Regulation of autophagy in oxygen-dependent cellular stress

Current Pharmaceutical Design

Volumn 19, Issue 15, 2013, Pages 2747-2756

  Ryter, Stefan W ^a   Choi, Augustine M K ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Autophagy; Carbon monoxide; Heme oxygenase 1; Hyperoxia; Hypoxia; Mitochondria; Oxidative stress; Reactive oxygen species

Indexed keywords

BECLIN 1; CIGARETTE SMOKE; HYDROGEN PEROXIDE; HYPOXIA INDUCIBLE FACTOR 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; SUPEROXIDE;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CELL ELONGATION; CELL MATURATION; CELL STRESS; CONJUGATION; HUMAN; HYPEROXIA; HYPOXIA; METABOLISM; MITOPHAGY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; AUTOPHAGY; HUMANS; OXIDATION-REDUCTION; OXIDATIVE STRESS; OXYGEN;

EID: 84876697580     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612811319150010     Document Type: Article

References (120)

1. Sies H. Oxidative stress: oxidants and antioxidants. Exp Physiol 1997; 82: 291-5.
2. Forman HJ, Maiorino M, Ursini F. Signaling functions of reactive oxygen species. Biochemistry 2010; 49: 835-42.
3. Dröge W. Free radicals in the physiological control of cell function. Physiol Rev 2002; 82: 47-95.
4. Sugamura K, Keaney JF. Reactive oxygen species in cardiovascular disease. Free Radic Biol Med 2011; 51: 978-92.
5. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine. New York: Oxford University Press 1999.
6. Davies KJ. Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life 2000; 50: 279-89.
7. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 2006; 86: 583-650.
8. Lee AS. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem Sci 2001; 26: 504-10.
9. Welch WJ. The mammalian heat shock (or stress) response: a cellular defense mechanism. Adv Exp Med Biol 1987; 225: 287-304.
10. Galluzzi L, Maiuri MC, Vitale I, et al. Cell death modalities: classification and pathophysiological implications. Cell Death Differ 2007; 14: 1237-43.
11. Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell 2010; 40: 280-93.
12. Kroemer G, Dallaporta B, Resche-Rigon M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu Rev Physiol 1998; 60: 619-42.
13. Majno G, Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 1995; 146: 3-15.
14. Kelekar A. Autophagy. Ann NY Acad Sci 2005; 1066: 259-71.
15. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Ann Rev Genet 2009; 43: 67-93.
16. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6: 463-77.
17. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451: 1069-75.
18. Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290: 1717-21.
19. Yorimitsu T, Klionsky DJ. Autophagy: molecular machinery for self-eating. Cell Death Diff 2005; 12: 1542-52.
20. Levine B, Mizushima N, Virgin HW. Autophagy immunity and inflammation. Nature 2011; 469: 323-35.
21. Ravikumar B, Sarkar S, Davies JE, et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 2010; 90: 1383-1435.
22. Eskelinen EL. New insights into the mechanisms of macroautophagy in mammalian cells. Int Rev Cell Mol Biol 2008; 266: 207-47.
23. Hansen TE, Johansen T. Following autophagy step by step. BMC Biology 2011; 9: 39.
24. Barth S, Glick D, Macleod KF. Autophagy: assays and artifacts. J Pathol 2010; 221: 117-24.
25. Boya P, González-Polo RA, Casares N, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005; 25: 1025-40.
26. Kanamori H, Takemura G, Maruyama R, et al. Functional significance and morphological characterization of starvation-induced autophagy in the adult heart. Am J Pathol 2009; 174: 1705-14.
27. Kuma A, Hatano M, Matsui M, et al. The role of autophagy during the early neonatal starvation period. Nature 2004; 432: 1032-36.
28. Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011; 7: 279-96.
29. Wang K, Klionsky DJ. Mitochondria removal by autophagy. Autophagy 2011; 7: 297-300.
30. Tanida I. Autophagosome formation and molecular mechanism of autophagy. Antioxid Redox Signal 2011; 14: 2201-14.
31. Lamark T, Johansen T. Aggrephagy: selective disposal of protein aggregates by macroautophagy. Int J Cell Biol 2012; 2012: 736905.
32. Santambrogio L, Cuervo AM. Chasing the elusive mammalian microautophagy. Autophagy 2011; 7: 652-4.
