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Stroke – A Synaptic Perspective

  • Robert Meller
  • Roger P. Simon

Keywords

NMDA Receptor Dendritic Spine Ischemic Precondition Global Ischemia Spreading Depression 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. N Engl J Med 333: 1581–1587, 1995.Google Scholar
  2. 2.
    Aarts M, Liu Y, Liu L, Besshoh S, Arundine M, Gurd JW, Wang YT, Salter MW, and Tymianski M. Treatment of ischemic brain damage by perturbing NMDA receptor- PSD-95 protein interactions. Science 298: 846–850, 2002.PubMedGoogle Scholar
  3. 3.
    Abe H and Nowak TS, Jr. Gene expression and induced ischemic tolerance following brief insults. Acta Neurobiol Exp 56: 3–8, 1996.Google Scholar
  4. 4.
    Back SA, Han BH, Luo NL, Chricton CA, Xanthoudakis S, Tam J, Arvin KL, and Holtzman DM. Selective vulnerability of late oligodendrocyte progenitors to hypoxiaischemia. J Neurosci 22: 455–463, 2002.PubMedGoogle Scholar
  5. 5.
    Barone FC, White RF, Spera PA, Ellison J, Currie RW, Wang X, and Feuerstein GZ. Ischemic preconditioning and brain tolerance: temporal histological and functional outcomes, protein synthesis requirement, and interleukin-1 receptor antagonist and early gene expression. Stroke 29: 1937–1950; discussion 1950–1931, 1998.PubMedGoogle Scholar
  6. 6.
    Biegon A, Fry PA, Paden CM, Alexandrovich A, Tsenter J, and Shohami E. Dynamic changes in N-methyl-D-aspartate receptors after closed head injury in mice: Implications for treatment of neurological and cognitive deficits. Proc Natl Acad Sci USA 101: 5117– 5122, 2004.PubMedGoogle Scholar
  7. 7.
    Bond A, Lodge D, Hicks CA, Ward MA, and O’Neill MJ. NMDA receptor antagonism, but not AMPA receptor antagonism attenuates induced ischaemic tolerance in the gerbil hippocampus. Eur J Pharmacol 380: 91–99, 1999.PubMedGoogle Scholar
  8. 8.
    Bossenmeyer C, Chihab R, Muller S, Schroeder H, and Daval JL. Hypoxia/reoxygenation induces apoptosis through biphasic induction of protein synthesis in cultured rat brain neurons. Brain Res 787: 107–116, 1998.PubMedGoogle Scholar
  9. 9.
    Brott T and Bogousslavsky J. Treatment of acute ischemic stroke. N Engl J Med 343: 710–722, 2000.PubMedGoogle Scholar
  10. 10.
    Brown CE, Li P, Boyd JD, Delaney KR, and Murphy TH. Extensive turnover of dendritic spines and vascular remodeling in cortical tissues recovering from stroke. J Neurosci 27: 4101–4109, 2007.PubMedGoogle Scholar
  11. 11.
    Buchan AM and Pulsinelli WA. Septo-hippocampal deafferentation protects CA1 neurons against ischemic injury. Brain Res 512: 7–14, 1990.PubMedGoogle Scholar
  12. 12.
    Buddle M, Eberhardt E, Ciminello LH, Levin T, Wing R, DiPasquale K, and Raley- Susman KM. Microtubule-associated protein 2 (MAP2) associates with the NMDA receptor and is spatially redistributed within rat hippocampal neurons after oxygenglucose deprivation. Brain Res 978: 38–50, 2003.PubMedGoogle Scholar
  13. 13.
    Cao G, Clark RS, Pei W, Yin W, Zhang F, Sun FY, Graham SH, and Chen J. Translocation of apoptosis-inducing factor in vulnerable neurons after transient cerebral ischemia and in neuronal cultures after oxygen-glucose deprivation. J Cereb Blood Flow Metab 23: 1137–1150, 2003.PubMedGoogle Scholar
  14. 14.
    Carmichael ST. Rodent models of Focal Stroke: Size, Mechanism and Purpose. NeuroRx 2: 396–409, 2005.PubMedGoogle Scholar
  15. 15.
    Centonze D, Saulle E, Pisani A, Bernardi G, and Calabresi P. Adenosine-mediated inhibition of striatal GABAergic synaptic transmission during in vitro ischaemia. Brain 124: 1855–1865, 2001.PubMedGoogle Scholar
  16. 16.
