Early Brain Injury or Cerebral Vasospasm pp 43-48 | Cite as
Apoptotic Mechanisms for Neuronal Cells in Early Brain Injury After Subarachnoid Hemorrhage
Abstract
Objects: The major causes of death and disability in subarachnoid hemorrhage (SAH) may be early brain injury (EBI) and cerebral vasospasm. Although cerebral vasospasm has been studied and treated by a lot of drugs, the outcome is not improved even if vasospasm is reversed. Based on these data, EBI is considered a primary target for future research, and apoptosis may be involved in EBI after experimental SAH.
Methods: We reviewed the published literature about the relationship between SAH induced EBI and apoptosis in PubMed.
Result: Most available information can be obtained from the endovascular filament perforation animal model. After onset of SAH, intracranial pressure is increased and then cerebral blood flow is reduced. Many factors are involved in the mechanism of apoptotic cell death in EBI after SAH. In the neuronal cells, both intrinsic and extrinsic pathways of apoptosis can occur. Some antiapoptotic drugs were studied and demonstrated a protective effect against EBI after SAH. However, apoptosis in EBI after SAH has been little studied and further studies will provide us more beneficial findings. Conclusions: The study of apoptosis in EBI after experimental SAH may give us new therapies for SAH.
Keywords
Apoptosis Cerebral blood flow Early brain injury Intracranial pressure Subarachnoid hemorrhageNotes
Acknowledgments
This study was partially supported by grants (NS053407) from the National Institutes of Health to J.H.Z.
Conflict of interest statement We declare that we have no conflict of interest.
References
- 1.Huang J, van Gelder JM. The probability of sudden death from rupture of intracranial aneurysms: a meta-analysis. Neurosurgery 2002;51:1101–5.PubMedCrossRefGoogle Scholar
- 2.O’Hare TH. Subarachnoid hemorrhage: a review. J Emerg Med. 1987;5:135–4PubMedCrossRefGoogle Scholar
- 3.Tseng MY, Czosnyka M, Richards H, Pickard JD, Kirkpatrick PJ. Effects of acute treatment with pravastatin on cerebral vasospasm, autoregulation, and delayed ischemic deficits after aneurysmal subarachnoid hemorrhage: a phase II randomized placebo-controlled trial. Stroke 2005;36:1627–32.PubMedCrossRefGoogle Scholar
- 4.Schievink WI, Riedinger M, Jhutty TK, Simon P. Racial disparities in subarachnoid hemorrhage mortality: Los Angeles County, California, 1985–1998. Neuroepidemiology 2004;23:299–305.PubMedCrossRefGoogle Scholar
- 5.Nau R, Haase S, Bunkowski S, Brück W. Neuronal apoptosis in the dentate gyrus in humans with subarachnoid hemorrhage and cerebral hypoxia. Brain Pathol. 2002;12:329–36.PubMedGoogle Scholar
- 6.Prunell GF, Mathiesen T, Diemer NH, Svendgaard NA. Experimental subarachnoid hemorrhage: subarachnoid blood volume, mortality rate, neuronal death, cerebral blood flow, and perfusion pressure in three different rat models. Neurosurgery 2003;52:165–75.PubMedGoogle Scholar
- 7.Bederson JB, Germano IM, Guarino L. Cortical blood flow and cerebral perfusion pressure in a new noncraniotomy model of subarachnoid hemorrhage in the rat. Stroke 1995;26:1086–91.PubMedCrossRefGoogle Scholar
- 8.Schwartz AY, Masago A, Sehba FA, Bederson JB. Experimental models of subarachnoid hemorrhage in the rat: a refinement of the endovascular filament model. J Neurosci Methods. 2000;96:161–7.PubMedCrossRefGoogle Scholar
