Autophagy in hemorrhagic stroke: Mechanisms and clinical implications

Progress in Neurobiology

Volumn 163-164, Issue , 2018, Pages 79-97

  Li, Haiying ^a   Wu, Jiang ^a   Shen, Haitao ^a   Yao, Xiyang ^a   Liu, Chenglin ^a   Pianta, S ^b   Han, J ^b   Borlongan, C V ^b   Chen, Gang ^a  

^a THE FIRST AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Autophagic flux; Autophagy; Hemorrhagic stroke

Indexed keywords

AUTOPHAGY RELATED PROTEIN; CASPASE; CELL PROTEIN; FERRITIN; INFLAMMASOME;

APOPTOSIS; ASTROCYTE; AUTOPHAGOSOME; AUTOPHAGY; BRAIN CELL; BRAIN HEMORRHAGE; BRAIN INJURY; BRAIN ISCHEMIA; CAPILLARY ENDOTHELIAL CELL; CELL DEATH; ENDOPLASMIC RETICULUM STRESS; FERRITINOPHAGY; HUMAN; INFLAMMATION; KNOCKOUT MOUSE; MICROGLIA; MITOPHAGY; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN SECRETION; REVIEW; SELECTIVE AUTOPHAGY; SUBARACHNOID HEMORRHAGE; ANIMAL; CEREBROVASCULAR ACCIDENT; DRUG EFFECT; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; AUTOPHAGY; CEREBRAL HEMORRHAGE; HUMANS; STROKE;

EID: 85018642857     PISSN: 03010082     EISSN: 18735118     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2017.04.002     Document Type: Review

References (235)

1. Acaz-Fonseca, E., Avila-Rodriguez, M., Garcia-Segura, L.M., Barreto, G.E., Regulation of astroglia by gonadal steroid hormones under physiological and pathological conditions. Prog. Neurobiol. 144 (2016), 5–26.
2. Adhami, F., Liao, G., Morozov, Y.M., Schloemer, A., Schmithorst, V.J., Lorenz, J.N., Dunn, R.S., Vorhees, C.V., Wills-Karp, M., Degen, J.L., Davis, R.J., Mizushima, N., Rakic, P., Dardzinski, B.J., Holland, S.K., Sharp, F.R., Kuan, C.Y., Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy. Am. J. Pathol. 169 (2006), 566–583.
3. Agostini, M., Tucci, P., Melino, G., Cell death pathology: perspective for human diseases. Biochem. Biophys. Res. Commun. 414 (2011), 451–455.
4. Alers, S., Loffler, A.S., Wesselborg, S., Stork, B., Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk shortcuts, and feedbacks. Mol. Cell. Biol. 32 (2012), 2–11.
5. Alnemri, E.S., Sensing cytoplasmic danger signals by the inflammasome. J. Clin. Immunol. 30 (2010), 512–519.
6. Althaus, J., Bernaudin, M., Petit, E., Toutain, J., Touzani, O., Rami, A., Expression of the gene encoding the pro-apoptotic BNIP3 protein and stimulation of hypoxia-inducible factor-1alpha (HIF-1alpha) protein following focal cerebral ischemia in rats. Neurochem. Int. 48 (2006), 687–695.
7. Arbo, B.D., Bennetti, F., Ribeiro, M.F., Astrocytes as a target for neuroprotection: modulation by progesterone and dehydroepiandrosterone. Prog. Neurobiol. 144 (2016), 27–47.
8. Ariosa, A.R., Klionsky, D.J., Autophagy core machinery: overcoming spatial barriers in neurons. J. Mol. Med., 2016, 1–11.
9. Aronowski, J., Strong, R., Grotta, J.C., Reperfusion injury: demonstration of brain damage produced by reperfusion after transient focal ischemia in rats. J. Cereb. Blood Flow Metab. 17 (1997), 1048–1056.
10. Arroyo, D.S., Soria, J.A., Gaviglio, E.A., Garcia-Keller, C., Cancela, L.M., Rodriguez-Galan, M.C., Wang, J.M., Iribarren, P., Toll-like receptor 2 ligands promote microglial cell death by inducing autophagy. FASEB J. 27 (2013), 299–312.
11. Bacher, A., Zornow, M.H., Lamotrigine inhibits extracellular glutamate accumulation during transient global cerebral ischemia in rabbits. Anesthesiology 86 (1997), 459–463.
12. Bakhshayesh, B., Hosseininezhad, M., Saadat, S.N., Ansar, M.M., Ramezani, H., Saadat, S.M., Iron overload is associated with perihematoma edema growth following intracerebral hemorrhage that may contribute to in-hospital mortality and long-term functional outcome. Curr. Neurovasc. Res. 11 (2014), 248–253.
13. Balduini, W., Carloni, S., Buonocore, G., Autophagy in hypoxia-ischemia induced brain injury: evidence and speculations. Autophagy 5 (2009), 221–223.
14. Balduini, W., Carloni, S., Buonocore, G., Autophagy in hypoxia-ischemia induced brain injury. J. Matern. Fetal Neonatal Med. 25:Suppl. 1 (2012), 30–34.
15. Baltan, S., Murphy, S.P., Danilov, C.A., Bachleda, A., Morrison, R.S., Histone deacetylase inhibitors preserve white matter structure and function during ischemia by conserving ATP and reducing excitotoxicity. J. Neurosci. 31 (2011), 3990–3999.
16. Baltan, S., Age-specific localization of NMDA receptors on oligodendrocytes dictates axon function recovery after ischemia. Neuropharmacology 110 (2016), 626–632.
17. Barreto, G.E., Targeting astrocytes in brain injuries: a translational research approach. Prog. Neurobiol. 144 (2016), 1–4.
18. Baxter, P., Chen, Y., Xu, Y., Swanson, R.A., Mitochondrial dysfunction induced by nuclear poly(ADP-ribose) polymerase-1: a treatable cause of cell death in stroke. Transl. Stroke Res. 5 (2014), 136–144.
19. Belanger, M., Allaman, I., Magistretti, P.J., Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 14 (2011), 724–738.
20. Bjørkøy, G.1, Lamark, T., Pankiv, S., Øvervatn, A., Brech, A., Johansen, T., Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol. 452 (2009), 181–197.
21. Bruder, M., Schuss, P., Berkefeld, J., Wagner, M., Vatter, H., Seifert, V., Guresir, E., Subarachnoid hemorrhage and intracerebral hematoma caused by aneurysms of the anterior circulation: influence of hematoma localization on outcome. Neurosurg. Rev. 37 (2014), 653–659.
22. Cao, L., Walker, M.P., Vaidya, N.K., Fu, M., Kumar, S., Kumar, A., Cocaine-mediated autophagy in astrocytes involves Sigma 1 receptor PI3K, mTOR, Atg5/7, Beclin-1 and induces type ii programed cell death. Mol. Neurobiol. 53 (2016), 4417–4430.
23. Carloni, S., Buonocore, G., Balduini, W., Protective role of autophagy in neonatal hypoxia-ischemia induced brain injury. Neurobiol. Dis. 32 (2008), 329–339.
24. 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 6 (2010), 366–377.
25. Cebollero, E., Reggiori, F., Kraft, C., Reticulophagy and ribophagy: regulated degradation of protein production factories. Int. J. Cell Biol., 2012, 2012, 182834.
