Structural insights into eukaryotic aquaporin regulation

FEBS Letters

Volumn 584, Issue 12, 2010, Pages 2580-2588

  Törnroth Horsefield, Susanna ^a   Hedfalk, Kristina ^a   Fischer, Gerhard ^a   Lindkvist Petersson, Karin ^a   Neutze, Richard ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Aquaporin; Membrane protein structural biology; X ray diffraction

Indexed keywords

AQUAPORIN; AQUAPORIN 1; AQUAPORIN 2; AQUAPORIN 4; AQUAPORIN 5; AQUAPORIN 8;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE TRANSPORT; CHANNEL GATING; CRYSTAL STRUCTURE; HUMAN; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; WATER TRANSPORT;

ANIMALS; AQUAPORINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; EUKARYOTA; HOMEOSTASIS; HUMANS; ION CHANNEL GATING; MODELS, MOLECULAR; PHOSPHORYLATION; WATER;

EUKARYOTA;

EID: 77953578957     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.04.037     Document Type: Review

References (93)

1. Preston G.M., Agre P. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc. Natl. Acad. Sci. USA 1991, 88:11110-11114.
2. Preston G.M., Carroll T.P., Guggino W.B., Agre P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 1992, 256:385-387.
3. Borgnia M., Nielsen S., Engel A., Agre P. Cellular and molecular biology of the aquaporin water channels. Annu. Rev. Biochem. 1999, 68:425-458.
4. Liu Z., Shen J., Carbrey J.M., Mukhopadhyay R., Agre P., Rosen B.P. Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc. Natl. Acad. Sci. USA 2002, 99:6053-6058.
5. Blank M.E., Ehmke H. Aquaporin-1 and HCO3(-)-Cl-transporter-mediated transport of CO2 across the human erythrocyte membrane. J. Physiol. 2003, 550:419-429.
6. Uehlein N., Lovisolo C., Siefritz F., Kaldenhoff R. The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 2003, 425:734-737.
7. Tanghe A., Van Dijck P., Thevelein J.M. Why do microorganisms have aquaporins?. Trends Microbiol. 2006, 14:78-85.
8. Chen Y.C., Cadnapaphornchai M.A., Schrier R.W. Clinical update on renal aquaporins. Biol. Cell 2005, 97:357-371.
9. Fruhbeck G. Obesity: aquaporin enters the picture. Nature 2005, 438:436-437.
10. Amiry-Moghaddam M., Ottersen O.P. The molecular basis of water transport in the brain. Nat. Rev. Neurosci. 2003, 4:991-1001.
11. Nejsum L.N., et al. Functional requirement of aquaporin-5 in plasma membranes of sweat glands. Proc. Natl. Acad. Sci. USA 2002, 99:511-516.
12. Fabra M., Raldua D., Power D.M., Deen P.M., Cerda J. Marine fish egg hydration is aquaporin-mediated. Science 2005, 307:545.
13. Maurel C., Javot H., Lauvergeat V., Gerbeau P., Tournaire C., Santoni V., Heyes J. Molecular physiology of aquaporins in plants. Int. Rev. Cytol. 2002, 215:105-148.
14. Azad A.K., Katsuhara M., Sawa Y., Ishikawa T., Shibata H. Characterization of four plasma membrane aquaporins in tulip petals: a putative homolog is regulated by phosphorylation. Plant Cell Physiol. 2008, 49:1196-1208.
15. Saadoun S., Papadopoulos M.C., Hara-Chikuma M., Verkman A.S. Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 2005, 434:786-792.
16. Promeneur D., Liu Y., Maciel J., Agre P., King L.S., Kumar N. Aquaglyceroporin PbAQP during intraerythrocytic development of the malaria parasite Plasmodium berghei. Proc. Natl. Acad. Sci. USA 2007, 104:2211-2216.
17. Manley G.T., Fujimura M., Ma T., Noshita N., Filiz F., Bollen A.W., Chan P., Verkman A.S. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat. Med. 2000, 6:159-163.