    Chen J, Graham SH, Zhu RL, and Simon RP. Stress proteins and tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 16: 566–577, 1996.PubMedGoogle Scholar
  17. 17.
    Cheung HH, Takagi N, Teves L, Logan R, Wallace MC, and Gurd JW. Altered association of protein tyrosine kinases with postsynaptic densities after transient cerebral ischemia in the rat brain. J Cereb Blood Flow Metab 20: 505–512, 2000.PubMedCrossRefGoogle Scholar
  18. 18.
    Choi DW. Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage. Trends Neurosci 11: 465–469, 1988.PubMedGoogle Scholar
  19. 19.
    Congar P, Gaiarsa JL, Popovici T, Ben-Ari Y, and Crepel V. Permanent reduction of seizure threshold in post-ischemic CA3 pyramidal neurons. J Neurophysiol 83: 2040– 2046, 2000.PubMedGoogle Scholar
  20. 20.
    Corbett D, Giles T, Evans S, McLean J, and Biernaskie J. Dynamic changes in CA1 dendritic spines associated with ischemic tolerance. Exp Neurol 202: 133–138, 2006.PubMedGoogle Scholar
  21. 21.
    Crepel V, Congar P, Aniksztejn L, Gozlan H, Hammond C, and Ben-Ari Y. Synaptic plasticity in ischemia: role of NMDA receptors. Prog Brain Res 116: 273–285, 1998.PubMedCrossRefGoogle Scholar
  22. 22.
    Crepel V, Epsztein J, and Ben-Ari Y. Ischemia induces short- and long-term remodeling of synaptic activity in the hippocampus. J Cell Mol Med 7: 401–407, 2003.PubMedGoogle Scholar
  23. 23.
    Currie RW, Ellison JA, White RF, Feuerstein GZ, Wang X, and Barone FC. Benign focal ischemic preconditioning induces neuronal Hsp70 and prolonged astrogliosis with expression of Hsp27. Brain Res 863: 169–181, 2000.PubMedGoogle Scholar
  24. 24.
    Dawson LA, Djali S, Gonzales C, Vinegra MA, and Zaleska MM. Characterization of transient focal ischemia-induced increases in extracellular glutamate and aspartate in spontaneously hypertensive rats. Brain Res Bull 53: 767-776, 2000.PubMedGoogle Scholar
  25. 25.
    del Zoppo GJ. Microvascular changes during cerebral ischemia and reperfusion. Cerebrovasc Brain Metab Rev 6: 47–96, 1994.PubMedGoogle Scholar
  26. 26.
    Diemer NH and Ekstrom von Lubitz DK. Cerebral ischaemia in the rat: increased permeability of post-synaptic membranes to horseradish peroxidase in the early postischaemic period. Neuropathol Appl Neurobiol 9: 403–414, 1983.PubMedGoogle Scholar
  27. 27.
    Dirnagl U. Bench to bedside: the quest for quality in experimental stroke research. J Cereb Blood Flow Metab 26: 1465–1478, 2006.PubMedGoogle Scholar
  28. 28.
    Dirnagl U, Iadecola C, and Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22: 391–397, 1999.PubMedGoogle Scholar
  29. 29.
    Dirnagl U, Simon RP, and Hallenbeck JM. Ischemic tolerance and endogenous neuroprotection. Trends Neurosci 26: 248–254, 2003.PubMedGoogle Scholar
  30. 30.
    Ehlers MD. Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6: 231–242, 2003.PubMedGoogle Scholar
  31. 31.
    Ekstrom von Lubitz DK and Diemer NH. Complete cerebral ischaemia in the rat: an ultrastructural and stereological analysis of the distal stratum radiatum in the hippocampal CA-1 region. Neuropathol Appl Neurobiol 8: 197–215, 1982.PubMedGoogle Scholar
  32. 32.
    Faddis BT, Hasbani MJ, and Goldberg MP. Calpain activation contributes to dendritic remodeling after brief excitotoxic injury in vitro. J Neurosci 17: 951–959, 1997.PubMedGoogle Scholar
  33. 33.
