by pressure overload. Circulation 2004; 109:3050-5; PMID:15184287; http://dx.doi.org/10.1161/01.CIR.0000130641.08705.45
25. Harada M, Hanada S, Toivola DM, Ghori N, Omary MB. Autophagy activation by rapamycin eliminates mouse Mallory-Denk bodies and blocks their proteasome inhibitor-mediated formation. Hepatology 2008; 47:2026-35; PMID:18454506; http://dx.doi.org/10.1002/hep.22294
26. Nakayama K, Okamoto F, Harada Y. Antimycin A: Isolation from a new Streptomyces and activity against rice plant blast fungi. J Antibiot (Tokyo) 1956; 9:63-6; PMID:13345726
27. Potter VR, Reif AE. Inhibition of an electron transport component by antimycin A. J Biol Chem 1952; 194:287-97; PMID:14927618
28. Pham NA, Robinson BH, Hedley DW. Simultaneous detection of mitochondrial respiratory chain activity and reactive oxygen in digitonin-permeabilized cells using flow cytometry. Cytometry 2000; 41:245-51; PMID:11084609; http://dx.doi.org/10.1002/1097-0320(20001201)41:4<245::AID-CYTO2>3.0. CO;2-#
29. Park WH, Han YW, Kim SH, Kim SZ. An ROS generator, antimycin A, inhibits the growth of HeLa cells via apoptosis. J Cell Biochem 2007; 102:98-109; PMID:17372917; http://dx.doi.org/10.1002/jcb.21280
30. Park WH, Han YW, Kim SW, Kim SH, Cho KW, Kim SZ. Antimycin A induces apoptosis in As4.1 juxtaglomerular cells. Cancer Lett 2007; 251:68-77; PMID:17189668; http://dx.doi.org/10.1016/j.canlet. 2006.11.002
31. Mukhopadhyay P, Rajesh M, Haskó G, Hawkins BJ, Madesh M, Pacher P. Simultaneous detection of apoptosis and mitochondrial superoxide production in live cells by flow cytometry and confocal microscopy. Nat Protoc 2007; 2:2295-301; PMID:17853886; http://dx.doi.org/10.1038/nprot.2007.327
32. Scaduto RC Jr., Grotyohann LW. Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys J 1999; 76:469-77; PMID:9876159; http://dx.doi.org/10.1016/S0006-3495(99)77214-0
33. Hofer T, Seo AY, Prudencio M, Leeuwenburgh C. A method to determine RNA and DNA oxidation simultaneously by HPLC-ECD: Greater RNA than DNA oxidation in rat liver after doxorubicin administration. Biol Chem 2006; 387:103-11; PMID:16497170; http://dx.doi.org/10.1515/BC.2006.014
34. Chen Y, Azad MB, Gibson SB. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ 2009; 16:1040-52; PMID:19407826; http://dx.doi.org/10.1038/cdd.2009.49
35. Hamacher-Brady A, Brady NR, Gottlieb RA. Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. J Biol Chem 2006; 281:29776-87; PMID:16882669; http://dx.doi.org/10.1074/jbc.M603783200
36. Yuan H, Perry CN, Huang C, Iwai-Kanai E, Carreira RS, Glembotski CC, et al. LPS-induced autophagy is mediated by oxidative signaling in cardiomyocytes and is associated with cytoprotection. Am J Physiol Heart Circ Physiol 2009; 296:H470-9; PMID:19098111; http://dx.doi.org/10.1152/ajpheart.01051.2008
37. Su H, Wang X. Autophagy and p62 in cardiac protein quality control. Autophagy 2011; 7:1382-3; PMID:21997373; http://dx.doi.org/10.4161/auto.7.11. 17339
38. Bjørkøy G, Lamark T, Pankiv S, Øvervatn A, Brech A, Johansen T. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 2009; 452:181-97; PMID:19200883; http://dx.doi.org/10.1016/S0076-6879(08)03612-4
39. Larsen KB, Lamark T, Øvervatn A, Harneshaug I, Johansen T, Bjørkøy G. A reporter cell system to monitor autophagy based on p62/SQSTM1. Autophagy 2010; 6:784-93; PMID:20574168; http://dx.doi.org/10.4161/ auto.6.6.12510
40. Henics T, Wheatley DN. Cytoplasmic vacuolation, adaptation and cell death: A view on new perspectives and features. Biol Cell 1999; 91:485-98; PMID:10572624; http://dx.doi.org/10.1016/S0248-4900(00)88205-2
41. Shang F, Taylor A. Ubiquitin-proteasome pathway and cellular responses to oxidative stress. Free Radic Biol Med 2011; 51:5-16; PMID:21530648; http://dx.doi.org/10.1016/j.freeradbiomed.2011.03.031
