Targeted over-expression of endothelin-1 in astrocytes leads to more severe brain damage and vasospasm after subarachnoid hemorrhage

BMC Neuroscience

Volumn 14, Issue , 2013, Pages

  Yeung, Patrick K K ^a   Shen, Jiangang ^b   Chung, Stephen S M ^d   Chung, Sookja K ^a,c  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b THE UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d BNU HKBU UNITED INTERNATIONAL COLLEGE   (China)

Author keywords

Astrocytes; Brain edema; Endothelium; Subarachnoid hemorrhage; Vasospasm

Indexed keywords

ATRASENTAN; CALCIUM ACTIVATED POTASSIUM CHANNEL; ENDOTHELIN 1; GLIAL FIBRILLARY ACIDIC PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PROTEIN KINASE C ALPHA; RELCOVAPTAN; VASOPRESSIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY CONSTRICTION; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BLOOD VESSEL DIAMETER; BRAIN BLOOD FLOW; BRAIN DAMAGE; BRAIN EDEMA; BRAIN PERFUSION; BRAIN VASOSPASM; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; IMMUNOCYTOCHEMISTRY; LASER DOPPLER FLOWMETRY; MIDDLE CEREBRAL ARTERY OCCLUSION; MORTALITY; MOUSE; NEUROLOGIC DISEASE; NEUROPATHOLOGY; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN TARGETING; SUBARACHNOID HEMORRHAGE; SURVIVAL RATE; TRANSGENIC MOUSE; UPREGULATION; WATER CONTENT;

ANIMALS; ASTROCYTES; DISEASE MODELS, ANIMAL; ENDOTHELIN-1; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; RECEPTOR, ENDOTHELIN A; SUBARACHNOID HEMORRHAGE; UP-REGULATION; VASOSPASM, INTRACRANIAL;

EID: 84886160406     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-14-131     Document Type: Article

References (79)

