The rodent endovascular puncture model of subarachnoid hemorrhage: Mechanisms of brain damage and therapeutic strategies

Journal of Neuroinflammation

Volumn 11, Issue , 2014, Pages

  Kooijman, Elke ^a   Nijboer, Cora H ^a   van Velthoven, Cindy T J ^a   Kavelaars, Annemieke ^b   Kesecioglu, Jozef ^a   Heijnen, Cobi J ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Cell death; Endovascular puncture; Inflammation; Neuroregeneration; Stem cells; Subarachnoid hemorrhage; Treatment options

Indexed keywords

CHEMOKINE; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAGNESIUM SULFATE; MITOGEN ACTIVATED PROTEIN KINASE; NIMODIPINE; SIALOGLYCOPROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1;

APOPTOSIS; AUTOPHAGY; BRAIN DAMAGE; BRAIN NECROSIS; CELL DEATH; CLINICAL FEATURE; CYTOKINE PRODUCTION; DRUG TARGETING; ENCEPHALITIS; HUMAN; INFLAMMATORY CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NECROPTOSIS; NERVE CELL INHIBITION; NERVE CELL LESION; NEUROPROTECTION; NONHUMAN; PARENCHYMA; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SUBARACHNOID HEMORRHAGE; SURVIVAL; UPREGULATION;

ANIMALS; APOPTOSIS; BRAIN INJURIES; CYTOKINES; DISEASE MODELS, ANIMAL; HUMANS; PUNCTURES; SIGNAL TRANSDUCTION; SUBARACHNOID HEMORRHAGE;

EID: 84892142596     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-11-2     Document Type: Review

References (150)

1. Anderson CS. The ACROSS group Epidemiology of aneurysmal subarachnoid hemorrhage in Australia and New Zealand: incidence and case fatality from the Australasian Cooperative Research on Subarachnoid Hemorrhage Study (ACROSS). Stroke 2000, 31:1843-1850. The ACROSS group.
2. de Rooij NK, Linn FH, van der Plas JA, Algra A, Rinkel GJ. Incidence of subarachnoid hemorrhage: a systematic review with emphasis on region, age, gender and time trends. J Neurol Neurosurg Psychiatry 2007, 78:1365-1372. 10.1136/jnnp.2007.117655, 2095631, 17470467.
3. Thrift AG, Dewey HM, Sturm JW, Srikanth VK, Gilligan AK, Gall SL, Macdonell RAL, McNeil JJ, Donnan GA. Incidence of stroke subtypes in the North East Melbourne Stroke Incidence Study (NEMESIS): differences between men and women. Neuroepidemiology 2009, 32:11-18. 10.1159/000170086, 18997472.
4. Van GJ, Kerr RS, Rinkel GJ. Subarachnoid hemorrhage. Lancet 2007, 369:306-318. 10.1016/S0140-6736(07)60153-6, 17258671.
5. Al-Tamimi YZ, Orsi NM, Quinn AC, Homer-Vanniasinkam S, Ross SA. A review of delayed ischemic neurologic deficit following aneurysmal subarachnoid hemorrhage: historical overview, current treatment, and pathophysiology. World Neurosurg 2010, 73:654-667. 10.1016/j.wneu.2010.02.005, 20934153.
6. Dankbaar JW, Rijsdijk M, Van DSI, Velthuis BK, Wermer MJ, Rinkel GJ. Relationship between vasospasm, cerebral perfusion, and delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Neuroradiology 2009, 51:813-819. 10.1007/s00234-009-0575-y, 2773037, 19623472.
7. Laskowitz DT, Kolls BJ. Neuroprotection in subarachnoid hemorrhage. Stroke 2010, 41:S79-S84. 10.1161/STROKEAHA.110.595090, 3376008, 20876512.
8. Bederson JB, Levy AL, Ding WH, Kahn R, DiPerna CA, Jenkins AL, Vallabhajosyula P. Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery 1998, 42:352-360. 10.1097/00006123-199802000-00091, 9482187.
9. Critchley GR, Bell BA. Acute cerebral tissue oxygenation changes following experimental subarachnoid hemorrhage. Neurol Res 2003, 25:451-456. 10.1179/016164103101201841, 12866191.
10. 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, 52:165-175.
11. Prunell GF, Mathiesen T, Svendgaard NA. Experimental subarachnoid hemorrhage: cerebral blood flow and brain metabolism during the acute phase in three different models in the rat. Neurosurgery 2004, 54:426-436. 10.1227/01.NEU.0000103670.09687.7A, 14744290.
12. Thal SC, Sporer S, Klopotowski M, Thal SE, Woitzik J, Schmid-Elsaesser R, Plesnila N, Zausinger S. Brain edema formation and neurological impairment after subarachnoid hemorrhage in rats. J Neurosurg 2009, 111:988-994. 10.3171/2009.3.JNS08412, 19425896.
13. Westermaier T, Jauss A, Eriskat J, Kunze E, Roosen K. Time-course of cerebral perfusion and tissue oxygenation in the first six hours after experimental subarachnoid hemorrhage in rats. J Cereb Blood Flow Metab 2009, 29:771-779. 10.1038/jcbfm.2008.169, 19156162.
14. Pluta RM, Hansen-Schwartz J, Dreier J, Vajkoczy P, Macdonald RL, Nishizawa S, Kasuya H, Wellman G, Keller E, Zauner A, et al. Cerebral vasospasm following subarachnoid hemorrhage: time for a new world of thought. Neurol Res 2009, 31:151-158. 10.1179/174313209X393564, 2706525, 19298755.
