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Stroke Research and Treatment
Volume 2013 (2013), Article ID 394036, 9 pages
http://dx.doi.org/10.1155/2013/394036
Early Brain Injury: A Common Mechanism in Subarachnoid Hemorrhage and Global Cerebral Ischemia
1Division of Neurosurgery, St. Michael's Hospital, 30 Bond Street, Toronto, ON, M5B 1W8, Canada
2Labatt Family Centre of Excellence in Brain Injury and Trauma Research, Keenan Research Centre, Li Ka Shing Knowledge Institute of St. Michael's Hospital, 209 Victoria Street, Toronto, ON, M5B 1T8, Canada
3Department of Surgery, University of Toronto, 30 Bond Street, Toronto, ON, M5B 1W8, Canada
Received 11 December 2012; Accepted 27 January 2013
Academic Editor: Ryszard M. Pluta
Copyright © 2013 Mohammed Sabri et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Linked References
- C. J. Graf and D. W. Nibbelink, “Cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Report on a randomized treatment study. 3. Intracranial surgery,” Stroke, vol. 5, no. 4, pp. 557–601, 1974. View at Scopus
- J. T. King Jr., “Epidemiology of aneurysmal subarachnoid hemorrhage,” Neuroimaging Clinics of North America, vol. 7, no. 4, pp. 659–668, 1997. View at Scopus
- J. van Gijn, R. S. Kerr, and G. J. Rinkel, “Subarachnoid haemorrhage,” The Lancet, vol. 369, no. 9558, pp. 306–318, 2007. View at Publisher · View at Google Scholar · View at Scopus
- J. Hansen-Schwartz, P. Vajkoczy, R. L. Macdonald, R. M. Pluta, and J. H. Zhang, “Cerebral vasospasm: looking beyond vasoconstriction,” Trends in Pharmacological Sciences, vol. 28, no. 6, pp. 252–256, 2007. View at Publisher · View at Google Scholar · View at Scopus
- R. L. Macdonald, R. M. Pluta, and J. H. Zhang, “Cerebral vasospasm after subarachnoid hemorrhage: the emerging revolution,” Nature Clinical Practice Neurology, vol. 3, no. 5, pp. 256–263, 2007. View at Publisher · View at Google Scholar · View at Scopus
- W. J. Cahill, J. H. Calvert, and J. H. Zhang, “Mechanisms of early brain injury after subarachnoid hemorrhage,” Journal of Cerebral Blood Flow and Metabolism, vol. 26, no. 11, pp. 1341–1353, 2006. View at Publisher · View at Google Scholar · View at Scopus
- R. M. Pluta, J. Hansen-Schwartz, J. Dreier et al., “Cerebral vasospasm following subarachnoid hemorrhage: time for a new world of thought,” Neurological Research, vol. 31, no. 2, pp. 151–158, 2009. View at Publisher · View at Google Scholar · View at Scopus
- F. A. Sehba and J. B. Bederson, “Mechanisms of acute brain injury after subarachnoid hemorrhage,” Neurological Research, vol. 28, no. 4, pp. 381–398, 2006. View at Publisher · View at Google Scholar · View at Scopus
- F. A. Sehba and V. Friedrich, “Early micro vascular changes after subarachnoid hemorrhage,” Acta Neurochirurgica, vol. 110, no. 1, pp. 49–55, 2011. View at Scopus
- F. A. Sehba, J. Hou, R. M. Pluta, and J. H. Zhang, “. The importance of early brain injury after subarachnoid hemorrhage,” Progress in Neurobiology, vol. 97, pp. 14–37, 2012.
- V. Friedrich, R. Flores, A. Muller, W. Bi, E. I. Peerschke, and F. A. Sehba, “Reduction of neutrophil activity decreases early microvascular injury after subarachnoid haemorrhage,” Journal of Neuroinflammation, vol. 8, article 103, 2011.