42. Dudek EJ, Shang F, Valverde P, Liu Q, Hobbs M, Taylor A. Selectivity of the ubiquitin pathway for oxidatively modified proteins: Relevance to protein precipitation diseases. FASEB J 2005; 19:1707-9; PMID:16099947
43. Gnaiger E. Polarographic oxygen sensors, the oxygraph, and high-resolution respirometry to assess mitochondrial function. In: Dykens; JA, Will; Y e, eds. Drug-Induced Mitochondrial Dysfunction. Hoboken, NJ, USA: John Wiley & Sons, Inc, 2008
44. Seglen PO, Gordon PB. 3-Methyladenine: Specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci U S A 1982; 79:1889-92; PMID:6952238; http://dx.doi.org/10.1073/pnas. 79.6.1889
45. Stroikin Y, Dalen H, Lööf S, Terman A. Inhibition of autophagy with 3-methyladenine results in impaired turnover of lysosomes and accumulation of lipofuscin-like material. Eur J Cell Biol 2004; 83:583-90; PMID:15679103; http://dx.doi.org/10.1078/0171-9335-00433
46. Sohal RS, Sohal BH. Hydrogen peroxide release by mitochondria increases during aging. Mech Ageing Dev 1991; 57:187-202; PMID:1904965; http://dx.doi.org/10.1016/0047-6374(91)90034-W
47. Ide T, Tsutsui H, Kinugawa S, Utsumi H, Kang D, Hattori N, et al. Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circ Res 1999; 85:357-63; PMID:10455064; http://dx.doi.org/10.1161/01. RES.85.4.357
48. Hüttemann M, Lee I, Pecinova A, Pecina P, Przyklenk K, Doan JW. Regulation of oxidative phosphorylation, the mitochondrial membrane potential, and their role in human disease. J Bioenerg Biomembr 2008; 40:445-56; PMID:18843528; http://dx.doi.org/10.1007/s10863-008-9169-3
49. Vayssier-Taussat M, Kreps SE, Adrie C, Dall'Ava J, Christiani D, Polla BS. Mitochondrial membrane potential: A novel biomarker of oxidative environmental stress. Environ Health Perspect 2002; 110:301-5; PMID:11882482; http://dx.doi.org/10.1289/ehp.02110301
50. Andreyev AY, Kushnareva YE, Starkov AA. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc) 2005; 70:200-14; PMID:15807660; http://dx.doi.org/10.1007/s10541-005-0102-7
51. Kuchino Y, Mori F, Kasai H, Inoue H, Iwai S, Miura K, et al. Misreading of DNA templates containing 8-hydroxydeoxyguanosine at the modified base and at adjacent residues. Nature 1987; 327:77-9; PMID:3574469; http://dx.doi.org/10. 1038/327077a0
52. Cheng KC, Cahill DS, Kasai H, Nishimura S, Loeb LA. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G-T and A-C substitutions. J Biol Chem 1992; 267:166-72; PMID:1730583
53. Lin HS, Jenner AM, Ong CN, Huang SH, Whiteman M, Halliwell B. A high-throughput and sensitive methodology for the quantification of urinary 8-hydroxy-2-deoxyguanosine: Measurement with gas chromatography-mass spectrometry after single solid-phase extraction. Biochem J 2004; 380:541-8; PMID:14992687; http://dx.doi.org/10.1042/BJ20040004
54. Gedik CM, Collins A; ESCODD (European Standards Committee on Oxidative DNA Damage). Establishing the background level of base oxidation in human lymphocyte DNA: Results of an interlaboratory validation study. FASEB J 2005; 19:82-4; PMID:15533950
55. Sachs HG, Colgan JA, Lazarus ML. Ultrastructure of the aging myocardium: A morphometric approach. Am J Anat 1977; 150:63-71; PMID:930852; http://dx.doi.org/10.1002/aja.1001500105
56. Bova MP, Tam D, McMahon G, Mattson MN. Troglitazone induces a rapid drop of mitochondrial membrane potential in liver HepG2 cells. Toxicol Lett 2005; 155:41-50; PMID:15585358; http://dx.doi.org/10.1016/j.toxlet.2004.08.009
57. Masubuchi Y, Kano S, Horie T. Mitochondrial permeability transition as a potential determinant of hepatotoxicity of antidiabetic thiazolidinediones. Toxicology 2006; 222:233-9; PMID:16621215; http://dx.doi.org/10.1016/j.tox.2006. 02.017
58. Kaufmann P, Török M, Zahno A, Waldhauser KM, Brecht K, Krähenbühl S. Toxicity of statins on rat skeletal muscle mitochondria. Cell Mol Life Sci 2006; 63:2415-25; PMID:17013560; http://dx.doi.org/10.1007/ s00018-006-6235-z
