Endothelin-1 overexpression leads to further water accumulation and brain edema after middle cerebral artery occlusion via aquaporin 4 expression in astrocytic end-feet

Journal of Cerebral Blood Flow and Metabolism

Volumn 25, Issue 8, 2005, Pages 998-1011

  Lo, Amy C Y ^a   Chen, Ann Y S ^a   Hung, Victor K L ^a   Yaw, Lai Ping ^a   Fung, Maggie K L ^a   Ho, Maggie C Y ^a   Tsang, Margaret C S ^a   Chung, Stephen S M ^a   Chung, Sookja K ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Cerebral infarct; Endothelin receptor antagonist; Hypoxia ischemia; Neurologic deficit; Stroke

Indexed keywords

AQUAPORIN 4; ATRASENTAN; ENDOTHELIN 1; ENDOTHELIN A RECEPTOR ANTAGONIST; GLIAL FIBRILLARY ACIDIC PROTEIN; WATER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN EDEMA; BRAIN HYPOXIA; BRAIN ISCHEMIA; CEREBROSPINAL FLUID; CONTROLLED STUDY; ENZYME INDUCTION; MEAN ARTERIAL PRESSURE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NONHUMAN; PLASMA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; STROKE; TRANSGENIC MOUSE; VASOCONSTRICTION;

ANIMALS; AQUAPORIN 4; AQUAPORINS; ASTROCYTES; BLOOD PRESSURE; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; BRAIN; BRAIN EDEMA; COLORING AGENTS; ENDOTHELIN-1; ENZYME-LINKED IMMUNOSORBENT ASSAY; EVANS BLUE; GLIAL FIBRILLARY ACIDIC PROTEIN; IN SITU HYBRIDIZATION; INFARCTION, MIDDLE CEREBRAL ARTERY; MICE; MICE, TRANSGENIC; NERVOUS SYSTEM DISEASES; RECEPTOR, ENDOTHELIN A; RECEPTOR, ENDOTHELIN B; REPERFUSION INJURY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; WATER;

EID: 23044459474     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.jcbfm.9600108     Document Type: Article

References (68)