- V. Friedrich, R. Flores, and F. A. Sehba, “Cell death starts early after subarachnoid hemorrhage,” Neuroscience Letters, vol. 512, pp. 6–11, 2012.
- F. A. Sehba, R. M. Pluta, and J. H. Zhang, “Metamorphosis of subarachnoid hemorrhage research: from delayed vasospasm to early brain injury,” Molecular Neurobiology, vol. 43, no. 1, pp. 27–40, 2011. View at Publisher · View at Google Scholar · View at Scopus
- K. P. Budohoski, M. Czosnyka, P. Smielewski et al., “Impairment of cerebral autoregulation predicts delayed cerebral ischemia after subarachnoid hemorrhage: a prospective observational study,” Stroke, vol. 43, pp. 3230–3237, 2012.
- J. P. Dreier, S. Major, A. Manning et al., “Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage,” Brain, vol. 132, no. 7, pp. 1866–1881, 2009. View at Publisher · View at Google Scholar · View at Scopus
- S. Yuksel, Y. B. Tosun, J. Cahill, and I. Solaroglu, “Early brain injury following aneurysmal subarachnoid hemorrhage: emphasis on cellular apoptosis,” Turkish Neurosurgery, vol. 22, pp. 529–533, 2012.
- S. A. Bernard, T. W. Gray, M. D. Buist et al., “Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia,” The New England Journal of Medicine, vol. 346, no. 8, pp. 557–563, 2002. View at Publisher · View at Google Scholar · View at Scopus
- N. A. Nussmeier, “A review of risk factors for adverse neurologic outcome after cardiac surgery,” Journal of Extra-Corporeal Technology, vol. 34, no. 1, pp. 4–10, 2002. View at Scopus
- I. Harukuni and A. Bhardwaj, “Mechanisms of brain injury after global cerebral ischemia,” Neurologic Clinics, vol. 24, no. 1, pp. 1–21, 2006. View at Publisher · View at Google Scholar · View at Scopus
- J. Hansen-Schwartz, N. L. Hoel, C. B. Xu, N. A. Svendgaard, and L. Edvinsson, “Subarachnoid hemorrhage-induced upregulation of the 5-HT1B receptor in cerebral arteries in rats,” Journal of Neurosurgery, vol. 99, no. 1, pp. 115–120, 2003. View at Scopus
- J. Hansen-Schwartz, N. L. Hoel, M. Zhou et al., “Subarachnoid hemorrhage enhances endothelin receptor expression and function in rat cerebral arteries,” Neurosurgery, vol. 52, no. 5, pp. 1188–1195, 2003. View at Scopus
- S. Johansson, G. K. Povlsen, and L. Edvinsson, “Expressional changes in cerebrovascular receptors after experimental transient forebrain ischemia,” PLoS ONE, vol. 7, Article ID e41852, 2012.