33. Kaushik S, Bandyopadhyay U, Sridhar S, et al. Chaperonemediated autophagy at a glance. J Cell Sci 2011; 124: 495-9.
34. Kaushik S, Cuervo AM. Autophagy as a cell-repair mechanism: activation of chaperone-mediated autophagy during oxidative stress. Mol Aspects Med 2006; 27: 444-54.
35. Yang Z, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol 2010; 22: 124-31.
36. Jung CH, Ro SH, Cao J, Otto NM, Kim DH. mTOR regulation of autophagy. FEBS Lett 2010; 584: 1287-95.
37. Jung CH, Jun CB, Ro SH, et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 2009; 20: 1992-2003.
38. Ganley IG, Lam DH, Wang J, Ding X, Chen S, Jiang X. ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem 2009; 284: 12297-305.
39. Mercer CA, Kaliappan A, Dennis PB. A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy 2009; 5: 649-62.
40. Chan EY, Kir S, Tooze SA. siRNA screening of the kinome identifies ULK1 as a multidomain modulator of autophagy. J Biol Chem 2007; 282: 25464-74.
41. Hosokawa N, Hara T, Kaizuka T, et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 2009; 20: 1981-91.
42. Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 2011;13: 132-41.
43. Liang XH, Jackson S, Seaman M, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999; 402: 672-76.
44. He C, Levine B. The Beclin 1 interactome. Curr Opin Cell Biol 2010; 22: 140-9.
45. Itakura E, Kishi C, Inoue K, Mizushima N. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 2008; 19: 5360-72.
46. Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol 2001; 2: 211-16.
47. Tanida I, Ueno T, Kominami E. LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 36: 2503-18.
48. Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19: 5720-28.
49. 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: 2805-12.
50. He H, Dang Y, Dai F, et al. Post-translational modifications of three members of the human MAP1LC3 family and detection of a novel type of modification for MAP1LC3B. J Biol Chem 2003; 278: 29278-287.
51. Gutierrez MG, Munafo DB, Beron W, Colombo MI. 2004. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci 117: 2687-97.
52. Jager S, Bucci C, Tanida I, et al. Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci 2004; 117: 4837-48.
53. Liang C, Lee JS, Inn KS, et al. Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol 2008; 10: 776-87.
54. Kaminskyy V, Zhivotovsky B. Proteases in autophagy. Biochim Biophys Acta 2012; 1824: 44-50.
55. Novak I, Kirkin V, McEwan DG, et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 2010; 11:45-51
56. Kiffin R, Bandyopadhyay U, Cuervo AM. Oxidative stress and autophagy. Antioxid Redox Signal 2006; 8: 152-62.
57. Lee J, Giordano S, Zhang J. Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J 2012; 441: 523-40.
58. Azad MB, Chen Y, Gibson SB. Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment. Antioxid Redox Signal 2009; 11: 777-9.
59. Chen Y, McMillan-Ward E, Kong J, Israels SJ, Gibson SB. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ 2008; 15: 171-82.
60. Pyo JO, Nah J, Kim HJ, et al. Compensatory activation of ERK1/2 in Atg5-deficient mouse embryo fibroblasts suppresses oxidative stress induced cell death. Autophagy 2008; 4: 315-21.
61. Wang Y, Singh R, Xiang Y, Czaja MJ. Macroautophagy and chaperone- mediated autophagy are required for hepatocyte resistance to oxidant stress. Hepatology 2010; 52: 266-77.
62. González-Polo RA, Niso-Santano M, Ortíz-Ortíz MA, et al. Inhibition of paraquat-induced autophagy accelerates the apoptotic cell death in neuroblastoma SH-SY5Y cells. Toxicol Sci 2007; 97: 448-58.
63. Vives-Bauza C, Zhou C, Huang Y, et al. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci USA 2010; 107: 378-83.
64. Chen Y, McMillan-Ward E, Kong J, Israels SJ, Gibson SB. Mitochondrial electron-transport-chain inhibitors of complexes I and II induce autophagic cell death mediated by reactive oxygen species. J Cell Sci 2007; 120: 4155-66.
65. Wang Y, Singh R, Massey AC, et al. Loss of macroautophagy promotes or prevents fibroblast apoptosis depending on the death stimulus. J Biol Chem 2008; 283: 4766-77.
66. Singh R, Czaja MJ. Compensatory mechanisms and the type of injury determine the fate of cells with impaired macroautophagy. Autophagy 2008; 4: 516-8.
