Neuronal autophagy in cerebral ischemia

Neuroscience Bulletin

Volumn 28, Issue 5, 2012, Pages 658-666

  Xu, Feng ^a   Gu, Jin Hua ^b   Qin, Zheng Hong ^c  

^a FUDAN UNIVERSITY   (China)

^b NANTONG MEDICAL COLLEGE   (China)

^c MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

Author keywords

Apoptosis; Autophagy; Cerebral ischemia; Necrosis; Neuron

Indexed keywords

3 METHYLADENINE; ADENYLATE KINASE; BECLIN 1; CATHEPSIN B INHIBITOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN P53; WORTMANNIN;

AUTOPHAGOSOME; AUTOPHAGY; BRAIN ISCHEMIA; BRAIN MATURATION; CELL EXPANSION; CELL VACUOLE; COMPLEX FORMATION; DEGRADATION KINETICS; DISEASE SEVERITY; DRUG TARGETING; HUMAN; HYPOXIC ISCHEMIC ENCEPHALOPATHY; NERVE CELL NECROSIS; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; AUTOPHAGY; BRAIN ISCHEMIA; HUMANS; NEURONS;

EID: 84871464536     PISSN: 16737067     EISSN: 19958218     Source Type: Journal    
DOI: 10.1007/s12264-012-1268-9     Document Type: Review

References (89)