    Fannjiang Y, Kim CH, Huganir RL, Zou S, Lindsten T, Thompson CB, Mito T, Traystman RJ, Larsen T, Griffin DE, Mandir AS, Dawson TM, Dike S, Sappington AL, Kerr DA, Jonas EA, Kaczmarek LK, and Hardwick JM. BAK Alters Neuronal Excitability and Can Switch from Anti- to Pro-Death Function during Postnatal Development. Dev Cell 4: 575–585, 2003.PubMedGoogle Scholar
  34. 34.
    Ferrer I and Planas AM. 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, 2003.PubMedGoogle Scholar
  35. 35.
    Fisher M, Hanley DF, Howard G, Jauch EC, and Warach S. Recommendations from the STAIR V meeting on acute stroke trials, technology and outcomes. Stroke 38: 245–248, 2007.PubMedGoogle Scholar
  36. 36.
    Freeland K, Boxer LM, and Latchman DS. The cyclic AMP response element in the Bcl- 2 promoter confers inducibility by hypoxia in neuronal cells. Brain Res Mol Brain Res 92: 98–106, 2001.PubMedGoogle Scholar
  37. 37.
    Gao TM, Howard EM, and Xu ZC. Transient neurophysiological changes in CA3 neurons and dentate granule cells after severe forebrain ischemia in vivo. J Neurophysiol 80: 2860–2869, 1998.PubMedGoogle Scholar
  38. 38.
    Gao TM, Pulsinelli WA, and Xu ZC. Prolonged enhancement and depression of synaptic transmission in CA1 pyramidal neurons induced by transient forebrain ischemia in vivo. Neuroscience 87: 371–383, 1998.PubMedGoogle Scholar
  39. 39.
    Gascon S, Sobrado M, Roda JM, Rodriguez-Pena A, and Diaz-Guerra M. Excitotoxicity and focal cerebral ischemia induce truncation of the NR2A and NR2B subunits of the NMDA receptor and cleavage of the scaffolding protein PSD-95. Mol Psychiatry, 13: 99–14, 2007.PubMedGoogle Scholar
  40. 40.
    Giffard RG and Swanson RA. Ischemia-induced programmed cell death in astrocytes. Glia 50: 299–306, 2005.PubMedGoogle Scholar
  41. 41.
    Gomez-Lazaro M, Galindo MF, Melero-Fernandez de Mera RM, Fernandez-Gomez FJ, Concannon CG, Segura MF, Comella JX, Prehn JH, and Jordan J. Reactive oxygen species and p38 mitogen-activated protein kinase activate Bax to induce mitochondrial cytochrome c release and apoptosis in response to malonate. Mol Pharmacol 71: 736– 743, 2007.PubMedGoogle Scholar
  42. 42.
    Gonzalez-Zulueta M, Feldman AB, Klesse LJ, Kalb RG, Dillman JF, Parada LF, Dawson TM, and Dawson VL. Requirement for nitric oxide activation of p21(ras)/extracellular regulated kinase in neuronal ischemic preconditioning. Proc Natl Acad Sci USA 97: 436–441, 2000.PubMedGoogle Scholar
  43. 43.
    Grabb MC and Choi DW. Ischemic tolerance in murine cortical cell culture: critical role for NMDA receptors. J Neurosci 19: 1657–1662, 1999.PubMedGoogle Scholar
  44. 44.
    Graber S, Maiti S, and Halpain S. Cathepsin B-like proteolysis and MARCKS degradation in sub-lethal NMDA-induced collapse of dendritic spines. Neuropharmacology 47: 706–713, 2004.PubMedGoogle Scholar
  45. 45.
    Graham SH and Chen J. Programmed cell death in cerebral ischemia. J Cereb Blood Flow Metab 21: 99–109, 2001.PubMedGoogle Scholar
  46. 46.
    Greenberg DA, Aminoff MJ, and R.P.Simon. Stroke. In: Clinical Neurology, edited by Greenberg DA, Aminoff MJ, and R.P.Simon: Lange medical Books/McGraw-Hill, pp. 282–316, 2002.Google Scholar
  47. 47.
    Gregersen R, Christensen T, Lehrmann E, Diemer NH, and Finsen B. Focal cerebral ischemia induces increased myelin basic protein and growth-associated protein-43 gene transcription in peri-infarct areas in the rat brain. Exp Brain Res 138: 384–392, 2001.PubMedGoogle Scholar
  48. 48.
    Hara T, Hamada J, Yano S, Morioka M, Kai Y, and Ushio Y. CREB is required for acquisition of ischemic tolerance in gerbil hippocampal CA1 region. J Neurochem 86: 805–814, 2003.PubMedGoogle Scholar
  49. 49.
