Aquaporins in cerebrovascular disease: A target for treatment of brain edema?

Cerebrovascular Diseases

Volumn 31, Issue 6, 2011, Pages 521-531

  Badaut, J ^a   Ashwal, S ^a   Obenaus, A ^a,b  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b School of Science and Technology   (United States)

Author keywords

Apparent diffusion coefficient; Blood brain barrier; Edema; Neuroimaging; Neurovascular unit; Stroke; Water channel

Indexed keywords

ACETAZOLAMIDE; AQUAPORIN 1; AQUAPORIN 4; AQUAPORIN 9; BUMETANIDE; ERYTHROPOIETIN; METHAZOLAMIDE; VALPROIC ACID;

BRAIN BLOOD VESSEL; BRAIN EDEMA; BRAIN INJURY; BRAIN TISSUE; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; CEREBROVASCULAR DISEASE; DRUG MECHANISM; ENERGY METABOLISM; HUMAN; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; STROKE; WATER PERMEABILITY;

ANIMALS; AQUAPORINS; BASAL GANGLIA CEREBROVASCULAR DISEASE; BRAIN EDEMA; HUMANS; WATER;

EID: 79953799183     PISSN: 10159770     EISSN: None     Source Type: Journal    
DOI: 10.1159/000324328     Document Type: Review

References (65)