1. Kunz JB, Schwarz H, Mayer A. Determination of four sequential stages during microautophagy in vitro. J Biol Chem 2004, 279: 9987-9996. (Pubitemid 38372601)
2. Dice JF. Chaperone-mediated autophagy. Autophagy 2007, 3: 295-299. (Pubitemid 46986334)
3. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008, 451: 1069-1075. (Pubitemid 351317450)
4. Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 2007, 8: 931-937. (Pubitemid 47622558)
5. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ. Potential therapeutic applications of autophagy. Nat Rev Drug Discov 2007, 6: 304-312. (Pubitemid 46505881)
6. Wong E, Cuervo AM. Autophagy gone awry in neurodegenerative diseases. Nat Neurosci 2010, 13: 805-811.
7. Nixon RA. Autophagy in neurodegenerative disease: friend, foe or turncoat? Trends Neurosci 2006, 29: 528-535. (Pubitemid 44291816)
8. Marino G, Madeo F, Kroemer G. Autophagy for tissue homeostasis and neuroprotection. Curr Opin Cell Biol 2011, 23: 198-206.
9. Banerjee R, Beal MF, Thomas B. Autophagy in neurodegenerative disorders: pathogenic roles and therapeutic implications. Trends Neurosci 2010, 33: 541-549.
10. Zhu C, Wang X, Xu F, Bahr BA, Shibata M, Uchiyama Y, et al. The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ 2005, 12: 162-176. (Pubitemid 40220647)
11. Zhu C, Xu F, Wang X, Shibata M, Uchiyama Y, Blomgren K, et al. Different apoptotic mechanisms are activated in male and female brains after neonatal hypoxia-ischaemia. J Neurochem 2006, 96: 1016-1027.
12. Adhami F, Liao G, Morozov YM, Schloemer A, Schmithorst VJ, Lorenz JN, et al. Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy. Am J Pathol 2006, 169: 566-583. (Pubitemid 44156315)
13. Adhami F, Schloemer A, Kuan CY. The roles of autophagy in cerebral ischemia. Autophagy 2007, 3: 42-44.
14. Koike M, Shibata M, Tadakoshi M, Gotoh K, Komatsu M, Waguri S, et al. Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 2008, 172: 454-469. (Pubitemid 351282032)
15. Chu CT. Eaten alive: autophagy and neuronal cell death after hypoxia-ischemia. Am J Pathol 2008, 172: 284-287. (Pubitemid 351282016)
16. Uchiyama Y, Koike M, Shibata M. Autophagic neuron death in neonatal brain ischemia/hypoxia. Autophagy 2008, 4: 404-408. (Pubitemid 351705135)
17. Carloni S, Buonocore G, Balduini W. Protective role of autophagy in neonatal hypoxia-ischemia induced brain injury. Neurobiol Dis 2008, 32: 329-339.
18. Balduini W, Carloni S, Buonocore G. Autophagy in hypoxia-ischemia induced brain injury: evidence and speculations. Autophagy 2009, 5: 221-223.
19. Ginet V, Puyal J, Clarke PG, Truttmann AC. Enhancement of autophagic flux after neonatal cerebral hypoxia-ischemia and its region-specific relationship to apoptotic mechanisms. Am J Pathol 2009, 175: 1962-1974.
20. Nitatori T, Sato N, Waguri S, Karasawa Y, Araki H, Shibanai K, et al. Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J Neurosci 1995, 15: 1001-1011.
21. Wang JY, Xia Q, Chu KT, Pan J, Sun LN, Zeng B, et al. Severe global cerebral ischemia-induced programmed necrosis of hippocampal CA1 neurons in rat is prevented by 3-methyladenine: a widely used inhibitor of autophagy. J Neuropathol Exp Neurol 2011, 70: 314-322.
22. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol2005, 1: 112-119.
23. Rami A, Langhagen A, Steiger S. Focal cerebral ischemia induces upregulation of Beclin 1 and autophagy-like cell death. Neurobiol Dis 2008, 29: 132-141. (Pubitemid 350186114)
24. Rami A. Upregulation of Beclin 1 in the ischemic penumbra. Autophagy 2008, 4: 227-229. (Pubitemid 351231186)
25. Rami A, Kogel D. Apoptosis meets autophagy-like cell death in the ischemic penumbra: Two sides of the same coin? Autophagy 2008, 4: 422-426.
26. Wen YD, Sheng R, Zhang LS, Han R, Zhang X, Zhang XD, et al. Neuronal injury in rat model of permanent focal cerebral ischemia is associated with activation of autophagic and lysosomal pathways. Autophagy 2008, 4: 762-769.
27. Puyal J, Vaslin A, Mottier V, Clarke PG. Postischemic treatment of neonatal cerebral ischemia should target autophagy. Ann Neurol 2009, 66: 378-389.
28. Puyal J, Clarke PG. Targeting autophagy to prevent neonatal stroke damage. Autophagy 2009, 5: 1060-1061.
29. Liu C, Gao Y, Barrett J, Hu B. Autophagy and protein aggregation after brain ischemia. J Neurochem 2010, 115: 68-78.
