Abstract
The review describes current views on the molecular structure, systematics, and functional regulation of aquaporins. These recently discovered channel proteins play a principal role in water transport across cell membranes in the majority of living organisms.
Similar content being viewed by others
REFERENCES
Tyerman, S., Bohnert, H., Maurel, C., Steudle, E., and Smith, J., Plant Aquaporins: Their Molecular Biology, Biophysics and Significance for Plant Water Relations, J. Exp. Bot., 1999, vol. 50, pp. 1055-1071.
Chrispeels, M., Crawford, N., and Schroeder, J., Proteins for Transport of Water and Mineral Nutrients across the Membranes of Plant Cells, Plant Cell, 1999, vol. 11, pp. 661-676.
Agre, P., Preston, G., Smith, B., Jung, J., Raina, S., Moon, C., Guggino, W., and Nielsen, S., Aquaporin CHIP: The Archetypal Molecular Water Channel, Am. J. Physiol., 1993, vol. 265, pp. 463-476.
Moura, T., Macey, R., Chien, D., Karan, D., and Santos, H., Thermodynamics of All-or-None Water Channel Closure in Red Cells, J. Membr. Biol., 1984, vol. 81, pp. 105-11.
Denker, B., Smith, B., Kuhajda, F., and Agre, P., Identification, Purification, and Partial Characterization of a Novel Mr 28.000 Integral Membrane Protein from Erythrocytes and Renal Tubules, J. Biol. Chem., 1988, vol. 263, pp. 15634-15642.
Preston, G. and 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, vol. 88, pp. 11110-11114.
Gorin, M., Yancey, S., Cline, J., Revel, J., and Horwitz, J., The Major Intrinsic Protein (MIP) of the Bovine Lens Fiber Membrane: Characterization and Structure Based on cDNA Cloning, Cell, 1984, vol. 39, pp. 49-59.
Johnson, K., Herman, E., and Chrispeels, M., An Abundant, Highly Conserved Tonoplast Protein in Seeds, Plant Physiol., 1992, vol. 91, pp. 1006-1013.
Agre, P., Molecular Physiology of Water Transport: Aquaporin Nomenclature Workshop. Mammalian Aquaporins, Biol. Cell, 1997, vol. 89, pp. 255-257.
Reizer, J., Reizer, A., and Saier, M., Jr., 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, vol. 28, pp. 235-257.
Weig, A., Deswarte, C., and Chrispeels, M., The Major Intrinsic Protein Family of Arabidopsis Has 23 Members That Form Three Distinct Groups with Functional Aquaporins in Each Group, Plant Physiol., 1997, vol. 114, pp. 1347-1357.
Johanson, U., Karlsson, M., Johansson, I., Gustavsson, S., Sjovall, S., Fraysse, L., Weig, A., and Kjellbom, P., 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, vol. 126, pp. 1358-1369.
Quigley, F., Rosenberg, J., Shachar-Hill, Y., and Bohnert, H., From Genome to Function: The Arabidopsis Aquaporins, Genome Biol., 2002, vol. 3, pp. RESEARCH0001.
Chaumont, F., Barrieu, F., Wojcik, E., Chrispeels, M., and Jung, R., Aquaporins Constitute a Large and Highly Divergent Protein Family in Maize, Plant Physiol., 2001, vol. 125, pp. 1206-1215.
Verkman, A., Water Permeability Measurement in Living Cells and Complex Tissues, J. Membr. Biol., 2000, vol. 173, pp. 73-87.
Fischbarg, J., Kuang, K., Vera, J., Arant, S., Silverstein, S., Loike, J., and Rosen, O., Glucose Transporters Serve as Water Channels, Proc. Natl. Acad. Sci. USA, 1990, vol. 87, pp. 3244-3247.
Zeidel, M., Nielsen, S., Smith, B., Ambudkar, S., Maunsbach, A., and Agre, P., Ultrastructure, Pharmacologic Inhibition, and Transport Selectivity of Aquaporin Channel-Forming Integral Protein in Proteoliposomes, Biochemistry, 1994, vol. 33, pp. 1606-1615.
