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Experimental Ischemia: Summary of Metabolic Encephalopathy

  • W. David Lust
  • Jennifer Zechel
  • Svetlana Pundik
Chapter

Abstract

Cerebral ischemia refers to a lack of adequate blood flow to the brain, which may be the result of an embolism, blood clot, blood vessel constriction secondary to increased intracranial pressure or a hemorrhage. Why the brain is so susceptible to alterations in Cerebral Blood Flow (CBF) has been extensively studied. The brain is a very demanding organ requiring an uninterrupted supply of nutrients to feed the tens of billions of cells which make up the CNS, necessary for the processing and storing of information and for controlling many vital functions within the organism. Maintaining the structure and function of this complex tissue requires a disproportionately large amount of energy when compared to most other organs of the body. This is clearly demonstrated by the fact that the brain comprises about 2% of total body mass and yet consumes about 20% of the total basal O2 and receives approximately 15% of the resting cardiac output. An important concept in normal brain metabolism is that energy production is tightly coupled to energy consumption (i.e., work).

Keywords

Cerebral Blood Flow Mitochondrial Permeability Transition Pore Ischemic Insult Global Ischemia Focal Ischemia 
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.

Reference

  1. Almeida, A., Allen, K.L., Bates, T.E., and Clark, J.B. (1995): Effect of reperfusion following cerebral ischaemia on the activity of the mitochondrial respiratory chain in the gerbil brain. J. Neurochem., 65:1698–1703.PubMedGoogle Scholar
  2. Antonsson, B., Montessuit, S., Lauper, S., Eskes, R., and Martinou, J.C. (2000): Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem. J., 345(Pt 2):271–278.PubMedGoogle Scholar
  3. Anderson GL and Whisnant JP. (1982): A comparison of trends in mortality from stroke in the United States and Rochester, Minnesota. Stroke. (6):804–9.Google Scholar
  4. Arai, H., Passonneau, J.V., and Lust, W.D. (1986): Energy metabolism in delayed neuronal death of CA1 neurons of the hippocampus following transient ischemia in the gerbil. Metab. Brain Dis., 1:263–278.PubMedGoogle Scholar
  5. Astrup, J., Siesjö, B.K., and Symon, L. (1981): Thresholds in cerebral ischemia — The ischemic penumbra. Stroke, 12(6):723–725.PubMedGoogle Scholar
  6. Astrup, J., Symon, L., Branston, N., and Lassen, N. (1977): Cortical evoked potential and extracellular K+ and H+ at critical levels of brain ischemia. Stroke, 8:51–57.PubMedGoogle Scholar
  7. Bazan, N.G. (2005): Synaptic signaling by lipids in the life and death of neurons. Mol. Neurobiol., 31:219–230.PubMedGoogle Scholar
  8. Berger, N.A. (1985): Poly(ADP-ribose) in the cellular response to DNA damage. Radiat. Res., 101:4–15.PubMedGoogle Scholar
  9. Betz, A.L., Randall, J., and Martz, D. (1991): Xanthine oxidase is not a major source of free radicals in focal cerebral ischemia. Am. J. Physiol., 260:H563–H568.PubMedGoogle Scholar
  10. Branston, N.M., Hope, D.T., and Symon, L. (1979): Barbiturates in focal ischemia of primate cortex: Effects on blood flow distribution, evoked potential and extracellular potassium. Stroke, 10:647–653.PubMedGoogle Scholar