    Hardingham GE and Bading H. Coupling of extrasynaptic NMDA receptors to a CREB shut-off pathway is developmentally regulated. Biochim Biophys Acta 1600: 148–153, 2002.PubMedGoogle Scholar
  50. 50.
    Hardingham GE, Fukunaga Y, and Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5: 405– 414, 2002.PubMedGoogle Scholar
  51. 51.
    Hargreaves RJ, Hill RG, and Iversen LL. Neuroprotective NMDA antagonists: the controversy over their potential for adverse effects on cortical neuronal morphology. Acta Neurochir Suppl (Wien) 60: 15–19, 1994.Google Scholar
  52. 52.
    Hasbani MJ, Schlief ML, Fisher DA, and Goldberg MP. Dendritic spines lost during glutamate receptor activation reemerge at original sites of synaptic contact. J Neurosci 21: 2393–2403, 2001.PubMedGoogle Scholar
  53. 53.
    Hasbani MJ, Viquez NM, and Goldberg MP. NMDA receptors mediate hypoxic spine loss in cultured neurons. Neuroreport 12: 2731–2735, 2001.PubMedGoogle Scholar
  54. 54.
    Henshall DC, Butcher SP, and Sharkey J. A rat model of endothelin-3-induced middle cerebral artery occlusion with controlled reperfusion. Brain Res 843: 105–111, 1999.PubMedGoogle Scholar
  55. 55.
    Hillion JA, Li Y, Maric D, Takanohashi A, Klimanis D, Barker JL, and Hallenbeck JM. Involvement of Akt in preconditioning-induced tolerance to ischemia in PC12 cells. J Cereb Blood Flow Metab 26: 1323–1331, 2006.PubMedGoogle Scholar
  56. 56.
    Hillion JA, Takahashi K, Maric D, Ruetzler C, Barker JL, and Hallenbeck JM. Development of an ischemic tolerance model in a PC12 cell line. J Cereb Blood Flow Metab 25: 154–162, 2005.PubMedGoogle Scholar
  57. 57.
    Hills CP. The Ultrastructure of Anoxic-Ischaemic Lesions in the Cerebral Cortex of the Adult Rat Brain. Guys Hosp Rep 113: 333–348, 1964.PubMedGoogle Scholar
  58. 58.
    Horner CH, Davies HA, and Stewart MG. Hippocampal synaptic density and glutamate immunoreactivity following transient cerebral ischaemia in the chick. Eur J Neurosci 10: 3913–3917, 1998.PubMedGoogle Scholar
  59. 59.
    Hossmann KA. Pathophysiology and therapy of experimental stroke. Cell Mol Neurobiol 26: 1057–1083, 2006.PubMedGoogle Scholar
  60. 60.
    Hou XY, Zhang GY, and Zong YY. Suppression of postsynaptic density protein 95 expression attenuates increased tyrosine phosphorylation of NR2A subunits of Nmethyl- D-aspartate receptors and interactions of Src and Fyn with NR2A after transient brain ischemia in rat hippocampus. Neurosci Lett 343: 125–128, 2003.PubMedGoogle Scholar
  61. 61.
    Hoyte L, Barber PA, Buchan AM, and Hill MD. The rise and fall of NMDA antagonists for ischemic stroke. Curr Mol Med 4: 131–136, 2004.PubMedGoogle Scholar
  62. 62.
    Hu BR, Martone ME, Jones YZ, and Liu CL. Protein aggregation after transient cerebral ischemia. J Neurosci 20: 3191–3199, 2000.PubMedGoogle Scholar
  63. 63.
    Hu XL, Olsson T, Johansson IM, Brannstrom T, and Wester P. Dynamic changes of the anti- and pro-apoptotic proteins Bcl-w, Bcl-2, and Bax with Smac/Diablo mitochondrial release after photothrombotic ring stroke in rats. Eur J Neurosci 20: 1177–1188, 2004.PubMedGoogle Scholar
  64. 64.
    Ikegaya Y, Kim JA, Baba M, Iwatsubo T, Nishiyama N, and Matsuki N. Rapid and reversible changes in dendrite morphology and synaptic efficacy following NMDA receptor activation: implication for a cellular defense against excitotoxicity. J Cell Sci 114: 4083–4093, 2001. Stroke-A Synaptic PerspectPubMedGoogle Scholar
  65. 65.