Zeidel, M., Ambudkar, S., Smith, B., and Agre, P., Reconstitution of Functional Water Channels in Liposomes Containing Purified Red Cell CHIP28 Protein, Biochemistry, 1992, vol. 31, pp. 7436-7440.
Cheng, A., van Hoek, A., Yeager, M., Verkman, A., and Mitra, A., Three-Dimensional Organization of a Human Water Channel, Nature, 1997, vol. 387, pp. 627-630.
Meinild, A., Klaerke, D., and Zeuthen, T., Bidirectional Water Fluxes and Specificity for Small Hydrophilic Molecules in Aquaporins 0–5, J. Biol. Chem., 1998, vol. 273, pp. 32 446-32 451.
Maurel, C., Reizer, J., Schroeder, J., and Chrispeels, M. The Vacuolar Membrane Protein Gamma-TIP Creates Water Specific Channels in Xenopus Oocytes, EMBO J., 1993, vol. 12, pp. 2241-2247.
Pohl, P., Saparov, S., Borgnia, M., and Agre, P., Highly Selective Water Channel Activity Measured by Voltage Clamp: Analysis of Planar Lipid Bilayers Reconstituted with Purified AqpZ, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 9624-9629.
Preston, G., Jung, J., Guggino, W., and Agre, P., The Mercury-Sensitive Residue at Cysteine 189 in the CHIP28 Water Channel, J. Biol. Chem., 1993, vol. 268, pp. 17-20.
Daniels, M., Chaumont, F., Mirkov, T., and Chrispeels, M., Characterization of a New Vacuolar Membrane Aquaporin Sensitive to Mercury at a Unique Site, Plant Cell, 1996, vol. 8, pp. 587-599.
Barone, L., Shih, C., and Wasserman, B., Mercury-Induced Conformational Changes and Identification of Conserved Surface Loops in Plasma Membrane Aquaporins from Higher Plants. Topology of PMIP31 from Beta vulgaris L., J. Biol. Chem., 1997, vol. 272, pp. 30672-30677.
Borgnia, M. and Agre, P., Reconstitution and Functional Comparison of Purified GlpF and AqpZ, the Glycerol and Water Channels from Escherichia coli, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 2888-2893.
Cooper, G., Zhou, Y., Bouyer, P., Grichtchenko, I., and Boron, W., Transport of Volatile Solutes through AQP1, J. Physiol., 2002, vol. 542, pp. 17-29.
Rivers, R., Dean, R., Chandy, G., Hall, J., Roberts, D., and Zeidel, M., Functional Analysis of Nodulin 26, an Aquaporin in Soybean Root Nodule Symbiosomes, J. Biol. Chem., 1997, vol. 272, pp. 16256-16261.
Otto, B. and Kaldenhoff, R., Cell-Specific Expression of the Mercury-Insensitive Plasma-Membrane Aquaporin NtAQP1 from Nicotiana tabacum, Planta, 2000, vol. 211, pp. 167-172.
Borgnia, M., Nielsen, S., Engel, A., and Agre, P., Cellular and Molecular Biology of the Aquaporin Water Channels, Annu. Rev. Biochem., 1999, vol. 68, pp. 425-458.
Henzler, T. and Steudle, E., Transport and Metabolic Degradation of Hydrogen Peroxide in Chara corallina: Model Calculations and Measurements with the Pressure Probe Suggest Transport of H2O2 across Water Channels, J. Exp. Bot., 2000, vol. 51, pp. 2053-2066.
Nakhoul, N., Davis, B., Romero, M., and Boron, W., Effect of Expressing the Water Channel Aquaporin-1 on the CO2 Permeability of Xenopus Oocytes, Am. J. Physiol., 1998, vol. 274, pp. 543-548.
Yang, B., Fukuda, N., van Hoek, A., Matthay, M., Ma, T., and Verkman, A., Carbon Dioxide Permeability of Aquaporin-1 Measured in Erythrocytes and Lung of Aquaporin-1 Null Mice and in Reconstituted Proteoliposomes, J. Biol. Chem., 2000, vol. 275, pp. 2686-2692.