  11. Branston, N.M., Symon, L., Crockard, H.A., and Pasztor, E. (1974): Relationship between the cortical evoked potential and local cortical blood flow following acute middle cerebral artery occlusion in the baboon. Exp. Neurol., 45:195–208.PubMedGoogle Scholar
  12. Camougrand, N., Grelaud-Coq, A., Marza, E., Priault, M., Bessoule, J.J., and Manon, S. (2003): The product of the UTH1 gene, required for Bax-induced cell death in yeast, is involved in the response to rapamycin. Mol. Microbiol., 47:495–506.Google Scholar
  13. Cardenas-Aguayo, M.C., Santa-Olalla, J., Baizabal, J.M., Salgado, L.M., and Covarrubias, L. (2003): Growth factor deprivation induces an alternative non-apoptotic death mechanism that is inhibited by Bcl2 in cells derived from neural precursor cells. J. Hematother. Stem Cell Res., 12:735–748.Google Scholar
  14. Carson, D.A., Seto, S., Wasson, D.B., and Carrera, C.J. (1986): DNA strand breaks, NAD metabolism, and programmed cell death. Exp. Cell Res., 164:273–281.PubMedGoogle Scholar
  15. Churn, S.B. and DeLorenzo, R.J. (1998): Intracellular Messengers and Mediators. In:Cerebrovascular Disease: Pathophysiology, Diagnosis and Management, Ginsberg MD et-al. (eds), pp. 433–439. Blackwell, Malden MA.Google Scholar
  16. Cory, S. and Adams, J.M. (2002): The Bcl2 family: Regulators of the cellular life-or-death switch. Nat. Rev. Cancer, 2:647–656.PubMedGoogle Scholar
  17. DeGracia, D.J. (2004): Acute and persistent protein synthesis inhibition following cerebral reperfusion. J. Neurosci. Res., 77:771–776.PubMedGoogle Scholar
  18. Degterev, A., Huang, Z., Boyce, M., Li, Y., Jagtap, P., Mizushima, N., Cuny, G.D., Mitchison, T.J., Moskowitz, M.A., and Yuan, J. (2005): Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol., 1:112–119.PubMedGoogle Scholar
  19. Deng, Y., Ren, X., Yang, L., Lin, Y., and Wu, X. (2003): A JNK-dependent pathway is required for TNFalpha-induced apoptosis. Cell, 115:61–70.PubMedGoogle Scholar
  20. Devin, A., Cook, A., Lin, Y., Rodriguez, Y., Kelliher, M., and Liu, Z. (2000): The distinct roles of TRAF2 and RIP in IKK activation by TNF-R1: TRAF2 recruits IKK to TNF-R1 while RIP mediates IKK activation. Immunity, 12:419–429.PubMedGoogle Scholar
  21. Devin, A., Lin, Y., and Liu, Z.G. (2003): The role of the death-domain kinase RIP in tumour-necrosis-factor-induced activation of mitogen-activated protein kinases. EMBO Rep., 4:623–627.PubMedGoogle Scholar
  22. Di Lisa, F. and Bernardi, P. (2005): Mitochondrial function and myocardial aging. A critical analysis of the role of permeability transition. Cardiovasc. Res., 66:222–232.PubMedGoogle Scholar
  23. Dirnagl, U., Simon, R.P., and Hallenbeck, J.M. (2003): Ischemic tolerance and endogenous neuroprotection. Trends Neurosci., 26:248–254.PubMedGoogle Scholar
  24. Eliasson, M.J., Huang, Z., Ferrante, R.J., Sasamata, M., Molliver, M.E., Snyder, S.H., and Moskowitz, M.A. (1999): Neuronal nitric oxide synthase activation and peroxynitrite formation in ischemic stroke linked to neural damage. J. Neurosci., 19:5910–5918.PubMedGoogle Scholar
  25. Elmore, S.P., Qian, T., Grissom, S.F., and Lemasters, J.J. (2001): The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J., 15:2286–2287.PubMedGoogle Scholar
  26. Erecinska, M. and Silver, I.A. (1989): ATP and brain function. J. Cereb. Blood Flow Metab., 9:2–19.PubMedGoogle Scholar