1. Abbott NJ (2002) Astrocyte-endothelial interactions and blood-brain barrier permeability. J Anat 200:629-38
2. Agre P, Kozono D (2003) Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett 555:72-8
3. Amiry-Moghaddam M, Otsuka T, Hum PD, Traystman RJ, Haug FM, Froehner SC, Adams ME, Neely JD, Agre P, Ottersen OP, Bhardwaj A (2003) An alpha-syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain. Proc Natl Acad Sci USA 100:2106-11
4. Asahi M, Wang X, Mori T, Sumii T, Jung JC, Moskowitz MA, Fini ME, Lo EH (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 21:7724-32
5. Ayata C, Ropper AH (2002) Ischaemic brain oedema. J Clin Neurosci 9:113-24
6. Badaut J, Hirt L, Granziera C, Bogousslavsky J, Magistretti PJ, Regli L (2001) Astrocyte-specific expression of aquaporin-9 in mouse brain is increased after transient focal cerebral ischemia. J Cereb Blood Flow Metab 21:477-82
7. Badaut J, Lasbennes F, Magistretti PJ, Regli L (2002) Aquaporins in brain: distribution, physiology, and pathophysiology. J Cereb Blood Flow Metab 22:367-78
8. Barone FC, Globus MY, Price WJ, White RF, Storer BL, Feuerstein GZ, Busto R, Ohlstein EH (1994) Endothelin levels increase in rat focal and global ischemia. J Cereb Blood Flow Metab 14:337-42
9. Barone FC, Ohlstein EH, Hunter AJ, Campbell CA, Hadingham SH, Parsons AA, Yang Y, Shohami E (2000) Selective antagonism of endothelin-A-receptors improves outcome in both head trauma and focal stroke in rat. J Cardiovasc Pharmacol 36:8357-61
10. Barone FC, White RF, Elliott JD, Feuerstein GZ, Ohlstein EH. (1995) The endothelin receptor antagonist SB 217242 reduces cerebral focal ischemic brain injury. J Cardiovasc Pharmacol 26(Suppl 3):S404-7
11. Baynash AG, Hosoda K, Giaid A, Richardson JA, Emoto N, Hammer RE, Yanagisawa M (1994) Interaction of endothelin-3 with endothelin-B receptor is essential for development of epidermal melanocytes and enteric neurons. Cell 79:1277-85
12. Bentzer P, Holbeck S, Grande P (2002) Endothelin-1 reduces microvascular fluid permeability through secondary release of prostacyclin in cat skeletal muscle. Microvasc Res 63:50-60
13. Bhardwaj A, Wu Y, Hum PD, Kirsch JR, Traystman RJ (2000) Administration of selective endothelin receptor type A antagonist Ro 61- 1790 does not improve outcome in focal cerebral ischemia in cat. J Cereb Blood Flow Metab 20:499-504
14. Bian LG, Zhang TX, Zhao WG, Shen JK, Yang GY (1994) Increased endothelin-1 in the rabbit model of middle cerebral artery occlusion. Neurosci Lett 174:47-50
15. Blomstrand F, Giaume C, Hansson E, Ronnback L (1999) Distinct pharmacological properties of ET-1 and ET-3 on astroglial gap junctions and Ca(2+) signaling. Am J Physiol 277:C616-27
16. Bonventre JV, Huang Z, Taheri MR, O'Leary E, Li E, Moskowitz MA, Sapirstein A (1997) Reduced fertility and postischaemic brain injury in mice deficient in cytosolic phospholipase A2. Nature 390:622-5
17. Chan TS, Lin CX, Chan WY, Chung SS, Chung SK (1995) Mouse preproendothelin-1 gene, cDNA cloning, sequence analysis and determination of sites of expression during embryonic development. Eur J Biochem 234:819-26
18. Chen JF, Huang Z, Ma J, Zhu J, Moratalla R, Standaert D, Moskowitz MA, Fink JS, Schwarzschild MA (1999) A(2A) adenosine receptor deficiency attenuates brain injury induced by transient focal ischemia in mice. J Neurosci 19:9192-200
19. Clouthier DE, Hosoda K, Richardson JA, Williams SC, Yanagisawa H, Kuwaki T, Kumada M, Hammer RE, Yanagisawa M (1998) Cranial and cardiac neural crest defects in endothelin-A receptor-deficient mice. Development 125:813-24
20. Cole DJ, Matsumura JS, Drummond JC, Schultz RL, Wong MH (1991) Time- and pressure-dependent changes in blood-brain barrier permeability after temporary middle cerebral artery occlusion in rats. Acta Neuropathol 82:266-73
21. Dawson DA, Sugano H, McCarron RM, Hallenbeck JM, Spatz M (1999) Endothelin receptor antagonist preserves microvascular perfusion and reduces ischemic brain damage following permanent focal ischemia. Neurochem Res 24:1499-505
22. Ellsworth JL, Garcia R, Yu J, Kindy MS (2003) Fibroblast growth factor-18 reduced infarct volumes and behavioral deficits after transient occlusion of the middle cerebral artery in rats. Stroke 34:1507-12
23. Endres M, Laufs U, Huang Z, Nakamura T, Huang P, Moskowitz MA, Liao JK (1998) Stroke protection by 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase inhibitors mediated by endothelial nitric oxide synthase. Proc Natl Acad Sci USA 95:8880-5