Fang, X., Yang, B., Matthay, M., and Verkman, A., Evidence against Aquaporin-1-Dependent CO2 Permeability in Lung and Kidney, J. Physiol., 2002, vol. 542, pp. 63-69.
Tchernov, D., Helman, Y., Keren, N., Luz, B., Ohad, I., Reinhold, L., Ogawa, T., and Kaplan, A., Passive Entry of CO2 and Its Energy-Dependent Intracellular Conversion to HCO −3 in Cyanobacteria Are Driven by a Photosystem I-Generated DeltamuH+, J. Biol. Chem., 2001, vol. 276, pp. 23450-23455.
Terashima, I. and Ono, K., Effects of HgCl2 on CO2 Dependence of Leaf Photosynthesis: Evidence Indicating Involvement of Aquaporins in CO2 Diffusion across the Plasma Membrane, Plant Cell Physiol., 2002, vol. 43, pp. 70-78.
Reuss, L., Focus on “Effect of Expressing the Water Channel Aquaporin-1 on the CO2 Permeability of Xenopus Oocytes,” Am. J. Physiol., 1998, vol. 274, pp. 297-298.
Anthony, T., Brooks, H., Boassa, D., Leonov, S., Yanochko, G., Regan, J., and Yool, A., Cloned Human Aquaporin-1 Is a Cyclic GMP-Gated Ion Channel, Mol. Pharmacol., 2000, vol. 57, pp. 576-588.
Boassa, D. and Yool, A., A Fascinating Tail: cGMP Activation of Aquaporin-1 Ion Channels, Trends Pharmacol. Sci., 2002, vol. 23, pp. 558-562.
Zampighi, G., Hall, J., and Kreman, M., Purified Lens Junctional Protein Forms Channels in Planar Lipid Films, Proc. Natl. Acad. Sci. USA, 1985, vol. 82, pp. 8468-8472.
Ehring, G., Zampighi, G., Horwitz, J., Bok, D., and Hall, J., Properties of Channels Reconstituted from the Major Intrinsic Protein of Lens Fiber Membranes, J. Gen. Physiol., 1990, vol. 96, pp. 631-664.
Modesto, E., Lampe, P., Ribeiro, M., Spray, D., and Campos de Carvalho, A., Properties of Chicken Lens MIP Channels Reconstituted into Planar Lipid Bilayers, J. Membr. Biol., 1996, vol. 154, pp. 239-249.
Yasui, M., Hazama, A., Kwon, T., Nielsen, S., Guggino, W., and Agre, P., Rapid Gating and Anion Permeability of an Intracellular Aquaporin, Nature, 1999, vol. 402, pp. 184-187.
Ikeda, M., Beitz, E., Kozono, D., Guggino, W., Agre, P., and Yasui, M., Characterization of Aquaporin-6 as a Nitrate Channel in Mammalian Cells. Requirement of Pore-Lining Residue Threonine 63, J. Biol. Chem., 2002, vol. 277, pp. 39873-39879.
Weaver, C., Shomer, N., Louis, C., and Roberts, D., Nodulin 26, a Nodule-Specific Symbiosome Membrane Protein from Soybean, Is an Ion Channel, J. Biol. Chem., 1994, vol. 269, pp. 17858-17862.
Bill, R., Hedfalk, K., Karlgren, S., Mullins, J., Rydstrom, J., and Hohmann, S., Analysis of the Pore of the Unusual Major Intrinsic Protein Channel, Yeast Fps1p, J. Biol. Chem., 2001, vol. 276, pp. 36543-36549.
Scheuring, S., Ringler, P., Borgnia, M., Stahlberg, H., Muller, D., Agre, P., and Engel, A., High Resolution AFM Topographs of the Escherichia coli Water Channel Aquaporin Z, EMBO J., 1999, vol. 18, pp. 4981-4987.
Verbavatz, J., Brown, D., Sabolic, I., Valenti, G., Ausiello, D., van Hoek, A., Ma, T., and Verkman, A., Tetrameric Assembly of CHIP28 Water Channels in Liposomes and Cell Membranes: A Freeze-Fracture Study, J. Cell Biol., 1993, vol. 123, pp. 605-618.
