The role of aquaporin-4 in the blood-brain barrier development and integrity: Studies in animal and cell culture models

Neuroscience

Volumn 129, Issue 4, 2004, Pages 935-944

  Nicchia, G P ^a   Nico, B ^b   Camassa, L M A ^a   Mola, M G ^a   Loh, N ^c   Dermietzel, R ^d   Spray, D C ^e   Svelto, M ^a   Frigeri, A ^a  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY OF BARI MEDICAL SCHOOL   (Italy)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d RUHR UNIVERSITY BOCHUM   (Germany)

^e ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

aquaporins; astrocytes; brain edema; co cultures; mdx; muscular dystrophy

Indexed keywords

AQUAPORIN 4; DYSTROPHIN; ISOPROTEIN; LIPOPOLYSACCHARIDE;

ANGIOGENESIS; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY; BRAIN DEVELOPMENT; CELL CULTURE; CELL TYPE; CELLULAR DISTRIBUTION; CHICKEN; COCULTURE; DEVELOPMENTAL STAGE; DIFFUSION; DUCHENNE MUSCULAR DYSTROPHY; ENDOTHELIUM; ENDOTHELIUM CELL; EXPERIMENTAL MODEL; GLIA; HOMEOSTASIS; HUMAN; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MACROGLIA; NERVE STIMULATION; NONHUMAN; OPTIC TECTUM; PATHOPHYSIOLOGY; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; STRUCTURE ANALYSIS; TIGHT JUNCTION; WATER FLOW;

EID: 9344249008     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2004.07.055     Document Type: Article

References (62)