1. Claassen J, Carhuapoma JR, Kreiter KT, Du EY, Connolly ES, Mayer SA. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke 2002, 33(5):1225-1232. 10.1161/01.STR.0000015624.29071.1F, 11988595.
2. Macdonald RL. Pathophysiology and molecular genetics of vasospasm. Acta Neurochir Suppl 2001, 77:7-11.
3. Molnar AH, Varga C, Berko A, Rojik I, Parducz A, Laszlo F, Laszlo FA. Inhibitory effect of vasopressin receptor antagonist OPC-31260 on experimental brain oedema induced by global cerebral ischaemia. Acta Neurochir (Wien) 2008, 150(3):265-271. 10.1007/s00701-007-1400-1, 18288441.
4. Liu X, Nakayama S, Amiry-Moghaddam M, Ottersen OP, Bhardwaj A. Arginine-vasopressin V1 but not V2 receptor antagonism modulates infarct volume, brain water content, and aquaporin-4 expression following experimental stroke. Neurocrit Care 2010, 12(1):124-131. 10.1007/s12028-009-9277-x, 19806476.
5. Kleindienst A, Fazzina G, Dunbar JG, Glisson R, Marmarou A. Protective effect of the V1a receptor antagonist SR 49059 on brain edema formation following middle cerebral artery occlusion in the rat. Acta Neurochir Suppl 2006, 96:303-306. 10.1007/3-211-30714-1_65, 16671476.
6. Sano K, Asano T, Tanishima T, Sasaki T. Lipid peroxidation as a cause of cerebral vasospasm. Neurol Res 1980, 2(3-4):253-272.
7. Kanamaru K, Waga S, Kojima T, Fujimoto K, Niwa S. Endothelium-dependent relaxation of canine basilar arteries. Part 2: Inhibition by hemoglobin and cerebrospinal fluid from patients with aneurysmal subarachnoid hemorrhage. Stroke 1987, 18(5):938-943. 10.1161/01.STR.18.5.938, 3114919.
8. Cocks TM, Malta E, King SJ, Woods RL, Angus JA. Oxyhaemoglobin increases the production of endothelin-1 by endothelial cells in culture. Eur J Pharmacol 1991, 196(2):177-182. 10.1016/0014-2999(91)90425-P, 1874284.
9. Macdonald RL, Weir BK. A review of hemoglobin and the pathogenesis of cerebral vasospasm. Stroke 1991, 22(8):971-982. 10.1161/01.STR.22.8.971, 1866764.
10. Asano T, Ikegaki I, Suzuki Y, Satoh S, Shibuya M. Endothelin and the production of cerebral vasospasm in dogs. Biochem Biophys Res Commun 1989, 159(3):1345-1351. 10.1016/0006-291X(89)92258-4, 2649099.
11. Mima T, Yanagisawa M, Shigeno T, Saito A, Goto K, Takakura K, Masaki T. Endothelin acts in feline and canine cerebral arteries from the adventitial side. Stroke 1989, 20(11):1553-1556. 10.1161/01.STR.20.11.1553, 2683245.
12. Giaid A, Gibson SJ, Ibrahim BN, Legon S, Bloom SR, Yanagisawa M, Masaki T, Varndell IM, Polak JM. Endothelin 1, an endothelium-derived peptide, is expressed in neurons of the human spinal cord and dorsal root ganglia. Proc Natl Acad Sci USA 1989, 86(19):7634-7638. 10.1073/pnas.86.19.7634, 298121, 2678110.
13. Lee ME, de la Monte SM, Ng SC, Bloch KD, Quertermous T. Expression of the potent vasoconstrictor endothelin in the human central nervous system. J Clin Invest 1990, 86(1):141-147. 10.1172/JCI114677, 296701, 2195059.
14. MacCumber MW, Ross CA, Snyder SH. Endothelin in brain: receptors, mitogenesis, and biosynthesis in glial cells. Proc Natl Acad Sci USA 1990, 87(6):2359-2363. 10.1073/pnas.87.6.2359, 53686, 2156267.
15. Fassbender K, Hodapp B, Rossol S, Bertsch T, Schmeck J, Schutt S, Fritzinger M, Horn P, Vajkoczy P, Wendel-Wellner M, et al. Endothelin-1 in subarachnoid hemorrhage: An acute-phase reactant produced by cerebrospinal fluid leukocytes. Stroke 2000, 31(12):2971-2975. 10.1161/01.STR.31.12.2971, 11108758.
16. Kasuya H, Weir BK, White DM, Stefansson K. Mechanism of oxyhemoglobin-induced release of endothelin-1 from cultured vascular endothelial cells and smooth-muscle cells. J Neurosurg 1993, 79(6):892-898. 10.3171/jns.1993.79.6.0892, 7504096.