26. Chang, P., Dong, W., Zhang, M., Wang, Z., Wang, Y., Wang, T., Gao, Y., Meng, H., Luo, B., Luo, C., Chen, X., Tao, L., Anti-necroptosis chemical necrostatin-1 can also suppress apoptotic and autophagic pathway to exert neuroprotective effect in mice intracerebral hemorrhage model. J. Mol. Neurosci. 52 (2014), 242–249.
27. Chen, C.W., Chen, T.Y., Tsai, K.L., Lin, C.L., Yokoyama, K.K., Lee, W.S., Chiueh, C.C., Hsu, C., Inhibition of autophagy as a therapeutic strategy of iron-induced brain injury after hemorrhage. Autophagy 8 (2012), 1510–1520.
28. Chen, F., Qi, Z., Luo, Y., Hinchliffe, T., Ding, G., Xia, Y., Ji, X., Non-pharmaceutical therapies for stroke: mechanisms and clinical implications. Prog. Neurobiol. 115 (2014), 246–269.
29. Chen, J., Wang, L., Wu, C., Hu, Q., Gu, C., Yan, F., Li, J., Yan, W., Chen, G., Melatonin-enhanced autophagy protects against neural apoptosis via a mitochondrial pathway in early brain injury following a subarachnoid hemorrhage. J. Pineal Res. 56 (2014), 12–19.
30. Chen, P., Cescon, M., Bonaldo, P., Autophagy-mediated regulation of macrophages and its applications for cancer. Autophagy 10 (2014), 192–200.
31. Chen, W., Sun, Y., Liu, K., Sun, X., Autophagy: a double-edged sword for neuronal survival after cerebral ischemia. Neural Regen. Res. 9 (2014), 1210–1216.
32. Chen, S., Wu, H., Tang, J., Zhang, J., Zhang, J.H., Neurovascular events after subarachnoid hemorrhage: focusing on subcellular organelles. Acta Neurochir. Suppl. 120 (2015), 39–46.
33. Chen, N., Dai, L., Jiang, Y., Wang, J., Hao, H., Ren, Y., Leng, X., Zang, L., Wu, Y., Endoplasmic reticulum stress intolerance in EIF2B3 mutant oligodendrocytes is modulated by depressed autophagy. Brain Dev. 38 (2016), 507–515.
34. Cho, M.H., Cho, K., Kang, H.J., Jeon, E.Y., Kim, H.S., Kwon, H.J., Kim, H.M., Kim, D.H., Yoon, S.Y., Autophagy in microglia degrades extracellular beta-amyloid fibrils and regulates the NLRP3 inflammasome. Autophagy 10 (2014), 1761–1775.
35. Chowen, J.A., Argente-Arizon, P., Freire-Regatillo, A., Frago, L.M., Horvath, T.L., Argente, J., The role of astrocytes in the hypothalamic response and adaptation to metabolic signals. Prog. Neurobiol. 144 (2016), 68–87.
36. Cui, Y., Duan, X., Li, H., Dang, B., Yin, J., Wang, Y., Gao, A., Yu, Z., Chen, G., Hydrogen sulfide ameliorates early brain injury following subarachnoid hemorrhage in rats. Mol. Neurobiol. 53 (2016), 3646–3657.
37. Curcio, M., Salazar, I.L., Mele, M., Canzoniero, L.M., Duarte, C.B., Calpains and neuronal damage in the ischemic brain: the swiss knife in synaptic injury. Prog. Neurobiol. 143 (2016), 1–35.
38. Cutting, A.S., Del Rosario, Y., Mu, R., Rodriguez, A., Till, A., Subramani, S., Gottlieb, R.A., Doran, K.S., The role of autophagy during group B Streptococcus infection of blood-brain barrier endothelium. J. Biol. Chem. 289 (2014), 35711–35723.
39. Dallerac, G., Rouach, N., Astrocytes as new targets to improve cognitive functions. Prog. Neurobiol. 144 (2016), 48–67.
40. Dang, B., Li, H., Xu, X., Shen, H., Wang, Y., Gao, A., He, W., Wang, Z., Chen, G., Cyclophilin A/cluster of differentiation 147 interactions participate in early brain injury after subarachnoid hemorrhage in rats. Crit. Care Med. 43 (2015), e369–381.
41. Davis, C.H., Kim, K.Y., Bushong, E.A., Mills, E.A., Boassa, D., Shih, T., Kinebuchi, M., Phan, S., Zhou, Y., Bihlmeyer, N.A., Nguyen, J.V., Jin, Y., Ellisman, M.H., Marsh-Armstrong, N., Transcellular degradation of axonal mitochondria. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 9633–9638.
42. De Meyer, G.R., Grootaert, M.O., Michiels, C.F., Kurdi, A., Schrijvers, D.M., Martinet, W., Autophagy in vascular disease. Circ. Res. 116 (2015), 468–479.
43. Del Grosso, A., Antonini, S., Angella, L., Tonazzini, I., Signore, G., Cecchini, M., Lithium improves cell viability in psychosine-treated MO3.13 human oligodendrocyte cell line via autophagy activation. J. Neurosci. Res. 94 (2016), 1246–1260.
44. Deretic, V., Jiang, S., Dupont, N., Autophagy intersections with conventional and unconventional secretion in tissue development, remodeling and inflammation. Trends Cell Biol. 22 (2012), 397–406.
45. Di Malta, C., Fryer, J.D., Settembre, C., Ballabio, A., Autophagy in astrocytes: a novel culprit in lysosomal storage disorders. Autophagy 8 (2012), 1871–1872.
46. Dong, Y., Li, Y., Feng, D., Wang, J., Wen, H., Liu, D., Zhao, D., Liu, H., Gao, G., Yin, Z., Qin, H., Protective effect of HIF-1alpha against hippocampal apoptosis and cognitive dysfunction in an experimental rat model of subarachnoid hemorrhage. Brain Res. 1517 (2013), 114–121.
47. Dunlop, E.A., Tee, A.R., mTOR and autophagy: a dynamic relationship governed by nutrients and energy. Semin. Cell Dev. Biol. 36 (2014), 121–129.
48. Edinger, A.L., Thompson, C.B., Death by design: apoptosis: necrosis and autophagy. Curr. Opin. Cell Biol. 16 (2004), 663–669.
49. Esteban-Martinez, L., Boya, P., Autophagic flux determination in vivo and ex vivo. Methods 75 (2015), 79–86.
50. Fang, L., Li, X., Zhong, Y., Yu, J., Yu, L., Dai, H., Yan, M., Autophagy protects human brain microvascular endothelial cells against methylglyoxal-induced injuries, reproducible in a cerebral ischemic model in diabetic rats. J. Neurochem. 135 (2015), 431–440.
51. Filous, A.R., Silver, J., Targeting astrocytes in CNS injury and disease: a translational research approach. Prog. Neurobiol. 144 (2016), 173–187.
52. Fimia, G.M., Stoykova, A., Romagnoli, A., Giunta, L., Di Bartolomeo, S., Nardacci, R., Corazzari, M., Fuoco, C., Ucar, A., Schwartz, P., Gruss, P., Piacentini, M., Chowdhury, K., Cecconi, F., Ambra1 regulates autophagy and development of the nervous system. Nature 447 (2007), 1121–1125.
53. Franco, R., Fernandez-Suarez, D., Alternatively activated microglia and macrophages in the central nervous system. Prog. Neurobiol. 131 (2015), 65–86.
54. Francois, A., Terro, F., Janet, T., Rioux Bilan, A., Paccalin, M., Page, G., Involvement of interleukin-1beta in the autophagic process of microglia: relevance to Alzheimer's disease. J. Neuroinflamm., 10, 2013, 151.
