Autophagy in health and disease. 5. Mitophagy as a way of life

American Journal of Physiology - Cell Physiology

Volumn 299, Issue 2, 2010, Pages

  Gottlieb, Roberta A ^a   Carreira, Raquel S ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

Cardioprotection; Ischemia reperfusion; Mitochondria

Indexed keywords

APOPTOSIS INDUCING FACTOR; BNIP3 LIKE PROTEIN; CYCLOPHILIN D; DNA DIRECTED DNA POLYMERASE GAMMA; FREE RADICAL; GREEN FLUORESCENT PROTEIN; HYDROGEN PEROXIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MITOCHONDRIAL DNA; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MITOCHONDRIAL TRANSCRIPTION FACTOR A; OUTER MEMBRANE PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEASOME; PROTEIN; PROTEIN BCL 2; PROTEIN BNIP3; REACTIVE OXYGEN METABOLITE; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SIRTUIN 1; TRANSCRIPTION FACTOR FKHR; UBIQUITIN; UNCLASSIFIED DRUG; UTH1 PROTEIN;

AGING; AMYOTROPHIC LATERAL SCLEROSIS; AUTOPHAGOSOME; AUTOPHAGY; BIOGENESIS; BRAIN; CALCIUM HOMEOSTASIS; CALORIC RESTRICTION; CELL DEATH; DNA DAMAGE; DNA REPAIR; ELECTRON MICROSCOPY; HEART; HEART MUSCLE CELL; HEART PROTECTION; HUMAN; IMMUNE SYSTEM; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; ISCHEMIA; KIDNEY PROXIMAL TUBULE; LONGEVITY; MEMORY T LYMPHOCYTE; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION; MITOPHAGY; NERVE CELL; OXIDATION; OXIDATIVE STRESS; PHAGOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION; TURNOVER TIME; ANIMAL; DEGENERATIVE DISEASE; HEALTH STATUS; HEART FAILURE; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; AUTOPHAGY; HEALTH STATUS; HEART FAILURE; HUMANS; MITOCHONDRIA; NEOPLASMS; NEURODEGENERATIVE DISEASES; SIGNAL TRANSDUCTION;

EID: 77955861146     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00097.2010     Document Type: Review

References (112)

1. Beau I, Esclatine A, Codogno P. Lost to translation: when autophagy targets mature ribosomes. Trends Cell Biol 18: 311-314, 2008.
2. Bernardi P. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev 79: 1127-1155, 1999.
3. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Metivier D, Meley D, Souquere S, Yoshimori T, Pierron G, Codogno P, Kroemer G. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25: 1025-1040, 2005.
4. Brady NR, Hamacher-Brady A, Westerhoff HV, Gottlieb RA. A wave of reactive oxygen species (ROS)-induced ROS release in a sea of excitable mitochondria. Antioxid Redox Signal 8: 1651-1665, 2006.
5. Brady NR, Hamacher-Brady A, Yuan H, Gottlieb RA. The autophagic response to nutrient deprivation in the HL-1 cardiac myocyte is modulated by Bcl-2 and sarco/endoplasmic reticulum calcium stores. FEBS J 274: 3184-3197, 2007.
6. Brunk UT, Terman A. The mitochondrial-lysosomal axis theory of aging: accumulation of damaged mitochondria as a result of imperfect autophagocytosis. Eur J Biochem 269: 1996-2002, 2002.
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.
8. Carreira RS, Lee Y, Ghochani M, Gustafsson AB, Gottlieb RA. Cyclophilin D is required for mitochondrial removal by autophagy in cardiac cells. Autophagy 6: 462-472, 2010.
9. Chan DC. Mitochondria: dynamic organelles in disease, aging, and development. Cell 125: 1241-1252, 2006.
10. Chen Y, Azad MB, Gibson SB. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ 16: 1040-1052, 2009.
11. Cherra SJ, Chu CT. Autophagy in neuroprotection and neurodegeneration: a question of balance. Future Neurol 3: 309-323, 2008.
12. Civitarese AE, Carling S, Heilbronn LK, Hulver MH, Ukropcova B, Deutsch WA, Smith SR, Ravussin E. Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med 4: e76, 2007.
