Involvement of Water Channel Aquaporin 4 in the Nervous Disorders

Abstract

Abstract: The aquaporins (AQP) are a family of water-transporting proteins. Aquaporin4 (AQP4) is expressed in astrocytes throughout the central nervous system, as well as in Müller cells in the retina, Claudius/Hensen cells in the inner ear and olfactory epithelial cells. There are two AQP4 isoforms, M1 and M23， produced by alternative splicing. M23 AQP4 forms heterotetramers that assemble in the cell membrane in supramolecular structures called orthogonal arrays of particles (OAP). Phenotype analysis of AQP4-null mice indicates the involvement of AQP4 in brain and spinal cord water balance, astrocyte migration, neural signal transduction and neuroinflammation. AQP4-null mice manifest reduced brain swelling in cytotoxic cerebral edema, but increased brain swelling in vasogenic edema and hydrocephalus. AQP4 deficiency increases seizure duration. AQP4 is also involved in the neuroin?ammatory demyelinating disease neuromyelitis optica, where autoantibodies (NMO-IgG) targeting AQP4 produce astrocyte damage and in?ammation. This review summarizes the effect and possible mechanism of AQP4 in nervous system diseases, such as epilepsy, edema and neuromyelitis optica.

Key words: aquaporin4 (AQP4), orthogonal arrays of particle, epilepsy, edema, neuromyelitis optica

CLC Number:

R341
R742

WANG Wei-ling，YANG Bao-xue. Involvement of Water Channel Aquaporin 4 in the Nervous Disorders[J]. Acta Neuropharmacologica, 2012, 2(1): 20-27.

References

[1] Bradley M Denker, Barbara L Smith, Francis P Kuhajda, et al. Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules[J]. J Biol Chem, 1988, 263(30):15634-15642.

[2] Preston Gregory M, Carroll Tiziana Piazza, Guggino William B, et al. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein[J]. Science, 1992, 256(5055):385-387.

[3] Nemeth-Cahalan Karin L, Kalman Katalin, Hall James E. Molecular basis of pH and Ca2+ regulation of aquaporin water permeability[J]. J Gen Physiol, 2004, 123(5):573-580.

[4] Jung Jin Sup, Bhat Ratan V, Preston Gregory M, et al. Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance[J]. Proc Natl Acad Sci USA, 1994, 91(26):13052-13056.

[5] Yang Baoxue, van Hoek Alfred N, Verkman Alan S. Very high single channel water permeability of aquaporin-4 in baculovirus-infected insect cells and liposomes reconstituted with purified aquaporin-4[J]. Biochemistry, 1997, 36(24):7625-7632.

[6] Yang Baoxue, Ma Tonghui, Verkman Alan S. cDNA cloning, gene organization, and chromosomal localization of a human mercurial insensitive water channel. evidence for distinct transcriptional units[J]. J Biol Chem, 1995, 270(39):22907-22913.

[7] Wolburg Hartwig, Wolburg-Buchholz Karen, Fallier-Becker Petra, et al. Structure and functions of aquaporin-4-based orthogonal arrays of particles[J]. Int Rev Cell Mol Biol, 2011, 287:1-41.

[8] Yang Baoxue, Brown Dennis, Verkman Alan S. The mercurial insensitive water channel (AQP-4) forms orthogonal arrays in stably transfected Chinese hamster ovary cells[J]. J Biol Chem, 1996, 271(9):4577-4580.

[9] Furman C. Sue, Gorelick-Feldman Daniel A, Davidson Kimberly G, et al. Aquaporin-4 square array assembly: opposing actions of M1 and M23 isoforms[J]. Proc Natl Acad Sci USA, 2003, 100(23):13609-13614.

[10] Tajima Masato, Crane Jonathan M, Verkman Alan S. Aquaporin-4 (AQP4) associations and array dynamics probed by photobleaching and single-molecule analysis of green fluorescent protein-AQP4 chimeras[J]. J Biol Chem, 2010, 285(11):8163-8170.

[11] Crane Jonathan M, Verkman Alan S. Determinants of aquaporin-4 assembly in orthogonal arrays revealed by live-cell single-molecule fluorescence imaging[J]. J Cell Sci, 2009, 122(Pt 6):813-821.

[12] Jin Byung-Ju, Rossi Andrea, Verkman Alan S. Model of aquaporin-4 supramolecular assembly in orthogonal arrays based on heterotetrameric association of M1-M23 isoforms[J]. Biophys J, 2011, 100(12):2936-2945.

[13] Papadopoulos M. C, Verkman A. S. Aquaporin 4 and neuromyelitis optica[J]. Lancet Neurol, 2012, 11(6):535-544.

[14] Alan S Verkman. Aquaporins at a glance[J]. J Cell Sci, 2011, 124(Pt 13):2107-2112.