15. Marbacher S, Fandino J, Kitchen ND. Standard intracranial in vivo animal models of delayed cerebral vasospasm. Br J Neurosurg 2010, 24:415-434. 10.3109/02688691003746274, 20726750.
16. Gules I, Satoh M, Clower BR, Nanda A, Zhang JH. Comparison of three rat models of cerebral vasospasm. Am J Physiol Heart Circ Physiol 2002, 283:H2551-H2559.
17. Ostrowski RP, Colohan ART, Zhang JH. Mechanisms of hyperbaric oxygen-induced neuroprotection in a rat model of subarachnoid hemorrhage. J Cereb Blood Flow Metab 2005, 25:554-571. 10.1038/sj.jcbfm.9600048, 15703702.
18. van den Bergh WM, Schepers J, Veldhuis WB, Nicolay K, Tulleken CA, Rinkel GJ. Magnetic resonance imaging in experimental subarachnoid hemorrhage. Acta Neurochir (Wien) 2005, 147:977-983. 10.1007/s00701-005-0539-x, 15900401.
19. Dankbaar JW, Slooter AJ, Rinkel GJ, Schaaf IC. Effect of different components of triple-H therapy on cerebral perfusion in patients with aneurysmal subarachnoid hemorrhage: a systematic review. Crit Care 2010, 14:R23. 10.1186/cc8886, 2875538, 20175912.
20. Li H, Pan R, Wang H, Rong X, Yin Z, Milgrom DP, Shi X, Tang Y, Peng Y. Clipping versus coiling for ruptured intracranial aneurysms: a systematic review and meta-analysis. Stroke 2013, 44:29-37. 10.1161/STROKEAHA.112.663559, 23238862.
21. Priebe HJ. Aneurysmal subarachnoid hemorrhage and the anesthetist. Br J Anaesth 2007, 99:102-118. 10.1093/bja/aem119, 17525049.
22. Linares G, Mayer SA. Hypothermia for the treatment of ischemic and hemorrhagic stroke. Crit Care Med 2009, 37:S243-S249. 10.1097/CCM.0b013e3181aa5de1, 19535954.
23. Scaravilli V, Tinchero G, Citerio G. Fever management in SAH. Neurocrit Care 2011, 15:287-294. 10.1007/s12028-011-9588-6, 21755388.
24. Schirmer CM, Ackil AA, Malek AM. Decompressive Craniectomy. Neurocrit Care 2008, 8:456-470. 10.1007/s12028-008-9082-y, 18392785.
25. Lee Y, Zuckerman SL, Mocco J. Current controversies in the prediction, diagnosis, and management of cerebral vasospasm: where do we stand?. Neurol Res Int 2013, 2013:373458. 3817677, 24228177.
26. Wong GK, Poon WS. Magnesium sulphate for aneurysmal subarachnoid hemorrhage: why, how, and current controversy. Acta Neurochir Suppl 2013, 115:45-48.
27. Fassbender K, Hodapp B, Rossol S, Bertsch T, Schmeck J, Schutt S, Fritzinger M, Horn P, Vajkoczy P, Kreisel S, et al. Inflammatory cytokines in subarachnoid hemorrhage: association with abnormal blood flow velocities in basal cerebral arteries. J Neurol Neurosurg Psychiatry 2001, 70:534-537. 10.1136/jnnp.70.4.534, 1737308, 11254783.
28. Naredi S, Lambert G, Friberg P, Zall S, Eden E, Rydenhag B, Tylman M, Bengtsson A. Sympathetic activation and inflammatory response in patients with subarachnoid hemorrhage. Intensive Care Med 2006, 32:1955-1961. 10.1007/s00134-006-0408-y, 17058068.
29. Yoshimoto Y, Tanaka Y, Hoya K. Acute systemic inflammatory response syndrome in subarachnoid hemorrhage. Stroke 2001, 32:1989-1993. 10.1161/hs0901.095646, 11546886.
30. Lee SJ, Benveniste EN. Adhesion molecule expression and regulation on cells of the central nervous system. J Neuroimmunol 1999, 98:77-88. 10.1016/S0165-5728(99)00084-3, 10430040.
31. Sercombe R, Dinh YR, Gomis P. Cerebrovascular inflammation following subarachnoid hemorrhage. Jpn J Pharmacol 2002, 88:227-249. 10.1254/jjp.88.227, 11949877.
32. Rothoerl RD, Schebesch KM, Kubitza M, Woertgen C, Brawanski A, Pina AL. ICAM-1 and VCAM-1 expression following aneurysmal subarachnoid hemorrhage and their possible role in the pathophysiology of subsequent ischemic deficits. Cerebrovasc Dis 2006, 22:143-149. 10.1159/000093243, 16691023.
33. Xie X, Wu X, Cui J, Li H, Yan X. Increase ICAM-1 and LFA-1 expression by cerebrospinal fluid of subarachnoid hemorrhage patients: involvement of TNF-α. Brain Res 2013, 1512:89-96.
34. Cahill J, Zhang JH. Subarachnoid hemorrhage: is it time for a new direction?. Stroke 2009, 40:S86-S87. 10.1161/STROKEAHA.108.533315, 2743545, 19064787.
35. Sozen T, Tsuchiyama R, Hasegawa Y, Suzuki H, Jadhav V, Nishizawa S, Zhang JH. Role of interleukin-1β in early brain injury after subarachnoid hemorrhage in mice. Stroke 2009, 40:2519-2525. 10.1161/STROKEAHA.109.549592, 2763121, 19461019.
36. Yamashita T, Abe K. Therapeutic approaches to vascular protection in ischemic stroke. Acta Med Okayama 2011, 65:219-223.