- M. A. Moskowitz, E. H. Lo, and C. Iadecola, “The science of stroke: mechanisms in search of treatments,” Neuron, vol. 67, no. 2, pp. 181–198, 2010. View at Publisher · View at Google Scholar · View at Scopus
- J. Yuan, “Neuroprotective strategies targeting apoptotic and necrotic cell death for stroke,” Apoptosis, vol. 14, no. 4, pp. 469–477, 2009. View at Publisher · View at Google Scholar · View at Scopus
- P. J. A. M. Brouwers, D. W. J. Dippel, M. Vermeulen, K. W. Lindsay, D. Hasan, and J. Van Gijn, “Amount of blood on computed tomography as an independent predictor after aneurysm rupture,” Stroke, vol. 24, no. 6, pp. 809–814, 1993. View at Scopus
- J. W. Hop, G. J. E. Rinkel, A. Algra, and J. Van Gijn, “Initial loss of consciousness and risk of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage,” Stroke, vol. 30, no. 11, pp. 2268–2271, 1999. View at Scopus
- J. M. Schmidt, F. Rincon, A. Fernandez et al., “Cerebral infarction associated with acute subarachnoid hemorrhage,” Neurocritical Care, vol. 7, no. 1, pp. 10–17, 2007. View at Publisher · View at Google Scholar · View at Scopus
- K. Aoki, A. Y. Zubkov, I. B. Ross, and J. H. Zhang, “Therapeutic effect of caspase inhibitors in the prevention of apoptosis and reversal of chronic cerebral vasospasm,” Journal of Clinical Neuroscience, vol. 9, no. 6, pp. 672–677, 2002. View at Publisher · View at Google Scholar · View at Scopus
- J. Cahill, J. W. Calvert, I. Solaroglu, and J. H. Zhang, “Vasospasm and p53-induced apoptosis in an experimental model of subarachnoid hemorrhage,” Stroke, vol. 37, no. 7, pp. 1868–1874, 2006. View at Publisher · View at Google Scholar · View at Scopus
- R. Nau, S. Haase, S. Bunkowski, and W. Brück, “Neuronal apoptosis in the denate gyrus in humans with subarachnoid hemorrage and cerebral hypoxia,” Brain Pathology, vol. 12, no. 3, pp. 329–336, 2002. View at Scopus
- G. F. Prunell, N. A. Svendgaard, K. Alkass, and T. Mathiesen, “Delayed cell death related to acute cerebral blood flow changes following subarachnoid hemorrhage in the rat brain,” Journal of Neurosurgery, vol. 102, no. 6, pp. 1046–1054, 2005. View at Publisher · View at Google Scholar · View at Scopus
- E. Güresir, A. Raabe, A. Jaiimsin et al., “Histological evidence of delayed ischemic brain tissue damage in the rat double-hemorrhage model,” Journal of the Neurological Sciences, vol. 293, no. 1-2, pp. 18–22, 2010. View at Publisher · View at Google Scholar · View at Scopus
- G. Cheng, L. Wei, S. Zhi-Dan, Z. Shi-Guang, and L. Xiang-Zhen, “Atorvastatin ameliorates cerebral vasospasm and early brain injury after subarachnoid hemorrhage and inhibits caspase-dependent apoptosis pathway,” BMC Neuroscience, vol. 10, article 7, 2009. View at Publisher · View at Google Scholar · View at Scopus
- H. Endo, C. Nito, H. Kamada, F. Yu, and P. H. Chan, “Reduction in oxidative stress by superoxide dismutase overexpression attenuates acute brain injury after subarachnoid hemorrhage via activation of Akt/glycogen synthase kinase-3β survival signaling,” Journal of Cerebral Blood Flow and Metabolism, vol. 27, no. 5, pp. 975–982, 2007. View at Publisher · View at Google Scholar · View at Scopus
- Y. Hasegawa, H. Suzuki, T. Sozen, O. Altay, and J. H. Zhang, “Apoptotic mechanisms for neuronal cells in early brain injury after subarachnoid hemorrhage,” Acta Neurochirurgica, vol. 110, no. 1, pp. 43–48, 2011. View at Scopus
- P. Matz, P. Weinstein, B. States, J. Honkaniemi, and F. R. Sharp, “Subarachnoid injections of lysed blood induce the hsp70 stress gene and produce DNA fragmentation in focal areas of the rat brain,” Stroke, vol. 27, no. 3, pp. 504–513, 1996. View at Scopus
- J. Dhawan, H. Benveniste, Z. Luo, M. Nawrocky, S. D. Smith, and A. Biegon, “A new look at glutamate and ischemia: NMDA agonist improves long-term functional outcome in a rat model of stroke,” Future Neurology, vol. 6, pp. 823–834, 2011.
