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Cellular distribution of the aquaporins: A family of water channel proteins

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Abstract

A group of transmembrane proteins that are related to the major intrinsic protein of lens fibers (MIP26) have been named “aquaporins” to reflect their role as water channels. These proteins are located at strategic membrane sites in a variety of epithelia, most of which have well-defined physiological functions in fluid absorption or secretion. However, some aquaporins have been localized in cell types where their role is at present unknown. Most of the aquaporins are delivered to the plasma membrane in a non-regulated (constitutive) fashion, but AQP2 enters the regulated exocytotic pathway and its membrane expression is controlled by the action of the antidiuretic hormone, vasopressin. These pathways of constitutive versus regulated delivery to the plasma membrane have been reconstituted in transfected LLC-PK1 epithelial cells, indicating that the information encoded within the protein sequence is sufficient to allow sorting of newly synthesized protein into distinct intracellular vesicles. Finally, different members of the aquaporin family can be targeted to apical, basolateral or both apical and basolateral plasma membrane domains of polarized epithelial cells. This implies that signals for the polarized targeting of these proteins also is located in non-homologous regions of these similar proteins. Thus, future investigations on the aquaporin family of proteins will provide important information not only on the physiology of membrane transport processes in many cell types, but also on the targeting and trafficking signals that allow proteins to enter distinct intracellular vesicular pathways in epithelial cells. In the case of AQP2, the availability of the transfected cell culture system will allow the intracellular signaling pathway, and the accessory molecules that are involved in this pathway, to be dissected and identified.

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References

  • Abramov M, Beauwens R, Cogan E (1987) Cellular events in vasopressin action. Kidney Int 32 [Suppl 21]:S56-S66

    Google Scholar 

  • Agre P, Preston GM, Smith BL, Jung JS, Raina S, Moon C, Guggino WB, Nielsen S (1993) Aquaporin CHIP: the archetypal molecular water channel. Am J Physiol 265:F463-F476

    PubMed  Google Scholar 

  • Bachinsky DR, Sabolic I, Emmanouel DS, Jefferson DM, Carone FA, Brown D, Perrone RD (1995) Water channel expression in human ADPKD kidneys. Am J Physiol 268:F398-F403

    PubMed  Google Scholar 

  • Breton S, Alper SL, Gluck SL, Sly WS, Barker JE, Brown D (1995) Depletion of intercalated cells from collecting ducts of carbonic anhydrase II deficient (CAR2 null) mice. Am J Physiol [Renal, Fluid, Electrolyte Physiol] (in press)

  • Brown D (1989) Membrane recycling and epithelial cell function. Am J Physiol 256:F1-F12

    PubMed  Google Scholar 

  • Brown, D, Orci L (1983) Vasopressin stimulates the formation of coated pits in rat kidney collecting ducts. Nature 302:253–255

    PubMed  Google Scholar 

  • Brown D, Grosso A, DeSousa RC (1983) Correlation between water flow and intramembrane particle aggregates in toad epidermis. Am J Physiol 245:C334-C342

    PubMed  Google Scholar 

  • Brown D, Weyer P, Orci L (1988) Vasopressin stimulates endocytosis in kidney collecting duct epithelial cells. Eur J Cell Biol 46:336–340

    PubMed  Google Scholar 

  • Brown D, Verbavatz J-M, Valenti G, Lui B, Sabolic I (1993) Localization of the CHIP28 water channel in reabsorptive segments of the rat male reproductive tract. Eur J Cell Biol 61:264–273

    PubMed  Google Scholar 

  • Calamita G, Mola MG Svelto M (1994) Presence in frog urinary bladder of proteins immunologically related to the aquaporin-CHIP. Eur J Cell Biol 64:222–228

    PubMed  Google Scholar 

  • Chevalier J, Bourguet J, Hugon JS (1974) Membrane-associated particles: distribution in frog urinary bladder epithelium at rest and after oxytocin treatment. Cell Tissue Res 152:129–140

