Skip to main content
Log in

Invertebrate aquaporins: a review

  • Review
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Aquaporins (AQPs) or water channels render the lipid bilayer of cell membranes permeable to water. The numerous AQP subtypes present in any given species, the transport properties of each subtype and the variety of methods of their regulation allows different cell types to be transiently or permanently permeable to water or other solutes that AQPs are capable of transporting (e.g. urea or glycerol). AQPs have been well characterized in all vertebrate classes, other than reptilia. Here we review the current state of knowledge of invertebrate AQPs set in the context of the much more thoroughly studied vertebrate AQPs. By phylogenetic analysis of the total AQP complement of several completed insect genomes, we propose a classification system of insect AQPs including three sub-families (DRIP, BIB and PRIP) that have one representative from all the complete insect genomes. The physiological role of AQPs in invertebrates (insects, ticks and nematodes) is discussed, including their function in common invertebrate phenomena such as high-volume liquid diets, cryoprotection and anhydrobiosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Agre P (2000) Aquaporin water channels in kidney. J Am Soc Nephrol 11:764–777

    PubMed  CAS  Google Scholar 

  • Agre P, Saboori AM, Asimos A, Smith BL (1987) Purification and partial characterization of the Mr 30, 000 integral membrane-protein associated with the erythrocyte Rh(d) antigen. J Biol Chem 262:17497–17503

    PubMed  CAS  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  CAS  Google Scholar 

  • Agre P, Bonhivers M, Borgnia MJ (1998) The aquaporins, blueprints for cellular plumbing systems. J Biol Chem 273:14659–14662

    Article  PubMed  CAS  Google Scholar 

  • Alcala J, Lieska N, Maisel H (1975) Protein composition of bovine lens cortical fiber cell-membranes. Exp Eye Res 21:581–595

    Article  PubMed  CAS  Google Scholar 

  • Anthony TL, Brooks HL, Boassa D, Leonov S, Yanochko GM, Regan JW, Yool AJ (2000) Cloned human aquaporin-1 is a cyclic GMP-gated ion channel. Mol Pharmacol 57:576–588

    PubMed  CAS  Google Scholar 

  • Bahamontes-Rosa N, Robin A, Ambrosio AR, Messias-Reason I, Beitz E, Flitsch SL, Kun JFJ (2008) Monoquaternary ammonium derivatives inhibit growth of protozoan parasites. Parasitol Int 57:132–137

    Article  PubMed  CAS  Google Scholar 

  • Baker ME, Saier MH (1990) A common ancestor for bovine lens fiber major intrinsic protein, soybean nodulin-26 protein, and Escherichia coli glycerol facilitator. Cell 60:185–186

    Article  PubMed  CAS  Google Scholar 

  • Beitz E (2000) TEXtopo: shaded membrane protein topology plots in LaTEX2. Bioinformatics 6:1050–1051

    Article  Google Scholar 

  • Beitz E (2005) Aquaporins from pathogenic protozoan parasites: structure, function and potential for chemotherapy. Biol Cell 97:373–383

    Article  PubMed  CAS  Google Scholar 

  • Beitz E (2006) Aquaporin water and solute channels from malaria parasites and other pathogenic protozoa. Chemmedchem 1:587–592

    Article  PubMed  CAS  Google Scholar 

  • Beitz E, Wu BH, Holm LM, Schultz JE, Zeuthen T (2006) Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons. Proc Natl Acad Sci USA 103:269–274

    Article  PubMed  CAS  Google Scholar 

  • Beuron F, Lecaherec F, Guillam MT, Cavalier A, Garret A, Tassan JP, Delamarche C, Schultz P, Mallouh V, Rolland JP, Hubert JF, Gouranton J, Thomas D (1995) Structural-analysis of at MIP family protein from the digestive-tract of Cicadella viridis. J Biol Chem 270:17414–17422

    Article  PubMed  CAS  Google Scholar 

  • Borgnia M, Nielsen S, Engel A, Agre P (1999) Cellular and molecular biology of the aquaporin water channels. Annu Rev Biochem 68:425–458

    Article  PubMed  CAS  Google Scholar 

  • Bowman AS, Sauer JR (2004) Tick salivary glands: function, physiology and future. Parasitology 129:S67–S81

    Article  PubMed  Google Scholar 

  • Bowman AS, Ball A, Sauer JR (2008) Tick salivery glands: the physiology of tick water balance and their role in pathogen trafficking and transmission. In: Bowman AS, Nuttall PA (eds) Ticks: biology, disease and control. Cambridge University Press, Cambridge, pp 73–91

    Google Scholar 

  • Cady C, Hagedorn HH (1999) The effect of putative diuretic factors on in vivo urine production in the mosquito, Aedes aegypti. J Insect Physiol 45:317–325

    Article  PubMed  CAS  Google Scholar 

  • Calamita G, Bishai WR, Preston GM, Guggino WB, Agre P (1995) Molecular-cloning and characterization of AQPz, a water channel from Escherichia coli. J Biol Chem 270:29063–29066

    Article  PubMed  CAS  Google Scholar 

  • Carbrey JM, Gorelick-Feldman DA, Kozono D, Praetorius J, Nielsen S, Agre P (2003) Aquaglyceroporin AQP9: solute permeation and metabolic control of expression in liver. Proc Natl Acad Sci USA 100:2945–2950