37. Chaichana KL, Pradilla G, Huang J, Tamargo RJ. Role of inflammation (leukocyte-endothelial cell interactions) in vasospasm after subarachnoid hemorrhage. World Neurosurg 2010, 73:22-41. 10.1016/j.surneu.2009.05.027, 20452866.
38. Kubota T, Handa Y, Tsuchida A, Kaneko M, Kobayashi H, Kubota T. The kinetics of lymphocyte subsets and macrophages in subarachnoid space after subarachnoid hemorrhage in rats. Stroke 1993, 24:1993-2000. 10.1161/01.STR.24.12.1993, 8248982.
39. Provencio J, Fu X, Siu A, Rasmussen P, Hazen S, Ransohoff R. CSF neutrophils are implicated in the development of vasospasm in subarachnoid hemorrhage. Neurocrit Care 2010, 12:244-251. 10.1007/s12028-009-9308-7, 2844469, 19967568.
40. Simard JM, Geng Z, Woo SK, Ivanova S, Tosun C, Melnichenko L, Gerzanich V. Glibenclamide reduces inflammation, vasogenic edema, and caspase-3 activation after subarachnoid hemorrhage. J Cereb Blood Flow Metab 2009, 29:317-330. 10.1038/jcbfm.2008.120, 2740919, 18854840.
41. Hendryk S, Jarzab B, Josko J. Increase of the IL-1 beta and IL-6 levels in CSF in patients with vasospasm following aneurysmal SAH. Neuro Endocrinol Lett 2004, 25:141-147.
42. Osuka K, Suzuki Y, Tanazawa T, Hattori K, Yamamoto N, Takayasu M, Shibuya M, Yoshida J. Interleukin-6 and development of vasospasm after subarachnoid hemorrhage. Acta Neurochir 1998, 140:943-951. 10.1007/s007010050197, 9842432.
43. Sarrafzadeh A, Schlenk F, Gericke C, Vajkoczy P. Relevance of cerebral interleukin-6 after aneurysmal subarachnoid hemorrhage. Neurocrit Care 2010, 13:339-346. 10.1007/s12028-010-9432-4, 20725805.
44. Magnoni S, Stocchetti N, Colombo G, Carlin A, Colombo A, Lipton JM, Catania A. α-melanocyte-stimulating hormone is decreased in plasma of patients with acute brain injury. J Neurotrauma 2003, 20:251-260. 10.1089/089771503321532833, 12820679.
45. Mathiesen T, Edner G, Ulfarsson E, Andersson B. Cerebrospinal fluid interleukin-1 receptor antagonist and tumor necrosis factor α following subarachnoid hemorrhage. J Neurosurg 1997, 87:215-220. 10.3171/jns.1997.87.2.0215, 9254084.
46. Nakahara T, Tsuruta R, Kaneko T, Yamashita S, Fujita M, Kasaoka S, Hashiguchi T, Suzuki M, Maruyama I, Maekawa T. High-mobility group box 1 protein in CSF of patients with subarachnoid hemorrhage. Neurocrit Care 2009, 11:362-368. 10.1007/s12028-009-9276-y, 19777384.
47. Prunell GF, Svendgaard NA, Alkass K, Mathiesen T. Inflammation in the brain after experimental subarachnoid hemorrhage. Neurosurgery 2005, 56:1082-1092.
48. Chou SH, Feske SK, Atherton J, Konigsberg RG, De Jager PL, Du R, Ogilvy CS, Lo EH, Ning M. Early elevation of serum tumor necrosis factor-alpha is associated with poor outcome in subarachnoid hemorrhage. J Investig Med 2012, 60:1054-1058. 3740211, 22918199.
49. Jiang Y, Liu DW, Han XY, Dong YN, Gao J, Du B, Meng L, Shi JG. Neuroprotective effects of anti-tumor necrosis factor-alpha antibody on apoptosis following subarachnoid hemorrhage in a rat model. J Clin Neurosci 2012, 19:866-872. 10.1016/j.jocn.2011.08.038, 22516550.
50. Vecchione C, Frati A, Di Pardo A, Cifelli G, Carnevale D, Gentile MT, Carangi R, Landolfi A, Carullo P, Bettarini U, et al. Tumor necrosis factor-α mediates hemolysis-induced vasoconstriction and the cerebral vasospasm evoked by subarachnoid hemorrhage. Hypertension 2009, 54:150-156. 10.1161/HYPERTENSIONAHA.108.128124, 19470883.
51. Seki S, Nakashima H, Nakashima M, Kinoshita M. Antitumor immunity produced by the liver Kupffer cells, NK cells, NKT cells, and CD8 CD122 T cells. Clin Dev Immunol 2011, 2011:868345. 3235445, 22190974.
52. Voloboueva LA, Giffard RG. Inflammation, mitochondria, and the inhibition of adult neurogenesis. J Neurosci Res 2011, 89:1989-1996. 10.1002/jnr.22768, 3671859, 21910136.
53. Behrens MM, Ali SS, Dugan LL. Interleukin-6 mediates the increase in NADPH-oxidase in the ketamine model of schizophrenia. J Neurosci 2008, 28:13957-13966. 10.1523/JNEUROSCI.4457-08.2008, 2752712, 19091984.
54. Wakade C, King MD, Laird MD, Alleyne CH, Dhandapani KM. Curcumin attenuates vascular inflammation and cerebral vasospasm after subarachnoid hemorrhage in mice. Antioxid Redox Signal 2009, 11:35-45. 10.1089/ars.2008.2056, 18752423.
