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Aquaporins: A Family of Highly Regulated Multifunctional Channels

  • Charles Hachez
  • François Chaumont
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 679)

Abstract

Aquaporins (AQPs) were discovered as channels facilitating water movement across cellular membranes. Whereas much of the research has focused on characterizing AQPs with respect to cell water homeostasis, recent discoveries in terms of the transport selectivity of AQP homologs has shed new light on their physiological roles. In fact, whereas some AQPs behave as “strict” water channels, others can conduct a wide range of nonpolar solutes, such as urea or glycerol and even more unconventional permeants, such as the nonpolar gases carbon dioxide and nitric oxide, the polar gas ammonia, the reactive oxygen species hydrogen peroxide and the metalloids antimonite, arsenite, boron and silicon. This suggests that AQPs are also key players in various physiological processes not related to water homeostasis. The function, regulation and biological importance of AQPs in the different kingdoms is reviewed in this chapter, with special emphasis on animal and plant AQPs.

Keywords

Water Permeability Water Channel Intrinsic Protein Major Intrinsic Protein Plasma Membrane Intrinsic Protein 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Stein WD, Danielli JF. Structure and function in red cell permeability. Discussion Faraday Soc 1956; 21:238–251.Google Scholar
  2. 2.
    Benga G. Birth of water channel proteins—the aquaporins. Cell Biol Int 2003; 27:701–709.PubMedGoogle Scholar
  3. 3.
    Ray PM. On the theory of osmotic water movement. Plant Physiol 1960; 35:783–795.PubMedGoogle Scholar
  4. 4.
    Benga G, Popescu O, Pop VI et al. P-(chloromercuri)benzenesulfonate binding by membrane proteins and the inhibition of water transport in human erythrocytes. Biochemistry 1986; 25:1535–1538.PubMedGoogle Scholar
  5. 5.
    Denker B, Smith B, Kuhajda F et al. Identification, purification and partial characterization of a novel mr 28,000 integral membrane protein from erythrocytes and renal tubules. J Biol Chem 1988; 263:15634–15642.PubMedGoogle Scholar
  6. 6.
    Agre P, Saboori AM, Asimos A et al. Purification and partial characterization of the mr 30,000 integral membrane protein associated with the erythrocyte rh(d) antigen. J Biol Chem 1987; 262:17497–17503.PubMedGoogle Scholar
  7. 7.
    Preston GM, 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.PubMedGoogle Scholar
  8. 8.
    Smith BL, Agre P. Erythrocyte mr 28,000 transmembrane protein exists as a multisubunit oligomer similar to channel proteins. J Biol Chem 1991; 266:6407–6415.PubMedGoogle Scholar
  9. 9.
    Preston GM, Carroll TP, Guggino WB et al. Appearance of water channels in xenopus oocytes expressing red cell CHIP28 protein. Science 1992; 256:385–387.PubMedGoogle Scholar
  10. 10.
    Mitsuoka K, Murata K, Walz T et al. The structure of aquaporin-1 at 4.5-a resolution reveals short alpha-helices in the center of the monomer. J Struct Biol 1999; 128:34–43.PubMedGoogle Scholar
  11. 11.
    Murata K, Mitsuoka K, Hirai T et al. Structural determinants of water permeation through aquaporin-1. Nature 2000; 407:599–605.PubMedGoogle Scholar
  12. 12.
    de Groot BL, Grubmüller H. The dynamics and energetics of water permeation and proton exclusion in aquaporins. Current Opinion in Structural Biology, Theory and simulation/Macromolecular assemblages 2005; 15:176–183.Google Scholar
  13. 13.
    Zardoya R. Phylogeny and evolution of the major intrinsic protein family. Biol Cell 2005; 97:397–414.PubMedGoogle Scholar
  14. 14.
    Campbell E, Ball A, Hoppler S et al. Invertebrate aquaporins: A review. J Comp Physiol B 2008; 178:935–955.PubMedGoogle Scholar
  15. 15.
    Gazzarrini S, Kang M, Epimashko S et al. Chlorella virus mt325 encodes water and potassium channels that interact synergistically. Proc Natl Acad Sci USA 2006; 103:5355–5360.PubMedGoogle Scholar
  16. 16.
    Ishibashi K. Aquaporin superfamily with unusual NPA boxes: S-aquaporins (superfamily, SIP-like and subcellular-aquaporins). Cell Mol Biol 2006; 52:20–27.PubMedGoogle Scholar
  17. 17.