    Article  PubMed  CAS  Google Scholar 

  • Casotti G, Waldron T, Misquith G, Powers D, Slusher L (2007) Expression and localization of an aquaporin-1 homologue in the avian kidney and lower intestinal tract. Comp Biochem Physiol A Mol Integr Physiol 147:355–362

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarti N, Roux B, Pomes R (2004a) Structural determinants of proton blockage in aquaporins. J Mol Biol 343:493–510

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarti N, Tajkhorshid E, Roux B, Pomes R (2004b) Molecular basis of proton blockage in aquaporins. Structure 12:65–74

    Article  PubMed  CAS  Google Scholar 

  • Chandy G, Zampighi GA, Kreman M, Hall JE (1997) Comparison of the water transporting properties of MIP and AQP1. J Membr Biol 159:29–39

    Article  PubMed  CAS  Google Scholar 

  • Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 125:1206–1215

    Article  PubMed  CAS  Google Scholar 

  • Chepelinsky AB (2003) The ocular lens fiber membrane specific protein MIP. J Exp Zool Part A 300A:41–46

    Article  CAS  Google Scholar 

  • Chretien S, Cartron JP, de Figueiredo M (1999) A single mutation inside the NPA motif of aquaporin-1 found in a Colton-null phenotype. Blood 93:4021–4023

    PubMed  CAS  Google Scholar 

  • Cutler C (2007) Aquaporin channels in teleost and elasmobranch fish. Comp Biochem Physiol A Mol Integr Physiol 146:S89–S89

    Article  Google Scholar 

  • Cutler CP, Martinez AS, Cramb G (2007) The role of aquaporin 3 in teleost fish. Comp Biochem Physiol A Mol Integr Physiol 148:82–91

    Article  PubMed  CAS  Google Scholar 

  • Deen PMT, Verdijk MAJ, Knoers NVAM, Wieringa B, Monnens LAH, Vanos CH, Vanoost BA (1994) Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine. Science 264:92–95

    Article  PubMed  CAS  Google Scholar 

  • Deen PMT, Croes H, Vanaubel RAMH, Ginsel LA, Vanos CH (1995) Water channels encoded by mutant aquaporin-2 genes in nephrogenic diabetes-insipidus are impaired in their cellular routing. J Clin Invest 95:2291–2296

    Article  PubMed  CAS  Google Scholar 

  • Delporte C, Steinfeld S (2006) Distribution and roles of aquaporins in salivary glands. Biochim Biophys Acta 1758:1061–1070

    Article  PubMed  CAS  Google Scholar 

  • Denker BM, Smith BL, Kuhajda FP, Agre P (1988) Identification, purification, and partial characterization of a novel Mr 28, 000 integral membrane protein from erythrocytes and renal tubules. J Biol Chem 263:15634–15642

    PubMed  CAS  Google Scholar 

  • Doherty D, Jan LY, Jan YN (1997) The Drosophila neurogenic gene big brain, which encodes a membrane-associated protein, acts cell autonomously and can act synergistically with Notch and Delta. Development 124:3881–3893

    PubMed  CAS  Google Scholar 

  • Dow JAT, Davies SA (2000) Integrative physiology of the V-ATPase in Drosophila melanogaster. Comp Biochem Physiol A Mol Integr Physiol 126A:S44

    Article  Google Scholar 

  • Dow JAT, Davies SA (2001) The Drosophila melanogaster Malpighian tubule. Adv Insect Physiol 28:1–83

    Article  CAS  Google Scholar 

  • Dow JAT, Davies SA (2003) Integrative physiology and functional genomics of epithelial function in a genetic model organism. Physiol Rev 83:687–729

    PubMed  CAS  Google Scholar 

  • Dow JAT, Kelly DC, Davies SA, Maddrell SHP, Brown D (1995) A novel member of the major intrinsic protein family in Drosophila—are aquaporins involved in insect Malpighian (renal) tubule fluid secretion? J Physiol 489P:P110–P111

    Google Scholar 

  • Drake KD, Schuette D, Chepelinsky AB, Jacob TJ, Crabbe MJC (2002) pH-dependent channel activity of heterologously-expressed main intrinsic protein (MIP) from rat lens. FEBS Lett 512:199–204

    Article  PubMed  CAS  Google Scholar 

  • Duchesne L, Hubert JF, Verbavatz JM, Thomas D, Pietrantonio PV (2003) Mosquito (Aedes aegypti) aquaporin, present in tracheolar cells, transports water, not glycerol, and forms orthogonal arrays in Xenopus oocyte membranes. Eur J Biochem 270:422–429

    Article  PubMed  CAS  Google Scholar 

  • Echevarria M, Ramirez-Lorca R, Hernandez CS, Gutierriez A, Mendez-Ferrer S, Gonzalez E, Toledo-Aral JJ, Ilundain AA, Whittembury G (2001) Identification of a new water channel (Rp-MIP) in the Malpighian tubules of the insect Rhodnius prolixus. Pflugers Arch 442:27–34

    Article  PubMed  CAS  Google Scholar 

  • Edashige K, Yamaji Y, Kleinhans FW, Kasai M (2003) Artificial expression of aquaporin-3 improves the survival of mouse oocytes after cryopreservation. Biol Reprod 68:87–94

    Article  PubMed  CAS  Google Scholar 

  • Elvin CM, Bunch R, Liyou NE, Pearson RD, Gough J, Drinkwater RD (1999) Molecular cloning and expression in Escherichia coli of an aquaporin-like gene from adult buffalo fly (Haematobia irritans exigua). Insect Mol Biol 8:369–380