    Jonas EA, Hoit D, Hickman JA, Brandt TA, Polster BM, Fannjiang Y, McCarthy E, Montanez MK, Hardwick JM, and Kaczmarek LK. Modulation of synaptic transmission by the BCL-2 family protein BCL-xL. J Neurosci 23: 8423–8431, 2003.PubMedGoogle Scholar
  66. 66.
    Kadotani H, Namura S, Katsuura G, Terashima T, and Kikuchi H. Attenuation of focal cerebral infarct in mice lacking NMDA receptor subunit NR2C. Neuroreport 9: 471–475, 1998.PubMedGoogle Scholar
  67. 67.
    Kirino T, Tamura A, and Sano K. Chronic maintenance of presynaptic terminals in gliotic hippocampus following ischemia. Brain Res 510: 17–25, 1990.PubMedGoogle Scholar
  68. 68.
    Lin CH, Lu YZ, Cheng FC, Chu LF, and Hsueh CM. Bax-regulated mitochondriamediated apoptosis is responsible for the in vitro ischemia induced neuronal cell death of Sprague Dawley rat. Neurosci Lett 387: 22–27, 2005.PubMedGoogle Scholar
  69. 69.
    Liou AKF, Clark RS, Henshall DC, Yin XM, and Chen J. To die or not to die for neurons in ischemia, traumatic brain injury and epilepsy: a review on the stress-activated signaling pathways and apoptotic pathways. Prog Neurobiol 69: 103–142, 2003.PubMedGoogle Scholar
  70. 70.
    Liu CL, Martone ME, and Hu BR. Protein ubiquitination in postsynaptic densities after transient cerebral ischemia. J Cereb Blood Flow Metab 24: 1219–1225, 2004.PubMedGoogle Scholar
  71. 71.
    Luque JM, Puig N, Martinez JM, Gonzalez-Garcia C, and Cena V. Glutamate N-methyl- D-aspartate receptor blockade prevents induction of GAP-43 after focal ischemia in rats. Neurosci Lett 305: 87–90, 2001.PubMedGoogle Scholar
  72. 72.
    Mabuchi T, Kitagawa K, Kuwabara K, Takasawa K, Ohtsuki T, Xia Z, Storm D, Yanagihara T, Hori M, and Matsumoto M. Phosphorylation of cAMP response elementbinding protein in hippocampal neurons as a protective response after exposure to glutamate in vitro and ischemia in vivo. J Neurosci 21: 9204–9213, 2001.PubMedGoogle Scholar
  73. 73.
    Magarinos AM, McEwen BS, Saboureau M, and Pevet P. Rapid and reversible changes in intrahippocampal connectivity during the course of hibernation in European hamsters. Proc Natl Acad Sci USA 103: 18775–18780, 2006.PubMedGoogle Scholar
  74. 74.
    Martone ME, Hu BR, and Ellisman MH. Alterations of hippocampal postsynaptic densities following transient ischemia. Hippocampus 10: 610–616, 2000.PubMedGoogle Scholar
  75. 75.
    McLaughlin B, Hartnett KA, Erhardt JA, Legos JJ, White RF, Barone FC, and Aizenman E. Caspase 3 activation is essential for neuroprotection in preconditioning. Proc Natl Acad Sci USA 100: 715–720, 2003.PubMedGoogle Scholar
  76. 76.
    Mehta SL, Manhas N, and Raghubir R. Molecular targets in cerebral ischemia for developing novel therapeutics. Brain Res Rev 54: 34–66, 2007.PubMedGoogle Scholar
  77. 77.
    Meldrum B. Excitotoxicity and epileptic brain damage. Epilepsy Res 10: 55–61, 1991.PubMedGoogle Scholar
  78. 78.
    Meldrum BS, Evans MC, Swan JH, and Simon RP. Protection against hypoxic/ischaemic brain damage with excitatory amino acid antagonists. Med Biol 65: 153–157, 1987.PubMedGoogle Scholar
  79. 79.
    Meller R, Cameron JA, Torrey DJ, Clayton CE, Ordonez AN, Henshall DC, Minami M, Schindler CK, Saugstad JA, and Simon RP. Rapid degradation of Bim by the ubiquitinproteasome pathway mediates short-term ischemic tolerance in cultured neurons. J Biol Chem 281: 7429–7436, 2006.PubMedGoogle Scholar
  80. 80.