13. Clark SL Jr. Cellular differentiation in the kidneys of newborn mice studies with the electron microscope. J Biophys Biochem Cytol 3: 349-362, 1957.
14. Coleman R, Silbermann M, Gershon D, Reznick AZ. Giant mitochondria in the myocardium of aging and endurance-trained mice. Gerontology 33: 34-39, 1987.
15. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J 341: 233-249, 1999.
16. Crouser ED, Julian MW, Huff JE, Struck J, Cook CH. Carbamoyl phosphate synthase-1: a marker of mitochondrial damage and depletion in the liver during sepsis. Crit Care Med 34: 2439-2446, 2006.
17. De Grey AD. A proposed refinement of the mitochondrial free radical theory of aging. Bioessays 19: 161-166, 1997.
18. De Grey AD. The reductive hotspot hypothesis of mammalian aging: membrane metabolism magnifies mutant mitochondrial mischief. Eur J Biochem 269: 2003-2009, 2002.
19. Decker RS, Wildenthal K. Lysosomal alterations in hypoxic and reoxygenated hearts. I. Ultrastructural and cytochemical changes. Am J Pathol 98: 425-444, 1980.
20. Deshmukh AS, Treebak JT, Long YC, Viollet B, Wojtaszewski JF, Zierath JR. Role of adenosine 5′-monophosphate-activated protein kinase subunits in skeletal muscle mammalian target of rapamycin signaling. Mol Endocrinol 22: 1105-1112, 2008.
21. Diwan A, Koesters AG, Odley AM, Pushkaran S, Baines CP, Spike BT, Daria D, Jegga AG, Geiger H, Aronow BJ, Molkentin JD, Macleod KF, Kalfa TA, Dorn GW 2nd. Unrestrained erythroblast development in Nix-/- mice reveals a mechanism for apoptotic modulation of erythropoiesis. Proc Natl Acad Sci USA 104: 6794-6799, 2007.
22. Duncan JG, Fong JL, Medeiros DM, Finck BN, Kelly DP. Insulin-resistant heart exhibits a mitochondrial biogenic response driven by the peroxisome proliferator-activated receptor-alpha/PGC-1alpha gene regulatory pathway. Circulation 115: 909-917, 2007.
23. Elmore SP, Qian T, Grissom SF, Lemasters JJ. The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J 15: 2286-2287, 2001.
24. Erlich S, Mizrachy L, Segev O, Lindenboim L, Zmira O, Adi-Harel S, Hirsch JA, Stein R, Pinkas-Kramarski R. Differential interactions between Beclin 1 and Bcl-2 family members. Autophagy 3: 561-568, 2007.
25. Fornai F, Longone P, Cafaro L, Kastsiuchenka O, Ferrucci M, Manca ML, Lazzeri G, Spalloni A, Bellio N, Lenzi P, Modugno N, Siciliano G, Isidoro C, Murri L, Ruggieri S, Paparelli A. Lithium delays progression of amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 105: 2052-2057, 2008. (Pubitemid 351439463)
26. Fornai F, Longone P, Ferrucci M, Lenzi P, Isidoro C, Ruggieri S, Paparelli A. Autophagy and amyotrophic lateral sclerosis: the multiple roles of lithium. Autophagy 4: 527-530, 2008. (Pubitemid 351705154)
27. Gao Z, Gammoh N, Wong PM, Erdjument-Bromage H, Tempst P, Jiang X. Processing of autophagic protein LC3 by the 20S proteasome. Autophagy 6: 126-137.
28. Geisler S, Holmstrom KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ, Springer W. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 12: 119-131.
29. Goffart S, von Kleist-Retzow JC, Wiesner RJ. Regulation of mitochondrial proliferation in the heart: power-plant failure contributes to cardiac failure in hypertrophy. Cardiovasc Res 64: 198-207, 2004.
30. Grivennikova VG, Kareyeva AV, Vinogradov AD. What are the sources of hydrogen peroxide production by heart mitochondria? Biochim Biophys Acta. In press.