18. King L.S., Kozono D., Agre P. From structure to disease: the evolving tale of aquaporin biology. Nat. Rev. Mol. Cell Biol. 2004, 5:687-698.
19. Morishita Y., Sakube Y., Sasaki S., Ishibashi K. Molecular mechanisms and drug development in aquaporin water channel diseases: aquaporin superfamily (superaquaporins): expansion of aquaporins restricted to multicellular organisms. J. Pharmacol. Sci. 2004, 96:276-279.
20. Castle N.A. Aquaporins as targets for drug discovery. Drug Discov. Today 2005, 10:485-493.
21. Murata K., Mitsuoka K., Hirai T., Walz T., Agre P., Heymann J.B., Engel A., Fujiyoshi Y. Structural determinants of water permeation through aquaporin-1. Nature 2000, 407:599-605.
22. Fu D., Libson A., Miercke L.J., Weitzman C., Nollert P., Krucinski J., Stroud R.M. Structure of a glycerol-conducting channel and the basis for its selectivity. Science 2000, 290:481-486.
23. Jung J.S., Preston G.M., Smith B.L., Guggino W.B., Agre P. Molecular structure of the water channel through aquaporin CHIP. The hourglass model. J. Biol. Chem. 1994, 269:14648-14654.
24. de Groot B.L., Grubmuller H. Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science 2001, 294:2353-2357.
25. Tajkhorshid E., Nollert P., Jensen M.O., Miercke L.J., O'Connell J., Stroud R.M., Schulten K. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 2002, 296:525-530.
26. de Groot B.L., Grubmuller H. The dynamics and energetics of water permeation and proton exclusion in aquaporins. Curr. Opin. Struct. Biol. 2005, 15:176-183.
27. Savage D.F., Egea P.F., Robles-Colmenares Y., O'Connell J.D., Stroud R.M. Architecture and selectivity in aquaporins: 2.5Å X-ray structure of aquaporin Z. PLoS Biol. 2003, 1:E72.
28. Wang Y., Schulten K., Tajkhorshid E. What makes an aquaporin a glycerol channel: a comparative study of AqpZ and GlpF. Structure 2005, 13:1107-1118.
29. Fushimi K., Sasaki S., Marumo F. Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel. J. Biol. Chem. 1997, 272:14800-14802.
30. Takata K., Matsuzaki T., Tajika Y. Aquaporins: water channel proteins of the cell membrane. Prog. Histochem. Cytochem. 2004, 39:1-83.
31. Prak S., Hem S., Boudet J., Viennois G., Sommerer N., Rossignol M., Maurel C., Santoni V. Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins: role in subcellular trafficking of AtPIP2;1 in response to salt stress. Mol. Cell Proteomics 2008, 7:1019-1030.
32. Hoffert J.D., et al. Vasopressin-stimulated increase in phosphorylation at Ser269 potentiates plasma membrane retention of aquaporin-2. J. Biol. Chem. 2008, 283:24617-24627.
33. Karabasil M.R., Hasegawa T., Azlina A., Purwanti N., Purevjav J., Yao C., Akamatsu T., Hosoi K. Trafficking of GFP-AQP5 chimeric proteins conferred with unphosphorylated amino acids at their PKA-target motif ((152)SRRTS) in MDCK-II cells. J. Med. Invest. 2009, 56:55-63.
34. Woo J., et al. Membrane trafficking of AQP5 and cAMP dependent phosphorylation in bronchial epithelium. Biochem. Biophys. Res. Commun. 2008, 366:321-327.
35. Nemeth-Cahalan K.L., Kalman K., Hall J.E. Molecular basis of pH and Ca2+ regulation of aquaporin water permeability. J. Gen. Physiol. 2004, 123:573-580.
36. Zelenina M., Bondar A.A., Zelenin S., Aperia A. Nickel and extracellular acidification inhibit the water permeability of human aquaporin-3 in lung epithelial cells. J. Biol. Chem. 2003, 278:30037-30043.