30. Zheng YQ, Liu JX, Li XZ, Xu L, Xu YG. RNA interference-mediated downregulation of Beclin1 attenuates cerebral ischemic injury in rats. Acta Pharmacol Sin 2009, 30: 919-927.
31. Chen Y, Klionsky DJ. The regulation of autophagy - unanswered questions. J Cell Sci 2011, 124: 161-170.
32. Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, et al. ULKAtg13- FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 2009, 20: 1992-2003.
33. Ganley IG, Lam du H, 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: 12297-12305.
34. Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, et al. Nutrient-dependent mTORC1 association with the ULK1- Atg13-FIP200 complex required for autophagy. Mol Biol Cell 2009, 20: 1981-1991.
35. Mercer CA, Kaliappan A, Dennis PB. A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy 2009, 5: 649-662.
36. Funderburk SF, Wang QJ, Yue Z. The Beclin 1-VPS34 complex- at the crossroads of autophagy and beyond. Trends Cell Biol 2010, 20: 355-362.
37. Yang Z, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol 2010, 22: 124-131.
38. Matsunaga K, Saitoh T, Tabata K, Omori H, Satoh T, Kurotori N, et al. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol 2009, 11: 385-396.
39. Zhong Y, Wang QJ, Li X, Yan Y, Backer JM, Chait BT, et al. Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat Cell Biol 2009, 11: 468-476.
40. Di Bartolomeo S, Corazzari M, Nazio F, Oliverio S, Lisi G, Antonioli M, et al. The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J Cell Biol 2010, 191: 155-168.
41. Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R, et al. Ambra1 regulates autophagy and development of the nervous system. Nature 2007, 447: 1121-1125. (Pubitemid 47014434)
42. Liang C, Lee JS, Inn KS, Gack MU, Li Q, Roberts EA, et al. Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol 2008, 10: 776-787. (Pubitemid 351927707)
43. Takahashi Y, Coppola D, Matsushita N, Cualing HD, Sun M, Sato Y, et al. Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 2007, 9: 1142-1151. (Pubitemid 47500490)
44. Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol 2001, 2: 211-216. (Pubitemid 33675746)
45. Geng J, Klionsky DJ. The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep 2008, 9: 859-864.
46. Fujita N, Itoh T, Omori H, Fukuda M, Noda T, Yoshimori T. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol Biol Cell 2008, 19: 2092-2100.
47. Hanada T, Noda NN, Satomi Y, Ichimura Y, Fujioka Y, Takao T, et al. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem 2007, 282: 37298-37302.
48. Jager S, Bucci C, Tanida I, Ueno T, Kominami E, Saftig P, et al. Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci 2004, 117: 4837-4848. (Pubitemid 39433449)
49. Tanaka Y, Guhde G, Suter A, Eskelinen EL, Hartmann D, Lullmann- Rauch R, et al. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 2000, 406: 902-906. (Pubitemid 30664267)
50. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004, 15: 1101-1111. (Pubitemid 38316219)
51. 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.
52. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006, 441: 880-884.
53. Komatsu M, Wang QJ, Holstein GR, Friedrich VL Jr, 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. (Pubitemid 350010651)
54. Wang QJ, Ding Y, Kohtz DS, Mizushima N, Cristea IM, Rout MP, et al. Induction of autophagy in axonal dystrophy and degeneration. J Neurosci 2006, 26: 8057-8068. (Pubitemid 44315130)
55. Rabinowitz JD, White E. Autophagy and metabolism. Science 2010, 330: 1344-1348.
56. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009, 43: 67-93.
57. Schmelzle T, Hall MN. TOR, a central controller of cell growth. Cell 2000, 103: 253-262.
58. Alessi DR, James SR, Downes CP, Holmes AB, Gaffney PR, Reese CB, et al. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr Biol 1997, 7: 261-269. (Pubitemid 27176852)
59. Stokoe D, Stephens LR, Copeland T, Gaffney PR, Reese CB, Painter GF, et al. Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 1997, 277: 567-570. (Pubitemid 27369005)
60. Inoki K, Zhu T, Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003, 115: 577-590. (Pubitemid 37506046)
61. Manning BD, Tee AR, Logsdon MN, Blenis J, Cantley LC. 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. (Pubitemid 34876569)
