Oxidative stress induces autophagy in response to multiple noxious stimuli in retinal ganglion cells

Autophagy

Volumn 10, Issue 10, 2014, Pages 1692-1701

  Lin, Wen Jian ^a   Kuang, Hong Yu ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Autophagy; Axon; Mitophagy; Oxidative stress; Retinal ganglion cells

Indexed keywords

ADENYLATE KINASE; AUTOPHAGY PROTEIN 4; HYPOXIA INDUCIBLE FACTOR; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG; REACTIVE OXYGEN METABOLITE;

AUTOPHAGY; CENTRAL NERVOUS SYSTEM; HUMAN; INTRAOCULAR PRESSURE; NONHUMAN; OXIDATIVE STRESS; RETINA GANGLION CELL; REVIEW; METABOLISM; MITOPHAGY; PATHOLOGY; ULTRASTRUCTURE;

AUTOPHAGY; CENTRAL NERVOUS SYSTEM; MITOCHONDRIAL DEGRADATION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RETINAL GANGLION CELLS;

EID: 84907887343     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.36076     Document Type: Review

References (108)

1. Ren R, Li Y, Liu Z, Liu K, He S. Long-term rescue of rat retinal ganglion cells and visual function by AAV-mediated BDNF expression after acute elevation of intraocular pressure. Invest Ophthalmol Vis Sci 2012; 53:1003-11; PMID:22247466; http://dx.doi.org/10.1167/iovs.11-8484
2. Caporale N, Kolstad KD, Lee T, Tochitsky I, Dalkara D, Trauner D, Kramer R, Dan Y, Isacoff EY, Flannery JG. LiGluR restores visual responses in rodent models of inherited blindness. Mol Ther 2011; 19:1212-9; PMID:21610698; http://dx.doi.org/10.1038/mt.2011.103
3. Chen H, Chan DC. Critical dependence of neurons on mitochondrial dynamics. Curr Opin Cell Biol 2006; 18:453-9; PMID:16781135; http://dx.doi.org/10.1016/j.ceb.2006.06.004
4. Russell FD, Hamilton KD. Nutrient deprivation increases vulnerability of endothelial cells to proinflammatory insults. Free Radic Biol Med 2014; 67:408-15; PMID:24334251; http://dx.doi.org/10.1016/j.freeradbiomed.2013.12.007
5. Cimini S, Rizzardini M, Biella G, Cantoni L. Hypoxia causes autophagic stress and derangement of metabolic adaptation in a cell model of amyotrophic lateral sclerosis. J Neurochem 2014; 129:413-25; PMID:24359187; http://dx.doi.org/10.1111/jnc.12642
6. Hariharan N, Zhai P, Sadoshima J. Oxidative stress stimulates autophagic flux during ischemia/reperfusion. Antioxid Redox Signal 2011; 14:2179-90; PMID:20812860; http://dx.doi.org/10.1089/ars.2010.3488
7. Essick EE, Sam F. Oxidative stress and autophagy in cardiac disease, neurological disorders, aging and cancer. Oxid Med Cell Longev 2010; 3:168-77; PMID:20716941; http://dx.doi.org/10.4161/oxim.3.3.12106
8. She C, Zhu LQ, Zhen YF, Wang XD, Dong QR. Activation of AMPK protects against hydrogen peroxide-induced osteoblast apoptosis through autophagy induction and NADPH maintenance: new implications for osteonecrosis treatment? Cell Signal 2014; 26:1-8; PMID:24080159; http://dx.doi.org/10.1016/j.cellsig.2013.08.046
9. Lee J, Giordano S, Zhang J. Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J 2012; 441:523-40; PMID:22187934; http://dx.doi.org/10.1042/BJ20111451
10. Cao J, Ying M, Xie N, Lin G, Dong R, Zhang J, Yan H, Yang X, He Q, Yang B. The Oxidation States of DJ-1 Dictate the Cell Fate in Response to Oxidative Stress Triggered by 4-HPR: Autophagy or Apoptosis? Antioxid Redox Signal 2014; •••:; PMID:24392637; http://dx.doi.org/10.1089/ars.2013.5446
