Generic placeholder image

Current Protein & Peptide Science

Editor-in-Chief

ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

Review Article

An Overview of Stroke: Mechanism, In vivo Experimental Models Thereof, and Neuroprotective Agents

Author(s): Mohd Muazzam Khan, Badruddeen*, Mohd Mujahid, Juber Akhtar, Mohammad Irfan Khan and Usama Ahmad

Volume 21, Issue 9, 2020

Page: [860 - 877] Pages: 18

DOI: 10.2174/1389203721666200617133903

Price: $65

Abstract

Background: Stroke is one of the causes of death and disability globally. Brain attack is because of the acute presentation of stroke, which highlights the requirement for decisive action to treat it.

Objective: The mechanism and in-vivo experimental models of stroke with various neuroprotective agents are highlighted in this review.

Method: The damaging mechanisms may proceed by rapid, nonspecific cell lysis (necrosis) or by the active form of cell death (apoptosis or necroptosis), depending upon the duration and severity and of the ischemic insult.

Results: Identification of injury mediators and pathways in a variety of experimental animal models of global cerebral ischemia has directed to explore the target-specific cytoprotective strategies, which are critical to clinical brain injury outcomes.

Conclusion: The injury mechanism, available encouraging medicaments thereof, and outcomes of natural and modern medicines for ischemia have been summarized. In spite of available therapeutic agents (thrombolytics, calcium channel blockers, NMDA receptor antagonists and antioxidants), there is a need for an ideal drug for strokes.

Keywords: Apoptosis, bilateral common carotid artery occlusion, cerebral ischemia, necroptosis, neuroprotection, stroke, NMDA.