55. Bowman G, Bonneau R, Chinchilli V, Tracey K, Cockroft K. A novel inhibitor of inflammatory cytokine production (CNI-1493) reduces rodent post-hemorrhagic vasospasm. Neurocrit Care 2006, 5:222-229. 10.1385/NCC:5:3:222, 17290094.
56. Kikuchi T, Okuda Y, Kaito N, Abe T. Cytokine production in cerebrospinal fluid after subarachnoid hemorrhage. Neurol Res 1995, 17:106-108.
57. 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, 22:1249-1255. 10.1023/A:1021985030331, 9342729.
58. 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, 40:1530-1532. 10.1161/STROKEAHA.108.531699, 2743552, 19228846.
59. Greenhalgh AD, Brough D, Robinson EM, Girard S, Rothwell NJ, Allan SM. Interleukin-1 receptor antagonist is beneficial after subarachnoid hemorrhage in rat by blocking hem-driven inflammatory pathology. Dis Model Mech 2012, 5:823-833. 10.1242/dmm.008557, 3484865, 22679224.
60. Chen S, Ma Q, Krafft PR, Hu Q, Rolland W, Sherchan P, Zhang J, Tang J, Zhang JH. P2X7R/cryopyrin inflammasome axis inhibition reduces neuroinflammation after SAH. Neurobiol Dis 2013, 58:296-307.
61. Suzuki H, Ayer R, Sugawara T, Chen W, Sozen T, Hasegawa Y, Kanamaru K, Zhang JH. Protective effects of recombinant osteopontin on early brain injury after subarachnoid hemorrhage in rats. Crit Care Med 2010, 38:612-618. 10.1097/CCM.0b013e3181c027ae, 2808465, 19851092.
62. Maddahi A, Ansar S, Chen Q, Edvinsson L. Blockade of the MEK/ERK pathway with a raf inhibitor prevents activation of pro-inflammatory mediators in cerebral arteries and reduction in cerebral blood flow after subarachnoid hemorrhage in a rat model. J Cereb Blood Flow Metab 2011, 31:144-154. 10.1038/jcbfm.2010.62, 3049479, 20424636.
63. Pan Y, Chen KF, Lin YX, Wu W, Zhou X, Zhang X, Zhang X, Shi J. Intracisternal administration of SB203580, a p38 mitogen-activated protein kinase inhibitor, attenuates cerebral vasospasm via inhibition of tumor-necrosis factor-alpha. J Clin Neurosci 2013, 20:726-730. 10.1016/j.jocn.2012.09.012, 23540891.
64. Ouyang L, Shi Z, Zhao S, Wang FT, Zhou TT, Liu B, Bao JK. Programmed cell death pathways in cancer: a review of apoptosis, autophagy and programmed necrosis. Cell Prolif 2012, 45:487-498. 10.1111/j.1365-2184.2012.00845.x, 23030059.
65. Perez-Pinzon MA, Stetler RA, Fiskum G. Novel mitochondrial targets for neuroprotection. J Cereb Blood Flow Metab 2012, 32:1362-1376. 10.1038/jcbfm.2012.32, 3390821, 22453628.
66. Gao C, Liu X, Liu W, Shi H, Zhao Z, Chen H, Zhao S. Anti-apoptotic and neuroprotective effects of tetramethylpyrazine following subarachnoid hemorrhage in rats. Auton Neurosci 2008, 141:22-30. 10.1016/j.autneu.2008.04.007, 18558517.
67. 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, 10:7. 10.1186/1471-2202-10-7, 2651177, 19159448.
68. Endo H, Nito C, Kamada H, Yu F, Chan PH. Akt/GSK3β survival signaling is involved in acute brain injury after subarachnoid hemorrhage in rats. Stroke 2006, 37:2140-2146. 10.1161/01.STR.0000229888.55078.72, 16794215.
69. Cahill J, Calvert JW, Zhang JH. Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab 2006, 26:1341-1353. 10.1038/sj.jcbfm.9600283, 16482081.
70. Palade C, Ciurea AV, Nica DA, Savu R, Moisa HA. Interference of apoptosis in the pathophysiology of subarachnoid hemorrhage. Asian J Neurosurg 2013, 8:106-111. 10.4103/1793-5482.116389, 3775181, 24049554.
71. Nijboer CH, Heijnen CJ, van der Kooij MA, Zijlstra J, van Velthoven CTJ, Culmsee C, van Bel F, Hagberg H, Kavelaars A. Targeting the p53 pathway to protect the neonatal ischemic brain. Ann Neurol 2011, 70:255-264. 10.1002/ana.22413, 21674585.
72. Cahill J, Calvert JW, Solaroglu I, Zhang JH. Vasospasm and p53-induced apoptosis in an experimental model of subarachnoid hemorrhage. Stroke 2006, 37:1868-1874. 10.1161/01.STR.0000226995.27230.96, 16741174.
73. Cahill J, Calvert JW, Marcantonio S, Zhang JH. p53 may play an orchestrating role in apoptotic cell death after experimental subarachnoid hemorrhage. Neurosurgery 2007, 60:531-545.
74. Yan J, Chen C, Hu Q, Yang X, Lei J, Yang L, Wang K, Qin L, Huang H, Zhou C. The role of p53 in brain edema after 24 hours of experimental subarachnoid hemorrhage in a rat model. Exp Neurol 2008, 214:37-46. 10.1016/j.expneurol.2008.07.006, 18691572.
75. Moll UM, Wolff S, Speidel D, Deppert W. Transcription-independent pro-apoptotic functions of p53. Curr Opin Cell Biol 2005, 17:631-636. 10.1016/j.ceb.2005.09.007, 16226451.