37. Tournaire-Roux C., Sutka M., Gabot H., Gout E., Gerbeau P., Luu D., Bligny R., Maurel C. Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 2003, 425:393-397.
38. Johansson I., Karlsson M., Shukla V.K., Chrispeels M.J., Larsson C., Kjellbom P. Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 1998, 10:451-459.
39. Zelenina M., Tritto S., Bondar A.A., Zelenin S., Aperia A. Copper inhibits the water and glycerol permeability of aquaporin-3. J. Biol. Chem. 2004, 279:51939-51943.
40. Gunnarson E., Axehult G., Baturina G., Zelenin S., Zelenina M., Aperia A. Lead induces increased water permeability in astrocytes expressing aquaporin 4. Neuroscience 2005, 136:105-114.
41. Tamas M.J., et al. A short regulatory domain restricts glycerol transport through yeast Fps1p. J. Biol. Chem. 2003, 278:6337-6345.
42. Johansson I., Larsson C., Ek B., Kjellbom P. The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2+ and apoplastic water potential. Plant Cell 1996, 8:1181-1191.
43. Conner M.T., Conner A.C., Brown J.E., Bill R.M. Membrane trafficking of aquaporin 1 is mediated by protein kinase C via microtubules and regulated by tonicity. Biochemistry 2010, 49:821-823.
44. Törnroth-Horsefield S., Wang Y., Hedfalk K., Johanson U., Karlsson M., Tajkhorshid E., Neutze R., Kjellbom P. Structural mechanism of plant aquaporin gating. Nature 2006, 439:688-694.
45. Fischer G., et al. Crystal structure of a yeast aquaporin at 1.15Å reveals a novel gating mechanism. PLoS Biol. 2009, 7:e1000130.
46. Ho J.D., Yeh R., Sandstrom A., Chorny I., Harries W.E., Robbins R.A., Miercke L.J., Stroud R.M. Crystal structure of human aquaporin 4 at 1.8A and its mechanism of conductance. Proc. Natl. Acad. Sci. USA 2009, 106:7437-7442.
47. 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.
48. Gonen T., Cheng Y., Sliz P., Hiroaki Y., Fujiyoshi Y., Harrison S.C., Walz T. Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 2005, 438:633-638.
49. Harries W.E., Akhavan D., Miercke L.J., Khademi S., Stroud R.M. The channel architecture of aquaporin 0 at a 2.2-A resolution. Proc. Natl. Acad. Sci. USA 2004, 101:14045-14050.
50. Sui H., Han B.G., Lee J.K., Walian P., Jap B.K. Structural basis of water-specific transport through the AQP1 water channel. Nature 2001, 414:872-878.
51. Hiroaki Y., et al. Implications of the aquaporin-4 structure on array formation and cell adhesion. J. Mol. Biol. 2006, 355:628-639.
52. Tani K., Mitsuma T., Hiroaki Y., Kamegawa A., Nishikawa K., Tanimura Y., Fujiyoshi Y. Mechanism of aquaporin-4's fast and highly selective water conduction and proton exclusion. J. Mol. Biol. 2009, 389:694-706.
53. Horsefield R., et al. High-resolution X-ray structure of human aquaporin 5. Proc. Natl. Acad. Sci. USA 2008, 105:13327-13332.
54. Jiang J., Daniels B.V., Fu D. Crystal structure of AqpZ tetramer reveals two distinct Arg-189 conformations associated with water permeation through the narrowest constriction of the water-conducting channel. J. Biol. Chem. 2006, 281:454-460.
55. Lee J.K., Kozono D., Remis J., Kitagawa Y., Agre P., Stroud R.M. Structural basis for conductance by the archaeal aquaporin AqpM at 1.68A. Proc. Natl. Acad. Sci. USA 2005, 102:18932-18937.
56. Newby Z.E.R., O'Connell J., Robles-Colmenares Y., Khademi S., Miercke L.J., Stroud R.M. Crystal structure of the aquaglyceroporin PfAQP from the malarial parasite Plasmodium falciparum. Nat. Struct. Mol. Biol. 2008, 15:619-625.