Graphical Abstract

[1]
Nussmeier, N.A. A review of risk factors for adverse neurologic outcome after cardiac surgery. J. Extra Corpor. Technol., 2002, 34(1), 4-10.
[PMID: 11911628]
[2]
Bernard, S.A.; Gray, T.W.; Buist, M.D.; Jones, B.M.; Silvester, W.; Gutteridge, G.; Smith, K. Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N. Engl. J. Med., 2002, 346(8), 557-563.
[http://dx.doi.org/10.1056/NEJMoa003289] [PMID: 11856794]
[3]
Atochin, D.N.; Chernysheva, G.A.; Aliev, O.I.; Smolyakova, V.I.; Osipenko, A.N.; Logvinov, S.V.; Zhdankina, A.A.; Plotnikova, T.M.; Plotnikov, M.B. An improved three-vessel occlusion model of global cerebral ischemia in rats. Brain Res. Bull., 2017, 132, 213-221.
[http://dx.doi.org/10.1016/j.brainresbull.2017.06.005] [PMID: 28603012]
[4]
Luo, Y.; Tang, H.; Li, H.; Zhao, R.; Huang, Q.; Liu, J. Recent advances in the development of neuroprotective agents and therapeutic targets in the treatment of cerebral ischemia. Eur. J. Med. Chem., 2019, 162, 132-146.
[http://dx.doi.org/10.1016/j.ejmech.2018.11.014] [PMID: 30445263]
[5]
Moskowitz, M.A.; Lo, E.H.; Iadecola, C. The science of stroke: mechanisms in search of treatments. Neuron, 2010, 67(2), 181-198.
[http://dx.doi.org/10.1016/j.neuron.2010.07.002] [PMID: 20670828]
[6]
Madl, C.; Holzer, M. Brain function after resuscitation from cardiac arrest. Curr. Opin. Crit. Care, 2004, 10(3), 213-217.
[http://dx.doi.org/10.1097/01.ccx.0000127542.32890.fa] [PMID: 15166839]
[7]
Cervantes, M.; Gonzalez-Burgos, I.; Letechipia-Vallejo, G.; Olvera-Cortés, M.E.; Moralí, G. Neuroprotection in animal models of global cerebral ischemia; Advances in the Preclinical Study of Ischemic Stroke, InTech: Rijeka, Croatia, 2012, pp. 305-346.
[http://dx.doi.org/10.5772/32322]
[8]
Kirino, T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res., 1982, 239(1), 57-69.
[http://dx.doi.org/10.1016/0006-8993(82)90833-2] [PMID: 7093691]
[9]
Pulsinelli, W.A.; Brierley, J.B.; Plum, F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol., 1982 a, 11(5), 491-498.
[http://dx.doi.org/10.1002/ana.410110509] [PMID: 7103425]
[10]
Pulsinelli, W.A.; Levy, D.E.; Duffy, T.E. Regional cerebral blood flow and glucose metabolism following transient forebrain ischemia. Ann. Neurol., 1982 b, 11(5), 499-502.
[http://dx.doi.org/10.1002/ana.410110510] [PMID: 7103426]
[11]
Mies, G.; Paschen, W.; Hossmann, K.A. Cerebral blood flow, glucose utilization, regional glucose, and ATP content during the maturation period of delayed ischemic injury in gerbil brain. J. Cereb. Blood Flow Metab., 1990, 10(5), 638-645.
[http://dx.doi.org/10.1038/jcbfm.1990.116] [PMID: 2384537]
[12]
Harukuni, I.; Bhardwaj, A. Mechanisms of brain injury after global cerebral ischemia. Neurol. Clin., 2006, 24(1), 1-21.
[http://dx.doi.org/10.1016/j.ncl.2005.10.004] [PMID: 16443127]
[13]
Mukherjee, A.; Sarkar, S.; Jana, S.; Swarnakar, S.; Das, N. Neuro-protective role of nanocapsulated curcumin against cerebral ischemia-reperfusion induced oxidative injury. Brain Res., 2019, 1704, 164-173.
[http://dx.doi.org/10.1016/j.brainres.2018.10.016] [PMID: 30326199]
[14]
Pulsinelli, W.A. Selective neuronal vulnerability: morphological and molecular characteristics. In: Prog. Brain Res; , 1985; 63, pp. 29-37.
[http://dx.doi.org/10.1016/S0079-6123(08)61973-1] [PMID: 2872695]
[15]
Petito, C.K.; Pulsinelli, W.A. Delayed neuronal recovery and neuronal death in rat hippocampus following severe cerebral ischemia: possible relationship to abnormalities in neuronal processes. J. Cereb. Blood Flow Metab., 1984, 4(2), 194-205.
[http://dx.doi.org/10.1038/jcbfm.1984.28] [PMID: 6725432]
[16]
Kaplan, B.; Brint, S.; Tanabe, J.; Jacewicz, M.; Wang, X.J.; Pulsinelli, W. Temporal thresholds for neocortical infarction in rats subjected to reversible focal cerebral ischemia. Stroke, 1991, 22(8), 1032-1039.
[http://dx.doi.org/10.1161/01.STR.22.8.1032] [PMID: 1866750]
[17]
Bhardwaj, A.; Alkayed, N.J.; Kirsch, J.R.; Hurn, P.D. Mechanisms of ischemic brain damage. Curr. Cardiol. Rep., 2003, 5(2), 160-167.
[http://dx.doi.org/10.1007/s11886-003-0085-1] [PMID: 12583862]
[18]
Thompson, C.B. Apoptosis in the pathogenesis and treatment of disease. Science, 1995, 267(5203), 1456-1462.