    Article  PubMed  CAS  Google Scholar 

  • Endeward V, Musa-Aziz R, Cooper GJ, Chen LM, Pelletier MF, Virkki LV, Supuran CT, King LS, Boron WF, Gros G (2006) Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. Faseb J 20:1974–1981

    Article  PubMed  CAS  Google Scholar 

  • Figarella K, Uzcategui NL, Zhou Y, LeFurgey A, Ouellette M, Bhattacharjee H, Mukhopadhyay R (2007) Biochemical characterization of Leishmania major aquaglyceroporin LmAQP1: possible role in volume regulation and osmotaxis. Mol Microbiol 65:1006–1017

    Article  PubMed  CAS  Google Scholar 

  • Fu D, Lu M (2007) The structural basis of water permeation and proton exclusion in aquaporins. Mol Membr Biol 24:366–374

    Article  PubMed  CAS  Google Scholar 

  • Funaki H, Yamamoto T, Koyama Y, Kondo D, Yaoita E, Kawasaki K, Kobayashi H, Sawaguchi S, Abe H, Kihara I (1998) Localization and expression of AQP5 in cornea, serous salivary glands, and pulmonary epithelial cells. Am J Physiol Cell Physiol 275:C1151–C1157

    CAS  Google Scholar 

  • Fuse M, Davey KG, Sommerville RI (1993) Osmoregulation in the parasitic nematode Pseudoterranova decipiens. J Exp Biol 175:127–142

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Gazzarrini S, Kang M, Epimashko S, Van Etten JL, Dainty J, Thiel G, Moroni A (2006) Chlorella virus MT325 encodes water and potassium channels that interact synergistically. Proc Natl Acad Sci USA 103:5355–5360

    Article  PubMed  CAS  Google Scholar 

  • Giffard-Mena I, Boulo V, Aujoulat F, Fowden H, Castille R, Charmantier G, Cramb G (2007) Aquaporin molecular characterization in the sea-bass (Dicentrarchus labrax): the effect of salinity on AQP1 and AQP3 expression. Comp Biochem Physiol A Mol Integr Physiol 148:430–444

    Article  PubMed  CAS  Google Scholar 

  • Gonen T, Walz T (2006) The structure of aquaporins. Q Rev Biophys 39:361–396

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Gouranton J (1968) Ultrastructure relative to water transport so-called filtering chambers of Cicadella viridis L. (Homoptera jassidae). J Microsc-Oxford 7:559

    Google Scholar 

  • Gresz V, Kwon TH, Hurley PT, Varga G, Zelles T, Nielsen S, Case RM, Steward MC (2001) Identification and localization of aquaporin water channels in human salivary glands. Am J Physiol Gastrointest Liver Physiol 281:G247–G254

    PubMed  CAS  Google Scholar 

  • de Groot BL, Grubmueller H (2003) Structure, dynamics and mechanism of water permeation through aquaporins. Eur Biophys J 32:182

    Google Scholar 

  • de Groot BL, Grubmuller H (2001) Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science 294:2353–2357

    Article  PubMed  Google Scholar 

  • de Groot BL, Grubmuller H (2005) The dynamics and energetics of water permeation and proton exclusion in aquaporins. Curr Opin Struct Biol 15:176–183

    Article  PubMed  CAS  Google Scholar 

  • Gros G, Virkki L, King LS, Cartron JP, Boron WF, Endeward V (2005) Aquaporin 1 is a CO2 channel in human red cell membranes. FASEB J 19:A1156

    Google Scholar 

  • Gunnarson E, Zelenina M, Aperia A (2004) Regulation of brain aquaporins. Neuroscience 129:947–955

    Article  PubMed  CAS  Google Scholar 

  • Hagedorn M, Lance SL, Fonseca DM, Kleinhans FW, Artimov D, Fleischer R, Hoque ATMS, Hamilton MB, Pukazhenthi BS (2002) Altering fish embryos with aquaporin-3: an essential step toward successful cryopreservation. Biol Reprod 67:961–966

    Article  PubMed  CAS  Google Scholar 

  • Han ZQ, Wax MB, Patil RV (1998) Regulation of aquaporin-4 water channels by phorbol ester-dependent protein phosphorylation. J Biol Chem 273:6001–6004

    Article  PubMed  CAS  Google Scholar 

  • Hansen M, Kun JFJ, Schultz JE, Beitz E (2002) A single, bi-functional aquaglyceroporin in blood-stage Plasmodium falciparum malaria parasites. J Biol Chem 277:4874–4882

    Article  PubMed  CAS  Google Scholar 

  • Hara-Chikuma M, Verkman AS (2003) Glycerol replacement corrects defective skin hydration, elasticity, and barrier function in aquaporin-3-deficient mice. Proc Natl Acad Sci USA 100:7360–7365

    Article  CAS  Google Scholar 

  • Hara-Chikuma M, Verkman AS (2005) Aquaporin-3 functions as a glycerol transporter in mammalian skin. Biol Cell 97:479–486

    Article  PubMed  CAS  Google Scholar 

  • Hara-Chikuma M, Sohara E, Rai T, Ikawa M, Okabe M, Sasaki S, Uchida S, Verkman AS (2005) Progressive adipocyte hypertrophy in aquaporin-7-deficient mice—adipocyte glycerol permeability as a novel regulator of fat accumulation. J Biol Chem 280:15493–15496