    Johanson U, Karlsson M, Johansson I et al. The complete set of genes encoding major intrinsic proteins in arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 2001; 126:1358–1369.PubMedGoogle Scholar
  18. 18.
    Sakurai J, Ishikawa F, Yamaguchi T et al. Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 2005; 46:1568–1577.PubMedGoogle Scholar
  19. 19.
    Chaumont F, Barrieu F, Wojcik E et al. Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 2001; 125:1206–1215.PubMedGoogle Scholar
  20. 20.
    Gustavsson S, Lebrun AS, Norden K et al. A novel plant major intrinsic protein in Physcomitrella patens most similar to bacterial glycerol channels. Plant Physiol 2005; 139:287–295.PubMedGoogle Scholar
  21. 21.
    Danielson JJ, Johanson U. Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 2008; 8.Google Scholar
  22. 22.
    Bienert GP, Schüssler MD, Jahn TP. Metalloids: Essential, beneficial or toxic? Major intrinsic proteins sort it out. Trends Biochem Sci 2008; 33:20–26.PubMedGoogle Scholar
  23. 23.
    Bienert GP, Moller ALB, Kristiansen KA et al. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 2007; 282:1183–1192.PubMedGoogle Scholar
  24. 24.
    Yool AJ. Aquaporins: Multiple roles in the central nervous system. Neuroscientist 2007; 13:470–485.PubMedGoogle Scholar
  25. 25.
    Lee W-K, Thevenod F. A role for mitochondrial aquaporins in cellular life-and-death decisions? Am J Physiol Cell Physiol 2006; 291:195–202.Google Scholar
  26. 26.
    Saadoun S, Papadopoulos MC, Watanabe H et al. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci 2005; 118:5691–5698.PubMedGoogle Scholar
  27. 27.
    Verkman AS. More than just water channels: Unexpected cellular roles of aquaporins. J Cell Sci 2005; 118:3225–3232.PubMedGoogle Scholar
  28. 28.
    Maurel C. Plant aquaporins: Novel functions and regulation properties. FEBS Letters 2007; 581:2227–2236.PubMedGoogle Scholar
  29. 29.
    Uehlein N, Otto B, Hanson DT et al. Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 2008; 20:648–657.PubMedGoogle Scholar
  30. 30.
    Reizer J, Reizer A, Saier MH. The MIP family of integral membrane channel proteins: Sequence comparisons, evolutionary relationships, reconstructed pathway of evolution and proposed functional differentiation of the two repeated halves of the proteins. Crit Rev Biochem Mol Biol 1993; 28:235–257.PubMedGoogle Scholar
  31. 31.
    Zeidel ML, Ambudkar SV, Smith BL et al. Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochemistry 1992; 31:7436–7440.PubMedGoogle Scholar
  32. 32.
    Walz T, Smith BL, Zeidel ML et al. Biologically active two-dimensional crystals of aquaporin chip. J Biol Chem 1994; 269:1583–1586.PubMedGoogle Scholar
  33. 33.
    Daniels MJ, Chrispeels MJ, Yeager M. Projection structure of a plant vacuole membrane aquaporin by electron cryo-crystallography. J Mol Biol 1999; 294:1337–1349.PubMedGoogle Scholar
  34. 34.
    Sui H, Han BG, Lee JK et al. Structural basis of water-specific transport through the AQP1 water channel. Nature 2001; 414:872–878.PubMedGoogle Scholar
  35. 35.
    Tornroth-Horsefield S, Wang Y, Hedfalk K et al. Structural mechanism of plant aquaporin gating. Nature 2006; 439:688–694.PubMedGoogle Scholar
  36. 36.
    Heymann JB, Engel A. Structural clues in the sequences of the aquaporins. J Mol Biol 2000; 295:1039–1053.PubMedGoogle Scholar
  37. 37.
    Kukulski W, Schenk AD, Johanson U et al. The 5Å structure of heterologously expressed plant aquaporin sopip2;1. J Mol Biol 2005; 350:611–616.PubMedGoogle Scholar
  38. 38.
    Hiroaki Y, Tani K, Kamegawa A et al. Implications of the aquaporin-4 structure on array formation and cell adhesion. J Mol Biol 2006; 355:628–639.PubMedGoogle Scholar
  39. 39.
    Gonen T, Sliz P, Kistler J et al. Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 2004; 429:193–197.PubMedGoogle Scholar
  40. 40.
    Schenk AD, Werten PJ, Scheuring S et al. The 4.5 Å structure of human AQP2. J Mol Biol 2005; 350:278–289.PubMedGoogle Scholar
  41. 41.