    Meller R, Minami M, Cameron JA, Impey S, Chen D, Lan JQ, Henshall DC, and Simon RP. CREB-mediated Bcl-2 protein expression after ischemic preconditioning. J Cereb Blood Flow Metab 25: 234–246, 2005.PubMedGoogle Scholar
  81. 81.
    Minami M, Jin KL, Li W, Nagayama T, Henshall DC, and Simon RP. Bcl-w expression is increased in brain regions affected by focal cerebral ischemia in the rat. Neurosci Lett 279: 193–195, 2000.PubMedGoogle Scholar
  82. 82.
    Mitani A, Matsuda S, Yamamoto H, Sakanaka M, and Kataoka K. The role of remaining presynaptic terminals in the hippocampal CA1 after selective neuronal death: ischemiainduced glutamate efflux. Acta Neuropathol (Berl) 91: 41–46, 1996.Google Scholar
  83. 83.
    Mitani A, Namba S, Ikemune K, Yanase H, Arai T, and Kataoka K. Postischemic enhancements of N-methyl-D-aspartic acid (NMDA) and non-NMDA receptor-mediated 756 responses in hippocampal CA1 pyramidal neurons. J Cereb Blood Flow Metab 18: 1088–1098, 1998.PubMedGoogle Scholar
  84. 84.
    Miyazaki S, Katayama Y, Furuichi M, Kinoshita K, Kawamata T, and Tsubokawa T. Impairment of hippocampal long-term potentiation following transient cerebral ischaemia in rat: effects of bifemelane, a potent inhibitor of ischaemia-induced acetylcholine release. Neurol Res 15: 249–252, 1993.PubMedGoogle Scholar
  85. 85.
    Monyer H, Giffard RG, Hartley DM, Dugan LL, Goldberg MP, and Choi DW. Oxygen or glucose deprivation-induced neuronal injury in cortical cell cultures is reduced by tetanus toxin. Neuron 8: 967–973, 1992.PubMedGoogle Scholar
  86. 86.
    Olney JW. Glutamate-induced neuronal necrosis in the infant mouse hypothalamus. An electron microscopic study. J Neuropathol Exp Neurol 30: 75-90, 1971.PubMedGoogle Scholar
  87. 87.
    Olney JW and Ho OL. Brain damage in infant mice following oral intake of glutamate, aspartate or cysteine. Nature 227: 609–611, 1970.PubMedGoogle Scholar
  88. 88.
    Park JS, Bateman MC, and Goldberg MP. Rapid alterations in dendrite morphology during sublethal hypoxia or glutamate receptor activation. Neurobiol Dis 3: 215–227, 1996.PubMedGoogle Scholar
  89. 89.
    Perez-Pinzon MA and Born JG. Rapid preconditioning neuroprotection following anoxia in hippocampal slices: role of the K+ ATP channel and protein kinase C. Neuroscience 89: 453–459, 1999.PubMedGoogle Scholar
  90. 90.
    Perez-Pinzon MA, Vitro TM, Dietrich WD, and Sick TJ. The effect of rapid preconditioning on the microglial, astrocytic and neuronal consequences of global cerebral ischemia. Acta Neuropathol (Berl) 97: 495–501, 1999.Google Scholar
  91. 91.
    Picconi B, Tortiglione A, Barone I, Centonze D, Gardoni F, Gubellini P, Bonsi P, Pisani A, Bernardi G, Di Luca M, and Calabresi P. NR2B subunit exerts a critical role in postischemic synaptic plasticity. Stroke 37: 1895–1901, 2006.PubMedGoogle Scholar
  92. 92.
    Pignataro G, Simon RP, and Xiong ZG. Prolonged activation of ASIC1a and the time window for neuroprotection in cerebral ischaemia. Brain 130: 151–158, 2007.PubMedGoogle Scholar
  93. 93.
    Popov VI and Bocharova LS. Hibernation-induced structural changes in synaptic contacts between mossy fibres and hippocampal pyramidal neurons. Neuroscience 48: 53–62, 1992.PubMedGoogle Scholar
  94. 94.
    Pugazhenthi S, Nesterova A, Sable C, Heidenreich KA, Boxer LM, Heasley LE, and Reusch JE. Akt/protein kinase B up-regulates Bcl-2 expression through cAMP- response element-binding protein. J Biol Chem 275: 10761–10766, 2000.PubMedGoogle Scholar
  95. 95.