- D. W. Choi, “Excitotoxic cell death,” Journal of Neurobiology, vol. 23, no. 9, pp. 1261–1276, 1992. View at Publisher · View at Google Scholar · View at Scopus
- C. Zhou, M. Yamaguchi, G. Kusaka, C. Schonholz, A. Nanda, and J. H. Zhang, “Caspase inhibitors prevent endothelial apoptosis and cerebral vasospasm in dog model of experimental subarachnoid hemorrhage,” Journal of Cerebral Blood Flow and Metabolism, vol. 24, no. 4, pp. 419–431, 2004. View at Scopus
- S. Park, M. Yamaguchi, C. Zhou, J. W. Calvert, J. Tang, and J. H. Zhang, “Neurovascular protection reduces early brain injury after subarachnoid hemorrhage,” Stroke, vol. 35, no. 10, pp. 2412–2417, 2004. View at Publisher · View at Google Scholar · View at Scopus
- H. Endo, C. Nito, H. Kamada, F. Yu, and P. H. Chan, “Akt/GSK3β survival signaling is involved in acute brain injury after subarachnoid hemorrhage in rats,” Stroke, vol. 37, no. 8, pp. 2140–2146, 2006. View at Publisher · View at Google Scholar · View at Scopus
- R. W. S. Li, C. M. Tse, R. Y. K. Man, P. M. Vanhoutte, and G. P. H. Leung, “Inhibition of human equilibrative nucleoside transporters by dihydropyridine-type calcium channel antagonists,” European Journal of Pharmacology, vol. 568, no. 1–3, pp. 75–82, 2007. View at Publisher · View at Google Scholar · View at Scopus
- T. Shintani and D. J. Klionsky, “Autophagy in health and disease: a double-edged sword,” Science, vol. 306, no. 5698, pp. 990–995, 2004. View at Publisher · View at Google Scholar · View at Scopus
- C. H. Jing, L. Wang, P. P. Liu, C. Wu, D. Ruan, and G. Chen, “Autophagy activation is associated with neuroprotection against apoptosis via a mitochondrial pathway in a rat model of subarachnoid hemorrhage,” Neuroscience, vol. 213, pp. 144–153, 2012.
- P. Codogno and A. J. Meijer, “Autophagy and signaling: their role in cell survival and cell death,” Cell Death and Differentiation, vol. 12, supplement 2, pp. 1509–1518, 2005. View at Publisher · View at Google Scholar · View at Scopus
- J. Y. Lee, Y. He, O. Sagher, R. Keep, Y. Hua, and G. Xi, “Activated autophagy pathway in experimental subarachnoid hemorrhage,” Brain Research, vol. 1287, pp. 126–135, 2009. View at Publisher · View at Google Scholar · View at Scopus
- Z. Wang, X. Y. Shi, J. Yin, G. Zuo, J. Zhang, and G. Chen, “Role of autophagy in early brain injury after experimental subarachnoid hemorrhage,” Journal of Molecular Neuroscience, vol. 46, pp. 192–202, 2012. View at Publisher · View at Google Scholar · View at Scopus
- U. Dirnagl, C. Iadecola, and M. A. Moskowitz, “Pathobiology of ischaemic stroke: an integrated view,” Trends in Neurosciences, vol. 22, no. 9, pp. 391–397, 1999. View at Publisher · View at Google Scholar · View at Scopus
- M. Leist and P. Nicotera, “The shape of cell death,” Biochemical and Biophysical Research Communications, vol. 236, no. 1, pp. 1–9, 1997. View at Publisher · View at Google Scholar · View at Scopus
- M. Ankarcrona, J. M. Dypbukt, E. Bonfoco et al., “Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function,” Neuron, vol. 15, no. 4, pp. 961–973, 1995. View at Scopus