- 9.Veelken JA, Laing RJ, Jakubowski J. The Sheffield model of subarachnoid hemorrhage in rats. Stroke 1995;26:1279–83PubMedCrossRefGoogle Scholar
- 10.Török E, Klopotowski M, Trabold R, Thal SC, Plesnila N, Schöller K. Mild hypothermia (33 degrees C) reduces intracranial hypertension and improves functional outcome after subarachnoid hemorrhage in rats. Neurosurgery 2009;65:352–9.PubMedCrossRefGoogle Scholar
- 11.Bederson JB, Levy AL, Ding WH, Kahn R, DiPerna CA, Jenkins AL III et al. Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery 1998;42:352–62.PubMedCrossRefGoogle Scholar
- 12.Park S, Yamaguchi M, Zhou C, Calvert JW, Tang J, Zhang JH. Neurovascular protection reduces early brain injury after subarachnoid hemorrhage. Stroke 2004;35:2412–7.PubMedCrossRefGoogle Scholar
- 13.Matz PG, Copin JC, Chan PH. Cell death after exposure to subarachnoid hemolysate correlates inversely with expression of CuZn-superoxide dismutase. Stroke 2000;31:2450–9.PubMedCrossRefGoogle Scholar
- 14.Endo H, Nito C, Kamada H, Yu F, Chan PH. Akt/GSK3beta survival signaling is involved in acute brain injury after subarachnoid hemorrhage in rats. Stroke 2006;37:2140–6.PubMedCrossRefGoogle Scholar
- 15.Xi G, Keep RF, Hoff JT. Erythrocytes and delayed brain edema formation following intracerebral hemorrhage in rats. J Neurosurg. 1998;89:991–6.PubMedCrossRefGoogle Scholar
- 16.Matz PG, Fujimura M, Chan PH. Subarachnoid hemolysate produces DNA fragmentation in a pattern similar to apoptosis in mouse brain. Brain Res. 2000;858:312–9.PubMedCrossRefGoogle Scholar
- 17.Matz PG, Fujimura M, Lewen A, Morita-Fujimura Y, Chan PH. Increased cytochrome c-mediated DNA fragmentation and cell death in manganese-superoxide dismutase-deficient mice after exposure to subarachnoid hemolysate. Stroke 2001;32:506–15.PubMedCrossRefGoogle Scholar
- 18.Kimura H, Gules I, Meguro T, Zhang JH. Cytotoxicity of cytokines in cerebral microvascular endothelial cell. Brain Res. 2003;990:148–56.PubMedCrossRefGoogle Scholar
- 19.Meguro T, Klett CP, Chen B, Parent AD, Zhang JH. Role of calcium channels in oxyhemoglobin-induced apoptosis in endothelial cells. J Neurosurg. 2000;93:640–6.PubMedCrossRefGoogle Scholar
- 20.Ogihara K, Zubkov AY, Bernanke DH, Lewis AI, Parent AD, Zhang JH. Oxyhemoglobin-induced apoptosis in cultured endothelial cells. J Neurosurg. 1999;91:459–65.PubMedCrossRefGoogle Scholar
- 21.Bazán NG, Rodríguez de Turco EB. Membrane lipids in the pathogenesis of brain edema: phospholipids and arachidonic acid, the earliest membrane components changed at the onset of ischemia. Adv Neurol. 1980;28:197–205.PubMedGoogle Scholar
- 22.Gules I, Satoh M, Nanda A, Zhang JH. Apoptosis, blood-brain barrier, and subarachnoid hemorrhage. Acta Neurochir Suppl. 2003;86:483–7.PubMedCrossRefGoogle Scholar
- 23.Chan PH. Mitochondria and neuronal death/survival signaling pathways in cerebral ischemia. Neurochem Res. 2004;29:1943–9.PubMedCrossRefGoogle Scholar
- 24.Cheng G, Wei L, Zhi-Dan S, Shi-Guang Z, Xiang-Zhen L. Atorvastatin ameliorates cerebral vasospasm and early brain injury after subarachnoid hemorrhage and inhibits caspase-dependent apoptosis pathway. BMC Neurosci. 2009; doi:10,1186/14712202107.Google Scholar
- 25.Yan J, Chen C, Hu Q, Yang X, Lei J, Yang Let al., The role of p53 in brain edema after 24 h of experimental subarachnoid hemorrhage in a rat model. Exp Neurol. 2008;214:37–46.PubMedCrossRefGoogle Scholar