67. González-Polo RA, Niso-Santano M, Ortíz-Ortíz MA, et al. Relationship between autophagy and apoptotic cell death in human neuroblastoma cells treated with paraquat: could autophagy be a brake in paraquat-induced apoptotic death? Autophagy 2007; 3: 366-7.
68. 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.
69. Chen Y, Azad MB, Gibson SB. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ 2009; 16: 1040-52.
70. Djavaheri-Mergny M, Amelotti M, Mathieu J, Besançon F, Bauvy C, Codogno P. Regulation of autophagy by NFkappaB transcription factor and reactive oxygen species. Autophagy 2007; 3:390-2.
71. Baregamian N, Song J, Bailey CE, Papaconstantinou J, Evers BM, Chung DH. Tumor necrosis factor-alpha and apoptosis signalregulating kinase 1 control reactive oxygen species release, mitochondrial autophagy, and c-Jun N-terminal kinase/p38 phosphorylation during necrotizing enterocolitis. Oxid Med Cell Longev 2009; 2: 297-306.
72. Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 2008; 183: 795-803.
73. Geisler S, Holmström KM, Skujat D, et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 2010; 12: 119-31.
74. Morris HR. Genetics of Parkinson's disease. Ann Med 2005; 37: 86-96.
75. Trancikova A, Tsika E, Moore DJ. Mitochondrial dysfunction in genetic animal models of Parkinson's disease. Antioxid Redox Signal 2012; 16: 896-919.
76. Meng F, Yao D, Shi Y, et al. Oxidation of the cysteine-rich regions of parkin perturbs its E3 ligase activity and contributes to protein aggregation. Mol Neurodegener 2011; 6: 34.
77. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, Fitzgerald KA, Ryter SW, Choi AM. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011; 12: 222-30.
78. Berra E, Benizri E, Ginouvès A, Volmat V, Roux D, Pouysségur J. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia. EMBO J 2003; 22: 4082-90.
79. Chandel NS, McClintock DS, Feliciano CE, et al. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxiainducible factor-1alpha during hypoxia: a mechanism of O2 sensing. 2000; J Biol Chem 275: 25130-8.
80. Zhang H, Bosch-Marce M, Shimoda LA, et al. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 2008; 283: 10892-903.
81. Bellot G, Garcia-Medina R, Gounon P, et al. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol 2009; 29: 2570-81.
82. Azad MB, Chen Y, Henson ES, et al. Hypoxia induces autophagic cell death in apoptosis-competent cells through a mechanism involving BNIP3. Autophagy 2008; 4:195-204.
83. Lee SJ, Smith A, Guo L, et al. Autophagic protein LC3B confers resistance against hypoxia-induced pulmonary hypertension. Am J Respir Crit Care Med 2011; 183: 649-58.
84. Lee SJ, Kim HP, Jin Y, Choi AM, Ryter SW. Beclin 1 deficiency is associated with increased hypoxia-induced angiogenesis. Autophagy 2011; 7: 829-39.
85. Parinandi NL, Kleinberg MA, Usatyuk PV, et al. Hyperoxiainduced NAD(P)H oxidase activation and regulation by MAP kinases in human lung endothelial cells. Am J Physiol Lung Cell Mol Physiol 2003; 284: L26-38.
86. Li J, Gao X, Qian M, Eaton JW. Mitochondrial metabolism underlies hyperoxic cell damage. Free Radic Biol Med 2004; 36: 1460-70.
87. Altemeier WA, Sinclair SE. Hyperoxia in the intensive care unit: why more is not always better. Curr Opin Crit Care 2007; 13: 73-8.
88. Crapo JD. Morphologic changes in pulmonary oxygen toxicity. Annu Rev Physiol 1986; 48: 721-31.
89. Tanaka A, Jin Y, Lee SJ, et al. Hyperoxia-induced LC3B interacts with the Fas apoptotic pathway in epithelial cell death. Am J Respir Cell Mol Biol 2012; 46: 507-14.
90. Church DF, Pryor WA. Free-radical chemistry of cigarette smoke and its toxicological implications. Environ Health Perspect 1985; 64: 111-26.
91. MacNee W, Rahman I. Oxidants and antioxidants as therapeutic targets in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999; 160: S58-S65.
92. Kim HP, Wang X, Chen ZH, et al. Autophagic proteins regulate cigarette smoke induced apoptosis: protective role of heme oxygenase- 1. Autophagy 2008; 4: 887-95.
93. Chen ZH, Kim HP, Sciurba FC, et al. Egr-1 regulates autophagy in cigarette smoke-induced chronic obstructive pulmonary disease. PLoS One 2008; 3: e3316.
94. Chen ZH, Lam HC, Jin Y, et al. Autophagy protein microtubuleassociated protein 1 light chain-3B (LC3B) activates extrinsic apoptosis during cigarette smoke-induced emphysema. Proc Natl Acad Sci USA 2010; 107: 18880-5.