- S. H. Graham and J. Chen, “Programmed cell death in cerebral ischemia,” Journal of Cerebral Blood Flow and Metabolism, vol. 21, no. 2, pp. 99–109, 2001. View at Scopus
- T. Sugawara, M. Fujimura, N. Noshita et al., “Neuronal death/survival signaling pathways in cerebral ischemia,” NeuroRx, vol. 1, no. 1, pp. 17–25, 2004. View at Publisher · View at Google Scholar · View at Scopus
- M. Sabri, A. Kawashima, J. Ai, and R. L. Macdonald, “Neuronal and astrocytic apoptosis after subarachnoid hemorrhage: a possible cause for poor prognosis,” Brain Research, vol. 1238, pp. 163–171, 2008. View at Publisher · View at Google Scholar · View at Scopus
- R. M. Pluta, “New regulatory, signaling pathways, and sources of nitric oxide,” Acta Neurochirurgica, vol. 110, no. 1, pp. 7–12, 2011. View at Scopus
- J. K. B. Afshar, R. M. Pluta, R. J. Boock, B. G. Thompson, and E. H. Oldfield, “Effect of intracarotid nitric oxide on primate cerebral vasospasm after subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 83, no. 1, pp. 118–122, 1995. View at Scopus
- R. M. Pluta, A. Dejam, G. Grimes, M. T. Gladwin, and E. H. Oldfield, “Nitrite infusions to prevent delayed cerebral vasospasm in a primate model of subarachnoid hemorrhage,” Journal of the American Medical Association, vol. 293, no. 12, pp. 1477–1484, 2005. View at Publisher · View at Google Scholar · View at Scopus
- A. Y. Schwartz, F. A. Sehba, and J. B. Bederson, “Decreased nitric oxide availability contributes to acute cerebral ischemia after subarachnoid hemorrhage,” Neurosurgery, vol. 47, no. 1, pp. 208–215, 2000. View at Publisher · View at Google Scholar · View at Scopus
- F. A. Sehba, A. Y. Schwartz, I. Chereshnev, and J. B. Bederson, “Acute decrease in cerebral nitric oxide levels after subarachnoid hemorrhage,” Journal of Cerebral Blood Flow and Metabolism, vol. 20, no. 3, pp. 604–611, 2000. View at Scopus
- H. Yatsushige, J. W. Calvert, J. Cahill, and J. H. Zhang, “Limited role of inducible nitric oxide synthase in blood-brain barrier function after experimental subarachnoid hemorrhage,” Journal of Neurotrauma, vol. 23, no. 12, pp. 1874–1882, 2006. View at Publisher · View at Google Scholar · View at Scopus
- M. Sabri, J. Ai, B. Knight et al., “Uncoupling of endothelial nitric oxide synthase after experimental subarachnoid hemorrhage,” Journal of Cerebral Blood Flow and Metabolism, vol. 31, no. 1, pp. 190–199, 2011. View at Publisher · View at Google Scholar · View at Scopus
- M. Sabri, J. Ai, P. A. Marsden, and R. L. Macdonald, “Simvastatin re-couples dysfunctional endothelial nitric oxide synthase in experimental subarachnoid hemorrhage,” PLoS ONE, vol. 6, no. 2, Article ID e17062, 2011. View at Publisher · View at Google Scholar · View at Scopus
- Z. Huang, P. L. Huang, J. Ma et al., “Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine,” Journal of Cerebral Blood Flow and Metabolism, vol. 16, no. 5, pp. 981–987, 1996. View at Scopus
- E. H. Lo, T. Dalkara, and M. A. Moskowitz, “Mechanisms, challenges and opportunities in stroke,” Nature Reviews Neuroscience, vol. 4, no. 5, pp. 399–415, 2003. View at Publisher · View at Google Scholar · View at Scopus