  27. Festjens, N., Vanden Berghe, T., and Vandenabeele, P. (2006): Necrosis, a well-orchestrated form of cell demise: Signalling cascades, important mediators and concomitant immune response. Biochim. Biophys. Acta, 1757:1371–1387.PubMedGoogle Scholar
  28. Flamm, E.S., Demopoulos, H.B., Seligman, M.L., Poser, R.G., and Ransohoff, J. (1978): Free radicals in cerebral ischemia. Stroke, 9:445–447.PubMedGoogle Scholar
  29. Folbergrova, J., Li, P.A., Uchino, H., Smith, M.L., and Siesjo, B.K. (1997): Changes in the bioenergetic state of rat hippocampus during 2.5 min of ischemia, and prevention of cell damage by cyclosporin A in hyperglycemic subjects. Exp. Brain Res., 114:44–50.PubMedGoogle Scholar
  30. Folbergrova, J., Memzawa, H., Smith, M.L., and Siesjo, B.K. (1992): Focal and perifocal changes in tissue energy state during middle cerebral artery occlusion in normo- and hyerglycemic rats. J. Cereb. Blood Flow Metab., 12:25–33.PubMedGoogle Scholar
  31. Folbergrova, J., Zhao, Q., Katsura, K., and Siesjo, B. (1995): N-tert-Buryl-a-phenylnitrone improves recovery of brain energy state in rats following transient focal ischemia. Proc. Natl. Acad. Sci. U S A., 92:5057–5061.PubMedGoogle Scholar
  32. Friberg, H. and Wieloch, T. (2002): Mitochondrial permeability transition in acute neurodegeneration. Biochimie, 84:241–250.PubMedGoogle Scholar
  33. Giffard, R.G., Monyer, H., Christine, C.W., and Choi, D.W. (1990): Acidosis reduces NMDA receptor activation, glutamate neurotoxicity, and oxygen-glucose deprivation neuronal injury in cortical cultures. Brain Res., 506:339–342.PubMedGoogle Scholar
  34. Ginsberg, M.D. and Bogousslavsky, J. (1998): Cerebrovascular Disease: Pathophysiology, Diagnosis and Management. Blackwell, Malden, MA.Google Scholar
  35. Gozuacik, D. and Kimchi, A. (2007): Autophagy and cell death. Curr. Top. Dev. Biol., 78:217–245.PubMedGoogle Scholar
  36. Graham, G.D. (2003): Tissue plasminogen activator for acute ischemic stroke in clinical practice: A meta-analysis of safety data. Stroke, 34:2847–2850.PubMedGoogle Scholar
  37. Gross, A., McDonnell, J.M., and Korsmeyer, S.J. (1999): BCL-2 family members and the mitochondria in apoptosis. Genes Dev., 13:1899–1911.PubMedGoogle Scholar
  38. Hamasaki, M., Noda, T., Baba, M., and Ohsumi, Y. (2005): Starvation triggers the delivery of the endoplasmic reticulum to the vacuole via autophagy in yeast. Traffic, 6:56–65.PubMedGoogle Scholar
  39. Harper, N., Hughes, M., MacFarlane, M., and Cohen, G.M. (2003): Fas-associated death domain protein and caspase-8 are not recruited to the tumor necrosis factor receptor 1 signaling complex during tumor necrosis factor-induced apoptosis. J. Biol. Chem., 278:25534–25541.PubMedGoogle Scholar
  40. Hata, R., Maeda, K., Hermann, D., Mies, G., and Hossmann, K.A. (2000): Evolution of brain infarction after transient focal cerebral ischemia in mice. J. Cereb. Blood Flow Metab., 20:937–946.PubMedGoogle Scholar
  41. Heiss, W.D., Hayakawa, T., and Waltz, A.G. (1976): Cortical neuronal function during ischemia. Effects of occlusion of one middle cerebral artery on single-unit activity in cats. Arch. Neurol., 33:813–820.PubMedGoogle Scholar