Eskandari, S., Wright, E., Kreman, M., Starace, D., and Zampighi, G., Structural Analysis of Cloned Plasma Membrane Proteins by Freeze-Fracture Electron Microscopy, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 11235-11240.
Fu, D., Libson, A., Miercke, L., Weitzman, C., Nollert, P., Krucinski, J., and Stroud, R., Structure of a Glycerol-Conducting Channel and the Basis for Its Selectivity, Science, 2000, vol. 290, pp. 481-486.
Sui, H., Walian, P., Tang, G., Oh, A., and Jap, B., Crystallization and Preliminary X-Ray Crystallographic Analysis of Water Channel AQP1, Acta Crystallogr. D. Biol. Crystallogr., 2000, vol. 56, pp. 1198-1200.
Sui, H., Han, B., Lee, J., Walian, P., and Jap, B., Structural Basis of Water-Specific Transport through the AQP1 Water Channel, Nature, 2001, vol. 414, pp. 872-878.
De Groot, B., Engel, A., and Grubmuller, H., The Structure of the Aquaporin-1 Water Channel: A Comparison between Cryo-Electron Microscopy and X-Ray Crystallography, J. Mol. Biol., 2003, vol. 325, pp. 485-493.
Thomas, D., Bron, P., Ranchy, G., Duchesne, L., Cavalier, A., Rolland, J., Raguenes-Nicol, C., Hubert, J., Haase, W., and Delamarche, C., Aquaglyceroporins: One Channel for Two Molecules, Biochim. Biophys. Acta, 2002, vol. 1555, pp. 181-186.
Jensen, M., Tajkhorshid, E., and Schulten, K., The Mechanism of Glycerol Conduction in Aquaglyceroporins, Structure (Cambridge), 2001, vol. 9, pp. 1083-1093.
Tajkhorshid, E., Nollert, P., Jensen, M., Miercke, L., O'Connell, J., Stroud, R., and Schulten, K., Control of the Selectivity of the Aquaporin Water Channel Family by Global Orientational Tuning, Science, 2002, vol. 296, pp. 525-530.
Kong, Y. and Ma, J., Dynamic Mechanisms of the Membrane Water Channel Aquaporin-1 (AQP1), Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 14345-14349.
Kozono, D., Ding, X., Iwasaki, I., Meng, X., Kamagata, Y., Agre, P., and Kitagawa, Y., Functional Expression and Characterization of an Archaeal Aquaporin: AqpM from Methanothermobacter marburgensis, J. Biol. Chem., 2003, vol. 278, pp. 10649-10656.
Park, J. and Saier, M., Jr., Phylogenetic Characterization of the MIP Family of Transmembrane Channel Proteins, J. Membr. Biol., 1996, vol. 153, pp. 171-180.
Heymann, J. and Engel, A., Aquaporins: Phylogeny, Structure, and Physiology of Water Channels, News Physiol. Sci., 1999, vol. 14, pp. 187-193.
Zardoya, R. and Villalba, S., A Phylogenetic Framework for the Aquaporin Family in Eukaryotes, J. Mol. Evol., 2001, vol. 52, pp. 391-404.
Echevarria, M. and Ilundain, A., Aquaporins, J. Physiol. Biochem., 1998, vol. 54, pp. 107-118.
Liu, Z., Shen, J., Carbrey, J., Mukhopadhyay, R., Agre, P., and Rosen, B., Arsenite Transport by Mammalian Aquaglyceroporins AQP7 and AQP9, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 6053-6058.
Fu, D., Libson, A., and Stroud, R., The Structure of GlpF, a Glycerol Conducting Channel, Novartis. Found. Symp., 2002, vol. 245, pp. 51-61.
Elkjaer, M., Nejsum, L., Gresz, V., Kwon, T., Jensen, U., Frokiaer, J., and Nielsen, S., Immunolocalization of Aquaporin-8 in Rat Kidney, Gastrointestinal Tract, Testis, and Airways, Am. J. Physiol. Renal Physiol., 2001, vol. 281, pp. F1047-F1057.