31. Gronowicz G, Swift H, Steck TL. Maturation of the reticulocyte in vitro. J Cell Sci 71: 177-197, 1984.
32. Gustafsson AB, Gottlieb RA. Autophagy in ischemic heart disease. Circ Res 104: 150-158, 2009.
33. Gustafsson AB, Gottlieb RA. Heart mitochondria: gates of life and death. Cardiovasc Res 77: 334-343, 2008.
34. Gutsaeva DR, Carraway MS, Suliman HB, Demchenko IT, Shitara H, Yonekawa H, Piantadosi CA. Transient hypoxia stimulates mitochondrial biogenesis in brain subcortex by a neuronal nitric oxide synthase-dependent mechanism. J Neurosci 28: 2015-2024, 2008.
35. Haigis MC, Guarente LP. Mammalian sirtuins - emerging roles in physiology, aging, and calorie restriction. Genes Dev 20: 2913-2921, 2006.
36. Halestrap AP, Pasdois P. The role of the mitochondrial permeability transition pore in heart disease. Biochim Biophys Acta 1787: 1402-1415, 2009.
37. Hamacher-Brady A, Brady NR, Gottlieb RA, Gustafsson AB. Autophagy as a protective response to Bnip3-mediated apoptotic signaling in the heart. Autophagy 2: 307-309, 2006.
38. Hamacher-Brady A, Brady NR, Logue SE, Sayen MR, Jinno M, Kirshenbaum LA, Gottlieb RA, Gustafsson AB. Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ 14: 146-157, 2007.
39. Hausenloy D, Wynne A, Duchen M, Yellon D. Transient mitochondrial permeability transition pore opening mediates preconditioning-induced protection. Circulation 109: 1714-1717, 2004.
40. Heynen MJ, Tricot G, Verwilghen RL. Autophagy of mitochondria in rat bone marrow erythroid cells. Relation to nuclear extrusion. Cell Tissue Res 239: 235-239, 1985.
41. Hickson-Bick DL, Jones C, Buja LM. Stimulation of mitochondrial biogenesis and autophagy by lipopolysaccharide in the neonatal rat cardiomyocyte protects against programmed cell death. J Mol Cell Cardiol 44: 411-418, 2008.
42. Hyde BB, Twig G, Shirihai OS. Organellar vs cellular control of mitochondrial dynamics. Semin Cell Dev Biol. In press.
43. Ichas F, Mazat JP. From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim Biophys Acta 1366: 33-50, 1998.
44. Ichimura Y, Kominami E, Tanaka K, Komatsu M. Selective turnover of p62/A170/SQSTM1 by autophagy. Autophagy 4: 1063-1066, 2008.
45. Kang HT, Hwang ES. Nicotinamide enhances mitochondria quality through autophagy activation in human cells. Aging Cell 8: 426-438, 2009.
46. Kanki T, Klionsky DJ. Mitophagy in yeast occurs through a selective mechanism. J Biol Chem 283: 32386-32393, 2008.
47. Kanki T, Wang K, Cao Y, Baba M, Klionsky DJ. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell 17: 98-109, 2009.
48. Keller JN, Dimayuga E, Chen Q, Thorpe J, Gee J, Ding Q. Autophagy, proteasomes, lipofuscin, and oxidative stress in the aging brain. Int J Biochem Cell Biol 36: 2376-2391, 2004.
49. Kissova I, Deffieu M, Manon S, Camougrand N. Uth1p is involved in the autophagic degradation of mitochondria. J Biol Chem 279: 39068-39074, 2004.
50. Kissova I, Salin B, Schaeffer J, Bhatia S, Manon S, Camougrand N. Selective and non-selective autophagic degradation of mitochondria in yeast. Autophagy 3: 329-336, 2007.
51. Korolchuk VI, Menzies FM, Rubinsztein DC. Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Lett 584: 1393-1398, 2010.
52. Koury MJ, Koury ST, Kopsombut P, Bondurant MC. In vitro maturation of nascent reticulocytes to erythrocytes. Blood 105: 2168-2174, 2005.
53. Kubasiak LA, Hernandez OM, Bishopric NH, Webster KA. Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc Natl Acad Sci USA 99: 12825-12830, 2002.
