Abstract
Water channel proteins, aquaporins, are integral membrane proteins serving in the permeation of water and some other small molecules. Eleven isoforms of aquaporins have been identified from various tissues to date. They are expressed in tissue- and cell-specific manners, and are closely related to the specific functions of tissues and cells. Aquaporins are usually localized to the plasma membrane. Some isoforms are present in cytoplasmic compartments, and their translocation to the plasma membrane is crucial in the regulation of water transfer. This review focuses on the localization of aquaporins in mammalian tissues and discusses the physiological importance of water channels.
Similar content being viewed by others
References
Agre P, Brown D, Nielsen S (1995) Aquaporin water channels: unanswered questions and unresolved controversies. Curr Opin Cell Biol 7, 472–83.
Agre P, Sasaki S, Chrispeels MJ (1993) Aquaporins: a family of water channel proteins. Am J Physiol Renal Fluid Electrolyte Physiol 265, F461.
Brown D, Verbavatz JM, Valenti G, Lui B, Sabolić I (1993) Localization of the CHIP28 water channel in reabsorptive segments of the rat male reproductive tract. Eur J Cell Biol 61, 264–73.
Cheng A, van Hoek AN, Yeager M, Verkman AS, Mitra AK (1997) Three-dimensional organization of a human water channel. Nature 387, 627–30.
Deen PMT, Verdijk MAJ, Knoers NVAM et al. (1994) Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine. Science 264, 92–5.
Denker BM, Smith BL, Kuhajda FP, Agre P (1988) Identification, purification, and partial characterization of a novel M r 28,000 integral membrane protein from erythrocytes and renal tubules. J Biol Chem 263, 15 634–42.
Echevarría M, Windhager EE, Frindt G (1996) Selectivity of the renal collecting duct water channel aquaporin-3. J Biol Chem 271, 25 079–82.
Elkjær ML, Nejsum LN, Gresz V et al. (2001) Immunolocalization of aquaporin-8 in rat kidney, gastrointestinal tract, testis, and airways. Am J Physiol Renal Physiol 281, F1047–57.
Elkjær ML, Vajda Z, Nejsum LN et al. (2000) Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem Biophys Res Commun 276, 1118–28.
Fisher JS, Turner KJ, Fraser HM, Saunders PTK, Brown D, Sharpe RM (1998) Immunoexpression of aquaporin-1 in the efferent ducts of the rat and marmoset monkey during development, its modulation by estrogens, and its possible role in fluid resorption. Endocrinology 139, 3935–45.
Francis P, Berry V, Bhattacharya S, Moore A (2000) Congenital progressive polymorphic cataract caused by a mutation in the major intrinsic protein of the lens, MIP (AQPO). Br J Ophthalmol 84, 1376–9.
Frigeri A, Gropper MA, Turck CW, Verkman AS (1995a) Im-munolocalization of the mercurial-insensitive water channel and glycerol intrinsic protein in epithelial cell plasma membranes. Proc Natl Acad Sci USA 92, 4328–31.
Frigeri A, Gropper MA, Umenishi F, Kawashima M, Brown D, Verkman AS (1995b) Localization of MIWC and GLIP water channel homologs in neuromuscular, epithelial and glandular tissues. J Cell Sci 108, 2993–3002.
Frigeri A, Nicchia GP, Verbavatz JM, Valenti G, Svelto M (1998) Expression of aquaporin-4 in fast-twitch fibers on mammalian skeletal muscle. J Clin Investig 102, 695–703.
Fushimi K, Uchida S, Hara Y, Hirata Y, Marumo F, Sasaki S (1993) Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature 361, 549–52.
Gorin MB, Yancey SB, Cline J, Revel JP, Horwitz J (1984) The major intrinsic protein (MIP) of the bovine lens fiber membrane: characterization and structure based on cDNA cloning. Cell 39, 49–59.
Gresz V, Kwon TH, Hurley PT et al. (2001) Identification and localization of aquaporin water channels in human salivary glands. Am J Physiol Gastrointest Liver Physiol 281, G247–54.
Hamann S, Zeuthen T, Cour ML et al. (1998) Aquaporins in complex tissues: distribution of aquaporins 1-5 in human and rat eye. Am J Physiol Cell Physiol 274, C1332–45.
Hatakeyama S, Yoshida Y, Tani T et al. (2001) Cloning of a new aquaporin (AQP10) abundantly expressed in duodenum and jejunum. Biochem Biophys Res Commun 287, 814–9.
Hatton JD, Cox GF, Miller AL, Nichol JA, Ellisman MH (1987) Identification of polypeptides associated with sarcolemmal vesicles enriched in orthogonal arrays. Biochem Biophys Acta 904, 373–80.
He X, Tse CM, Donowitz M, Alper SL, Gabriel SE, Baum BJ (1997) Polarized distribution of key membrane transport proteins in the rat submandibular gland. Pflügers Arch Eur J Physiol 433, 260–8.
Ishibashi K, Imai M, Sasaki S (2000) Cellular localization of aquaporin 7 in the rat kidney. Exp Nephrol 8, 252–7.