Hohmann, I., Bill, R., Kayingo, I., and Prior, B., Microbial MIP Channels, Trends Microbiol., 2000, vol. 8, pp. 33-38.
Chaumont, F., Barrieu, F., Jung, R., and Chrispeels, M., Plasma Membrane Intrinsic Proteins from Maize Cluster in Two Sequence Subgroups with Differential Aquaporin Activity, Plant Physiol., 2000, vol. 122, pp. 1025-1034.
Maurel, C., Tacnet, F., Guclu, J., Guern, J., and Ripoche, P., Purified Vesicles of Tobacco Cell Vacuolar and Plasma Membranes Exhibit Dramatically Different Water Permeability and Water Channel Activity, Proc. Natl. Acad. Sci. USA, 1997, vol. 94, pp. 7103-7108.
Jauh, G., Fischer, A., Grimes, H., Ryan, C., Jr., and Rogers, J., Delta-Tonoplast Intrinsic Protein Defines Unique Plant Vacuole Functions, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 12995-12999.
Jauh, G., Phillips, T., and Rogers, J., Tonoplast Intrinsic Protein Isoforms as Markers for Vacuolar Functions, Plant Cell, 1999, vol. 11, pp. 1867-1882.
Karlsson, M., Johansson, I., Bush M., McCann, M., Maurel, C., Larsson, C., and Kjellbom, P., An Abundant TIP Expressed in Mature Highly Vacuolated Cells, Plant J., 2000, vol. 21, pp. 83-90.
Johanson, U. and Gustavsson, S., A New Subfamily of Major Intrinsic Proteins in Plants, Mol. Biol. Evol., 2002, vol. 19, pp. 456-461.
Wallace, I., Wills, D., Guenther, J., and Roberts, D., Functional Selectivity for Glycerol of the Nodulin 26 Subfamily of Plant Membrane Intrinsic Proteins, FEBS Lett., 2002, vol. 523, pp. 109-112.
Zardoya, R., Ding, X., Kitagawa, Y., and Chrispeels, M., Origin of Plant Glycerol Transporters by Horizontal Gene Transfer and Functional Recruitment, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 14893-14896.
Johansson, I., Larsson, C., Ek, B., and 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, vol. 8, pp. 1181-1191.
Phillips, A. and Huttly, A., Cloning of Two Gibberellin-Regulated cDNAs from Arabidopsis thaliana by Subtractive Hybridization: Expression of the Tonoplast Water Channel, Gamma-TIP, Is Increased by GA3, Plant Mol. Biol., 1994, vol. 24, pp. 603-615.
Kaldenhoff, R., Kolling, A., and Richter, G., Regulation of the Arabidopsis thaliana Aquaporin Gene AthH2 (PIP1b), J. Photochem. Photobiol. B., 1996, vol. 36, pp. 351-354.
Suga, S., Komatsu, S., and Maeshima, M., Aquaporin Isoforms Responsive to Salt and Water Stresses and Phytohormones in Radish Seedlings, Plant Cell Physiol., 2002, vol. 43, pp. 1229-1237.
Yamada, S., Katsuhara, M., Kelly, W., Michalowski, C., and Bohnert, H., A Family of Transcripts Encoding Water Channel Proteins: Tissue-Specific Expression in the Common Ice Plant, Plant Cell, 1995, vol. 7, pp. 1129-1142.
Morillon, R., Catterou, M., Sangwan, R., Sangwan, B., and Lassalles, J., Brassinolide May Control Aquaporin Activities in Arabidopsis thaliana, Planta, 2001, vol. 212, pp. 199-204.
Yamamoto, Y., Taylor, C., Acedo, G., Cheng, C., and Conkling, M., Characterization of Cis-Acting Sequences Regulating Root-Specific Gene Expression in Tobacco, Plant Cell, 1991, vol. 3, pp. 371-82.