- 26.Zhang F, Yin W, Chen J. Apoptosis in cerebral ischemia: executional and regulatory signaling mechanisms. Neurol Res. 2004;26:835–45.PubMedCrossRefGoogle Scholar
- 27.Hemmings BA. Akt signaling: linking membrane events to life and death decisions. Science 1997;275:628–30.PubMedCrossRefGoogle Scholar
- 28.Pugazhenthi S, Nesterova A, Sable C, Heidenreich KA, Boxer LM, Heasley LE et al. Akt/protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein. J Biol Chem. 2000;275:10761–6.PubMedCrossRefGoogle Scholar
- 29.Hasegawa Y, Hamada J, Morioka M, Yano S, Kawano T, Kai Yet al., Neuroprotective effect of postischemic administration of sodium orthovanadate in rats with transient middle cerebral artery occlusion. J Cereb Blood Flow Metab. 2003;23:1040–51.PubMedCrossRefGoogle Scholar
- 30.Hasegawa Y, Morioka M, Hasegawa S, Matsumoto J, Kawano T, Kai Y et al. Therapeutic time window and dose dependence of neuroprotective effects of sodium orthovanadate following transient middle cerebral artery occlusion in rats. J Pharmacol Exp Ther. 2006;317:875–81.PubMedCrossRefGoogle Scholar
- 31.Shioda N, Ishigami T, Han F, Moriguchi S, Shibuya M, Iwabuchi Y et al. Activation of phosphatidylinositol 3-kinase/protein kinase B pathway by a vanadyl compound mediates its neuroprotective effect in mouse brain ischemia. Neuroscience 2007;148:221–9.PubMedCrossRefGoogle Scholar
- 32.Endo H, Nito C, Kamada H, Yu F, Chan PH. Reduction in oxidative stress by superoxide dismutase overexpression attenuates acute brain injury after subarachnoid hemorrhage via activation of Akt/glycogen synthase kinase-3beta survival signaling. J Cereb Blood Flow Metab. 2007;27:975–82.PubMedGoogle Scholar
- 33.Kusaka G, Ishikawa M, Nanda A, Granger DN, Zhang JH. Signaling pathways for early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2004;24:916–25.PubMedCrossRefGoogle Scholar
- 34.Irving EA, Bamford M. Role of mitogen- and stress-activated kinases in ischemic injury. J Cereb Blood Flow Metab. 2002;22:631–47.PubMedCrossRefGoogle Scholar
- 35.Chakraborti S, Chakraborti T. Oxidant-mediated activation of mitogen-activated protein kinases and nuclear transcription factors in the cardiovascular system: a brief overview. Cell Signal. 1988;10:675–83.CrossRefGoogle Scholar
- 36.Chow J, Ogunshola O, Fan SY, Li Y, Ment LR, Madri JA. Astrocyte-derived VEGF mediates survival and tube stabilization of hypoxic brain microvascular endothelial cells in vitro. Brain Res Dev Brain Res. 2001;130:123–32.PubMedCrossRefGoogle Scholar
- 37.Parker LC, Luheshi GN, Rothwell NJ, Pinteaux E. IL-1 beta signalling in glial cells in wildtype and IL-1RI deficient mice. Br J Pharmacol. 2002;136:312–20.PubMedCrossRefGoogle Scholar
- 38.Sugden PH, Clerk A. “Stress-responsive” mitogen-activated protein kinases (c-Jun N-terminal kinases and p38 mitogen-activated protein kinases) in the myocardium. Circ Res. 1998;83:345–52.PubMedCrossRefGoogle Scholar
- 39.Sozen T, Tsuchiyama R, Hasegawa Y, Suzuki H, Jadhav V, Nishizawa Set al., Role of interleukin-1beta in early brain injury after subarachnoid hemorrhage in mice. Stroke 2009;40:2519–25.PubMedCrossRefGoogle Scholar
- 40.Yatsushige H, Ostrowski RP, Tsubokawa T, Colohan A, Zhang JH. Role of c-Jun N-terminal kinase in early brain injury after subarachnoid hemorrhage. J Neurosci Res. 2007;85:1436–48.PubMedCrossRefGoogle Scholar