17. Ehrenreich H, Lange M, Near KA, Anneser F, Schoeller LA, Schmid R, Winkler PA, Kehrl JH, Schmiedek P, Goebel FD. Long term monitoring of immunoreactive endothelin-1 and endothelin-3 in ventricular cerebrospinal fluid, plasma, and 24-h urine of patients with subarachnoid hemorrhage. Res Exp Med (Berl) 1992, 192(4):257-268.
18. Fujimori A, Yanagisawa M, Saito A, Goto K, Masaki T, Mima T, Takakura K, Shigeno T. Endothelin in plasma and cerebrospinal fluid of patients with subarachnoid haemorrhage. Lancet 1990, 336(8715):633.
19. Suzuki R, Masaoka H, Hirata Y, Marumo F, Isotani E, Hirakawa K. The role of endothelin-1 in the origin of cerebral vasospasm in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg 1992, 77(1):96-100. 10.3171/jns.1992.77.1.0096, 1607979.
20. Lo AC, Chen AY, Hung VK, Yaw LP, Fung MK, Ho MC, Tsang MC, Chung SS, Chung SK. Endothelin-1 overexpression leads to further water accumulation and brain edema after middle cerebral artery occlusion via aquaporin 4 expression in astrocytic end-feet. J Cereb Blood Flow Metab 2005, 25(8):998-1011. 10.1038/sj.jcbfm.9600108, 15815585.
21. Yeung PK, Lo AC, Leung JW, Chung SS, Chung SK. Targeted overexpression of endothelin-1 in astrocytes leads to more severe cytotoxic brain edema and higher mortality. J Cereb Blood Flow Metab 2009, 29(12):1891-1902. 10.1038/jcbfm.2009.175, 19707218.
22. 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(6):1086-1091. discussion 1091-1082, 10.1161/01.STR.26.6.1086, 7762027.
23. Huang Z, Huang PL, Panahian N, Dalkara T, Fishman MC, Moskowitz MA. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 1994, 265(5180):1883-1885. 10.1126/science.7522345, 7522345.
24. Carrillo P, Takasu A, Safar P, Tisherman S, Stezoski SW, Stolz G, Dixon CE, Radovsky A. Prolonged severe hemorrhagic shock and resuscitation in rats does not cause subtle brain damage. J Trauma 1998, 45(2):239-248. discussion 248-239, 10.1097/00005373-199808000-00007, 9715179.
25. Kamii H, Kato I, Kinouchi H, Chan PH, Epstein CJ, Akabane A, Okamoto H, Yoshimoto T. Amelioration of vasospasm after subarachnoid hemorrhage in transgenic mice overexpressing CuZn-superoxide dismutase. Stroke 1999, 30(4):867-871. discussion 872, 10.1161/01.STR.30.4.867, 10187893.
26. Mesis RG, Wang H, Lombard FW, Yates R, Vitek MP, Borel CO, Warner DS, Laskowitz DT. Dissociation between vasospasm and functional improvement in a murine model of subarachnoid hemorrhage. Neurosurg Focus 2006, 21(3):E4.
27. McGirt MJ, Lynch JR, Parra A, Sheng H, Pearlstein RD, Laskowitz DT, Pelligrino DA, Warner DS. Simvastatin increases endothelial nitric oxide synthase and ameliorates cerebral vasospasm resulting from subarachnoid hemorrhage. Stroke 2002, 33(12):2950-2956. 10.1161/01.STR.0000038986.68044.39, 12468796.
28. 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(5):554-571. 10.1038/sj.jcbfm.9600048, 15703702.
29. Altay O, Suzuki H, Hasegawa Y, Caner B, Krafft PR, Fujii M, Tang J, Zhang JH. Isoflurane attenuates blood-brain barrier disruption in ipsilateral hemisphere after subarachnoid hemorrhage in mice. Stroke 2012, 43(9):2513-2516. 10.1161/STROKEAHA.112.661728, 3429639, 22773559.
30. 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(7):1436-1448. 10.1002/jnr.21281, 17410600.
31. Sabri M, Jeon H, Ai J, Tariq A, Shang X, Chen G, Macdonald RL. Anterior circulation mouse model of subarachnoid hemorrhage. Brain Res 2009, 1295:179-185.
32. Mak KM, Lo AC, Lam AK, Yeung PK, Ko BC, Chung SS, Chung SK. Nuclear factor of activated T cells 5 deficiency increases the severity of neuronal cell death in ischemic injury. Neurosignals 2012, 20(4):237-251.
