Late cerebral ischaemia after subarachnoid haemorrhage: Is cerebrovascular receptor upregulation the mechanism behind?

Acta Physiologica

Volumn 203, Issue 1, 2011, Pages 209-224

  Edvinsson, L ^a,b   Povlsen, G K ^b  

^a LUND UNIVERSITY   (Sweden)

^b GLOSTRUP UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Blood brain barrier; Endothelin; Inflammation; Signal transduction; Subarachnoid haemorrhage; Vasoconstrictor receptors

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; CLASOZENTAN; ENDOTHELIN 1; ENDOTHELIN RECEPTOR; ENDOTHELIN RECEPTOR ANTAGONIST; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; NIMODIPINE; SEROTONIN; SEROTONIN RECEPTOR; THROMBOXANE A2; THROMBOXANE A2 RECEPTOR; UNCLASSIFIED DRUG;

BLOOD BRAIN BARRIER; BRAIN ARTERY; BRAIN BLOOD FLOW; BRAIN FUNCTION; BRAIN ISCHEMIA; DISEASE ASSOCIATION; DRUG MEGADOSE; DRUG TARGETING; HUMAN; INFLAMMATION; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE; SMOOTH MUSCLE FIBER; SUBARACHNOID HEMORRHAGE;

ANIMALS; BRAIN ISCHEMIA; CEREBROVASCULAR CIRCULATION; HUMANS; RECEPTORS, ENDOTHELIN; SIGNAL TRANSDUCTION; SUBARACHNOID HEMORRHAGE; UP-REGULATION; VASOCONSTRICTION;

EID: 80051672374     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2010.02227.x     Document Type: Review

References (120)

1. Adner, M., Cantera, L., Ehlert, F., Nilsson, L. & Edvinsson, L. 1996. Plasticity of contractile endothelin-B receptors in human arteries after organ culture. Br J Pharmacol 119, 1159-1166.
2. Adner, M., Geary, G.G. & Edvinsson, L. 1998. Appearance of contractile endothelin-B receptors in rat mesenteric arterial segments following organ culture. Acta Physiol Scand 163, 121-129.
3. Adner, M., Shankley, N. & Edvinsson, L. 2001. Evidence that ET-1, but not ET-3 and S6b, ET(A)-receptor mediated contractions in isolated rat mesenteric arteries are modulated by co-activation of ET(B) receptors. Br J Pharmacol 133, 927-935.
4. Aihara, Y., Kasuya, H., Onda, H., Hori, T., Takeda, J. & Faraci, F.M. 2001. Quantitative analysis of gene expressions related to inflammation in canine spastic artery after subarachnoid hemorrhage editorial comment. Stroke 32, 212-217.
5. Ansar, S. & Edvinsson, L. 2008. Subtype activation and interaction of protein kinase C and mitogen-activated protein kinase controlling receptor expression in cerebral arteries and microvessels after subarachnoid hemorrhage. Stroke 39, 185-190.
6. Ansar, S. & Edvinsson, L. 2009. Equal contribution of increased intracranial pressure and subarachnoid blood to cerebral blood flow reduction and receptor upregulation after subarachnoid hemorrhage. J Neurosurg 111, 978-987.
7. Ansar, S., Vikman, P., Nielsen, M. & Edvinsson, L. 2008. Cerebrovascular ETB, 5-HT1B and AT1 receptor upregulation correlates with reduction in regional CBF after subarachnoid hemorrhage. Am J Physiol Heart Circ Physiol 294, H3750-H3758.
8. Ansar, S., Larsen, C., Maddahi, A. & Edvinsson, L. 2010. Subarachnoid hemorrhage induces enhanced expression of thromboxane A2 receptors in rat cerebral arteries. Brain Res 1316, 163-172.
9. Asahi, M., Asahi, K., Jung, J.C., del Zoppo, G.J., Fini, M.E. & Lo, E.H. 2000. Role for matrix metalloproteinase 9 after focal cerebral ischemia: effects of gene knockout and enzyme inhibition with BB-94. J Cereb Blood Flow Metab 20, 1681-1689.