    Article  PubMed  CAS  Google Scholar 

  • Henzler T, Steudle E (2000) 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 51:2053–2066

    Article  PubMed  CAS  Google Scholar 

  • Herrera M, Hong NJ, Garvin JL (2006) Aquaporin-1 transports NO across cell membranes. Hypertension 48:157–164

    Article  PubMed  CAS  Google Scholar 

  • Hibuse T, Maeda N, Nagasawa A, Funahashi T (2006) Aquaporins and glycerol metabolism. Biochim Biophys Acta 1758:1004–1011

    Article  PubMed  CAS  Google Scholar 

  • Hiroaki Y, Tani K, Kamegawa A, Gyobu N, Nishikawa K, Suzuki H, Walz T, Sasaki S, Mitsuoka K, Kimura K, Mizoguchi A, Fujiyoshi Y (2006) Implications of the aquaporin-4 structure on array formation and cell adhesion. J Mol Biol 355:628–639

    Article  PubMed  CAS  Google Scholar 

  • Holmes SP, Li D, Ceraul SM, Azad AF (2008) An aquaporin-like protein from the ovaries and gut of American dog tick (Acari: Ixodidae). J Med Entomol 45:68–74

    Article  PubMed  CAS  Google Scholar 

  • Huang CG, Lamitina T, Agre P, Strange K (2007) Functional analysis of the aquaporin gene family in Caenorhabditis elegans. Am J Physiol Cell Physiol 292:C1867–C1873

    Article  PubMed  CAS  Google Scholar 

  • Hub JS, De Groot BL (2008) Mechanism of selectivity in aquaporins and aquaglyceroporins. Proc Natl Acad Sci USA 105:1198–1203

    Article  PubMed  CAS  Google Scholar 

  • Ishibashi K (2006) Aquaporin subfamily with unusual NPA boxes. Biochim Biophys Acta 1758:989–993

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa Y, Ishida H (2000) Aquaporin water channel in salivary glands. Jpn J Pharmacol 83:95–101

    Article  PubMed  CAS  Google Scholar 

  • Izumi Y, Sonoda S, Yoshida H, Danks HV, Tsumuki H (2006) Role of membrane transport of water and glycerol in the freeze tolerance of the rice stem borer, Chilo suppressalis walker (Lepidoptera: Pyralidae). J Insect Physiol 52:215–220

    Article  PubMed  CAS  Google Scholar 

  • Izumi Y, Sonoda S, Tsumuki H (2007) Effects of diapause and cold-acclimation on the avoidance of freezing injury in fat body tissue of the rice stem borer, Chilo suppressalis walker. J Insect Physiol 53:685–690

    Article  PubMed  CAS  Google Scholar 

  • Jahn TP, Moller ALB, Zeuthen T, Holm LM, Klaerke DA, Mohsin B, Kuhlbrandt W, Schjoerring JK (2004) Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett 574:31–36

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jung JS, Preston GM, Smith BL, Guggino WB, Agre P (1994b) Molecular structure of the water channel through aquaporin CHIP—the hourglass model. J Biol Chem 269:14648–14654

    PubMed  CAS  Google Scholar 

  • Kaldenhoff R, Fischer M (2006) Functional aquaporin diversity in plants. Biochim Biophys Acta 1758:1134–1141

    Article  PubMed  CAS  Google Scholar 

  • Kaufmann N, Mathai JC, Hill WG, Dow JAT, Zeidel ML, Brodsky JL (2005) Developmental expression and biophysical characterization of a Drosophila melanogaster aquaporin. Am J Physiol Cell Physiol 289:C397–C407

    Article  PubMed  CAS  Google Scholar 

  • Kikawada T, Saito A, Kanamori Y, Fujita M, Snigorska K, Watanabe M, Okuda T (2008) Dehydration-inducible changes in expression of two aquaporins in the sleeping Chironomid, Polypedilum vanderplanki. Biochim Biophys Acta 1778:514–520

    Article  PubMed  CAS  Google Scholar 

  • Kishida K, Kuriyama H, Funahashi T, Shimomura I, Kihara S, Ouchi N, Nishida M, Nishizawa H, Matsuda M, Takahashi M, Hotta K, Nakamura T, Yamashita S, Tochino Y, Matsuzawa Y (2000) Aquaporin adipose, a putative glycerol channel in adipocytes. J Biol Chem 275:20896–20902

    Article  PubMed  CAS  Google Scholar 

  • Krane CM, Goldstein DL (2007) Comparative functional analysis of aquaporins. Mamm Genome 18:452–462

    Article  PubMed  CAS  Google Scholar 

  • Kuwahara M, Ishibashi K, Gu Y, Terada Y, Kohara Y, Marumo F, Sasaki S (1998) A water channel of the nematode C. elegans and its implications for channel selectivity of MIP proteins. Am J Physiol 275:C1459–C1464

    PubMed  CAS  Google Scholar 

  • Kuwahara M, Asai T, Sato K, Shinbo I, Terada Y, Marumo F, Sasaki S (2000) Functional characterization of a water channel of the nematode Caenorhabditis elegans. Biochim Biophys Acta 1517:107–112

    PubMed  CAS  Google Scholar 

  • LeCaherec F, Bron P, Verbavatz JM, Garret A, Morel G, Cavalier A, Bonnec G, Thomas D, Gouranton J, Hubert JF (1996a) Incorporation of proteins into (Xenopus) oocytes by proteoliposome microinjection: functional characterization of a novel aquaporin. J Cell Sci 109:1285–1295