  42. Hoffman, T.L., LaManna, J.C., Pundik, S., Selman, W.R., Whittingham, T.S., Ratcheson, R.A., and Lust, W.D. (1994): Early reversal of acidosis and metabolic recovery following ischemia. J. Neurosurg., 81:567–573.PubMedGoogle Scholar
  43. Holler, N., Zaru, R., Micheau, O., Thome, M., Attinger, A., Valitutti, S., Bodmer, J.L., Schneider, P., Seed, B., and Tschopp, J. (2000): Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol., 1:489–495.PubMedGoogle Scholar
  44. Hossmann, K.A. (1998): Thresholds of Ischemic Injury. In: Cerebrovascular Disease: Pathophysiology, Diagnosis, and Management, Ginsberg, Met-al (eds), pp. 193–204. Blackwell, Malden.Google Scholar
  45. Hossmann, K.A. (2006): Pathophysiology and therapy of experimental stroke. Cell. Mol. Neurobiol., 26:1057–1083.PubMedGoogle Scholar
  46. Iwata, J., Ezaki, J., Komatsu, M., Yokota, S., Ueno, T., Tanida, I., Chiba, T., Tanaka, K., and Kominami, E. (2006): Excess peroxisomes are degraded by autophagic machinery in mammals. J. Biol. Chem., 281:4035–4041.PubMedGoogle Scholar
  47. Kagansky, N., Levy, S., and Knobler, H. (2001): The role of hyperglycemia in acute stroke. Arch. Neurol., 58:1209–1212.PubMedGoogle Scholar
  48. Kelliher, M.A., Grimm, S., Ishida, Y., Kuo, F., Stanger, B.Z., and Leder, P. (1998): The death domain kinase RIP mediates the TNF-induced NF-kappaB signal. Immunity, 8:297–303.PubMedGoogle Scholar
  49. Kempski, O., Otsuka, H., Seiwert, T., and Heimann, A. (2000): Spreading depression induces permanent cell swelling under penumbra conditions. Acta Neurochir. Suppl., 76:251–255.PubMedGoogle Scholar
  50. Kimelberg, H.K. (2005): Astrocytic swelling in cerebral ischemia as a possible cause of injury and target for therapy. Glia, 50:389–397.PubMedGoogle Scholar
  51. King, M.A. (1997): Pocket companion to robbins pathologic basis of disease — Robbins, SL, Cotran, RS, Kumar, V. N&Hc-Perspectives on Community, 18:99.[R21]Google Scholar
  52. Kirino, T. (1982): Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res., 239:57–69.PubMedGoogle Scholar
  53. Kirino, T. (2000): Delayed neuronal death. Neuropathology, 20 (Suppl):S95–S97PubMedGoogle Scholar
  54. Kobayashi, M., Lust, W.D., and Passonneau, J.V. (1977): Concentrations of energy metabolites and cyclic nucleotides during and after bilateral ischemia in the gerbil cerebral cortex. J. Neurochem., 29:53–59.PubMedGoogle Scholar
  55. Koumenis, C., Naczki, C., Koritzinsky, M., Rastani, S., Diehl, A., Sonenberg, N., Koromilas, A., and Wouters, B.G. (2002): Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol. Cell Biol., 22:7405–7416.PubMedGoogle Scholar
  56. Lapchak, P.A. and Araujo, D.M. (2007): Advances in ischemic stroke treatment: Neuroprotective and combination therapies. Expert Opin. Emerg. Drugs, 12:97–112.PubMedGoogle Scholar
  57. Leao, A.A.P. (1944): Spreading depression of activity in cerebral cortex. J. Neurophysiol., 7:359–390.Google Scholar
  58. Lee, C.K., Weindruch, R., and Prolla, T.A. (2000): Gene-expression profile of the ageing brain in mice. Nat. Genet., 25:294–297.PubMedGoogle Scholar
  59. Lehninger, A.L., Nelson, D.L., and Cos, M.M. (1993):. Worth Publishers, New York.Google Scholar
  60. Lemasters, J.J., Nieminen, A.L., Qian, T., Trost, L.C., Elmore, S.P., Nishimura, Y., Crowe, R.A., Cascio, W.E., Bradham, C.A., Brenner, D.A., and Herman, B. (1998): The mitochondrial permeability transition in cell death: A common mechanism in necrosis, apoptosis and autophagy. Biochim. Biophys. Acta, 1366:177–196.PubMedGoogle Scholar