1. + clearance associated with aquaporin-4 mislocalization: phenotypic defects in brains of alpha-syntrophin-null mice Proc Natl Acad Sci USA 100 2003 13615 13620
2. M. Amiry-Moghaddam, T. Otsuka, P.D. Hurn, R.J. Traystman, F.M. Haug, S.C. Froehner, M.E. Adams, J.D. Neely, P. Agre, O.P. Ottersen, A. Bhardwaj 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 2003 2106 2111
3. M. Amiry-Moghaddam, R. Xue, F.M. Haug, J.D. Neely, A. Bhardwaj, P. Agre, M.E. Adams, S.C. Froehner, S. Mori, O.P. Ottersen 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 18 2004 542 544
4. H.C. Bauer, H. Bauer Neural induction of the blood-brain barrier: still an enigma Cell Mol Neurobiol 20 2000 13 28
5. M. Bertossi, L. Roncali, B. Nico, D. Ribatti, L. Mancini, D. Virgintini, G. Fabiani, A. Guidazzoli Perivascular astrocytes and endothelium in development of the blood-brain barrier: I The optic tectum of the chick embryo Anat Embryol 188 1993 21 29
6. C.T. Beuckmann, H.J. Galla Tissue culture of brain endothelial cells: induction of blood-brain barrier properties by brain factors W.M. Pardridge Introduction to the blood-brain barrier: methodology, biology, and pathology 1998 Cambridge University Press Cambridge 79 85
7. D.J. Blake, S. Kroger The neurobiology of Duchenne muscular dystrophy: learning lessons from muscle Trends Neurosci 23 2000 92 99
8. D.J. Blake, R. Hawkes, M.A. Benson, P.W. Beesley Different dystrophin-like complexes are expressed in neurons and glia J Cell Biol 147 1999 645 658
9. G. Bulfield, W.G. Siller, P.A. Wight, K.J. Moore X-Chromosome-linked muscular dystrophy (mdx) in the mouse Proc Natl Acad Sci USA 81 1984 1189 1192
10. + accumulation in the developing rat optic nerve Science 216 1982 1341 1343
11. N.C. Connors, P. Kofuji Dystrophin DP71 is critical for the clustered localization of potassium channels in retinal glial cells J Neurosci 22 2002 4321 4327
12. G.A. Cox, S.F. Phelps, V.M. Chapman, J.S. Chamberlain New mdx mutation disrupts expression of muscle and nonmuscle isoforms of dystrophin Nat Genet 4 1993 87 93
13. D.C. Davies Blood-brain barrier breakdown in septic encephalopathy and brain tumours J Anat 200 2002 639 646
14. R. Dermietzel Junctions in the central nervous system of the cat: 3 Gap junctions and membrane-associated orthogonal particle complexes (MOPC) in astrocytic membranes. Cell Tissue Res 149 1974 121 135
15. H.E. De Vries, J. Kuiper, A.G. de Boer, T.J. Van Berkel, D.D. Breimer The blood-brain barrier in neuroinflammatory diseases Pharmacol Rev 49 1997 143 155
16. Emery AEH (1987) Duchenne muscular dystrophy. In: Oxford monographs on medical genetics, Vol. 15. Oxford, UK: Oxford University Press.
17. C. Estrada, J.V. Bready, J.A. Berliner, W.M. Pardrige, P.A. Cancilla Astrocyte growth stimulation by a soluble factor produced by cerebral endothelial cells in vitro J Neuropathol Exp Neurol 49 1990 539 549
18. A. Frigeri, G.P. Nicchia, R. Balena, B. Nico, M. Svelto Aquaporins in skeletal muscle: reassessment of the functional role of AQP4 FASEB J 18 2004 905 907
19. A. Frigeri, G.P. Nicchia, S. Repetto, M. Bado, C. Minetti, M. Svelto Altered aquaporin-4 expression in human muscular dystrophies: a common feature FASEB J 16 2002 1120 1122
20. A. Frigeri, G.P. Nicchia, B. Nico, F. Quondamatteo, R. Herken, L. Roncali, M. Svelto Aquaporin-4 deficiency in skeletal muscle and brain of dystrophic mdx-mice FASEB J 15 2001 90 97
21. A. Frigeri, G.P. Nicchia, J.M. Verbavatz, G. Valenti, M. Svelto Expression of aquaporin-4 in fast-twitch fibers of mammalian skeletal muscle J Clin Invest 102 1998 695 703
22. A. Frigeri, M.A. Gropper, F. Umenishi, M. Kawashima, M. Brown, A.S. Verkman Localization of MIWC and GLIP water channel homologs in neuromuscular, epithelial and glandular tissues J Cell Sci 108 1995 2993 3002
23. A. Frigeri, M.A. Gropper, C.W. Turck, A.S. Verkman Immunolocalization of the mercurial-insensitive water channel and glycerol intrinsic protein in epithelial cell plasma membranes Proc Natl Acad Sci USA 92 1995 4328 4331
