Advertisement

Metabolic Brain Disease

, Volume 22, Issue 3–4, pp 251–263 | Cite as

Aquaporins in the brain: from aqueduct to “multi-duct”

  • Jérôme BadautEmail author
  • Jean-François Brunet
  • Luca Regli
ORIGINAL PAPER

Abstract

The aquaporin channel family was first considered as a family of water channels, however it is now clear that some of these channels are also permeable to small solutes such glycerol, urea and monocarboxylates. In this review, we will consider AQP4 and AQP9 expressed in the rodent brain. AQP4 is present on astrocytic end-feet in contact with brain vessels and could be involved in ionic homeostasis. However, AQP4 may also be involved in cell adhesion. AQP4 expression is highly modified in several brain disorders and it can play a key role in the cerebral edema formation. However, the exact role of AQP4 in edema formation is still debated. Recently, AQP4 has been shown to be also involved in astrocyte migration during glial scar formation. AQP9 is expressed in astrocytes and in catecholaminergic neurons. Two isoforms of AQP9 are expressed in brain cells, the shortest isoform is localized in the inner membrane of mitochondria and the longest in the cell membrane. The level of expression of AQP9 is negatively regulated by high concentrations of insulin. Taken together, these results suggest that AQP9 could be involved in brain energy metabolism. The induction of AQP9 in astrocytes is observed with time after stroke onset suggesting participation in the clearance of excess lactate in the extracellular space. These recent exciting results suggest that AQPs may not only be involved in water homeostasis in the brain but could also participate in other important physiological functions.

Keywords

Water channel Glycerol Lactate Catecholaminergic neurons Edema Ischemia 

Notes

Acknowledgements

The authors wish thank Dr M. Price for critical comments on the manuscript. This study was supported by grants from the Swiss Science Foundation (FN 3100AO-108001); Fondazione Per Lo Studio Delle Malattie Neurodegenerative Delle Persone Adulte e Dell’ Anziano”, from Lugano, Switzerland; SwissHeart foundation.

