Advances in Astrocyte-targeted Approaches for Stroke Therapy: An Emerging Role for Mitochondria and microRNAS

Neurochemical Research

Volumn 40, Issue 2, 2015, Pages 301-307

  Stary, Creed M ^a   Giffard, Rona G ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ATP; Cerebral ischemia; Chaperones; Metabolism; miR; Neuron

Indexed keywords

MICRORNA;

ANIMAL; ASTROCYTE; DISEASE MODEL; HUMAN; MITOCHONDRION; PATHOLOGY; PHYSIOLOGY; STROKE;

ANIMALS; ASTROCYTES; DISEASE MODELS, ANIMAL; HUMANS; MICRORNAS; MITOCHONDRIA; STROKE;

EID: 84940261292     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-014-1373-4     Document Type: Review

References (72)

1. Roger V, Go A, Lloyd-Jones D, Adams R, Berry J, Brown T, Carnethon M, Dai S, de Simone G, Ford E, Fox C, Fullerton H, Gillespie C, Greenlund K, Hailpern S, Heit J, Ho P, Howard V, Kissela B, Kittner S, Lackland D, Lichtman J, Lisabeth L, Makuc D, Marcus G, Marelli A, Matchar D, McDermott M, Meigs J, Moy C, Mozaffarian D, Mussolino M, Nichol G, Paynter N, Rosamond W, Sorlie P, Stafford R, Turan T, Turner M, Wong N, Wylie-Rosett J (2011) Heart disease and stroke statistics–2011 update: a report from the American Heart Association. Circulation 123:e18–e209
2. Blakeley J, Llinas R (2007) Thrombolytic therapy for acute ischemic stroke. J Neurol Sci 261:55–62
3. Ogata K, Kosaka T (2002) Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience 113:221–233
4. Bushong E, Martone M, Jones Y, Ellisman M (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22:183–192
5. Halassa M, Fellin T, Takano H, Dong J, Haydon P (2007) Synaptic islands defined by the territory of a single astrocyte. J Neurosci 27:6473–6477
6. Bass N, Hess H, Pope A, Thalheimer C (1971) Quantitative cytoarchitectonic distribution of neurons, glia, and DNA in rat cerebral cortex. J Comp Neurol 143:481–490
7. Rouach N, Glowinski J, Giaume C (2000) Activity-dependent neuronal control of gap-junctional communication in astrocytes. J Cell Biol 149:1513–1526
8. Araque A, Sanzgiri R, Parpura V, Haydon P (1999) Astrocyte-induced modulation of synaptic transmission. Can J Physiol Pharmacol 77:699–706
9. Giordano G, Kavanagh T, Costa L (2009) Mouse cerebellar astrocytes protect cerebellar granule neurons against toxicity of the polybrominated diphenyl ether (PBDE) mixture DE-71. Neurotoxicology 30:326–329
10. Noguchi Y, Shinozaki Y, Fujishita K, Shibata K, Imura Y, Morizawa Y, Gachet C, Koizumi S (2013) Astrocytes protect neurons against methylmercury via ATP/P2Y(1) receptor-mediated pathways in astrocytes. PLoS One 8:e57898
11. Rathinam M, Watts L, Narasimhan M, Riar A, Mahimainathan L, Henderson G (2012) Astrocyte mediated protection of fetal cerebral cortical neurons from rotenone and paraquat. Environ Toxicol Pharmacol 33:353–360
12. Pekny M, Nilsson M (2005) Astrocyte activation and reactive gliosis. Glia 50:427–434
13. Swanson R, Ying W, Kauppinen T (2004) Astrocyte influences on ischemic neuronal death. Curr Mol Med 4:193–205
14. Zhao Y, Rempe D (2010) Targeting astrocytes for stroke therapy. Neurotherapeutics 7:439–451
15. Ferrer I, Planas A (2003) Signaling of cell death and cell survival following focal cerebral ischemia: life and death struggle in the penumbra. J Neuropathol Exp Neurol 62:329–339