76. Kaiser M, Kuhnl A, Reins J, Fischer S, Ortiz-Tanchez J, Schlee C, Mochmann LH, Heesch S, Benlasfer O, Hofmann WK, et al. Antileukemic activity of the HSP70 inhibitor pifithrin-mu in acute leukemia. Blood Cancer J 2011, 1:e28. 10.1038/bcj.2011.28, 3255249, 22829184.
77. Matz PG, Sundaresan S, Sharp FR, Weinstein PR. Induction of HSP70 in rat brain following subarachnoid hemorrhage produced by endovascular perforation. J Neurosurg 1996, 85:138-145. 10.3171/jns.1996.85.1.0138, 8683263.
78. van den Tweel ER, Peeters-Scholte CM, Van BF, Heijnen CJ, Groenendaal F. Inhibition of nNOS and iNOS following hypoxia-ischemia improves long-term outcome but does not influence the inflammatory response in the neonatal rat brain. Dev Neurosci 2002, 24:389-395. 10.1159/000069044, 12640177.
79. Heck TG, Schaler CM, de Bittencourt PIH. HSP70 expression: does it a novel fatigue signaling factor from immune system to the brain?. Cell Biochem Funct 2011, 29:215-226. 10.1002/cbf.1739, 21374645.
80. Turturici G, Sconzo G, Geraci F. Hsp70 and its molecular role in nervous system diseases. Biochem Res Int 2011, 2011:618127. 3049350, 21403864.
81. Sekihara K, Harashima N, Tongu M, Tamaki Y, Uchida N, Inomata T, Harada M. Pifithrin-mu, an inhibitor of Heat-Shock Protein 70, can increase the antitumor effects of hyperthermia against human prostate cancer cells. PLoS One 2013, 8:e78772. 10.1371/journal.pone.0078772, 3828328, 24244355.
82. Ayer RE, Zhang JH. The clinical significance of acute brain injury in subarachnoid hemorrhage and opportunity for intervention. Acta Neurochir Suppl 2008, 105:179-184. 10.1007/978-3-211-09469-3_35, 19066106.
83. Prunell GF, Svendgaard NA, Alkass K, Mathiesen T. Delayed cell death related to acute cerebral blood flow changes following subarachnoid hemorrhage in the rat brain. J Neurosurg 2005, 102:1046-1054. 10.3171/jns.2005.102.6.1046, 16028764.
84. Yan J, Li L, Khatibi NH, Yang L, Wang K, Zhang W, Martin RD, Han J, Zhang J, Zhou C. Blood-brain barrier disruption following subarachnoid hemorrhage may be facilitated through PUMA induction of endothelial cell apoptosis from the endoplasmic reticulum. Exp Neurol 2011, 230:240-247. 10.1016/j.expneurol.2011.04.022, 21586287.
85. Jing CH, Wang L, Liu PP, Wu C, Ruan D, Chen G. Autophagy activation is associated with neuroprotection against apoptosis via a mitochondrial pathway in a rat model of subarachnoid hemorrhage. Neuroscience 2012, 213:144-153.
86. Wang X, Han W, Du X, Zhu C, Carlsson Y, Mallard C, Jacotot E, Hagberg H. Neuroprotective effect of Bax-inhibiting peptide on neonatal brain injury. Stroke 2010, 41:2050-2055. 10.1161/STROKEAHA.110.589051, 20671246.
87. Zhou C, Yamaguchi M, Kusaka G, Schonholz C, Nanda A, Zhang JH. Caspase inhibitors prevent endothelial apoptosis and cerebral vasospasm in dog model of experimental subarachnoid hemorrhage. J Cereb Blood Flow Metab 2004, 24:419-431. 10.1097/00004647-200404000-00007, 15087711.
88. Iseda K, Ono S, Onoda K, Satoh M, Manabe H, Nishiguchi M, Takahashi K, Tokunaga K, Sugiu K, Date I. Antivasospastic and antiinflammatory effects of caspase inhibitor in experimental subarachnoid hemorrhage. J Neurosurg 2007, 107:128-135. 10.3171/JNS-07/07/0128, 17639882.
89. Park S, Yamaguchi M, Zhou C, Calvert JW, Tang J, Zhang JH. Neurovascular protection reduces early brain injury after subarachnoid hemorrhage. Stroke 2004, 35:2412-2417. 10.1161/01.STR.0000141162.29864.e9, 15322302.
90. Krafft PR, Caner B, Klebe D, Rolland WB, Tang J, Zhang JH. PHA-543613 preserves blood brain barrier integrity after intracerebral hemorrhage in mice. Stroke 2013, 44:1743-1747. 10.1161/STROKEAHA.111.000427, 23613493.
91. Neumar RW. Molecular mechanisms of ischemic neuronal injury. Ann Emerg Med 2000, 36:483-506.
92. Harris HE, Andersson U, Pisetsky DS. HMGB1: a multifunctional alarmin driving autoimmune and inflammatory disease. Nat Rev Rheumatol 2012, 8:195-202. 10.1038/nrrheum.2011.222, 22293756.
93. Kang R, Livesey KM, Zeh HJ, Lotze MT, Tang D. HMGB1 as an autophagy sensor in oxidative stress. Autophagy 2011, 7:904-906. 10.4161/auto.7.8.15704, 21487246.
94. Venereau E, Casalgrandi M, Schiraldi M, Antoine DJ, Cattaneo A, De MF, Liu J, Antonelli A, Preti A, Raeli L, et al. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J Exp Med 2012, 209:1519-1528. 10.1084/jem.20120189, 3428943, 22869893.