10. Asahi, M., Wang, X., Mori, T., Sumii, T., Jung, J.C., Moskowitz, M.A., Fini, M.E. & Lo, E.H. 2001. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 21, 7724-7732.
11. Baker, A.H., Edwards, D.R. & Murphy, G. 2002. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci 115, 3719-3727.
12. Beg, S.A., Hansen-Schwartz, J.A., Vikman, P.J., Xu, C.B. & Edvinsson, L.I. 2006. ERK1/2 inhibition attenuates cerebral blood flow reduction and abolishes ET(B) and 5-HT(1B) receptor upregulation after subarachnoid hemorrhage in rat. J Cereb Blood Flow Metab 26, 846-856.
13. Beg, S., Hansen.-Schwartz, J.A., Vikman, P., Xu, C.B. & Edvinsson, L. 2007. Protein kinase C inhibition prevents upregulation of vascular ET(B) and 5-HT(1B) receptors and reverses cerebral blood flow reduction after subarachnoid hemorrhage in rats. J Cereb Blood Flow Metab 27, 21-32.
14. Brawley, B.W., Strandness, D.E. Jr & Kelly, W.A. 1968. The biphasic response of cerebral vasospasm in experimental subarachnoid hemorrhage. J Neurosurg 28, 1-8.
15. Candelario-Jalil, E., Yang, Y. & Rosenberg, G.A. 2009. Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia. Neuroscience 158, 983-994.
16. Claassen, J., Carhuapoma, J.R., Kreiter, K.T., Du, E.Y., Connolly, E.S. & Mayer, S.A. 2002. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke 33, 1225-1232.
17. Cockerham, C., Webb, M.L., Hedberg, S.A. & Runge, M.S. 1991. Regulation of the rat aortic smooth muscle cell thromboxane A2 receptor. Trans Assoc Am Physicians 104, 173-180.
18. Coyle, A.T., Miggin, S.M. & Kinsella, B.T. 2002. Characterization of the 5' untranslated region of α and β isoforms of the human thromboxane A2 receptor (TP). Eur J Biochem 269, 4058-4073.
19. Cuadrado, E., Rosell, A., Penalba, A., Slevin, M., Alvarez-SabiÌn, J., Ortega-Aznar, A. & Montaner, J. 2009. Vascular MMP-9/TIMP-2 and neuronal MMP-10 up-regulation in human brain after stroke: a combined laser microdissection and protein array study. J Proteome Res 8, 3191-3197.
20. Cunningham, L.A., Wetzel, M. & Rosenberg, G.A. 2005. Multiple roles for MMPs and TIMPs in cerebral ischemia. Glia 50, 329-339.
21. Davis, R.P., Zappulla, R.A., Spigelman, M.K., Feuer, E.J., Malis, L.I. & Holland, J.F. 1986. The protective effect of experimental subarachnoid haemorrhage on sodium dehydrocholate-induced blood-brain barrier disruption. Acta Neurochir (Wien) 83, 138-143.
22. Delgado, T.J., Brismar, J. & Svendgaard, N.A. 1985. Subarachnoid haemorrhage in the rat: angiography and fluorescence microscopy of the major cerebral arteries. Stroke 16, 595-602.
23. Doczi, T. 1985. The pathogenetic and prognostic significance of blood-brain barrier damage at the acute stage of aneurysmal subarachnoid haemorrhage. Clinical and experimental studies. Acta Neurochir (Wien) 77, 110-132.
24. Doczi, T., Joo, F., Adam, G., Bozoky, B. & Szerdahelyi, P. 1986. Blood-brain barrier damage during the acute stage of subarachnoid hemorrhage, as exemplified by a new animal model. Neurosurgery 18, 733-739.
25. Dorhout Mees, S.M., Rinkel, G.J., Feigin, V.L., Algra, A., van den Bergh, W.M., Vermeulen, M. & van Gijn, J. 2007. Calcium antagonists for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev 18, CD000277.