11. Jiang P, Mizushima N. Autophagy and human diseases. Cell Res 2014; 24:69-79; PMID:24323045; http://dx.doi.org/10.1038/cr.2013.161
12. Wirawan E, Vanden Berghe T, Lippens S, Agostinis P, Vandenabeele P. Autophagy: for better or for worse. Cell Res 2012; 22:43-61; PMID:21912435; http://dx.doi.org/10.1038/cr.2011.152
13. Müller M, Reichert AS. Mitophagy, mitochondrial dynamics and the general stress response in yeast. Biochem Soc Trans 2011; 39:1514-9; PMID:21936844; http://dx.doi.org/10.1042/BST0391514
14. Tanida I. Autophagosome formation and molecular mechanism of autophagy. Antioxid Redox Signal 2011; 14:2201-14; PMID:20712405; http://dx.doi.org/10.1089/ars.2010.3482
15. Oku M, Sakai Y. Peroxisomes as dynamic organelles: autophagic degradation. FEBS J 2010; 277:3289-94; PMID:20629742; http://dx.doi.org/10.1111/j.1742-4658.2010.07741.x
16. Knodler LA, Celli J. Eating the strangers within: host control of intracellular bacteria via xenophagy. Cell Microbiol 2011; 13:1319-27; PMID:21740500; http://dx.doi.org/10.1111/j.1462-5822.2011.01632.x
17. Mijaljica D, Prescott M, Devenish RJ. The intricacy of nuclear membrane dynamics during nucleophagy. Nucleus 2010; 1:213-23; PMID:21327066; http://dx.doi.org/10.4161/nucl.1.3.11738
18. Yang Z, Klionsky DJ. An overview of the molecular mechanism of autophagy. Curr Top Microbiol Immunol 2009; 335:1-32; PMID:19802558; http://dx.doi.org/10.1007/978-3-642-00302-8-1
19. Stanley RE, Ragusa MJ, Hurley JH. The beginning of the end: how scaffolds nucleate autophagosome biogenesis. Trends Cell Biol 2014; 24:73-81; PMID:23999079; http://dx.doi.org/10.1016/j.tcb.2013.07.008
20. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132:27-42; PMID:18191218; http://dx.doi.org/10.1016/j.cell.2007.12.018
21. Høyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, Bianchi K, Fehrenbacher N, Elling F, Rizzuto R, et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol Cell 2007; 25:193-205; PMID:17244528; http://dx.doi.org/10.1016/j.molcel.2006.12.009
22. Mizushima N. The pleiotropic role of autophagy: from protein metabolism to bactericide. Cell Death Differ 2005; 12(Suppl 2):1535-41; PMID:16247501; http://dx.doi.org/10.1038/sj.cdd.4401728
23. Yue Z, Friedman L, Komatsu M, Tanaka K. The cellular pathways of neuronal autophagy and their implication in neurodegenerative diseases. Biochim Biophys Acta 2009; 1793:1496-507; PMID:19339210; http://dx.doi.org/10.1016/j.bbamcr.2009.01.016
24. Martinez-Vicente M, Talloczy Z, Kaushik S, Massey AC, Mazzulli J, Mosharov EV, Hodara R, Fredenburg R, Wu DC, Follenzi A, et al. Dopamine-modified α-synuclein blocks chaperone-mediated autophagy. J Clin Invest 2008; 118:777-88; PMID:18172548; http://dx.doi.org/10.1172/JCI3280
25. Xilouri M, Vogiatzi T, Vekrellis K, Park D, Stefanis L. Abberant alpha-synuclein confers toxicity to neurons in part through inhibition of chaperonemediated autophagy. PLoS One 2009; 4:e5515; PMID:19436756; http://dx.doi.org/10.1371/journal.pone.0005515
26. Nixon RA. Autophagy, amyloidogenesis and Alzheimer disease. J Cell Sci 2007; 120:4081-91; PMID:18032783; http://dx.doi.org/10.1242/jcs.019265