55. Gabryel, B., Kost, A., Kasprowska, D., Neuronal autophagy in cerebral ischemia?a potential target for neuroprotective strategies?. Pharmacol. Rep. 64 (2012), 1–15.
56. Gabryel, B., Kost, A., Kasprowska, D., Liber, S., Machnik, G., Wiaderkiewicz, R., Labuzek, K., AMP-activated protein kinase is involved in induction of protective autophagy in astrocytes exposed to oxygen-glucose deprivation. Cell Biol. Int. 38 (2014), 1086–1097.
57. Gao, B., Zhang, X.Y., Han, R., Zhang, T.T., Chen, C., Qin, Z.H., Sheng, R., The endoplasmic reticulum stress inhibitor salubrinal inhibits the activation of autophagy and neuroprotection induced by brain ischemic preconditioning. Acta Pharmacol. Sin. 34 (2013), 657–666.
58. Gao, M., Monian, P., Pan, Q., Zhang, W., Xiang, J., Jiang, X., Ferroptosis is an autophagic cell death process. Cell Res. 26 (2016), 1021–1032.
59. Gasparini, C., Feldmann, M., NF-kappaB as a target for modulating inflammatory responses. Curr. Pharm. Des. 18 (2012), 5735–5745.
60. Ginet, V., Puyal, J., Clarke, P.G., Truttmann, A.C., Enhancement of autophagic flux after neonatal cerebral hypoxia-ischemia and its region-specific relationship to apoptotic mechanisms. Am. J. Pathol. 175 (2009), 1962–1974.
61. Ginet, V., Spiehlmann, A., Rummel, C., Rudinskiy, N., Grishchuk, Y., Luthi-Carter, R., Clarke, P.G., Truttmann, A.C., Puyal, J., Involvement of autophagy in hypoxic-excitotoxic neuronal death. Autophagy 10 (2014), 846–860.
62. Ginsberg, M.D., Expanding the concept of neuroprotection for acute ischemic stroke: the pivotal roles of reperfusion and the collateral circulation. Prog. Neurobiol. 145–146:October–November (2016), 46–77, 10.1016/j.pneurobio.2016.09.002.
63. Glick, D., Barth, S., Macleod, K.F., Autophagy: cellular and molecular mechanisms. J. Pathol. 221 (2010), 3–12.
64. Goldman, S.A., Kuypers, N.J., How to make an oligodendrocyte. Development 142 (2015), 3983–3995.
65. Gong, Y., He, Y., Gu, Y., Keep, R.F., Xi, G., Hua, Y., Effects of aging on autophagy after experimental intracerebral hemorrhage. Acta Neurochir. Suppl. 111 (2011), 113–117.
66. Gonzalez-Rodriguez, A., Mayoral, R., Agra, N., Valdecantos, M.P., Pardo, V., Miquilena-Colina, M.E., Vargas-Castrillon, J., Lo Iacono, O., Corazzari, M., Fimia, G.M., Piacentini, M., Muntane, J., Bosca, L., Garcia-Monzon, C., Martin-Sanz, P., Valverde, A.M., Impaired autophagic flux is associated with increased endoplasmic reticulum stress during the development of NAFLD. Cell. Death. Dis., 5, 2014, e1179.
67. Guo, Z., Cao, G., Yang, H., Zhou, H., Li, L., Cao, Z., Yu, B., Kou, J., A combination of four active compounds alleviates cerebral ischemia-reperfusion injury in correlation with inhibition of autophagy and modulation of AMPK/mTOR and JNK pathways. J. Neurosci. Res. 92 (2014), 1295–1306.
68. Guo, X., Sun, X., Hu, D., Wang, Y.J., Fujioka, H., Vyas, R., Chakrapani, S., Joshi, A.U., Luo, Y., Mochly-Rosen, D., Qi, X., VCP recruitment to mitochondria causes mitophagy impairment and neurodegeneration in models of Huntington's disease. Nat. Commun., 7, 2016, 12646.
69. Hacke, W., Kaste, M., Bluhmki, E., Brozman, M., Dávalos, A., Guidetti, D., Larrue, V., Lees, K.R., Medeghri, Z., Machnig, T., Schneider, D., von Kummer, R., Wahlgren, N., Toni, D., ECASS Investigators, Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N. Engl. J. Med. 13 (2008), 1317–1329.
70. Hallenbeck, J.M., Dutka, A.J., Background review and current concepts of reperfusion injury. Arch. Neurol. 47 (1990), 1245–1254.
71. Ham, P.B., Raju, R. 3rd, Mitochondrial function in hypoxic ischemic injury and influence of aging. Prog. Neurobiol., 2016, 10.1016/j.pneurobio.2016.06.006 pii: S0301-0082(15)30065-4.
72. Han, H.E., Kim, T.K., Son, H.J., Park, W.J., Han, P.L., Activation of autophagy pathway suppresses the expression of inos: il6 and cell death of lps-stimulated microglia cells. Biomol. Ther. (Seoul) 21 (2013), 21–28.
73. Hasegawa, H., Zinsser, S., Rhee, Y., Vik-Mo, E.O., Davanger, S., Hay, J.C., Mammalian ykt6 is a neuronal SNARE targeted to a specialized compartment by its profilin-like amino terminal domain. Mol. Biol. Cell 14 (2003), 698–720.
74. He, C., Klionsky, D.J., Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43 (2009), 67–93.
75. He, Y., Wan, S., Hua, Y., Keep, R.F., Xi, G., Autophagy after experimental intracerebral hemorrhage. J. Cereb. Blood Flow Metab. 28 (2008), 897–905.
76. He, S., Wang, C., Dong, H., Xia, F., Zhou, H., Jiang, X., Pei, C., Ren, H., Li, H., Li, R., Xu, H., Immune-related GTPase M (IRGM1) regulates neuronal autophagy in a mouse model of stroke. Autophagy 8 (2012), 1621–1627.
77. He, Z., Ostrowski, R.P., Sun, X., Ma, Q., Huang, B., Zhan, Y., Zhang, J.H., CHOP silencing reduces acute brain injury in the rat model of subarachnoid hemorrhage. Stroke 43 (2012), 484–490.
78. He, Z., Ostrowski, R.P., Sun, X., Ma, Q., Tang, J., Zhang, J.H., Targeting C/EBP homologous protein with siRNA attenuates cerebral vasospasm after experimental subarachnoid hemorrhage. Exp. Neurol. 238 (2012), 218–224.
79. Hetz, C., Mollereau, B., Disturbance of endoplasmic reticulum proteostasis in neurodegenerative diseases. Nat. Rev. Neurosci. 15 (2014), 233–249.
80. Hirota, Y., Kang, D., Kanki, T., The physiological role of mitophagy: new insights into phosphorylation events. Int. J. Cell Biol., 2012, 2012, 354914.
81. Hollenbeck, P., Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J. Cell Biol. 21 (1993), 305–315.
82. Hostenbach, S., D'Haeseleer, M., Kooijman, R., De Keyser, J., The pathophysiological role of astrocytic endothelin-1. Prog. Neurobiol. 144 (2016), 88–102.
83. Hou, W., Xie, Y., Song, X., Sun, X., Lotze, M.T., Zeh, H.J. 3rd, Kang, R., Tang, D., Autophagy promotes ferroptosis by degradation of ferritin. Autophagy 12 (2016), 1425–1428.
84. Hu, S., Xi, G., Jin, H., He, Y., Keep, R.F., Hua, Y., Thrombin-induced autophagy: a potential role in intracerebral hemorrhage. Brain Res. 1424 (2011), 60–66.
