Aquaporin-4-dependent K+ and water transport modeled in brain extracellular space following neuroexcitation

Journal of General Physiology

Volumn 141, Issue 1, 2013, Pages 119-132

  Jin, Byung Ju ^a   Zhang, Hua ^a   Binder, Devin K ^c   Verkman, A S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN 4; POTASSIUM; WATER;

ANIMAL; ANIMAL MODEL; ARTICLE; ASTROCYTE; BIOLOGICAL MODEL; BRAIN; CELL COMMUNICATION; CELL MEMBRANE PERMEABILITY; CYTOLOGY; ELECTROPHYSIOLOGY; EXTRACELLULAR SPACE; GLIA; HUMAN; METABOLISM; MOUSE; NERVE CELL; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; AQUAPORIN 4; ASTROCYTES; BIOLOGICAL TRANSPORT; BRAIN; CELL COMMUNICATION; CELL MEMBRANE PERMEABILITY; ELECTROPHYSIOLOGICAL PHENOMENA; EXTRACELLULAR SPACE; HUMANS; MICE; MODELS, ANIMAL; MODELS, BIOLOGICAL; NEUROGLIA; NEURONS; POTASSIUM; WATER;

EID: 84872251822     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201210883     Document Type: Article

References (61)

1. Allen, N.J., and B.A. Barres. 2009. Neuroscience: Glia - more than just brain glue. Nature. 457:675-677. http://dx.doi.org/10.1038/457675a
2. + clearance associated with aquaporin-4 mislocalization: phenotypic defects in brains of alpha-syntrophin-null mice. Proc. Natl. Acad. Sci. USA. 100:13615-13620. http://dx.doi.org/10.1073/pnas.2336064100
3. Auguste, K.I., S. Jin, K. Uchida, D. Yan, G.T. Manley, M.C. Papadopoulos, and A.S. Verkman. 2007. Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury. FASEB J. 21:108-116. http://dx.doi.org/10.1096/fj.06-6848com
4. Ballanyi, K., P. Grafe, and G. ten Bruggencate. 1987. Ion activities and potassium uptake mechanisms of glial cells in guinea-pig olfactory cortex slices. J. Physiol. 382:159-174.
5. Bay, V., and A.M. Butt. 2012. Relationship between glial potassium regulation and axon excitability: a role for glial Kir4.1 channels. Glia. 60:651-660. http://dx.doi.org/10.1002/glia.22299
6. Binder, D.K., M.C. Papadopoulos, P.M. Haggie, and A.S. Verkman. 2004. In vivo measurement of brain extracellular space diffusion by cortical surface photobleaching. J. Neurosci. 24: 8049-8056. http://dx.doi.org/10.1523/JNEUROSCI.2294-04.2004
7. Binder, D.K., X. Yao, Z. Zador, T.J. Sick, A.S. Verkman, and G.T. Manley. 2006. Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia. 53:631-636. http://dx.doi.org/10.1002/glia.20318
8. Chen, K.C., and C. Nicholson. 2000. Spatial buffering of potassium ions in brain extracellular space. Biophys. J. 78:2776-2797. http://dx.doi.org/10.1016/S0006-3495(00)76822-6
9. Chever, O., B. Djukic, K.D. McCarthy, and F. Amzica. 2010. Implication of Kir4.1 channel in excess potassium clearance: an in vivo study on anesthetized glial-conditional Kir4.1 knock-out mice. J. Neurosci. 30:15769-15777. http://dx.doi.org/10.1523/JNEUROSCI.2078-10.2010
10. Chow, S.Y., Y.C. Yen-Chow, H.S. White, L. Hertz, and D.M. Woodbury. 1991. Effects of potassium on the anion and cation contents of primary cultures of mouse astrocytes and neurons. Neurochem. Res. 16:1275-1283. http://dx.doi.org/10.1007/BF00966658
11. + in rat hippocampus. J. Neurophysiol. 87:87-102.
12. - concentration in relation to changes in the size of the extracellular space. Exp. Brain Res. 46:73-84. http://dx.doi.org/10.1007/BF00238100