    Pulsinelli WA and Buchan AM. The four-vessel occlusion rat model: method for complete occlusion of vertebral arteries and control of collateral circulation. Stroke 19: 913–914, 1988.PubMedGoogle Scholar
  96. 96.
    Reshef A, Sperling O, and Zoref-Shani E. Activation and inhibition of protein kinase C protect rat neuronal cultures against ischemia-reperfusion insult. Neurosci Lett 238: 37– 40, 1997.PubMedGoogle Scholar
  97. 97.
    Rod MR and Auer RN. Pre- and post-ischemic administration of dizocilpine (MK-801) reduces cerebral necrosis in the rat. Can J Neurol Sci 16: 340–344, 1989.PubMedGoogle Scholar
  98. 98.
    Romera C, Hurtado O, Botella SH, Lizasoain I, Cardenas A, Fernandez-Tome P, Leza JC, Lorenzo P, and Moro MA. In vitro ischemic tolerance involves upregulation of glutamate transport partly mediated by the TACE/ADAM17-tumor necrosis factor-alpha pathway. J Neurosci 24: 1350–1357, 2004.PubMedGoogle Scholar
  99. 99.
    Ruscher K, Freyer D, Karsch M, Isaev N, Megow D, Sawitzki B, Priller J, Dirnagl U, and Meisel A. Erythropoietin is a paracrine mediator of ischemic tolerance in the brain: evidence from an in vitro model. J Neurosci 22: 10291–10301, 2002.PubMedGoogle Scholar
  100. 100.
    Sattler R, Xiong Z, Lu WY, MacDonald JF, and Tymianski M. Distinct roles of synaptic and extrasynaptic NMDA receptors in excitotoxicity. J Neurosci 20: 22–33, 2000.PubMedGoogle Scholar
  101. 101.
    Savitz SI. A critical appraisal of the NXY-059 neuroprotection studies for acute stroke: a need for more rigorous testing of neuroprotective agents in animal models of stroke. Exp Neurol 205: 20–25, 2007.PubMedGoogle Scholar
  102. 102.
    Savitz SI and Fisher M. Future of neuroprotection for acute stroke: in the aftermath of the SAINT trials. Ann Neurol 61: 396–402, 2007.PubMedGoogle Scholar
  103. 103.
    Selim M. Perioperative stroke. N Engl J Med 356: 706–713, 2007.PubMedGoogle Scholar
  104. 104.
    Shelton MK and McCarthy KD. Mature hippocampal astrocytes exhibit functional metabotropic and ionotropic glutamate receptors in situ. Glia 26: 1–11, 1999.PubMedGoogle Scholar
  105. 105.
    Shimizu S, Nagayama T, Jin KL, Zhu L, Loeffert JE, Watkins SC, Graham SH, and Simon RP. bcl-2 Antisense treatment prevents induction of tolerance to focal ischemia in the rat brain. J Cereb Blood Flow Metab 21: 233–243, 2001.PubMedGoogle Scholar
  106. 106.
    Sloviter RS. Apoptosis: a guide for the perplexed. Trends Pharmacol Sci 23: 19–24, 2002.PubMedGoogle Scholar
  107. 107.
    Small DL, Poulter MO, Buchan AM, and Morley P. Alteration in NMDA receptor subunit mRNA expression in vulnerable and resistant regions of in vitro ischemic rat hippocampal slices. Neurosci Lett 232: 87–90, 1997.PubMedGoogle Scholar
  108. 108.
    Somjen GG, Aitken PG, Czeh G, Jing J, and Young JN. Cellular physiology of hypoxia of the mammalian central nervous system. Res Publ Assoc Res Nerv Ment Dis 71: 51–65, 1993.PubMedGoogle Scholar
  109. 109.
    Stenzel-Poore MP, Stevens SL, King JS, and Simon RP. Preconditioning reprograms the response to ischemic injury and primes the emergence of unique endogenous neuroprotective phenotypes: a speculative synthesis. Stroke 38: 680–685, 2007.PubMedGoogle Scholar
  110. 110.
    Stenzel-Poore MP, Stevens SL, Xiong Z, Lessov NS, Harrington CA, Mori M, Meller R, Rosenzweig HL, Tobar E, Shaw TE, Chu X, and Simon RP. Effect of ischaemic preconditioning on genomic response to cerebral ischaemia: similarity to neuroprotective strategies in hibernation and hypoxia-tolerant states. Lancet 362: 1028–1037, 2003.PubMedGoogle Scholar
  111. 111.