27. Boland B, Kumar A, Lee S, Platt FM, Wegiel J, Yu WH, Nixon RA. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J Neurosci 2008; 28:6926-37; PMID:18596167; http://dx.doi.org/10.1523/JNEUROSCI.0800-08.2008
28. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF, Duden R, O'Kane CJ, 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
29. Ravikumar B, Duden R, Rubinsztein DC. Aggregateprone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum Mol Genet 2002; 11:1107-17; PMID:11978769; http://dx.doi.org/10.1093/hmg/11.9.1107
30. Zhu C, Wang X, Xu F, Bahr BA, Shibata M, Uchiyama Y, Hagberg H, Blomgren K. The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ 2005; 12:162-76; PMID:15592434; http://dx.doi.org/10.1038/sj.cdd.4401545
31. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, Cuny GD, Mitchison TJ, Moskowitz MA, Yuan J. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 2005; 1:112-9; PMID:16408008; http://dx.doi.org/10.1038/nchembio711
32. Wen YD, Sheng R, Zhang LS, Han R, Zhang X, Zhang XD, Han F, Fukunaga K, Qin ZH. Neuronal injury in rat model of permanent focal cerebral ischemia is associated with activation of autophagic and lysosomal pathways. Autophagy 2008; 4:762-9; PMID:18567942; http://dx.doi.org/10.4161/auto.6412
33. Puyal J, Vaslin A, Mottier V, Clarke PG. Postischemic treatment of neonatal cerebral ischemia should target autophagy. Ann Neurol 2009; 66:378-89; PMID:19551849; http://dx.doi.org/10.1002/ana.21714
34. Borsello T, Croquelois K, Hornung JP, Clarke PG. N-methyl-d-aspartate-triggered neuronal death in organotypic hippocampal cultures is endocytic, autophagic and mediated by the c-Jun N-terminal kinase pathway. Eur J Neurosci 2003; 18:473-85; PMID:12911744; http://dx.doi.org/10.1046/j.1460-9568.2003.02757.x
35. Guimarães CA, Benchimol M, Amarante-Mendes GP, Linden R. Alternative programs of cell death in developing retinal tissue. J Biol Chem 2003; 278:41938-46; PMID:12917395; http://dx.doi.org/10.1074/jbc.M306547200
36. Larsen KE, Fon EA, Hastings TG, Edwards RH, Sulzer D. Methamphetamine-induced degeneration of dopaminergic neurons involves autophagy and upregulation of dopamine synthesis. J Neurosci 2002; 22:8951-60; PMID:12388602
37. Erlich S, Alexandrovich A, Shohami E, Pinkas-Kramarski R. Rapamycin is a neuroprotective treatment for traumatic brain injury. Neurobiol Dis 2007; 26:86-93; PMID:17270455; http://dx.doi.org/10.1016/j.nbd.2006.12.003
38. Erlich S, Shohami E, Pinkas-Kramarski R. Neurodegeneration induces upregulation of Beclin 1. Autophagy 2006; 2:49-51; PMID:16874043; http://dx.doi.org/10.4161/auto.2156
39. Adhami F, Liao G, Morozov YM, Schloemer A, Schmithorst VJ, Lorenz JN, Dunn RS, Vorhees CV, Wills-Karp M, Degen JL, et al. Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy. Am J Pathol 2006; 169:566-83; PMID:16877357; http://dx.doi.org/10.2353/ajpath.2006.051066
40. Tian F, Deguchi K, Yamashita T, Ohta Y, Morimoto N, Shang J, Zhang X, Liu N, Ikeda Y, Matsuura T, et al. In vivo imaging of autophagy in a mouse stroke model. Autophagy 2010; 6:1107-14; PMID:20930570; http://dx.doi.org/10.4161/auto.6.8.13427