85. Huang, X.P., Ding, H., Lu, J.D., Tang, Y.H., Deng, B.X., Deng, C.Q., Autophagy in cerebral ischemia and the effects of traditional Chinese medicine. J. Integr. Med. 13 (2015), 289–296.
86. Huang, W., Huang, Y., Huang, R.Q., Huang, C.G., Wang, W.H., Gu, J.M., Dong, Y., SIRT3 expression decreases with reactive oxygen species generation in rat cortical neurons during early brain injury induced by experimental subarachnoid hemorrhage. BioMed Res. Int., 2016, 2016, 8263926, 10.1155/2016/8263926.
87. Huber, L.A., Teis, D., Lysosomal signaling in control of degradation pathways. Curr. Opin. Cell Biol. 39 (2016), 8–14.
88. Huenchuguala, S., Munoz, P., Zavala, P., Villa, M., Cuevas, C., Ahumada, U., Graumann, R., Nore, B.F., Couve, E., Mannervik, B., Paris, I., Segura-Aguilar, J., Glutathione transferase mu 2 protects glioblastoma cells against aminochrome toxicity by preventing autophagy and lysosome dysfunction. Autophagy 10 (2014), 618–630.
89. Janda, E., Lascala, A., Carresi, C., Parafati, M., Aprigliano, S., Russo, V., Savoia, C., Ziviani, E., Musolino, V., Morani, F., Isidoro, C., Mollace, V., Parkinsonian toxin-induced oxidative stress inhibits basal autophagy in astrocytes via NQO2/quinone oxidoreductase 2: Implications for neuroprotection. Autophagy 11 (2015), 1063–1080.
90. Ji, C., Chen, G., Signaling pathway in early brain injury after subarachnoid hemorrhage: news update. Acta Neurochir. Suppl. 121 (2016), 123–126.
91. Jiang, Y., Zhu, J., Wu, L., Xu, G., Dai, J., Liu, X., Tetracycline inhibits local inflammation induced by cerebral ischemia via modulating autophagy. PLoS One, 7, 2012, e48672.
92. Jiang, T., Yu, J.T., Zhu, X.C., Wang, H.F., Tan, M.S., Cao, L., Zhang, Q.Q., Gao, L., Shi, J.Q., Zhang, Y.D., Tan, L., Acute metformin preconditioning confers neuroprotection against focal cerebral ischaemia by pre-activation of AMPK-dependent autophagy. Br. J. Pharmacol. 171 (2014), 3146–3157.
93. Jiang, T., Yu, J.T., Zhu, X.C., Zhang, Q.Q., Tan, M.S., Cao, L., Wang, H.F., Shi, J.Q., Gao, L., Qin, H., Zhang, Y.D., Tan, L., Ischemic preconditioning provides neuroprotection by induction of AMP-activated protein kinase-dependent autophagy in a rat model of ischemic stroke. Mol. Neurobiol. 51 (2015), 220–229.
94. Jimenez, R.E., Kubli, D.A., Gustafsson, A.B., Autophagy and mitophagy in the myocardium: therapeutic potential and concerns. Br. J. Pharmacol. 171 (2014), 1907–1916.
95. Joers, V., Tansey, M.G., Mulas, G., Carta, A.R., Microglial phenotypes in Parkinson's disease and animal models of the disease. Prog. Neurobiol, 2016, 10.1016/j.pneurobio.2016.04.006 pii: S0301-0082(15)30053-8.
96. Kang, C., Avery, L., To be or not to be: the level of autophagy is the question: dual roles of autophagy in the survival response to starvation. Autophagy 4 (2008), 82–84.
97. Kim, Y.C., Guan, K.L., mTOR: a pharmacologic target for autophagy regulation. J. Clin. Invest. 125 (2015), 25–32.
98. Kim, J., Kundu, M., Viollet, B., Guan, K.L., AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13 (2011), 132–141.
99. Klionsky, D.J., Abdalla, F.C., Abeliovich, H., Abraham, R.T., Acevedo-Arozena, A., et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8 (2012), 445–544.
100. Koike, M., Shibata, M., Tadakoshi, M., Gotoh, K., Komatsu, M., Waguri, S., Kawahara, N., Kuida, K., Nagata, S., Kominami, E., Tanaka, K., Uchiyama, Y., Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am. J. Pathol. 172 (2008), 454–469.
101. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E., Tanaka, K., Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441 (2006), 880–884.
102. Komatsu, M., Ueno, T., Waguri, S., Uchiyama, Y., Kominami, E., Tanaka, K., Constitutive autophagy: vital role in clearance of unfavorable proteins in neurons. Cell Death Differ. 14 (2007), 887–894.
103. Kouroku, Y., Fujita, E., Tanida, I., Ueno, T., Isoai, A., Kumagai, H., Ogawa, S., Kaufman, R.J., Kominami, E., Momoi, T., ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ. 14 (2007), 230–239.
104. Kraft, C., Reggiori, F., Peter, M., Selective types of autophagy in yeast. Biochim. Biophys. Acta 1793 (2009), 1404–1412.
105. Kroemer, G., Autophagy: a druggable process that is deregulated in aging and human disease. J. Clin. Invest. 125 (2015), 1–4.
106. Kulbe, J.R., Mulcahy Levy, J.M., Coultrap, S.J., Thorburn, A., Bayer, K.U., Excitotoxic glutamate insults block autophagic flux in hippocampal neurons. Brain Res. 1542 (2014), 12–19.
107. Lantigua, H., Ortega-Gutierrez, S., Schmidt, J.M., Lee, K., Badjatia, N., Agarwal, S., Claassen, J., Connolly, E.S., Mayer, S.A., Subarachnoid hemorrhage: who dies, and why?. Crit. Care, 19(309), 2015, 10.1186/s13054-015-1036-0.
108. Lebovitz, C.B., DeVorkin, L., Bosc, D., Rothe, K., Singh, J., Bally, M., Jiang, X., Young, R.N., Lum, J.J., Gorski, S.M., Precision autophagy: will the next wave of selective autophagy markers and specific autophagy inhibitors feed clinical pipelines?. Autophagy 11 (2015), 1949–1952.
109. Lee, J.Y., He, Y., Sagher, O., Keep, R., Hua, Y., Xi, G., Activated autophagy pathway in experimental subarachnoid hemorrhage. Brain Res. 1287 (2009), 126–135.
110. Li, W.W., Li, J., Bao, J.K., Microautophagy: lesser-known self-eating. Cell. Mol. Life Sci. 7 (2012), 1125–1136.
111. Li, H., Huang, S., Wang, S., Zhao, J., Su, L., Zhao, B., Zhang, Y., Zhang, S., Miao, J., Targeting annexin A7 by a small molecule suppressed the activity of phosphatidylcholine-specific phospholipase C in vascular endothelial cells and inhibited atherosclerosis in apolipoprotein E(−)/(−)mice. Cell. Death. Dis., 4, 2013, e806.
112. Li, W.L., Yu, S.P., Chen, D., Yu, S.S., Jiang, Y.J., Genetta, T., Wei, L., The regulatory role of NF-kappaB in autophagy-like cell death after focal cerebral ischemia in mice. Neuroscience 244 (2013), 16–30.
113. Li, H., Gao, A., Feng, D., Wang, Y., Zhang, L., Cui, Y., Li, B., Wang, Z., Chen, G., Evaluation of the protective potential of brain microvascular endothelial cell autophagy on blood-brain barrier integrity during experimental cerebral ischemia-reperfusion injury. Transl. Stroke Res. 5 (2014), 618–626.