26. Dumont, A., Dumont, R., Chow, M., Lin, C., Calisaneller, T., Ley, K., Kassell, N. & Lee, K. 2003. Cerebral vasospasm after subarachnoid hemorrhage: putative role of inflammation. Neurosurgery 53, 123-135.
27. Ecker, A. & Riemenschneider, P.A. 1951. Arteriographic demonstration of spasm of the intracranial arteries, with special reference to saccular arterial aneurysms. J Neurosurg 8, 660-667.
28. Edvinsson, L., Nilsson, E. & Jansen-Olesen, I. 2007. Inhibitory effect of BIBN4096BS, CGRP(8-37), a CGRP antibody and an RNA-Spiegelmer on CGRP induced vasodilatation in the perfused and non-perfused rat middle cerebral artery. Br J Pharmacol 150, 633-640.
29. Engelhorn, T., Goerike, S., Doerfler, A., Okorn, C., Forsting, M., Heusch, G. & Schulz, R. 2004. The angiotensin II type 1-receptor blocker candesartan increases cerebral blood flow, reduces infarct size, and improves neurologic outcome after transient cerebral ischemia in rats. J Cereb Blood Flow Metab 24, 467-474.
30. Fassbender, K., Hodapp, B., Rossol, S., Bertsch, T., Schmeck, J., Schutt, S., Fritzinger, M., Horn, P., Vajkoczy, P., Wendel-Wellner, M. et al. 2000. Endothelin-1 in subarachnoid hemorrhage: an acute-phase reactant produced by cerebrospinal fluid leukocytes. Stroke 31, 2971-2975.
31. Fassbender, K., Hodapp, B., Rossol, S., Bertsch, T., Schmeck, J., Schutt, S., Fritzinger, M., Horn, P., Vajkoczy, P., Kreisel, S., Brunner, J., Schmiedek, P. & Hennerici, M. 2001. Inflammatory cytokines in subarachnoid haemorrhage: association with abnormal blood flow velocities in basal cerebral arteries. J Neurol Neurosurg Psychiatry 70, 534-537.
32. Fornezza, U., Carraro, R., Demo, P., Zamperetti, N., Volpin, L., Landi, A., De Luca, G.P. & Benedetti, A. 1990. The transcranial Doppler ultrasonography in the evaluation of vasospasm and of intracranial hypertension after subarachnoid hemorrhage. Agressologie 31, 259-261.
33. Forster, C., Whalley, E.T., Mohan, J. & Dutton, J. 1980. Vascular smooth muscle response to fibrinogen degradation products and 5-hydroxytryptamine: possible role in cerebral vasospasm in man. Br J Clin Pharmacol 10, 231-236.
34. Gaetani, P., Tartara, F., Pignatti, P., Tancioni, F., Rodriguez y Baena, R. & De Benedetti, F. 1998. Cisternal CSF levels of cytokines after subarachnoid hemorrhage. Neurol Res 20, 337-342.
35. Gallia, G.L. & Tamargo, R.J. 2006. Leukocyte-endothelial cell interactions in chronic vasospasm after subarachnoid hemorrhage. Neurol Res 28, 750-758.
36. Germano, A., d'Avella, D., Cicciarello, R., Hayes, R.L. & Tomasello, F. 1992. Blood-brain barrier permeability changes after experimental subarachnoid hemorrhage. Neurosurgery 30, 882-886.
37. van Gijn, J., Kerr, R.S. & Rinkel, G.J. 2007. Subarachnoid haemorrhage. Lancet 369, 306-318.
38. Guo, Z., Sun, X., He, Z., Jiang, Y., Zhang, X. & Zhang, J.H. 2010. Matrix metalloproteinase-9 potentiates early brain injury after subarachnoid hemorrhage. Neurol Res 2, 715-720.
39. Hamann, G.F., Okada, Y., Fitridge, R. & del Zoppo, G.J. 1995. Microvascular basal lamina antigens disappear during cerebral ischemia and reperfusion. Stroke 26, 2120-2126.