Ishibashi K, Kuwahara M, Gu Y et al. (1997) Cloning and functional expression of a new water channel abundantly expressed in the testis permeable to water, glycerol, and urea. J Biol Chem 272, 20782–6.
Ishibashi K, Kuwahara M, Gu Y, Tanaka Y, Marumo F, Sasaki S (1998) Cloning and functional expression of a new aquaporin (AQP9) abundantly expressed in the peripheral leukocytes permeable to water and urea, but not to glycerol. Biochem Biophys Res Commun 244, 268–74.
Ishibashi K, Sasaki S, Fushimi K et al. (1994) Molecular cloning and expression of a member of the aquaporin family with permeability to glycerol and urea in addition to water expressed at the basolateral membrane of kidney collecting duct cells. Proc Natl Acad Sci USA 91, 6269–73.
Jung JS, Preston GM, Smith BL, Guggino WB, Agre P (1994) Molecular structure of the water channel through aquaporin CHIP. The hourglass model. J Biol Chem 269, 14 648–54.
Landis DMD, Reese TS (1974) Arrays of particles in freeze-fractured astrocytic membranes. J Cell Biol 60, 316–20.
van Lieburg AF, Verdijk MAJ, Knoers VVAM et al. (1994) Patients with autosomal nephrogenic diabetes insipidus homozygous for mutations in the aquaporin 2 water-channel gene. Am J Hum Genet 55, 648–52.
Loo DDF, Zeuthen T, Chandy G, Wright EM (1996) Cotransport of water by the Na+/glucose cotransporter. Proc Natl Acad Sci USA 93, 13 367–70.
Ma T, Frigeri A, Hasegawa H, Verkman AS (1994) Cloning of a water channel homolog expressed in brain meningeal cells and kidney collecting duct that functions as a stilbene-sensitive glycerol transporter. J Biol Chem 269, 21 845–9.
Ma T, Song Y, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS (1999) Defective secretion of saliva in transgenic mice lacking aquaporin-5 water channels. J Biol Chem 274, 20 071–4.
Ma T, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS (1998) Severely impaired urinary concentrating ability in transgenic mice lacking aquaporin-1 water channels. J Biol Chem 273, 4296–9.
Marinelli RA, LaRusso NF (1997) Aquaporin water channels in liver: their significance in bile formation. Hepatology 26, 1081–4.
Marinelli RA, Tietz PS, Pham LD, Rueckert L, Agre P, LaRusso NF (1999) Secretin induces the apical insertion of aquaporin-1 water channels in rat cholangiocytes. Am J Physiol Gastrointest Liver Physiol 276, G280–86.
Marples D, Knepper MA, Christensen EI, Nielsen S (1995) Redistribution of aquaporin-2 water channels induced by vasopressin in rat kidney inner medullary collecting duct. Am J Physiol Cell Physiol 269, C655–64.
Matsuzaki T, Suzuki T, Koyama H, Tanaka S, Takata K (1999a) Aquaporin-5 (AQP5), a water channel protein, in the rat salivary and lacrimal glands: immunolocalization and effect of secretory stimulation. Cell Tissue Res 295, 513–21.
Matsuzaki T, Suzuki T, Koyama H, Tanaka S, Takata K (1999b) Water channel protein AQP3 is present in epithelia exposed to the environment of possible water loss. J Histochem Cytochem 47, 1275–86.
Matsuzaki T, Suzuki T, Takata K (2000) Water channel protein, aquaporin 3, in epithelial cells. In: Molecular Biology and Physiology of Water and Solute Transport (Hohmann S, Nielsen S, eds). Kluwer Academic / Plenum Publishers, New York, 167–72.
Matsuzaki T, Suzuki T, Takata K (2001) Hypertonicity-induced expression of aquaporin 3 in MDCK cells. Am J Physiol Cell Physiol 281, C55–63.
Mulders SM, Preston GM, Deen PMT, Guggino WB, van Os CH, Agre P (1995) Water channel properties of major intrinsic protein of lens. J Biol Chem 270, 9010–6.
Murata K, Mitsuoka K, Hirai T et al. (2000) Structural determinants of water permeation through aquaporin-1. Nature 407, 599–605.
Nejsum LN, Elkjær ML, Hager H, Frøkiær J, Kwon TH, Nielsen S (2000) Localization of aquaporin-7 in rat and mouse kidney using RT-PCR, immunoblotting, and immunocytochemistry. Biochem Biophys Res Commun 277, 164–70.
Nelson RD, Stricklett P, Gustafson C et al. (1998) Expression of an AQP2 Cre recombinase transgene in kidney and male reproductive system of transgenic mice. Am J Physiol Cell Physiol 275, C216–26.
Nielsen S, Chou CL, Marples D, Christensen EI, Kishore BK, Knepper MA (1995a) Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci USA 92, 1013–7.
Nielsen S, King LS, Christensen BM, Agre P (1997a) Aquaporins in complex tissues. II. Subcellular distribution in respiratory and glandular tissues of rat. Am J Physiol Cell Physiol 273, C1549–61.
Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP (1997b) Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17, 171–80.