    Sydserff SG, Borrelli AR, Palmer GC, and Cross AJ. Ischaemic tolerance is blocked by NMDA antagonism. Soc Neurosci Abstr 24: P87.86, 1998.Google Scholar
  112. 112.
    Takamatsu H, Kondo K, Ikeda Y, and Umemura K. Neuroprotective effects depend on the model of focal ischemia following middle cerebral artery occlusion. Eur J Pharmacol 362: 137–142, 1998.PubMedGoogle Scholar
  113. 113.
    Traystman RJ. Animal models of focal and global cerebral ischemia. Ilar J 44: 85–95, 2003.PubMedGoogle Scholar
  114. 114.
    von der Ohe CG, Darian-Smith C, Garner CC, and Heller HC. Ubiquitous and temperature-dependent neural plasticity in hibernators. J Neurosci 26: 10590–10598, 2006.PubMedGoogle Scholar
  115. 115.
    Vornov JJ, Tasker RC, and Coyle JT. Delayed protection by MK-801 and tetrodotoxin in a rat organotypic hippocampal culture model of ischemia. Stroke 25: 457–464; discussion 464–455, 1994.PubMedGoogle Scholar
  116. 116.
    Walton M, Woodgate AM, Muravlev A, Xu R, During MJ, and Dragunow M. CREB phosphorylation promotes nerve cell survival. J Neurochem 73: 1836–1842, 1999.PubMedGoogle Scholar
  117. 117.
    Weih M, Bergk A, Isaev NK, Ruscher K, Megow D, Riepe M, Meisel A, Victorov IV, and Dirnagl U. Induction of ischemic tolerance in rat cortical neurons by 3- nitropropionic acid: chemical preconditioning. Neurosci Lett 272: 207–210, 1999.PubMedGoogle Scholar
  118. 118.
    Williams V and Grossman RG. Ultrastructure of cortical synapses after failure of presynaptic activity in ischemia. Anat Rec 166: 131–141, 1970.PubMedGoogle Scholar
  119. 119.
    Wilson BE, Mochon E, and Boxer LM. Induction of bcl-2 expression by phosphorylated CREB proteins during B- cell activation and rescue from apoptosis. Mol Cell Biol 16: 5546–5556, 1996.PubMedGoogle Scholar
  120. 120.
    Wood PL and Hawkinson JE. N-methyl-D-aspartate antagonists for stroke and head trauma. Expert Opin Investig Drugs 6: 389–397, 1997.PubMedGoogle Scholar
  121. 121.
    Wu HY, Yuen EY, Lu YF, Matsushita M, Matsui H, Yan Z, and Tomizawa K. Regulation of N-methyl-D-aspartate receptors by calpain in cortical neurons. J Biol Chem 280: 21588–21593, 2005.PubMedGoogle Scholar
  122. 122.
    Yagita Y, Kitagawa K, Ohtsuki T, Tanaka S, Hori M, and Matsumoto M. Induction of the HSP110/105 family in the rat hippocampus in cerebral ischemia and ischemic tolerance. J Cereb Blood Flow Metab 21: 811–819, 2001.PubMedGoogle Scholar
  123. 123.
    Zhang L, Hsu JC, Takagi N, Gurd JW, Wallace MC, and Eubanks JH. Transient global ischemia alters NMDA receptor expression in rat hippocampus: correlation with decreased immunoreactive protein levels of the NR2A/2B subunits, and an altered NMDA receptor functionality. J Neurochem 69: 1983–1994, 1997.PubMedCrossRefGoogle Scholar
  124. 124.
    Zhang S, Boyd J, Delaney K, and Murphy TH. Rapid reversible changes in dendritic spine structure in vivo gated by the degree of ischemia. J Neurosci 25: 5333–5338, 2005.PubMedGoogle Scholar
  125. 125.
    Zhang S and Murphy TH. Imaging the impact of cortical microcirculation on synaptic structure and sensory-evoked hemodynamic responses in vivo. PLoS Biol 5: e119, 2007.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Robert Meller
    • 1
  • Roger P. Simon
    • 1
  1. 1.RS Dow Neurobiology Laboratory, Legacy Clinical Research and Technology CenterPortlandUSA

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