    Savage DF, Egea PF, Robles-Colmenares Y et al. Architecture and selectivity in aquaporins: 2.5 Å x-ray structure of aquaporin z. PLoS Biol 2003; 1:334–340.Google Scholar
  42. 42.
    Ringler P, Borgnia MJ, Stahlberg H et al. Structure of the water channel AQPz from Escherichia coli revealed by electron crystallography. J Mol Biol 1999; 291:1181–1190.PubMedGoogle Scholar
  43. 43.
    Fu D, Libson A, Miercke LJ et al. Structure of a glycerol-conducting channel and the basis for its selectivity. Science 2000; 290:481–486.PubMedGoogle Scholar
  44. 44.
    Lee JK, Kozono D, Remis J et al. Structural basis for conductance by the archaeal aquaporin aqpm at 1.68 a. Proc Natl Acad Sci USA 2005; 102:18932–18937.PubMedGoogle Scholar
  45. 45.
    Horsefield R, Nordén K, Fellert M et al. High-resolution x-ray structure of human aquaporin 5. Proc Natl Acad Sci USA 2008; 105:13327–13332.PubMedGoogle Scholar
  46. 46.
    Maurel C, Verdoucq L, Luu D-T et al. Plant aquaporins: Membrane channels with multiple integrated functions. Ann Rev Plant Biol 2008; 59:595–624.Google Scholar
  47. 47.
    de Groot BL, Frigato T, Helms V et al. The mechanism of proton exclusion in the aquaporin-1 water channel. J Mol Biol 2003; 333:279–293.PubMedGoogle Scholar
  48. 48.
    Tajkhorshid E, Nollert P, Jensen MO et al. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 2002; 296:525–530.PubMedGoogle Scholar
  49. 49.
    Chakrabarti N, Roux B, Pomes R. Structural determinants of proton blockage in aquaporins. J Mol Biol 2004; 343:493–510.PubMedGoogle Scholar
  50. 50.
    Borgnia M, Nielsen S, Engel A et al. Cellular and molecular biology of the aquaporin water channels. Annu Rev Biochem 1999; 68:425–458.PubMedGoogle Scholar
  51. 51.
    Zelazny E, Borst JW, Muylaert M et al. Fret imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proc Natl Acad Sci USA 2007; 104: 12359–12364.PubMedGoogle Scholar
  52. 52.
    Preston GM, Jung JS, Guggino WB et al. The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel. J Biol Chem 1993; 268:17–20.PubMedGoogle Scholar
  53. 53.
    Verkman AS, Shi LB, Frigeri A et al. Structure and function of kidney water channels. Kidney Int 1995; 48:1069–1081.PubMedGoogle Scholar
  54. 54.
    Németh-Cahalan KL, Froger A, Hall JE. Zinc modulation of water permeability reveals that aquaporin 0 functions as a cooperative tetramer. J Gen Physiol 2007; 130:457–464.PubMedGoogle Scholar
  55. 55.
    Wu B, Beitz E. Aquaporins with selectivity for unconventional permeants. Cell Mol Life Sci 2007; 64:2413–2421.PubMedGoogle Scholar
  56. 56.
    Johansson I, Karlsson M, Johanson U et al. The role of aquaporins in cellular and whole plant water balance. Biochim Biophys Acta 2000; 1465:324–342.PubMedGoogle Scholar
  57. 57.
    Hachez C, Moshelion M, Zelazny E et al. Localization and quantification of plasma membrane aquaporin expression in maize primary root: A clue to understanding their role as cellular plumbers. Plant Mol Biol 2006; 62:305–323.PubMedGoogle Scholar
  58. 58.
    Hara-Chikuma M, Verkman A. Physiological roles of glycerol-transporting aquaporins: The aquaglyceroporins. Cell Mol Life Sci 2006; 63:1386–1392.PubMedGoogle Scholar
  59. 59.
    Liu LH, Ludewig U, Gassert B et al. Urea transport by nitrogen-regulated tonoplast intrinsic proteins in arabidopsis. Plant Physiol 2003; 133:1220–1228.PubMedGoogle Scholar
  60. 60.
    Gerbeau P, Guclu J, Ripoche P et al. Aquaporin nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes. Plant J 1999; 18:577–587.PubMedGoogle Scholar
  61. 61.
    Biela A, Grote K, Otto B et al. The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol. Plant J 1999; 18:565–570.PubMedGoogle Scholar
  62. 62.