References

  1. Ainscow EK, Mirshamsi S, Tang T, Ashford ML, Rutter GA (2002) Dynamic imaging of free cytosolic ATP concentration during fuel sensing by rat hypothalamic neurones: evidence for ATP-independent control of ATP-sensitive K(+) channels. J Physiol 544:429–445PubMedCrossRefGoogle Scholar
  2. Amiry-Moghaddam M, Ottersen OP (2003) The molecular basis of water transport in the brain. Nat Rev Neurosci 4:991–1001PubMedGoogle Scholar
  3. Amiry-Moghaddam M, Otsuka T, Hurn PD, Traystman RJ, Haug FM, Froehner SC, Adams ME, Neely JD, Agre P, Ottersen OP, Bhardwaj A (2003a) An alpha-syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain. Proc Natl Acad Sci U S A 100:2106–2111PubMedCrossRefGoogle Scholar
  4. Amiry-Moghaddam M, Williamson A, Palomba M, Eid T, de Lanerolle NC, Nagelhus EA, Adams ME, Froehner SC, Agre P, Ottersen OP (2003b) Delayed K+clearance associated with aquaporin-4 mislocalization: phenotypic defects in brains of alpha-syntrophin-null mice. Proc Natl Acad Sci U S A 100:13615–13620PubMedCrossRefGoogle Scholar
  5. Amiry-Moghaddam M, Xue R, Haug FM, Neely JD, Bhardwaj A, Agre P, Adams ME, Froehner SC, Mori S, Ottersen OP (2004) 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 18:542–544PubMedGoogle Scholar
  6. Amiry-Moghaddam M, Lindland H, Zelenin S, Roberg BA, Gundersen BB, Petersen P, Rinvik E, Torgner IA, Ottersen OP (2005) Brain mitochondria contain aquaporin water channels: evidence for the expression of a short AQP9 isoform in the inner mitochondrial membrane. FASEB J 19:1459–1467PubMedCrossRefGoogle Scholar
  7. Arima H, Yamamoto N, Sobue K, Umenishi F, Tada T, Katsuya H, Asai K (2003) Hyperosmolar mannitol stimulates expression of aquaporin 4 and 9 through a p38 mitogen activated protein kinase-dependent pathway in rat astrocytes. J Biol Chem 27:27Google Scholar
  8. Badaut J, Regli L (2004) Distribution and possible roles of aquaporin 9 in the brain. Neuroscience 129:969–979CrossRefGoogle Scholar
  9. Badaut J, Nehlig A, Verbavatz J, Stoeckel M, Freund-Mercier MJ, Lasbennes F (2000a) Hypervascularization in the magnocellular nuclei of the rat hypothalamus: relationship with the distribution of aquaporin-4 and markers of energy metabolism. J Neuroendocrinol 12:960–969PubMedCrossRefGoogle Scholar
  10. Badaut J, Verbavatz JM, Freund-Mercier MJ, Lasbennes F (2000b) Presence of aquaporin-4 and muscarinic receptors in astrocytes and ependymal cells in rat brain: a clue to a common function. Neurosci Lett 292:75–78PubMedCrossRefGoogle Scholar
  11. Badaut J, Hirt L, Granziera C, Bogousslavsky J, Magistretti PJ, Regli L (2001) Astrocyte-specific expression of aquaporin-9 in mouse brain is increased after transient focal cerebral ischemia. J Cereb Blood Flow Metab 21:477–482PubMedCrossRefGoogle Scholar
  12. Badaut J, Lasbennes F, Magistretti PJ, Regli L (2002) Aquaporins in brain: distribution, physiology, and pathophysiology. J Cereb Blood Flow Metab 22:367–378PubMedCrossRefGoogle Scholar
  13. Badaut J, Brunet JF, Grollimund L, Hamou MF, Magistretti PJ, Villemure JG, Regli L (2003) Aquaporin 1 and aquaporin 4 expression in human brain after subarachnoid hemorrhage and in peritumoral tissue. Acta Neurochir Suppl 86:495–498PubMedGoogle Scholar
  14. Badaut J, Petit JM, Brunet JF, Magistretti PJ, Charriaut-Marlangue C, Regli L (2004) Distribution of Aquaporin 9 in the adult rat brain: preferential expression in catecholaminergic neurons and in glial cells. Neuroscience 128:27–38PubMedCrossRefGoogle Scholar
  15. Badaut J, Petit JM, Brunet JF, Magistretti P, Regli F (2005) Brain aquaporin 9 (AQP9) regulation by systemic insulin in rat. J Cereb Blood Flow Metab 25:246CrossRefGoogle Scholar
  16. Bergersen L, Rafiki A, Ottersen OP (2002) Immunogold cytochemistry identifies specialized membrane domains for monocarboxylate transport in the central nervous system. Neurochem Res 27:89–96PubMedCrossRefGoogle Scholar