    PubMed  Google Scholar 

  • Corvera S, Chawla A, Chakrabarti R, Joly M, Buxton J, Czech MP (1994) A double leucine within the GLUT4 glucose transporter COOH-terminal domain functions as an endocytosis signal. J Cell Biol 126:979–989

    PubMed  Google Scholar 

  • Dunia I, Manenti S, Rousselet A, Benedetti EI (1987) Electron microscopic observations of reconstituted proteoliposomes with the purified major intrinsic membrane protein of eye lens fibers. J Cell Biol 105:1679–1689

    PubMed  Google Scholar 

  • Echevarria M, Windhager EE, Tate SS, Frindl G (1994) Cloning and expression of AQP3, a water channel from the medullary collecting duct of rat kidney. Proc Natl Acad Sci USA 91:10997–11001

    PubMed  Google Scholar 

  • Finkelstein A (1987) Water movement through lipid bilayers, pores and plasma membranes: theory and reality. In: Finkelstein A (ed) Distinguished lecture series of the Society of General Physiologists. Wiley Interscience, New York, pp 153–201

    Google Scholar 

  • Frigeri A, Gropper MA, Kawashima M, Brown D, Verkman AS (1995) Localization of MIWC and GLIP water channel homologs in neuromuscular, epithelial and glandular tissues. J Cell Sci (in press)

  • 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 361:549–552

    PubMed  Google Scholar 

  • Fushimi K, Sasaki S, Yamamoto T, Hayashi M, Furukawa T, Uchida S, Suwahara M, Ishibashi K, Kawasaki M, Kihara I, Marumo F (1994) Functional characterization and cell immunolocalization of AQP-CD water channel in kidney collecting duct. Am J Physiol 267:F573-F582

    PubMed  Google Scholar 

  • Harris HW Jr, Kikeri D, Janoshazi A, Solomon AK, Zeidel ML (1990) High proton flux through membranes containing antidiuretic water channels. Am J Physiol 259:F366-F371

    PubMed  Google Scholar 

  • Harris HW Jr, Strange K, Zeidel ML (1991) Current understanding of the cellular biology and molecular structure of the antidiuretic hormone-stimulated water transport pathway. J Clin Invest 88:1–8

    PubMed  Google Scholar 

  • Hasegawa H, Ma T, Skach W, Matthay MA, Verkman AS (1994) Molecular cloning of a mercurial-insensitive water channel expressed in selected water-transporting tissues. J Biol Chem 269:5497–5500

    PubMed  Google Scholar 

  • Ishibashi K, Sasaki S, Fushimi K, Uchida S, Kuwahara M, Saito H, Furukawa T, Nakajima K, Yamaguchi Y, Gojobori T, Marumo F (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 91:6269–6273

    PubMed  Google Scholar 

  • Jung FF, Tang S-S, Sabolic L, Verbavatz J-M, Diamant D, Brown D, Ingelfinger JR (1994a) Angiotensin II (ANG II) upregulates CHIP28 expression in immortalized, transformed rat proximal tubule cells (IRPTC). J Am Soc Nephrol 5:274a

    Google Scholar 

  • Jung JS, Bhat RV, Preston GM, Guggino WB, Baraban JM, Agre P (1994b) Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci USA 91:13052–13056

    PubMed  Google Scholar 

  • Kachadorian WA, Wade JB, DiScala VA (1975) Vasopressin: induced structural changes in road bladder luminal membrane. Science 190:67–69

    PubMed  Google Scholar 

  • Katsura T, Verbavatz J-M, Farinas J, Ma T, Ausiello DA, Verkman AS, Brown D (1995) Constitutive and regulated membrane expression of aquaporin-1 and aquaporin-2 water channels in stably transfected LLC-PK1 epithelial cells. Proc Natl Acad Sci USA (in press)

  • Knepper MA (1994) The aquaporin family of molecular water channels. Proc Natl Acad Sci USA 91:6255–6258