95. Murakami K, Koide M, Dumont TM, Russell SR, Tranmer BI, Wellman GC. Subarachnoid hemorrhage induces gliosis and increased expression of the pro-inflammatory cytokine high mobility group box 1 protein. Transl Stroke Res 2011, 2:72-79. 10.1007/s12975-010-0052-2, 3072171, 21479116.
96. Hreggvidsdottir HS, Lundberg AM, Aveberger AC, Klevenvall L, Andersson U, Harris HE. High mobility group box protein 1 (HMGB1)-partner molecule complexes enhance cytokine production by signaling through the partner molecule receptor. Mol Med 2012, 18:224-230. 3320135, 22076468.
97. Edye ME, Lopez-Castejon G, Allan SM, Brough D. Acidosis drives damage-associated molecular pattern (DAMP)-induced interleukin-1 secretion via a caspase-1-independent pathway. J Biol Chem 2013, 288:30485-30494. 10.1074/jbc.M113.478941, 3798512, 24022484.
98. Sun Q, Wang F, Li W, Li W, Hu Y, Li S, Zhu J, Zhou M, Hang C. Glycyrrhizic acid confers neuroprotection after subarachnoid hemorrhage via inhibition of high mobility group box-1 protein: a hypothesis for novel therapy of subarachnoid hemorrhage. Med Hypotheses 2013, 81:268-268. 10.1016/j.mehy.2013.04.032, 23669373.
99. Bialik S, Zalckvar E, Ber Y, Rubinstein AD, Kimchi A. Systems biology analysis of programmed cell death. Trends Biochem Sci 2010, 35:556-564. 10.1016/j.tibs.2010.04.008, 20537543.
100. Lee JY, He Y, Sagher O, Keep R, Hua Y, Xi G. Activated autophagy pathway in experimental subarachnoid hemorrhage. Brain Res 2009, 1287:126-135.
101. Wang Z, Shi XY, Yin J, Zuo G, Zhang J, Chen G. Role of autophagy in early brain injury after experimental subarachnoid hemorrhage. J Mol Neurosci 2012, 46:192-202. 10.1007/s12031-011-9575-6, 21728063.
102. Zhao H, Ji Z, Tang D, Yan C, Zhao W, Gao C. Role of autophagy in early brain injury after subarachnoid hemorrhage in rats. Mol Biol Rep 2013, 40:819-827. 10.1007/s11033-012-2120-z, 23054025.
103. Fayaz S, Suvanish KV, Rajanikant G. Necroptosis: who knew there were so many interesting ways to die?. CNS Neurol Disord Drug Targets 2013, in press.
104. Northington FJ, Chavez-Valdez R, Graham EM, Razdan S, Gauda EB, Martin LJ. Necrostatin decreases oxidative damage, inflammation, and injury after neonatal HI. J Cereb Blood Flow Metab 2011, 31:178-189. 10.1038/jcbfm.2010.72, 3049482, 20571523.
105. Chavez-Valdez R, Martin LJ, Flock DL, Northington FJ. Necrostatin-1 attenuates mitochondrial dysfunction in neurons and astrocytes following neonatal hypoxia-ischemia. Neuroscience 2012, 219:192-203.
106. Wang YQ, Wang L, Zhang MY, Wang T, Bao HJ, Liu WL, Dai DK, Zhang L, Chang P, Dong WW, et al. Necrostatin-1 suppresses autophagy and apoptosis in mice traumatic brain injury model. Neurochem Res 2012, 37:1849-1858. 10.1007/s11064-012-0791-4, 22736198.
107. Chang P, Dong W, Zhang M, Wang Z, Wang Y, Wang T, Gao Y, Meng H, Luo B, Luo C, et al. Anti-necroptosis chemical necrostatin-1 can also suppress apoptotic and autophagic pathway to exert neuroprotective effect in mice intracerebral hemorrhage model. J Mol Neurosci 2013, in press.
108. Wagner EF. AP-1 - Introductory remarks. Oncogene 2001, 20:2334-2335. 10.1038/sj.onc.1204416, 11402330.
109. Chen D, Wei X, Guan J, Yuan J, Peng Y, Song L, Liu Y. Inhibition of c-Jun N-terminal kinase prevents blood brain barrier disruption and normalizes the expression of tight junction proteins clautin-5 and ZO-1 in a rat model of subarachnoid hemorrhage. Acta Neurochir 2012, 154:1469-1476. 10.1007/s00701-012-1328-y, 22661329.
110. Yatsushige H, Yamaguchi M, Zhou C, Calvert JW, Zhang JH. Role of c-Jun N-terminal kinase in cerebral vasospasm after experimental subarachnoid hemorrhage. Stroke 2005, 36:1538-1543. 10.1161/01.STR.0000170713.22011.c8, 15947258.
111. 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, 85:1436-1448. 10.1002/jnr.21281, 17410600.
112. Borsello T, Clarke PGH, Hirt L, Vercelli A, Repici M, Schorderet DF, Bogousslavsky J, Bonny C. A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat Med 2003, 9:1180-1186. 10.1038/nm911, 12937412.
113. Esneault E, Castagne V, Moser P, Bonny C, Bernaudin M. D-JNKi, a peptide inhibitor of c-Jun N-terminal kinase, promotes functional recovery after transient focal cerebral ischemia in rats. Neuroscience 2008, 152:308-320. 10.1016/j.neuroscience.2007.12.036, 18262367.
114. Michel-Monigadon D, Bonny C, Hirt L. c-Jun N-terminal kinase pathway inhibition in intracerebral hemorrhage. Cerebrovasc Dis 2010, 29:564-570. 10.1159/000306643, 20375499.