[http://dx.doi.org/10.1126/science.7878464] [PMID: 7878464]
[19]
Dirnagl, U.; Iadecola, C.; Moskowitz, M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci., 1999, 22(9), 391-397.
[http://dx.doi.org/10.1016/S0166-2236(99)01401-0] [PMID: 10441299]
[20]
Ankarcrona, M.; Dypbukt, J.M.; Bonfoco, E. Necrosis and apoptosis elicited by glutamate in cerebellar granule cells: a temporal sequence depending on mitochondrial function. Neuron, 1995, 15, 961-973.
[http://dx.doi.org/10.1016/0896-6273(95)90186-8] [PMID: 7576644]
[21]
Olney, J.W. Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science, 1969, 164(3880), 719-721.
[http://dx.doi.org/10.1126/science.164.3880.719] [PMID: 5778021]
[22]
Choi, D.W. Glutamate neurotoxicity and diseases of the nervous system. Neuron, 1988, 1(8), 623-634.
[http://dx.doi.org/10.1016/0896-6273(88)90162-6] [PMID: 2908446]
[23]
Benveniste, H.; Drejer, J.; Schousboe, A.; Diemer, N.H. Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J. Neurochem., 1984, 43(5), 1369-1374.
[http://dx.doi.org/10.1111/j.1471-4159.1984.tb05396.x] [PMID: 6149259]
[24]
Choi, D.W. Excitotoxic cell death. J. Neurobiol., 1992, 23(9), 1261-1276.
[http://dx.doi.org/10.1002/neu.480230915] [PMID: 1361523]
[25]
Dawson, T.M.; Dawson, V.L.; Snyder, S.H. A novel neuronal messenger molecule in brain: the free radical, nitric oxide. Ann. Neurol., 1992, 32(3), 297-311.
[http://dx.doi.org/10.1002/ana.410320302] [PMID: 1384420]
[26]
Samdani, A.F.; Dawson, T.M.; Dawson, V.L. Nitric oxide synthase in models of focal ischemia. Stroke, 1997, 28(6), 1283-1288.
[http://dx.doi.org/10.1161/01.STR.28.6.1283] [PMID: 9183363]
[27]
Dawson, T.M.; Dawson, V.L. Nitric oxide: actions and pathological roles. Neuroscientist, 1995, 1, 7-18.
[http://dx.doi.org/10.1177/107385849500100103]
[28]
Hurn, P.D.; Vannucci, S.J.; Hagberg, H. Adult or perinatal brain injury: does sex matter? Stroke, 2005, 36(2), 193-195.
[http://dx.doi.org/10.1161/01.STR.0000153064.41332.f6] [PMID: 15625289]
[29]
Thorvaldsen, P.; Kuulasmaa, K.; Rajakangas, A.M.; Rastenyte, D.; Sarti, C.; Wilhelmsen, L. Stroke trends in the WHO MONICA project. Stroke, 1997, 28(3), 500-506.
[http://dx.doi.org/10.1161/01.STR.28.3.500] [PMID: 9056602]
[30]
McCullough, L.D.; Hurn, P.D. Estrogen and ischemic neuroprotection: an integrated view. Trends Endocrinol. Metab., 2003, 14(5), 228-235.
[http://dx.doi.org/10.1016/S1043-2760(03)00076-6] [PMID: 12826329]
[31]
Alkayed, N.J.; Harukuni, I.; Kimes, A.S.; London, E.D.; Traystman, R.J.; Hurn, P.D. Gender-linked brain injury in experimental stroke. Stroke, 1998, 29(1), 159-165.
[http://dx.doi.org/10.1161/01.STR.29.1.159] [PMID: 9445346]
[32]
Hurn, P.D.; Macrae, I.M. Estrogen as a neuroprotectant in stroke. J. Cereb. Blood Flow Metab., 2000, 20(4), 631-652.
[http://dx.doi.org/10.1097/00004647-200004000-00001] [PMID: 10779008]
[33]
Hurn, P.D.; Brass, L.M. Estrogen and stroke: a balanced analysis. Stroke, 2003, 34(2), 338-341.
[http://dx.doi.org/10.1161/01.STR.0000054051.88378.25] [PMID: 12574529]
[34]
Yang, E.; Zha, J.; Jockel, J.; Boise, L.H.; Thompson, C.B.; Korsmeyer, S.J. Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell, 1995, 80(2), 285-291.
[http://dx.doi.org/10.1016/0092-8674(95)90411-5] [PMID: 7834748]
[35]
Hagberg, H.; Wilson, M.A.; Matsushita, H.; Zhu, C.; Lange, M.; Gustavsson, M.; Poitras, M.F.; Dawson, T.M.; Dawson, V.L.; Northington, F.; Johnston, M.V. PARP-1 gene disruption in mice preferentially protects males from perinatal brain injury. J. Neurochem., 2004, 90(5), 1068-1075.
[http://dx.doi.org/10.1111/j.1471-4159.2004.02547.x] [PMID: 15312162]
[36]
Hossmann, K.A. Periinfarct depolarizations. Cerebrovasc. Brain Metab. Rev., 1996, 8(3), 195-208.
[PMID: 8870974]
[37]
Giffard, R.G.; Swanson, R.A. Ischemia-induced programmed cell death in astrocytes. Glia, 2005, 50(4), 299-306.
[http://dx.doi.org/10.1002/glia.20167] [PMID: 15846803]
[38]
Budd, S.L. Mechanisms of neuronal damage in brain hypoxia/ischemia: focus on the role of mitochondrial calcium accumulation. Pharmacol. Ther., 1998, 80(2), 203-229.
[http://dx.doi.org/10.1016/S0163-7258(98)00029-1] [PMID: 9839772]
[39]