- 41.Sawe N, Steinberg G, Zhao H. Dual roles of the MAPK/ERK1/2 cell signaling pathway after stroke. J Neurosci Res. 2008;86:1659–69.PubMedCrossRefGoogle Scholar
- 42.Fassbender K, Hodapp B, Rossol S, Bertsch T, Schmeck J, Schütt Set al., Inflammatory cytokines in subarachnoid haemorrhage: association with abnormal blood flow velocities in basal cerebral arteries. J Neurol Neurosurg Psychiatry. 2001;70:534–7.PubMedCrossRefGoogle Scholar
- 43.Hirashima Y, Nakamura S, Endo S, Kuwayama N, Naruse Y, Takaku A. Elevation of platelet activating factor, inflammatory cytokines, and coagulation factors in the internal jugular vein of patients with subarachnoid hemorrhage. Neurochem Res. 1997;22:1249–55.PubMedCrossRefGoogle Scholar
- 44.Kuan CY, Whitmarsh AJ, Yang DD, Liao G, Schloemer AJ, Dong Cet al., A critical role of neural-specific JNK3 for ischemic apoptosis. Proc Natl Acad Sci USA. 2003;100:15184–9.PubMedCrossRefGoogle Scholar
- 45.Yuan J, Yankner BA. Apoptosis in the nervous system. Nature 2000;407:802–9.PubMedCrossRefGoogle Scholar
- 46.Harada S, Kamiya K, Masago A, Iwata A, Yamada K. Subarachnoid hemorrhage induces c-fos, c-jun and hsp70 mRNA expression in rat brain. Neuroreport 1997;8:3399–404.PubMedCrossRefGoogle Scholar
- 47.Kawamura Y, Yamada K, Masago A, Katano H, Matsumoto T, Mase M. Hypothermia modulates induction of hsp70 and c-jun mRNA in the rat brain after subarachnoid hemorrhage. J Neurotrauma. 2000;17:243–50.PubMedCrossRefGoogle Scholar
- 48.Cheng A, Chan SL, Milhavet O, Wang S, Mattson MP. p38 MAP kinase mediates nitric oxide-induced apoptosis of neural progenitor cells. J Biol Chem. 2001;276:43320–7.PubMedCrossRefGoogle Scholar
- 49.Nito C, Kamada H, Endo H, Niizuma K, Myer DJ, Chan PH. Role of the p38 mitogen-activated protein kinase/cytosolic phospholipase A2 signaling pathway in blood-brain barrier disruption after focal cerebral ischemia and reperfusion. J Cereb Blood Flow Metab. 2008;28:1686–96.PubMedCrossRefGoogle Scholar
- 50.Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007;35:495–516.PubMedCrossRefGoogle Scholar
- 51.Cho BB, Toledo-Pereyra LH. Caspase-independent programmed cell death following ischemic stroke. J Invest Surg. 2008;21:141–7.PubMedCrossRefGoogle Scholar
- 52.Li X, Nemoto M, Xu Z, Yu SW, Shimoji M, Andrabi SA, et al. Influence of duration of focal cerebral ischemia and neuronal nitric oxide synthase on translocation of apoptosis-inducing factor to the nucleus. Neuroscience 2007;144:56–65.PubMedCrossRefGoogle Scholar
- 53.Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJet al., Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 2002;297:200–1.CrossRefGoogle Scholar
- 54.Loh KP, Huang SH, De Silva R, Tan BK, Zhu YZ. Oxidative stress: apoptosis in neuronal injury. Curr Alzheimer Res. 2006;3:327–37.PubMedCrossRefGoogle Scholar
- 55.Sugawara T, Chan PH. Reactive oxygen radicals and pathogenesis of neuronal death after cerebral ischemia. Antioxid Redox Signal. 2003;5:597–607.PubMedCrossRefGoogle Scholar
- 56.Ayer RE, Zhang JH. Oxidative stress in subarachnoid haemorrhage: significance in acute brain injury and vasospasm. Acta Neurochir Suppl. 2008;104:33–41.PubMedCrossRefGoogle Scholar
- 57.Asano T. Oxyhemoglobin as the principal cause of cerebral vasospasm: a holistic view of its actions. Crit Rev Neurosurg. 1999;9:303–18.PubMedCrossRefGoogle Scholar
- 58.Gaetani P, Lombardi D. Brain damage following subarachnoid hemorrhage: the imbalance between anti-oxidant systems and lipid peroxidative processes. J Neurosurg Sci. 1992;36:1–10.PubMedGoogle Scholar