95. Keyse SM, Tyrrell RM. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci USA 1989; 86: 99-103.
96. Keyse SM, Applegate LA, Tromvoukis Y, Tyrrell RM. Oxidant stress leads to transcriptional activation of the human heme oxygenase gene in cultured skin fibroblasts. Mol Cell Biol 1990; 10: 4967-9.
97. Applegate LA, Luscher P, Tyrrell RM. Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Res 1991; 51: 974-8.
98. Tenhunen R, Marver HS, Schmid R. Microsomal heme oxygenase. Characterization of the enzyme. J Biol Chem 1969; 244: 6388-94.
99. Otterbein LE, Bach FH, Alam J, et al. Carbon monoxide has antiinflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000; 6: 422-28.
100. Petrache I, Otterbein LE, Alam J, Wiegand GW, Choi AM. Heme oxygenase-1inhibits TNF-alpha-induced apoptosis in cultured fibroblasts. Am J Physiol Lung Cell Mol Physiol 2000; 278: L312-9.
101. Carchman EH, Rao J, Loughran PA, Rosengart MR, Zuckerbraun BS. Heme oxygenase-1-mediated autophagy protects against hepatocyte cell death and hepatic injury from infection/sepsis in mice. Hepatology 2011; 53: 2053-62.
102. Waltz P, Carchman EH, Young AC, et al. Lipopolysaccaride induces autophagic signaling in macrophages via a TLR4, heme oxygenase-1 dependent pathway. Autophagy 2011; 7: 315-20.
103. Ryter SW, Tyrrell RM. The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both proand antioxidant properties. Free Radic Biol Med. 2000; 28: 289-309
104. Balla J, Jacob HS, Balla G, Nath K, Eaton JW, Vercellotti GM. Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc Natl Acad Sci USA 1993; 90: 9285-9.
105. Higdon AN, Benavides GA, Chacko BK, et al. Hemin causes mitochondrial dysfunction in endothelial cells through promoting lipid peroxidation: the protective role of autophagy. Am J Physiol Heart Circ Physiol 2012; 302: H1394-409.
106. Zhou C, Zhou J, Sheng F, et al. The heme oxygenase-1 inhibitor ZnPPIX induces non-canonical, Beclin 1-independent, autophagy through p38 MAPK pathway. Acta Biochim Biophys Sin (Shanghai) 2012; Aug 7 [Epub ahead of print].
107. Zukor H, Song W, Liberman A, Mui J, Vali H, Fillebeen C, Pantapoulos K, Wu TD, Guerquin-Kern JL, Schipper HM. HO-1- mediated macroautophagy: a mechanism for unregulated iron deposition in aging and degenerating neural tissues. J Neurochem 2009; 109: 776-91.
108. Song W, Zukor H, Lin SH, et al. Schizophrenia-like features in transgenic mice overexpressing human HO-1 in the astrocytic compartment. J Neurosci 2012; 32:10841-53.
109. Bolisetty S, Traylor AM, Kim J, et al. Heme oxygenase-1 inhibits renal tubular macroautophagy in acute kidney injury. J Am Soc Nephrol 2010; 21: 1702-12.
110. Banerjee P, Basu A, Wegiel B, et al. Heme oxygenase-1 promotes survival of renal cancer cells through modulation of apoptosis and autophagy-regulating molecules. J Biol Chem 2012; Jul 26. [Epub ahead of print]
111. Kondo Y, Kanzawa T, Sawaya R, Kondo S. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 2005; 5: 726-34.
112. Lee SJ, Ryter SW, Xu JF, et al. Carbon monoxide activates autophagy via mitochondrial reactive oxygen species formation. Am J Respir Cell Mol Biol 2011; 45: 867-73.
113. Ray PD, Huang BW, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 2012; 24: 981-90.
114. Ryter SW, Nakahira K, Haspel JA, Choi AM. Autophagy in pulmonary diseases. Annu Rev Physiol 2012; 74:377-401.
115. Ryter SW, Lee SJ, Choi AM. Autophagy in cigarette smokeinduced chronic obstructive pulmonary disease. Expert Rev Respir Med 2010; 4:573-84.
116. Ryter SW, Lee SJ, Smith A, Choi AM. Autophagy in vascular disease. Proc Am Thorac Soc 2010; 7:40-7.
117. Martinet W, De Meyer GR. Autophagy in atherosclerosis: a cell survival and death phenomenon with therapeutic potential. Circ Res 2009; 104: 304-17.
118. Martinet W, Agostinis P, Vanhoecke B, Dewaele M, De Meyer GR. Autophagy in disease: a double-edged sword with therapeutic potential. Clin Sci (Lond) 2009; 116: 697-712
119. Rioux JD, Xavier RJ, Taylor KD, et al. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat Genet 2007; 39: 596-604.
120. García-Ma S, Alcaide A, Domínguez C. Pharmacological control of autophagy: Therapeutic perspectives in inflammatory bowel disease and colorectal cancer. Curr Pharm Des 2012; 18: 3853-73.