16. Qu W, Wang Y, Wang J, Tang Y, Zhang Q, Tian D, Yu Z, Xie M, Wang W (2010) Galectin-1 enhances astrocytic BDNF production and improves functional outcome in rats following ischemia. Neurochem Res 35:1716–1724
17. Miao Y, Qiu Y, Lin Y, Miao Z, Zhang J, Lu X (2011) Protection by pyruvate against glutamate neurotoxicity is mediated by astrocytes through a glutathione-dependent mechanism. Mol Biol Rep 38:3235–3242
18. Ouyang Y, Voloboueva L, Xu L, Giffard R (2007) Selective dysfunction of hippocampal CA1 astrocytes contributes to delayed neuronal damage after transient forebrain ischemia. J Neurosci 27:4253–4260
19. Xu L, Emery JF, Ouyang Y-B, Voloboueva LA, Giffard RG (2010) Astrocyte targeted overexpression of Hsp72 or SOD2 reduces neuronal vulnerability to forebrain ischemia. Glia 58:1042–1049
20. Weller ML, Stone IM, Goss A, Rau T, Rova C, Poulsen DJ (2008) Selective overexpression of excitatory amino acid transporter 2 (EAAT2) in astrocytes enhances neuroprotection from moderate but not severe hypoxia–ischemia. Neuroscience 155:1204–1211
21. Pinton P, Giorgi C, Siviero R, Zecchini E, Rizzuto R (2008) Calcium and apoptosis: ER-mitochondria Ca2 + transfer in the control of apoptosis. Oncogene 27:6407–6418
22. Ruiz A, Matute C, Alberdi E (2009) Endoplasmic reticulum Ca2 + release through ryanodine and IP3 receptors contributes to neuronal excitotoxicity. Cell Calcium 46:273–281
23. Green D, Galluzzi L, Kroemer G (2011) Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 333:1109–1112
24. Tait SWG, Green DR (2010) Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 11:621–632
25. Penna C, Perrelli M-G, Pagliaro P (2013) Mitochondrial pathways, permeability transition pore, and redox signaling in cardioprotection: therapeutic implications. Antioxid Redox Signal 18:556–599
26. Webster KA (2012) Mitochondrial membrane permeabilization and cell death during myocardial infarction: roles of calcium and reactive oxygen species. Future Cardiol 8:863–884
27. Giffard R, Han R, Emery J, Duan M, Pittet J (2008) Regulation of apoptotic and inflammatory cell signaling in cerebral ischemia: the complex roles of heat shock protein 70. Anesthesiology 109:339–348
28. Szabadkai G, Bianchi K, Várnai P, De Stefani D, Wieckowski MR, Cavagna D, Nagy AI, Balla T, Rizzuto R (2006) Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2 + channels. J Cell Biol 175:901–911
29. Voloboueva LA, Duan M, Ouyang Y, Emery JF, Stoy C, Giffard RG (2007) Overexpression of mitochondrial Hsp70/Hsp75 protects astrocytes against ischemic injury in vitro. J Cereb Blood Flow Metab 28:1009–1016
30. Xu L, Voloboueva LA, Ouyang Y, Emery JF, Giffard RG (2009) Overexpression of mitochondrial Hsp70/Hsp75 in rat brain protects mitochondria, reduces oxidative stress, and protects from focal ischemia. J Cereb Blood Flow Metab 29:365–374
31. Sun F-C, Wei S, Li C-W, Chang Y-S, Chao C–C, Lai Y-K (2006) Localization of GRP78 to mitochondria under the unfolded protein response. Biochem J 396:31–39
32. Ouyang Y, Xu L, Emery J, Lee A, Giffard R (2011) Overexpressing GRP78 influences Ca2 + handling and function of mitochondria in astrocytes after ischemia-like stress. Mitochondrion 11:279–286
33. Adams J, Cory S (2007) Bcl-2-regulated apoptosis: mechanism and therapeutic potential. Curr Opin Immunol 19:488–496
34. Parsons M, Green D (2010) Mitochondria in cell death. Essays Biochem 47:99–114