  17. Bertrand N, Ishii H, Spatz M (1992) Regional and temporal glycerol changes induced by forebrain ischemia in gerbils. Neurosci Lett 148:81–84PubMedCrossRefGoogle Scholar
  18. Binder DK, Yao X, Zador Z, Sick TJ, Verkman AS, Manley GT (2006) Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia 53:631–636PubMedCrossRefGoogle Scholar
  19. Brown PD, Davies SL, Speake T, Millar ID (2004) Molecular mechanisms of cerebrospinal fluid production. Neuroscience 129:955–968CrossRefGoogle Scholar
  20. Carbrey JM, Gorelick-Feldman DA, Kozono D, Praetorius J, Nielsen S, Agre P (2003) Aquaglyceroporin AQP9: solute permeation and metabolic control of expression in liver. Proc Natl Acad Sci U S A 100:2945–2950PubMedCrossRefGoogle Scholar
  21. Cooper GJ, Zhou Y, Bouyer P, Grichtchenko II, Boron WF (2002) Transport of volatile solutes through AQP1. J Physiol 542:17–29PubMedCrossRefGoogle Scholar
  22. de Castro Ribeiro M, Hirt L, Bogousslavsky J, Regli L, Badaut J (2006) Time course of aquaporin expression after transient focal cerebral ischemia in mice. J Neurosci Res 83:1231–1240CrossRefGoogle Scholar
  23. Dolman D, Drndarski S, Abbott NJ, Rattray M (2005) Induction of aquaporin 1 but not aquaporin 4 messenger RNA in rat primary brain microvessel endothelial cells in culture. J Neurochem 93:825–833PubMedCrossRefGoogle Scholar
  24. Eid T, Lee TS, Thomas MJ, Amiry-Moghaddam M, Bjornsen LP, Spencer DD, Agre P, Ottersen OP, de Lanerolle NC (2005) Loss of perivascular aquaporin 4 may underlie deficient water and K + homeostasis in the human epileptogenic hippocampus. Proc Natl Acad Sci U S A 102:1193–1198PubMedCrossRefGoogle Scholar
  25. Elkjaer M, Vajda Z, Nejsum LN, Kwon T, Jensen UB, Amiry-Moghaddam M, Frokiaer J, Nielsen S (2000) Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem Biophys Res Commun 276:1118–1128PubMedCrossRefGoogle Scholar
  26. 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 15:90–98PubMedCrossRefGoogle Scholar
  27. Frykholm P, Hillered L, Langstrom B, Persson L, Valtysson J, Watanabe Y, Enblad P (2001) Increase of interstitial glycerol reflects the degree of ischaemic brain damage: a PET and microdialysis study in a middle cerebral artery occlusion-reperfusion primate model. J Neurol Neurosurg Psychiatry 71:455–461PubMedCrossRefGoogle Scholar
  28. Gerhart DZ, Enerson BE, Zhdankina OY, Leino RL, Drewes LR (1997) Expression of monocarboxylate transporter MCT1 by brain endothelium and glia in adult and suckling rats. Am J Physiol 273:E207–E213PubMedGoogle Scholar
  29. Gonen T, Sliz P, Kistler J, Cheng Y, Walz T (2004) Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 429:193–197PubMedCrossRefGoogle Scholar
  30. Grange-Messent V, Raison D, Bouchaud C (1996) Compared effects of extracellular K + ions and soman, a neurotoxic, on cerebral astrocyte morphology. An in vitro study. J Submicrosc Cytol Pathol 28:151–159PubMedGoogle Scholar
  31. Grill HJ, Kaplan JM (2002) The neuroanatomical axis for control of energy balance. Front Neuroendocrinol 23:2–40PubMedCrossRefGoogle Scholar
  32. Guadagno E, Moukhles H (2004) Laminin-induced aggregation of the inwardly rectifying potassium channel, Kir4.1, and the water-permeable channel, AQP4, via a dystroglycan-containing complex in astrocytes. Glia 47:138–149PubMedCrossRefGoogle Scholar
  33. Han Z, Wax MB, Patil RV (1998) Regulation of aquaporin-4 water channels by phorbol ester-dependent protein phosphorylation. J Biol Chem 273:6001–6004PubMedCrossRefGoogle Scholar
  34. Hellstrom M, Gerhardt H, Kalen M, Li X, Eriksson U, Wolburg H, Betsholtz C (2001) Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 153:543–553PubMedCrossRefGoogle Scholar