[15] Ma Tonghui, Yang Baoxue, Gillespie Annemarie, et al. Generation and phenotype of a transgenic knockout mouse lacking the mercurial-insensitive water channel aquaporin-4[J]. J Clin Invest, 1997, 100(5):957-962.

[16] Haj-Yasein Nadia Nabil, Vindedal Gry Fluge, Eilert-Olsen Martine, et al. Glial-conditional deletion of aquaporin-4 (Aqp4) reduces blood-brain water uptake and confers barrier function on perivascular astrocyte endfeet[J]. Proc Natl Acad Sci USA, 2011, 108(43):17815-17820.

[17] Saadoun S, Tait M. J, Reza A, et al. AQP4 gene deletion in mice does not alter blood-brain barrier integrity or brain morphology[J]. Neuroscience, 2009, 161(3):764-772.

[18] Li Jiang, Verkman A S. Impaired hearing in mice lacking aquaporin-4 water channels[J]. J Biol Chem, 2001, 276(33):31233-31237.

[19] Li Jiang, Patil Rajkumar V, Verkman A S. Mildly abnormal retinal function in transgenic mice without Muller cell aquaporin-4 water channels[J]. Invest Ophthalmol Vis Sci, 2002, 43(2):573-579.

[20] Lu Daniel C, Zhang Hua, Zador Zsolt, et al. Impaired olfaction in mice lacking aquaporin-4 water channels[J]. FASEB J, 2008, 22(9):3216-3223.

[21] Devin K Binder , Yao Xiao-ming, Zador Zsolt, et al. Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels[J]. Glia, 2006, 53(6):631-636.

[22] Padmawar Prashant, Yao Xiao-ming, Bloch Orin, et al. K+ waves in brain cortex visualized using a long-wavelength K+-sensing fluorescent indicator[J]. Nat Methods, 2005, 2(11):825-827.

[23] Zhang Hua, Verkman Alan S. Microfiberoptic measurement of extracellular space volume in brain and tumor slices based on fluorescent dye partitioning[J]. Biophys J, 2010, 99(4):1284-1291.

[24] Bosco Alejandra, Cusato Karen, Nicchia Grazia P, et al. A developmental switch in the expression of aquaporin-4 and Kir4.1 from horizontal to Muller cells in mouse retina[J]. Invest Ophthalmol Vis Sci, 2005, 46(10):3869-3875.

[25] Lichter-Konecki Uta, Mangin Jean Marie, Gordish-Dressman Heather, et al. Gene expression profiling of astrocytes from hyperammonemic mice reveals altered pathways for water and potassium homeostasis in vivo[J]. Glia, 2008, 56(4):365-377.

[26] Ruiz-Ederra Javier, Zhang Hua, Verkman Alan S. Evidence against functional interaction between aquaporin-4 water channels and Kir4.1 potassium channels in retinal Muller cells[J]. J Biol Chem, 2007, 282(30):21866-21872.

[27] 蒙兰青, 韦世革, 黄瑞雅. 大鼠癫痫持续状态后水通道蛋白-4的表达[J]. 中华神经医学杂志, 2007, 6(2):144.

[28] Binder D. K, Oshio K, Ma T, et al. Increased seizure threshold in mice lacking aquaporin-4 water channels[J]. Neuroreport, 2004, 15(2):259-262.

[29] Kimelberg Harold K. Current concepts of brain edema. Review of laboratory investigations[J]. J Neurosurg, 1995, 83(6):1051-1059.

[30] MacAulay N, Zeuthen T. Water transport between CNS compartments: contributions of aquaporins and cotransporters[J]. Neuroscience, 2010, 168(4):941-956.

[31] Zelenina Marina. Regulation of brain aquaporins[J]. Neurochem Int, 2010, 57(4):468-488.

[32] Papadopoulos M. C, Saadoun S, Verkman A S. Aquaporins and cell migration[J]. Pflugers Arch, 2008, 456(4):693-700.

[33] Saadoun Samira, Papadopoulos Marios C, Watanabe Hiroyuki, et al. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation[J]. J Cell Sci, 2005, 118(Pt 24):5691-5698.

[34] Auguste Kurtis I, Jin Songwan, Uchida Kazunori, et al. Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury[J]. FASEB J, 2007, 21(1):108-116.

[35] Benfenati V, Ferroni S. Water transport between CNS compartments: functional and molecular interactions between aquaporins and ion channels[J]. Neuroscience, 2010, 168(4):926-940.

[36] Manley Geoffrey T, Fujimura Miki, Ma Tonghui, et al. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke[J]. Nat Med, 2000, 6(2):159-163.

[37] Yang Baoxue, Zador Zsolt, Verkman Alan S. Glial cell aquaporin-4 overexpression in transgenic mice accelerates cytotoxic brain swelling[J]. J Biol Chem, 2008, 283(22):15280-15286.

[38] Papadopoulos Marios C, Manley Geoffrey T, Krishna Sanjeev, et al. Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema[J]. FASEB J, 2004, 18(11):1291-1293.

[39] Bloch Orin, Papadopoulos Marios C, Manley Geoffrey T, et al. Aquaporin-4 gene deletion in mice increases focal edema associated with staphylococcal brain abscess[J]. J Neurochem, 2005, 95(1):254-262.

[40] Bloch Orin, Auguste Kurtis I, Manley Geoffrey T, et al. Accelerated progression of kaolin-induced hydrocephalus in aquaporin-4-deficient mice[J]. J Cereb Blood Flow Metab, 2006, 26(12):1527-1537.

[41] Saadoun Samira, Bell B Anthony, Verkman Alan S, et al. Greatly improved neurological outcome after spinal cord compression injury in AQP4-deficient mice[J]. Brain, 2008, 131(Pt 4):1087-1098.

[42] Kimura Atsushi, Hsu Mike, Seldin Marcus, et al. Protective role of aquaporin-4 water channels after contusion spinal cord injury[J]. Ann Neurol, 2010, 67(6):794-801.

[43] Bizzoco Elisa, Lolli Francesco, Repice Anna Maria, et al. Prevalence of neuromyelitis optica spectrum disorder and phenotype distribution[J]. J Neurol, 2009, 256(11):1891-1898.

[44] Jarius Sven, Wildemann Brigitte. AQP4 antibodies in neuromyelitis optica: diagnostic and pathogenetic relevance[J]. Nat Rev Neurol, 2010, 6(7):383-392.

[45] Saadoun Samira, Waters Patrick, Bell B Anthony, et al. Intra-cerebral injection of neuromyelitis optica immunoglobulin G and human complement produces neuromyelitis optica lesions in mice[J]. Brain, 2010, 133(Pt 2):349-361.

[46] Parratt J. D, Prineas J. W. Neuromyelitis optica: a demyelinating disease characterized by acute destruction and regeneration of perivascular astrocytes[J]. Mult Scler, 2010, 16(10):1156-1172.

[47] Marignier Romain, Nicolle Adeline, Watrin Chantal, et al. Oligodendrocytes are damaged by neuromyelitis optica immunoglobulin G via astrocyte injury[J]. Brain, 2010, 133(9):2578-2591.

[48] Misu T, Fujihara K, Kakita A, et al. Loss of aquaporin 4 in lesions of neuromyelitis optica: distinction from multiple sclerosis[J]. Brain, 2007, 130(Pt 5):1224-1234.

[49] Kinoshita Makoto, Nakatsuji Yuji, Moriya Moriya, et al. Astrocytic necrosis is induced by anti-aquaporin-4 antibody-positive serum[J]. Neuroreport, 2009, 20(5):508-512.

[50] Saadoun Samira, Waters Patrick, MacDonald Claire, et al. Neutrophil protease inhibition reduces neuromyelitis optica-immunoglobulin G-induced damage in mouse brain[J]. Ann Neurol, 2012, 71(3):323-333.

[51] Zhang Hhua, Bennett Jeffrey L, Verkman Alan S. Ex vivo spinal cord slice model of neuromyelitis optica reveals novel immunopathogenic mechanisms[J]. Ann Neurol, 2011, 70(6):943-954.

[52] Kira Jun-ichi. Autoimmunity in neuromyelitis optica and opticospinal multiple sclerosis: astrocytopathy as a common denominator in demyelinating disorders[J]. J Neurol Sci, 2011, 311(1-2):69-77.

[53] Bennett Jeffrey L, Lam Chiwan, Kalluri Sudhakar Reddy, et al. Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica[J]. Ann Neurol, 2009, 66(5):617-629.

[54] Tradtrantip L, Zhang H, Anderson M O, et al. Small-molecule inhibitors of NMO-IgG binding to aquaporin-4 reduce astrocyte cytotoxicity in neuromyelitis optica[J]. FASEB J, 2012, 26(5):2197-2208.

[55] Tradtrantip Lukmanee, Zhang Hua, Saadoun Samira, et al. Anti-aquaporin-4 monoclonal antibody blocker therapy for neuromyelitis optica[J]. Ann Neurol, 2012, 71(3):314-322.

[56] Verkman Alan S, Hara-Chikuma Mariko, Papadopoulos Marios C. Aquaporins--new players in cancer biology[J]. J Mol Med (Berl), 2008, 86(5):523-529.

[57] Zeng Xiaoning, Xie LuLu, Liang Rui, et al. AQP4 knockout aggravates ischemia/reperfusion injury in mice[J]. CNS Neurosci Ther, 2012, 18(5):388-394.