Slivka, A.; Brannan, T.S.; Weinberger, J.; Knott, P.J.; Cohen, G. Increase in extracellular dopamine in the striatum during cerebral ischemia: a study utilizing cerebral microdialysis. J. Neurochem., 1988, 50(6), 1714-1718.
[http://dx.doi.org/10.1111/j.1471-4159.1988.tb02468.x] [PMID: 3373210]
[40]
Lu, X.C.; Williams, A.J.; Wagstaff, J.D.; Tortella, F.C.; Hartings, J.A. Effects of delayed intrathecal infusion of an NMDA receptor antagonist on ischemic injury and peri-infarct depolarizations. Brain Res., 2005, 1056(2), 200-208.
[http://dx.doi.org/10.1016/j.brainres.2005.07.041] [PMID: 16112094]
[41]
Ohta, K.; Graf, R.; Rosner, G.; Heiss, W.D. Calcium ion transients in peri-infarct depolarizations may deteriorate ion homeostasis and expand infarction in focal cerebral ischemia in cats. Stroke, 2001, 32(2), 535-543.
[http://dx.doi.org/10.1161/01.STR.32.2.535] [PMID: 11157194]
[42]
Fabricius, M.; Fuhr, S.; Bhatia, R.; Boutelle, M.; Hashemi, P.; Strong, A.J.; Lauritzen, M. Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain, 2006, 129(Pt 3), 778-790.
[http://dx.doi.org/10.1093/brain/awh716] [PMID: 16364954]
[43]
Beckman, J.S.; Beckman, T.W.; Chen, J.; Marshall, P.A.; Freeman, B.A. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA, 1990, 87(4), 1620-1624.
[http://dx.doi.org/10.1073/pnas.87.4.1620] [PMID: 2154753]
[44]
Aarts, M.; Liu, Y.; Liu, L.; Besshoh, S.; Arundine, M.; Gurd, J.W.; Wang, Y.T.; Salter, M.W.; Tymianski, M. Treatment of ischemic brain damage by perturbing NMDA receptor- PSD-95 protein interactions. Science, 2002, 298(5594), 846-850.
[http://dx.doi.org/10.1126/science.1072873] [PMID: 12399596]
[45]
Meller, R.; Minami, M.; Cameron, J.A.; Impey, S.; Chen, D.; Lan, J.Q.; Henshall, D.C.; Simon, R.P. CREB-mediated Bcl-2 protein expression after ischemic preconditioning. J. Cereb. Blood Flow Metab., 2005, 25(2), 234-246.
[http://dx.doi.org/10.1038/sj.jcbfm.9600024] [PMID: 15647742]
[46]
Yano, S.; Morioka, M.; Kuratsu, J.; Fukunaga, K. Functional proteins involved in regulation of intracellular Ca(2+) for drug development: role of calcium/calmodulin-dependent protein kinases in ischemic neuronal death. J. Pharmacol. Sci., 2005, 97(3), 351-354.
[http://dx.doi.org/10.1254/jphs.FMJ04007X5] [PMID: 15764842]
[47]
Sinha, K.; Degaonkar, M.N.; Jagannathan, N.R.; Gupta, Y.K. Effect of melatonin on ischemia reperfusion injury induced by middle cerebral artery occlusion in rats. Eur. J. Pharmacol., 2001, 428(2), 185-192.
[http://dx.doi.org/10.1016/S0014-2999(01)01253-5] [PMID: 11675035]
[48]
Mohan, N.; Sadeghi, K.; Reiter, R.J.; Meltz, M.L. The neurohormone melatonin inhibits cytokine, mitogen and ionizing radiation induced NF-kappa B. Biochem. Mol. Biol. Int., 1995, 37(6), 1063-1070.
[PMID: 8747536]
[49]
Cao, J.; Viholainen, J.I.; Dart, C.; Warwick, H.K.; Leyland, M.L.; Courtney, M.J. The PSD95-nNOS interface: a target for inhibition of excitotoxic p38 stress-activated protein kinase activation and cell death. J. Cell Biol., 2005, 168(1), 117-126.
[http://dx.doi.org/10.1083/jcb.200407024] [PMID: 15631993]
[50]
Nozaki, K.; Nishimura, M.; Hashimoto, N. Mitogen-activated protein kinases and cerebral ischemia. Mol. Neurobiol., 2001, 23(1), 1-19.
[http://dx.doi.org/10.1385/MN:23:1:01] [PMID: 11642541]
[51]
Machado, L.S.; Kozak, A.; Ergul, A.; Hess, D.C.; Borlongan, C.V.; Fagan, S.C. Delayed minocycline inhibits ischemia-activated matrix metalloproteinases 2 and 9 after experimental stroke. BMC Neurosci., 2006, 7, 56.
[http://dx.doi.org/10.1186/1471-2202-7-56] [PMID: 16846501]
[52]
Fukuda, S.; Fini, C.A.; Mabuchi, T.; Koziol, J.A.; Eggleston, L.L., Jr; del Zoppo, G.J. Focal cerebral ischemia induces active proteases that degrade microvascular matrix. Stroke, 2004, 35(4), 998-1004.
[http://dx.doi.org/10.1161/01.STR.0000119383.76447.05] [PMID: 15001799]
[53]
Huang, J.; Choudhri, T.F.; Winfree, C.J.; McTaggart, R.A.; Kiss, S.; Mocco, J.; Kim, L.J.; Protopsaltis, T.S.; Zhang, Y.; Pinsky, D.J.; Connolly, E.S. Jr Postischemic cerebrovascular E-selectin expression mediates tissue injury in murine stroke. Stroke, 2000, 31(12), 3047-3053.
[http://dx.doi.org/10.1161/01.STR.31.12.3047] [PMID: 11108771]
[54]
