Acute vascular disruption and aquaporin 4 loss after atroke

Stroke

Volumn 40, Issue 6, 2009, Pages 2182-2190

  Friedman, Beth ^a,b   Schachtrup, Christian ^a,b   Tsai, Philbert S ^a,b   Shih, Andy Y ^a,b   Akassoglou, Katerina ^a,b   Kleinfeld, David ^a,b   Lyden, Patrick D ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Stroke Center   (United States)

Author keywords

Aquaporin 4; Blood brain barrier breakdown; Stroke

Indexed keywords

AQUAPORIN 4; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN G; MESSENGER RNA; COLORING AGENT; PROPIDIUM IODIDE; RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD VESSEL INJURY; CONTROLLED STUDY; CORPUS STRIATUM; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STROKE; TRANSGENIC MOUSE; ACUTE DISEASE; ANIMAL; BIOSYNTHESIS; BLOOD VESSEL; BRAIN EDEMA; CAPILLARY; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; ISOLATION AND PURIFICATION; METABOLISM; MIDDLE CEREBRAL ARTERY; MULTIPHOTON MICROSCOPY; PATHOLOGY; REPERFUSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ACUTE DISEASE; ANIMALS; AQUAPORIN 4; ASTROCYTES; BLOOD VESSELS; BLOTTING, WESTERN; BRAIN EDEMA; CAPILLARIES; COLORING AGENTS; GLIAL FIBRILLARY ACIDIC PROTEIN; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; MIDDLE CEREBRAL ARTERY; PROPIDIUM; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; STROKE;

EID: 66849135273     PISSN: 00392499     EISSN: None     Source Type: Journal    
DOI: 10.1161/STROKEAHA.108.523720     Document Type: Article

References (38)