41. He S, Wang C, Dong H, Xia F, Zhou H, Jiang X, Pei C, Ren H, Li H, Li R, et al. Immune-related GTPase M (IRGM1) regulates neuronal autophagy in a mouse model of stroke. Autophagy 2012; 8:1621-7; PMID:22874556; http://dx.doi.org/10.4161/auto.21561
42. 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; 18:224-36; PMID:21525331; http://dx.doi.org/10.1177/1073858411404948
43. Pandey UB, Nie Z, Batlevi Y, McCray BA, Ritson GP, Nedelsky NB, Schwartz SL, DiProspero NA, Knight MA, Schuldiner O, et al. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 2007; 447:859-63; PMID:17568747; http://dx.doi.org/10.1038/nature05853
44. Yang DS, Stavrides P, Mohan PS, Kaushik S, Kumar A, Ohno M, Schmidt SD, Wesson D, Bandyopadhyay U, Jiang Y, et al. Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain 2011; 134:258-77; PMID:21186265; http://dx.doi.org/10.1093/brain/awq341
45. Koike M, Shibata M, Tadakoshi M, Gotoh K, Komatsu M, Waguri S, Kawahara N, Kuida K, Nagata S, Kominami E, et al. Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 2008; 172:454-69; PMID:18187572; http://dx.doi.org/10.2353/ajpath.2008.070876
46. Bernstein SL, Guo Y, Kelman SE, Flower RW, Johnson MA. Functional and cellular responses in a novel rodent model of anterior ischemic optic neuropathy. Invest Ophthalmol Vis Sci 2003; 44:4153-62; PMID:14507856; http://dx.doi.org/10.1167/iovs.03-0274
47. Guillot-Sestier MV, Sunyach C, Druon C, Scarzello S, Checler F. The alpha-secretase-derived N-terminal product of cellular prion, N1, displays neuroprotective function in vitro and in vivo. J Biol Chem 2009; 284:35973-86; PMID:19850936; http://dx.doi.org/10.1074/jbc.M109.051086
48. Russo R, Berliocchi L, Adornetto A, Varano GP, Cavaliere F, Nucci C, Rotiroti D, Morrone LA, Bagetta G, Corasaniti MT. Calpain-mediated cleavage of Beclin-1 and autophagy deregulation following retinal ischemic injury in vivo. Cell Death Dis 2011; 2:e144; PMID:21490676; http://dx.doi.org/10.1038/cddis.2011.29
49. Park HY, Kim JH, Park CK. Activation of autophagy induces retinal ganglion cell death in a chronic hypertensive glaucoma model. Cell Death Dis 2012; 3:e290; PMID:22476098; http://dx.doi.org/10.1038/cddis.2012.26
50. Piras A, Gianetto D, Conte D, Bosone A, Vercelli A. Activation of autophagy in a rat model of retinal ischemia following high intraocular pressure. PLoS One 2011; 6:e22514; PMID:21799881; http://dx.doi.org/10.1371/journal.pone.0022514
51. Sternberg C, Benchimol M, Linden R. Caspase dependence of the death of neonatal retinal ganglion cells induced by axon damage and induction of autophagy as a survival mechanism. Braz J Med Biol Res 2010; 43:950-6; PMID:20802972; http://dx.doi.org/10.1590/S0100-879X2010007500082
52. Kim SH, Munemasa Y, Kwong JM, Ahn JH, Mareninov S, Gordon LK, Caprioli J, Piri N. Activation of autophagy in retinal ganglion cells. J Neurosci Res 2008; 86:2943-51; PMID:18521932; http://dx.doi.org/10.1002/jnr.21738
53. Rodríguez-Muela N, Germain F, Mariño G, Fitze PS, Boya P. Autophagy promotes survival of retinal ganglion cells after optic nerve axotomy in mice. Cell Death Differ 2012; 19:162-9; PMID:21701497; http://dx.doi.org/10.1038/cdd.2011.88