57. Alleva K., Niemietz C.M., Sutka M., Maurel C., Parisi M., Tyerman S.D., Amodeo G. Plasma membrane of beta vulgaris storage root shows high water channel activity regulated by cytoplasmic pH and a dual range of calcium concentrations. J. Exp. Bot. 2006, 57:609-621.
58. Verdoucq L., Grondin A., Maurel C. Structure-function analysis of plant aquaporin AtPIP2;1 gating by divalent cations and protons. Biochem. J. 2008, 415:409-416.
59. Chen T.H., Murata N. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr. Opin. Plant Biol. 2002, 5:250-257.
60. Holbrook N.M., Zwieniecki M.A. Plant biology: water gate. Nature 2003, 425:361.
61. Kim Y.X., Steudle E. Gating of aquaporins by light and reactive oxygen species in leaf parenchyma cells of the midrib of Zea mays. J. Exp. Bot. 2009, 60:547-556.
62. Tamas M.J., et al. Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation. Mol. Microbiol. 1999, 31:1087-1104.
63. Hedfalk K., et al. A regulatory domain in the C-terminal extension of the yeast glycerol channel Fps1p. J. Biol. Chem. 2004, 279:14954-14960.
64. Costello M.J., McIntosh T.J., Robertson J.D. Distribution of gap junctions and square array junctions in the mammalian lens. Invest. Ophthalmol. Vis. Sci. 1989, 30:975-989.
65. Francis P., Berry V., Bhattacharya S., Moore A. Congenital progressive polymorphic cataract caused by a mutation in the major intrinsic protein of the lens, MIP (AQP0). Brit. J. Ophthalmol. 2000, 84:1376-1379.
66. Geyer D.D., et al. Novel single-base deletional mutation in major intrinsic protein (MIP) in autosomal dominant cataract. Am. J. Ophthalmol. 2006, 141:761-763.
67. Chandy G., Zampighi G.A., Kreman M., Hall J.E. Comparison of the water transporting properties of MIP and AQP1. J. Membr. Biol. 1997, 159:29-39.
68. Nemeth-Cahalan K.L., Hall J.E. pH and calcium regulate the water permeability of aquaporin 0. J. Biol. Chem. 2000, 275:6777-6782.
69. Zelenina M., Zelenin S., Bondar A.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:F309-F318.
70. Deen P.M., Verdijk M.A., Knoers N.V., Wieringa B., Monnens L.A., van Os C.H., van Oost B.A. Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine. Science 1994, 264:92-95.
71. Knepper M.A., Inoue T. Regulation of aquaporin-2 water channel trafficking by vasopressin. Curr. Opin. Cell Biol. 1997, 9:560-564.
72. Nedvetsky P.I., Tamma G., Beulshausen S., Valenti G., Rosenthal W., Klussmann E. Regulation of aquaporin-2 trafficking. Handbook Exp. Pharmacol. 2009, 133-157.
73. Han Z., Patil R.V. Protein kinase A-dependent phosphorylation of aquaporin-1. Biochem. Biophys. Res. Commun. 2000, 273:328-332.
74. de Mattia F., Savelkoul P.J., Kamsteeg E.J., Konings I.B., van der Sluijs P., Mallmann R., Oksche A., Deen P.M. Lack of arginine vasopressin-induced phosphorylation of aquaporin-2 mutant AQP2-R254L explains dominant nephrogenic diabetes insipidus. J. Am. Soc. Nephrol. 2005, 16:2872-2880.
75. McDill B.W., Li S.Z., Kovach P.A., Ding L., Chen F. Congenital progressive hydronephrosis (cph) is caused by an S256L mutation in aquaporin-2 that affects its phosphorylation and apical membrane accumulation. Proc. Natl. Acad. Sci. USA 2006, 103:6952-6957.