  35. Hiroaki Y, Tani K, Kamegawa A, Gyobu N, Nishikawa K, Suzuki H, Walz T, Sasaki S, Mitsuoka K, Kimura K (2006) Implications of the aquaporin-4 structure on array formation and cell adhesion. J Mol Biol 355:628–639PubMedCrossRefGoogle Scholar
  36. Ishibashi K, Kuwahara M, Gu Y, Tanaka Y, Marumo F, Sasaki S (1998) Cloning and functional expression of a new aquaporin (AQP9) abundantly expressed in the peripheral leukocytes permeable to water and urea, but not to glycerol. Biochem Biophys Res Commun 244:268–274PubMedCrossRefGoogle Scholar
  37. Jung JS, Bhat RV, Preston GM, Guggino WB, Baraban JM, Agre P (1994) Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci U S A 91:13052–13056PubMedCrossRefGoogle Scholar
  38. Ke C, Poon WS, Ng HK, Pang JC, Chan Y (2001) Heterogeneous responses of aquaporin-4 in oedema formation in a replicated severe traumatic brain injury model in rats. Neurosci Lett 301:21–24PubMedCrossRefGoogle Scholar
  39. Ke C, Poon WS, Ng HK, Lai FM, Tang NL, Pang JC (2002) 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 178:194–206PubMedCrossRefGoogle Scholar
  40. Kiening KL, van Landeghem FK, Schreiber S, Thomale UW, von Deimling A, Unterberg AW, Stover JF (2002) Decreased hemispheric aquaporin-4 is linked to evolving brain edema following controlled cortical impact injury in rats. Neurosci Lett 324:105–108PubMedCrossRefGoogle Scholar
  41. Kimelberg HK (2004) Water homeostasis in the brain: Basic concepts. Neuroscience 129:851–860PubMedCrossRefGoogle Scholar
  42. King LS, Yasui M, Agre P (2000) Aquaporins in health and disease. Mol Med Today 6:60–65PubMedCrossRefGoogle Scholar
  43. Klatzo I (1985) Brain oedema following brain ischaemia and the influence of therapy. Br J Anaesth 57:18–22PubMedCrossRefGoogle Scholar
  44. Ko SB, Uchida S, Naruse S, Kuwahara M, Ishibashi K, Marumo F, Hayakawa T, Sasaki S (1999) Cloning and functional expression of rAOP9L a new member of aquaporin family from rat liver. Biochem Mol Biol Int 47:309–318PubMedGoogle Scholar
  45. Kuo JR, Lin CL, Chio CC, Wang JJ, Lin MT (2003) Effects of hypertonic (3%) saline in rats with circulatory shock and cerebral ischemia after heatstroke. Intensive Care Med 29:1567–1573PubMedCrossRefGoogle Scholar
  46. Kuriyama H, Shimomura I, Kishida K, Kondo H, Furuyama N, Nishizawa H, Maeda N, Matsuda M, Nagaretani H, Kihara S, Nakamura T, Tochino Y, Funahashi T, Matsuzawa Y (2002) Coordinated regulation of fat-specific and liver-specific glycerol channels, aquaporin adipose and aquaporin 9. Diabetes 51:2915–2921PubMedCrossRefGoogle Scholar
  47. Kyriaki G (2003) Brain insulin: regulation, mechanisms of action and functions. Cell Mol Neurobiol 23:1–25PubMedCrossRefGoogle Scholar
  48. Levin BE, Dunn-Meynell AA, Routh VH (1999) Brain glucose sensing and body energy homeostasis: role in obesity and diabetes. Am J Physiol 276:R1223–R1231PubMedGoogle Scholar
  49. Liu Z, Shen J, Carbrey JM, Mukhopadhyay R, Agre P, Rosen BP (2002) Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc Natl Acad Sci U S A 99:6053–6058PubMedCrossRefGoogle Scholar
  50. Magistretti PJ, Pellerin L (1999) Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos Trans R Soc Lond B Biol Sci 354:1155–1163PubMedCrossRefGoogle Scholar
  51. Magistretti PJ, Pellerin L, Rothman DL, Shulman RG (1999) Energy on demand. Science 283:496–497PubMedCrossRefGoogle Scholar
  52. 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 6:159–163PubMedCrossRefGoogle Scholar
  53. McKenna MC, Bezold LI, Kimatian SJ, Tildon JT, Fife MM (1986) Competition of glycerol with other oxidizable substrates in rat brain. Biochem J 237:47–51PubMedGoogle Scholar
  54. Meng S, Qiao M, Lin L, Del Bigio MR, Tomanek B, Tuor UI (2004) Correspondence of AQP4 expression and hypoxic-ischaemic brain oedema monitored by magnetic resonance imaging in the immature and juvenile rat. Eur J Neurosci 19:2261–2269PubMedCrossRefGoogle Scholar