Siefritz, F., Biela, A., Eckert, M., Otto, B., Uehlein, N., and Kaldenhoff, R., The Tobacco Plasma Membrane Aquaporin NtAQP1, J. Exp. Bot., 2001, vol. 52, pp. 1953-1957.
Morillon, R. and Chrispeels, M., 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, vol. 98, pp. 14138-14143.
Ohshima, Y., Iwasaki, I., Suga, S., Murakami, M., Inoue, K., and Maeshima, M., 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, vol. 42, pp. 1119-1129.
Sarda, X., Tousch, D., Ferrare, K., Legrand, E., Dupuis, J., Casse-Delbart, F., and Lamaze, T., Two TIP-Like Genes Encoding Aquaporins Are Expressed in Sunflower Guard Cells, Plant J., 1997, vol. 12, pp. 1103-1111.
Weaver, C., Crombie, B., Stacey, G., and Roberts, D., Calcium-Dependent Phosphorylation of Symbiosome Membrane Proteins from Nitrogen-Fixing Soybean Nodules, Plant Physiol., 1991, vol. 95, pp. 222-227.
Inoue, K., Takeuchi, Y., Nishimura, M., and Hara-Nishimura, I., Characterization of Two Integral Membrane Proteins Located in the Protein Bodies of Pumpkin Seeds, Plant Mol. Biol., 1995, vol. 28, pp. 1089-1101.
Higuchi, T., Suga, S., Tsuchiya, T., Hisada, H., Morishima, S., Okada, Y., and Maeshima, M., Molecular Cloning, Water Channel Activity and Tissue Specific Expression of Two Isoforms of Radish Vacuolar Aquaporin, Plant Cell Physiol., 1998, vol. 9, pp. 905-913.
Johansson, I., Karlsson, M., Johanson, U., Larsson, C., and Kjellbom, P. The Role of Aquaporins in Cellular and Whole Plant Water Balance, Biochim. Biophys. Acta, 2000, vol. 1465, pp. 324-342.
Gouraud, S., Laera, A., Calamita, G., Carmosino, M., Procino, G., Rossetto, O., Mannucci, R., Rosenthal, W., Svelto, M., and Valenti, G., Functional Involvement of VAMP/Synaptobrevin-2 in CAMP-Stimulated Aquaporin 2 Translocation in Renal Collecting Duct Cells, J. Cell Sci., 2002, vol. 115, pp. 3667-3674.
Nielsen, S., Chou, C., Marples, D., Christensen, E., Kishore, B., and Knepper, M., 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, vol. 92, pp. 1013-1017.
Kirch, H., Vera-Estrella, R., Golldack, D., Quigley, F., Michalowski, C., Barkla, B., and Bohnert, H., Expression of Water Channel Proteins in Mesembryanthemum crystallinum, Plant Physiol., 2000, vol. 123, pp. 111-124.
Wayne, R. and Tazawa, M., The Actin Cytoskeleton and Polar Water Permeability in Characean Cells, Protoplasma, 1988, vol. 2, pp. 116-130.
Girsch, S. and Peracchia, C., Calmodulin Interacts with a C-Terminus Peptide from the Lens Membrane Protein MIP26, Curr. Eye Res., 1991, vol. 10, pp. 839-849.
Swamy-Mruthinti, S., Glycation Decreases Calmodulin Binding to Lens Transmembrane Protein, MIP, Biochim. Biophys. Acta, 2001, vol. 1536, pp. 64-72.
Chen, T., Hsu, C., Tsai, P., Ho, Y., and Lin, N., Heterotrimeric G-Protein and Signal Transduction in the Nematode-Trapping Fungus Arthrobotrys dactyloides, Planta, 2001, vol. 212, pp. 858-863.
Fotiadis, D., Suda, K., Tittmann, P., Jeno, P., Philippsen, A., Muller, D., Gross, H., and Engel, A., Identification and Structure of a Putative Ca2+-Binding Domain at the C Terminus of AQP1, J. Mol. Biol., 2002, vol. 318, pp. 1381-1394.