    CAS  Google Scholar 

  • LeCaherec F, Deschamps S, Delamarche C, Pellerin I, Bonnec G, Guillam MT, Thomas D, Gouranton J, Hubert JF (1996b) Molecular cloning and characterization of an insect aquaporin—functional comparison with aquaporin 1. Eur J Biochem 241:707–715

    Article  CAS  Google Scholar 

  • LeCaherec F, Guillam MT, Beuron F, Cavalier A, Thomas D, Gouranton J, Hubert JF (1997) Aquaporin-related proteins in the filter chamber of Homopteran insects. Cell Tissue Res 290:143–151

    Article  CAS  Google Scholar 

  • Lee DW, Pietrantonio PV (2003) In vitro expression and pharmacology of the 5-HT7-like receptor present in the mosquito Aedes aegypti tracheolar cells and hindgut-associated nerves. Insect Mol Biol 12:561–569

    Article  PubMed  CAS  Google Scholar 

  • Lee WK, Thevenod F (2006) A role for mitochondrial aquaporins in cellular life-and-death decisions? Am J Physiol Cell Physiol 291:C195–C202

    Article  PubMed  CAS  Google Scholar 

  • Lee KS, Kim SR, Lee SM, Lee KR, Sohn HD, Jin BR (2001) Molecular cloning and expression of a cDNA encoding the aquaporin homologue from the firefly, Pyrocoelia rufa. Korean J Entomology 31:269–279

    CAS  Google Scholar 

  • Liu ZJ, Shen J, Carbrey JM, Mukhopadhyay R, Agre P, Rosen BP (2002) Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc Natl Acad Sci USA 99:6053–6058

    Article  PubMed  CAS  Google Scholar 

  • Liu ZJ, Styblo M, Rosen BP (2006) Methylarsonous acid transport by aquaglyceroporins. Environ Health Perspect 114:527–531

    Article  PubMed  CAS  Google Scholar 

  • Liu YJ, Promeneur D, Rojek A, Kumar N, Frokiaer J, Nielsen S, King LS, Agre P, Carbrey JM (2007) Aquaporin 9 is the major pathway for glycerol uptake by mouse erythrocytes, with implications for malarial virulence. Proc Natl Acad Sci USA 104:12560–12564

    Google Scholar 

  • Loukas A, Hunt P, Maizels RM (1999) Cloning and expression of an aquaporin-like gene from a parasitic nematode. Mol Biochem Parasitol 99:287–293

    Article  PubMed  CAS  Google Scholar 

  • Maddrell SHP (1963) Excretion in blood-sucking bug, Rhodnius prolixus Stal. 1. The control of diuresis. J Exp Biol 40:247–257

    CAS  Google Scholar 

  • Mah AK, Armstrong KR, Chew DS, Chu JS, Tu DK, Johnsen RC, Chen N, Chamberlin HM, Baillie DL (2007) Transcriptional regulation of AQP-8, a Caenorhabditis elegans aquaporin exclusively expressed in the excretory system, by the POU homeobox transcription factor CEH-6. J Biol Chem 282:28074–28086

    Article  PubMed  CAS  Google Scholar 

  • Martini SV, Goldenberg RC, Fortes FSA, Campos-de-Carvalho AC, Falkenstein D, Morales MM (2004) Rhodnius prolixus Malpighian tubule’s aquaporin expression is modulated by 5-hydroxytryptamine. Arch Insect Biochem Physiol 57:133–141

    Article  PubMed  CAS  Google Scholar 

  • Mathai JC, Agre P (1999) Hourglass pore-forming domains restrict aquaporin-1 tetramer assembly. Biochemistry 38:923–928

    Article  PubMed  CAS  Google Scholar 

  • Mitra BN, Yoshino R, Morio T, Yokoyama M, Maeda M, Urushihara H, Tanaka Y (2000) Loss of a member of the aquaporin gene family, aqpA affects spore dormancy in Dictyostelium. Gene 251:131–139

    Article  PubMed  CAS  Google Scholar 

  • Mitsuoka K, Murata K, Walz T, Hirai T, Agre P, Heymann JB, Engel A, Fujiyoshi Y (1999) The structure of aquaporin-1 at 4.5-angstrom resolution reveals short alpha-helices in the center of the monomer. J Struct Biol 128:34–43

    Article  PubMed  CAS  Google Scholar 

  • Montalvetti A, Rohloff P, Docampo R (2004) A functional aquaporin co-localizes with the vacuolar proton pyrophosphatase to acidocalcisomes and the contractile vacuole complex of Trypanosoma cruzi. J Biol Chem 279:38673–38682

    Article  PubMed  CAS  Google Scholar 

  • Morishita Y, Sakube Y, Sasaki S, Ishibashi K (2004) Molecular mechanisms and drug development in aquaporin water channel diseases: aquaporin superfamily (superaquaporins): expansion of aquaporins restricted to multicellular organisms. J Pharmacol Sci 96:276–279

    Article  PubMed  CAS  Google Scholar 

  • Mulders SM, Preston GM, Deen PMT, Guggino WB, Vanos CH, Agre P (1995) Water channel properties of major intrinsic protein of lens. J Biol Chem 270:9010–9016

    Article  PubMed  CAS  Google Scholar 

  • Murata K, Mitsuoka K, Hirai T, Walz T, Agre P, Heymann JB, Engel A, Fujiyoshi Y (2000) Structural determinants of water permeation through aquaporin-1. Nature 407:599–605