  61. Levine, B. and Klionsky, D.J. (2004): Development by self-digestion: Molecular mechanisms and biological functions of autophagy. Dev. Cell, 6:463–477.PubMedGoogle Scholar
  62. Lewis, J., Devin, A., Miller, A., Lin, Y., Rodriguez, Y., Neckers, L., and Liu, Z.G. (2000): Disruption of hsp90 function results in degradation of the death domain kinase, receptor-interacting protein (RIP), and blockage of tumor necrosis factor-induced nuclear factor-kappaB activation. J. Biol. Chem., 275:10519–10526.PubMedGoogle Scholar
  63. Li, P.A., Kristian, T., Shamloo, M., and Siesjo, K. (1996): Effects of preischemic hyperglycemia on brain damage incurred by rats subjected to 2.5 or 5 minutes of forebrain ischemia. Stroke, 27:1592–1601.PubMedGoogle Scholar
  64. Lipton, P. (1999): Ischemic cell death in brain neurons. Physiol. Rev., 79:1431–1568.PubMedGoogle Scholar
  65. Lowry, O.H., Passonneau, J.V., Hasselberger, F.X., and Schulz, D.W. (1964): Effect of ischemia on known substrates and cofactors of the glycolytic pathway in brain. J. Biol. Chem., 239:18–30.PubMedGoogle Scholar
  66. Lust, W.D. and Passonneau, J.V. (1976): Cyclic nucleotides in murine brain: Effect of hypothermia on adenosine 3?,5? monophosphate, glycogen phosphorylase, glycogen synthase and metabolites following maximal electroshock or decapitation. J. Neurochem., 26:11–16.PubMedGoogle Scholar
  67. Lust, W.D., Taylor, C., Pundik, S., Selman, W.R., and Ratcheson, R.A. (2002): Ischemic cell death: Dynamics of delayed secondary energy failure during reperfusion following focal ischemia. Metab. Brain Dis., 17:113–121.PubMedGoogle Scholar
  68. Margaill, I., Plotkine, M., and Lerouet, D. (2005): Antioxidant strategies in the treatment of stroke. Free Radic. Biol. Med., 39:429–443.PubMedGoogle Scholar
  69. Martinez-Vila, E. and Irimia, P. (2005): Challenges of neuroprotection and neurorestoration in ischemic stroke treatment. Cerebrovasc. Dis., 20 (Suppl 2):148–158.PubMedGoogle Scholar
  70. Maundrell, K., Antonsson, B., Magnenat, E., Camps, M., Muda, M., Chabert, C., Gillieron, C., Boschert, U., Vial-Knecht, E., Martinou, J.C., and Arkinstall, S. (1997): Bcl-2 undergoes phosphorylation by c-Jun N-terminal kinase/stress-activated protein kinases in the ­presence of the constitutively active GTP-binding protein Rac1. J. Biol. Chem., 272:25238–25242.PubMedGoogle Scholar
  71. Mehta, S.L., Manhas, N., and Raghubir, R. (2007): Molecular targets in cerebral ischemia for developing novel therapeutics. Brain Res. Rev., 54:34–66.PubMedGoogle Scholar
  72. Mergenthaler, P., Dirnagl, U., and Meisel, A. (2004): Pathophysiology of stroke: Lessons from animal models. Metab. Brain Dis., 19:151–167.PubMedGoogle Scholar
  73. Melov, S. (2002): Animal models of oxidative stress, aging, and therapeutic antioxidant interventions. Int J Biochem Cell Biol., 34(11):1395–400.PubMedGoogle Scholar
  74. Meylan, E., Burns, K., Hofmann, K., Blancheteau, V., Martinon, F., Kelliher, M., and Tschopp, J. (2004): RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation. Nat. Immunol., 5:503–507.PubMedGoogle Scholar