40. Hamann, G.F., Okada, Y. & del Zoppo, G.J. 1996. Hemorrhagic transformation and microvascular integrity during focal cerebral ischemia/reperfusion. J Cereb Blood Flow Metab 16, 1373-1378.
41. Handa, Y., Kabuto, M., Kobayashi, H., Kawano, H., Takeuchi, H. & Hayashi, M. 1991. The correlation between immunological reaction in the arterial wall and the time course of the development of cerebral vasospasm in a primate model. Neurosurgery 28, 542-549.
42. Handa, Y., Kubota, T., Kaneko, M., Tsuchida, A., Kobayashi, H. & Kawano, H. 1995. Expression of intercellular adhesion molecule 1 (ICAM-1) on the cerebral artery following subarachnoid haemorrhage in rats. Acta Neurochir (Wien) 132, 92-97.
43. Hansen-Schwartz, J. 2004. Cerebral vasospasm. Neurocrit Care 1, 235-246.
44. Hansen-Schwartz, J. & Edvinsson, L. 2000. Increased sensitivity to ET-1 in rat cerebral arteries following organ culture. Neuroreport 11, 649-652.
45. Hansen-Schwartz, J., Nordstrom, C.H. & Edvinsson, L. 2002a. Human endothelin subtype A receptor enhancement during tissue culture via de novo transcription. Neurosurgery 50, 127-133 discussion 133-5.
46. Hansen-Schwartz, J., Svensson, C.L., Xu, C.B. & Edvinsson, L. 2002b. Protein kinase mediated upregulation of endothelin A, endothelin B and 5-hydroxytryptamine 1B/1D receptors during organ culture in rat basilar artery. Br J Pharmacol 137, 118-126.
47. Hansen-Schwartz, J., Hoel, N.L., Xu, C.B., Svendgaard, N.A. & Edvinsson, L. 2003a. Subarachnoid hemorrhage-induced upregulation of the 5-HT1B receptor in cerebral arteries in rats. J Neurosurg 99, 115-120.
48. Hansen-Schwartz, J., Hoel, N.L., Zhou, M., Xu, C.B., Svendgaard, N.A. & Edvinsson, L. 2003b. Subarachnoid hemorrhage enhances endothelin receptor expression and function in rat cerebral arteries. Neurosurgery 52, 1188-1194.
49. Harkness, K.A., Adamson, P., Sussman, J.D., Davies-Jones, G.A., Greenwood, J. & Woodroofe, M.N. 2000. Dexamethasone regulation of matrix metalloproteinase expression in CNS vascular endothelium. Brain 123, 698-709.
50. Hayashi, M., Marukawa, S., Fujii, H., Kitano, T., Kobayashi, H. & Yamamoto, S. 1977. Intracranial hypertension in patients with ruptured intracranial aneurysm. J Neurosurg 46, 584-590.
51. Henriksson, M., Stenman, E. & Edvinsson, L. 2003. Intracellular pathways involved in upregulation of vascular endothelin type B receptors in cerebral arteries of the rat. Stroke 34, 1479-1483.
52. Henriksson, M., Xu, C.B. & Edvinsson, L. 2004. Importance of ERK1/2 in upregulation of endothelin type B receptors in cerebral arteries. Br J Pharmacol 142, 1155-1161.
53. Henriksson, M., Vikman, P., Stenman, E., Beg, S. & Edvinsson, L. 2006. Inhibition of PKC activity blocks the increase of ETB receptor expression in cerebral arteries. BMC Pharmacol 6, 13.
54. Hirashima, Y., Nakamura, S., Endo, S., Kuwayama, N., Naruse, Y. & Takaku, A. 1997. Elevation of platelet activating factor, inflammatory cytokines, and coagulation factors in the internal jugular vein of patients with subarachnoid hemorrhage. Neurochem Res 22, 1249-1255.
55. Hoel, N.L., Hansen-Schwartz, J. & Edvinsson, L. 2001. Selective up-regulation of 5-HT(1B/1D) receptors during organ culture of cerebral arteries. Neuroreport 12, 1605-1608.