13. Dix, J.A., and A.S. Verkman. 2008. Crowding effects on diffusion in solutions and cells. Annu Rev Biophys. 37:247-263. http://dx.doi.org/10.1146/annurev.biophys.37.032807.125824
14. Djukic, B., K.B. Casper, B.D. Philpot, L.S. Chin, and K.D. McCarthy. 2007. Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J. Neurosci. 27:11354-11365. http://dx.doi.org/10.1523/JNEUROSCI.0723-07.2007
15. + homeostasis in the human epileptogenic hippocampus. Proc. Natl. Acad. Sci. USA. 102:1193-1198. http://dx.doi.org/10.1073/pnas.0409308102
16. Eilert-Olsen, M., N.N. Haj-Yasein, G.F. Vindedal, R. Enger, G.A. Gundersen, E.H. Hoddevik, P.H. Petersen, F.M. Haug, O. Skare, M.E. Adams, et al. 2012. Deletion of aquaporin-4 changes the perivascular glial protein scaffold without disrupting the brain endothelial barrier. Glia. 60:432-440. http://dx.doi.org/10.1002/glia.22277
17. Fenstermacher, J., and T. Kaye. 1988. Drug "diffusion" within the brain. Ann. N. Y. Acad. Sci. 531:29-39. http://dx.doi.org/10.1111/j.1749-6632.1988.tb31809.x
18. Frigeri, A., M.A. Gropper, C.W. Turck, and A.S. Verkman. 1995. Immunolocalization of the mercurial-insensitive water channel and glycerol intrinsic protein in epithelial cell plasma membranes. Proc. Natl. Acad. Sci. USA. 92:4328-4331. http://dx.doi.org/10.1073/pnas.92.10.4328
19. + pump in epilepsy. Ann. Neurol. 16(Suppl):S128-S134. http://dx.doi.org/10.1002/ana.410160719
20. + spatial buffering contributes to the epileptogenic effect of mutations in the human Kir4.1 gene (KCNJ10). Glia. 59:1635-1642. http://dx.doi.org/10.1002/glia.21205
21. Haj-Yasein, N.N., G.F. Vindedal, M. Eilert-Olsen, G.A. Gundersen, O. Skare, P. Laake, A. Klungland, A.E. Thorén, J.M. Burkhardt, O.P. Ottersen, and E.A. Nagelhus. 2011b. Glial-conditional deletion of aquaporin-4 (Aqp4) reduces blood-brain water uptake and confers barrier function on perivascular astrocyte endfeet. Proc. Natl. Acad. Sci. USA. 108:17815-17820. http://dx.doi.org/10.1073/pnas.1110655108
22. Haj-Yasein, N.N., V. Jensen, I. Østby, S.W. Omholt, J. Voipio, K. Kaila, O.P. Ottersen, O. Hvalby, and E.A. Nagelhus. 2012. Aquaporin-4 regulates extracellular space volume dynamics during high-frequency synaptic stimulation: a gene deletion study in mouse hippocampus. Glia. 60:867-874. http://dx.doi.org/10.1002/glia.22319
23. Jauch, R., O. Windmüller, T.N. Lehmann, U. Heinemann, and S. Gabriel. 2002. Effects of barium, furosemide, ouabaine and 4,4'-diisothiocyanatostilbene-2,2'-disulfonic acid (DIDS) on ionophoretically-induced changes in extracellular potassium concentration in hippocampal slices from rats and from patients with epilepsy. Brain Res. 925:18-27. http://dx.doi.org/10.1016/S0006-8993(01)03254-1
24. Li, J., and A.S. Verkman. 2001. Impaired hearing in mice lacking aquaporin-4 water channels. J. Biol. Chem. 276:31233-31237. http://dx.doi.org/10.1074/jbc.M104368200
25. Li, J., R.V. Patil, and A.S. Verkman. 2002. Mildly abnormal retinal function in transgenic mice without Müller cell aquaporin-4 water channels. Invest. Ophthalmol. Vis. Sci. 43:573-579.
26. Lu, D.C., H. Zhang, Z. Zador, and A.S. Verkman. 2008. Impaired olfaction in mice lacking aquaporin-4 water channels. FASEB J. 22:3216-3223. http://dx.doi.org/10.1096/fj.07-104836