59. Bjelakovic G, Nikolova D, Gluud LL, Simonetti RG, Gluud C. Mortality in randomized trials of antioxidant supplements for primary and secondary prevention: Systematic review and meta-analysis. JAMA 2007; 297:842-57; PMID:17327526; http://dx.doi.org/10.1001/jama.297.8.842
60. Levonen AL, Vähäkangas E, Koponen JK, Ylä-Herttuala S. Antioxidant gene therapy for cardiovascular disease: Current status and future perspectives. Circulation 2008; 117:2142-50; PMID:18427144; http://dx.doi.org/ 10.1161/CIRCULATIONAHA.107.718585
61. Tinkel J, Hassanain H, Khouri SJ. Cardiovascular antioxidant therapy: A review of supplements, pharmacotherapies, and mechanisms. Cardiol Rev 2012; 20:77-83; PMID:22293859
62. Kiffin R, Bandyopadhyay U, Cuervo AM. Oxidative stress and autophagy. Antioxid Redox Signal 2006; 8:152-62; PMID:16487049; http://dx.doi.org/10.1089/ ars.2006.8.152
63. Mendl N, Occhipinti A, Müller M, Wild P, Dikic I, Reichert AS. Mitophagy in yeast is independent of mitochondrial fission and requires the stress response gene WHI2. J Cell Sci 2011; 124:1339-50; PMID:21429936; http://dx.doi.org/10.1242/jcs.076406
64. Ma X, Jin M, Cai Y, Xia H, Long K, Liu J, et al. Mitochondrial electron transport chain complex III is required for antimycin A to inhibit autophagy. Chem Biol 2011; 18:1474-81; PMID:22118681; http://dx.doi.org/10.1016/j.chembiol. 2011.08.009
65. Pan T, Rawal P, Wu Y, Xie W, Jankovic J, Le W. Rapamycin protects against rotenone-induced apoptosis through autophagy induction. Neuroscience 2009; 164:541-51; PMID:19682553; http://dx.doi.org/10.1016/j.neuroscience.2009.08.014
66. Ravikumar B, Berger Z, Vacher C, O'Kane CJ, Rubinsztein DC. Rapamycin pre-treatment protects against apoptosis. Hum Mol Genet 2006; 15:1209-16; PMID:16497721; http://dx.doi.org/10.1093/hmg/ddl036
67. Gershon H, Gershon D. Detection of inactive enzyme molecules in ageing organisms. Nature 1970; 227:1214-7; PMID:5212575; http://dx.doi.org/10.1038/ 2271214a0
68. Miquel J, Tappel AL, Dillard CJ, Herman MM, Bensch KG. Fluorescent products and lysosomal components in aging Drosophila melanogaster. J Gerontol 1974; 29:622-37; PMID:4214300; http://dx.doi.org/10.1093/geronj/29.6.622
69. Iwai K, Drake SK, Wehr NB, Weissman AM, LaVaute T, Minato N, et al. Iron-dependent oxidation, ubiquitination, and degradation of iron regulatory protein 2: Implications for degradation of oxidized proteins. Proc Natl Acad Sci U S A 1998; 95:4924-8; PMID:9560204; http://dx.doi.org/10.1073/pnas.95.9.4924
70. Webb JL, Ravikumar B, Atkins J, Skepper JN, Rubinsztein DC. Alpha-Synuclein is degraded by both autophagy and the proteasome. J Biol Chem 2003; 278:25009-13; PMID:12719433; http://dx.doi.org/10.1074/jbc.M300227200
71. Dosenko VE, Nagibin VS, Tumanovska LV, Moibenko AA. Protective effect of autophagy in anoxia-reoxygenation of isolated cardiomyocyte? Autophagy 2006; 2:305-6; PMID:16874046
72. Cohen MV, Downey JM. Adenosine: Trigger and mediator of cardioprotection. Basic Res Cardiol 2008; 103:203-15; PMID:17999026; http://dx.doi.org/10.1007/ s00395-007-0687-7
73. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, et al. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med 2007; 13:619-24; PMID:17450150; http://dx.doi.org/ 10.1038/nm1574
74. Kitsis RN, Peng CF, Cuervo AM. Eat your heart out. Nat Med 2007; 13:539-41; PMID:17479097; http://dx.doi.org/10.1038/nm0507-539
75. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19:5720-8; PMID:11060023; http://dx.doi.org/10.1093/emboj/19.21.5720
76. Kuma A, Matsui M, Mizushima N. LC3, an autophagosome marker, can be incorporated into protein aggregates independent of autophagy: Caution in the interpretation of LC3 localization. Autophagy 2007; 3:323-8; PMID:17387262
77. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248-54; PMID:942051; http://dx.doi.org/10.1016/0003- 2697(76)90527-3