- 59.Kaynar MY, Tanriverdi T, Kemerdere R, Atukeren P, Gumustas K. Cerebrospinal fluid superoxide dismutase and serum malondialdehyde levels in patients with aneurysmal subarachnoid hemorrhage: preliminary results. Neurol Res. 2005;27:562–7.PubMedCrossRefGoogle Scholar
- 60.Fridman JS, Lowe SW. Control of apoptosis by p53. Oncogene 2003;22:9030–40.PubMedCrossRefGoogle Scholar
- 61.Culmsee C, Mattson MP. p53 in neuronal apoptosis. Biochem Biophys Res Commun. 2005;331:761–77.PubMedCrossRefGoogle Scholar
- 62.Cahill J, Calvert JW, Marcantonio S, Zhang JH. p53 may play an orchestrating role in apoptotic cell death after experimental subarachnoid hemorrhage. Neurosurgery 2007;60:531–45PubMedCrossRefGoogle Scholar
- 63.Gao C, Liu X, Liu W, Shi H, Zhao Z, Chen Het al., Anti-apoptotic and neuroprotective effects of Tetramethylpyrazine following subarachnoid hemorrhage in rats. Auton Neurosci. 2008;141:22–30.PubMedCrossRefGoogle Scholar
- 64.Martin-Villalba A, Herr I, Jeremias I, Hahne M, Brandt R, Vogel J et al. CD95 ligand (Fas-L/APO-1L) and tumor necrosis factor-related apoptosis-inducing ligand mediate ischemia-induced apoptosis in neurons. J Neurosci. 1999;19:3809–17.PubMedGoogle Scholar
- 65.Rosenbaum DM, Gupta G, D’Amore J, Singh M, Weidenheim K, Zhang Het al., Fas (CD95/APO-1) plays a role in the pathophysiology of focal cerebral ischemia. J Neurosci Res. 2000;61:686–92.PubMedCrossRefGoogle Scholar
- 66.Yuan J, Horvitz HR. A first insight into the molecular mechanisms of apoptosis. Cell 2004;116(Suppl):53–6CrossRefGoogle Scholar
- 67.Kawano T, Morioka M, Yano S, Hamada J, Ushio Y, Miyamoto E et al. Decreased akt activity is associated with activation of forkhead transcription factor after transient forebrain ischemia in gerbil hippocampus. J Cereb Blood Flow Metab. 2002;22:926–34.PubMedCrossRefGoogle Scholar
- 68.Ma CX, Yin WN, Cai BW, He M, Wu J, Wang JY, et al. Activation of TLR4/NF-kappaB signaling pathway in early brain injury after subarachnoid hemorrhage. Neurol Res. doi:10,1179/016164109x12445616596283.Google Scholar
- 69.Ostrowski RP, Colohan AR, Zhang JH. Mechanisms of hyperbaric oxygen-induced neuroprotection in a rat model of subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2005;25:554–71.PubMedCrossRefGoogle Scholar
- 70.Ostrowski RP, Tang J, Zhang JH. Hyperbaric oxygen suppresses NADPH oxidase in a rat subarachnoid hemorrhage model. Stroke 2006;37:1314–8.PubMedCrossRefGoogle Scholar
- 71.Sugawara T, Jadhav V, Ayer R, Chen W, Suzuki H, Zhang JH. Thrombin inhibition by argatroban ameliorates early brain injury and improves neurological outcomes after experimental subarachnoid hemorrhage in rats. Stroke 2009;40:1530–2.PubMedCrossRefGoogle Scholar
- 72.Ersahin M, Toklu HZ, Cetinel S, Yüksel M, Yeğen BC, Sener G. Melatonin reduces experimental subarachnoid hemorrhage-induced oxidative brain damage and neurological symptoms. J Pineal Res. 2009;46:324–32.PubMedCrossRefGoogle Scholar
- 73.Lu H, Zhang DM, Chen HL, Lin YX, Hang CH, Yin HX, et al. N-acetylcysteine suppresses oxidative stress in experimental rats with subarachnoid hemorrhage. J Clin Neurosci. 2009;16:684–8.PubMedCrossRefGoogle Scholar
- 74.Lin CL, Dumont AS, Tsai YJ, Huang JH, Chang KP, Kwan AL, et al. 17beta-estradiol activates adenosine A(2a) receptor after subarachnoid hemorrhage. J Surg Res. doi:10,3171/20093JNS081660.Google Scholar