54. Kubli DA, Quinsay MN, Huang C, Lee Y, Gustafsson AB. Bnip3 functions as a mitochondrial sensor of oxidative stress during myocardial ischemia and reperfusion. Am J Physiol Heart Circ Physiol 295: H2025-H2031, 2008.
55. Kujoth GC, Bradshaw PC, Haroon S, Prolla TA. The role of mitochondrial DNA mutations in mammalian aging. PLoS Genet 3: e24, 2007.
56. Kundu M, Lindsten T, Yang CY, Wu J, Zhao F, Zhang J, Selak MA, Ney PA, Thompson CB. Ulk1 plays a critical role in the autophagic clearance of mitochondria and ribosomes during reticulocyte maturation. Blood 112: 1493-1502, 2008.
57. Lee IH, Cao L, Mostoslavsky R, Lombard DB, Liu J, Bruns NE, Tsokos M, Alt FW, Finkel T. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc Natl Acad Sci USA 105: 3374-3379, 2008.
58. Li W, Bengtson MH, Ulbrich A, Matsuda A, Reddy VA, Orth A, Chanda SK, Batalov S, Joazeiro CA. Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the organelle's dynamics and signaling. PLoS One 3: e1487, 2008.
59. Lim SY, Davidson SM, Hausenloy DJ, Yellon DM. Preconditioning and postconditioning: the essential role of the mitochondrial permeability transition pore. Cardiovasc Res 75: 530-535, 2007.
60. Little JP, Safdar A, Cermak NM, Tarnopolsky MA, Gibala MJ. Acute endurance exercise increases the nuclear abundance of PGC-1α in trained human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 298: R912-R917, 2010.
61. Little JP, Safdar AS, Wilkin GP, Tarnopolsky MA, Gibala MJ. A practical model of low-volume high-intensity interval training induces mitochondrial biogenesis in human skeletal muscle: potential mechanisms. J Physiol 588: 1011-1022, 2010.
62. Lopez-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, Cascajo MV, Allard J, Ingram DK, Navas P, de Cabo R. Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc Natl Acad Sci USA 103: 1768-1773, 2006.
63. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P, Tasdemir E, Pierron G, Troulinaki K, Tavernarakis N, Hickman JA, Geneste O, Kroemer G. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J 26: 2527-2539, 2007.
64. Mancuso DJ, Abendschein DR, Jenkins CM, Han X, Saffitz JE, Schuessler RB, Gross RW. Cardiac ischemia activates calcium-independent phospholipase A2beta, precipitating ventricular tachyarrhythmias in transgenic mice: rescue of the lethal electrophysiologic phenotype by mechanism-based inhibition. J Biol Chem 278: 22231-22236, 2003.
65. Matsui M, Yamamoto A, Kuma A, Ohsumi Y, Mizushima N. Organelle degradation during the lens and erythroid differentiation is independent of autophagy. Biochem Biophys Res Commun 339: 485-489, 2006.
66. Mazure NM, Pouyssegur J. Atypical BH3-domains of BNIP3 and BNIP3L lead to autophagy in hypoxia. Autophagy 5: 868-869, 2009.
67. McLeod CJ, Jeyabalan AP, Minners JO, Clevenger R, Hoyt RF Jr, Sack MN. Delayed ischemic preconditioning activates nuclear-encoded electron-transfer- chain gene expression in parallel with enhanced post-anoxic mitochondrial respiratory recovery. Circulation 110: 534-539, 2004.
68. Menshikova EV, Ritov VB, Fairfull L, Ferrell RE, Kelley DE, Goodpaster BH. Effects of exercise on mitochondrial content and function in aging human skeletal muscle. J Gerontol A Biol Sci Med Sci 61: 534-540, 2006.
69. Menzies RA, Gold PH. The turnover of mitochondria in a variety of tissues of young adult and aged rats. J Biol Chem 246: 2425-2429, 1971.
70. Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183: 795-803, 2008.
71. Nekhaeva E, Bodyak ND, Kraytsberg Y, McGrath SB, Van Orsouw NJ, Pluzhnikov A, Wei JY, Vijg J, Khrapko K. Clonally expanded mtDNA point mutations are abundant in individual cells of human tissues. Proc Natl Acad Sci USA 99: 5521-5526, 2002.