Lorenz, A., Kaldenhoff, R., and Hertel, R., A Major Integral Protein of the Plant Plasma Membrane Binds Flavin, Protoplasma, 2003, vol. 221, pp. 19-30.
Kuwahara, M., Fushimi, K., Terada, Y., Bai, L., Marumo, F., and Sasaki, S., cAMP-Dependent Phosphorylation Stimulates Water Permeability of Aquaporin-Collecting Duct Water Channel Protein Expressed in Xenopus Oocytes, J. Biol. Chem., 1995, vol. 270, pp. 10 384-10 387.
Maurel, C., Kado, R., Guern, J., and Chrispeels, M., Phosphorylation Regulates the Water Channel Activity of the Seed-Specific Aquaporin Alpha-TIP, EMBO J., 1995, vol. 14, pp. 3028-3035.
Miao, G., Hong, Z., and Verma, D., Topology and Phosphorylation of Soybean Nodulin-26, an Intrinsic Protein of the Peribacteroid Membrane, J. Cell Biol., 1992, vol. 118, pp. 481-490.
Johnson, K. and Chrispeels, M., Tonoplast-Bound Protein Kinase Phosphorylates Tonoplast Intrinsic Protein, Plant Physiol., 1992, vol. 100, pp. 1787-1795.
Johansson, I., Karlsson, M., Shukla, V., Chrispeels, M., Larsson, C., and Kjellbom, P., Water Transport Activity of the Plasma Membrane Aquaporin PM28A Is Regulated by Phosphorylation, Plant Cell, 1998, vol. 10, pp. 451-459.
Kjellbom, P., Larsson, C., Johansson, I., Karlsson, M., and Johanson, U., Aquaporins and Water Homeostasis in Plants, Trends Plant Sci., 1999, vol. 4, pp. 308-314.
Maurel, C., Javot, H., Lauvergeat, V., Gerbeau, P., Tournaire, C., Santoni, V., and Heyes, J., Molecular Physiology of Aquaporins in Plants, Int. Rev. Cytol., 2002, vol. 215, pp. 105-148.
Tyerman, S., Niemietz, C., and Bramley, H., Plant Aquaporins: Multifunctional Water and Solute Channels with Expanding Roles, Plant Cell Environ., 2002, vol. 25, pp. 173-194.
Baiges, I., Schaffner, A., Affenzeller, M., and Mas, A., Plant Aquaporins, Physiol.Plant., 2002, vol. 115, pp. 175-182.
Allakhverdiev, S., Sakamoto, A., Nishiyama, Y., and Murata, N., Inactivation of Photosystems I and II in Response to Osmotic Stress in Synechococcus. Contribution of Water Channels, Plant Physiol., 2000, vol. 122, pp. 1201-1208.
Barrowclough, D., Peterson, C., and Steudle, E., Radial Hydraulic Conductivity along Developing Onion Roots, J. Exp. Bot., 2000, vol. 51, pp. 547-557.
Martre, P., North, G., and Nobel, P., Hydraulic Conductance and Mercury-Sensitive Water Transport for Roots of Opuntia acanthocarpa in Relation to Soil Drying and Rewetting, Plant Physiol., 2001, vol. 126, pp. 352-362.
Tazawa, M., Sutou, E., and Shibasaka, M., Onion Root Water Transport Sensitive to Water Channel and K+ Channel Inhibitors, Plant Cell Physiol., 2001, vol. 42, pp. 28-36.
Siefritz, F., Tyree, M., Lovisolo, C., Schubert, A., and Kaldenhoff, R., PIP1 Plasma Membrane Aquaporins in Tobacco: From Cellular Effects to Function in Plants, Plant Cell, 2002, vol. 14, pp. 869-876.
Javot, H., Lauvergeat, V., Santoni, V., Martin-Laurent, F., Guclu, J., Vinh, J., Heyes, J., Franck, K., Schaffner, A., Bouchez, D., and Maurel, C., Role of a Single Aquaporin Isoform in Root Water Uptake, Plant Cell, 2003, vol. 15, pp. 509-522.