54. Knöferle J, Koch JC, Ostendorf T, Michel U, Planchamp V, Vutova P, Tönges L, Stadelmann C, Brück W, Bähr M, et al. Mechanisms of acute axonal degeneration in the optic nerve in vivo. Proc Natl Acad Sci U S A 2010; 107:6064-9; PMID:20231460; http://dx.doi.org/10.1073/pnas.0909794107
55. Rubinsztein DC, DiFiglia M, Heintz N, Nixon RA, Qin ZH, Ravikumar B, Stefanis L, Tolkovsky A. Autophagy and its possible roles in nervous system diseases, damage and repair. Autophagy 2005; 1:11-22; PMID:16874045; http://dx.doi.org/10.4161/auto.1.1.1513
56. Dixon JS. "Phagocytic" lysosomes in chromatolytic neurones. Nature 1967; 215:657-8; PMID:6050233; http://dx.doi.org/10.1038/215657a0
57. Matthews MR, Raisman G. A light and electron microscopic study of the cellular response to axonal injury in the superior cervical ganglion of the rat. Proc R Soc Lond B Biol Sci 1972; 181:43-79; PMID:4402334; http://dx.doi.org/10.1098/rspb.1972.0040
58. Zherebitskaya E, Akude E, Smith DR, Fernyhough P. Development of selective axonopathy in adult sensory neurons isolated from diabetic rats: role of glucoseinduced oxidative stress. Diabetes 2009; 58:1356-64; PMID:19252136; http://dx.doi.org/10.2337/db09-0034
59. Almasieh M, Wilson AM, Morquette B, Cueva Vargas JL, Di Polo A. The molecular basis of retinal ganglion cell death in glaucoma. Prog Retin Eye Res 2012; 31:152-81; PMID:22155051; http://dx.doi.org/10.1016/j.preteyeres.2011.11.002
60. Hein TW, Ren Y, Potts LB, Yuan Z, Kuo E, Rosa RH Jr., Kuo L. Acute retinal ischemia inhibits endothelium-dependent nitric oxide-mediated dilation of retinal arterioles via enhanced superoxide production. Invest Ophthalmol Vis Sci 2012; 53:30-6; PMID:22110081; http://dx.doi.org/10.1167/iovs.11-8753
61. Zhu C, Xu F, Wang X, Shibata M, Uchiyama Y, Blomgren K, Hagberg H. Different apoptotic mechanisms are activated in male and female brains after neonatal hypoxia-ischaemia. J Neurochem 2006; 96:1016-27; PMID:16412092; http://dx.doi.org/10.1111/j.1471-4159.2005.03639.x
62. Adhami F, Schloemer A, Kuan CY. The roles of autophagy in cerebral ischemia. Autophagy 2007; 3:42-4; PMID:17035724; http://dx.doi.org/10.4161/auto.3412
63. Levine B, Yuan J. Autophagy in cell death: an innocent convict? J Clin Invest 2005; 115:2679-88; PMID:16200202; http://dx.doi.org/10.1172/JCI26390
64. Fitzgerald M, Bartlett CA, Payne SC, Hart NS, Rodger J, Harvey AR, Dunlop SA. Near infrared light reduces oxidative stress and preserves function in CNS tissue vulnerable to secondary degeneration following partial transection of the optic nerve. J Neurotrauma 2010; 27:2107-19; PMID:20822460; http://dx.doi.org/10.1089/neu.2010.1426
65. Sayir F, Kavak S, Meral I, Demir H, Cengiz N, Cobanoʇlu U. Effects of crush and axotomy on oxidative stress and some trace element levels in phrenic nerve of rats. Brain Res Bull 2013; 92:84-8; PMID:21803127; http://dx.doi.org/10.1016/j.brainresbull.2011.07.013
66. Fitzgerald M, Payne SC, Bartlett CA, Evill L, Harvey AR, Dunlop SA. Secondary retinal ganglion cell death and the neuroprotective effects of the calcium channel blocker lomerizine. Invest Ophthalmol Vis Sci 2009; 50:5456-62; PMID:19474405; http://dx.doi.org/10.1167/iovs.09-3717