  75. Morawetz, R.B., Crowell, R.H., DeGirolami, U., Marcoux, F.W., Jones, T.H., and Halsey, J.H. (1979): Regional cerebral blood flow thresholds during cerebral ischemia. Fed. Proc., 38:2493–2494.PubMedGoogle Scholar
  76. Morawetz, R.B., DeGirolami, U., Ojemann, R.G., Marcoux, F.W., and Crowell, R.M. (1978): Cerebral blood flow determined by hydrogen clearance during middle cerebral artery occlusion in unanesthetized monkeys. Stroke, 9:143–149.PubMedGoogle Scholar
  77. Mund, T., Gewies, A., Schoenfeld, N., Bauer, M.K., and Grimm, S. (2003): Spike, a novel BH3-only protein, regulates apoptosis at the endoplasmic reticulum. FASEB J., 17:696–698.PubMedGoogle Scholar
  78. Nitatori, T., Sato, N., Waguri, S., Karasawa, Y., Araki, H., Shibanai, K., Kominami, E., and Uchiyama, Y. (1995): Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J. Neurosci., 15:1001–1011.PubMedGoogle Scholar
  79. Nogawa, S., Zhang, F., Ross, M.E., and Iadecola, C. (1997): Cyclo-oxygenase-2 gene expression in neurons contributes to ischemic brain damage. J. Neurosci., 17:2746–2755.PubMedGoogle Scholar
  80. Oleinick, N.L. and Evans, H.H. (1985): Poly(ADP-ribose) and the response of cells to ionizing radiation. Radiat. Res., 101:29–46.PubMedGoogle Scholar
  81. Pelligrino, D.A. and Wang, Q. (1998): Cyclic nucleotide crosstalk and the regulation of cerebral vasodilation. Prog. Neurobiol., 56:1–18.PubMedGoogle Scholar
  82. Phillis, J.W., Diaz, F.G., O’Regan, M.H., and Pilitsis, J.G. (2002): Effects of immunosuppressants, calcineurin inhibition, and blockade of endoplasmic reticulum calcium channels on free fatty acid efflux from the ischemic/reperfused rat cerebral cortex. Brain Res., 957:12–24.PubMedGoogle Scholar
  83. Pundik, S., Robinson, S., Lust, W.D., Zechel, J., Buczek, M., Selman, W.R. (2006): Regional metabolic status of the E-18 rat fetal brain following transient hypoxia/ischemia. Metab Brain Dis., 21(4):309–17.PubMedGoogle Scholar
  84. Robins M, Baum HM. (1981) The National Survey of Stroke. Incidence. Stroke. (Suppl 1):I45–57.Google Scholar
  85. Sacco, R.L., Wolf, P.A., Kannel, W.B., McNamara, P.M. (1982): Survival and recurrence following stroke. The Framingham study. Stroke., 13(3):290–5.Google Scholar
  86. Saeki, K., Yuo, A., Okuma, E., Yazaki, Y., Susin, S.A., Kroemer, G., and Takaku, F. (2000): Bcl-2 down-regulation causes autophagy in a caspase-independent manner in human leukemic HL60 cells. Cell Death Differ., 7:1263–1269.PubMedGoogle Scholar
  87. Sastre, J., Pallardo, F.V., and Vina, J. (2003): The role of mitochondrial oxidative stress in aging. Free Radic. Biol. Med., 35:1–8.PubMedGoogle Scholar
  88. Selman, W.R., Crumrine, R.C., Ricci, A.J., LaManna, J.C., Ratcheson, R.A., and Lust, W.D. (1990): Impairment of metabolic recovery with increasing periods of middle cerebral artery occlusion in rats. Stroke, 21:467–471.PubMedGoogle Scholar
  89. Selman, W.R., Lust, W.D., Pundik, S., Zhou, Y., and Ratcheson, R.A. (2004): Compromised metabolic recovery following spontaneous spreading depression in the penumbra. Brain Res., 999:167–174.PubMedGoogle Scholar
  90. Selman, W.R., Zhou, Y., Pundik, S., Ratcheson, R.A., and Lust, W.D. (1999): A role for secondary energy failure in the evolution of ischemic cell death following reversible focal ischemia. J. Cereb. Blood Flow Metab., 19:S618.(Abstract)Google Scholar