  55. Nagelhus EA, Mathiisen TM, Ottersen OP (2004) Aquaporin-4 in the central nervous system: Cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience 129:905–913PubMedCrossRefGoogle Scholar
  56. Nakahama K, Nagano M, Fujioka A, Shinoda K, Sasaki H (1999) Effect of TPA on aquaporin 4 mRNA expression in cultured rat astrocytes. Glia 25:240–246PubMedCrossRefGoogle Scholar
  57. 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 U S A 98:14108–14113PubMedCrossRefGoogle Scholar
  58. Nguyen NH, Brathe A, Hassel B (2003) Neuronal uptake and metabolism of glycerol and the neuronal expression of mitochondrial glycerol-3-phosphate dehydrogenase. J Neurochem 85:831–842PubMedCrossRefGoogle Scholar
  59. Nicchia GP, Frigeri A, Nico B, Ribatti D, Svelto M (2001) Tissue distribution and membrane localization of aquaporin-9 water channel: evidence for sex-linked differences in liver. J Histochem Cytochem 49:1547–1556PubMedGoogle Scholar
  60. Nielsen S, Smith BL, Christensen EI, Agre P (1993) Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia. Proc Natl Acad Sci U S A 90:7275–7279PubMedCrossRefGoogle Scholar
  61. 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 17:171–180PubMedGoogle Scholar
  62. Niermann H, Amiry-Moghaddam M, Holthoff K, Witte OW, Ottersen OP (2001) A novel role of vasopressin in the brain: modulation of activity-dependent water flux in the neocortex. J Neurosci 21:3045–3051PubMedGoogle Scholar
  63. Nihei K, Koyama Y, Tani T, Yaoita E, Ohshiro K, Adhikary LP, Kurosaki I, Shirai Y, Hatakeyama K, Yamamoto T (2001) Immunolocalization of aquaporin-9 in rat hepatocytes and Leydig cells. Arch Histol Cytol 64:81–88PubMedCrossRefGoogle Scholar
  64. Oldendorf WH (1970) Measurement of brain uptake of radiolabeled substances using a tritiated water internal standard. Brain Res 24:372–376PubMedCrossRefGoogle Scholar
  65. Papadopoulos MC, Manley GT, Krishna S, Verkman AS (2004) Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J 18:1291–1293PubMedGoogle Scholar
  66. Pappius HM (1974) Part I: tumors of the brain and skull. In: Vinken PJ, Bruyn GW (eds) Handbook of clinical neurology, vol. 16. North Holland Publishing Company, New York, pp 167–185Google Scholar
  67. Penicaud L, Leloup C, Lorsignol A, Alquier T, Guillod E (2002) Brain glucose sensing mechanism and glucose homeostasis. Curr Opin Clin Nutr Metab Care 5:539–543PubMedCrossRefGoogle Scholar
  68. Pierre K, Pellerin L, Debernardi R, Riederer BM, Magistretti PJ (2000) Cell-specific localization of monocarboxylate transporters, MCT1 and MCT2, in the adult mouse brain revealed by double immunohistochemical labeling and confocal microscopy. Neuroscience 100:617–627PubMedCrossRefGoogle Scholar
  69. Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387PubMedCrossRefGoogle Scholar
  70. Rash JE, Yasumura T, Hudson CS, Agre P, Nielsen S (1998) 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 U S A 95:11981–11986PubMedCrossRefGoogle Scholar
  71. Rash JE, Davidson KGV, Yasumura T, Furman CS (2004) Freeze-fracture and immunogold analysis of aquaporin-4 (AQP4) square arrays, with models of AQP4 lattice assembly. Neuroscience 129:915–934PubMedCrossRefGoogle Scholar
  72. Saadoun S, Papadopoulos MC, Watanabe H, Yan D, Manley GT, Verkman AS (2005) Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci 118:5691–5698PubMedCrossRefGoogle Scholar
  73. Santoni V, Gerbeau P, Javot H, Maurel C (2000) The high diversity of aquaporins reveals novel facets of plant membrane functions. Curr Opin Plant Biol 3:476–481PubMedCrossRefGoogle Scholar
  74. Schulz MK, Wang LP, Tange M, Bjerre P (2000) Cerebral microdialysis monitoring: determination of normal and ischemic cerebral metabolisms in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg 93:808–814PubMedCrossRefGoogle Scholar