- M. Erşahin, H. Z. Toklu, S. Çetinel et al., “Alpha lipoic acid alleviates oxidative stress and preserves blood brain permeability in rats with subarachnoid hemorrhage,” Neurochemical Research, vol. 35, no. 3, pp. 418–428, 2010. View at Publisher · View at Google Scholar · View at Scopus
- C. Imperatore, A. Germanò, D. D'Avella, F. Tomasello, and G. Costa, “Effects of the radical scavenger AVS on behavioral and BBB changes after experimental subarachnoid hemorrhage,” Life Sciences, vol. 66, no. 9, pp. 779–790, 2000. View at Publisher · View at Google Scholar · View at Scopus
- C. L. Lin, Y. T. Hsu, T. K. Lin et al., “Increased levels of F2-isoprostanes following aneurysmal subarachnoid hemorrhage in humans,” Free Radical Biology and Medicine, vol. 40, no. 8, pp. 1466–1473, 2006. View at Publisher · View at Google Scholar · View at Scopus
- R. L. Macdonald and B. K. Weir, “Cerebral vasospasm and free radicalse,” Free Radical Biology and Medicine, vol. 16, no. 5, pp. 633–643, 1994. View at Publisher · View at Google Scholar · View at Scopus
- F. Marzatico, P. Gaetani, F. Tartara et al., “Antioxidant status and α1-antiproteinase activity in subarachnoid hemorrhage patients,” Life Sciences, vol. 63, no. 10, pp. 821–826, 1998. View at Publisher · View at Google Scholar · View at Scopus
- S. Sakaki, H. Kuwabara, and S. Ohta, “Biological defence mechanism in the pathogenesis of prolonged cerebral vasospasm in the patients with ruptured intracranial aneurysms,” Stroke, vol. 17, no. 2, pp. 196–202, 1986. View at Scopus
- A. A. Miller, K. Budzyn, and C. G. Sobey, “Vascular dysfunction in cerebrovascular disease: mechanisms and therapeutic intervention,” Clinical Science, vol. 119, no. 1, pp. 1–17, 2010. View at Publisher · View at Google Scholar · View at Scopus
- T. M. Paravicini and C. G. Sobey, “Cerebral vascular effects of reactive oxygen species: recent evidence for a role of NADPH-oxidase,” Clinical and Experimental Pharmacology and Physiology, vol. 30, no. 11, pp. 855–859, 2003. View at Publisher · View at Google Scholar · View at Scopus
- S. P. Didion and F. M. Faraci, “Effects of NADH and NADPH on superoxide levels and cerebral vascular tone,” American Journal of Physiology, vol. 282, no. 2, pp. H688–H695, 2002. View at Scopus
- D. E. Kim, Y. S. Suh, M. S. Lee et al., “Vascular NAD(P)H oxidase triggers delayed cerebral vasospasm after subarachnoid hemorrhage in rats,” Stroke, vol. 33, no. 11, pp. 2687–2691, 2002. View at Publisher · View at Google Scholar · View at Scopus
- R. E. Ayer and J. H. Zhang, “Oxidative stress in subarachnoid haemorrhage: significance in acute brain injury and vasospasm,” Acta Neurochirurgica, vol. 104, pp. 33–41, 2008. View at Publisher · View at Google Scholar · View at Scopus
- N. Marklund, B. Östman, L. Nalmo, L. Persson, and L. Hillered, “Hypoxanthine, uric acid and allantoin as indicators of in vivo free radical reactions. Description of a HPLC method and human brain microdialysis data,” Acta Neurochirurgica, vol. 142, no. 10, pp. 1135–1142, 2000. View at Publisher · View at Google Scholar · View at Scopus