56. Honda, Y., Minato, H., Fujitani, B., Masuda, Y. & Hosoki, K. 1997. Alacepril, an angiotensin-converting enzyme inhibitor, prevents cerebral vasospasm in subarachnoid hemorrhage model in rats. Methods Find Exp Clin Pharmacol 19, 699-706.
57. Honma, Y., Clower, B.R., Haining, J.L. & Smith, R.R. 1989. Comparison of intimal platelet accumulation in cerebral arteries in two experimental models of subarachnoid hemorrhage. Neurosurgery 24, 487-490.
58. Huang, J.-S., Ramamurthy, S.K., Lin, X. & Le Breton, G.C. 2004. Cell signalling through thromboxane A2 receptors. Cell Signal 16, 521-533.
59. Hughes, J.T. & Schianchi, P.M. 1978. Cerebral artery spasm. A histological study at necropsy of the blood vessels in cases of subarachnoid hemorrhage. J Neurosurg 48, 515-525.
60. Iadecola, C., Zhang, F. & Xu, X. 1995. Inhibition of inducible nitric oxide synthase ameliorates cerebral ischemic damage. Am J Physiol Regul Integr Comp Physiol 268, R286-R292.
61. Irving, E.A. & Bamford, M. 2002. Role of mitogen- and stress-activated kinases in ischemic injury. J Cereb Blood Flow Metab 22, 631-647.
62. Josko, J., Gwozdz, B., Hendryk, S., Jedrzejowska-Szypulka, H., Slowinski, J. & Jochem, J. 2001. Expression of vascular endothelial growth factor (VEGF) in rat brain after subarachnoid haemorrhage and endothelin receptor blockage with BQ-123. Folia Neuropathol 39, 243-251.
63. Kaminska, B. 2005. MAPK signalling pathways as molecular targets for anti-inflammatory therapy - from molecular mechanisms to therapeutic benefits. Biochim Biophys Acta 1754, 253-262.
64. Kaneko, Y., Nakayama, T., Saito, K., Morita, A., Sato, I., Maruyama, A., Soma, M., Takahashi, T. & Sato, N. 2006. Relationship between the thromboxane A2 receptor gene and susceptibility to cerebral infarction. Hypertens Res 29, 665-671.
65. Kasuya, H. & Shimizu, T. 1989. Activated complement components C3a and C4a in cerebrospinal fluid and plasma following subarachnoid hemorrhage. J Neurosurg 71, 741-746.
66. Kikuchi, T., Okuda, Y., Kaito, N. & Abe, T. 1995. Cytokine production in cerebrospinal fluid after subarachnoid haemorrhage. Neurol Res 17, 106-108.
67. Komitova, M., Zhao, L.R., Gidö, G., Johansson, B.B. & Eriksson, P. 2005. Postischemic exercise attenuates whereas enriched environment has certain enhancing effects on lesion-induced subventricular zone activation in the adult rat. Eur J Neurosci 21, 2397-2405.
68. van Kooten, F., Ciabattoni, G., Koudstaal, P.J., Grobbee, D.E., Kluft, C. & Patrono, C. 1999. Increased thromboxane biosynthesis is associated with poststroke dementia. Stroke 30, 1542-1547.
69. Koudstaal, P., Ciabattoni, G., van Gijn, J., Nieuwenhuis, H., de Groot, P., Sixma, J. & Patrono, C. 1993. Increased thromboxane biosynthesis in patients with acute cerebral ischemia. Stroke 24, 219-223.
70. Kusaka, G., Ishikawa, M., Nanda, A., Granger, D.N. & Zhang, J.H. 2004. Signaling pathways for early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab 24, 916-925.
71. 1B receptor upregulation after subarachnoid hemorrhage in the rat. J Neurosurg: DOI.
72. Lye, R.H., Paul, K.S., Forster, C.M., Whalley, E.T. & Dutton, J. 1982. Effect of fibrin-fibrinogen degradation products on human basilar artery preparations. J Neurosurg 56, 339-343.