114. Li, H., Wang, Y., Feng, D., Liu, Y., Xu, M., Gao, A., Tian, F., Zhang, L., Cui, Y., Wang, Z., Chen, G., Alterations in the time course of expression of the Nox family in the brain in a rat experimental cerebral ischemia and reperfusion model: effects of melatonin. J. Pineal Res. 57 (2014), 110–119.
115. Li, J., Lu, J., Mi, Y., Shi, Z., Chen, C., Riley, J., Zhou, C., Voltage-dependent anion channels (VDACs) promote mitophagy to protect neuron from death in an early brain injury following a subarachnoid hemorrhage in rats. Brain Res. 1573 (2014), 74–83.
116. Li, Q., Zhang, T., Wang, J., Zhang, Z., Zhai, Y., Yang, G.Y., Sun, X., Rapamycin attenuates mitochondrial dysfunction via activation of mitophagy in experimental ischemic stroke. Biochem. Biophys. Res. Commun. 444 (2014), 182–188.
117. Li, T., Sun, K.J., Wang, H.D., Zhou, M.L., Ding, K., Lu, X.Y., Wei, W.T., Wang, C.X., Zhou, X.M., Tert-butylhydroquinone ameliorates early brain injury after experimental subarachnoid hemorrhage in mice by enhancing nrf2-independent autophagy. Neurochem. Res. 40 (2015), 1829–1838.
118. Liu, Z., Chopp, M., Astrocytes: therapeutic targets for neuroprotection and neurorestoration in ischemic stroke. Prog. Neurobiol. 144 (2016), 103–120.
119. Liu, C., Gao, Y., Barrett, J., Hu, B., Autophagy and protein aggregation after brain ischemia. J. Neurochem. 115 (2010), 68–78.
120. Liu, Y., Cai, H., Wang, Z., Li, J., Wang, K., Yu, Z., Chen, G., Induction of autophagy by cystatin C: a potential mechanism for prevention of cerebral vasospasm after experimental subarachnoid hemorrhage. Eur. J. Med. Res., 18, 2013, 21.
121. Liu, R.Y., Wang, J.J., Qiu, X., Wu, J.M., Acute hyperglycemia together with hematoma of high-glucose blood exacerbates neurological injury in a rat model of intracerebral hemorrhage. Neurosci. Bull. 30 (2014), 90–98.
122. Liu, Y., Grumbles, R.M., Thomas, C.K., Electrical stimulation of transplanted motoneurons improves motor unit formation. J. Neurophysiol. 112 (2014), 660–670.
123. Liu, Y., Li, J., Wang, Z., Yu, Z., Chen, G., Attenuation of early brain injury and learning deficits following experimental subarachnoid hemorrhage secondary to Cystatin C: possible involvement of the autophagy pathway. Mol. Neurobiol. 49 (2014), 1043–1054.
124. Ma, J., Wan, J., Meng, J., Banerjee, S., Ramakrishnan, S., Roy, S., Methamphetamine induces autophagy as a pro-survival response against apoptotic endothelial cell death through the Kappa opioid receptor. Cell. Death. Dis., 5, 2014, e1099.
125. Ma, Y., Wang, J., Wang, Y., Yang, G.Y., The biphasic function of microglia in ischemic stroke. Prog. Neurobiol, 2016, 10.1016/j.pneurobio.2016.01.005 pii: S0301-0082(15)30070-8.
126. Mancias, J.D., Wang, X., Gygi, S.P., Harper, J.W., Kimmelman, A.C., Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy. Nature 509 (2014), 105–109.
127. Manjithaya, R., Subramani, S., Autophagy: a broad role in unconventional protein secretion?. Trends Cell Biol. 21 (2011), 67–73.
128. Manwani, B., McCullough, L.D., Function of the master energy regulator adenosine monophosphate-activated protein kinase in stroke. J. Neurosci. Res. 91 (2013), 1018–1029.
129. Mauvezin, C., Neufeld, T.P., Bafilomycin A1 disrupts autophagic flux by inhibiting both V-ATPase-dependent acidification and Ca-P60A/SERCA-dependent autophagosome-lysosome fusion. Autophagy 11 (2015), 1437–1438.
130. May, A.I., Devenish, R.J., Prescott, M., The many faces of mitochondrial autophagy: making sense of contrasting observations in recent research. Int. J. Cell Biol., 2012, 2012, 431684.
131. Mayer, S.A., Rincon, F., Treatment of intracerebral haemorrhage. Lancet Neurol. 4 (2005), 662–672.
132. Mengesdorf, T., Jensen, P.H., Mies, G., Aufenberg, C., Paschen, W., Down-regulation of parkin protein in transient focal cerebral ischemia: a link between stroke and degenerative disease?. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 15042–15047.
133. Mizushima, N., Yamamoto, A., Hatano, M., Kobayashi, Y., Kabeya, Y., Suzuki, K., Tokuhisa, T., Ohsumi, Y., Yoshimori, T., Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 152 (2001), 657–668.
134. 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 15 (2004), 1101–1111.
135. Morgan, M.J., Gamez, G., Menke, C., Hernandez, A., Thorburn, J., Gidan, F., Staskiewicz, L., Morgan, S., Cummings, C., Maycotte, P., Thorburn, A., Regulation of autophagy and chloroquine sensitivity by oncogenic RAS in vitro is context-dependent. Autophagy 10 (2014), 1814–1826.
136. Motori, E., Puyal, J., Toni, N., Ghanem, A., Angeloni, C., Malaguti, M., Cantelli-Forti, G., Berninger, B., Conzelmann, K.K., Gotz, M., Winklhofer, K.F., Hrelia, S., Bergami, M., Inflammation-induced alteration of astrocyte mitochondrial dynamics requires autophagy for mitochondrial network maintenance. Cell Metab. 18 (2013), 844–859.
137. Mracsko, E., Veltkamp, R., Neuroinflammation after intracerebral hemorrhage. Front. Cell. Neurosci., 8, 2014, 388.
138. Mukhopadhyay, S., Panda, P.K., Sinha, N., Das, D.N., Bhutia, S.K., Autophagy and apoptosis: where do they meet?. Apoptosis 19 (2014), 555–566.
139. Mura, E., Lepore, G., Zedda, M., Giua, S., Farina, V., Sheep primary astrocytes under starvation conditions express higher amount of LC3 II autophagy marker than neurons. Arch. Ital. Biol. 152 (2014), 47–56.
140. Nakatogawa, H., Two ubiquitin-like conjugation systems that mediate membrane formation during autophagy. Essays Biochem. 55 (2013), 39–50.
141. Nakka, V.P., Prakash-babu, P., Vemuganti, R., Crosstalk between endoplasmic reticulum stress oxidative stress, and autophagy: potential therapeutic targets for acute cns injuries. Mol. Neurobiol. 53 (2016), 532–544.
142. Nathanson, D., Mischel, P.S., Charting the course across the blood-brain barrier. J. Clin. Invest. 121 (2011), 31–33.
143. Netea-Maier, R.T., Plantinga, T.S., Van De Veerdonk, F.L., Smit, J.W., Netea, M.G., Modulation of inflammation by autophagy: consequences for human disease. Autophagy 12 (2015), 245–260.
144. Ni, M., Zhang, Y., Lee, A.S., Beyond the endoplasmic reticulum: atypical GRP78 in cell viability: signalling and therapeutic targeting. Biochem. J. 434 (2011), 181–188.