33. Lin EY, Li JF, Gnatovskiy L, Deng Y, Zhu L, Grzesik DA, Qian H, Xue XN, Pollard JW. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res 2006, 66(23):11238-11246. 10.1158/0008-5472.CAN-06-1278, 17114237.
34. Shuaib A, Xu Wang C, Yang T, Noor R. Effects of nonpeptide V(1) vasopressin receptor antagonist SR-49059 on infarction volume and recovery of function in a focal embolic stroke model. Stroke 2002, 33(12):3033-3037. 10.1161/01.STR.0000039405.31526.06, 12468809.
35. Laszlo FA, Varga C, Nakamura S. Vasopressin receptor antagonist OPC-31260 prevents cerebral oedema after subarachnoid haemorrhage. Eur J Pharmacol 1999, 364(2-3):115-122.
36. Liao CW, Fan CK, Kao TC, Ji DD, Su KE, Lin YH, Cho WL. Brain injury-associated biomarkers of TGF-beta1, S100B, GFAP, NF-L, tTG, AbetaPP, and tau were concomitantly enhanced and the UPS was impaired during acute brain injury caused by Toxocara canis in mice. BMC Infect Dis 2008, 8:84. 10.1186/1471-2334-8-84, 2442079, 18573219.
37. Pekny M, Pekna M. Astrocyte intermediate filaments in CNS pathologies and regeneration. J Pathol 2004, 204(4):428-437. 10.1002/path.1645, 15495269.
38. Pekny M, Wilhelmsson U, Bogestal YR, Pekna M. The role of astrocytes and complement system in neural plasticity. Int Rev Neurobiol 2007, 82:95-111.
39. Ignarro LJ. Nitric oxide as a unique signaling molecule in the vascular system: a historical overview. J Physiol Pharmacol 2002, 53(4 Pt 1):503-514.
40. Pluta RM. Dysfunction of nitric oxide synthases as a cause and therapeutic target in delayed cerebral vasospasm after SAH. Acta Neurochir Suppl 2008, 104:139-147. 10.1007/978-3-211-75718-5_28, 18456999.
41. Pluta RM, Thompson BG, Dawson TM, Snyder SH, Boock RJ, Oldfield EH. Loss of nitric oxide synthase immunoreactivity in cerebral vasospasm. J Neurosurg 1996, 84(4):648-654. 10.3171/jns.1996.84.4.0648, 8613858.
42. Ramzy D, Rao V, Tumiati LC, Xu N, Sheshgiri R, Miriuka S, Delgado DH, Ross HJ. Elevated endothelin-1 levels impair nitric oxide homeostasis through a PKC-dependent pathway. Circulation 2006, 114(1 Suppl):I319-I326.
43. Nishizawa S, Chen D, Yokoyama T, Yokota N, Otha S. Endothelin-1 initiates the development of vasospasm after subarachnoid haemorrhage through protein kinase C activation, but does not contribute to prolonged vasospasm. Acta Neurochir 2000, 142(12):1409-1415. 10.1007/s007010070013, 11214636.
44. Aihara Y, Jahromi BS, Yassari R, Nikitina E, Agbaje-Williams M, Macdonald RL. Molecular profile of vascular ion channels after experimental subarachnoid hemorrhage. J Cereb Blood Flow Metab 2004, 24(1):75-83.
45. Standen NB, Quayle JM. K + channel modulation in arterial smooth muscle. Acta Physiol Scand 1998, 164(4):549-557. 10.1046/j.1365-201X.1998.00433.x, 9887977.
46. Zimmermann M, Seifert V. Endothelin and subarachnoid hemorrhage: an overview. Neurosurgery 1998, 43(4):863-875. discussion 875-866, 10.1097/00006123-199810000-00083, 9766314.
47. Zimmermann M, Seifert V. Endothelin receptor antagonists and cerebral vasospasm. Clin Auton Res 2004, 14(3):143-145.
48. Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, Yazaki Y, Goto K, Masaki T. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 1988, 332(6163):411-415. 10.1038/332411a0, 2451132.
49. Yoshizawa T, Shinmi O, Giaid A, Yanagisawa M, Gibson SJ, Kimura S, Uchiyama Y, Polak JM, Masaki T, Kanazawa I. Endothelin: a novel peptide in the posterior pituitary system. Science 1990, 247(4941):462-464. 10.1126/science.2405487, 2405487.
50. Ehrenreich H, Costa T, Clouse KA, Pluta RM, Ogino Y, Coligan JE, Burd PR. Thrombin is a regulator of astrocytic endothelin-1. Brain Res 1993, 600(2):201-207. 10.1016/0006-8993(93)91374-2, 7679602.
