The protective roles of autophagy in ischemic preconditioning

Acta Pharmacologica Sinica

Volumn 34, Issue 5, 2013, Pages 636-643

  Yan, Wen Jun ^a,b   Dong, Hai Long ^b   Xiong, Li Ze ^b  

^a GANSU PROVINCIAL HOSPITAL   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

AMPK; apoptosis; autophagy; Beclin1; endoplasmic reticulum stress; ischemia reperfusion injury; ischemic preconditioning; mitochondria; mTOR; P13K; reactive oxygen species (ROS)

Indexed keywords

BECLIN 1; CYCLOSPORIN A; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; AUTOPHAGY; CELL SURVIVAL; ENDOPLASMIC RETICULUM STRESS; ISCHEMIC PRECONDITIONING; MITOCHONDRION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; UNFOLDED PROTEIN RESPONSE; UPREGULATION;

ANIMALS; AUTOPHAGY; CELL SURVIVAL; HUMANS; ISCHEMIC PRECONDITIONING; SIGNAL TRANSDUCTION;

EID: 84877621251     PISSN: 16714083     EISSN: 17457254     Source Type: Journal    
DOI: 10.1038/aps.2013.18     Document Type: Review

References (79)

1. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6: 463-77.
2. Mizushima N. Autophagy: process and function. Genes Dev 2007; 21: 2861-73.
3. Huang J, Klionsky DJ. Autophagy and human disease. Cell Cycle 2007; 6: 1837-49.
4. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986; 74: 1124-36.
5. Bonventre JV. Kidney ischemic preconditioning. Curr Opin Nephrol Hypertens 2002; 11: 43-8.
6. Kirino T. Ischemic tolerance. J Cereb Blood Flow Metab 2002; 22: 1283-96.
7. Sheng R, Zhang LS, Han R, Liu XQ, Gao B, Qin ZH. Autophagy activation is associated with neuroprotection in a rat model of focal cerebral ischemic preconditioning. Autophagy 2010; 6: 482-94.
8. Yan W, Zhang H, Bai X, Lu Y, Dong H, Xiong L. Autophagy activation is involved in neuroprotection induced by hyperbaric oxygen preconditioning against focal cerebral ischemia in rats. Brain Res 2011; 1402: 109-21.
9. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43: 67-93.
10. Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol 2010; 12: 814-822.
11. Kiffin R, Christian C, Knecht E, Cuervo AM. Activation of chaperonemediated autophagy during oxidative stress. Mol Biol Cell 2004; 15: 4829-40.
12. Mijaljica D, Prescott M, Devenish RJ. Mitophagy and mitoptosis in disease processes. Methods Mol Biol 2010; 648: 93-106.
13. Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 2008; 182: 685-701.
14. Geng J, Nair U, Yasumura-Yorimitsu K, Klionsky DJ. Post-Golgi Sec proteins are required for autophagy in Saccharomyces cerevisiae. Mol Biol Cell 2010; 21: 2257-69.
15. Reggiori F, Shintani T, Nair U, Klionsky DJ. Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy 2005; 1: 101-9.
16. Hoyer-Hansen M, Jaattela M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 2007; 14: 1576-82.
17. Mizushima N, Kuma A, Kobayashi Y, Yamamoto A, Matsubae M, Takao T, et al. Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J Cell Sci 2003; 116: 1679-88.
18. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 2001; 152: 657-68.
19. Ravikumar B, Acevedo-Arozena A, Imarisio S, Berger Z, Vacher C, O'Kane CJ, et al. Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat Genet 2005; 37: 771-6.
20. Webb JL, Ravikumar B, Rubinsztein DC. Microtubule disruption inhibits autophagosome-lysosome fusion: implications for studying the roles of aggresomes in polyglutamine diseases. Int J Biochem Cell Biol 2004; 36: 2541-50.
21. Eskelinen EL. Maturation of autophagic vacuoles in mammalian cells. Autophagy 2005; 1: 1-10.
22. Koike M, Shibata M, Waguri S, Yoshimura K, Tanida I, Kominami E, et al. Participation of autophagy in storage of lysosomes in neurons from mouse models of neuronal ceroid-lipofuscinoses (Batten disease). Am J Pathol 2005; 167: 1713-28.
23. Mousavi SA, Brech A, Berg T, Kjeken R. Phosphoinositide 3-kinase regulates maturation of lysosomes in rat hepatocytes. Biochem J 2003; 372: 861-9.
24. Takagi H, Matsui Y, Hirotani S, Sakoda H, Asano T, Sadoshima J. AMPK mediates autophagy during myocardial ischemia in vivo. Autophagy 2007; 3: 405-7.
25. Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, et al. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res 2007; 100: 914-22.
26. 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.
27. Wang C, Wang Y, McNutt MA, Zhu WG. Autophagy process is associated with anti-neoplastic function. Acta Biochim Biophys Sin 2011; 43: 425-32.