1. 1. Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP. Specialized membrane domains for water transport in glial cells: High-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci. 1997;17:171-180.
2. Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S. Aquaporin water channels-from atomic structure to clinical medicine. J Physiol. 2002;542:3-16.
3. Jung JS, Bhat RV, Preston GM, Guggino WB, Baraban JM, Agre P. Molecular characterization of an aquaporin cdna from brain: Candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci USA. 1994;91:13052-13056.
4. Neely JD, Amiry-Moghaddam M, Ottersen OP, Froehner SC, Agre P, Adams ME. Syntrophin-dependent expression and localization of aquaporin-4 water channel protein. Proc Natl Acad Sci U S A. 2001;98:14108-14113.
5. Amiry-Moghaddam M, Xue R, Haug FM, Neely JD, Bhardwaj A, Agre P, Adams ME, Froehner SC, Mori S, Ottersen OP. Alpha-syntrophin deletion removes the perivascular but not endothelial pool of aquaporin-4 at the blood-brain barrier and delays the development of brain edema in an experimental model of acute hyponatremia. Faseb J. 2004;18:542-544.
6. Ma T, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS. Generation and phenotype of a transgenic knockout mouse lacking the mercurial-insensitive water channel aquaporin-4. J Clin Invest. 1997;100:957-962.
7. Papadopoulos MC, Verkman AS. Aquaporin-4 and brain edema. Pediatr Nephrol. 2007;22:778 -784.
8. Manley GT, Fujimura M, Ma T, Noshita N, Filiz F, Bollen AW, Chan P, Verkman AS. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat Med. 2000;6:159-163.
9. Manley GT, Binder DK, Papadopoulos MC, Verkman AS. New insights into water transport and edema in the central nervous system from phenotype analysis of aquaporin-4 null mice. Neuroscience. 2004;129:983-991.
10. Amiry-Moghaddam M, Otsuka T, Hurn PD, Traystman RJ, Haug FM, Froehner SC, Adams ME, Neely JD, Agre P, Ottersen OP, Bhardwaj A. An alpha-syntrophin- dependent pool of aqp4 in astroglial end-feet confers bidirectional water flow between blood and brain. Proc Natl Acad Sci U S A. 2003;100:2106-2111.
11. Vizuete ML, Venero JL, Vargas C, Ilundain AA, Echevarria M, Machado A, Cano J. Differential upregulation of aquaporin-4 mrna expression in reactive astrocytes after brain injury: Potential role in brain edema. Neurobiol Dis. 1999;6:245-258.
12. Ke C, Poon WS, Ng HK, Pang JC, Chan Y. Heterogeneous responses of aquaporin-4 in oedema formation in a replicated severe traumatic brain injury model in rats. Neurosci Lett. 2001;301:21-24.
13. Ribeiro Mde C, Hirt L, Bogousslavsky J, Regli L, Badaut J. Time course of aquaporin expression after transient focal cerebral ischemia in mice. J Neurosci Res. 2006;83:1231-1240.
14. Frydenlund DS, Bhardwaj A, Otsuka T, Mylonakou MN, Yasumura T, Davidson KG, Zeynalov E, Skare O, Laake P, Haug FM, Rash JE, Agre P, Ottersen OP, Amiry-Moghaddam M. Temporary loss of perivascular aquaporin-4 in neocortex after transient middle cerebral artery occlusion in mice. Proc Natl Acad Sci U S A. 2006;103:13532-13536.
15. Nagaraja TN, Keenan KA, Brown SL, Fenstermacher JD, Knight RA. Relative distribution of plasma flow markers and red blood cells across bbb openings in acute cerebral ischemia. Neurol Res. 2007;29:78 -80.
16. Nagaraja TN, Keenan KA, Fenstermacher JD, Knight RA. Acute leakage patterns of fluorescent plasma flow markers after transient focal cerebral ischemia suggest large openings in blood-brain barrier. Microcirculation. 2008;15:1-14.
17. Nishimura N, Schaffer CB, Friedman B, Tsai PS, Lyden PD, Kleinfeld D. Targeted insult to subsurface cortical blood vessels using ultrashort laser pulses: Three models of stroke. Nat Methods. 2006;3:99-108.
18. Schaffer CB, Friedman B, Nishimura N, Schroeder LF, Tsai PS, Ebner FF, Lyden PD, Kleinfeld D. Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol. 2006;4:e22.
19. Neumann-Haefelin T, Kastrup A, de Crespigny A, Yenari MA, Ringer T, Sun GH, Moseley ME Serial mri after transient focal cerebral ischemia in rats: Dynamics of tissue injury, blood-brain barrier damage, and edema formation. Stroke 2000;31:1965-1972; discussion 1972-1963.
20. Matsumoto K, Lo EH, Pierce AR, Wei H, Garrido L, Kowall NW. Role of vasogenic edema and tissue cavitation in ischemic evolution on diffusion-weighted imaging: Comparison with multiparameter mr and immunohistochemistry. AJNR Am J Neuroradiol. 1995;16:1107-1115.
21. Barber PA, Hoyte L, Kirk D, Foniok T, Buchan A, Tuor U. Early t1- and t2-weighted mri signatures of transient and permanent middle cerebral artery occlusion in a murine stroke model studied at 9.4t. Neurosci Lett. 2005;388:54-59.
22. Landis DM, Reese TS. Astrocyte membrane structure: Changes after circulatory arrest. J Cell Biol. 1981;88:660-663.
23. You X, Boyle DL, Hammaker D, Firestein GS. Puma-mediated apoptosis in fibroblast-like synoviocytes does not require p53. Arthritis Res Ther. 2006;8:R157.
24. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative pcr and the 2(-delta delta c(t)) method. Methods. 2001;25:402-408.
25. Paxinos G, Watson C, Pennisi M, Topple A. Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight. J Neurosci Methods. 1985;13:139-143.
26. Tsai PS, Friedman B, Ifarraguerri AI, Thompson BD, Lev-Ram V, Schaffer CB, Xiong Q, Tsien RY, Squier JA, Kleinfeld D. All-optical histology using ultrashort laser pulses. Neuron. 2003;39:27-41.
27. Whalen MJ, Dalkara T, You Z, Qiu J, Bermpohl D, Mehta N, Suter B, Bhide PG, Lo EH, Ericsson M, Moskowitz MA. Acute plasmalemma permeability and protracted clearance of injured cells after controlled cortical impact in mice. J Cereb Blood Flow Metab. 2008;28:490-505.
28. Aoki K, Uchihara T, Tsuchiya K, Nakamura A, Ikeda K, Wakayama Y. Enhanced expression of aquaporin 4 in human brain with infarction. Acta Neuropathol (Berl). 2003;106:121-124.
29. Qi X, Mochly-Rosen D. The pkc{delta} -abl complex communicates er stress to the mitochondria - an essential step in subsequent apoptosis. J Cell Sci. 2008;121:804 -813.
30. Rash JE, Yasumura T, Hudson CS, Agre P, Nielsen S. Direct immu- nogold labeling of aquaporin-4 in square arrays of astrocyte and ependy- mocyte plasma membranes in rat brain and spinal cord. Proc Natl Acad Sci U S A. 1998;95:11981-11986.
31. Tomas-Camardiel M, Venero JL, Herrera AJ, De Pablos RM, Pintor-Toro JA, Machado A, Cano J. Blood-brain barrier disruption highly induces aquaporin-4 mrna and protein in perivascular and parenchymal astro- cytes: Protective effect by estradiol treatment in ovariectomized animals. J Neurosci Res. 2005;80:235-246.
32. Ito H, Yamamoto N, Arima H, Hirate H, Morishima T, Umenishi F, Tada T, Asai K, Katsuya H, Sobue K. Interleukin-1beta induces the expression of aquaporin-4 through a nuclear factor-kappab pathway in rat astrocytes. J Neurochem. 2006;99:107-118.
33. Nicchia GP, Nico B, Camassa LM, Mola MG, Loh N, Dermietzel R, Spray DC, Svelto M, Frigeri A. The role of aquaporin-4 in the blood-brain barrier development and integrity: Studies in animal and cell culture models. Neuroscience. 2004;129:935-945.
34. Simard JM, Kent TA, Chen M, Tarasov KV, Gerzanich V. Brain oedema in focal ischaemia: Molecular pathophysiology and theoretical implications. Lancet Neurol. 2007;6:258 -268.
35. Quick AM, Cipolla MJ. Pregnancy-induced up-regulation of aquaporin-4 protein in brain and its role in eclampsia. Faseb J. 2005;19:170-175.
36. Jeyaseelan K, Lim KY, Armugam A. Microrna expression in the blood and brain of rats subjected to transient focal ischemia by middle cerebral artery occlusion. Stroke 2008;39:959-966.
37. Kamsteeg EJ, Hendriks G, Boone M, Konings IB, Oorschot V, van der Sluijs P, Klumperman J, Deen PM. Short-chain ubiquitination mediates the regulated endocytosis of the aquaporin-2 water channel. Proc Natl Acad Sci U S A. 2006;103:18344-18349.
38. Carmosino M, Procino G, Nicchia GP, Mannucci R, Verbavatz JM, Gobin R, Svelto M, Valenti G. Histamine treatment induces rearrangements of orthogonal arrays of particles (oaps) in human aqp4- expressing gastric cells. J Cell Biol. 2001;154:1235-1243.