115. Nijboer CH, van der Kooij MA, van Bel F, Ohl F, Heijnen CJ, Kavelaars A. Inhibition of the JNK/AP-1 pathway reduces neuronal death and improves behavioral outcome after neonatal hypoxic -ischemic brain injury. Brain Behav Immun 2010, 24:812-821. 10.1016/j.bbi.2009.09.008, 19766183.
116. Benakis C, Vaslin A, Pasquali C, Hirt L. Neuroprotection by inhibiting the c-Jun N-terminal kinase pathway after cerebral ischemia occurs independently of interleukin-6 and keratinocyte-derived chemokine (KC/CXCL1) secretion. J Neuroinflammation 2012, 9:76. 10.1186/1742-2094-9-76, 3416579, 22533966.
117. Nijboer CH, Bonestroo HJ, Zijlstra J, Kavelaars A, Heijnen CJ. Mitochondrial JNK phosphorylation as a novel therapeutic target to inhibit neuroinflammation and apoptosis after neonatal ischemic brain damage. Neurobiol Dis 2013, 54:432-444.
118. Park GH, Jeon SJ, Ko HM, Ryu JR, Lee JM, Kim HY, Han SH, Kang YS, Park SH, Shin CY, et al. Activation of microglial cells via protease-activated receptor 2 mediates neuronal cell death in cultured rat primary neuron. Nitric Oxide 2010, 22:18-29. 10.1016/j.niox.2009.10.008, 19887113.
119. Shishodia S, Aggarwal BB. Nuclear factor-kappaB activation: a question of life or death. J Biochem Mol Biol 2002, 35:28-40. 10.5483/BMBRep.2002.35.1.028, 16248967.
120. Aoki T, Kataoka H, Shimamura M, Nakagami H, Wakayama K, Moriwaki T, Ishibashi R, Nozaki K, Morishita R, Hashimoto N. NF-κB is a key mediator of cerebral aneurysm formation. Circulation 2007, 116:2830-2840. 10.1161/CIRCULATIONAHA.107.728303, 18025535.
121. You WC, Wang C, Pan Y, Zhang X, Zhou X, Zhang X, Shi J, Zhou M. Activation of nuclear factor-κB in the brain after experimental subarachnoid hemorrhage and its potential role in delayed brain injury. PLoS One 2013, 8:e60290. 10.1371/journal.pone.0060290, 3607578, 23536907.
122. Nijboer CHA, Heijnen CJ, Groenendaal F, May MJ, van Bel F, Kavelaars A. Strong neuroprotection by inhibition of NF-κB after neonatal hypoxia-ischemia involves apoptotic mechanisms but is independent of cytokines. Stroke 2008, 39:2129-2137. 10.1161/STROKEAHA.107.504175, 18420952.
123. van der Kooij MA, Nijboer CH, Ohl F, Groenendaal F, Heijnen CJ, van Bel F, Kavelaars A. NF-κB inhibition after neonatal cerebral hypoxia-ischemia improves long-term motor and cognitive outcome in rats. Neurobiol Dis 2010, 38:266-272. 10.1016/j.nbd.2010.01.016, 20132887.
124. Suzuki H, Hasegawa Y, Chen W, Kanamaru K, Zhang JH. Recombinant osteopontin in cerebral vasospasm after subarachnoid hemorrhage. Ann Neurol 2010, 68:650-660. 10.1002/ana.22102, 2967465, 21031580.
125. Sodek J, Ganss B, McKee MD. Osteopontin. Crit Rev Oral Biol Med 2000, 11:279-303. 10.1177/10454411000110030101, 11021631.
126. Grasso G, Tomasello F. Erythropoietin for subarachnoid hemorrhage: is there a reason for hope?. World Neurosurg 2012, 77:46-48. 10.1016/j.wneu.2011.01.028, 22079816.
127. Helbok R, Shaker E, Beer R, Chemelli A, Sojer M, Sohm F, Broessner G, Lackner P, Beck M, Zangerle A, et al. High dose erythropoietin increases brain tissue oxygen tension in severe vasospasm after subarachnoid hemorrhage. BMC Neurol 2012, 12:32. 10.1186/1471-2377-12-32, 3502085, 22672319.
128. Turner JD, Mammis A, Prestigiacomo CJ. Erythropoietin for the treatment of subarachnoid hemorrhage: a review. World Neurosurg 2010, 73:500-507. 10.1016/j.wneu.2010.02.026, 20920933.
129. Fan X, Heijnen CJ, van der Kooij MA, Groenendaal F, van Bel F. Beneficial effect of erythropoietin on sensorimotor function and white matter after hypoxia-ischemia in neonatal mice. Pediatr Res 2011, 69:56-61. 10.1203/PDR.0b013e3181fcbef3, 20856165.
130. Gonzalez FF, Larpthaveesarp A, McQuillen P, Derugin N, Wendland M, Spadafora R, Ferriero DM. Erythropoietin increases neurogenesis and oligodendrogliosis of subventricular zone precursor cells after neonatal stroke. Stroke 2013, in press.
131. Juul S. Neuroprotective role of erythropoietin in neonates. J Matern Fetal Neonatal Med 2012, 25:97-99.
132. Xiong T, Qu Y, Mu D, Ferriero D. Erythropoietin for neonatal brain injury: opportunity and challenge. Int J Dev Neurosci 2011, 29:583-591. 10.1016/j.ijdevneu.2010.12.007, 21277366.