145. Ni, J., Wu, Z., Peterts, C., Yamamoto, K., Qing, H., Nakanishi, H., The critical role of proteolytic relay through cathepsins b and e in the phenotypic change of microglia/macrophage. J. Neurosci. 35 (2015), 12488–12501.
146. Nikoletopoulou, V., Markaki, M., Palikaras, K., Tavernarakis, N., Crosstalk between apoptosis: necrosis and autophagy. Biochim. Biophys. Acta 1833 (2013), 3448–3459.
147. Nixon, R.A., Yang, D.S., Autophagy and neuronal cell death in neurological disorders. Cold Spring Harb. Perspect. Biol., 4, 2012.
148. Noack, M., Richter-Landsberg, C., Activation of autophagy by rapamycin does not protect oligodendrocytes against protein aggregate formation and cell death induced by proteasomal inhibition. J. Mol. Neurosci. 55 (2015), 99–108.
149. Ogata, M., Hino, S., Saito, A., Morikawa, K., Kondo, S., Kanemoto, S., Murakami, T., Taniguchi, M., Tanii, I., Yoshinaga, K., Shiosaka, S., Hammarback, J.A., Urano, F., Imaizumi, K., Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell. Biol. 26 (2006), 9220–9231.
150. Oliveira, C.S., Pereira, H., Alves, S., Castro, L., Baltazar, F., Chaves, S.R., Preto, A., Corte-Real, M., Cathepsin D protects colorectal cancer cells from acetate-induced apoptosis through autophagy-independent degradation of damaged mitochondria. Cell. Death. Dis., 6, 2015, e1788.
151. Osborn, L.M., Kamphuis, W., Wadman, W.J., Hol, E.M., Astrogliosis: an integral player in the pathogenesis of Alzheimer's disease. Prog. Neurobiol. 144 (2016), 121–141.
152. Ostrowski, R.P., Colohan, A.R., Zhang, J.H., Mechanisms of hyperbaric oxygen-induced neuroprotection in a rat model of subarachnoid hemorrhage. J. Cereb. Blood Flow Metab. 25 (2005), 554–571.
153. Ouyang, L., Shi, Z., Zhao, S., Wang, F.T., Zhou, T.T., Liu, B., Bao, J.K., Programmed cell death pathways in cancer: a review of apoptosis: autophagy and programmed necrosis. Cell Prolif. 45 (2012), 487–498.
154. Ozpolat, B., Benbrook, D.M., Targeting autophagy in cancer management – strategies and developments. Cancer Manage. Res. 7 (2015), 291–299.
155. Pamenter, M.E., Perkins, G.A., McGinness, A.K., Gu, X.Q., Ellisman, M.H., Haddad, G.G., Autophagy and apoptosis are differentially induced in neurons and astrocytes treated with an in vitro mimic of the ischemic penumbra. PLoS One, 7, 2012, e51469.
156. Parzych, K.R., Klionsky, D.J., An overview of autophagy: morphology mechanism, and regulation. Antioxid. Redox Signal. 20 (2014), 460–473.
157. Pimentel-Muinos, F.X., Boada-Romero, E., Selective autophagy against membranous compartments: canonical and unconventional purposes and mechanisms. Autophagy 10 (2014), 397–407.
158. Placido, A.I., Pereira, C.M., Duarte, A.I., Candeias, E., Correia, S.C., Carvalho, C., Cardoso, S., Oliveira, C.R., Moreira, P.I., Modulation of endoplasmic reticulum stress: an opportunity to prevent neurodegeneration?. CNS Neurol. Disord. Drug Targets 14 (2015), 518–533.
159. Pukaß K., Goldbaum, O., Richter-Landsberg, C., Mitochondrial impairment and oxidative stress compromise autophagosomal degradation of α-synuclein in oligodendroglial cells. J. Neurochem. 135 (2015), 194–205.
160. Puyal, J., Clarke, P.G., Targeting autophagy to prevent neonatal stroke damage. Autophagy 5 (2009), 1060–1061.
161. Puyal, J., Vaslin, A., Mottier, V., Clarke, P.G., Postischemic treatment of neonatal cerebral ischemia should target autophagy. Ann. Neurol. 66 (2009), 378–389.
162. Qin, A.P., Liu, C.F., Qin, Y.Y., Hong, L.Z., Xu, M., Yang, L., Liu, J., Qin, Z.H., Zhang, H.L., Autophagy was activated in injured astrocytes and mildly decreased cell survival following glucose and oxygen deprivation and focal cerebral ischemia. Autophagy 6 (2010), 738–753.
163. Quinones, Q.J., de Ridder, G.G., Pizzo, S.V., GRP78: a chaperone with diverse roles beyond the endoplasmic reticulum. Histol. Histopathol. 23 (2008), 1409–1416.
164. Rami, A., Langhagen, A., Steiger, S., Focal cerebral ischemia induces upregulation of Beclin 1 and autophagy-like cell death. Neurobiol. Dis. 29 (2008), 132–141.
165. Ramos, E., Patiño, P., Reiter, R.J., Gil-Martín, E., Marco-Contelles, J., Parada, E., Los Rios, C., Romero, A., Egea, J., Ischemic brain injury: new insights on the protective role of melatonin. Free Radic. Biol. Med. 104 (2017), 32–53.
166. Ravikumar, B., Sarkar, S., Davies, J.E., Futter, M., Garcia-Arencibia, M., Green-Thompson, Z.W., Jimenez-Sanchez, M., Korolchuk, V.I., Lichtenberg, M., Luo, S., Massey, D.C., Menzies, F.M., Moreau, K., Narayanan, U., Renna, M., Siddiqi, F.H., Underwood, B.R., Winslow, A.R., Rubinsztein, D.C., Regulation of mammalian autophagy in physiology and pathophysiology. Physiol. Rev. 90 (2010), 1383–1435.
167. Reggiori, F., Komatsu, M., Finley, K., Simonsen, A., Selective types of autophagy. Int. J. Cell Biol., 2012, 2012, 156272.
168. Rodgers, M.A., Bowman, J.W., Liang, Q., Jung, J.U., Regulation where autophagy intersects the inflammasome. Antioxid. Redox Signal. 20 (2014), 495–506.
169. Rolland, W.B., Lekic, T., Krafft, P.R., Hasegawa, Y., Altay, O., Hartman, R., Ostrowski, R., Manaenko, A., Tang, J., Zhang, J.H., Fingolimod reduces cerebral lymphocyte infiltration in experimental models of rodent intracerebral hemorrhage. Exp. Neurol. 241 (2013), 45–55.
170. Rossi, D., Astrocyte physiopathology: at the crossroads of intercellular networking: inflammation and cell death. Prog. Neurobiol. 130 (2015), 86–120.
171. Rubinsztein, D.C., Bento, C.F., Deretic, V., Therapeutic targeting of autophagy in neurodegenerative and infectious diseases. J. Exp. Med. 212 (2015), 979–990.
172. Sabri, M., Lass, E., Macdonald, R.L., Early brain injury: a common mechanism in subarachnoid hemorrhage and global cerebral ischemia. Stroke Res. Treat., 2013, 2013, 394036.
173. Santos, R.X., Correia, S.C., Wang, X., Perry, G., Smith, M.A., Moreira, P.I., Zhu, X., A synergistic dysfunction of mitochondrial fission/fusion dynamics and mitophagy in Alzheimer's disease. J. Alzheimers Dis. 20:Suppl. 2 (2010), S401–412.