24. Endres M, Wang ZQ, Namura S, Waeber C, Moskowitz MA (1997) Ischemic brain injury is mediated by the activation of poly(ADP-ribose)polymerase. J Cereb Blood Flow Metab 17:1143-51
25. Feuerstein G, Gu JL, Ohlstein EH, Barone FC, Yue TL (1994) Peptidic endothelin-1 receptor antagonist, BQ-123, and neuroprotection. Peptides 15:467-9
26. Foley PL, Caner HH, Kassell NF, Lee KS (1994) Reversal of subarachnoid hemorrhage-induced vasoconstriction with an endothelin receptor antagonist. Neurosurgery 34:108-12
27. Franceschini R, Gandolfo C, Cataldi A, Del Sette M, Rolandi A, Corsini G, Rolandi E, Barreca T (2001) Twenty-four-hour endothelin-1 secretory pattern in stroke patients. Biomed Pharmacother 55:272-6
28. Franklin KBJ, Paxinos G (1997) The mouse brain in sterotaxic coordinates. San Diego: Academic Press
29. Fujii M, Hara H, Meng W, Vonsattel JP, Huang Z, Moskowitz MA (1997) Strain-related differences in susceptibility to transient forebrain ischemia in SV-129 and C57black/6 mice. Stroke 28:1805-10
30. Hara H, Huang PL, Panahian N, Fishman MC, Moskowitz MA (1996) Reduced brain edema and infarction volume in mice lacking the neuronal isoform of nitric oxide synthase after transient MCA occlusion. J Cereb Blood Flow Metab 16:605-11
31. Ho MC, Lo AC, Kurihara H, Yu AC, Chung SS, Chung SK (2001) Endothelin-1 protects astrocytes from hypoxic/ischemic injury. FASEB J 15:618-26
32. Huang Z, Huang PL, Panahian N, Dalkara T, Fishman MC, Moskowitz MA (1994) Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 265:1883-5
33. Hunter AJ, Green AR, Cross AJ (1995) Animal models of acute ischaemic stroke: can they predict clinically successful neuroprotective drugs? Trends Pharmacol Sci 16:123-8
34. Ishikawa K, Ihara M, Noguchi K, Mase T, Mino N, Saeki T, Fukuroda T, Fukami T, Ozaki S, Nagase T et al (1994) Biochemical and pharmacological profile of a potent and selective endothelin B-receptor antagonist, BQ-788. Proc Natl Acad Sci USA 91:4892-6
35. Jarvis MP, Wessale JL, Zhu CZ, Lynch JJ, Dayton BD, Calzadilla SV, Padley RJ, Opgenorth TJ, Kowaluk EA (2000) ABT-627, an endothelin ET(A) receptor-selective antagonist, attenuates tactile allodynia in a diabetic rat model of neuropathic pain. Eur J Pharmacol 388:29-35
36. Kobari M, Fukuuchi Y, Tomita M, Tanahashi N, Konno S, Takeda H (1994) Constriction/dilatation of the cerebral microvessels by intravascular endothelin-1 in cats. J Cereb Blood Flow Metab 14:64-9
37. Kondo T, Reaume AG, Huang TT, Carlson E, Murakami K, Chen SF, Hoffman EK, Scott RW, Epstein CJ, Chan PH (1997) Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema formation after transient focal cerebral ischemia. J Neurosci 17:4180-9
38. Kurihara Y, Kurihara H, Suzuki H, Kodama T, Maemura K, Nagai R, Oda H, Kuwaki T, Cao WH, Kamada N, Jishage K, Ouchi Y, Azuma S, Toyoda Y, Ishikawa T, Kumada M, Yazaki Y (1994) Elevated blood pressure and craniofacial abnormalities in mice deficient in endothelin-1. Nature 368:703-10
39. Kuro T, Kohnou K, Kobayashi Y, Takaoka M, Opgenorth TJ, Wessale JL, Matsumura Y (2000) Selective antagonism of the ETA receptor, but not the ETB receptor, is protective against ischemic acute renal failure in rats. Jpn J Pharmacol 82:307-16
40. Kuwaki T, Kurihara H, Cao WH, Kurihara Y, Unekawa M, Yazaki Y, Kumada M (1997) Physiological role of brain endothelin in the central autonomic control: from neuron to knockout mouse. Prog Neurobiol 51:545-79
41. Lo AC, Haass C, Wagner SL, Teplow DB, Sisodia SS (1994) Metabolism of the "Swedish" amyloid precursor protein variant in Madin-Darby canine kidney cells. J Biol Chem 269:30966-73
42. Macrae IM, Robinson MJ, Graham DI, Reid JL, McCulloch J (1993) Endothelin-1-induced reductions in cerebral blood flow: dose dependency, time course, and neuropathological consequences. J Cereb Blood Flow Metab 13:276-84
43. Manley GT, Fujimura M, Ma T, Noshita N, Filiz F, Bollen AW, Chan P, Verkman AS (2000) Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat Med 6:159-63
44. Matsuo Y, Mihara S, Ninomiya M, Fujimoto M (2001) Protective effect of endothelin type A receptor antagonist on brain edema and injury after transient middle cerebral artery occlusion in rats. Stroke 32:2143-8