- P. Kim, T. L. Yaksh, S. D. Romero, and T. M. Sundt Jr., “Production of uric acid in cerebrospinal fluid after subarachnoid hemorrhage in dogs: investigation of the possible role of xanthine oxidase in chronic vasospasm,” Neurosurgery, vol. 21, no. 1, pp. 39–44, 1987. View at Scopus
- S. Goto, R. Xue, N. Sugo et al., “Poly(ADP-ribose) polymerase impairs early and long-term experimental stroke recovery,” Stroke, vol. 33, no. 4, pp. 1101–1106, 2002. View at Publisher · View at Google Scholar · View at Scopus
- K. L. Chaichana, G. Pradilla, J. Huang, and R. J. Tamargo, “Role of inflammation (leukocyte-endothelial cell interactions) in vasospasm after subarachnoid hemorrhage,” World Neurosurgery, vol. 73, no. 1, pp. 22–41, 2010. View at Publisher · View at Google Scholar · View at Scopus
- A. S. Dumont, R. J. Dumont, M. M. Chow et al., “Cerebral vasospasm after subarachnoid hemorrhage: putative role of inflammation,” Neurosurgery, vol. 53, no. 1, pp. 123–135, 2003. View at Scopus
- M. Erşahin, H. Z. Toklu, C. Erzik et al., “The anti-inflammatory and neuroprotective effects of ghrelin in subarachnoid hemorrhage-induced oxidative brain damage in rats,” Journal of Neurotrauma, vol. 27, no. 6, pp. 1143–1155, 2010. View at Publisher · View at Google Scholar · View at Scopus
- T. Sozen, R. Tsuchiyama, Y. Hasegawa et al., “Role of interleukin-1β in early brain injury after subarachnoid hemorrhage in mice,” Stroke, vol. 40, no. 7, pp. 2519–2525, 2009. View at Publisher · View at Google Scholar · View at Scopus
- T. Sugawara, V. Jadhav, R. Ayer, W. Chen, H. Suzuki, and J. H. Zhang, “Thrombin inhibition by argatroban ameliorates early brain injury and improves neurological outcomes after experimental subarachnoid hemorrhage in rats,” Stroke, vol. 40, no. 4, pp. 1530–1532, 2009. View at Publisher · View at Google Scholar · View at Scopus
- M. L. Zhou, J. X. Shi, C. H. Hang et al., “Potential contribution of nuclear factor-κB to cerebral vasospasm after experimental subarachnoid hemorrhage in rabbits,” Journal of Cerebral Blood Flow and Metabolism, vol. 27, no. 9, pp. 1583–1592, 2007. View at Publisher · View at Google Scholar · View at Scopus
- K. Fassbender, B. Hodapp, S. Rossol et al., “Endothelin-1 in subarachnoid hemorrhage: an acute-phase reactant produced by cerebrospinal fluid leukocytes,” Stroke, vol. 31, pp. 2971–2975, 2000.
- M. J. McGirt, J. C. Mavropoulos, L. Y. McGirt et al., “Leukocytosis as an independent risk factor for cerebral vasospasm following aneurysmal subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 98, no. 6, pp. 1222–1226, 2003. View at Scopus
- E. N. Momin, K. E. Schwab, K. L. Chaichana, R. Miller-Lotan, A. P. Levy, and R. J. Tamargo, “Controlled delivery of nitric oxide inhibits leukocyte migration and prevents vasospasm in haptoglobin 2-2 mice after subarachnoid hemorrhage,” Neurosurgery, vol. 65, no. 5, pp. 937–945, 2009. View at Publisher · View at Google Scholar · View at Scopus
- W. Jia, R. Wang, J. Zhao et al., “E-selectin expression increased in human ruptured cerebral aneurysm tissues,” Canadian Journal of Neurological Sciences, vol. 38, pp. 858–862, 2011.