174. Sarkaki, A., Farbood, Y., Badavi, M., Khalaj, L., Khodagholi, F., Ashabi, G., Metformin improves anxiety-like behaviors through AMPK-dependent regulation of autophagy following transient forebrain ischemia. Metab. Brain Dis. 30 (2015), 1139–1150.
175. Scherz-Shouval, R., Elazar, Z., Regulation of autophagy by ROS: physiology and pathology. Trends Biochem. Sci. 36 (2011), 30–38.
176. Schreiber, A., Peter, M., Substrate recognition in selective autophagy and the ubiquitin-proteasome system. Biochim. Biophys. Acta 1843 (2014), 163–181.
177. Schrijvers, D.M., De Meyer, G.R., Martinet, W., Autophagy in atherosclerosis: a potential drug target for plaque stabilization. Arterioscler. Thromb. Vasc. Biol. 31 (2011), 2787–2791.
178. Shao, A., Wang, Z., Wu, H., Dong, X., Li, Y., Tu, S., Tang, J., Zhao, M., Zhang, J., Hong, Y., Enhancement of autophagy by histone deacetylase inhibitor trichostatin a ameliorates neuronal apoptosis after subarachnoid hemorrhage in rats. Mol. Neurobiol. 53 (2016), 18–27.
179. Sheng, R., Zhang, L.S., Han, R., Liu, X.Q., Gao, B., Qin, Z.H., Autophagy activation is associated with neuroprotection in a rat model of focal cerebral ischemic preconditioning. Autophagy 6 (2010), 482–494.
180. Sheng, R., Liu, X.Q., Zhang, L.S., Gao, B., Han, R., Wu, Y.Q., Zhang, X.Y., Qin, Z.H., Autophagy regulates endoplasmic reticulum stress in ischemic preconditioning. Autophagy 8 (2012), 310–325.
181. Shi, R., Weng, J., Zhao, L., Li, X.M., Gao, T.M., Kong, J., Excessive autophagy contributes to neuron death in cerebral ischemia. CNS Neurosci. Ther. 18 (2012), 250–260.
182. Shintani, T., Klionsky, D.J., Autophagy in health and disease: a double-edged sword. Science 306 (2004), 990–995.
183. Shuvaev, V.V., Muzykantov, V.R., Targeted modulation of reactive oxygen species in the vascular endothelium. J. Control. Release 153 (2011), 56–63.
184. Simpson, I.A., Carruthers, A., Vannucci, S.J., Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J. Cereb. Blood Flow Metab. 27 (2007), 1766–1791.
185. Singh, R., Cuervo, A.M., Lipophagy: connecting autophagy and lipid metabolism. Int. J. Cell Biol., 2012, 2012, 282041.
186. Smith, C.M., Mayer, J.A., Duncan, I.D., Autophagy promotes oligodendrocyte survival and function following dysmyelination in a long-lived myelin mutant. J. Neurosci. 33 (2013), 8088–8100.
187. Song, C.Y., Guo, J.F., Liu, Y., Tang, B.S., Autophagy and its comprehensive impact on ALS. Int. J. Neurosci. 122 (2012), 695–703.
188. Song, J., Oh, Y., Lee, J.E., miR-Let7A modulates autophagy induction in LPS-activated microglia. Exp. Neurobiol. 24 (2015), 117–125.
189. Sun, Y., Zhang, L., Chen, Y., Zhan, L., Gao, Z., Therapeutic targets for cerebral ischemia based on the signaling pathways of the GluN2 B C terminus. Stroke 46 (2015), 2347–2353.
190. Svenning, S., Johansen, T., Selective autophagy. Essays Biochem. 55 (2013), 79–92.
191. Tang, Y.C., Tian, H.X., Yi, T., Chen, H.B., The critical roles of mitophagy in cerebral ischemia. Protein Cell 7 (2016), 699–713.
192. Tasset, I., Cuervo, A.M., Role of chaperone-mediated autophagy in metabolism. FEBS J. 13 (2016), 2403–2413.
193. Till, A., Lakhani, R., Burnett, S.F., Subramani, S., Pexophagy: the selective degradation of peroxisomes. Int. J. Cell Biol., 2012, 2012, 512721.
194. Ulamek-Koziol, M., Furmaga-Jablonska, W., Januszewski, S., Brzozowska, J., Scislewska, M., Jablonski, M., Pluta, R., Neuronal autophagy: self-eating or self-cannibalism in Alzheimer's disease. Neurochem. Res. 38 (2013), 1769–1773.
195. Unal Cevik, I., Dalkara, T., Intravenously administered propidium iodide labels necrotic cells in the intact mouse brain after injury. Cell Death Differ. 10 (2003), 928–929.
196. Urday, S., Kimberly, W.T., Beslow, L.A., Vortmeyer, A.O., Selim, M.H., Rosand, J., Simard, J.M., Sheth, K.N., Targeting secondary injury in intracerebral haemorrhage?perihaematomal oedema. Nat. Rev. Neurol. 11 (2015), 111–122.
197. Vartak-Sharma, N., Nooka, S., Ghorpade, A., Astrocyte elevated gene -1 (AEG -1) and the A(E)Ging HIV/AIDS-HAND. Prog. Neurobiol., 2016, 10.1016/j.pneurobio.2016.03.006 pii: S0301-0082(15)30091-5 [Epub ahead of print].
198. Verkhratsky, A., Steardo, L., Parpura, V., Montana, V., Translational potential of astrocytes in brain disorders. Prog. Neurobiol. 144 (2016), 188–205.
199. Vidal, R.L., Matus, S., Bargsted, L., Hetz, C., Targeting autophagy in neurodegenerative diseases. Trends Pharmacol. Sci. 35 (2014), 583–591.
200. Vives-Bauza, C., Przedborski, S., Mitophagy: the latest problem for Parkinson's disease. Trends Mol. Med. 17 (2011), 158–165.
201. Wang, P., Guan, Y.F., Du, H., Zhai, Q.W., Su, D.F., Miao, C.Y., Induction of autophagy contributes to the neuroprotection of nicotinamide phosphoribosyltransferase in cerebral ischemia. Autophagy 8 (2012), 77–87.
202. Wang, Z., Shi, X.Y., Yin, J., Zuo, G., Zhang, J., Chen, G., Role of autophagy in early brain injury after experimental subarachnoid hemorrhage. J. Mol. Neurosci. 46 (2012), 192–202.
203. Wang, L.F., Yokoyama, K.K., Chen, T.Y., Hsiao, H.W., Chiang, P.C., Hsieh, Y.C., Lo, S., Hsu, C., Male-specific alleviation of iron-induced striatal injury by inhibition of autophagy. PLoS One, 10, 2015, e0131224.
204. Wang, Y., Liu, G., Hong, D., Chen, F., Ji, X., Cao, G., White matter injury in ischemic stroke. Prog. Neurobiol. 141 (2016), 45–60.
205. Wei, K., Wang, P., Miao, C.Y., A double-edged sword with therapeutic potential: an updated role of autophagy in ischemic cerebral injury. CNS Neurosci. Ther. 18 (2012), 879–886.
206. Wen, Y.D., Sheng, R., Zhang, L.S., Han, R., Zhang, X., Zhang, X.D., Han, F., Fukunaga, K., Qin, Z.H., Neuronal injury in rat model of permanent focal cerebral ischemia is associated with activation of autophagic and lysosomal pathways. Autophagy 4 (2008), 762–769.
207. Wu, Y.T., Tan, H.L., Shui, G., Bauvy, C., Huang, Q., Wenk, M.R., Ong, C.N., Codogno, P., Shen, H.M., 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. 285 (2010), 10850–10861.
