Differential Water Permeability and Regulation of Three Aquaporin 4 Isoforms

Overview

Journal Cell Mol Life Sci

Publisher Springer

Specialty Biology

Date 2009 Dec 17

PMID 20013023

Citations 52

Authors

Robert A Fenton

Hanne B Moeller

Marina Zelenina

Marteinn T Snaebjornsson

Torgeir Holen

Nanna MacAulay

Affiliations

Soon will be listed here.

Abstract

Aquaporin 4 (AQP4) is expressed in the perivascular glial endfeet and is an important pathway for water during formation and resolution of brain edema. In this study, we examined the functional properties and relative unit water permeability of three functional isoforms of AQP4 expressed in the brain (M1, M23, Mz). The M23 isoform gave rise to square arrays when expressed in Xenopus laevis oocytes. The relative unit water permeability differed significantly between the isoforms in the order of M1 > Mz > M23. None of the three isoforms were permeable to small osmolytes nor were they affected by changes in external K(+) concentration. Upon protein kinase C (PKC) activation, oocytes expressing the three isoforms demonstrated rapid reduction of water permeability, which correlated with AQP4 internalization. The M23 isoform was more sensitive to PKC regulation than the longer isoforms and was internalized significantly faster. Our results suggest a specific role for square array formation.

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References

Noell S, Fallier-Becker P, Beyer C, Kroger S, Mack A, Wolburg H . Effects of agrin on the expression and distribution of the water channel protein aquaporin-4 and volume regulation in cultured astrocytes. Eur J Neurosci. 2007; 26(8):2109-18. DOI: 10.1111/j.1460-9568.2007.05850.x. View

Fenton R, Brond L, Nielsen S, Praetorius J . Cellular and subcellular distribution of the type-2 vasopressin receptor in the kidney. Am J Physiol Renal Physiol. 2007; 293(3):F748-60. DOI: 10.1152/ajprenal.00316.2006. View

Sorbo J, Moe S, Ottersen O, Holen T . The molecular composition of square arrays. Biochemistry. 2008; 47(8):2631-7. DOI: 10.1021/bi702146k. View

Rash J, Yasumura T, Hudson C, Agre P, Nielsen S . 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. 1998; 95(20):11981-6. PMC: 21751. DOI: 10.1073/pnas.95.20.11981. View

Zeuthen T, Belhage B, Zeuthen E . Water transport by Na+-coupled cotransporters of glucose (SGLT1) and of iodide (NIS). The dependence of substrate size studied at high resolution. J Physiol. 2005; 570(Pt 3):485-99. PMC: 1479871. DOI: 10.1113/jphysiol.2005.100933. View

Amiry-Moghaddam M, Ottersen O . The molecular basis of water transport in the brain. Nat Rev Neurosci. 2003; 4(12):991-1001. DOI: 10.1038/nrn1252. View

Nagelhus E, Horio Y, Inanobe A, Fujita A, Haug F, Nielsen S . Immunogold evidence suggests that coupling of K+ siphoning and water transport in rat retinal Müller cells is mediated by a coenrichment of Kir4.1 and AQP4 in specific membrane domains. Glia. 1999; 26(1):47-54. DOI: 10.1002/(sici)1098-1136(199903)26:1<47::aid-glia5>3.0.co;2-5. View

Zampighi G, Kreman M, Boorer K, Loo D, Bezanilla F, Chandy G . A method for determining the unitary functional capacity of cloned channels and transporters expressed in Xenopus laevis oocytes. J Membr Biol. 1995; 148(1):65-78. DOI: 10.1007/BF00234157. View

Madrid R, Le Maout S, Barrault M, Janvier K, Benichou S, Merot J . Polarized trafficking and surface expression of the AQP4 water channel are coordinated by serial and regulated interactions with different clathrin-adaptor complexes. EMBO J. 2001; 20(24):7008-21. PMC: 125333. DOI: 10.1093/emboj/20.24.7008. View

10.

Zhang H, Verkman A . Aquaporin-4 independent Kir4.1 K+ channel function in brain glial cells. Mol Cell Neurosci. 2007; 37(1):1-10. PMC: 2904300. DOI: 10.1016/j.mcn.2007.08.007. View

11.

Ruiz-Ederra J, Zhang H, Verkman A . Evidence against functional interaction between aquaporin-4 water channels and Kir4.1 potassium channels in retinal Müller cells. J Biol Chem. 2007; 282(30):21866-72. DOI: 10.1074/jbc.M703236200. View

12.

Cuevas P, Gutierrez Diaz J, Dujovny M, Diaz F, Ausman J . Disturbance of plasmalemmal astrocytic assemblies in focal and selective cerebral ischemia. Anat Embryol (Berl). 1985; 172(2):171-5. DOI: 10.1007/BF00319599. View

13.

Kadohira I, Abe Y, Nuriya M, Sano K, Tsuji S, Arimitsu T . Phosphorylation in the C-terminal domain of Aquaporin-4 is required for Golgi transition in primary cultured astrocytes. Biochem Biophys Res Commun. 2008; 377(2):463-468. DOI: 10.1016/j.bbrc.2008.09.155. View

14.

Zeidel M, Nielsen S, Smith B, Ambudkar S, MAUNSBACH A, Agre P . Ultrastructure, pharmacologic inhibition, and transport selectivity of aquaporin channel-forming integral protein in proteoliposomes. Biochemistry. 1994; 33(6):1606-15. DOI: 10.1021/bi00172a042. View

15.

Strand L, Moe S, Solbu T, Vaadal M, Holen T . Roles of aquaporin-4 isoforms and amino acids in square array assembly. Biochemistry. 2009; 48(25):5785-93. DOI: 10.1021/bi802231q. View

16.

Jung J, Bhat R, Preston G, Guggino W, Baraban J, Agre P . Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci U S A. 1994; 91(26):13052-6. PMC: 45579. DOI: 10.1073/pnas.91.26.13052. View

17.

Zelenina M, Zelenin S, Bondar A, Brismar H, Aperia A . Water permeability of aquaporin-4 is decreased by protein kinase C and dopamine. Am J Physiol Renal Physiol. 2002; 283(2):F309-18. DOI: 10.1152/ajprenal.00260.2001. View

18.

Nagelhus E, Mathiisen T, Ottersen O . Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience. 2004; 129(4):905-13. DOI: 10.1016/j.neuroscience.2004.08.053. View

19.

Gunnarson E, Zelenina M, Axehult G, Song Y, Bondar A, Krieger P . Identification of a molecular target for glutamate regulation of astrocyte water permeability. Glia. 2008; 56(6):587-96. DOI: 10.1002/glia.20627. View

20.

Suzuki H, Nishikawa K, Hiroaki Y, Fujiyoshi Y . Formation of aquaporin-4 arrays is inhibited by palmitoylation of N-terminal cysteine residues. Biochim Biophys Acta. 2008; 1778(4):1181-9. DOI: 10.1016/j.bbamem.2007.12.007. View