51. Laszlo FA, Varga C, Doczi T. Cerebral oedema after subarachnoid haemorrhage. Pathogenetic significance of vasopressin. Acta Neurochir (Wien) 1995, 133(3-4):122-133.
52. Serradeil-Le Gal C, Wagnon J, Garcia C, Lacour C, Guiraudou P, Christophe B, Villanova G, Nisato D, Maffrand JP, Le Fur G, et al. Biochemical and pharmacological properties of SR 49059, a new, potent, nonpeptide antagonist of rat and human vasopressin V1a receptors. J Clin Invest 1993, 92(1):224-231. 10.1172/JCI116554, 293574, 8392086.
53. Thibonnier M, Kilani A, Rahman M, DiBlasi TP, Warner K, Smith MC, Leenhardt AF, Brouard R. Effects of the nonpeptide V(1) vasopressin receptor antagonist SR 49059 in hypertensive patients. Hypertension 1999, 34(6):1293-1300. 10.1161/01.HYP.34.6.1293, 10601133.
54. Manaenko A, Fathali N, Khatibi NH, Lekic T, Hasegawa Y, Martin R, Tang J, Zhang JH. Arginine-vasopressin V1a receptor inhibition improves neurologic outcomes following an intracerebral hemorrhagic brain injury. Neurochem Int 2011, 58(4):542-548. 10.1016/j.neuint.2011.01.018, 3063401, 21256175.
55. Manaenko A, Fathali N, Khatibi NH, Lekic T, Shum KJ, Martin R, Zhang JH, Tang J. Post-treatment with SR 49059 improves outcomes following an intracerebral hemorrhagic stroke in mice. Acta Neurochir Suppl 2011, 111:191-196. 10.1007/978-3-7091-0693-8_32, 3563694, 21725754.
56. Pluta RM, Boock RJ, Afshar JK, Clouse K, Bacic M, Ehrenreich H, Oldfield EH. Source and cause of endothelin-1 release into cerebrospinal fluid after subarachnoid hemorrhage. J Neurosurg 1997, 87(2):287-293. 10.3171/jns.1997.87.2.0287, 9254095.
57. Bian LG, Zhang TX, Zhao WG, Shen JK, Yang GY. Increased endothelin-1 in the rabbit model of middle cerebral artery occlusion. Neurosci Lett 1994, 174(1):47-50. 10.1016/0304-3940(94)90115-5, 7970153.
58. Matsumura K, Abe I, Tsuchihashi T, Tominaga M, Kobayashi K, Fujishima M. Central effect of endothelin on neurohormonal responses in conscious rabbits. Hypertension 1991, 17(6 Pt 2):1192-1196.
59. Nishizawa S, Obara K, Koide M, Nakayama K, Ohta S, Yokoyama T. Attenuation of canine cerebral vasospasm after subarachnoid hemorrhage by protein kinase C inhibitors despite augmented phosphorylation of myosin light chain. J Vasc Res 2003, 40(2):169-178. 10.1159/000070714, 12808353.
60. Yang G, Li T, Xu J, Liu L. PKC plays an important mediated effect in arginine vasopressin induced restoration of vascular responsiveness and calcium sensitization following hemorrhagic shock in rats. Eur J Pharmacol 2010, 628(1-3):148-154.
61. Povlsen GK, Johansson SE, Larsen CC, Samraj AK, Edvinsson L. Early events triggering delayed vasoconstrictor receptor upregulation and cerebral ischemia after subarachnoid hemorrhage. BMC Neurosci 2013, 14(1):34. 10.1186/1471-2202-14-34, 3618233, 23496889.
62. Chow M, Dumont AS, Kassell NF. Endothelin receptor antagonists and cerebral vasospasm: an update. Neurosurgery 2002, 51(6):1333-1341. discussion 1342.
63. Hansen-Schwartz J, Ansar S, Edvinsson L. Cerebral vasoconstriction after subarachnoid hemorrhage-role of changes in vascular receptor phenotype. Front Biosci 2008, 13:2160-2164. 10.2741/2831, 17981699.
64. Vatter H, Konczalla J, Weidauer S, Preibisch C, Zimmermann M, Raabe A, Seifert V. Effect of delayed cerebral vasospasm on cerebrovascular endothelin A receptor expression and function. J Neurosurg 2007, 107(1):121-127. 10.3171/JNS-07/07/0121, 17639881.
65. Clozel M, Watanabe H. BQ-123, a peptidic endothelin ETA receptor antagonist, prevents the early cerebral vasospasm following subarachnoid hemorrhage after intracisternal but not intravenous injection. Life Sci 1993, 52(9):825-834. 10.1016/0024-3205(93)90081-D, 8437512.