208. Wu, C., Hu, Q., Chen, J., Yan, F., Li, J., Wang, L., Mo, H., Gu, C., Zhang, P., Chen, G., Inhibiting HIF-1alpha by 2ME2 ameliorates early brain injury after experimental subarachnoid hemorrhage in rats. Biochem. Biophys. Res. Commun. 437 (2013), 469–474.
209. Wu, H., Che, X., Zheng, Q., Wu, A., Pan, K., Shao, A., Wu, Q., Zhang, J., Hong, Y., Caspases: a molecular switch node in the crosstalk between autophagy and apoptosis. Int. J. Biol. Sci. 10 (2014), 1072–1083.
210. Xie, Y., Kang, R., Sun, X., Zhong, M., Huang, J., Klionsky, D.J., Tang, D., Posttranslational modification of autophagy-related proteins in macroautophagy. Autophagy 11 (2015), 28–45.
211. Xin, X.Y., Pan, J., Wang, X.Q., Ma, J.F., Ding, J.Q., Yang, G.Y., Chen, S.D., 2-methoxyestradiol attenuates autophagy activation after global ischemia. Can. J. Neurol. Sci. 38 (2011), 631–638.
212. Xing, S., Zhang, Y., Li, J., Zhang, J., Li, Y., Dang, C., Li, C., Fan, Y., Yu, J., Pei, Z., Zeng, J., Beclin 1 knockdown inhibits autophagic activation and prevents the secondary neurodegenerative damage in the ipsilateral thalamus following focal cerebral infarction. Autophagy 8 (2012), 63–76.
213. Xiong, X.Y., Liu, L., Yang, Q.W., Functions and mechanisms of microglia/macrophages in neuroinflammation and neurogenesis after stroke. Prog. Neurobiol. 142 (2016), 23–44.
214. Xu, Q., Si, L.Y., Resveratrol role in cardiovascular and metabolic health and potential mechanisms of action. Nutr. Res. 32 (2012), 648–658.
215. Xu, F., Gu, J.H., Qin, Z.H., Neuronal autophagy in cerebral ischemia. Neurosci. Bull. 28 (2012), 658–666.
216. Xu, Z., Yang, L., Xu, S., Zhang, Z., Cao, Y., The receptor proteins: pivotal roles in selective autophagy. Acta Biochim. Biophys. Sin. (Shanghai) 47 (2015), 571–580.
217. Yabu, T., Imamura, S., Mizusawa, N., Touhata, K., Yamashita, M., Induction of autophagy by amino acid starvation in fish cells. Mar. Biotechnol. (NY) 14 (2012), 491–501.
218. Yan, F., Li, J., Chen, J., Hu, Q., Gu, C., Lin, W., Chen, G., Endoplasmic reticulum stress is associated with neuroprotection against apoptosis via autophagy activation in a rat model of subarachnoid hemorrhage. Neurosci. Lett. 563 (2014), 160–165.
219. Yang, Z., Zhao, T.Z., Zou, Y.J., Zhang, J.H., Feng, H., Hypoxia Induces autophagic cell death through hypoxia-inducible factor 1alpha in microglia. PLoS One, 9, 2014, e96509.
220. Yang, Z., Liu, B., Zhong, L., Shen, H., Lin, C., Lin, L., Zhang, N., Yuan, B., Toll-like receptor-4-mediated autophagy contributes to microglial activation and inflammatory injury in mouse models of intracerebral haemorrhage. Neuropathol. Appl. Neurobiol. 41 (2015), e95–106.
221. Yang, Z., Zhong, L., Zhong, S., Xian, R., Yuan, B., Hypoxia induces microglia autophagy and neural inflammation injury in focal cerebral ischemia model. Exp. Mol. Pathol. 98 (2015), 219–224.
222. Young, P.G., Bartel, B., Pexophagy and peroxisomal protein turnover in plants. Biochim. Biophys. Acta 1863 (2015), 999–1005.
223. Yuntao, F., Chenjia, G., Panpan, Z., Wenjun, Z., Suhua, W., Guangwei, X., Haifeng, S., Jian, L., Wanxin, P., Yun, F., Cai, J., Aschner, M., Rongzhu, L., Role of autophagy in methylmercury-induced neurotoxicity in rat primary astrocytes. Arch. Toxicol. 90 (2016), 333–345.
224. Zhang, J., Ney, P.A., Mechanisms and biology of B-cell leukemia/lymphoma 2/adenovirus E1 B interacting protein 3 and Nip-like protein X. Antioxid. Redox Signal. 14 (2011), 1959–1969.
225. Zhang, X., Yan, H., Yuan, Y., Gao, J., Shen, Z., Cheng, Y., Shen, Y., Wang, R.R., Wang, X., Hu, W.W., Wang, G., Chen, Z., Cerebral ischemia-reperfusion-induced autophagy protects against neuronal injury by mitochondrial clearance. Autophagy 9 (2013), 1321–1333.
226. Zhang, X., Yuan, Y., Jiang, L., Zhang, J., Gao, J., Shen, Z., Zheng, Y., Deng, T., Yan, H., Li, W., Hou, W.W., Lu, J., Shen, Y., Dai, H., Hu, W.W., Zhang, Z., Chen, Z., Endoplasmic reticulum stress induced by tunicamycin and thapsigargin protects against transient ischemic brain injury: involvement of PARK2-dependent mitophagy. Autophagy 10 (2014), 1801–1813.
227. Zhang, B., Song, C., Feng, B., Fan, W., Neuroprotection by triptolide against cerebral ischemia/reperfusion injury through the inhibition of NF-κB/PUMA signal in rats. Ther. Clin. Risk Manage. 12 (2016), 817–824.
228. Zhao, H., Ji, Z., Tang, D., Yan, C., Zhao, W., Gao, C., Role of autophagy in early brain injury after subarachnoid hemorrhage in rats. Mol. Biol. Rep. 40 (2013), 819–827.
229. Zheng, Y.Q., Liu, J.X., Li, X.Z., Xu, L., Xu, Y.G., RNA interference-mediated downregulation of Beclin1 attenuates cerebral ischemic injury in rats. Acta Pharmacol. Sin. 30 (2009), 919–927.
230. Zhou, W., Yuan, J., Necroptosis in health and diseases. Semin. Cell Dev. Biol. 35 (2014), 14–23.
231. Zhou, X.J., Zhang, H., Autophagy in immunity: implications in etiology of autoimmune/autoinflammatory diseases. Autophagy 8 (2012), 1286–1299.
232. Zhou, R., Yazdi, A.S., Menu, P., Tschopp, J., A role for mitochondria in NLRP3 inflammasome activation. Nature 469 (2011), 221–225.
233. van Asch, C.J., Luitse, M.J., Rinkel, G.J., van der Tweel, I., Algra, A., Klijn, C.J., Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time according to age, sex, and ethnic origin: a systematic review and meta-analysis. Lancet Neurol. 9 (2010), 167–176.
234. van der Burgh, R., Boes, M., Mitochondria in autoinflammation: cause, mediator or bystander?. Trends Endocrinol. Metab. 26 (2015), 263–271.
235. Zhou, Y., Zheng, B., Ye, L., Zhang, H., Zhu, S., Zheng, X., Xia, Q., He, Z., Wang, Q., Xiao, J., Xu, H., Retinoic acid prevents disruption of blood-spinal cord barrier by inducing autophagic flux after spinal cord injury. Neurochem. Res. 41 (2016), 813–825.