27. + uptake via NKCC1 and swelling of astrocytes. Glia. 37:114-123. http://dx.doi.org/10.1002/glia.10023
28. Manley, G.T., M. Fujimura, T. Ma, N. Noshita, F. Filiz, A.W. Bollen, P. Chan, and A.S. Verkman. 2000. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat. Med. 6:159-163. http://dx.doi.org/10.1038/72256
29. Meeks, J.P., and S. Mennerick. 2007. Astrocyte membrane responses and potassium accumulation during neuronal activity. Hippocampus. 17:1100-1108. http://dx.doi.org/10.1002/hipo.20344
30. + siphoning and water transport in rat retinal Müller cells is mediated by a coenrichment of Kir4.1 and AQP4 in specific membrane domains. Glia. 26:47-54. http://dx.doi.org/10.1002/(SICI)1098-1136(199903)26:1<47::AID-GLIA5>3.0.CO;2-5
31. Nagelhus, E.A., T.M. Mathiisen, and O.P. Ottersen. 2004. Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience. 129:905-913. http://dx.doi.org/10.1016/j.neuroscience.2004.08.053
32. Nicholson, C., and E. Syková. 1998. Extracellular space structure revealed by diffusion analysis. Trends Neurosci. 21:207-215. http://dx.doi.org/10.1016/S0166-2236(98)01261-2
33. Nielsen, S., E.A. Nagelhus, M. Amiry-Moghaddam, C. Bourque, P. Agre, and O.P. Ottersen. 1997. Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci. 17:171-180.
34. Odette, L.L., and E.A. Newman. 1988. Model of potassium dynamics in the central nervous system. Glia. 1:198-210. http://dx.doi.org/10.1002/glia.440010305
35. Østby, I., L. Øyehaug, G.T. Einevoll, E.A. Nagelhus, E. Plahte, T. Zeuthen, C.M. Lloyd, O.P. Ottersen, and S.W. Omholt. 2009. Astrocytic mechanisms explaining neural-activity-induced shrinkage of extraneuronal space. PLOS Comput. Biol. 5:e1000272. http://dx.doi.org/10.1371/journal.pcbi.1000272
36. +-sensing fluorescent indicator. Nat. Methods. 2:825-827. http://dx.doi.org/10.1038/nmeth801
37. Papadopoulos, M.C., G.T. Manley, S. Krishna, and A.S. Verkman. 2004. Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J. 18:1291-1293.
38. Ransom, B.R., C.L. Yamate, and B.W. Connors. 1985. Activity-dependent shrinkage of extracellular space in rat optic nerve: a developmental study. J. Neurosci. 5:532-535.
39. + pumps. J. Physiol. 522:427-442. http://dx.doi.org/10.1111/j.1469-7793.2000.00427.x
40. Ruiz-Ederra, J., H. Zhang, and A.S. Verkman. 2007. Evidence against functional interaction between aquaporin-4 water channels and Kir4.1 potassium channels in retinal Müller cells. J. Biol. Chem. 282:21866-21872. http://dx.doi.org/10.1074/jbc.M703236200
41. Saadoun, S., M.C. Papadopoulos, H. Watanabe, D. Yan, G.T. Manley, and A.S. Verkman. 2005. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J. Cell Sci. 118:5691-5698. http://dx.doi.org/10.1242/jcs.02680
42. Sick, T.J., E.L. Solow, and E.L. Roberts Jr. 1987. Extracellular potassium ion activity and electrophysiology in the hippocampal slice: paradoxical recovery of synaptic transmission during anoxia. Brain Res. 418:227-234. http://dx.doi.org/10.1016/0006-8993(87)90090-4
43. Solenov, E., H. Watanabe, G.T. Manley, and A.S. Verkman. 2004. Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. Am. J. Physiol. Cell Physiol. 286:C426-C432. http://dx.doi.org/10.1152/ajpcell.00298.2003
44. Somjen, G.G. 1979. Extracellular potassium in the mammalian central nervous system. Annu. Rev. Physiol. 41:159-177. http://dx.doi.org/10.1146/annurev.ph.41.030179.001111