Mocco, J.; Choudhri, T.; Huang, J.; Harfeldt, E.; Efros, L.; Klingbeil, C.; Vexler, V.; Hall, W.; Zhang, Y.; Mack, W.; Popilskis, S.; Pinsky, D.J.; Connolly, E.S., Jr HuEP5C7 as a humanized monoclonal anti-E/P-selectin neurovascular protective strategy in a blinded placebo-controlled trial of nonhuman primate stroke. Circ. Res., 2002, 91(10), 907-914.
[http://dx.doi.org/10.1161/01.RES.0000042063.15901.20] [PMID: 12433835]
[55]
Thoren, A.E.; Helps, S.C.; Nilsson, M.; Sims, N.R. Astrocytic function assessed from 1-14C-acetate metabolism after temporary focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab., 2005, 25(4), 440-450.
[http://dx.doi.org/10.1038/sj.jcbfm.9600035] [PMID: 15674239]
[56]
Guégan, C.; Ceballos-Picot, I.; Nicole, A.; Kato, H.; Onténiente, B.; Sola, B. Recruitment of several neuroprotective pathways after permanent focal ischemia in mice. Exp. Neurol., 1998, 154(2), 371-380.
[http://dx.doi.org/10.1006/exnr.1998.6913] [PMID: 9878175]
[57]
Pulsinelli, W.A.; Brierley, J.B.; Plum, F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol., 1982, 11(5), 491-498.
[http://dx.doi.org/10.1002/ana.410110509] [PMID: 7103425]
[58]
Kågström, E.; Smith, M-L.; Siesjö, B.K. Local cerebral blood flow in the recovery period following complete cerebral ischemia in the rat. J. Cereb. Blood Flow Metab., 1983, 3(2), 170-182.
[http://dx.doi.org/10.1038/jcbfm.1983.24] [PMID: 6841464]
[59]
Pulsinelli, W.A.; Duffy, T.E. Regional energy balance in rat brain after transient forebrain ischemia. J. Neurochem., 1983, 40(5), 1500-1503.
[http://dx.doi.org/10.1111/j.1471-4159.1983.tb13599.x] [PMID: 6834075]
[60]
Nishijima, M.K.; Koehler, R.C.; Hurn, P.D.; Eleff, S.M.; Norris, S.; Jacobus, W.E.; Traystman, R.J. Postischemic recovery rate of cerebral ATP, phosphocreatine, pH, and evoked potentials. Am. J. Physiol., 1989, 257(6 Pt 2), H1860-H1870.
[PMID: 2513729]
[61]
Fonnum, F. Glutamate: a neurotransmitter in mammalian brain. J. Neurochem., 1984, 42(1), 1-11.
[http://dx.doi.org/10.1111/j.1471-4159.1984.tb09689.x] [PMID: 6139418]
[62]
Rossberg, M.I.; Bhardwaj, A.; Hurn, P.D. Principles of cerebroprotection.Critical care medicine: perioperative management; Murray, M.J.; Coursin, D.B; Pearl, R.G., Ed.; Lipincott Williams & Williams: Philadelphia, 2002, pp. 225-235.
[63]
Weigl, M.; Tenze, G.; Steinlechner, B.; Skhirtladze, K.; Reining, G.; Bernardo, M.; Pedicelli, E.; Dworschak, M. A systematic review of currently available pharmacological neuroprotective agents as a sole intervention before anticipated or induced cardiac arrest. Resuscitation, 2005, 65(1), 21-39.
[http://dx.doi.org/10.1016/j.resuscitation.2004.11.004] [PMID: 15797272]
[64]
Li, M.M.; Payne, R.S.; Reid, K.H.; Tseng, M.T.; Rigor, B.M.; Schurr, A. Correlates of delayed neuronal damage and neuroprotection in a rat model of cardiac-arrest-induced cerebral ischemia. Brain Res., 1999, 826(1), 44-52.
[http://dx.doi.org/10.1016/S0006-8993(99)01221-4] [PMID: 10216195]
[65]
Dietrich, W.D.; Lin, B.; Globus, M.Y.; Green, E.J.; Ginsberg, M.D.; Busto, R. Effect of delayed MK-801 (dizocilpine) treatment with or without immediate postischemic hypothermia on chronic neuronal survival after global forebrain ischemia in rats. J. Cereb. Blood Flow Metab., 1995, 15(6), 960-968.
[http://dx.doi.org/10.1038/jcbfm.1995.122] [PMID: 7593357]
[66]
Aronowski, J.; Waxham, M.N.; Grotta, J.C. Neuronal protection and preservation of calcium/calmodulin-dependent protein kinase II and protein kinase C activity by dextrorphan treatment in global ischemia. J. Cereb. Blood Flow Metab., 1993, 13(4), 550-557.
[http://dx.doi.org/10.1038/jcbfm.1993.72] [PMID: 7686173]
[67]
Artru, A.A.; Michenfelder, J.D. Anoxic cerebral potassium accumulation reduced by phenytoin: mechanism of cerebral protection? Anesth. Analg., 1981, 60(1), 41-45.
[http://dx.doi.org/10.1213/00000539-198101000-00009] [PMID: 7192948]
[68]
Imaizumi, S.; Kurosawa, K.; Kinouchi, H.; Yoshimoto, T. Effect of phenytoin on cortical Na(+)-K(+)-ATPase activity in global ischemic rat brain. J. Neurotrauma, 1995, 12(2), 231-234.
[http://dx.doi.org/10.1089/neu.1995.12.231] [PMID: 7629869]
[69]
Shuaib, A.; Murabit, M.A.; Kanthan, R.; Howlett, W.; Wishart, T. The neuroprotective effects of gamma-vinyl GABA in transient global ischemia: a morphological study with early and delayed evaluations. Neurosci. Lett., 1996, 204(1-2), 1-4.