73. Macdonald, R.L. & Weir, B.K. 1994. Cerebral vasospasm and free radicals. Free Radic Biol Med 16, 633-643.
74. Macdonald, R.L., Kassell, N.F., Mayer, S., Ruefenacht, D., Schmiedek, P., Weidauer, S., Frey, A., Roux, S., Pasqualin, A. & on behalf of the CONSCIOUS-1 Investigators. 2008. Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke 39, 3015-3021.
75. Mack, W.J., Mocco, J., Hoh, D.J., Huang, J., Choudhri, T.F., Kreiter, K.T., Lozier, A., Opperman, M., Poisik, A., Yorgason, J., Solomon, R.A., Mayer, S.A. & Connolly, E.S. 2002. Outcome prediction with serum intercellular adhesion molecule-1 levels after aneurysmal subarachnoid hemorrhage. J Neurosurg 96, 71-75.
76. Maddahi, A., Ansar, S., Chen, Q. & Edvinsson, L. 2010. 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: DOI.
77. Mathiesen, T., Andersson, B., Loftenius, A. & von Holst, H. 1993. Increased interleukin-6 levels in cerebrospinal fluid following subarachnoid hemorrhage. J Neurosurg 78, 562-567.
78. Mathiesen, T., Edner, G., Ulfarsson, E. & Andersson, B. 1997. Cerebrospinal fluid interleukin-1 receptor antagonist and tumor necrosis factor-alpha following subarachnoid hemorrhage. J Neurosurg 87, 215-220.
79. Mattiasson, G.J., Philips, M.F., Tomasevic, G., Johansson, B.B., Wieloch, T. & McIntosh, T.K. 2000. The rotating pole test: evaluation of its effectiveness in assessing functional motor deficits following experimental head injury in the rat. J Neurosci Methods 95, 75-82.
80. Mayhan, W.G. 1999. VEGF increases permeability of the blood-brain barrier via a nitric oxide synthase/cGMP-dependent pathway. Am J Physiol 276, C1148-C1153.
81. McGirt, M.J., Lynch, J.R., Blessing, R., Warner, D.S., Friedman, A.H. & Laskowitz, D.T. 2002. Serum von Willebrand factor, matrix metalloproteinase-9, and vascular endothelial growth factor levels predict the onset of cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurgery 51, 1128-1135.
82. Mendelow, A.D. 1988. Pathophysiology of delayed ischaemic dysfunction after subarachnoid haemorrhage: experimental and clinical data. Acta Neurochir Suppl (Wien) 45, 7-10.
83. Mickley, E.J., Gray, G.A. & Webb, D.J. 1997. Activation of endothelin ETA receptors masks the constrictor role of endothelin ETB receptors in rat isolated small mesenteric arteries. Br J Pharmacol 120, 1376-1382.
84. Montaner, J., Alvarez-Sabin, J., Molina, C., Angles, A., Abilleira, S., Arenillas, J., Gonzalez, M.A. & Monasterio, J. 2001a. Matrix metalloproteinase expression after human cardioembolic stroke: temporal profile and relation to neurological impairment. Stroke 32, 1759-1766.
85. Montaner, J., Alvarez-Sabin, J., Molina, C.A., Angles, A., Abilleira, S., Arenillas, J. & Monasterio, J. 2001b. Matrix metalloproteinase expression is related to hemorrhagic transformation after cardioembolic stroke. Stroke 32, 2762-2767.
86. Neil-Dwyer, G. & Cruickshank, J. 1974. The blood leucocyte count and its prognostic significance in subarachnoid haemorrhage. Brain 97, 79-86.
87. Nilsson, T., Cantera, L., Adner, M. & Edvinsson, L. 1997. Presence of contractile endothelin-A and dilatory endothelin-B receptors in human cerebral arteries. Neurosurgery 40, 346-351 discussion 351-3.