72. Nishida K, Kyoi S, Yamaguchi O, Sadoshima J, Otsu K. The role of autophagy in the heart. Cell Death Differ 16: 31-38, 2009.
73. Novak I, Kirkin V, McEwan DG, Zhang J, Wild P, Rozenknop A, Rogov V, Lohr F, Popovic D, Occhipinti A, Reichert AS, Terzic J, Dotsch V, Ney PA, Dikic I. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 11: 45-51.
74. + exchange activity, osmotic swelling and mitophagy. Cell Death Differ 14: 1647-1656, 2007.
75. Okamoto K, Kondo-Okamoto N, Ohsumi Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 17: 87-97, 2009.
76. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. Bcl-2 antiapoptotic proteins inhibit beclin 1-dependent autophagy. Cell 122: 927-939, 2005.
77. Pfeifer U. Inhibition by insulin of the formation of autophagic vacuoles in rat liver. A morphometric approach to the kinetics of intracellular degradation by autophagy. J Cell Biol 78: 152-167, 1978.
78. Pinotti MF, Leopoldo AS, Silva MD, Sugizaki MM, do Nascimento AF, Lima-Leopoldo AP, Aragon FF, Padovani CR, Cicogna AC. A comparative study of myocardial function and morphology during fasting/refeeding and food restriction in rats. Cardiovasc Pathol. In press.
79. Priault M, Salin B, Schaeffer J, Vallette FM, di Rago JP, Martinou JC. Impairing the bioenergetic status and the biogenesis of mitochondria triggers mitophagy in yeast. Cell Death Differ 12: 1613-1621, 2005.
80. Quinsay MN, Lee Y, Rikka S, Sayen MR, Molkentin JD, Gottlieb RA, Gustafsson AB. Bnip3 mediates permeabilization of mitochondria and release of cytochrome c via a novel mechanism. J Mol Cell Cardiol 48: 1146-1156, 2010.
81. Rabinowitz M, Swift H. Mitochondrial nucleic acids and their relation to the biogenesis of mitochondria. Physiol Rev 50: 376-427, 1970.
82. Rabinowitz M, Zak R. Mitochondria and cardiac hypertrophy. Circ Res 36: 367-376, 1975.
83. Rasbach KA, Schnellmann RG. Signaling of mitochondrial biogenesis following oxidant injury. J Biol Chem 282: 2355-2362, 2007.
84. Rasola A, Bernardi P. The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis 12: 815-833, 2007.
85. Ravikumar B, Acevedo-Arozena A, Imarisio S, Berger Z, Vacher C, O'Kane CJ, Brown SD, Rubinsztein DC. Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat Genet 37: 771-776, 2005.
86. Regula KM, Ens K, Kirshenbaum LA. Inducible expression of BNIP3 provokes mitochondrial defects and hypoxia-mediated cell death of ventricular myocytes. Circ Res 91: 226-231, 2002.
87. Rodriguez-Enriquez S, Kim I, Currin RT, Lemasters JJ. Tracker dyes to probe mitochondrial autophagy (mitophagy) in rat hepatocytes. Autophagy 2: 39-46, 2006.
88. Ross CA, Poirier MA. Protein aggregation and neurodegenerative disease. Nat Med 10, Suppl: S10-S17, 2004.
89. Sandoval H, Thiagarajan P, Dasgupta SK, Schumacher A, Prchal JT, Chen M, Wang J. Essential role for Nix in autophagic maturation of erythroid cells. Nature 454: 232-235, 2008.
90. 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 26: 1749-1760, 2007.
91. Schweers RL, Zhang J, Randall MS, Loyd MR, Li W, Dorsey FC, Kundu M, Opferman JT, Cleveland JL, Miller JL, Ney PA. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci USA 104: 19500-19505, 2007.
92. Shen X, Zheng S, Thongboonkerd V, Xu M, PierceWMJr, Klein JB, Epstein PN. Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am J Physiol Endocrinol Metab 287: E896-E905, 2004.