  75. Schurr A (2002) Lactate, glucose and energy metabolism in the ischemic brain (Review). Int J Mol Med 10:131–136PubMedGoogle Scholar
  76. Sun MC, Honey CR, Berk C, Wong NL, Tsui JK (2003) Regulation of aquaporin-4 in a traumatic brain injury model in rats. J Neurosurg 98:565–569PubMedGoogle Scholar
  77. Taniguchi M, Yamashita T, Kumura E, Tamatani M, Kobayashi A, Yokawa T, Maruno M, Kato A, Ohnishi T, Kohmura E, Tohyama M, Yoshimine T (2000) Induction of aquaporin-4 water channel mRNA after focal cerebral ischemia in rat. Brain Res Mol Brain Res 78:131–137PubMedCrossRefGoogle Scholar
  78. Tsukaguchi H, Shayakul C, Berger UV, Mackenzie B, Devidas S, Guggino WB, van Hoek AN, Hediger MA (1998) Molecular characterization of a broad selectivity neutral solute channel. J Biol Chem 273:24737–24743PubMedCrossRefGoogle Scholar
  79. Tsukaguchi H, Weremowicz S, Morton CC, Hediger MA (1999) Functional and molecular characterization of the human neutral solute channel aquaporin-9. Am J Physiol 277:F685–F696PubMedGoogle Scholar
  80. Unger JW, Livingston JN, Moss AM (1991) Insulin receptors in the central nervous system: localization, signalling mechanisms and functional aspects. Prog Neurobiol 36:343–362PubMedCrossRefGoogle Scholar
  81. Unterberg AW, Stover J, Kress B, Kiening KL (2004) Edema and brain trauma. Neuroscience 129:1019–1027CrossRefGoogle Scholar
  82. Vajda Z, Promeneur D, Doczi T, Sulyok E, Frokiaer J, Ottersen OP, Nielsen S (2000) Increased aquaporin-4 immunoreactivity in rat brain in response to systemic hyponatremia. Biochem Biophys Res Commun 270:495–503PubMedCrossRefGoogle Scholar
  83. 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 U S A 99:13131–13136PubMedCrossRefGoogle Scholar
  84. Venero JL, Vizuete ML, Ilundain AA, Machado A, Echevarria M, Cano J (1999) Detailed localization of aquaporin-4 messenger RNA in the CNS: preferential expression in periventricular organs. Neuroscience 94:239–250PubMedCrossRefGoogle Scholar
  85. Verbavatz JM, Ma T, Gobin R, Verkman AS (1997) Absence of orthogonal arrays in kidney, brain and muscle from transgenic knockout mice lacking water channel aquaporin-4. J Cell Sci 110:2855–2860PubMedGoogle Scholar
  86. Warth A, Kroger S, Wolburg H (2004) Redistribution of aquaporin-4 in human glioblastoma correlates with loss of agrin immunoreactivity from brain capillary basal laminae. Acta Neuropathol (Berl) 107:311–318CrossRefGoogle Scholar
  87. Wells T (1998) Vesicular osmometers, vasopression secretion and aquaporin-4: a new mechanism for osmoreception. Mol Cell Endocrinol 136:103–107PubMedCrossRefGoogle Scholar
  88. Yamamoto N, Sobue K, Miyachi T, Inagaki M, Miura Y, Katsuya H, Asai K (2001) Differential regulation of aquaporin expression in astrocytes by protein kinase C. Brain Res Mol Brain Res 95:110–116PubMedCrossRefGoogle Scholar
  89. Yamamoto N, Sobue K, Fujita M, Katsuya H, Asai K (2002) Differential regulation of aquaporin-5 and -9 expression in astrocytes by protein kinase A. Brain Res Mol Brain Res 104:96–102PubMedCrossRefGoogle Scholar
  90. Yang XJ, Kow LM, Funabashi T, Mobbs CV (1999) Hypothalamic glucose sensor: similarities to and differences from pancreatic beta-cell mechanisms. Diabetes 48:1763–1772PubMedCrossRefGoogle Scholar
  91. Zhao J, Moore AN, Clifton GL, Dash PK (2005) Sulforaphane enhances aquaporin-4 expression and decreases cerebral edema following traumatic brain injury. J Neurosci Res 82:499–506PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Jérôme Badaut
    • 1
    Email author
  • Jean-François Brunet
    • 1
  • Luca Regli
    • 1
  1. 1.Department of NeurosurgeryCHUV-UNILLausanneSwitzerland

Personalised recommendations