    Jahn TP, Moller ALB, Zeuthen T et al. Aquaporin homologues in plants and mammals transport ammonia. FEBS Letters 2004; 574:31–36.PubMedGoogle Scholar
  63. 63.
    Ma JF, Tamai K, Yamaji N et al. A silicon transporter in rice. Nature 2006; 440:688–691.PubMedGoogle Scholar
  64. 64.
    Takano JWM, Ludewig U, Schaaf G et al. The arabidopsis major intrinsic protein NIP5; 1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 2006; 18: 1498–1509.PubMedGoogle Scholar
  65. 65.
    Choi WG, Roberts DM. Arabidopsis NIP2; 1, a major intrinsic protein transporter of lactic acid induced by anoxic stress. J Biol Chem 2007; 282:24209–24218.PubMedGoogle Scholar
  66. 66.
    Flexas J, Ribas-Carbo M, Hanson DT et al. Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. Plant J 2006; 48:427–439.PubMedGoogle Scholar
  67. 67.
    Bienert GP, Schjoerring JK, Jahn TP. Membrane transport of hydrogen peroxide. Biochim Biophys Acta 2006; 1758:994–1003.PubMedGoogle Scholar
  68. 68.
    Fetter K, Van Wilder V, Moshelion M et al. Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 2004; 16:215–228.PubMedGoogle Scholar
  69. 69.
    Van Wilder V, Miecielica U, Degand H et al. Maize plasma membrane aquaporins belonging to the PIP1 and PIP2 subgroups are in vivo phosphorylated. Plant Cell Physiol 2008; 49:1364–1377.PubMedGoogle Scholar
  70. 70.
    Nakhoul NL, Davis BA, Romero MF et al. Effect of expressing the water channel aquaporin-1 on the CO2 permeability of xenopus oocytes. Ame J of Phys-Cell Physiol 1998; 43:543–548.Google Scholar
  71. 71.
    Ma JF, Yamaji N, Mitani N et al. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 2008; 105:9931–9935.PubMedGoogle Scholar
  72. 72.
    Tanaka M, Wallace IS, Takano J et al. NIP6; 1 is a boric acid channel for preferential transport of boron to growing shoot tissues in arabidopsis. Plant Cell 2008; 20:2860–2875.PubMedGoogle Scholar
  73. 73.
    Ramahaleo T, Morillon R, Alexandre J et al. Osmotic water permeability of isolated protoplasts. Modifications during development. Plant Physiol 1999; 119:885–896.PubMedGoogle Scholar
  74. 74.
    Morillon R, Chrispeels MJ. The role of aba and the transpiration stream in the regulation of the osmotic water permeability of leaf cells. Proc Natl Acad Sci USA 2001; 98:14138–14143.PubMedGoogle Scholar
  75. 75.
    Moshelion M, Moran N, Chaumont F. Dynamic changes in the osmotic water permeability of protoplast plasma membrane. Plant Physiol 2004; 135:2301–2317.PubMedGoogle Scholar
  76. 76.
    Kaldenhoff R, Grote K, Zhu JJ et al. Significance of plasmalemma aquaporins for water-transport in Arabidopsis thaliana. Plant J 1998; 14:121–128.PubMedGoogle Scholar
  77. 77.
    Volkov V, Hachez C, Moshelion M et al. Water permeability differs between growing and nongrowing barley leaf tissues. J Exp Bot 2007; 58:377–390.PubMedGoogle Scholar
  78. 78.
    Sommer A, Geist B, Da Ines O et al. Ectopic expression of Arabidopsis thaliana plasma membrane intrinsic protein 2 aquaporins in lily pollen increases the plasma membrane water permeability of grain but not of tube protoplasts. New Phytologist 2008; 180:787–797.PubMedGoogle Scholar
  79. 79.
    Zelazny EM, Miecilica U, Borst JW et al. An n-terminal diacidic motif is required for the trafficking of maize aquaporins ZmPIP2; 4 and ZmPIP2; 5 to the plasma membrane. Plant J 2008; in press.Google Scholar
  80. 80.
    Ohshima Y, Iwasaki I, Suga S et al. Low aquaporin content and low osmotic water permeability of the plasma and vacuolar membranes of a cam plant Graptopetalum paraguayense: Comparison with radish. Plant Cell Physiol 2001; 42:1119–1129.PubMedGoogle Scholar
  81. 81.
    Hubert J-Fo, Duchesne L, Delamarche C et al. Pore selectivity analysis of an aquaglyceroporin by stopped-flow spectrophotometry on bacterial cell suspensions. Biol Cell 2005; 97:675–686.PubMedGoogle Scholar
  82. 82.