  91. Shen, H.M., Lin, Y., Choksi, S., Tran, J., Jin, T., Chang, L., Karin, M., Zhang, J., and Liu, Z.G. (2004): Essential roles of receptor-interacting protein and TRAF2 in oxidative stress-induced cell death. Mol. Cell Biol., 24:5914–5922.PubMedGoogle Scholar
  92. Siesjo, B.K. (1978): Brain Energy Metabolism. Wiley, Chichester.Google Scholar
  93. Siesjo, B.K. (1992a): Pathophysiology and treatment of focal cerebral ischemia. Part II: Mechanisms of damage and treatment. J. Neurosurg., 77:337–354.Google Scholar
  94. Siesjo, B.K. (1992b): Pathophysiology and treatment of focal cerebral ischemia. Part I: Pathophysiology. J. Neurosurg., 77:169–184.Google Scholar
  95. Siesjo, B.K. and Bengtsson, F. (1989): Calcium fluxes, calcium antagonists, and calcium-related pathology in brain ischemia, hypoglycemia, and spreading depression: A unifying hypothesis. J. Cereb. Blood Flow Metab., 9:127–140.PubMedGoogle Scholar
  96. Siesjo, B.K., Elmer, E., Janelidze, S., Keep, M., Kristian, T., Ouyang, Y.B., and Uchino, H. (1999): Role and mechanisms of secondary mitochondrial failure. Acta Neurochir. Suppl. (Wien), 73:7–13.Google Scholar
  97. Siesjo, B.K., Kristian, T., and Katsura, K. (1998): Overview of Bioenergetic Failure and Metabolic Cascades in Brain Ischemia. In: Cerebrovascular Disease: Pathophysiology, Diagnosis and Management, Ginsberg M.D. et-al. (eds), pp.3–13. Blackwell, Malden, MA.Google Scholar
  98. Siesjo, B.K. and Siesjo, P. (1996): Mechanisms of secondary brain injury. Anasethesiology, 13:247–268.Google Scholar
  99. Sims, N.R. and Pulsinelli, W.A. (1987): Altered mitochondrial respiration in selectively vulnerable brain subregions following transient forebrain ischemia in the rat. J. Neurochem., 49:1367–1374.PubMedGoogle Scholar
  100. Strong, A.J. and Dardis, R. (2005): Depolarisation phenomena in traumatic and ischaemic brain injury. Adv. Tech. Stand. Neurosurg., 30:3–49.PubMedGoogle Scholar
  101. Symon, L., Pasztor, E., and Branston, N.M. (1974): The distribution and density of reduced cerebral blood flow following acute middle cerebral artery occlusion: An experimental study by the technique of hydrogen clearance in baboons. Stroke, 5:355–364.PubMedGoogle Scholar
  102. Takizawa, S., Fukuyama, N., Hirabayashi, H., Nakazawa, H., and Shinohara, Y. (1999): Dynamics of nitrotyrosine formation and decay in rat brain during focal ischemia-reperfusion. J. Cereb. Blood Flow Metab., 19:667–672.PubMedGoogle Scholar
  103. Talloczy, Z., Jiang, W., Virgin, H.W., Leib, D.A., Scheuner, D., Kaufman, R.J., Eskelinen, E.L., and Levine, B. (2002): Regulation of starvation- and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc. Natl. Acad. Sci. U S A, 99:190–195.PubMedGoogle Scholar
  104. Tanveer, A., Virji, S., Andreeva, L., Totty, N.F., Hsuan, J.J., Ward, J.M., and Crompton, M. (1996): Involvement of cyclophilin D in the activation of a mitochondrial pore by Ca2− and oxidant stress. Eur. J. Biochem., 238:166–172.PubMedGoogle Scholar
  105. Ting, A.T., Pimentel-Muinos, F.X., and Seed, B. (1996): RIP mediates tumor necrosis factor receptor 1 activation of NF-kappaB but not Fas/APO-1-initiated apoptosis. EMBO J., 15:6189–6196.PubMedGoogle Scholar
  106. Trivedi, B. and Danforth, W.H. (1966): Effect of pH on the kinetics of frog muscle phosphofructokinase. J. Biol. Chem., 241:4110–4112.PubMedGoogle Scholar