67. Fitzgerald M, Bartlett CA, Harvey AR, Dunlop SA. Early events of secondary degeneration after partial optic nerve transection: an immunohistochemical study. J Neurotrauma 2010; 27:439-52; PMID:19852581; http://dx.doi.org/10.1089/neu.2009.1112
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; PMID:17347651; http://dx.doi.org/10.1038/sj.emboj.7601623
69. Yoshimura K, Shibata M, Koike M, Gotoh K, Fukaya M, Watanabe M, Uchiyama Y. Effects of RNA interference of Atg4B on the limited proteolysis of LC3 in PC12 cells and expression of Atg4B in various rat tissues. Autophagy 2006; 2:200-8; PMID:16874114; http://dx.doi.org/10.4161/auto.2744
70. Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 1995; 270:1230-7; PMID:7836384; http://dx.doi.org/10.1074/jbc.270.3.1230
71. Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A 1995; 92:5510-4; PMID:7539918; http://dx.doi.org/10.1073/pnas.92.12.5510
72. Ali YO, McCormack R, Darr A, Zhai RG. Nicotinamide mononucleotide adenylyltransferase is a stress response protein regulated by the heat shock factor/hypoxia-inducible factor 1α pathway. J Biol Chem 2011; 286:19089-99; PMID:21478149; http://dx.doi.org/10.1074/jbc.M111.219295
73. Zhai RG, Cao Y, Hiesinger PR, Zhou Y, Mehta SQ, Schulze KL, Verstreken P, Bellen HJ. Drosophila NMNAT maintains neural integrity independent of its NAD synthesis activity. PLoS Biol 2006; 4:e416; PMID:17132048; http://dx.doi.org/10.1371/journal.pbio.0040416
74. Zhai RG, Zhang F, Hiesinger PR, Cao Y, Haueter CM, Bellen HJ. NAD synthase NMNAT acts as a chaperone to protect against neurodegeneration. Nature 2008; 452:887-91; PMID:18344983; http://dx.doi.org/10.1038/nature06721
75. MacDonald JM, Beach MG, Porpiglia E, Sheehan AE, Watts RJ, Freeman MR. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 2006; 50:869-81; PMID:16772169; http://dx.doi.org/10.1016/j.neuron.2006.04.028
76. Sasaki Y, Vohra BP, Lund FE, Milbrandt J. Nicotinamide mononucleotide adenylyl transferase-mediated axonal protection requires enzymatic activity but not increased levels of neuronal nicotinamide adenine dinucleotide. J Neurosci 2009; 29:5525-35; PMID:19403820; http://dx.doi.org/10.1523/JNEUROSCI.5469-08.2009
77. Yan T, Feng Y, Zheng J, Ge X, Zhang Y, Wu D, Zhao J, Zhai Q. Nmnat2 delays axon degeneration in superior cervical ganglia dependent on its NAD synthesis activity. Neurochem Int 2010; 56:101-6; PMID:19778564; http://dx.doi.org/10.1016/j.neuint.2009.09.007
78. Gilley J, Coleman MP. Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol 2010; 8:e1000300; PMID:20126265; http://dx.doi.org/10.1371/journal.pbio.1000300
79. Press C, Milbrandt J. Nmnat delays axonal degeneration caused by mitochondrial and oxidative stress. J Neurosci 2008; 28:4861-71; PMID:18463239; http://dx.doi.org/10.1523/JNEUROSCI.0525-08.2008
80. Berger F, Lau C, Dahlmann M, Ziegler M. Subcellular compartmentation and differential catalytic properties of the three human nicotinamide mononucleotide adenylyltransferase isoforms. J Biol Chem 2005; 280:36334-41; PMID:16118205; http://dx.doi.org/10.1074/jbc.M508660200
81. Kitaoka Y, Munemasa Y, Kojima K, Hirano A, Ueno S, Takagi H. Axonal protection by Nmnat3 overexpression with involvement of autophagy in optic nerve degeneration. Cell Death Dis 2013; 4:e860; PMID:24136224; http://dx.doi.org/10.1038/cddis.2013.391