133. Celik M, Gakmen N, Erbayraktar S, Akhisaroglu M, Konakc S, Ulukus C, Genc S, Genc K, Sagiroglu E, Cerami A, et al. Erythropoietin prevents motor neuron apoptosis and neurologic disability in experimental spinal cord ischemic injury. Proc Natl Acad Sci 2002, 99:2258-2263. 10.1073/pnas.042693799, 122352, 11854521.
134. Juul SE, Anderson DK, Li Y, Christensen RD. Erythropoietin and erythropoietin receptor in the developing human central nervous system. Pediatr Res 1998, 43:40-49.
135. Siren AL, Fratelli M, Brines M, Goemans C, Casagrande S, Lewczuk P, Keenan S, Gleiter C, Pasquali C, Capobianco A, et al. Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci 2001, 98:4044-4049. 10.1073/pnas.051606598, 31176, 11259643.
136. Villa P, Bigini P, Mennini T, Agnello D, Laragione T, Cagnotto A, Viviani B, Marinovich M, Cerami A, Coleman TR, et al. Erythropoietin selectively attenuates cytokine production and inflammation in cerebral ischemia by targeting neuronal apoptosis. J Exp Med 2003, 198:971-975. 10.1084/jem.20021067, 2194205, 12975460.
137. Wang L, Zhang Z, Wang Y, Zhang R, Chopp M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 2004, 35:1732-1737. 10.1161/01.STR.0000132196.49028.a4, 15178821.
138. Chen G, Zhang S, Shi J, Ai J, Hang C. Effects of recombinant human erythropoietin (rhEPO) on JAK2/STAT3 pathway and endothelial apoptosis in the rabbit basilar artery after subarachnoid hemorrhage. Cytokine 2009, 45:162-168. 10.1016/j.cyto.2008.11.015, 19144539.
139. Grasso G, Buemi M, Alafaci C, Sfacteria A, Passalacqua M, Sturiale A, Calapai G, De Vico G, Piedimonte G, Salpietro FM, et al. Beneficial effects of systemic administration of recombinant human erythropoietin in rabbits subjected to subarachnoid hemorrhage. Proc Natl Acad Sci 2002, 99:5627-5631. 10.1073/pnas.082097299, 122821, 11943864.
140. Zhang ZG, Chopp M. Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic. Lancet Neurol 2009, 8:491-500. 10.1016/S1474-4422(09)70061-4, 2727708, 19375666.
141. Kocsis JD, Honmou O. Chapter 6 - bone marrow stem cells in experimental stroke. Progress in Brain Research 2012, 201:79-98.
142. Scheibe F, Ladhoff J, Huck J, Grohmann M, Blazej K, Oersal A, Baeva N, Seifert M, Priller J. Immune effects of mesenchymal stromal cells in experimental stroke. J Cereb Blood Flow Metab 2012, 32:1578-1588. 10.1038/jcbfm.2012.55, 3421097, 22549620.
143. Wakabayashi K, Nagai A, Sheikh AM, Shiota Y, Narantuya D, Watanabe T, Masuda J, Kobayashi S, Kim SU, Yamaguchi S. Transplantation of human mesenchymal stem cells promotes functional improvement and increased expression of neurotrophic factors in a rat focal cerebral ischemia model. J Neurosci Res 2010, 88:1017-1025.
144. Donega V, van Velthoven CT, Nijboer CH, Kavelaars A, Heijnen CJ. The endogenous regenerative capacity of the damaged newborn brain: boosting neurogenesis with mesenchymal stem cell treatment. J Cereb Blood Flow Metab 2013, 33:625-634. 10.1038/jcbfm.2013.3, 23403379.
145. Onda T, Honmou O, Harada K, Houkin K, Hamada H, Kocsis JD. Therapeutic benefits by human mesenchymal stem cells (hMSCs) and Ang-1 gene-modified hMSCs after cerebral ischemia. J Cereb Blood Flow Metab 2007, 28:329-340. 2605394, 17637706.
146. van Velthoven CTJ, Kavelaars A, van Bel F, Heijnen CJ. Repeated mesenchymal stem cell treatment after neonatal hypoxia-ischemia has distinct effects on formation and maturation of new neurons and oligodendrocytes leading to restoration of damage, corticospinal motor tract activity, and sensorimotor function. J Neurosci 2010, 30:9603-9611. 10.1523/JNEUROSCI.1835-10.2010, 20631189.
147. Donega V, Van Velthoven CT, Nijboer CH, Van BF, Kas MJ, Kavelaars A, Heijnen CJ. Intranasal mesenchymal stem cell treatment for neonatal brain damage: long-term cognitive and sensorimotor improvement. PLoS One 2013, 8:e51253. 10.1371/journal.pone.0051253, 3536775, 23300948.
148. Khalili MA, Anvari M, Hekmati-Moghadam SH, Sadeghian-Nodoushan F, Fesahat F, Miresmaeili SM. Therapeutic benefit of intravenous transplantation of mesenchymal stem cells after experimental subarachnoid hemorrhage in rats. J Stroke Cerebrovasc Dis 2012, 21:445-451. 10.1016/j.jstrokecerebrovasdis.2010.10.005, 21282068.
149. Keohane A, Ryan S, Maloney E, Sullivan AM, Nolan YM. Tumor necrosis factor-α impairs neuronal differentiation but not proliferation of hippocampal neural precursor cells: role of Hes1. Mol Cell Neurosci 2010, 43:127-135. 10.1016/j.mcn.2009.10.003, 19840854.
150. Turbic A, Leong SY, Turnley AM. Chemokines and inflammatory mediators interact to regulate adult murine neural precursor cell proliferation, survival and differentiation. PLoS One 2011, 6:e25406. 10.1371/journal.pone.0025406, 3179517, 21966521.