[http://dx.doi.org/10.1016/0304-3940(96)12336-3] [PMID: 8929963]
[70]
Thaminy, S.; Reymann, J.M.; Heresbach, N.; Allain, H.; Lechat, P.; Bentué-Ferrer, D. Is chlormethiazole neuroprotective in experimental global cerebral ischemia? A microdialysis and behavioral study. Pharmacol. Biochem. Behav., 1997, 56(4), 737-745.
[http://dx.doi.org/10.1016/S0091-3057(96)00517-5] [PMID: 9130301]
[71]
Vergoni, A.V.; Ottani, A.; Botticelli, A.R.; Zaffe, D.; Guano, L.; Loche, A.; Genedani, S.; Gessa, G.L.; Bertolini, A. Neuroprotective effect of gamma-hydroxybutyrate in transient global cerebral ischemia in the rat. Eur. J. Pharmacol., 2000, 397(1), 75-84.
[http://dx.doi.org/10.1016/S0014-2999(00)00246-6] [PMID: 10844101]
[72]
Lazarewicz, J.W.; Pluta, R.; Puka, M.; Salinska, E. Diverse mechanisms of neuronal protection by nimodipine in experimental rabbit brain ischemia. Stroke, 1990, 21(12)(Suppl.), IV108-IV110.
[PMID: 1979699]
[73]
Miles, A.N.; Majda, B.T.; Meloni, B.P.; Knuckey, N.W. Postischemic intravenous administration of magnesium sulfate inhibits hippocampal CA1 neuronal death after transient global ischemia in rats. Neurosurgery, 2001, 49(6), 1443-1450.
[http://dx.doi.org/10.1097/00006123-200112000-00025] [PMID: 11846945]
[74]
Zhu, H.; Meloni, B.P.; Bojarski, C.; Knuckey, M.W.; Knuckey, N.W. Post-ischemic modest hypothermia (35 degrees C) combined with intravenous magnesium is more effective at reducing CA1 neuronal death than either treatment used alone following global cerebral ischemia in rats. Exp. Neurol., 2005, 193(2), 361-368.
[http://dx.doi.org/10.1016/j.expneurol.2005.01.022] [PMID: 15869938]
[75]
Candelario-Jalil, E.; Alvarez, D.; González-Falcón, A.; García-Cabrera, M.; Martínez-Sánchez, G.; Merino, N.; Giuliani, A.; León, O.S. Neuroprotective efficacy of nimesulide against hippocampal neuronal damage following transient forebrain ischemia. Eur. J. Pharmacol., 2002, 453(2-3), 189-195.
[http://dx.doi.org/10.1016/S0014-2999(02)02422-6] [PMID: 12398903]
[76]
Loihl, A.K.; Asensio, V.; Campbell, I.L.; Murphy, S. Expression of nitric oxide synthase (NOS)-2 following permanent focal ischemia and the role of nitric oxide in infarct generation in male, female and NOS-2 gene-deficient mice. Brain Res., 1999, 830(1), 155-164.
[http://dx.doi.org/10.1016/S0006-8993(99)01388-8] [PMID: 10350569]
[77]
McCullough, L.D.; Zeng, Z.; Blizzard, K.K.; Debchoudhury, I.; Hurn, P.D. Ischemic nitric oxide and poly (ADP-ribose) polymerase-1 in cerebral ischemia: male toxicity, female protection. J. Cereb. Blood Flow Metab., 2005, 25(4), 502-512.
[http://dx.doi.org/10.1038/sj.jcbfm.9600059] [PMID: 15689952]
[78]
Noppens, R.R.; Kofler, J.; Hurn, P.D.; Traystman, R.J. Dose-dependent neuroprotection by 17beta-estradiol after cardiac arrest and cardiopulmonary resuscitation. Crit. Care Med., 2005, 33(7), 1595-1602.
[http://dx.doi.org/10.1097/01.CCM.0000169884.81769.F7] [PMID: 16003068]
[79]
Garcia-Segura, L.M.; Azcoitia, I.; DonCarlos, L.L. Neuroprotection by estradiol. Prog. Neurobiol., 2001, 63(1), 29-60.
[http://dx.doi.org/10.1016/S0301-0082(00)00025-3] [PMID: 11040417]
[80]
Fried, R.L.; Nowak, T.S., Jr Opioid peptide levels in gerbil brain after transient ischemia: lasting depletion of hippocampal dynorphin. Stroke, 1987, 18(4), 765-770.
[http://dx.doi.org/10.1161/01.STR.18.4.765] [PMID: 2885947]
[81]
Zabramski, J.M.; Spetzler, R.F.; Selman, W.R.; Roessmann, U.R.; Hershey, L.A.; Crumrine, R.C.; Macko, R. Naloxone therapy during focal cerebral ischemia evaluation in a primate model. Stroke, 1984, 15(4), 621-627.
[http://dx.doi.org/10.1161/01.STR.15.4.621] [PMID: 6464054]
[82]
Mackay, K.B.; Kusumoto, K.; Graham, D.I.; McCulloch, J. Effect of the kappa-1 opioid agonist CI-977 on ischemic brain damage and cerebral blood flow after middle cerebral artery occlusion in the rat. Brain Res., 1993, 629(1), 10-18.
[http://dx.doi.org/10.1016/0006-8993(93)90474-2] [PMID: 8287264]
[83]
Baskin, D.S.; Widmayer, M.A.; Browning, J.L.; Heizer, M.L.; Schmidt, W.K. Evaluation of delayed treatment of focal cerebral ischemia with three selective kappa-opioid agonists in cats. Stroke, 1994, 25(10), 2047-2053.