    Article  PubMed  CAS  Google Scholar 

  • Nejsum LN, Zelenina M, Aperia A, Frokiaer J, Nielsen S (2005) Bidirectional regulation of AQP2 trafficking and recycling: involvement of AQP2–S256 phosphorylation. Am J Physiol Renal Physiol 288:F930–F938

    Article  PubMed  CAS  Google Scholar 

  • Nemeth-Cahalan KL, Kalman K, Hall JE (2004) Molecular basis of pH and Ca2+ regulation of aquaporin water permeability. J Gen Physiol 123:573–580

    Article  PubMed  CAS  Google Scholar 

  • Nemeth-Cahalan KL, Kalman K, Froger A, Hall JE (2007) Zinc modulation of water permeability reveals that aquaporin 0 functions as a cooperative tetramer. J Gen Physiol 130:457–464

    Article  PubMed  CAS  Google Scholar 

  • Nishihara E, Yokota E, Tazaki A, Orii H, Katsuhara M, Kataoka K, Igarashi H, Moriyama Y, Shimmen T, Sonobe S (2008) Presence of aquaporin and V-ATPase on the contractile vacuole of Amoeba proteus. Biol Cell 100:179–188

    Article  PubMed  CAS  Google Scholar 

  • Nishimoto G, Sasaki G, Yaoita E, Nameta M, Li HP, Furuse K, Fujinaka H, Yoshida Y, Mitsudome A, Yamamoto T (2007) Molecular characterization of water-selective AQP (EbAQP4) in hagfish: insight into ancestral origin of AQP4. Am J Physiol Regul Integr Comp Physiol 292:R644–R651

    PubMed  CAS  Google Scholar 

  • van Os CH, Kamsteeg EJ, Marr N, Deen PMT (2000) Physiological relevance of aquaporins: luxury or necessity? Pflugers Arch 440:513–520

    PubMed  Google Scholar 

  • Pao GM, Wu LF, Johnson KD, Hofte H, Chrispeels MJ, Sweet G, Sandal NN, Saier MH (1991) Evolution of the MIP family of integral membrane-transport proteins. Mol Microbiol 5:33–37

    Article  PubMed  CAS  Google Scholar 

  • Pavlovic-Djuranovic S, Schultz JE, Beitz E (2003) A single aquaporin gene encodes a water/glycerol/urea facilitator in Toxoplasma gondii with similarity to plant tonoplast intrinsic proteins. FEBS Lett 555:500–504

    Article  PubMed  CAS  Google Scholar 

  • Philip BN, Yi SX, Elnitsky MA, Lee RE (2008) Aquaporins play a role in desiccation and freeze tolerance in larvae of the goldenrod gall fly, Eurosta solidaginis. J Exp Biol 211:1114–1119

    Article  PubMed  CAS  Google Scholar 

  • Pietrantonio PV, Jagge C, Keeley LL, Ross LS (2000) Cloning of an aquaporin-like cDNA and in situ hybridization in adults of the mosquito Aedes aegypti (Diptera: Culicidae). Insect Mol Biol 9:407–418

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Preston GM, Carroll TP, Guggino WB, Agre P (1992b) CHIP28 is the membrane water channel of red-cells and proximal renal tubules. Clin Res 40:A252

    Google Scholar 

  • Preston GM, Jung JS, Guggino WB, Agre P (1993) The Hg2+ sensitive residue at cys-189 in the CHIP28 water channel. Biophys J 64:A185

    Google Scholar 

  • Preston GM, Jung JS, Guggino WB, Agre P (1994) Membrane topology of functional aquaporin CHIP molecules. Biophys J 66:A226

    Google Scholar 

  • Rao Y, Jan LY, Jan YN (1990) Similarity of the product of the Drosophila neurogenic gene big brain to transmembrane channel proteins. Nature 345:163–167

    Article  PubMed  CAS  Google Scholar 

  • Rao Y, Bodmer R, Jan LY, Jan YN (1992) The big brain gene of Drosophila functions to control the number of neuronal precursors in the peripheral nervous-system. Development 116:31

    PubMed  CAS  Google Scholar 

  • Rojek A, Praetorius J, Frokiaer J, Nielsen S, Fenton RA (2008) A current view of the mammalian aquaglyceroporins. Annu Rev Physiol 70:301–327

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sandal NN, Marcker KA (1988) Soybean nodulin-26 is homologous to the major intrinsic protein of the bovine lens fiber membrane. Nucleic Acids Res 16:9347–9347

    Article  PubMed  CAS  Google Scholar 

  • Saparov SM, Liu K, Agre P, Pohl P (2007) Fast and selective ammonia transport by aquaporin-8. J Biol Chem 282:5296–5301

    Article  PubMed  CAS  Google Scholar 

  • Sauer JR, Essenberg RC, Bowman AS (2000) Salivary glands in ixodid ticks: control and mechanism of secretion. J Insect Physiol 46:1069–1078

    Article  PubMed  CAS  Google Scholar 

  • Savage DF, Egea PF, Robles-Colmenares Y, O’Connell JD, Stroud RM (2003) Architecture and selectivity in aquaporins: 2.5 angstrom X-ray structure of aquaporin Z. Plos Biology 1:334–340