76. Yang F., Kawedia J.D., Menon A.G. Cyclic AMP regulates aquaporin 5 expression at both the transcriptional and post-transcriptional levels through a protein-kinase pathway. J. Biol. Chem. 2003, 278:2775-2779.
77. Ishikawa Y., et al. Identification of AQP5 in lipid rafts and its translocation to apical membranes by activation of M3 mAChRs in interlobular ducts of rat parotid gland. Am. J. Physiol. Cell Physiol. 2005, 289:C1303-C1311.
78. Kosugi-Tanaka C., Li X., Yao C., Akamatsu T., Kanamori N., Hosoi K. Protein kinase A-regulated membrane trafficking of a green fluorescent protein-aquaporin 5 chimera in MDCK cells. Biochim. Biophys. Acta 2006, 1763:337-344.
79. Garcia F., Kierbel A., Larocca M.C., Gradilone S.A., Splinter P., Larusso N.F., Marinelli R.A. The water channel aquaporin-8 is mainly intracellular in rat hepatocytes, and its plasma membrane insertion is stimulated by cyclic AMP. J. Biol. Chem. 2001, 276:12147-12152.
80. Nyblom M., et al. Structural and functional analysis of SoPIP2;1 mutants adds insight into plant aquaporin gating. J. Mol. Biol. 2009, 387:653-668.
81. Chang G., Spencer R.H., Lee A.T., Barclay M.T., Rees D.C. Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 1998, 282:2220-2226.
82. Soveral G., Madeira A., Loureiro-Dias M.C., Moura T.F. Membrane tension regulates water transport in yeast. Biochim. Biophys. Acta 2008, 1778:2573-2579.
83. Wan X., Steudle E., Hartung W. Gating of water channels (aquaporins) in cortical cells of young corn roots by mechanical stimuli (pressure pulses): effects of ABA and of HgCl2. J. Exp. Bot. 2004, 55:411-422.
84. Hedfalk K., Tornroth-Horsefield S., Nyblom M., Johanson U., Kjellbom P., Neutze R. Aquaporin gating. Curr. Opin. Struct. Biol. 2006, 16:447-456.
85. Van Wilder V., Miecielica U., Degand H., Derua R., Waelkens E., Chaumont F. Maize plasma membrane aquaporins belonging to the PIP1 and PIP2 subgroups are in vivo phosphorylated. Plant Cell Physiol. 2008, 49:1364-1377.
86. Gunnarson E., et al. Identification of a molecular target for glutamate regulation of astrocyte water permeability. Glia 2008, 56:587-596.
87. Illarionova, N.B., Gunnarson, E., Li, Y., Brismar, H., Bondar, A., Zelenin, S. and Aperia, A. (2009) Functional and molecular interactions between aquaporins and Na,K-ATPase. Neuroscience, in press [Epub ahead of print].
88. Thorsen M., et al. The MAPK Hog1p modulates Fps1p-dependent arsenite uptake and tolerance in yeast. Mol. Biol. Cell 2006, 17:4400-4410.
89. Noda Y., Sasaki S. Trafficking mechanism of water channel aquaporin-2. Biol. Cell 2005, 97:885-892.
90. Schenk A.D., Werten P.J., Scheuring S., de Groot B.L., Muller S.A., Stahlberg H., Philippsen A., Engel A. The 4.5A structure of human AQP2. J. Mol. Biol. 2005, 350:278-289.
91. Fotiadis D., Suda K., Tittmann P., Jeno P., Philippsen A., Muller D.J., Gross H., Engel A. Identification and structure of a putative Ca2+-binding domain at the C terminus of AQP1. J. Mol. Biol. 2002, 318:1381-1394.
92. Beitz E., Pavlovic-Djuranovic S., Yasui M., Agre P., Schultz J.E. Molecular dissection of water and glycerol permeability of the aquaglyceroporin from Plasmodium falciparum by mutational analysis. Proc. Natl. Acad. Sci. USA 2004, 101:1153-1158.
93. Oberg F., Ekvall M., Nyblom M., Backmark A., Neutze R., Hedfalk K. Insight into factors directing high production of eukaryotic membrane proteins; production of 13 human AQPs in Pichia pastoris. Mol. Membr. Biol. 2009, 26:215-227.