    Suga S, Maeshima M. Water channel activity of radish plasma membrane aquaporins heterologously expressed in yeast and their modification by site-directed mutagenesis. Plant Cell Physiol 2004; 45: 823–830.PubMedGoogle Scholar
  83. 83.
    Verdoucq LGA, Maurel C. Structure-function analysis of plant aquaporin AtPIP2; 1 gating by divalent cations and protons. Biochem J 2008; 415:409–416.PubMedGoogle Scholar
  84. 84.
    Steudle E. Pressure probe techniques: Basic principles and application to studies of water and solute relations at the cell tissue and organ level. In: Smith JAC, Griffiths H, eds. Water Deficits: Plant Responses from Cell to Community. Oxford: Bios Scientific Publisher Ltd, 1993:5–36.Google Scholar
  85. 85.
    Steudle E, Murrmann M, Peterson CA. Transport of water and solutes across maize roots modified by puncturing the endodermis—further evidence for the composite transport model of the root. Plant Physiol 1993; 103:335–349.PubMedGoogle Scholar
  86. 86.
    Van der Toorn A, Zemah H, Van As H et al. Developmental changes and water status in tulip bulbs during storage: Visualization by NMR imaging. J Exp Bot 2000; 51:1277–1287.PubMedGoogle Scholar
  87. 87.
    Scheenen TWJ, van Dusschoten D, de Jager PA et al. Quantification of water transport in plants with NMR imaging. J Exp Bot 2000; 51:1751–1759.PubMedGoogle Scholar
  88. 88.
    Köckenberger WDP, De Panfilis C, Santoro D et al. High resolution NMR microscopy of plants and fungi. J Microsc 2004; 214:182–189.PubMedGoogle Scholar
  89. 89.
    Van As H, Lens P. Use of 1h NMR to study transport processes in porous biosystems. J Ind Microbiol Biotechnol 2001; 26:43–52.Google Scholar
  90. 90.
    Javot H, Maurel C. The role of aquaporins in root water uptake. Ann Bot (Lond) 2002; 90:301–313.Google Scholar
  91. 91.
    Abrami L, Berthonaud V, Deen PM et al. Glycerol permeability of mutant aquaporin 1 and other AQP-MIP proteins: Inhibition studies. Pflugers Arch 1996; 431:408–414.PubMedGoogle Scholar
  92. 92.
    Echevarria M, Windhager EE, Frindt G. Selectivity of the renal collecting duct water channel aquaporin-3. J Biol Chem 1996; 271:25079–25082.PubMedGoogle Scholar
  93. 93.
    Dordas C, Chrispeels MJ, Brown PH. Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol 2000; 124:1349–1362.PubMedGoogle Scholar
  94. 94.
    Moshelion M, Becker D, Biela A et al. Plasma membrane aquaporins in the motor cells of Samanea saman: Diurnal and circadian regulation. Plant Cell 2002; 14:727–739.PubMedGoogle Scholar
  95. 95.
    Tournaire-Roux C, Sutka M, Javot H et al. Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 2003; 425:393–397.PubMedGoogle Scholar
  96. 96.
    Deen PM VM, Knoers NV, Wieringa B et al. Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine. Science 1994; 264:92–95.PubMedGoogle Scholar
  97. 97.
    King LS, Kozono D, Agre P. From structure to disease: The evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 2004; 5:687–698.PubMedGoogle Scholar
  98. 98.
    King LS, Yasui M, Agre P. Aquaporins in health and disease. Mol Med Today 2000; 6:60–65.PubMedGoogle Scholar
  99. 99.
    Hachez C, Zelazny E, Chaumont F. Modulating the expression of aquaporin genes in planta: A key to understand their physiological functions? Biochim Biophys Acta 2006; 1758:1142–1156.PubMedGoogle Scholar
  100. 100.
    Verkman A, Hara-Chikuma M, Papadopoulos M. Aquaporins: New players in cancer biology. J Mol Med 2008; 86:523–529.PubMedGoogle Scholar
  101. 101.
    Martre P, Morillon R, Barrieu F et al. Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol 2002; 130:2101–2110.PubMedGoogle Scholar
  102. 102.
    Javot H, Lauvergeat V, Santoni V et al. Role of a single aquaporin isoform in root water uptake. Plant Cell 2003; 15:509–522.PubMedGoogle Scholar
  103. 103.