    Article  CAS  Google Scholar 

  • Shi LB, Skach WR, Verkman AS (1994) Functional independence of monomeric CHIP28 water channels revealed by expression of wild-type-mutant heterodimers. J Biol Chem 269:10417–10422

    PubMed  CAS  Google Scholar 

  • Silberstein C, Bouley R, Huang Y, Fang PK, Pastor-Soler N, Brown D, Van Hoek AN (2004) Membrane organization and function of M1 and M23 isoforms of aquaporin-4 in epithelial cells. Am J Physiol Renal Physiol 287:F501–F511

    Article  PubMed  CAS  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  CAS  Google Scholar 

  • Spring JH, Robichaux SR, Kaufmann N, Brodsky JL (2007) Localization of a Drosophila DRIP-like aquaporin in the Malpighian tubules of the House cricket, Acheta domesticus. Comp Biochem Physiol A Mol Integr Physiol 148:92–100

    Article  PubMed  CAS  Google Scholar 

  • Stroud RM, Savage D, Miercke LJW, Lee JK, Khademi S, Harries W (2003) Selectivity and conductance among the glycerol and water conducting aquaporin family of channels. FEBS Lett 555:79–84

    Article  PubMed  CAS  Google Scholar 

  • Suzuki M, Ogushi THY, Tanaka S (2007) Amphibian aquaporins and adaptation to terrestrial environments: a review. Comp Biochem Physiol A Mol Integr Physiol 148:72–81

    Article  PubMed  CAS  Google Scholar 

  • Sweet G, Gandor C, Voegele R, Wittelkindt N, Beuerle J, Truniger V, Lin ECC, Boos W (1989) Glycerol facilitator of Escherichia coli cloning of Glp-F and identification of the Glp-F product. J Bacteriol 72:424–430

    Google Scholar 

  • Tajkhorshid E, Nollert P, Jensen MO, Miercke LJW, O’Connell J, Stroud RM, Schulten K (2002) Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296:525–530

    Article  PubMed  CAS  Google Scholar 

  • Takata K, Matsuzaki T, Tajika Y (2004) Aquaporins: water channel proteins of the cell membrane. Prog Histochem Cytochem 39:1–83

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tanghe A, Van Dijck P, Dumortier F, Teunissen A, Hohmann S, Thevelein JA (2002) Aquaporin expression correlates with freeze tolerance in baker’s yeast, and overexpression improves freeze tolerance in industrial strains. Appl Environ Microbiol 68:5981–5989

    Article  PubMed  CAS  Google Scholar 

  • Tsubota K, Hirai S, King LS, Agre P, Ishida N (2001) Defective cellular trafficking of lacrimal gland aquaporin-5 in Sjogren’s syndrome. Lancet 357:688–689

    Article  PubMed  CAS  Google Scholar 

  • Tsukaguchi H, Shayakul C, Berger UV, Mackenzie B, Devidas S, Guggino WB, van Hoek AN, Hediger MA (1998a) Molecular characterization of a broad selectivity neutral solute channel. J Biol Chem 273:24737–24743

    Article  PubMed  CAS  Google Scholar 

  • Tsukaguchi H, Shayakul C, Mackenzie B, Berger UV, van Hoek AN, Hediger MA (1998b) Expression cloning and characterization of an osmotic solute channel from rat liver. FASEB J 12:A1043

    Google Scholar 

  • Uzcategui NL, Palmada M, Szallies A, Lang F, Duszenko M (2004a) Aquaglyceroporins of Trypanosoma brucei. Int J Med Microbiol 293:106

    Google Scholar 

  • Uzcategui NL, Szallies A, Pavlovic-Djuranovic S, Palmada M, Figarella K, Boehmer C, Lang F, Beitz E, Duszenko M (2004b) Cloning, heterologous expression, and characterization of three aquaglyceroporins from Trypanosoma brucei. J Biol Chem 279:42669–42676

    Article  PubMed  CAS  Google Scholar 

  • Vanlieburg AF, Verdijk MAJ, Knoers VVAM, Vanessen AJ, Proesmans W, Mallmann R, Monnens LAH, Vanoost BA, Vanos CH, Deen PMT (1994) Patients with autosomal nephrogenic diabetes-insipidus homozygous for mutations in the aquaporin-2 water-channel gene. Am J Hum Genet 55:648–652

    CAS  Google Scholar 

  • Varadaraj K, Kushmerick C, Baldo GJ, Bassnett S, Shiels A, Mathias RT (1999) The role of MIP in lens fiber cell membrane transport. J Membr Biol 170:191–203

    Article  PubMed  CAS  Google Scholar 

  • Verkman AS (2002a) Physiological importance of aquaporin water channels. Ann Med 34:192–200

    Article  PubMed  CAS  Google Scholar 

  • Verkman AS (2002b) Renal concentrating and diluting function in deficiency of specific aquaporin genes. Exp Nephrol 10:235–240

    Article  PubMed  CAS  Google Scholar 

  • Verkman AS (2003) Role of aquaporin water channels in eye function. Exp Eye Res 176:137–143

    Article  Google Scholar 

  • Verkman AS (2005) Novel roles of aquaporins revealed by phenotype analysis of knockout mice. Rev Physiol Biochem Pharmacol 155:31–55

    Article  PubMed  CAS  Google Scholar 

  • Virkki LV, Cooper GJ, Boron WF (2000) Cloning and functional expression of MIPfun, a major intrinsic protein homolog from killifish (Fundulus heteroclitus) lens. FASEB J 14:A344