Maggio, A. and Joly, R., Effects of Mercuric Chloride on the Hydraulic Conductivity of Tomato Root Systems (Evidence for a Channel-Mediated Water Pathway), Plant Physiol., 1995, vol. 109, pp. 331-335.
Daniels, M., Mirkov, T., and Chrispeels, M., 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, vol. 106, pp. 1325-1333.
Hasegawa, H., Ma, T., Skach, W., Matthay, M., and Verkman, A., Molecular Cloning of a Mercurial-Insensitive Water Channel Expressed in Selected Water-Transporting Tissues, J. Biol. Chem., 1994, vol. 269, pp. 5497-5500.
Kaldenhoff, R., Grote, K., Zhu, J., and Zimmermann, U., Significance of Plasmalemma Aquaporins for Water-Transport in Arabidopsis thaliana, Plant J., 1998, vol. 14, pp. 121-128.
Aharon, R., Shahak, Y., Wininger, S., Bendov, R., Kapulnik, Y., and Galili, G., Overexpression of a Plasma Membrane Aquaporin in Transgenic Tobacco Improves Plant Vigor under Favorable Growth Conditions but Not under Drought or Salt Stress, Plant Cell, 2003, vol. 15, pp. 439-447.
Dixit, R., Rizzo, C., Nasrallah, M., and Nasrallah, J., The Brassica MIP-mod Gene Encodes a Functional Water Channel that Is Expressed in the Stigma Epidermis, Plant Mol. Biol., 2001, vol. 45, pp. 51-62.
Hukin., D., Doering-Saad, C., Thomas, C., and Pritchard, J., Sensitivity of Cell Hydraulic Conductivity to Mercury Is Coincident with Symplasmic Isolation and Expression of Plasmalemma Aquaporin Genes in Growing Maize Roots, Planta, 2002, vol. 215, pp. 1047-1056.
Ikeda, S., Nasrallah, J., Dixit, R., Preiss, S., and Nasrallah, M., An Aquaporin-Like Gene Required for the Brassica Self-Incompatibility Response, Science, 1997, vol. 276, pp. 1564-1566.
Marin-Olivier, M., Chevalier, T., Fobis-Loisy, I., Dumas, C., and Gaude, T., Aquaporin pip Genes Are Not Expressed in the Stigma Papillae in Brassica oleracea, Plant J., 2000, vol. 24, pp. 231-240.
Steudle, E. and Peterson, C., How Does Water Get through Roots?, J. Exp. Bot., 1998, vol. 49, pp. 775-788.
Santoni, V., Gerbeau, P., Javot, H., and Maurel, C., The High Diversity of Aquaporins Reveals Novel Facets of Plant Membrane Functions, Curr. Opin. Plant Biol., 2000, vol. 3, pp. 476-481.
Javot, H. and Maurel, C., The Role of Aquaporins in Root Water Uptake, Ann. Bot., 2002, vol. 90, pp. 301-313.
Henzler, T., Waterhouse, R., Smyth, A., Carvajal, M., Cooke, D., Schaffner, A., Steudle, E., and Clarkson, D., Diurnal Variations in Hydraulic Conductivity and Root Pressure Can Be Correlated with the Expression of Putative Aquaporins in the Roots of Lotus japonicus, Planta, 1999, vol. 210, pp. 50-60.
Carvajal, M., Cooke, D., Clarkson, D., Responses of Wheat Plants to Nutrition Deprivation May Involve the Regulation of Water-Channel Function, Planta, 1996, vol. 199, pp. 372-381.
Clarkson, D., Carvajal, M., Henzler, T., Waterhouse, R., Smyth, A., Cooke, D., and Steudle, E., Root Hydraulic Conductance: Diurnal Aquaporin Expression and the Effects of Nutrient Stress, J. Exp. Bot., 2000, vol. 51, pp. 61-70.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Shapiguzov, A.Y. Aquaporins: Structure, Systematics, and Regulatory Features. Russian Journal of Plant Physiology 51, 127–137 (2004). https://doi.org/10.1023/B:RUPP.0000011313.02617.49
Issue Date:
DOI: https://doi.org/10.1023/B:RUPP.0000011313.02617.49