    PubMed  Google Scholar 

  • Ma T, Frigeri A, Tsai S-T, Verbavatz J-M, Verkman AS (1993) Localization and functional analysis of CHIP28k water channels in stably transfected Chinese hamster ovary cells. J Biol Chem 268:22756–22764

    PubMed  Google Scholar 

  • 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 269:21845–21849

    PubMed  Google Scholar 

  • Maurel C, Reizer J, Schroeder JI, Chrispeels MJ (1993) The vacuolar membrane protein gamma-TIP creates water specific channels inXenopus oocytes. EMBO J 12:2241–2247

    PubMed  Google Scholar 

  • Nielsen S, DiGiovanni SR, Christensen EI, Knepper MA, Harris HW (1993a) Cellular and subcellular immunolocalization of vasopressin-regulated water channel in rat kidney. Proc Natl Acad Sci USA 90:11663–11667

    PubMed  Google Scholar 

  • Nielsen S, Smith BL, Christensen EI, Agre P (1993b) Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capilary endothelia. Proc Natl Acad Sci USA 90:7275–7279

    PubMed  Google Scholar 

  • Nielsen S, Smith BL, Christensen EI, Knepper MA, Agre P (1993c) CHIP28 water channels are localized in constitutively water permeable segments of the nephron. J Cell Biol 120:371–383

    PubMed  Google Scholar 

  • Nielsen S, Chou C-L, Marples D, Christensen EI, Kishore BK, Knepper MA (1995) Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci USA 92:1013–1017

    PubMed  Google Scholar 

  • Orci L, Humbert F, Brown D, Perrelet A (1981) Membrane ultrastructure in urinary tubules. Int Rev Cytol 73:183–242

    PubMed  Google Scholar 

  • 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 88:11110–11114

    PubMed  Google Scholar 

  • Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels inXenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387

    PubMed  Google Scholar 

  • Preston GM, Jung JS, Guggino WB, Agre P (1993) The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel. J Biol Chem 268:17–20

    PubMed  Google Scholar 

  • Raina S, Preston GM, Guggino WB, Agre P (1995) Molecular cloning and characterization of an aquaporin cDNA from salivary, lacrimal, and respiratory tissues. J Biol Chem 270:1908–1912

    PubMed  Google Scholar 

  • Sabolic I, Valenti G, Verbavatz J-M, Van Hoek AN, Verkman AS Ausiello DA, Brown D (1992) Localization of the CHIP28 water channel in rat kidney. Am J Physiol 263:C1225-C1233

    PubMed  Google Scholar 

  • Sabolic I, Katsura T, Verbavatz J-M, Brown D (1995) The AQP2 water channel: effect of vasopressin treatment, microtubule disruption, and distribution in neonatal rats. J Membr Biol 143:165–175

    Google Scholar 

  • Sasaki S, Fushimi K, Saito H, Saito F, Uchida S, Ishibashi K, Kuwahara M, Ikeuchi T, Inui K, Nakajima K, Watanabe TX, Marumo F (1994) Cloning, characterization, and chromosomal mapping of human aquaporin of collecting duct. J Clin Invest 93:1250–1256

    PubMed  Google Scholar 

  • Shi L-B, Brown D, Verkman AS (1990) Water, proton and urea transport in toad bladder endosomes that contain the vasopressin-sensitive water channel. J Gen Physiol 95:941–960

    PubMed  Google Scholar 

  • Smith BL, Agre P (1991) Erythrocyte Mr 28,000 transmembrane protein exists as a multisubunit oligomer similar to channel proteins. J Biol Chem 266:6407–6415

    PubMed  Google Scholar 

  • Stamer WD, Snyder RW, Smith BL, Agre P, Regan JW (1994) Localization of aquaporin CHIP in the human eye: implications in the pathogenesis of glaucoma and other disorders of ocular fluid balance. Invest Ophthalmol Vis Sci 35:3867–3872

    PubMed  Google Scholar 

  • Stankovic T, Adams JC, Brown D (1995) Immunolocalization of aquaporin CHIP in the guinea pig inner ear. Am J Physiol [Cell Physiol] (in press)