1. Klatzo I: Brain oedema following brain ischaemia and the influence of therapy. Br J Anaesth 1985; 57: 18-22. (Pubitemid 15151647)
2. Gonen T, Walz T: The structure of aquaporins. Q Rev Biophys 2006; 39: 361-396. (Pubitemid 44950380)
3. 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. (Pubitemid 44339604)
4. Musa-Aziz R, Chen LM, Pelletier MF, Boron WF: Relative CO 2 /NH 3 selectivities of AQP1, AQP4, AQP5, AmtB, and RhAG. Proc Natl Acad Sci USA 2009; 106: 5406-5411.
5. 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. (Pubitemid 27008860)
6. Brown PD, Davies SL, Speake T, Millar ID: Molecular mechanisms of cerebrospinal fluid production. Neuroscience 2004; 129: 955-968.
7. Arciénega II, Brunet JF, Bloch J, Badaut J: Cell locations for AQP1, AQP4 and 9 in the non-human primate brain. Neuroscience 2010; 167: 1103-1114.
8. Shields SD, Mazario J, Skinner K, Basbaum AI: Anatomical and functional analysis of aquaporin 1, a water channel in primary afferent neurons. Pain 2007; 131: 8-20. (Pubitemid 47187881)
9. 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.
10. 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.
11. 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.
12. 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. (Pubitemid 39556244)
13. 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. (Pubitemid 37444788)
14. 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.
15. 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. (Pubitemid 41817624)
16. Gonen T, Sliz P, Kistler J, Cheng Y, Walz T: Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 2004; 429: 193-197. (Pubitemid 38656196)
17. Saadoun S, Tait MJ, Reza A, Davies DC, Bell BA, Verkman AS, Papadopoulos MC: AQP4 gene deletion in mice does not alter bloodbrain barrier integrity or brain morphology. Neuroscience 2009; 161: 764-772.
18. 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. (Pubitemid 351339611)
19. 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. (Pubitemid 43079263)
20. Badaut J, Hirt L, Granziera C, Bogousslavsky J, Magistretti PJ, Regli L: Astrocyte-specific expression of aquaporin-9 in mouse brain is increased after transient focal cerebral ischemia. J Cereb Blood Flow Metab 2001; 21: 477-482. (Pubitemid 32422867)
21. Badaut J, Petit JM, Brunet JF, Magistretti PJ, Charriaut-Marlangue C, Regli L: Distribution of aquaporin 9 in the adult rat brain: preferential expression in catecholaminergic neurons and in glial cells. Neuroscience 2004; 128: 27-38. (Pubitemid 39140677)
22. de Castro Ribeiro M, 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. (Pubitemid 43668006)
23. Amiry-Moghaddam M, Lindland H, Zelenin S, Roberg BA, Gundersen BB, Petersen P, Rinvik E, Torgner IA, Ottersen OP: Brain mitochondria contain aquaporin water channels: evidence for the expression of a short AQP9 isoform in the inner mitochondrial membrane. FASEB J 2005; 19: 1459-1467. (Pubitemid 41279004)
24. Badaut J, Brunet JF, Petit JM, Guerin CF, Magistretti PJ, Regli L: Induction of brain aquaporin 9 (AQP9) in catecholaminergic neurons in diabetic rats. Brain Res 2008; 1188: 17-24. (Pubitemid 350296067)
25. Badaut J, Brunet JF, Grollimund L, Hamou MF, Magistretti PJ, Villemure JG, Regli L: Aquaporin 1 and aquaporin 4 expression in human brain after subarachnoid hemorrhage and in peritumoral tissue. Acta Neurochir 2003; 86(suppl):495-498.
26. Yatsushige H, Ostrowski RP, Tsubokawa T, Colohan A, Zhang JH: Role of c-Jun N-terminal kinase in early brain injury after subarachnoid hemorrhage. J Neurosci Res 2007; 85: 1436-1448. (Pubitemid 46724387)
27. Nesic O, Lee J, Unabia GC, Johnson K, Ye Z, Vergara L, Hulsebosch CE, Perez-Polo JR: Aquaporin 1 -a novel player in spinal cord injury. J Neurochem 2008; 105: 628-640. (Pubitemid 351565710)
28. 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. (Pubitemid 32182385)
29. 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. (Pubitemid 38582214)
30. 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. (Pubitemid 30082359)
31. Zador Z, Stiver S, Wang V, Manley GT: Role of aquaporin-4 in cerebral edema and stroke. Handb Exp Pharmacol 2009: 159-170.
32. Hirt L, Price M, Ternon B, Mastour N, Brunet JF, Badaut J: Early induction of AQP4 contributes the limitation of the edema formation in the brain ischemia. J Cereb Blood Flow Metab 2009; 29: 423-433.
33. Friedman B, Schachtrup C, Tsai PS, Shih AY, Akassoglou K, Kleinfeld D, Lyden PD: Acute vascular disruption and aquaporin 4 loss after stroke. Stroke 2009; 40: 2182-2190.
34. 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. (Pubitemid 14104101)
35. Badaut J, Ashwal S, Tone B, Regli L, Tian HR, Obenaus A: Temporal and regional evolution of aquaporin-4 expression and magnetic resonance imaging in a rat pup model of neonatal stroke. Pediatr Res 2007; 62: 248-254. (Pubitemid 47301470)
36. Papadopoulos MC, Manley GT, Krishna S, Verkman AS: Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J 2004; 18: 1291-1293. (Pubitemid 39561580)
37. Saadoun S, Papadopoulos MC: Aquaporin-4 in brain and spinal cord oedema. Neuroscience 2010; 168: 1036-1046.
38. Nesic O, Lee J, Ye Z, Unabia GC, Rafati D, Hulsebosch CE, Perez-Polo JR: Acute and chronic changes in aquaporin 4 expression after spinal cord injury. Neuroscience 2006; 143: 779-792. (Pubitemid 44751372)