45. McAuley MA, Breu V, Graham DI, McCulloch J (1996) The effects of bosentan on cerebral blood flow and histopathology following middle cerebral artery occlusion in the rat. Eur J Pharmacol 307:171-81
46. Neely JD, Christensen BM, Nielsen S, Agre P (1999) Heterotetrameric composition of aquaporin-4 water channels. Biochemistry 38:11156-63
47. Papadopoulos MC, Krishna S, Verkman AS (2002) Aquaporin water channels and brain edema. Mt Sinai J Med 69:242-8
48. Papadopoulos MC, Manley GT, Krishna S, Verkman AS (2004) Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J 18:1291-3
49. Patel TR, Galbraith S, Graham DI, Hallak H, Doherty AM, McCulloch J (1996) Endothelin receptor antagonist increases cerebral perfusion and reduces ischaemic damage in feline focal cerebral ischaemia. J Cereb Blood Flow Metab 16:950-8
50. Patel TR, McAuley MA, Doherty AM, McCulloch J (1995) Pharmacological characterisation of peptide and nonpeptide endothelin antagonists in cerebral arterioles in situ. J Cereb Blood Flow Metab 15:S537
51. Patel TR, McCulloch J (1996) Failure of an endothelin antagonist to modify hypoperfusion after transient global ischaemia in the rat. J Cereb Blood Flow Metab 16:490-9
52. Sakai S, Miyauchi T, Sakurai T, Kasuya Y, Ihara M, Yamaguchi I, Goto K, Sugishita Y (1996) Endogenous endothelin-1 participates in the maintenance of cardiac function in rats with congestive heart failure. Marked increase in endothelin-1 production in the failing heart. Circulation 93:1214-22
53. Solenov E, Watanabe H, Manley GT, Verkman AS (2004) Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. Am J Physiol Cell Physiol 286:C426-32
54. Sonntag M, Wang MH, Huang MH, Wong NL (2004) Endothelin upregulates the expression of vasopressin V2 mRNA in the inner medullary collecting duct of the rat. Metabolism 53:1177-83
55. Stenman E, Malmsjo M, Uddman E, Gido G, Wieloch T, Edvinsson L (2002) Cerebral ischemia upregulates vascular endothelin ET(B) receptors in rat. Stroke 33:2311-6
56. Taniguchi M, Yamashita T, Kumura E, Tamatani M, Kobayashi A, Yokawa T, Maruno M, Kato A, Ohnishi T, Kohmura E, Tohyama M, Yoshimine T (2000) Induction of aquaporin-4 water channel mRNA after focal cerebral ischemia in rat. Brain Res Mol Brain Res 78:131-7
57. Tatlisumak T, Carano RA, Takano K, Opgenorth TJ, Sotak CH, Fisher M (1998) A novel endothelin antagonist, A-127722, attenuates ischemic lesion size in rats with temporary middle cerebral artery occlusion: a diffusion and perfusion MRI study. Stroke 29:850-7
58. Terris J, Ecelbarger CA, Marples D, Knepper MA, Nielsen S (1995) Distribution of aquaporin-4 water channel expression within rat kidney. Am J Physiol 269:F775-85
59. Toggas SM, Masliah E, Rockenstein EM, Rail GF, Abraham CR, Mucke L (1994) Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367:188-93
60. Tsang MC, Lo AC, Cheung PT, Chung SS, Chung SK (2001) Perinatal hypoxia-/ischemia-induced endothelin-1 mRNA in astrocyte-like and endothelial cells. Neuroreport 12:2265-70
61. Vajda Z, Pedersen M, Fuchtbauer EM, Wertz K, Stodkilde-Jorgensen H, Sulyok E, Doczi T, Neely JD, Agre P, Frokiaer J, Nielsen S (2002) Delayed onset of brain edema and mislocalization of aquaporin-4 in dystrophin-null transgenic mice. Proc Natl Acad Sci USA 99:13131-6
62. Vizuete ML, Venero JL, Vargas C, Ilundain AA, Echevarria M, Machado A, Cano J (1999) Differential upregulation of aquaporin-4 mRNA expression in reactive astrocytes after brain injury: potential role in brain edema. Neurobiol Dis 6:245-58
63. Volpe M, Cosentina F (2000) Abnormalities of endothelial function in the pathogenesis of stroke: the importance of endothelin. J Cardiovasc Pharmacol 35:845-8
64. Willette RN, Sauermelch C, Ezekiel M, Feuerstein G, Ohlstein EH (1990) Effect of endothelin on cortical microvascular perfusion in rats. Stroke 21:451-8
65. Wong NL, Sonntag M, Tsui JK (2003) Attenuation of renal vasopressin V2 receptor upregulation by bosentan, an ETA/ETB receptor antagonist. Metabolism 52:1141-6
66. Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, Yazaki Y, Goto K, Masaki T (1988) A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332:411-5
67. Yang GY, Betz AL (1994) Reperfusion-induced injury to the blood-brain barrier after middle cerebral artery occlusion in rats. Stroke 25:1658-64
68. Yang GY, Chen SF, Kinouchi H, Chan PH, Weinstein PR (1992) Edema, cation content, and ATPase activity after middle cerebral artery occlusion in rats. Stroke 23:1331-6