    Siefritz F, Tyree MT, Lovisolo C et al. PIP1 plasma membrane aquaporins in tobacco: From cellular effects to function in plants. Plant Cell 2002; 14:869–876.PubMedGoogle Scholar
  104. 104.
    Ma S, Quist TM, Ulanov A et al. Loss of TIP1; 1 aquaporin in arabidopsis leads to cell and plant death. Plant J 2004; 40:845–859.PubMedGoogle Scholar
  105. 105.
    Jang JY, Rhee JY, Kim DG et al. Ectopic expression of a foreign aquaporin disrupts the natural expression patterns of endogenous aquaporin genes and alters plant responses to different stress conditions. Plant Cell Physiol 2007; 48:1331–1339.PubMedGoogle Scholar
  106. 106.
    Uehlein N, Lovisolo C, Siefritz F et al. The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 2003; 425:734–737.PubMedGoogle Scholar
  107. 107.
    Missner A, Kugler P, Saparov SM et al. Carbon dioxide transport through membranes. J Biol Chem 2008; 283:25340–25347.PubMedGoogle Scholar
  108. 108.
    Schüssler MD, Bienert GP, Kichey T et al. The effects of the loss of TIP1; 1 and TIP1; 2 aquaporins in Arabidopsis thaliana. The Plant Journal 2008; 56:756–767.PubMedGoogle Scholar
  109. 109.
    Verkman AS. Role of aquaporin water channels in kidney and lung. Am J Med Sci 1998; 316: 310–320.PubMedGoogle Scholar
  110. 110.
    Verkman AS, Matthay MA, Song Y. Aquaporin water channels and lung physiology. Am J Physiol Lung Cell Mol Physiol 2000; 278: 867-879.Google Scholar
  111. 111.
    Fraysse LC, Wells B, McCann MC et al. Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells. Biol Cell 2005; 97:519–534.PubMedGoogle Scholar
  112. 112.
    Hachez C, Heinen R, Draye X et al. The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation. Plant Mol Biol 2008; 68:337–353.PubMedGoogle Scholar
  113. 113.
    Alexandersson E, Fraysse L, Sjovall-Larsen S et al. Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 2005; 59:469–484.PubMedGoogle Scholar
  114. 114.
    Chaumont F, Moshelion M, Daniels MJ. Regulation of plant aquaporin activity. Biol Cell 2005; 97:749–764.PubMedGoogle Scholar
  115. 115.
    Maurel C, Chrispeels MJ. Aquaporins. A molecular entry into plant water relations. Plant Physiol 2001; 125:135–138.PubMedGoogle Scholar
  116. 116.
    Cochard H, Venisse JS, Barigah TS et al. Putative role of aquaporins in variable hydraulic conductance of leaves in response to light. Plant Physiol 2007; 143:122–133.PubMedGoogle Scholar
  117. 117.
    Santoni V, Vinh J, Pflieger D et al. A proteomic study reveals novel insights into the diversity of aquaporin forms expressed in the plasma membrane of plant roots. Biochem J 2003; 373:289–296.PubMedGoogle Scholar
  118. 118.
    Takata KM, Tajika T, Ablimit Y et al. Localization and trafficking of aquaporin 2 in the kidney. Histochem Cell Biol 2008; 130:197–209.PubMedGoogle Scholar
  119. 119.
    Boursiac Y, Chen S, Luu DT et al. Early effects of salinity on water transport in arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 2005; 139:790–805.PubMedGoogle Scholar
  120. 120.
    Maurel C, Kado RT, Guern J et al. Phosphorylation regulates the water channel activity of the seedspecific aquaporin alpha-TIP. EMBO J 1995; 14:3028–3035.PubMedGoogle Scholar
  121. 121.
    Zhang W, Zitron E, Homme M et al. Aquaporin-1 channel function is positively regulated by protein kinase C. J Biol Chem 2007; 282:20933–20940.PubMedGoogle Scholar
  122. 122.
    Han Z, Wax MB, Patil RV. Regulation of aquaporin-4 water channels by phorbol ester-dependent protein phosphorylation. J Biol Chem 1998; 273:6001–6004.PubMedGoogle Scholar
  123. 123.
    Johansson I, Karlsson M, Shukla VK et al. Water transport activity of the plasma membrane aquaporin PM28a is regulated by phosphorylation. Plant Cell 1998; 10:451–459.PubMedGoogle Scholar
  124. 124.