62. Long X, Lin Y, Ortiz-Vega S, Yonezawa K, Avruch J. Rheb binds and regulates the mTOR kinase. Curr Biol 2005, 15: 702-713. (Pubitemid 40599924)
63. 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 hypoxia-ischemia. Autophagy 2010, 6: 366-377.
64. Liang J, Shao SH, Xu ZX, Hennessy B, Ding Z, Larrea M, et al. The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat Cell Biol 2007, 9: 218-224. (Pubitemid 46420865)
65. Hoyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol Cell 2007, 25: 193-205. (Pubitemid 46109606)
66. Wang P, Guan YF, Du H, Zhai QW, Su DF, Miao CY. Induction of autophagy contributes to the neuroprotection of nicotinamide phosphoribosyltransferase in cerebral ischemia. Autophagy 2012, 8: 77-87.
67. Oberstein A, Jeffrey PD, Shi Y. Crystal structure of the Bcl-XLBeclin 1 peptide complex: Beclin 1 is a novel BH3-only protein. J Biol Chem 2007, 282: 13123-13132. (Pubitemid 47100641)
68. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122: 927-939. (Pubitemid 41345209)
69. He C, Levine B. The Beclin 1 interactome. Curr Opin Cell Biol 2010, 22: 140-149.
70. Maiuri MC, Criollo A, Kroemer G. Crosstalk between apoptosis and autophagy within the Beclin 1 interactome. EMBO J 2010, 29: 515-516.
71. 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: 914-922. (Pubitemid 46555697)
72. Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011, 18: 571- 580.
73. Xin XY, Pan J, Wang XQ, Ma JF, Ding JQ, Yang GY, et al. 2-methoxyestradiol attenuates autophagy activation after global ischemia. Can J Neurol Sci 2011, 38: 631-638.
74. 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- 10903.
75. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P, et al. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J 2007, 26: 2527-2539. (Pubitemid 46788315)
76. Banasiak KJ, Haddad GG. Hypoxia-induced apoptosis: effect of hypoxic severity and role of p53 in neuronal cell death. Brain Res 1998, 797: 295-304. (Pubitemid 28332742)
77. Crighton D, Wilkinson S, O'Prey J, Syed N, Smith P, Harrison PR, et al. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 2006, 126: 121-134. (Pubitemid 44040988)
78. Zhang XD, Wang Y, Zhang X, Han R, Wu JC, Liang ZQ, et al. p53 mediates mitochondria dysfunction-triggered autophagy activation and cell death in rat striatum. Autophagy 2009, 5: 339-350.
79. Wang Y, Dong XX, Cao Y, Liang ZQ, Han R, Wu JC, et al. p53 induction contributes to excitotoxic neuronal death in rat striatum through apoptotic and autophagic mechanisms. Eur J Neurosci 2009, 30: 2258-2270.
80. Wu YT, Tan HL, Shui G, Bauvy C, Huang Q, Wenk MR, et al. Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J Biol Chem 2010, 285: 10850-10861.
81. 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: 482-494.
82. Northington FJ, Chavez-Valdez R, Martin LJ. Neuronal cell death in neonatal hypoxia-ischemia. Ann Neurol 2011, 69: 743-758.
83. Puyal J, Ginet V, Grishchuk Y, Truttmann AC, Clarke PG. Neuronal autophagy as a mediator of life and death: contrasting roles in chronic neurodegenerative and acute neural disorders. Neuroscientist 2012, 18: 224-236.
84. Carloni S, Carnevali A, Cimino M, Balduini W. Extended role of necrotic cell death after hypoxia-ischemia-induced neurodegeneration in the neonatal rat. Neurobiol Dis 2007, 27: 354-361. (Pubitemid 47333193)
85. Northington FJ, Zelaya ME, O'Riordan DP, Blomgren K, Flock DL, Hagberg H, et al. Failure to complete apoptosis following neonatal hypoxia-ischemia manifests as continuum phenotype of cell death and occurs with multiple manifestations of mitochondrial dysfunction in rodent forebrain. Neuroscience 2007, 149: 822-833. (Pubitemid 350130287)
86. Portera-Cailliau C, Price DL, Martin LJ. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comp Neurol 1997, 378: 70-87. (Pubitemid 27057532)
87. Nakajima W, Ishida A, Lange MS, Gabrielson KL, Wilson MA, Martin LJ, et al. Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat. J Neurosci 2000, 20: 7994-8004.
88. Sheldon RA, Hall JJ, Noble LJ, Ferriero DM. Delayed cell death in neonatal mouse hippocampus from hypoxia-ischemia is neither apoptotic nor necrotic. Neurosci Lett 2001, 304: 165-168. (Pubitemid 32436402)
89. Grishchuk Y, Ginet V, Truttmann AC, Clarke PG, Puyal J. Beclin 1-independent autophagy contributes to apoptosis in cortical neurons. Autophagy 2011, 7: 1115-1131