[http://dx.doi.org/10.1161/01.STR.25.10.2047] [PMID: 7916503]
[84]
Tang, A.H. Protection from cerebral ischemia by U-50,488E, a specific kappa opioid analgesic agent. Life Sci., 1985, 37(16), 1475-1482.
[http://dx.doi.org/10.1016/0024-3205(85)90178-X] [PMID: 2995747]
[85]
Vu, T.H.; Weissman, A.D.; London, E.D. Pharmacological characteristics and distributions of sigma- and phencyclidine receptors in the animal kingdom. J. Neurochem., 1990, 54(2), 598-604.
[http://dx.doi.org/10.1111/j.1471-4159.1990.tb01913.x] [PMID: 2153756]
[86]
Sugawara, T.; Fujimura, M.; Noshita, N.; Kim, G.W.; Saito, A.; Hayashi, T.; Narasimhan, P.; Maier, C.M.; Chan, P.H. Neuronal death/survival signaling pathways in cerebral ischemia. NeuroRx, 2004, 1(1), 17-25.
[http://dx.doi.org/10.1602/neurorx.1.1.17] [PMID: 15717004]
[87]
Su, T.P.; London, E.D.; Jaffe, J.H. Steroid binding at sigma receptors suggests a link between endocrine, nervous, and immune systems. Science, 1988, 240(4849), 219-221.
[http://dx.doi.org/10.1126/science.2832949] [PMID: 2832949]
[88]
Goyagi, T.; Toung, T.J.; Kirsch, J.R.; Traystman, R.J.; Koehler, R.C.; Hurn, P.D.; Bhardwaj, A. Neuroprotective kappa-opioid receptor agonist BRL 52537 attenuates ischemia-evoked nitric oxide production in vivo in rats. Stroke, 2003, 34(6), 1533-1538.
[http://dx.doi.org/10.1161/01.STR.0000072512.30658.E7] [PMID: 12738895]
[89]
Lipton, P. Ischemic cell death in brain neurons. Physiol. Rev., 1999, 79(4), 1431-1568.
[http://dx.doi.org/10.1152/physrev.1999.79.4.1431] [PMID: 10508238]
[90]
Schneider, A.; Böttiger, B.W.; Popp, E. Cerebral resuscitation after cardiocirculatory arrest. Anesth. Analg., 2009, 108(3), 971-979.
[http://dx.doi.org/10.1213/ane.0b013e318193ca99] [PMID: 19224811]
[91]
Lakhan, S.E.; Kirchgessner, A.; Hofer, M. Inflammatory mechanisms in ischemic stroke: therapeutic approaches. J. Transl. Med., 2009, 7, 97.
[http://dx.doi.org/10.1186/1479-5876-7-97] [PMID: 19919699]
[92]
Hatziagapiou, K.; Kakouri, E.; Lambrou, G.I.; Bethanis, K.; Tarantilis, P.A. Antioxidant properties of Crocus sativus L. and its constituents and relevance to neurodegenerative diseases; focus on Alzheimer’s and Parkinson’s disease. Curr. Neuropharmacol., 2019, 17(4), 377-402.
[http://dx.doi.org/10.2174/1570159X16666180321095705] [PMID: 29564976]
[93]
Muley, M.M.; Thakare, V.N.; Patil, R.R.; Bafna, P.A.; Naik, S.R. Amelioration of cognitive, motor and endogenous defense functions with silymarin, piracetam and protocatechuic acid in the cerebral global ischemic rat model. Life Sci., 2013, 93(1), 51-57.
[http://dx.doi.org/10.1016/j.lfs.2013.05.020] [PMID: 23743171]
[94]
Llorente, I.L.; Pérez-Rodríguez, D.; Burgin, T.C.; Gonzalo-Orden, J.M.; Martínez-Villayandre, B.; Fernández-López, A. Age and meloxicam modify the response of the glutamate vesicular transporters (VGLUTs) after transient global cerebral ischemia in the rat brain. Brain Res. Bull., 2013, 94, 90-97.
[http://dx.doi.org/10.1016/j.brainresbull.2013.02.006] [PMID: 23458738]
[95]
Kim, S.J.; Lee, S.R. Protective effect of melatonin against transient global cerebral ischemia-induced neuronal cell damage via inhibition of matrix metalloproteinase-9. Life Sci., 2014, 94(1), 8-16.
[http://dx.doi.org/10.1016/j.lfs.2013.11.013] [PMID: 24269215]
[96]
Jincai, W.; Tingfang, D.; Yongheng, Z.; Zhongmin, L.; Kaihua, Z.; Xiaohong, L. Effects of vinpocetine and ozagrel on behavioral recovery of rats after global brain ischemia. J. Clin. Neurosci., 2014, 21(4), 661-663.
[http://dx.doi.org/10.1016/j.jocn.2013.07.039] [PMID: 24291485]
[97]
Kakkar, V.; Muppu, S.K.; Chopra, K.; Kaur, I.P. Curcumin loaded solid lipid nanoparticles: an efficient formulation approach for cerebral ischemic reperfusion injury in rats. Eur. J. Pharm. Biopharm., 2013, 85(3 Pt A), 339-345.
[http://dx.doi.org/10.1016/j.ejpb.2013.02.005] [PMID: 23454202]
[98]
Canal Castro, C.; Pagnussat, A.S.; Orlandi, L.; Worm, P.; Moura, N.; Etgen, A.M.; Alexandre Netto, C. Coumestrol has neuroprotective effects before and after global cerebral ischemia in female rats. Brain Res., 2012, 1474, 82-90.
[http://dx.doi.org/10.1016/j.brainres.2012.07.025] [PMID: 22824334]