88. Nishizawa, S. & Laher, I. 2005. Signaling mechanisms in cerebral vasospasm. Trends Cardiovasc Med 15, 24-34.
89. Nissen, J.J., Mantle, D., Gregson, B. & Mendelow, A.D. 2001. Serum concentration of adhesion molecules in patients with delayed ischaemic neurological deficit after aneurysmal subarachnoid haemorrhage: the immunoglobulin and selectin superfamilies. J Neurol Neurosurg Psychiatry 71, 329-333.
90. Osaka, K. 1977. Prolonged vasospasm produced by the breakdown products of erythrocytes. J Neurosurg 47, 403-411.
91. Osuka, K., Suzuki, Y., Tanazawa, T., Hattori, K., Yamamoto, N., Takayasu, M., Shibuya, M. & Yoshida, J. 1998. Interleukin-6 and development of vasospasm after subarachnoid haemorrhage. Acta Neurochir 140, 943-951.
92. Peterson, J.W., Kwun, B.-D., Hackett, J.D. & Zervas, N.T. 1990. The role of inflammation in experimental cerebral vasospasm. J Neurosurg 72, 767-774.
93. Pickard, J.D., Walker, V., Brandt, L., Zygmunt, S. & Smythe, J. 1994. Effect of intraventricular haemorrhage and rebleeding following subarachnoid haemorrhage on CSF eicosanoids. Acta Neurochir (Wien) 129, 152-157.
94. Prunell, G.F., Mathiesen, T. & Svendgaard, N.A. 2002. A new experimental model in rats for study of the pathophysiology of subarachnoid hemorrhage. Neuroreport 13, 2553-2556.
95. Radomski, M. 1985. The biological role of thromboxane A2 in the process of hemostasis and thrombosis; pharmacology and perspectives of therapeutical use of thromboxane synthetase inhibitors and receptor PGH2/TXA2 antagonists. Acta Physiol Pol 36, 153-164.
96. Raja, P.V., Huang, J., Germanwala, A.V., Gailloud, P., Murphy, K.P. & Tamargo, R.J. 2008. Microsurgical clipping and endovascular coiling of intracranial aneurysms: a critical review of the literature. Neurosurgery 62, 1187-1202 discussion 1202-3.
97. Ries, S., Schminke, U., Fassbender, K., Daffertshofer, M., Steinke, W. & Hennerici, M. 1996. Cerebrovascular involvement in the acute phase of bacterial meningitis. J Neurol 244, 51-55.
98. Rosell, A., Ortega-Aznar, A., Alvarez-Sabin, J., Fernandez-Cadenas, I., Ribo, M., Molina, C.A., Lo, E.H. & Montaner, J. 2006. Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke 37, 1399-1406.
99. Rosenberg, G.A. 2002. Matrix metalloproteinases in neuroinflammation. Glia 39, 279-291.
100. Rousseaux, P., Scherpereel, B., Bernard, M.H., Graftieaux, J.P. & Guyot, J.F. 1980. Fever and cerebral vasospasm in ruptured intracranial aneurysms. Surg Neurol 14, 459-465.
101. Saavedra, J.M., Benicky, J. & Zhou, J. 2006. Mechanisms of the anti-ischemic effect of angiotensin II AT(1) receptor antagonists in the brain. Cell Mol Neurobiol 26, 1099-1111.
102. Saloheimo, P., Juvela, S., Riutta, A., Pyhtinen, J. & Hillbom, M. 2005. Thromboxane and prostacyclin biosynthesis in patients with acute spontaneous intracerebral hemorrhage. Thromb Res 115, 367-373.
103. Sasaki, T., Wakai, S., Asano, T., Takakura, K. & Sano, K. 1982. Prevention of cerebral vasospasm after SAH with a thromboxane synthetase inhibitor, OKY-1581. J Neurosurg 57, 74-82.
104. Sayama, C.M., Liu, J.K. & Couldwell, W.T. 2006. Update on endovascular therapies for cerebral vasospasm induced by aneurysmal subarachnoid hemorrhage. Neurosurg Focus 21, E12.
105. Schrader, J., Luders, S., Kulschewski, A., Berger, J., Zidek, W., Treib, J., Einhaupl, K., Diener, H.C. & Dominiak, P. 2003. The ACCESS study: evaluation of acute candesartan cilexetil therapy in stroke survivors. Stroke 34, 1699-1703.
