Deletion of aquaporin-4 changes the perivascular glial protein scaffold without disrupting the brain endothelial barrier

GLIA

Volumn 60, Issue 3, 2012, Pages 432-440

  Eilert Olsen, Martine ^a   Haj Yasein, Nadia Nabil ^a   Vindedal, Gry Fluge ^a   Enger, Rune ^a   Gundersen, Georg Andreas ^a   Hoddevik, Eystein Hellstrøm ^a   Petersen, Pétur Henry ^b   Haug, Finn Mogens S ^a   Skare, Øivind ^c,d   Adams, Marvin E ^e   Froehner, Stanley C ^e   Burkhardt, John Michael ^a   Thoren, Anna E ^a   Nagelhus, Erlend A ^a,f  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF ICELAND   (Iceland)

^c NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^d UNIVERSITY OF BERGEN   (Norway)

^e UNIVERSITY OF WASHINGTON   (United States)

^f OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

AQP4; Astrocytes; Blood brain barrier; Endfeet; Syntrophin

Indexed keywords

AQUAPORIN 4; BETA DYSTROGLYCAN; CLAUDIN 5; DYSTROPHIN; EVANS BLUE; HORSERADISH PEROXIDASE; OCCLUDIN; PROTEIN ZO1; SCAFFOLD PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; BRAIN CAPILLARY; BRAIN HOMOGENATE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; IMMUNOCYTOCHEMISTRY; IMMUNOGOLD LABELING; IMMUNOREACTIVITY; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIGENS, CD31; AQUAPORIN 4; BLOOD VESSELS; BLOOD-BRAIN BARRIER; CALCIUM-BINDING PROTEINS; CAPILLARY PERMEABILITY; CEREBRAL CORTEX; ENDOTHELIUM; EVANS BLUE; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MICROSCOPY, IMMUNOELECTRON; MUSCLE PROTEINS; NEUROGLIA;

EID: 84856213513     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22277     Document Type: Article

References (46)

1. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. 2010. Structure and function of the blood-brain barrier. Neurobiol Dis 37: 13-25.
2. Adams ME, Kramarcy N, Krall SP, Rossi SG, Rotundo RL, Sealock R, Froehner SC. 2000. Absence of alpha-syntrophin leads to structurally aberrant neuromuscular synapses deficient in utrophin. J Cell Biol 150: 1385-1398.
3. Amiry-Moghaddam M, Otsuka T, Hurn 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: 2106-2111.
4. Amiry-Moghaddam M, Ottersen OP. 2003. The molecular basis of water transport in the brain. Nat Rev Neurosci 4: 991-1001.
5. Armulik A, Genove G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, He L, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C. 2010. Pericytes regulate the blood-brain barrier. Nature 468: 557-561.
6. Blake DJ, Weir A, Newey SE, Davies KE. 2002. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 82: 291-329.
7. Bloch O, Auguste KI, Manley GT, Verkman AS. 2006. Accelerated progression of kaolin-induced hydrocephalus in aquaporin-4-deficient mice. J Cereb Blood Flow Metab 26: 1527-1537.
8. Bloch O, Papadopoulos MC, Manley GT, Verkman AS. 2005. Aquaporin-4 gene deletion in mice increases focal edema associated with staphylococcal brain abscess. J Neurochem 95: 254-262.
9. Bragg AD, Amiry-Moghaddam M, Ottersen OP, Adams ME, Froehner SC. 2006. Assembly of a perivascular astrocyte protein scaffold at the mammalian blood-brain barrier is dependent on alpha-syntrophin. Glia 53: 879-890.
10. Bragg AD, Das SS, Froehner SC. 2010. Dystrophin-associated protein scaffolding in brain requires alpha-dystrobrevin. Neuroreport 21: 695-699.
11. Brignone MS, Lanciotti A, Macioce P, Macchia G, Gaetani M, Aloisi F, Petrucci TC, Ambrosini E. 2010. The {beta}1 subunit of the Na, K-ATPase pump interacts with megalencephalic leucoencephalopathy with subcortical cysts protein 1 (MLC1) in brain astrocytes: New insights into MLC pathogenesis. Hum Mol Genet 20: 90-103.
12. Cnaan A, Laird NM, Slasor P. 1997. Using the general linear mixed model to analyse unbalanced repeated measures and longitudinal data. Stat Med 16: 2349-2380.
13. Connors NC, Adams ME, Froehner SC, Kofuji P. 2004. The potassium channel Kir4.1 associates with the dystrophin-glycoprotein complex via alpha-syntrophin in glia. J Biol Chem 279: 28387-28392.
14. Daneman R, Zhou L, Kebede AA, Barres BA. 2010. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468: 562-566
15. Dibaj P, Kaiser M, Hirrlinger J, Kirchhoff F, Neusch C. 2007. Kir4.1 channels regulate swelling of astroglial processes in experimental spinal cord edema. J Neurochem 103: 2620-2628.
16. Feng X, Papadopoulos MC, Liu J, Li L, Zhang D, Zhang H, Verkman AS, Ma T. 2009. Sporadic obstructive hydrocephalus in Aqp4 null mice. J Neurosci Res 87: 1150-1155.
17. Fort PE, Sene A, Pannicke T, Roux MJ, Forster V, Mornet D, Nudel U, Yaffe D, Reichenbach A, Sahel JA, Rendon A. 2008. Kir4.1 and AQP4 associate with Dp71- and utrophin-DAPs complexes in specific and defined microdomains of Muller retinal glial cell membrane. Glia 56: 597-610.
18. Frigeri A, Gropper MA, Umenishi F, Kawashima M, Brown D, Verkman AS. 1995. Localization of MIWC and GLIP water channel homologs in neuromuscular, epithelial and glandular tissues. J Cell Sci 108(Part 9): 2993-3002.
19. Frigeri A, Nicchia GP, Nico B, Quondamatteo F, Herken R, Roncali L, Svelto M. 2001. Aquaporin-4 deficiency in skeletal muscle and brain of dystrophic mdx mice. FASEB J 15: 90-98.
20. Haj-Yasein NN, Vindedal GF, Eilert-Olsen M, Gundersen GA, Skare Ø, Laake P, Klungland A, Thoren AE, Burkhardt JM, Ottersen OP, Nagelhus EA. 2011a. Glial-conditional deletion of Aqp4 reduces blood-brain water uptake and confers barrier function on perivascular astrocyte endfeet. Proc Natl Acad Sci USA 108: 17815-17820.
21. Haj-Yasein NN, Jensen V, Vindedal GF, Gundersen GA, Klungland A, Ottersen OP, Hvalby O, Nagelhus EA. 2011b. Evidence that compromised K(+) spatial buffering contributes to the epileptogenic effect of mutations in the human kir4.1 gene (KCNJ10). Glia 59: 1635-1642.
22. Kramarcy NR, Vidal A, Froehner SC, Sealock R. 1994. Association of utrophin and multiple dystrophin short forms with the mammalian M® 58, 000 dystrophin-associated protein (syntrophin). J Biol Chem 269: 2870-2876.