    Procino G, Carmosino M, Marin O et al. Ser-256 phosphorylation dynamics of aquaporin 2 during maturation from the endoplasmic reticulum to the vesicular compartment in renal cells. FASEB J 2003; 17: 1886–1888.PubMedGoogle Scholar
  125. 125.
    van Balkom BWM, Savelkoul PJM, Markovich D et al. The role of putative phosphorylation sites in the targeting and shuttling of the aquaporin-2 water channel. J Biol Chem 2002; 277:41473–41479.PubMedGoogle Scholar
  126. 126.
    Weaver CD, Roberts DM. Phosphorylation of nodulin-26 by a calcium-dependent protein-kinase. FASEB J 1991; 5:A426–A426.Google Scholar
  127. 127.
    Johnson KD, Chrispeels MJ. Tonoplast-bound protein-kinase phosphorylates tonoplast intrinsic protein. Plant Physiol 1992; 100:1787–1795.PubMedGoogle Scholar
  128. 128.
    Johansson I, Larsson C, Ek B et al. 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.PubMedGoogle Scholar
  129. 129.
    Santoni V, Verdoucq L, Sommerer N et al. Methylation of aquaporins in plant plasma membrane. Biochem J 2006; 400:189–197.PubMedGoogle Scholar
  130. 130.
    Miao GH, Hong Z, Verma DP. Topology and phosphorylation of soybean nodulin-26, an intrinsic protein of the peribacteroid membrane. J Cell Biol 1992; 118:481–490.PubMedGoogle Scholar
  131. 131.
    Weaver CD, Roberts DM. Determination of the site of phosphorylation of nodulin 26 by the calcium-dependent protein kinase from soybean nodules. Biochemistry 1992; 31:8954–8959.PubMedGoogle Scholar
  132. 132.
    Prak S, Hem S, Boudet J et al. Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins. Role in sub-cellular trafficking of AtPIP2; 1 in response to salt stress. Mol Cell Proteomics 2008; 7:1019–1030.PubMedGoogle Scholar
  133. 133.
    Guenther JF, Chanmanivone N, Galetovic MP et al. Phosphorylation of soybean nodulin 26 on serine 262 enhances water permeability and is regulated developmentally and by osmotic signals. Plant Cell 2003; 15:981–991.PubMedGoogle Scholar
  134. 134.
    Sjövall-Larsen S, Alexandersson E, Johansson I et al. Purification and characterization of two protein kinases acting on the aquaporin SoPIP2; 1. Biochim Biophys Acta 2006; 1758:1157–1164.PubMedGoogle Scholar
  135. 135.
    Yasui M, Hazama A, Kwon TH et al. Rapid gating and anion permeability of an intracellular aquaporin. Nature 1999; 402:184–187.PubMedGoogle Scholar
  136. 136.
    Zeuthen T, Klaerke. Transport of water and glycerol in aquaporin 3 is gated by H+. J Biol Chem1999. 274:21631–21636.Google Scholar
  137. 137.
    Nemeth-Cahalan KL, Hall JE, pH and calcium regulate the water permeability of aquaporin O. J Biol Chem, 2000; 275:6777–6782.PubMedGoogle Scholar
  138. 138.
    Nemeth-Cahalan KL, Kalman K, Hall JE. Molecular basis of pH and Ca2+ regulation of aquaporin water permeability. J Gen Physiol 2004; 123:573–580.PubMedGoogle Scholar
  139. 139.
    Gerbeau P, Amodeo G, Henzler T et al. The water permeability of arabidopsis plasma membrane is regulated by divalent cations and pH. Plant J 2002; 30:71–81.PubMedGoogle Scholar
  140. 140.
    Zeuthen T, Klaerke DA Transport of water and glycerol in aquaporin 3 is gated by h(+). J Biol Chem 1999; 274:21631–21636.PubMedGoogle Scholar
  141. 141.
    Sutka M, Alleva K, Parisi M et al. Tonoplast vesicles of Beta vulgaris storage root show functional aquaporins regulated by protons. Biol Cell 2005; 97:837–846.PubMedGoogle Scholar
  142. 142.
    Hedfalk K, Tornröth-Horsefield S, Nyblom M et al. Aquaporin gating. Current Opinion in Structural Biology Membranes/Engineering and design 2006; 16:447–456.Google Scholar
  143. 143.
    Kalman K, Nemeth-Cahalan KL, Froger A et al. Phosphorylation determines the calmodulin-mediated Ca2+ response and water permeability of AQP0. J Biol Chem 2008; 283:21278–21283.PubMedGoogle Scholar
  144. 144.