106. Schubert, G.A., Schilling, L. & Thome, C. 2008. Clazosentan, an endothelin receptor antagonist, prevents early hypoperfusion during the acute phase of massive experimental subarachnoid hemorrhage: a laser Doppler flowmetry study in rats. J Neurosurg 109, 1134-1140.
107. Shigeno, T., Fritschka, E., Brock, M., Schramm, J., Shigeno, S. & Cervos-Navarro, J. 1982. Cerebral edema following experimental subarachnoid hemorrhage. Stroke 13, 368-379.
108. Sills, A.K. Jr, Clatterbuck, R.E., Thompson, R.C., Cohen, P.L. & Tamargo, R.J. 1997. Endothelial cell expression of intercellular adhesion molecule 1 in experimental posthemorrhagic vasospasm. Neurosurgery 41, 453-460 discussion 460-1.
109. Suzuki, S., Kimura, M., Souma, M., Ohkima, H., Shimizu, T. & Iwabuchi, T. 1990. Cerebral microthrombosis in symptomatic cerebral vasospasm - a quantitative histological study in autopsy cases. Neurol Med Chir (Tokyo) 30, 309-316.
110. Szok, D., Hansen-Schwartz, J. & Edvinsson, L. 2001. In depth pharmacological characterization of endothelin B receptors in the rat middle cerebral artery. Neurosci Lett 314, 69-72.
111. Takizawa, T., Tada, T., Kitazawa, K., Tanaka, Y., Hongo, K., Kameko, M. & Uemura, K.I. 2001. Inflammatory cytokine cascade released by leukocytes in cerebrospinal fluid after subarachnoid hemorrhage. Neurol Res 23, 724-730.
112. Torner, J.C., Kassell, N.F. & Haley, E.C. Jr 1990. The timing of surgery and vasospasm. Neurosurg Clin N Am 1, 335-347.
113. Vajkoczy, P., Meyer, B., Weidauer, S., Raabe, A., Thome, C., Ringel, F., Breu, V. & Schmiedek, P. 2005. Clazosentan (AXV-034343), a selective endothelin A receptor antagonist, in the prevention of cerebral vasospasm following severe aneurysmal subarachnoid hemorrhage: results of a randomized, double-blind, placebo-controlled, multicenter Phase IIa study. J Neurosurg 103, 9-17.
114. Vatter, H., Konczalla, J., Weidauer, S., Preibisch, C., Raabe, A., Zimmermann, M. & Seifert, V. 2007a. Characterization of the endothelin-B receptor expression and vasomotor function during experimental cerebral vasospasm. Neurosurgery 60, 1100-1108 discussion 1108-9.
115. Vatter, H., Konczalla, J., Weidauer, S., Preibisch, C., Zimmermann, M., Raabe, A. & Seifert, V. 2007b. Effect of delayed cerebral vasospasm on cerebrovascular endothelin A receptor expression and function. J Neurosurg 107, 121-127.
116. Vikman, P., Beg, S., Khurana, T.S., Hansen-Schwartz, J. & Edvinsson, L. 2006. Gene expression and molecular changes in cerebral arteries following subarachnoid hemorrhage in the rat. J Neurosurg 105, 438-444.
117. Vollrath, B.A., Weir, B.K., Macdonald, R.L. & Cook, D.A. 1994. Intracellular mechanisms involved in the responses of cerebrovascular smooth-muscle cells to hemoglobin. J Neurosurg 80, 261-268.
118. Wilkins, R.H. 1990. Cerebral vasospasm. Crit Rev Neurobiol 6, 51-77.
119. Yang, Y., Estrada, E.Y., Thompson, J.F., Liu, W. & Rosenberg, G.A. 2007. Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J Cereb Blood Flow Metab 27, 697-709.
120. Zubkov, A.Y., Nanda, A. & Zhang, J.H. 2003. Signal transduction pathways in cerebral vasospasm. Pathophysiology 9, 47-61.