[99]
Brückner, M.; Lasarzik, I.; Jahn-Eimermacher, A.; Peetz, D.; Werner, C.; Engelhard, K.; Thal, S.C. High dose infusion of activated protein C (rhAPC) fails to improve neuronal damage and cognitive deficit after global cerebral ischemia in rats. Neurosci. Lett., 2013, 551, 28-33.
[http://dx.doi.org/10.1016/j.neulet.2013.06.055] [PMID: 23831347]
[100]
Bendi, V.S.M.; Annapurna, A.; Avupati, V.R. Studies on cerebroprotective potential of 2, 4, 6-trisubstituted-1, 3, 5-pyrimidines in global ischemia/reperfusion induced cerebral infarction in rats. J. Pharm. Res., 2013, 6(9), 939-944.
[http://dx.doi.org/10.1016/j.jopr.2013.08.030]
[101]
Viswanatha, G.L.; Shylaja, H.; Mohan, C.G. Alleviation of transient global ischemia/reperfusion-induced brain injury in rats with 1,2,3,4,6-penta-O-galloyl-β-d-glucopyranose isolated from Mangifera indica. Eur. J. Pharmacol., 2013, 720(1-3), 286-293.
[http://dx.doi.org/10.1016/j.ejphar.2013.10.016] [PMID: 24157980]
[102]
Xu, L.; Wang, J.; Pan, J.; Sun, L.; Xia, Q.; Luo, B. Effect of enoxaparin and aspirin on hemodynamic disturbances after global cerebral ischemia in rats. Resuscitation, 2010, 81(12), 1709-1713.
[http://dx.doi.org/10.1016/j.resuscitation.2010.07.018] [PMID: 20850215]
[103]
Yin, J.; Tu, C.; Zhao, J.; Ou, D.; Chen, G.; Liu, Y.; Xiao, X. Exogenous hydrogen sulfide protects against global cerebral ischemia/reperfusion injury via its anti-oxidative, anti-inflammatory and anti-apoptotic effects in rats. Brain Res., 2013, 1491, 188-196.
[http://dx.doi.org/10.1016/j.brainres.2012.10.046] [PMID: 23123706]
[104]
Gaur, V.; Aggarwal, A.; Kumar, A. Protective effect of naringin against ischemic reperfusion cerebral injury: possible neurobehavioral, biochemical and cellular alterations in rat brain. Eur. J. Pharmacol., 2009, 616(1-3), 147-154.
[http://dx.doi.org/10.1016/j.ejphar.2009.06.056] [PMID: 19577560]
[105]
Cho, J.Y.; Kim, I.S.; Jang, Y.H.; Kim, A.R.; Lee, S.R. Protective effect of quercetin, a natural flavonoid against neuronal damage after transient global cerebral ischemia. Neurosci. Lett., 2006, 404(3), 330-335.
[http://dx.doi.org/10.1016/j.neulet.2006.06.010] [PMID: 16806698]
[106]
Xuan, A.; Long, D.; Li, J.; Ji, W.; Hong, L.; Zhang, M.; Zhang, W. Neuroprotective effects of valproic acid following transient global ischemia in rats. Life Sci., 2012, 90(11-12), 463-468.
[http://dx.doi.org/10.1016/j.lfs.2012.01.001] [PMID: 22285595]
[107]
Singh, D.P.; Chopra, K. Verapamil augments the neuroprotectant action of berberine in rat model of transient global cerebral ischemia. Eur. J. Pharmacol., 2013, 720(1-3), 98-106.
[http://dx.doi.org/10.1016/j.ejphar.2013.10.043] [PMID: 24177287]
[108]
Simão, F.; Matté, A.; Pagnussat, A.S.; Netto, C.A.; Salbego, C.G. Resveratrol preconditioning modulates inflammatory response in the rat hippocampus following global cerebral ischemia. Neurochem. Int., 2012, 61(5), 659-665.
[http://dx.doi.org/10.1016/j.neuint.2012.06.009] [PMID: 22709670]
[109]
Chen, L.; Wei, X.; Hou, Y.; Liu, X.; Li, S.; Sun, B.; Liu, X.; Liu, H. Tetramethylpyrazine analogue CXC195 protects against cerebral ischemia/reperfusion-induced apoptosis through PI3K/Akt/GSK3β pathway in rats. Neurochem. Int., 2014, 66, 27-32.
[http://dx.doi.org/10.1016/j.neuint.2014.01.006] [PMID: 24462584]
[110]
Candelario-Jalil, E. Nimesulide as a promising neuroprotectant in brain ischemia: new experimental evidences. Pharmacol. Res., 2008, 57(4), 266-273.
[http://dx.doi.org/10.1016/j.phrs.2008.03.003] [PMID: 18439837]
[111]
Tu, Q.; Wang, R.; Ding, B.; Zhong, W.; Cao, H. Protective and antioxidant effect of Danshen polysaccharides on cerebral ischemia/reperfusion injury in rats. Int. J. Biol. Macromol., 2013, 60, 268-271.
[http://dx.doi.org/10.1016/j.ijbiomac.2013.05.035] [PMID: 23748011]
[112]
Schiavon, A.P.; Milani, H.; Romanini, C.V.; Foresti, M.L.; Castro, O.W.; Garcia-Cairasco, N.; de Oliveira, R.M. Imipramine enhances cell proliferation and decreases neurodegeneration in the hippocampus after transient global cerebral ischemia in rats. Neurosci. Lett., 2010, 470(1), 43-48.
[http://dx.doi.org/10.1016/j.neulet.2009.12.052] [PMID: 20036317]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy