Aquaporin 4: a player in cerebral edema and neuroinflammation

Journal of Neuroinflammation

Jerome Badaut²  Andrew M Fukuda¹ 

[1] Departments of Physiology, Loma Linda University School of Medicine, Loma Linda, CA, 92354, USA;Departments of Pediatrics, Loma Linda University School of Medicine, Loma Linda, CA, 92354, USA

关键词: Neuroinflammation;    Traumatic brain injury;    Stroke;    Blood brain barrier;    Astrocyte;    Aquaporin;   

Others  :  1160091
DOI  :  10.1186/1742-2094-9-279

 received in 2012-11-01, accepted in 2012-12-07,  发布年份 2012

【 摘 要 】

Neuroinflammation is a common pathological event observed in many different brain diseases, frequently associated with blood brain barrier (BBB) dysfunction and followed by cerebral edema. Neuroinflammation is characterized with microglia activation and astrogliosis, which is a hypertrophy of the astrocytes. Astrocytes express aquaporin 4, the water channel protein, involved in water homeostasis and edema formation. Aside from its function in water homeostasis, recent studies started to show possible interrelations between aquaporin 4 and neuroinflammation. In this review the roles of aquaporin 4 in neuroinflammation associated with BBB disruption and cerebral edema will be discussed with recent studies in the field.

【 授权许可】

   
2012 Fukuda and Badaut; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Li L, Zhang H, Varrin-Doyer M, Zamvil SS, Verkman AS: Proinflammatory role of aquaporin-4 in autoimmune neuroinflammation. FASEB J 2011, 25:1556-1566.
• [2]Tourdias T, Mori N, Dragonu I, Cassagno N, Boiziau C, Aussudre J, Brochet B, Moonen C, Petry KG, Dousset V: Differential aquaporin 4 expression during edema build-up and resolution phases of brain inflammation. J Neuroinflammation 2011, 8:143. BioMed Central Full Text
• [3]Verkman AS: Aquaporins in clinical medicine. Annu Rev Med 2012, 63:303-316.
• [4]Badaut J, Copin JC, Fukuda AM, Gasche Y, Schaller K, da Silva RF: Increase of arginase activity in old apolipoprotein E deficient mice under Western diet associated with changes in neurovascular unit. J Neuroinflammation 2012, 9:132. BioMed Central Full Text
• [5]Chi Y, Fan Y, He L, Liu W, Wen X, Zhou S, Wang X, Zhang C, Kong H, Sonoda L, Tripathi P, Li CJ, Yu MS, Su C, Hu G: Novel role of aquaporin-4 in CD4+ CD25+ T regulatory cell development and severity of Parkinson’s disease. Aging Cell 2011, 10:368-382.
• [6]Hinson SR, Romero MF, Popescu BF, Lucchinetti CF, Fryer JP, Wolburg H, Fallier-Becker P, Noell S, Lennon VA: Molecular outcomes of neuromyelitis optica (NMO)-IgG binding to aquaporin-4 in astrocytes. Proc Natl Acad Sci USA 2012, 109:1245-1250.
• [7]Huang XN, Wang WZ, Fu J, Wang HB: The relationship between aquaporin-4 expression and blood–brain and spinal cord barrier permeability following experimental autoimmune encephalomyelitis in the rat. Anat Rec (Hoboken) 2011, 294:46-54.
• [8]Kinoshita M, Nakatsuji Y, Kimura T, Moriya M, Takata K, Okuno T, Kumanogoh A, Kajiyama K, Yoshikawa H, Sakoda S: Anti-aquaporin-4 antibody induces astrocytic cytotoxicity in the absence of CNS antigen-specific T cells. Biochem Biophys Res Commun 2010, 394:205-210.
• [9]Villaran RF, de Pablos RM, Arguelles S, Espinosa-Oliva AM, Tomas-Camardiel M, Herrera AJ, Cano J, Machado A: The intranigral injection of tissue plasminogen activator induced blood–brain barrier disruption, inflammatory process and degeneration of the dopaminergic system of the rat. Neurotoxicology 2009, 30:403-413.
• [10]Pham H, Doerrbecker J, Ramp AA, D’Souza CS, Gorasia DG, Purcell AW, Ayers MM, Orian JM: Experimental autoimmune encephalomyelitis (EAE) IN C57Bl/6 mice is not associated with astrogliosis. J Neuroimmunol 2011, 232:51-62.
• [11]Zador Z, Stiver S, Wang V, Manley GT: Role of aquaporin-4 in cerebral edema and stroke. Handb Exp Pharmacol 2009, 190:159-170.
• [12]Li L, Zhang H, Verkman AS: Greatly attenuated experimental autoimmune encephalomyelitis in aquaporin-4 knockout mice. BMC Neurosci 2009, 10:94. BioMed Central Full Text
• [13]Badaut J, Lasbennes F, Magistretti PJ, Regli L: Aquaporins in brain: distribution, physiology, and pathophysiology. J Cereb Blood Flow Metab 2002, 22:367-378.
• [14]Gonen T, Walz T: The structure of aquaporins. Q Rev Biophys 2006, 39:361-396.
• [15]Yu J, Yool AJ, Schulten K, Tajkhorshid E: Mechanism of gating and ion conductivity of a possible tetrameric pore in aquaporin-1. Structure 2006, 14:1411-1423.
• [16]Musa-Aziz R, Chen LM, Pelletier MF, Boron WF: Relative CO2/NH3 selectivities of AQP1, AQP4, AQP5, AmtB, and RhAG. Proc Natl Acad Sci USA 2009, 106:5406-5411.
• [17]Rash JE, Davidson KGV, Yasumura T, Furman CS: Freeze-fracture and immunogold analysis of aquaporin-4 (AQP4) square arrays, with models of AQP4 lattice assembly. Neuroscience 2004, 129:915-934.
• [18]Furman CS, Gorelick-Feldman DA, Davidson KG, Yasumura T, Neely JD, Agre P, Rash JE: Aquaporin-4 square array assembly: opposing actions of M1 and M23 isoforms. Proc Natl Acad Sci USA 2003, 100:13609-13614.
• [19]Hirt L, Ternon B, Price M, Mastour N, Brunet JF, Badaut J: Protective role of early aquaporin 4 induction against postischemic edema formation. J Cereb Blood Flow Metab 2009, 29:423-433.
• [20]Suzuki M, Iwasaki Y, Yamamoto T, Konno H, Yoshimoto T, Suzuki J: Disintegration of orthogonal arrays in perivascular astrocytic processes as an early event in acute global ischemia. Brain Res 1984, 300:141-145.
• [21]Saadoun S, Tait MJ, Reza A, Davies DC, Bell BA, Verkman AS, Papadopoulos MC: AQP4 gene deletion in mice does not alter blood–brain barrier integrity or brain morphology. Neuroscience 2009, 161:764-772.
• [22]Zhou J, Kong H, Hua X, Xiao M, Ding J, Hu G: Altered blood–brain barrier integrity in adult aquaporin-4 knockout mice. Neuroreport 2008, 19:1-5.
• [23]Grange-Messent V, Bouchaud C: Effects of soman on cerebral astrocyte plasma membranes: a freeze-fracture study. Neurosci Lett 1994, 178:77-80.
• [24]Grange-Messent V, Raison D, Bouchaud C: Compared effects of extracellular K + ions and soman, a neurotoxic, on cerebral astrocyte morphology. An in vitro study. J Submicrosc Cytol Pathol 1996, 28:151-159.
• [25]Badaut J, Nehlig A, Verbavatz J, Stoeckel M, Freund-Mercier MJ, Lasbennes F: Hypervascularization in the magnocellular nuclei of the rat hypothalamus: relationship with the distribution of aquaporin-4 and markers of energy metabolism. J Neuroendocrinol 2000, 12:960-969.
• [26]Badaut J, Verbavatz JM, Freund-Mercier MJ, Lasbennes F: Presence of aquaporin-4 and muscarinic receptors in astrocytes and ependymal cells in rat brain: a clue to a common function? Neurosci Lett 2000, 292:75-78.
• [27]Binder DK, Yao X, Zador Z, Sick TJ, Verkman AS, Manley GT: Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia 2006, 53:631-636.
• [28]Hiroaki Y, Tani K, Kamegawa A, Gyobu N, Nishikawa K, Suzuki H, Walz T, Sasaki S, Mitsuoka K, Kimura K: Implications of the Aquaporin-4 structure on array formation and cell adhesion. J Mol Biol 2006, 355:628-639.
• [29]Saadoun S, Papadopoulos MC, Watanabe H, Yan D, Manley GT, Verkman AS: Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci 2005, 118:5691-5698.
• [30]Graeber MB, Li W, Rodriguez ML: Role of microglia in CNS inflammation. FEBS Lett 2011, 585:3798-3805.
• [31]Kelley KW, Dantzer R: Alcoholism and inflammation: neuroimmunology of behavioral and mood disorders. Brain Behav Immun 2011, Suppl 1:S13-S20.
• [32]Galea I, Bechmann I, Perry VH: What is immune privilege (not)? Trends Immunol 2007, 28:12-18.
• [33]Kreutzberg GW: Microglia: a sensor for pathological events in the CNS. Trends Neurosci 1996, 19:312-318.
• [34]Liu W, Tang Y, Feng J: Cross talk between activation of microglia and astrocytes in pathological conditions in the central nervous system. Life Sci 2011, 89:141-146.
• [35]Faustino JV, Wang X, Johnson CE, Klibanov A, Derugin N, Wendland MF, Vexler ZS: Microglial cells contribute to endogenous brain defenses after acute neonatal focal stroke. J Neurosci 2011, 31:12992-13001.
• [36]Loane DJ, Byrnes KR: Role of microglia in neurotrauma. Neurotherapeutics 2010, 7:366-377.
• [37]Soliman ML, Puig KL, Combs CK, Rosenberger TA: Acetate reduces microglia inflammatory signaling in vitro. J Neurochem 2012, 123:555-567.
• [38]Sofroniew MV: Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 2009, 32:638-647.
• [39]Sofroniew MV, Vinters HV: Astrocytes: biology and pathology. Acta Neuropathol 2010, 119:7-35.
• [40]Auguste KI, Jin S, Uchida K, Yan D, Manley GT, Papadopoulos MC, Verkman AS: Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury. FASEB J 2007, 21:108-116.
• [41]Fukuda AM, Pop V, Spagnoli D, Ashwal S, Obenaus A, Badaut J: Delayed increase of astrocytic aquaporin 4 after juvenile traumatic brain injury: Possible role in edema resolution? Neuroscience 2012, 222:366-378.
• [42]Tomas-Camardiel M, Venero JL, de Pablos RM, Rite I, Machado A, Cano J: In vivo expression of aquaporin-4 by reactive microglia. J Neurochem 2004, 91:891-899.
• [43]Marignier R, Giraudon P, Vukusic S, Confavreux C, Honnorat J: Anti-aquaporin-4 antibodies in Devic's neuromyelitis optica: therapeutic implications. Ther Adv Neurol Disord 2010, 3:311-321.
• [44]Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR: IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med 2005, 202:473-477.
• [45]Lennon VA, Wingerchuk DM, Kryzer TJ, Pittock SJ, Lucchinetti CF, Fujihara K, Nakashima I, Weinshenker BG: A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 2004, 364:2106-2112.
• [46]Nicchia GP, Mastrototaro M, Rossi A, Pisani F, Tortorella C, Ruggieri M, Lia A, Trojano M, Frigeri A, Svelto M: Aquaporin-4 orthogonal arrays of particles are the target for neuromyelitis optica autoantibodies. Glia 2009, 57:1363-1373.
• [47]Crane JM, Lam C, Rossi A, Gupta T, Bennett JL, Verkman AS: Binding affinity and specificity of neuromyelitis optica autoantibodies to aquaporin-4 M1/M23 isoforms and orthogonal arrays. J Biol Chem 2011, 286:16516-16524.
• [48]Bennett JL, Lam C, Kalluri SR, Saikali P, Bautista K, Dupree C, Glogowska M, Case D, Antel JP, Owens GP, Gilden D, Nessler S, Stadelamann C, Hemmer B: Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica. Ann Neurol 2009, 66:617-629.
• [49]Bradl M, Misu T, Takahashi T, Watanabe M, Mader S, Reindl M, Adzemovic M, Bauer J, Berger T, Fujihara K, Itoyama Y, Lassmann H: Neuromyelitis optica: pathogenicity of patient immunoglobulin in vivo. Ann Neurol 2009, 66:630-643.
• [50]Uzawa A, Mori M, Iwai Y, Kobayashi M, Hayakawa S, Kawaguchi N, Kuwabara S: Association of anti-aquaporin-4 antibody-positive neuromyelitis optica with myasthenia gravis. J Neurol Sci 2009, 287:105-107.
• [51]Ogaki K, Hirayama T, Chijiiwa K, Fukae J, Furuya T, Noda K, Fujishima K, Hattori N, Takahashi T, Okuma Y: Anti-aquaporin-4 antibody-positive definite neuromyelitis optica in a patient with thymectomy for myasthenia gravis. Neurologist 2012, 18:76-79.
• [52]Jarius S, Paul F, Franciotta D, de Seze J, Munch C, Salvetti M, Ruprecht K, Liebetrau M, Wandinger KP, Akman-Demir G, Melms A, Kristoferitsch W, Wildemann B: Neuromyelitis optica spectrum disorders in patients with myasthenia gravis: ten new aquaporin-4 antibody positive cases and a review of the literature. Mult Scler 2012, 18:1135-1143.
• [53]Leite MI, Coutinho E, Lana-Peixoto M, Apostolos S, Waters P, Sato D, Melamud L, Marta M, Graham A, Spillane J, Villa AM, Callegaro D, Santos E, da Silva AM, Jarius S, Howard R, Nakashima I, Giovanni G, Buckley C, Hilton-Jones D, Vincent A, Palace J: Myasthenia gravis and neuromyelitis optica spectrum disorder: a multicenter study of 16 patients. Neurology 2012, 78:1601-1607.
• [54]Etemadifar M, Abtahi SH, Dehghani A, Abtahi MA, Akbari M, Tabrizi N, Goodarzi T: Myasthenia gravis during the dourse of neuromyelitis optica. Case Rep Neurol 2011, 3:268-273.
• [55]Vaknin-Dembinsky A, Abramsky O, Petrou P, Ben-Hur T, Gotkine M, Brill L, Brenner T, Argov Z, Karussis D: Myasthenia gravis-associated neuromyelitis optica-like disease: an immunological link between the central nervous system and muscle? Arch Neurol 2011, 68:1557-1561.
• [56]Kay CS, Scola RH, Lorenzoni PJ, Jarius S, Arruda WO, Werneck LC: NMO-IgG positive neuromyelitis optica in a patient with myasthenia gravis but no thymectomy. J Neurol Sci 2008, 275:148-150.
• [57]Badaut J, Ashwal S, Obenaus A: Aquaporins in cerebrovascular disease: a target for treatment of brain edema? Cerebrovasc Dis 2011, 31:521-531.
• [58]Badaut J, Ashwal S, Adami A, Tone B, Recker R, Spagnoli D, Ternon B, Obenaus A: Brain water mobility decreases after astrocytic aquaporin-4 inhibition using RNA interference. J Cereb Blood Flow Metab 2011, 31:819-831.
• [59]Berezowski V, Fukuda AM, Cecchelli R, Badaut J: Endothelial cells and astrocytes: a concerto en duo in ischemic pathophysiology. Int J Cell Biol 2012, 2012:176287.
• [60]Rosell A, Ortega-Aznar A, Alvarez-Sabin J, Fernandez-Cadenas I, Ribo M, Molina CA, Lo EH, Montaner J: Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke 2006, 37:1399-1406.
• [61]Rosenberg GA, Estrada EY, Dencoff JE: Matrix metalloproteinases and TIMPs are associated with blood–brain barrier opening after reperfusion in rat brain. Stroke 1998, 29:2189-2195.
• [62]Candelario-Jalil E, Yang Y, Rosenberg GA: Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia. Neuroscience 2009, 158:983-994.
• [63]Wolburg-Buchholz K, Mack AF, Steiner E, Pfeiffer F, Engelhardt B, Wolburg H: Loss of astrocyte polarity marks blood–brain barrier impairment during experimental autoimmune encephalomyelitis. Acta Neuropathol 2009, 118:219-233.
• [64]Fallier-Becker P, Sperveslage J, Wolburg H, Noell S: The impact of agrin on the formation of orthogonal arrays of particles in cultured astrocytes from wild-type and agrin-null mice. Brain Res 2011, 1367:2-12.
• [65]Noell S, Wolburg-Buchholz K, Mack AF, Beedle AM, Satz JS, Campbell KP, Wolburg H, Fallier-Becker P: Evidence for a role of dystroglycan regulating the membrane architecture of astroglial endfeet. Eur J Neurosci 2011, 33:2179-2186.
• [66]Noell S, Fallier-Becker P, Deutsch U, Mack AF, Wolburg H: Agrin defines polarized distribution of orthogonal arrays of particles in astrocytes. Cell Tissue Res 2009, 337:185-195.
• [67]Wolburg H, Noell S, Wolburg-Buchholz K, Mack A, Fallier-Becker P: Agrin, aquaporin-4, and astrocyte polarity as an important feature of the blood–brain barrier. Neuroscientist 2009, 15:180-193.