23. Lassmann H, Zimprich F, Vass K, Hickey WF. 1991. Microglial cells are a component of the perivascular glia limitans. J Neurosci Res 28: 236-243.
24. Leis JA, Bekar LK, Walz W. 2005. Potassium homeostasis in the ischemic brain. Glia 50: 407-416.
25. Li L, Zhang H, Varrin-Doyer M, Zamvil SS, Verkman AS. 2011. Proinflammatory role of aquaporin-4 in autoimmune neuroinflammation. Faseb J 25: 1556-1566.
26. 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: 159-163.
27. Mintorovitch J, Yang GY, Shimizu H, Kucharczyk J, Chan PH, Weinstein PR. 1994. Diffusion-weighted magnetic resonance imaging of acute focal cerebral ischemia: Comparison of signal intensity with changes in brain water and Na+, K(+)-ATPase activity. J Cereb Blood Flow Metab 14: 332-336.
28. Nagelhus EA, Veruki ML, Torp R, Haug FM, Laake JH, Nielsen S, Agre P, Ottersen OP. 1998. Aquaporin-4 water channel protein in the rat retina and optic nerve: Polarized expression in Muller cells and fibrous astrocytes. J Neurosci 18: 2506-2519.
29. Neely JD, Amiry-Moghaddam M, Ottersen OP, Froehner SC, Agre P, Adams ME. 2001. Syntrophin-dependent expression and localization of Aquaporin-4 water channel protein. Proc Natl Acad Sci USA 98: 14108-14113.
30. Nicchia GP, Nico B, Camassa LM, Mola MG, Loh N, Dermietzel R, Spray DC, Svelto M, Frigeri A. 2004. The role of aquaporin-4 in the blood-brain barrier development and integrity: Studies in animal and cell culture models. Neuroscience 129: 935-945.
31. Nico B, Frigeri A, Nicchia GP, Corsi P, Ribatti D, Quondamatteo F, Herken R, Girolamo F, Marzullo A, Svelto M, Roncali L. 2003. Severe alterations of endothelial and glial cells in the blood-brain barrier of dystrophic mdx mice. Glia 42: 235-251.
32. Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP. 1997. Specialized membrane domains for water transport in glial cells: High-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17: 171-180.
33. Papadopoulos MC, Manley GT, Krishna S, Verkman AS. 2004. Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. Faseb J 18: 1291-1293.
34. Papadopoulos MC, Verkman AS. 2005. Aquaporin-4 gene disruption in mice reduces brain swelling and mortality in pneumococcal meningitis. J Biol Chem 280: 13906-13912.
35. Papadopoulos MC, Verkman AS. 2008. Potential utility of aquaporin modulators for therapy of brain disorders. Prog Brain Res 170: 589-601.
36. Peters MF, Adams ME, Froehner SC. 1997. Differential association of syntrophin pairs with the dystrophin complex. J Cell Biol 138: 81-93.
37. Pinheiro JC, Bates DM. 2000. Mixed-Effect models in S and S-PLUS. New York: Springer-Verlag.
38. Saadoun S, Papadopoulos MC, Davies DC, Krishna S, Bell BA. 2002. Aquaporin-4 expression is increased in oedematous human brain tumours. J Neurol Neurosurg Psychiatry 72: 262-265.
39. Saadoun S, Tait MJ, Reza A, Davies DC, Bell BA, Verkman AS, Papadopoulos MC. 2009. AQP4 gene deletion in mice does not alter blood-brain barrier integrity or brain morphology. Neuroscience 161: 764-772.
40. Taya K, Marmarou CR, Okuno K, Prieto R, Marmarou A. 2010. Effect of secondary insults upon aquaporin-4 water channels following experimental cortical contusion in rats. J Neurotrauma 27: 229-239.
41. Thrane AS, Rappold PM, Fujita T, Torres A, Bekar LK, Takano T, Peng W, Wang F, Thrane VR, Enger R, Haj-Yasein NN, Skare O, Holen T, Klungland A, Ottersen OP, Nedergaard M, Nagelhus EA. 2011. Critical role of aquaporin-4 (AQP4) in astrocytic Ca2+ signaling events elicited by cerebral edema. Proc Natl Acad Sci USA 108: 846-851.
42. 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: 13131-13136.
43. Wen H, Nagelhus EA, Amiry-Moghaddam M, Agre P, Ottersen OP, Nielsen S. 1999. Ontogeny of water transport in rat brain: Postnatal expression of the aquaporin-4 water channel. Eur J Neurosci 11: 935-945.
44. Xu Q, Qaum T, Adamis AP. 2001. Sensitive blood-retinal barrier breakdown quantitation using Evans blue. Invest Ophthalmol Vis Sci 42: 789-794.
45. Zeynalov E, Chen CH, Froehner SC, Adams ME, Ottersen OP, Amiry-Moghaddam M, Bhardwaj A. 2008. The perivascular pool of aquaporin-4 mediates the effect of osmotherapy in postischemic cerebral edema. Crit Care Med 36: 2634-2640.
46. Zhou J, Kong H, Hua X, Xiao M, Ding J, Hu G. 2008. Altered blood-brain barrier integrity in adult aquaporin-4 knockout mice. Neuroreport 19: 1-5.