93. Stewart JB, Freyer C, Elson JL, Wredenberg A, Cansu Z, Trifunovic A, Larsson NG. Strong purifying selection in transmission of mammalian mitochondrial DNA. PLoS Biol 6: e10, 2008.
94. Tal R, Winter G, Ecker N, Klionsky DJ, Abeliovich H. Aup1p, a yeast mitochondrial protein phosphatase homolog, is required for efficient stationary phase mitophagy and cell survival. J Biol Chem 282: 5617-5624, 2007.
95. Terman A. Garbage catastrophe theory of aging: imperfect removal of oxidative damage? Redox Rep 6: 15-26, 2001.
96. Terman A, Brunk UT. Autophagy in cardiac myocyte homeostasis, aging, and pathology. Cardiovasc Res 68: 355-365, 2005.
97. Terman A, Brunk UT. Oxidative stress, accumulation of biological 'garbage', and aging. Antioxid Redox Signal 8: 197-204, 2006.
98. Terman A, Dalen H, Eaton JW, Neuzil J, Brunk UT. Mitochondrial recycling and aging of cardiac myocytes: the role of autophagocytosis. Exp Gerontol 38: 863-876, 2003.
99. Terman A, Gustafsson B, Brunk UT. The lysosomal-mitochondrial axis theory of postmitotic aging and cell death. Chem Biol Interact 163: 29-37, 2006.
100. Tolkovsky AM, Xue L, Fletcher GC, Borutaite V. Mitochondrial disappearance from cells: a clue to the role of autophagy in programmed cell death and disease? Biochimie 84: 233-240, 2002.
101. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, Las G, Alroy J, Wu M, Py BF, Yuan J, Deeney JT, Corkey BE, Shirihai OS. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27: 433-446, 2008.
102. Vande Velde C, Cizeau J, Dubik D, Alimonti J, Brown T, Israels S, Hakem R, Greenberg AH. BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol Cell Biol 20: 5454-5468, 2000.
103. Ventura-Clapier R, Garnier A, Veksler V. Transcriptional control of mitochondrial biogenesis: the central role of PGC-1alpha. Cardiovasc Res 79: 208-217, 2008.
104. Vermulst M, Wanagat J, Kujoth GC, Bielas JH, Rabinovitch PS, Prolla TA, Loeb LA. DNA deletions and clonal mutations drive pre-mature aging in mitochondrial mutator mice. Nat Genet 40: 392-394, 2008.
105. Vina J, Gomez-Cabrera MC, Borras C, Froio T, Sanchis-Gomar F, Martinez-Bello VE, Pallardo FV. Mitochondrial biogenesis in exercise and in ageing. Adv Drug Deliv Rev 61: 1369-1374, 2009.
106. Weiss JN, Korge P, Honda HM, Ping P. Role of the mitochondrial permeability transition in myocardial disease. Circ Res 93: 292-301, 2003.
107. Xue L, Fletcher GC, Tolkovsky AM. Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution. Mol Cell Neurosci 14: 180-198, 1999.
108. Xue L, Fletcher GC, Tolkovsky AM. Mitochondria are selectively eliminated from eukaryotic cells after blockade of caspases during apoptosis. Curr Biol 11: 361-365, 2001.
109. Yuan H, Perry CN, Huang C, Iwai-Kanai E, Carreira RS, Glembotski CC, Gottlieb RA. LPS-induced autophagy is mediated by oxidative signaling in cardiomyocytes and is associated with cytoprotection. Am J Physiol Heart Circ Physiol 296: H470-H479, 2009.
110. Zhang J, Randall MS, Loyd MR, Dorsey FC, Kundu M, Cleveland JL, Ney PA. Mitochondrial clearance is regulated by Atg7-dependent and -independent mechanisms during reticulocyte maturation. Blood 114: 157-164, 2009.
111. Zhang X, Zhou J, Fernandes AF, Sparrow JR, Pereira P, Taylor A, Shang F. The proteasome: a target of oxidative damage in cultured human retina pigment epithelial cells. Invest Ophthalmol Vis Sci 49: 3622-3630, 2008.
112. Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192: 1001-1014, 2000.