35. Kitagawa K, Matsumoto M, Tsujimoto Y, Ohtsuki T, Kuwabara K, Matsushita K, Yang G, Tanabe H, Martinou J, Hori M, Yanagihara T (1998) Amelioration of hippocampal neuronal damage after global ischemia by neuronal overexpression of BCL-2 in transgenic mice. Stroke 29:2616–2621
36. Zhao H, Yenari MA, Cheng D, Sapolsky RM, Steinberg GK (2003) Bcl-2 overexpression protects against neuron loss within the ischemic margin following experimental stroke and inhibits cytochrome c translocation and caspase-3 activity. J Neurochem 85:1026–1036
37. Ouyang Y, Carriedo S, Giffard R (2002) Effect of Bcl-x(L) overexpression on reactive oxygen species, intracellular calcium, and mitochondrial membrane potential following injury in astrocytes. Free Radic Biol Med 33:544–551
38. Szegezdi E, MacDonald DC, Chonghaile TNí, Gupta S, Samali A (2009) Bcl-2 family on guard at the ER. Am J Physiol Cell Physiol 296:C941–C953
39. Ouyang Y, Giffard R (2012) ER-mitochondria crosstalk during cerebral ischemia: molecular chaperones and ER-mitochondrial calcium transfer. Int J Cell Biol 2012:493934
40. Ouyang Y, Stary C, Yang G, Giffard R (2013) Micrornas: innovative targets for cerebral ischemia and stroke. Curr Drug Targets 14:90–101
41. Hertz L (2008) Bioenergetics of cerebral ischemia: a cellular perspective. Neuropharmacology 55:289–309
42. Simpson IA, Carruthers A, Vannucci SJ (2007) Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J Cereb Blood Flow Metab 27:1766–1791
43. Hertz L, Dienel G (2002) Energy metabolism in the brain. Int Rev Neurobiol 51:1–102
44. Wender R, Brown AM, Fern R, Swanson RA, Farrell K, Ransom BR (2000) Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter. J Neurosci 20:6804–6810
45. Fox P, Raichle M, Mintun M, Dence C (1988) Nonoxidative glucose consumption during focal physiologic neural activity. Science 241:462–464
46. Pellerin L, Magistretti P (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci USA 91:10625–10629
47. Amato S, Man H (2011) Bioenergy sensing in the brain: the role of AMP-activated protein kinase in neuronal metabolism, development and neurological diseases. Cell Cycle 10:3452–3460
48. An J, Haile W, Wu F, Torre E, Yepes M (2014) Tissue-type plasminogen activator mediates neuroglial coupling in the central nervous system. Neuroscience 257:41–48
49. Rose CR, Ransom BR (1997) Gap junctions equalize intracellular Na + concentration in astrocytes. Glia 20:299–307
50. Nakase T, Sohl G, Theis M, Willecke K, Naus C (2004) Increased apoptosis and inflammation after focal brain ischemia in mice lacking connexin43 in astrocytes. Am J Pathol 164:2067–2075
51. Martinez A, Saez J (2000) Regulation of astrocyte gap junctions by hypoxia-reoxygenation. Brain Res Brain Res Rev 32:250–258
52. Lin J, Weigel H, Cotrina M, Liu S, Bueno E, Hansen A, Hansen T, Goldman S, Nedergaard M (1998) Gap-junction-mediated propagation and amplification of cell injury. Nat Neurosci 1:494–500
53. Janssen H, Reesink H, Lawitz E, Zeuzem S, Rodriguez-Torres M, Patel K, van der Meer A, Patick A, Chen A, Zhou Y, Persson R, King B, Kauppinen S, Levin A, Hodges M (2013) Treatment of HCV infection by targeting microRNA. N Engl J Med 368:1685–1694
54. Dharap A, Bowen K, Place R, Li L, Vemuganti R (2009) Transient focal ischemia induces extensive temporal changes in rat cerebral microRNAome. J Cereb Blood Flow Metab 29:675–687