45. + buffering and gap junction coupling in the hippocampus. Glia. 59:973-980. http://dx.doi.org/10.1002/glia.21169
46. - cotransporter-null mice exhibit absence of swelling and decrease in EAA release. Am. J. Physiol. Cell Physiol. 282:C1147-C1160.
47. Syková, E., and C. Nicholson. 2008. Diffusion in brain extracellular space. Physiol. Rev. 88:1277-1340. http://dx.doi.org/10.1152/physrev.00027.2007
48. Takumi, Y., E.A. Nagelhus, J. Eidet, A. Matsubara, S. Usami, H. Shinkawa, S. Nielsen, and O.P. Ottersen. 1998. Select types of supporting cell in the inner ear express aquaporin-4 water channel protein. Eur. J. Neurosci. 10:3584-3595. http://dx.doi.org/10.1046/j.1460-9568.1998.00360.x
49. Thiagarajah, J.R., M.C. Papadopoulos, and A.S. Verkman. 2005. Noninvasive early detection of brain edema in mice by near-infrared light scattering. J. Neurosci. Res. 80:293-299. http://dx.doi.org/10.1002/jnr.20439
50. Truc, O., J.P. Ollivier, and L.O. Nilsson. 2000. Numerical simulation of multi-species diffusion. Materials and Structures. 33:566-573. http://dx.doi.org/10.1007/BF02480537
51. Verkman, A.S. 2012. Aquaporins in clinical medicine. Annu. Rev. Med. 63:303-316. http://dx.doi.org/10.1146/annurev-med-043010-193843
52. Verkman, A.S., J. Ratelade, A. Rossi, H. Zhang, and L. Tradtrantip. 2011. Aquaporin-4: orthogonal array assembly, CNS functions, and role in neuromyelitis optica. Acta Pharmacol. Sin. 32:702-710. http://dx.doi.org/10.1038/aps.2011.27
53. Walz, W., and L. Hertz. 1982. Ouabain-sensitive and ouabain-resistant net uptake of potassium into astrocytes and neurons in primary cultures. J. Neurochem. 39:70-77. http://dx.doi.org/10.1111/j.1471-4159.1982.tb04702.x
54. Walz, W., and L. Hertz. 1983. Intracellular ion changes of astrocytes in response to extracellular potassium. J. Neurosci. Res. 10:411-423. http://dx.doi.org/10.1002/jnr.490100408
55. + levels by astrocytes. Brain Res. 343:44-51. http:// dx.doi.org/10.1016/0006-8993(85)91156-4
56. Xu, X., and C.J. Karwoski. 1994. Current source density analysis of retinal field potentials. II. Pharmacological analysis of the b-wave and M-wave. J. Neurophysiol. 72:96-105.
57. Yao, X., S. Hrabetová, C. Nicholson, and G.T. Manley. 2008. Aquaporin-4-deficient mice have increased extracellular space without tortuosity change. J. Neurosci. 28:5460-5464. http://dx.doi.org/10.1523/JNEUROSCI.0257-08.2008
58. Zador, Z., M. Magzoub, S. Jin, G.T. Manley, M.C. Papadopoulos, and A.S. Verkman. 2008. Microfiberoptic fluorescence photobleaching reveals size-dependent macromolecule diffusion in extracellular space deep in brain. FASEB J. 22:870-879. http://dx.doi.org/10.1096/fj.07-9468com
59. Zeng, X.N., X.L. Sun, L. Gao, Y. Fan, J.H. Ding, and G. Hu. 2007. Aquaporin-4 deficiency down-regulates glutamate uptake and GLT-1 expression in astrocytes. Mol. Cell. Neurosci. 34:34-39. http://dx.doi.org/10.1016/j.mcn.2006.09.008
60. + channel function in brain glial cells. Mol. Cell. Neurosci. 37:1-10. http://dx.doi.org/10.1016/j.mcn.2007.08.007
61. Zhang, H., and A.S. Verkman. 2010. Microfiberoptic measurement of extracellular space volume in brain and tumor slices based on fluorescent dye partitioning. Biophys. J. 99:1284-1291. http://dx.doi.org/10.1016/j.bpj.2010.06.023