66. Kita T, Kubo K, Hiramatsu K, Sakaki T, Yonetani Y, Sato S, Fujimoto M, Nakashima T. Profiles of an intravenously available endothelin A-receptor antagonist, S-0139, for preventing cerebral vasospasm in a canine two-hemorrhage model. Life Sci 1998, 63(4):305-315. 10.1016/S0024-3205(98)00274-4, 9698039.
67. Zuccarello M, Lewis AI, Rapoport RM. Endothelin ETA and ETB receptors in subarachnoid hemorrhage-induced cerebral vasospasm. Eur J Pharmacol 1994, 259(1):R1-R2. 10.1016/0014-2999(94)90167-8, 7957585.
68. Kramer A, Fletcher J. Do endothelin-receptor antagonists prevent delayed neurological deficits and poor outcomes after aneurysmal subarachnoid hemorrhage?: a meta-analysis. Stroke 2009, 40(10):3403-3406. 10.1161/STROKEAHA.109.560243, 19679843.
69. Macdonald RL, Higashida RT, Keller E, Mayer SA, Molyneux A, Raabe A, Vajkoczy P, Wanke I, Bach D, Frey A, et al. Clazosentan, an endothelin receptor antagonist, in patients with aneurysmal subarachnoid haemorrhage undergoing surgical clipping: a randomised, double-blind, placebo-controlled phase 3 trial (CONSCIOUS-2). Lancet Neurol 2011, 10(7):618-625. 10.1016/S1474-4422(11)70108-9, 21640651.
70. Guo J, Shi Z, Yang K, Tian JH, Jiang L. Endothelin receptor antagonists for subarachnoid hemorrhage. Cochrane Database Syst Rev 2012, 9:CD008354.
71. Zemke D, Farooq MU, Mohammed Yahia A, Majid A. Delayed ischemia after subarachnoid hemorrhage: result of vasospasm alone or a broader vasculopathy?. Vasc Med 2007, 12(3):243-249. 10.1177/1358863X07081316, 17848485.
72. Vatter H, Konczalla J, Weidauer S, Preibisch C, Raabe A, Zimmermann M, Seifert V. Characterization of the endothelin-B receptor expression and vasomotor function during experimental cerebral vasospasm. Neurosurgery 2007, 60(6):1100-1108. discussion 1108-1109.
73. Pluta RM. Delayed cerebral vasospasm and nitric oxide: review, new hypothesis, and proposed treatment. Pharmacol Ther 2005, 105(1):23-56. 10.1016/j.pharmthera.2004.10.002, 15626454.
74. Thomas JE, Nemirovsky A, Zelman V, Giannotta SL. Rapid reversal of endothelin-1-induced cerebral vasoconstriction by intrathecal administration of nitric oxide donors. Neurosurgery 1997, 40(6):1245-1249. 10.1097/00006123-199706000-00026, 9179898.
75. Rubanyi GM, Polokoff MA. Endothelins: molecular biology, biochemistry, pharmacology, physiology, and pathophysiology. Pharmacol Rev 1994, 46(3):325-415.
76. Nishizawa S, Yokota N, Yokoyama T, Uemura K. Obligatory roles of protein kinase C and nitric oxide in the regulation of cerebral vascular tone: an implication of a pathogenesis of vasospasm after subarachnoid haemorrhage. Acta Neurochir (Wien) 1998, 140(10):1063-1068. 10.1007/s007010050215, 9856250.
77. Gilbert P, Tremblay J, Thorin E. Endothelium-derived endothelin-1 reduces cerebral artery sensitivity to nitric oxide by a protein kinase C-independent pathway. Stroke 2001, 32(10):2351-2355. 10.1161/hs1001.096007, 11588325.
78. Jahromi BS, Aihara Y, Ai J, Zhang ZD, Weyer G, Nikitina E, Yassari R, Houamed KM, Macdonald RL. Temporal profile of potassium channel dysfunction in cerebrovascular smooth muscle after experimental subarachnoid haemorrhage. Neurosci Lett 2008, 440(1):81-86. 10.1016/j.neulet.2008.05.015, 2518203, 18547725.
79. Ishiguro M, Morielli AD, Zvarova K, Tranmer BI, Penar PL, Wellman GC. Oxyhemoglobin-induced suppression of voltage-dependent K + channels in cerebral arteries by enhanced tyrosine kinase activity. Circ Res 2006, 99(11):1252-1260. 10.1161/01.RES.0000250821.32324.e1, 17068294.