  107. Tsujimoto, Y. and Shimizu, S. (2000): VDAC regulation by the Bcl-2 family of proteins. Cell Death Differ., 7:1174–1181.PubMedGoogle Scholar
  108. Vande, V.C., Cizeau, J., Dubik, D., Alimonti, J., Brown, T., Israels, S., Hakem, R., and Greenberg, A.H. (2000): BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol. Cell Biol., 20:5454–5468.Google Scholar
  109. Vanden Berghe, T., Kalai, M., Denecker, G., Meeus, A., Saelens, X., and Vandenabeele, P. (2006): Necrosis is associated with IL-6 production but apoptosis is not. Cell Signal., 18:328–335.PubMedGoogle Scholar
  110. Veech, R.L., Lawson, J.W., Cornell, N.W., and Krebs, H.A. (1979): Cytosolic phosphorylation potential. J. Biol. Chem., 254:6538–6547.PubMedGoogle Scholar
  111. Walker, G. and Marx, J.L. (1981): The national surveyof stroke: Clinical findings. Stroke, 12(supp 1):1–13.Google Scholar
  112. Wallace, D. (2001): A mitochondrial paradigm for degenerative diseases and ageing. Novartis Found Symp., 235:247–63.PubMedGoogle Scholar
  113. Welsch, K.M., Caplan, L., Reis, D., Siesjo, B.K., and Weir, R. (1997): Primer on Cerebrovascular Disease. Academic Press, San Diego, CA.Google Scholar
  114. Xu, Y., Huang, S., Liu, Z.G., and Han, J. (2006): Poly(ADP-ribose) polymerase-1 signaling to mitochondria in necrotic cell death requires RIP1/TRAF2-mediated JNK1 activation. J. Biol. Chem., 281:8788–8795.PubMedGoogle Scholar
  115. Xu, K., Puchowicz, M.A., Lust, W.D., and LaManna, J.C. (2006): Adenosine treatment delays postischemic hippocampal CA1 loss after cardiac arrest and resuscitation in rats. Brain Res., 1071:208–217.PubMedGoogle Scholar
  116. Yang, H. and Smith, D.L. (1997): Kinetics of cytochrome c folding examined by hydrogen exchange and mass spectrometry. Biochemistry, 36:14992–14999.PubMedGoogle Scholar
  117. Yu, L., Alva, A., Su, H., Dutt, P., Freundt, E., Welsh, S., Baehrecke, E.H., and Lenardo, M.J. (2004): Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science, 304:1500–1502.PubMedGoogle Scholar
  118. Yu, L., Wan, F., Dutta, S., Welsh, S., Liu, Z., Freundt, E., Baehrecke, E.H., and Lenardo, M. (2006): Autophagic programmed cell death by selective catalase degradation. Proc. Natl. Acad. Sci. U S A, 103:4952–4957.PubMedGoogle Scholar
  119. Zaidan, E. and Sims, N.R. (1994): The calcium content of mitochondria from brain subregions following short-term forebrain ischemia and recirculation in the rat. J. Neurochem., 63:1812–1819.PubMedGoogle Scholar
  120. Zhang, S.Q., Kovalenko, A., Cantarella, G., and Wallach, D. (2000): Recruitment of the IKK signalosome to the p55 TNF receptor: RIP and A20 bind to NEMO (IKKgamma) upon receptor stimulation. Immunity, 12:301–311.PubMedGoogle Scholar
  121. Zhu, C., Wang, X., Xu, F., Bahr, B.A., Shibata, M., Uchiyama, Y., Hagberg, H., and Blomgren, K. (2005): The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death. Differ., 12:162–176.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • W. David Lust
    • 1
  • Jennifer Zechel
    • 1
  • Svetlana Pundik
    • 2
  1. 1.Department of Neurological SurgeryLaboratory of Experimental Neurological Surgery, Case Western Reserve UniversityClevelandUSA
  2. 2.University Hospitals of ClevelandClevelandUSA

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