55. Jeyaseelan K, Lim K, Armugam A (2008) MicroRNA expression in the blood and brain of rats subjected to transient focal ischemia by middle cerebral artery occlusion. Stroke 39:959–966
56. Liu D, Tian Y, Ander B, Xu H, Stamova B, Zhan X, Turner R, Jickling G, Sharp F (2010) Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J Cereb Blood Flow Metab 30:92–101
57. Kernagis D, Laskowitz D (2012) Evolving role of biomarkers in acute cerebrovascular disease. Ann Neurol 71:289–303
58. Chopp M, Li Y (1996) Apoptosis in focal cerebral ischemia. Acta Neurochir Suppl 66:21–26
59. Mattson M, Culmsee C, Yu Z (2000) Apoptotic and antiapoptotic mechanisms in stroke. Cell Tissue Res 301:173–187
60. Yin K-J, Deng Z, Huang H, Hamblin M, Xie C, Zhang J, Chen YE (2010) MiR-497 regulates neuronal death in mouse brain after transient focal cerebral ischemia. Neurobiol Dis 38:17–26
61. Jovicic A, Roshan R, Moisoi N, Pradervand S, Moser R, Pillai B, Luthi-Carter R (2013) Comprehensive expression analyses of neural cell-type-specific miRNAs identify new determinants of the specification and maintenance of neuronal phenotypes. J Neurosci 33:5127–5137
62. Ouyang Y, Xu L, Lu Y, Sun X, Yue S, Xiong X, Giffard R (2013) Astrocyte-enriched miR-29a targets PUMA and reduces neuronal vulnerability to forebrain ischemia. Glia 61:1784–1794
63. Hutchison E, Kawamoto E, Taub D, Lal A, Abdelmohsen K, Zhang Y, Wood Wr, Lehrmann E, Camandola S, Becker K, Gorospe M, Mattson M (2013) Evidence for miR-181 involvement in neuroinflammatory responses of astrocytes. Glia 61:1018–1028
64. Ouyang Y, Xu L, Yue S, Liu S, Giffard R (2014) Neuroprotection by astrocytes in brain ischemia: importance of microRNAs. Neurosci Lett 565C:53–58
65. Ouyang Y, Lu Y, Yue S, Xu L, Xiong X, White R, Sun X, Giffard R (2012) miR-181 regulates GRP78 and influences outcome from cerebral ischemia in vitro and in vivo. Neurobiol Dis 45:555–563
66. Ouyang Y, Lu Y, Yue S, Giffard R (2012) miR-181 targets multiple Bcl-2 family members and influences apoptosis and mitochondrial function in astrocytes. Mitochondrion 12:213–219
67. Ouyang Y, Stary C, White R, Giffard R (2014) The use of microRNAs to modulate redox and immune response to stroke. Antioxid redox signal:epub ahead of print
68. Moon J, Xu L, Giffard R (2013) Inhibition of microRNA-181 reduces forebrain ischemia-induced neuronal loss. J Cereb Blood Flow Metab 33:1976–1982
69. Ye Y, Perez-Polo JR, Qian J, Birnbaum Y (2011) The role of microRNA in modulating myocardial ischemia-reperfusion injury. Physiol Genomics 43:534–542
70. Khanna S, Rink C, Ghoorkhanian R, Gnyawali S, Heigel M, Wijesinghe D, Chalfant C, Chan Y, Banerjee J, Huang Y, Roy S, Sen C (2013) Loss of miR-29b following acute ischemic stroke contributes to neural cell death and infarct size. J Cereb Blood Flow Metab 33:1197–1206
71. Sepramaniam S, Tan J-R, Tan K-S, DeSilva D, Tavintharan S, Woon F-P, Wang C-W, Yong F-L, Karolina D-S, Kaur P, Liu F-J, Lim K-Y, Armugam A, Jeyaseelan K (2014) Circulating microRNAs as biomarkers of acute stroke. Int J Mol Sci 15:1418–1432
72. Morel L, Regan M, Higashimori H, Ng S, Esau C, Vidensky S, Rothstein J, Yang Y (2013) Neuronal exosomal miRNA-dependent translational regulation of astroglial glutamate transporter GLT1. J Biol Chem 288:7105–7116