• [68]Tourdias T, Hiba B, Raffard G, Biran M, Nishiguchi T, Aussudre J, Franconi JM, Brochet B, Petry KG, Dousset V: Adapted focal experimental autoimmune encephalomyelitis to allow MRI exploration of multiple sclerosis features. Exp Neurol 2011, 230:248-257.
• [69]Chastain CA, Oyoyo UE, Zipperman M, Joo E, Ashwal S, Shutter LA, Tong KA: Predicting outcomes of traumatic brain injury by imaging modality and injury distribution. J Neurotrauma 2009, 26:1183-1196.
• [70]Obenaus A, Ashwal S: Magnetic resonance imaging in cerebral ischemia: focus on neonates. Neuropharmacology 2008, 55:271-280.
• [71]Tourdias T, Dragonu I, Fushimi Y, Deloire MS, Boiziau C, Brochet B, Moonen C, Petry KG, Dousset V: Aquaporin 4 correlates with apparent diffusion coefficient and hydrocephalus severity in the rat brain: a combined MRI-histological study. Neuroimage 2009, 47:659-666.
• [72]Meng S, Qiao M, Lin L, Del Bigio MR, Tomanek B, Tuor UI: Correspondence of AQP4 expression and hypoxic-ischaemic brain oedema monitored by magnetic resonance imaging in the immature and juvenile rat. Eur J Neurosci 2004, 19:2261-2269.
• [73]Budde MD, Janes L, Gold E, Turtzo LC, Frank JA: The contribution of gliosis to diffusion tensor anisotropy and tractography following traumatic brain injury: validation in the rat using Fourier analysis of stained tissue sections. Brain 2011, 134:2248-2260.
• [74]Harsan LA, Poulet P, Guignard B, Parizel N, Skoff RP, Ghandour MS: Astrocytic hypertrophy in dysmyelination influences the diffusion anisotropy of white matter. J Neurosci Res 2007, 85:935-944.
• [75]Denes A, Ferenczi S, Kovacs KJ: Systemic inflammatory challenges compromise survival after experimental stroke via augmenting brain inflammation, blood–brain barrier damage and brain oedema independently of infarct size. J Neuroinflammation 2011, 8:164. BioMed Central Full Text
• [76]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.
• [77]Laird MD, Sukumari-Ramesh S, Swift AE, Meiler SE, Vender JR, Dhandapani KM: Curcumin attenuates cerebral edema following traumatic brain injury in mice: a possible role for aquaporin-4? J Neurochem 2010, 113:637-648.
• [78]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.
• [79]Clausen F, Hanell A, Israelsson C, Hedin J, Ebendal T, Mir AK, Gram H, Marklund N: Neutralization of interleukin-1beta reduces cerebral edema and tissue loss and improves late cognitive outcome following traumatic brain injury in mice. Eur J Neurosci 2011, 34:110-123.
• [80]Stoll G, Bendszus M: Inflammation and atherosclerosis: novel insights into plaque formation and destabilization. Stroke 2006, 37:1923-1932.
• [81]Crisby M, Rahman SM, Sylven C, Winblad B, Schultzberg M: Effects of high cholesterol diet on gliosis in apolipoprotein E knockout mice. Implications for Alzheimer’s disease and stroke. Neurosci Lett 2004, 369:87-92.
• [82]Lu DC, Zador Z, Yao J, Fazlollahi F, Manley GT: Aquaporin-4 reduces post-traumatic seizure susceptibility by promoting astrocytic glial scar formation in mice. J Neurotrauma 2011. Sep 22 [Epub ahead of print]
• [83]Shi WZ, Zhao CZ, Zhao B, Zheng XL, Fang SH, Lu YB, Zhang WP, Chen Z, Wei EQ: Aquaporin-4 deficiency attenuates acute lesions but aggravates delayed lesions and microgliosis after cryoinjury to mouse brain. Neurosci Bull 2012, 28:61-68.
• [84]Higashida T, Kreipke CW, Rafols JA, Peng C, Schafer S, Schafer P, Ding JY, Dornbos D, Li X, Guthikonda M, Rossi NF, Ding Y: The role of hypoxia-inducible factor-1alpha, aquaporin-4, and matrix metalloproteinase-9 in blood–brain barrier disruption and brain edema after traumatic brain injury. J Neurosurg 2011, 114:92-101.
• [85]Wang Z, Meng CJ, Shen XM, Shu Z, Ma C, Zhu GQ, Liu HX, He WC, Sun XB, Huo L, Zhang J, Chen G: Potential contribution of hypoxia-inducible factor-1alpha, aquaporin-4, and matrix metalloproteinase-9 to blood–brain barrier disruption and brain edema after experimental subarachnoid hemorrhage. J Mol Neurosci 2012, 48:273-280.
• [86]Eder C, Klee R, Heinemann U: Involvement of stretch-activated Cl- channels in ramification of murine microglia. J Neurosci 1998, 18:7127-7137.
• [87]Schlichter LC, Mertens T, Liu B: Swelling activated Cl- channels in microglia: Biophysics, pharmacology and role in glutamate release. Channels (Austin) 2011, 5:128-137.
• [88]Lewis RS, Ross PE, Cahalan MD: Chloride channels activated by osmotic stress in T lymphocytes. J Gen Physiol 1993, 101:801-826.