Nielsen S, Pallone T, Smith BL, Christensen EI, Agre P, Maunsbach AB (1995b) Aquaporin-1 water channels in short and long loop descending thin limbs and in descending vasa recta in rat kidney. Am J Physiol Renal Fluid Electrolyte Physiol 268, F1023–37.
Nielsen S, Smith BL, Christensen EI, Agre P (1993a) Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia. Proc Natl Acad Sci USA 90, 7275–9.
Nielsen S, Smith BL, Christensen EI, Knepper MA, Agre P (1993b) CHIP28 water channels are localized in constitutively water-permeable segments of the nephron. J Cell Biol 120, 371–83.
Nihei K, Koyama Y, Tani T et al. (2001) Immunolocalization of aquaporin-9 in rat hepatocytes and Leydig cells. Arch Histol Cytol 64, 81–8.
Ohshiro K, Yaoita E, Yoshida Y et al. (2001) Expression and immunolocalization of AQP6 in intercalated cells of the rat kidney collecting duct. Arch Histol Cytol 64, 329–38.
Orci L, Humbert F, Brown D, Perrelet A (1981) Membrane ultrastructure in urinary tubules. Int Rev Cytol 73, 183–242.
Preston GM, Agre P (1991) Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc Natl Acad Sci USA 88, 11 110–4.
Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256, 385–7.
Schnermann J, Chou CL, Ma T, Traynor T, Knepper MA, Verkman AS (1998) Defective proximal tubular fluid reab-sorption in transgenic aquaporin-1 null mice. Proc Natl Acad Sci USA 95, 9660–4.
Steinfeld S, Cogan E, King LS, Agre P, Kiss R, Delporte C (2001) Abnormal distribution of aquaporin-5 water channel protein in salivary glands from Sjögren’s syndrome patients. Lab Investig 81, 143–8.
Stevens AL, Breton S, Gustafson CE et al. (2000) Aquaporin 2 is a vasopressin-independent, constitutive apical membrane protein in rat vas deferens. Am J Physiol Cell Physiol 278, C791–802.
Suzuki-Toyota F, Ishibashi K, Yuasa S (1999) Immunohisto-chemical localization of a water channel, aquaporin 7 (AQP7), in the rat testis. Cell Tissue Res 295, 279–85.
Tani T, Koyama Y, Nihei K et al. (2001) Immunolocalization of aquaporin-8 in rat digestive organs and testis. Arch Histol Cytol 64, 159–68.
Terris J, Ecelbarger CA, Marples D, Knepper MA, Nielsen S (1995) Distribution of aquaporin-4 water channel expression within rat kidney. Am J Physiol Renal Fluid Electrolyte Physiol 269, F775–85.
Vallon V, Verkman AS, Schnermann J (2000) Luminal hypotonicity in proximal tubules of aquaporin-1-knockout mice. Am J Physiol Renal Physiol 278, F1030–3.
Verbavatz JM, Ma T, Gobin R, Verkman AS (1997) Absence of orthogonal arrays in kidney, brain and muscle from trans-genic knockout mice lacking water channel aquaporin-4. J Cell Sci 110, 2855–60.
Walz T, Hirai T, Murata K et al. (1997) The three-dimensional structure of aquaporin-1. Nature 387, 624–7.
Wang KS, Komar AR, Ma T et al. (2000) Gastric acid secretion in aquaporin-4 knockout mice. Am J Physiol Gastrointest Liver Physiol 279, G448–53.
Wellner RB, Hoque ATMS, Goldsmith CM, Baum BJ (2000) Evidence that aquaporin-8 is located in the basolateral membrane of rat submandibular gland acinar cells. Pflügers Arch Eur J Physiol 441, 49–56.
Yamamoto T, Sasaki S, Fushimi K et al. (1995) Vasopressin increases AQP-CD water channel in apical membrane of collecting duct cells in Brattleboro rats. Am J Physiol Cell Physiol 268, C1546–51.
Yang B, Brown D, Verkman AS (1996) The mercurial insensitive water channel (AQP-4) forms orthogonal arrays in stably transfected chinese hamster ovary cells. J Biol Chem 271, 4577–80.
Yang B, Verbavatz JM, Song Y et al. (2000) Skeletal muscle function and water permeability in aquaporin-4 deficient mice. Am J Physiol Cell Physiol 278, C1108–15.
Yasui M, Hazama A, Kwon TH, Nielsen S, Guggino WB, Agre P (1999a) Rapid gating and anion permeability of an intracellular aquaporin. Nature 402, 184–7.
Yasui M, Kwon TH, Knepper MA, Nielsen S, Agre P (1999b) Aquaporin-6: an intracellular vesicle water channel protein in renal epithelia. Proc Natl Acad Sci USA 96, 5808–13.
Zampighi GA, Hall JE, Ehring GR, Simon SA (1989) The structural organization and protein composition of lens fiber junctions. J Cell Biol 108, 2255–75.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Matsuzaki, T., Tajika, Y., Tserentsoodol, N. et al. Aquaporins: a water channel family. Anato Sci Int 77, 85–93 (2002). https://doi.org/10.1046/j.0022-7722.2002.00020.x
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1046/j.0022-7722.2002.00020.x