- I. Ginis, R. Jaiswal, D. Klimanis, J. Liu, J. Greenspon, and J. M. Hallenbeck, “TNF-α-induced tolerance to ischemic injury involves differential control of NF-κB transactivation: the role of NF-κB association with p300 adaptor,” Journal of Cerebral Blood Flow and Metabolism, vol. 22, no. 2, pp. 142–152, 2002. View at Scopus
- R. Ayer, V. Jadhav, T. Sugawara, and J. H. Zhang, “The neuroprotective effects of cyclooxygenase-2 inhibition in a mouse model of aneurysmal subarachnoid hemorrhage,” Acta Neurochirurgica, vol. 111, pp. 145–149, 2011. View at Publisher · View at Google Scholar · View at Scopus
- J. Claassen, J. R. Carhuapoma, K. T. Kreiter, E. Y. Du, E. S. Connolly, and S. A. Mayer, “Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome,” Stroke, vol. 33, no. 5, pp. 1225–1232, 2002. View at Publisher · View at Google Scholar · View at Scopus
- T. Meguro, B. Chen, J. Lancon, and J. H. Zhang, “Oxyhemoglobin induces caspase-mediated cell death in cerebral endothelial cells,” Journal of Neurochemistry, vol. 77, no. 4, pp. 1128–1135, 2001. View at Publisher · View at Google Scholar · View at Scopus
- Y. Gao, R. Yokota, S. Tang, A. W. Ashton, and J. A. Ware, “Reversal of angiogenesis in vitro, induction of apoptosis, and inhibition of Akt phosphorylation in endothelial cells by thromboxane A2,” Circulation Research, vol. 87, no. 9, pp. 739–745, 2000. View at Scopus
- J. Yan, L. Li, N. H. Khatibi et al., “Blood-brain barrier disruption following subarchnoid hemorrhage may be faciliated through PUMA induction of endothelial cell apoptosis from the endoplasmic reticulum,” Experimental Neurology, vol. 230, no. 2, pp. 240–247, 2011. View at Publisher · View at Google Scholar · View at Scopus
- Z. Guo, X. Sun, Z. He, Y. Jiang, X. Zhang, and J. H. Zhang, “Matrix metalloproteinase-9 potentiates early brain injury after subarachnoid hemorrhage,” Neurological Research, vol. 32, no. 7, pp. 715–720, 2010. View at Publisher · View at Google Scholar · View at Scopus
- F. A. Sehba, G. Mostafa, J. Knopman, V. Friedrich Jr., and J. B. Bederson, “Acute alterations in microvascular basal lamina after subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 101, no. 4, pp. 633–640, 2004. View at Publisher · View at Google Scholar · View at Scopus
- H. Suzuki, Y. Hasegawa, W. Chen, K. Kanamaru, and J. H. Zhang, “Recombinant osteopontin in cerebral vasospasm after subarachnoid hemorrhage,” Annals of Neurology, vol. 68, no. 5, pp. 650–660, 2010. View at Publisher · View at Google Scholar · View at Scopus
- H. Yatsushige, R. P. Ostrowski, T. Tsubokawa, A. Colohan, and J. H. Zhang, “Role of c-Jun N-terminal kinase in early brain injury after subarachnoid hemorrhage,” Journal of Neuroscience Research, vol. 85, no. 7, pp. 1436–1448, 2007. View at Publisher · View at Google Scholar · View at Scopus
- K. Schöller, A. Trinkl, M. Klopotowski et al., “Characterization of microvascular basal lamina damage and blood-brain barrier dysfunction following subarachnoid hemorrhage in rats,” Brain Research, vol. 1142, no. 1, pp. 237–246, 2007. View at Publisher · View at Google Scholar · View at Scopus
- G. H. Danton and W. D. Dietrich, “Inflammatory mechanisms after ischemia and stroke,” Journal of Neuropathology and Experimental Neurology, vol. 62, no. 2, pp. 127–136, 2003. View at Scopus
- H. S. Han and M. A. Yenari, “Cellular targets of brain inflammation in stroke,” Current Opinion in Investigational Drugs, vol. 4, no. 5, pp. 522–529, 2003. View at Scopus
- A. Germanò, M. Caffo, F. F. Angileri et al., “NMDA receptor antagonist felbamate reduces behavioral deficits and blood-brain barrier permeability changes after experimental subarachnoid hemorrhage in the rat,” Journal of Neurotrauma, vol. 24, no. 4, pp. 732–744, 2007. View at Publisher · View at Google Scholar · View at Scopus
- A. W. Unterberg, O. W. Sakowitz, A. S. Sarrafzadeh, G. Benndorf, and W. R. Lanksch, “Role of bedside microdialysis in the diagnosis of cerebral vasospasm following aneurysmal subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 94, no. 5, pp. 740–749, 2001. View at Scopus