39. Hwang IK, Yoo KY, Li H, Lee BH, Suh HW, Kwon YG, Won MH: Aquaporin 9 changes in pyramidal cells before and is expressed in astrocytes after delayed neuronal death in the ischemic hippocampal CA1 region of the gerbil. J Neurosci Res 2007; 85: 2470-2479. (Pubitemid 47204761)
40. Unterberg AW, Stover J, Kress B, Kiening KL: Edema and brain trauma. Neuroscience 2004; 129: 1019-1027.
41. 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. (Pubitemid 46228081)
42. Risher WC, Andrew RD, Kirov SA: Realtime passive volume responses of astrocytes to acute osmotic and ischemic stress in cortical slices and in vivo revealed by two-photon microscopy. Glia 2009; 57: 207-221.
43. O'Donnell ME, Tran L, Lam TI, Liu XB, Anderson SE: Bumetanide inhibition of the blood-brain barrier Na-K-Cl cotransporter reduces edema formation in the rat middle cerebral artery occlusion model of stroke. J Cereb Blood Flow Metab 2004; 24: 1046-1056. (Pubitemid 39223628)
44. Strbian D, Durukan A, Pitkonen M, Marinkovic I, Tatlisumak E, Pedrono E, Abo-Ramadan U, Tatlisumak T: The bloodbrain barrier is continuously open for several weeks following transient focal cerebral ischemia. Neuroscience 2008; 153: 175-181.
45. 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 USA 2003; 100: 2106-2111. (Pubitemid 36254581)
46. Obenaus A, Ashwal S: Magnetic resonance imaging in cerebral ischemia: focus on neonates. Neuropharmacology 2008; 55: 271-280.
47. 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.
48. Chen CH, Xue R, Zhang J, Li X, Mori S, Bhardwaj A: Effect of osmotherapy with hypertonic saline on regional cerebral edema following experimental stroke: a study utilizing magnetic resonance imaging. Neurocrit Care 2007; 7: 92-100. (Pubitemid 350242687)
49. Zeynalov E, Chen CH, Froehner SC, Adams ME, Ottersen OP, Amiry-Moghaddam M, Bhardwaj A: The perivascular pool of aquaporin-4 mediates the effect of osmotherapy in postischemic cerebral edema. Crit Care Med 2008; 36: 2634-2640.
50. Migliati E, Meurice N, DuBois P, Fang JS, Somasekharan S, Beckett E, Flynn G, Yool AJ: Inhibition of aquaporin-1 and aquaporin-4 water permeability by a derivative of the loop diuretic bumetanide acting at an internal pore-occluding binding site. Mol Pharmacol 2009; 76: 105-112.
51. Migliati ER, Amiry-Moghaddam M, Froehner SC, Adams ME, Ottersen OP, Bhardwaj A: Na + -K + -2Cl -cotransport inhibitor attenuates cerebral edema following experimental stroke via the perivascular pool of aquaporin-4. Neurocrit Care 2010; 13: 123-131.
52. Huber VJ, Tsujita M, Yamazaki M, Sakimura K, Nakada T: Identification of arylsulfonamides as aquaporin 4 inhibitors. Bioorg Med Chem Lett 2007; 17: 1270-1273. (Pubitemid 46240848)
53. Tanimura Y, Hiroaki Y, Fujiyoshi Y: Acetazolamide reversibly inhibits water conduction by aquaporin-4. J Struct Biol 2009; 166: 16-21.
54. Yang B, Zhang H, Verkman AS: Lack of aquaporin-4 water transport inhibition by antiepileptics and arylsulfonamides. Bioorg Med Chem 2008; 16: 7489-7493.
55. Sogaard R, Zeuthen T: Test of blockers of AQP1 water permeability by a high-resolution method: no effects of tetraethylammonium ions or acetazolamide. Pflügers Arch 2008; 456: 285-292.
56. Huber VJ, Tsujita M, Kwee IL, Nakada T: Inhibition of aquaporin 4 by antiepileptic drugs. Bioorg Med Chem 2009; 17: 418-424.
57. Gunnarson E, Song Y, Kowalewski JM, Brismar H, Brines M, Cerami A, Andersson U, Zelenina M, Aperia A: Erythropoietin modulation of astrocyte water permeability as a component of neuroprotection. Proc Natl Acad Sci USA 2009; 106: 1602-1607.
58. Kikuchi K, Tancharoen S, Matsuda F, Biswas KK, Ito T, Morimoto Y, Oyama Y, Takenouchi K, Miura N, Arimura N, Nawa Y, Meng X, Shrestha B, Arimura S, Iwata M, Mera K, Sameshima H, Ohno Y, Maenosono R, Tajima Y, Uchikado H, Kuramoto T, Nakayama K, Shigemori M, Yoshida Y, Hashiguchi T, Maruyama I, Kawahara K: Edaravone attenuates cerebral ischemic injury by suppressing aquaporin-4. Biochem Biophys Res Commun 2009;390:1121-1125.
59. Kleindienst A, Fazzina G, Amorini AM, Dunbar JG, Glisson R, Marmarou A: Modulation of AQP4 expression by the protein kinase C activator, phorbol myristate acetate, decreases ischemia-induced brain edema. Acta Neurochir Suppl 2006;96:393-397.
60. Zheng YY, Lan YP, Tang HF, Zhu SM: Propofol pretreatment attenuates aquaporin-4 over-expression and alleviates cerebral edema after transient focal brain ischemia reperfusion in rats. Anesth Analg 2008;107: 2009-2016.
61. Yeung CM, Lo AC, Cheung AK, Chung SS, Wong D, Chung SK: More severe type 2 diabetes-associated ischemic stroke injury is alleviated in aldose reductase-deficient mice. J Neurosci Res 2010;88:2026-2034.
62. Zeng HK, Wang QS, Deng YY, Fang M, Chen CB, Fu YH, Jiang WQ, Jiang X: Hypertonic saline ameliorates cerebral edema through downregulation of aquaporin-4 expression in the astrocytes. Neuroscience 2010; 166: 878-885.
63. Michel-Monigadon D, Bonny C, Hirt L: c-Jun N-terminal kinase pathway inhibition in intracerebral hemorrhage. Cerebrovasc Dis 2010; 29: 564-570.
64. Liu X, Nakayama S, Amiry-Moghaddam M, Ottersen OP, Bhardwaj A: Arginine-vasopressin v1 but not v2 receptor antagonism modulates infarct volume, brain water content, and aquaporin-4 expression following experimental stroke. Neurocrit Care 2010; 12:124-131.
65. Li Q, Li Z, Mei Y, Guo Y: Neuregulin attenuated cerebral ischemia-creperfusion injury via inhibiting apoptosis and upregulating aquaporin-4. Neurosci Lett 2008;443:155-159.