82. Lee Y, Kim EK. AMP-activated protein kinase as a key molecular link between metabolism and clockwork. Exp Mol Med 2013; 45:e33; PMID:23887727; http://dx.doi.org/10.1038/emm.2013.65
83. Rubinsztein DC, Mariño G, Kroemer G. Autophagy and aging. Cell 2011; 146:682-95; PMID:21884931; http://dx.doi.org/10.1016/j.cell.2011.07.030
84. Avruch J, Long X, Lin Y, Ortiz-Vega S, Rapley J, Papageorgiou A, Oshiro N, Kikkawa U. Activation of mTORC1 in two steps: Rheb-GTP activation of catalytic function and increased binding of substrates to raptor. Biochem Soc Trans 2009; 37:223-6; PMID:19143636; http://dx.doi.org/10.1042/BST0370223
85. Poels J, Spasić MR, Callaerts P, Norga KK. Expanding roles for AMP-activated protein kinase in neuronal survival and autophagy. Bioessays 2009; 31:944-52; PMID:19644919; http://dx.doi.org/10.1002/bies.200900003
86. Steinberg GR, Kemp BE. AMPK in health and disease. Physiol Rev 2009; 89:1025-78; PMID:19584320; http://dx.doi.org/10.1152/physrev.00011.2008
87. Wang Y, Nartiss Y, Steipe B, McQuibban GA, Kim PK. ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy. Autophagy 2012; 8:1462-76; PMID:22889933; http://dx.doi.org/10.4161/auto.21211
88. Schweers RL, Zhang J, Randall MS, Loyd MR, Li W, Dorsey FC, Kundu M, Opferman JT, Cleveland JL, Miller JL, et al. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci U S A 2007; 104:19500-5; PMID:18048346; http://dx.doi.org/10.1073/pnas.0708818104
89. 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; PMID:17576813; http://dx.doi.org/10.1128/MCB.02246-06
90. 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; PMID:19029340; http://dx.doi.org/10.1083/jcb.200809125
91. Mowat FM, Luhmann UF, Smith AJ, Lange C, Duran Y, Harten S, Shukla D, Maxwell PH, Ali RR, Bainbridge JW. HIF-1alpha and HIF-2alpha are differentially activated in distinct cell populations in retinal ischaemia. PLoS One 2010; 5:e11103; PMID:20559438; http://dx.doi.org/10.1371/journal.pone.0011103
92. Scherz-Shouval R, Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci 2011; 36:30-8; PMID:20728362; http://dx.doi.org/10.1016/j.tibs.2010.07.007
93. Naves T, Jawhari S, Jauberteau MO, Ratinaud MH, Verdier M. Autophagy takes place in mutated p53 neuroblastoma cells in response to hypoxia mimetic CoCl(2). Biochem Pharmacol 2013; 85:1153-61; PMID:23380477; http://dx.doi.org/10.1016/j.bcp.2013.01.022
94. Yang L, Tan P, Zhou W, Zhu X, Cui Y, Zhu L, Feng X, Qi H, Zheng J, Gu P, et al. N-acetylcysteine protects against hypoxia mimetic-induced autophagy by targeting the HIF-1α pathway in retinal ganglion cells. Cell Mol Neurobiol 2012; 32:1275-85; PMID:22618532; http://dx.doi.org/10.1007/s10571-012-9852-0
95. Zhu X, Zhou W, Cui Y, Zhu L, Li J, Feng X, Shao B, Qi H, Zheng J, Wang H, et al. Pilocarpine protects cobalt chloride-induced apoptosis of RGC-5 cells: involvement of muscarinic receptors and HIF-1 α pathway. Cell Mol Neurobiol 2010; 30:427-35; PMID:19816768; http://dx.doi.org/10.1007/s10571-009-9467-2
96. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, Cookson MR, Youle RJ. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 2010; 8:e1000298; PMID:20126261; http://dx.doi.org/10.1371/journal.pbio.1000298