28. Liang XH, Kleeman LK, Jiang HH, Gordon G, Goldman JE, Berry G, et al. Protection against fatal Sindbis virus encephalitis by Beclin1, a novel Bcl-2 interacting protein. J Virol 1998; 72: 8586-96.
29. Hamacher-Brady A, Brady NR, Gottlieb RA. Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. J Biol Chem 2006; 281: 29776-87.
30. Carloni S, Girelli S, Scopa C, Buonocore G, Longini M, Balduini W. Activation of autophagy and Akt/CREB signaling play an equivalent role in the neuroprotective effect of rapamycin in neonatal hypoxiaischemia. Autophagy 2010; 6: 366-77.
31. Valentim L, Laurence KM, Townsend PA, Carroll CJ, Soond S, Scarabelli TM, et al. Urocortin inhibits Beclin1-mediated autophagic cell death in cardiac myocytes exposed to ischaemia/reperfusion injury. J Mol Cell Cardiol 2006; 40: 846-52.
32. Obara K, Sekito T, Ohsumi Y. Assortment of phosphatidylinositol 3-kinase complexes-Atg14p directs association of complex I to the pre-autophagosomal structure in Saccharomyces cerevisiae. Mol Biol Cell 2006; 17: 1527-39.
33. Liang C, Feng P, Ku B, Dotan I, Canaani D, Oh BH, et al. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol 2006; 8: 688-99.
34. Gu Y, Wang C, Cohen A. Effect of IGF-1 on the balance between autophagy of dysfunctional mitochondria and apoptosis. FEBS Lett 2004; 577: 357-60.
35. Zeng X, Overmeyer JH, Maltese WA. Functional specificity of the mammalian Beclin-Vps34 PI3-kinase complex in macroautophagy versus endocytosis and lysosomal enzyme trafficking. J Cell Sci 2006; 119: 259-70.
36. Aki T, Yamaguchi K, Fujimiya T, Mizukami Y. Phosphoinositide 3-kinase accelerates autophagic cell death during glucose deprivation in the rat cardiomyocyte-derived cell line H9c2. Oncogene 2003; 22: 8529-35.
37. Takemura G, Maruyama R, Goto K, Kanamori H, Tsujimoto A, Minatoguchi S, et al. Fate of isolated adult cardiomyocytes undergoing starvation-induced autophagic degeneration. Autophagy 2009; 5: 90-2.
38. Park HK, Chu K, Jung KH, Lee ST, Bahn JJ, Kim M, et al. Autophagy is involved in the ischemic preconditioning. Neurosci Lett 2009; 451: 16-9.
39. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 2008; 27: 433-46.
40. Gurusamy N, Lekli I, Gorbunov NV, Gherghiceanu M, Popescu LM, Das DK. Cardioprotection by adaptation to ischaemia augments autophagy in association with BAG-1 protein. J Cell Mol Med 2009; 13: 373-87.
41. Elmore SP, Qian T, Grissom SF, Lemasters JJ. The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J 2001; 15: 2286-7.
42. Degli ED, Sebagh M, Pham P, Reffas M, Pous C, Brenner C, et al. Ischemic preconditioning induces autophagy and limits necrosis in human recipients of fatty liver grafts, decreasing the incidence of rejection episodes. Cell Death Dis 2011; 2: e111.
43. Brunk UT, Terman A. The mitochondrial-lysosomal axis theory of aging: accumulation of damaged mitochondria as a result of imperfect autophagocytosis. Eur J Biochem 2002; 269: 1996-2002.
44. Brady NR, Hamacher-Brady A, Gottlieb RA. Proapoptotic BCL-2 family members and mitochondrial dysfunction during ischemia/reperfusion injury, a study employing cardiac HL-1 cells and GFP biosensors. Biochim Biophys Acta 2006; 1757: 667-78.
45. Halestrap AP, Clarke SJ, Javadov SA. Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc Res 2004; 61: 372-85.
46. Tracy K, Dibling BC, Spike BT, Knabb JR, Schumacker P, Macleod KF. BNIP3 is an RB/E2F target gene required for hypoxia-induced autophagy. Mol Cell Biol 2007; 27: 6229-42.
47. Zhang H, Bosch-Marce M, Shimoda LA, Tan YS, Baek JH, Wesley JB, et al. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 2008; 283: 10892-903.
48. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 2010; 8: e1000298.
49. Geisler S, Holmstrom KM, Treis A, Skujat D, Weber SS, Fiesel FC, et al. The PINK1/Parkin-mediated mitophagy is compromised by PDassociated mutations. Autophagy 2010; 6: 871-8.
50. Rutkowski DT, Kaufman RJ. A trip to the ER: coping with stress. Trends Cell Biol 2004; 14: 20-8.
51. Thuerauf DJ, Marcinko M, Gude N, Rubio M, Sussman MA, Glembotski CC. Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes. Circ Res 2006; 99: 275-82.
52. Yorimitsu T, Klionsky DJ. Endoplasmic reticulum stress: a new pathway to induce autophagy. Autophagy 2007; 3: 160-12.
53. Li J, Ni M, Lee B, Barron E, Hinton DR, Lee AS. The unfolded protein response regulator GRP78/BiP is required for endoplasmic reticulum integrity and stress-induced autophagy in mammalian cells. Cell Death Differ 2008; 15: 1460-71.
54. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H, et al. ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamineinduced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 2007; 14: 230-9.
55. 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 2007; 274: 3184-97.
56. Sheng R, Liu XQ, Zhang LS, Gao B, Han R, Wu YQ, et al. Autophagy regulates endoplasmic reticulum stress in ischemic preconditioning. Autophagy 2012; 8: 310-25.
57. Vanden HT, Li C, Shao Z, Schumacker PT, Becker LB. Significant levels of oxidants are generated by isolated cardiomyocytes during ischemia prior to reperfusion. J Mol Cell Cardiol 1997; 29: 2571-83.
58. Khadour FH, Panas D, Ferdinandy P, Schulze C, Csont T, Lalu MM, et al. Enhanced NO and superoxide generation in dysfunctional hearts from endotoxemic rats. Am J Physiol Heart Circ Physiol 2002; 283: H1108-15.
59. Yang J, Wu LJ, Tashino S, Onodera S, Ikejima T. Reactive oxygen species and nitric oxide regulate mitochondria-dependent apoptosis and autophagy in evodiamine-treated human cervix carcinoma HeLa cells. Free Radic Res 2008; 42: 492-504.
60. 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.
61. 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.
62. Li Q, Li J, Zhang L, Wang B, Xiong L. Preconditioning with hyperbaric oxygen induces tolerance against oxidative injury via increased expression of heme oxygenase-1 in primary cultured spinal cord neurons. Life Sci 2007; 80: 1087-93.
63. Nie H, Xiong L, Lao N, Chen S, Xu N, Zhu Z. Hyperbaric oxygen preconditioning induces tolerance against spinal cord ischemia by upregulation of antioxidant enzymes in rabbits. J Cereb Blood Flow Metab 2006; 26: 666-74.
64. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and selfkilling: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007; 8: 741-52.
65. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005; 25: 1025-40.
66. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, et al. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 2006; 8: 1124-32.
67. Pattingre S, Levine B. Bcl-2 inhibition of autophagy: a new route to cancer? Cancer Res 2006; 66: 2885-8.
68. Wirawan E, Vande WL, Kersse K, Cornelis S, Claerhout S, Vanoverberghe I, et al. Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria. Cell Death Dis 2010; 1: e18.
69. Ginet V, Puyal J, Clarke PG, Truttmann AC. Enhancement of autophagic flux after neonatal cerebral hypoxia-ischemia and its regionspecific relationship to apoptotic mechanisms. Am J Pathol 2009; 175: 1962-74.
70. Domart MC, Esposti DD, Sebagh M, Olaya N, Harper F, Pierron G, et al. Concurrent induction of necrosis, apoptosis, and autophagy in ischemic preconditioned human livers formerly treated by chemotherapy. J Hepatol 2009; 51: 881-9.
71. Meriin AB, Sherman MY. Role of molecular chaperones in neurodegenerative disorders. Int J Hyperthermia 2005; 21: 403-19.
72. Dosenko VE, Nagibin VS, Tumanovska LV, Moibenko AA. Protective effect of autophagy in anoxia-reoxygenation of isolated cardiomyocyte? Autophagy 2006; 2: 305-6.
73. Dosenko VE, Nagibin VS, Tumanovskaya LV, Zagoriy VY, Moibenko AA, Vaage J. Proteasome inhibitors eliminate protective effect of postconditioning in cultured neonatal cardiomyocytes. Fiziol Zh 2006; 52: 15-24.
74. Huang C, Yitzhaki S, Perry CN, Liu W, Giricz Z, Mentzer RJ, et al. Autophagy induced by ischemic preconditioning is essential for cardio protection. J Cardiovasc Transl Res 2010; 3: 365-73.
75. Townsend PA, Cutress RI, Carroll CJ, Lawrence KM, Scarabelli TM, Packham G, et al. BAG-1 proteins protect cardiac myocytes from simulated ischemia/reperfusion-induced apoptosis via an alternate mechanism of cell survival independent of the proteasome. J Biol Chem 2004; 279: 20723-8.
76. Gurusamy N, Lekli I, Gherghiceanu M, Popescu LM, Das DK. BAG-1 induces autophagy for cardiac cell survival. Autophagy 2009; 5: 120-1.
77. 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.
78. Yitzhaki S, Huang C, Liu W, Lee Y, Gustafsson AB, Mentzer RJ, et al. Autophagy is required for preconditioning by the adenosine A1 receptor-selective agonist CCPA. Basic Res Cardiol 2009; 104: 157-67.
79. Wu HH, Hsiao TY, Chien CT, Lai MK. Ischemic conditioning by short periods of reperfusion attenuates renal ischemia/reperfusion induced apoptosis and autophagy in the rat. J Biomed Sci 2009; 16: 19.