    Torvinen M, Marcellino D, Canals M et al. Adenosine A2A receptor and dopamine D3 receptor interactions: Evidence of functional A2A/D3 heteromeric complexes. Mol Pharmacol 2005; 67:400–407.PubMedGoogle Scholar
  145. 145.
    Etxeberria A, Santana-Castro I, Regalado MP et al. Three mechanisms underlie KCNQ2/3 heteromeric potassium m-channel potentiation. J Neurosci 2004; 24:9146–9152.PubMedGoogle Scholar
  146. 146.
    Xicluna J, Lacombe B, Dreyer I et al. Increased functional diversity of plant K+ channels by preferential heteromerization of the shaker-like subunits AKT2 and KAT2. J Biol Chem 2007; 282:486–494.PubMedGoogle Scholar
  147. 147.
    Daram P, Urbach S, Gaymard F et al. Tetramerization of the AKT1 plant potassium channel involves its C-terminal cytoplasmic domain. EMBO J 1997; 16:3455–3463.PubMedGoogle Scholar
  148. 148.
    Liu DT, Tibbs GR, Siegelbaum SA. Subunit stoichiometry of cyclic nucleotide-gated channels and effects of subunit order on channel function. Neuron 1996; 16:983–990.PubMedGoogle Scholar
  149. 149.
    Isacoff EY, Jan YN, Jan LY. Evidence for the formation of heteromultimeric potassium channels in xenopus oocytes. Nature 1990; 345:530–534.PubMedGoogle Scholar
  150. 150.
    Fotiadis D, Jeno P, Mini T et al. Structural characterization of two aquaporins isolated from native spinach leaf plasma membranes. J Biol Chem 2001; 276:1707–1714.PubMedGoogle Scholar
  151. 151.
    Harvengt P, Vlerick A, Fuks B et al. Lentil seed aquaporins form a hetero-oligomer which is phosphorylated by a Mg2+-dependent and Ca2+-regulated kinase. Biochem J 2000; 352:1183–1190.Google Scholar
  152. 152.
    Daniels MJ, Mirkov TE, Chrispeels MJ. The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is a homolog of the tonoplast water channel protein TIP. Plant Physiol 1994; 106:1325–1333.PubMedGoogle Scholar
  153. 153.
    Yamada S, Katsuhara M, Kelly WB et al. A family of transcripts encoding water channel proteins: Tissue-specific expression in the common ice plant. Plant Cell 1995; 7:1129–1142.PubMedGoogle Scholar
  154. 154.
    Chaumont F, Barrieu F, Jung R et al. Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol 2000; 122:1025–1034.PubMedGoogle Scholar
  155. 155.
    Temmei Y, Uchida S, Hoshino D et al. Water channel activities of mimosa pudica plasma membrane intrinsic proteins are regulated by direct interaction and phosphorylation. FEBS Lett 2005; 579: 4417–4422.PubMedGoogle Scholar
  156. 156.
    Christensen BM, Zelenina M, Aperia A et al. Localization and regulation of PKA-phosphorylated AQP2 in response to V(2)-receptor agonist/antagonist treatment. Am J Physiol Renal Physiol 2000; 278: 29–42.Google Scholar
  157. 157.
    Nielsen S, Chou CL, Marples D et al. Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-cd water channels to plasma-membrane. Proc Natl Acad Sci USA 1995; 92:1013–1017.PubMedGoogle Scholar
  158. 158.
    Marples D, Frokiaer J, Nielsen S. Long-term regulation of aquaporins in the kidney. Am J Physiol Renal Physiol 1999; 276:331–339.Google Scholar
  159. 159.
    Verkman AS. Lessons on renal physiology from transgenic mice lacking aquaporin water channels. J Am Soc Nephrol 1999; 10:1126–1135.PubMedGoogle Scholar
  160. 160.
    Boursiac Y, Chen S, Luu D-T et al. Early effects of salinity on water transport in arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 2005; 139:790–805.PubMedGoogle Scholar
  161. 161.
    Dhonukshe P, Aniento F, Hwang I et al. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in arabidopsis. Current Biology 2007; 17:520–527.PubMedGoogle Scholar
  162. 162.
    Vera-Estrella R, Barkla BJ, Bohnert HJ et al. Novel regulation of aquaporins during osmotic stress. Plant Physiol 2004; 135:2318–2329.PubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2010

Authors and Affiliations

  1. 1.François Chaumont-Institut des Sciences de la VieUniversité catholique de LouvainLouvain-la-NeuveBelgium
  2. 2.Institut des Sciences de la VieUniversité catholique de LouvainLouvain-la-NeuveBelgium

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