  • Strange K, Spring KR (1987) Cell membrane water permeability of rabbit cortical collecting duct. J Membr Biol 96:27–43

    PubMed  Google Scholar 

  • Strange K, Willingham MC, Handler JS, Harris HW Jr (1988) Apical membrane endocytosis via coated pits is stimulated by removal of antidiuretic hormone from isolated, perfused rabbit cortical collecting tubule. J Membr Biol 103:17–28

    PubMed  Google Scholar 

  • Valenti G, Verbavatz J-M, Sabolic I, Ausiello DA, Verkman AS, Brown D (1994) A basolateral CHIP28/MIP26-related protein (BLIP) in kidney principal cells and gastric parietal cells. Am J Physiol 267:C812-C820

    PubMed  Google Scholar 

  • Vallon O, Dunia I, Favard-Sereno C, Hoebeke J, Benedetti EL (1985) MP26 in the bovine lens: a post-embedding immunocytochemical study. Biol Cell 53:85–88

    PubMed  Google Scholar 

  • Van Hoek A, Hom M, Luthjen L, Jong M de, Dempster J, Van Os C (1991) Functional unit of 30 kDa for proximal tubule water channels as revealed by radiation inactivation. J Biol Chem 266:16633–16635

    PubMed  Google Scholar 

  • Van Hoek AN, Verkman AS (1992) Functional reconstitution of the isolated erythrocyte water channel CHIP28. J Biol Chem 267:18267–18269

    PubMed  Google Scholar 

  • Verbavatz J-M, Brown D, Sabolic I, Valenti G, Van Hoek AN, Ma T, Ausiello DA, Verkman AS (1993) Tetrameric assembly of CHIP28 water channels in liposomes and cell membranes: a freeze-fracture study. J Cell Biol 123:605–618

    PubMed  Google Scholar 

  • Verbavatz J-M, Van Hoek AN, Ma T, Sabolic I, Valenti G, Ellisman MH, Ausiello DA, Verkman AS, Brown D (1994) A 28 kD sarcolemmal antigen in kidney principal cell basolateral membranes: relationship to orthogonal arrays and MIP26. J Cell Sci 107:1083–1094

    PubMed  Google Scholar 

  • Verhey KJ, Birnbaum MJ (1994) A Leu-Leu sequence is essential for COOH-terminal targeting signal of GLUT4 glucose transporter in fibroblasts. J Biol Chem 269:2353–2356

    PubMed  Google Scholar 

  • Verkman AS (1992) Water channels in cell membranes. Annu Rev Physiol 54:97–106

    PubMed  Google Scholar 

  • Verkman AS, Lencer WI, Brown D, Ausiello DA (1988) Endosomes from kidney collecting tubule cells contain the vasopressin-sensitive water channel. Nature 333:268–269

    PubMed  Google Scholar 

  • Wade JB, Stetson DL, Lewis SA (1981) ADH action: evidence for a membrane shuttle mechanism. Ann N Y Acad Sci 372:106–117

    PubMed  Google Scholar 

  • Zeidel ML, Ambudkar SV, Smith BL, Agre P (1992) Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochemistry 31:7436–7440

    PubMed  Google Scholar 

  • Zhang R, Skach W, Hasegawa H, Van Hoek AN, Verkman AS (1993a) Cloning, functional analysis and cell localization of a kidney proximal rubule water transporter homologous to CHIP28. J Cell Biol 120:359–369

    PubMed  Google Scholar 

  • Zhang R, Van Hoek A, Biwersi J, Verkman A (1993b) A point mutation at cysteine 189 blocks the water permeability of rat kidney water channel CHIP28k. Biochemistry 32:2938–2941

    PubMed  Google Scholar 

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Brown, D., Katsura, T., Kawashima, M. et al. Cellular distribution of the aquaporins: A family of water channel proteins. Histochem Cell Biol 104, 1–9 (1995). https://doi.org/10.1007/BF01464780

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