97. Matsuda N, Sato S, Shiba K, Okatsu K, Saisho K, Gautier CA, Sou YS, Saiki S, Kawajiri S, Sato F, et al. PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J Cell Biol 2010; 189:211-21; PMID:20404107; http://dx.doi.org/10.1083/jcb.200910140
98. Ziviani E, Tao RN, Whitworth AJ. Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc Natl Acad Sci U S A 2010; 107:5018-23; PMID:20194754; http://dx.doi.org/10.1073/pnas.0913485107
99. Park J, Kim Y, Chung J. Mitochondrial dysfunction and Parkinson's disease genes: insights from Drosophila. Dis Model Mech 2009; 2:336-40; PMID:19553694; http://dx.doi.org/10.1242/dmm.003178
100. Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RL, Kim J, May J, Tocilescu MA, Liu W, Ko HS, et al. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci U S A 2010; 107:378-83; PMID:19966284; http://dx.doi.org/10.1073/pnas.0911187107
101. Wang HL, Chou AH, Wu AS, Chen SY, Weng YH, Kao YC, Yeh TH, Chu PJ, Lu CS. PARK6 PINK1 mutants are defective in maintaining mitochondrial membrane potential and inhibiting ROS formation of substantia nigra dopaminergic neurons. Biochim Biophys Acta 2011; 1812:674-84; PMID:21421046; http://dx.doi.org/10.1016/j.bbadis.2011.03.007
102. Horowitz JM, Myers J, Stachowiak MK, Torres G. Identification and distribution of Parkin in rat brain. Neuroreport 1999; 10:3393-7; PMID:10599851; http://dx.doi.org/10.1097/00001756-199911080-00025
103. Shimura H, Hattori N, Kubo S, Yoshikawa M, Kitada T, Matsumine H, Asakawa S, Minoshima S, Yamamura Y, Shimizu N, et al. Immunohistochemical and subcellular localization of Parkin protein: absence of protein in autosomal recessive juvenile parkinsonism patients. Ann Neurol 1999; 45:668-72; PMID:10319893; http://dx.doi.org/10.1002/1531-8249(199905)45:5〈668::AID-ANA19〉3.0.CO;2-Z
104. Stichel CC, Augustin M, Kühn K, Zhu XR, Engels P, Ullmer C, Lübbert H. Parkin expression in the adult mouse brain. Eur J Neurosci 2000; 12:4181-94; PMID:11122330; http://dx.doi.org/10.1111/j.1460-9568.2000.01314.x
105. Zarate-Lagunes M, Gu WJ, Blanchard V, Francois C, Muriel MP, Mouatt-Prigent A, Bonici B, Parent A, Hartmann A, Yelnik J, et al. Parkin immunoreactivity in the brain of human and non-human primates: an immunohistochemical analysis in normal conditions and in Parkinsonian syndromes. J Comp Neurol 2001; 432:184-96; PMID:11241385; http://dx.doi.org/10.1002/cne.1096
106. Esteve-Rudd J, Campello L, Herrero MT, Cuenca N, Martín-Nieto J. Expression in the mammalian retina of parkin and UCH-L1, two components of the ubiquitin-proteasome system. Brain Res 2010; 1352:70-82; PMID:20638372; http://dx.doi.org/10.1016/j.brainres.2010.07.019
107. Cai Q, Zakaria HM, Sheng ZH. Long time-lapse imaging reveals unique features of PARK2/Parkinmediated mitophagy in mature cortical neurons. Autophagy 2012; 8:976-8; PMID:22739253; http://dx.doi.org/10.4161/auto.20218
108. Joselin AP, Hewitt SJ, Callaghan SM, Kim RH, Chung YH, Mak TW, Shen J, Slack RS, Park DS. ROS-dependent regulation of Parkin and DJ-1 localization during oxidative stress in neurons. Hum Mol Genet 2012; 21:4888-903; PMID:22872702; http://dx.doi.org/10.1093/hmg/dds325