24. D.C. Gorecki, A.P. Monaco, M.J. Derry, A.P. Walker, E.A. Barnard, P.J. Barnard Expression of four alternative dystrophin transcripts in brain regions regulated by different promoters Hum Mol Genet 1 1992 505 510
25. M. Imamura, E. Ozawa Differential expression of dystrophin isoforms and utrophin during dibutyryl-cAMP-induced morphological differentiation of rat brain astrocytes Proc Natl Acad Sci USA 95 1998 6139 6144
26. V. Jancsik, F. Hajos The demonstration of immunoreactive dystrophin and its developmental expression in perivascular astrocytes Brain Res 831 1999 200 205
27. C. Ke, W.S. Poon, H.K. Ng, F.M. Lai, N.L. Tang, J.C. Pang Impact of experimental acute hyponatremia on severe traumatic brain injury in rats: influences on injuries, permeability of blood-brain barrier, ultrastructural features, and aquaporin-4 expression Exp Neurol 178 2002 194 206
28. C. Ke, Ws Poon, H.K. Ng, J.C. Pang, Y. Chan Heterogeneous responses of aquaporin-4 in oedema formation in a replicated severe traumatic brain injury model in the rats Neurosci Lett 301 2001 21 24
29. G.T. Manley, M. Fujimura, T. Ma, N. Noshita, F. Filiz, A.W. Bollen, P. Chan, A.S. Verkman Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke Nat Med 6 2000 159 163
30. + siphoning and water transport in rat retinal Muller cells is mediated by a coenrichment of Kir 4.1 and AQP4 in specific membrane domains Glia 26 1999 47 54
31. J.D. Neely, M. Amiry-Moghaddam, O.P. Ottersen, S.C. Froehner, P. Agre, M.E. Adams Syntrophin-dependent expression and localization of Aquaporin-4 water channel protein Proc Natl Acad Sci USA 98 2001 14108 14113
32. G.P. Nicchia, A. Frigeri, G.M. Liuzzi, M.P. Santacroce, B. Nico, G. Procino, F. Quondamatteo, R. Herken, L. Roncali, M. Svelto Aquaporin-4- containing astrocytes sustain a temperature- and mercury-insensitive swelling in vitro Glia 31 2000 29 38
33. G.P. Nicchia, A. Frigeri, M.G. Liuzzi, M. Svelto Inhibition of aquaporin-4 expression in astrocytes by RNAi determines alterations in cell morphology, growth and water transport and induces changes in ischemia related genes FASEB J 17 2003 1508 1510
34. B. Nico, A. Frigeri, G.P. Nicchia, P. Corsi, D. Ribatti, F. Quondamatteo, R. Herken, F. Girolamo, A. Marzullo, M. Svelto, L. Roncali Severe alterations of endothelial and glial cells in the blood-brain barrier of dystrophic mdx mice Glia 42 2003 235 251
35. Nico B, Nicchia GP, Frigeri A, Corsi P, Mangieri D, Ribatti D, Svelto M, Roncali L (2004) Altered blood-brain barrier development in dystrophic mdx mice. Neuroscience 125:921-935.
36. B. Nico, A. Frigeri, G.P. Nicchia, F. Quondamatteo, R. Herken, M. Errede, D. Ribatti, M. Svelto, L. Roncali Role of aquaporin-4 water channel in development and integrity of the blood-brain barrier J Cell Sci 114 2001 1297 1307
37. B. Nico, F. Quondamatteo, R. Herken, A. Marzullo, P. Corsi, M. Bertossi, G. Russo, D. Ribatti, L. Roncali Developmental expression of ZO-1 antigen in the mouse blood-brain barrier Dev Brain Res 114 1999 161 169
38. B. Nico, F. Quondamatteo, D. Ribatti, M. Bertossi, G. Russo, R. Herken, L. Roncalli Ultrastructural localization of lectin binding sites in the developing brain microvasculature Anat Embryol 197 1998 305 315
39. B. Nico, P. Cardelli, A. Fiori, L. Riccetelli, R.M. Giglio, R. Strom, M. Sasso-Pognetto, D. Cantino, M. Bertossi, D. Ribatti, L. Roncali Developmental study of ultrastructural and biochemical changes in isolated chick brain microvessels Microvasc Res 53 1997 79 91
40. B. Nico, D. Cantino, M. Sasso-Pognetto, M. Bertossi, D. Ribatti, L. Roncali Orthogonal array of particles (OAPs) in perivascular astrocytes and tight junctions in endothelial cells: a comparative study in developing and adult brain microvessels J Submicrosc Cytol Pathol 26 1994 193 209
41. S. Nielsen, E.A. Nagelhus, M. Amiry-Moghaddam, C. Bourque, P. Agre, O.P. Ottersen Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain J Neurosci 17 1997 171 180
42. V.J. Quagliarello, W.J. Long, W.M. Scheld Morphologic alteration of blood-brain barrier with experimental meningitis in the rat: temporal sequence and role of encapsulation J Clin Invest 77 1986 1084 1095
43. J.E. Rash, T. Yasumura, C.S. Hudson, P. Agre, S. Nielsen Direct immunogold labeling of aquaporin-4 in square arrays of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord Proc Natl Acad Sci USA 95 1998 11981 11986
44. C.A. Reinhart, S.M. Gloor Co-culture blood-brain barrier models and their use for pharmatoxicological screening Toxicol Vitro 11 1997 513 518
45. P.L. Robertson, M. Du Bois, P.D. Bowman, G.W. Goldstein Angiogenesis in developing rat brain: an in vivo and in vitro study Dev Brain Res 23 1985 219 223
46. L. Roncali, B. Nico, D. Ribatti, M. Bertossi, L. Mancini Microscopical and ultrastructural investigations on the development of the blood-barrier in the chick embryo optic tectum Acta Neuropathol 70 1986 193 201
47. S. Saadoun, M.C. Papadopoulos, D.C. Davies, S. Krishna, B.A. Bell Aquaporin-4 expression is increased in oedematous human brain tumours J Neurol Neurosurg Psychiatry 72 2002 262 265
48. C. Schulze, A.J. Firth Interendothelian junctions during blood-brain barrier development in the rat: morphological changes at the level of individual tight junctional contacts Dev Brain Res 69 1992 85 95
49. P.E. Sperri, M.B. Grant, J. Gomez, A. Vernadakis Endothelial cell conditioned media mediated regulation of glutamine synthase activity in glial cells Dev Brain Res 104 1997 205 208
50. P.A. Stewart Glial-vascular relations K. Welch L. Caplan D. Reis B. Siesjo B. Weir Primer on cerebrovascular disease 1997 Academic Press San Diego 70 75
51. Z. Vajda, M. Pedersen, E.M. Fuchtbauer, K. Wertz, H. Stodkilde-Jorgensen, E. Sulyok, T. Doczi, J.D. Neely, P. Agre, J. Frokiaer, S. Nielsen Delayed onset of brain edema and mislocalization of aquaporin-4 in dystrophin-null transgenic mice Proc Natl Acad Sci USA 99 2002 13131 13136
52. Z. Vajda, D. Promeneur, T. Doczi, E. Sulyok, J. Frokiaer, O.P. Ottersen, S. Nielsen Increased aquaporin-4 immunoreactivity in rat brain in response to systemic hyponatremia Biochem Biophys Res Commun 270 2000 495 503
53. J.M. Verbavatz, T. Ma, R. Gobin, A.S. Verkman Absence of orthogonal arrays in kidney, brain and muscle from transgenic knockout mice lacking water channel aquaporin-4 J Cell Sci 110 1997 2855 2860
54. M.L. Vizuete, M.L. Vizuete, J.L. Venero, C. Vargas, A.A. Ilundain, M. Echevarria, A. Machado, J. Cano Differential upregulation of aquaporin-4 mRNA expression in reactive astrocytes after brain injury: potential role in brain edema Neurobiol Dis 6 1999 245 258
55. S. Wagner, H. Gardner Modes of regulation of laminin-5 production by rat astrocytes Neurosci Lett 284 2000 105 108
56. S. Wakai, N. Hirokawa Development of the blood-brain barrier to horseradish peroxidase in the chick embryo Cell Tissue Res 195 1978 195 203
57. H. Wen, E.A. Nagelhus, M. Amiry-Moghaddam, P. Agre, O.P. Ottersen, S. Nielsen Ontogeny of water transport in rat brain: postnatal expression of the aquaporin-4 water channel Eur J Neurosci 11 1999 935 994
58. R.L. Williams, S.A. Courtneidge, E.F. Wagner Embryonic lethalities and endothelial tumors in chimeric mice expressing polyoma virus middle T oncogene Cell 52 1988 121 131
59. R.L. Williams, W. Risau, H.G. Zerwes, H. Drexler, A. Aguzzi, E.F. Wagner Endothelioma cells expressing the polyoma middle T oncogene induce hemangiomas by host cell recruitment Cell 57 1989 1053 1063
60. B. Yang, D. Brown, A.S. Verkman The mercurial insensitive water channel (AQP-4) forms orthogonal arrays in stably transfected Chinese hamster ovary cells J Biol Chem 271 1996 4577 4580
61. Yoder EJ (2002) Modifications in astrocyte morphology and calcium signaling induced by a brain capillary endothelial cell line 38:137-145.
62. T. Yokota, Y. Miyagoe, Y. Hosaka, K. Tsukita, S. Kameya, S. Shibuya, R. Matsuda, Y. Wakayama, S. Takeda Aquaporin-4 is absent at the sarcolemma and at perivascular astrocyte endfeet in alpha 1-syntrophin knockout mice Proc Jpn Acad 76 2000 22 27