    Google Scholar 

  • Weig A, Deswarte C, Chrispeels MJ (1997) The major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiol 114:1347–1357

    Article  PubMed  CAS  Google Scholar 

  • Wigglesworth VB, Lee WM (1982) The supply of oxygen to the flight muscles of insects—a theory of tracheole physiology. Tissue Cell 14:501–518

    Article  PubMed  CAS  Google Scholar 

  • Willart JF, De Gusseme A, Hemon S, Descamps M, Leveiller F, Rameau A (2002) Vitrification and polymorphism of trehalose induced by dehydration of trehalose dihydrate. J Phys Chem B 106:3365–3370

    Article  CAS  Google Scholar 

  • Wistow GJ, Pisano MM, Chepelinsky AB (1991) Tandem sequence repeats in transmembrane channel proteins. Trends Biochem Sci 16:170–171

    Article  PubMed  CAS  Google Scholar 

  • Wu B, Beitz E (2007) Aquaporins with selectivity for unconventional permeants. Cell Mol Life Sci 64:2413–2421

    Article  PubMed  CAS  Google Scholar 

  • Yakata K, Hiroaki Y, Ishibashi K, Sohara E, Sasaki S, Mitsuoka K, Fujiyoshi Y (2007) Aquaporin-11 containing a divergent NPA motif has normal water channel activity. Biochim Biophys Acta 1768:688–693

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto N, Sobue K, Miyachi T, Inagaki M, Miura Y, Katsuya H, Asai K (2001) Differential regulation of aquaporin expression in astrocytes by protein kinase C. Mol Brain Res 95:110–116

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Cui Y, Wang W, Zhang L, Bufford L, Sasaki S, Fan Z, Nishimura H (2004a) Molecular and functional characterization of a vasotocin- sensitive aquaporin water channel in quail kidney. Am J Physiol Regul Integr Comp Physiol 287:R915–R924

    PubMed  CAS  Google Scholar 

  • Yang Y, Nishimura H, Fan Z (2004b) Molecular cloning and expression of aquaporin 1 in Japanese quail kidneys. FASEB J 18, Abst. 239.3

  • Yang BX, Zhao D, Solenov E, Verkman AS (2006) Evidence from knockout mice against physiologically significant aquaporin 8-facilitated ammonia transport. Am J Physiol Cell Physiol 291:C417–C423

    Article  PubMed  CAS  Google Scholar 

  • Yanochko GM, Yool AJ (2002) Regulated cationic channel function in Xenopus oocytes expressing Drosophila big brain. J Neurosci 22:2530–2540

    PubMed  CAS  Google Scholar 

  • Yanochko GM, Yool AJ (2004) Block by extracellular divalent cations of Drosophila big brain channels expressed in Xenopus oocytes. Biophys J 86:1470–1478

    PubMed  CAS  Google Scholar 

  • Yasui M (2004) Molecular mechanisms and drug development in aquaporin water channel diseases: structure and function of aquaporins. J Pharmacol Sci 96:260–263

    Article  PubMed  CAS  Google Scholar 

  • Yasui M, Hazama A, Kwon TH, Nielsen S, Guggino WB, Agre P (1999a) Rapid gating and anion permeability of an intracellular aquaporin. Nature 402:184–187

    Article  PubMed  CAS  Google Scholar 

  • 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 96:5808–5813

    Article  PubMed  CAS  Google Scholar 

  • Yasui M, Hazama A, Kwon T, Nielsen S, Guggino WB, Agre P (1999c) pH gating of AQP6, an intracellular water channel with chloride conductance. J Am Soc Nephrol 10:26A–27A

    Google Scholar 

  • Yool AJ (2007a) Aquaporins: multiple roles in the central nervous system. Neuroscientist 13:470–485

    Article  PubMed  CAS  Google Scholar 

  • Yool AJ (2007b) Dominant-negative suppression of big brain ion channel activity by mutation of a conserved glutamate in the first transmembrane domain. Gene Expr 13:329–337

    Article  PubMed  Google Scholar 

  • Yu J, Yool AJ, Schulten K, Tajkhorshid E (2006) Mechanism of gating and ion conductivity of a possible tetrameric pore in aquaporin-1. Structure 14:1411–1423

    Article  PubMed  CAS  Google Scholar 

  • Zardoya R (2005) Phylogeny and evolution of the major intrinsic protein family. Biol Cell 97:397–414

    Article  PubMed  CAS  Google Scholar 

  • Zardoya R, Villalba S (2001) A phylogenetic framework for the aquaporin family in eukaryotes. J Mol Evol 52:391–404

    PubMed  CAS  Google Scholar 

  • Zelenina M, Zelenin S, Bondar AA, Brismar H, Aperia A (2002) Water permeability of aquaporin-4 is decreased by protein kinase C and dopamine. Am J Physiol Renal Physiol 283:F309–F318

    PubMed  CAS  Google Scholar 

  • Zhang R, Logee KA, Verkman AS (1990) Expression of messenger-RNA coding for kidney and red-cell water channels in Xenopus oocytes. J Biol Chem 265:15375–15378

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by the Biotechnology and Biological Sciences Research Council (BB/C517833/1). We are grateful to Dr Steve Bird for valuable discussions regarding phylogentic analysis of insect AQPs.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alan S. Bowman.

Additional information

Communicated by I.D. Hume.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Campbell, E.M., Ball, A., Hoppler, S. et al. Invertebrate aquaporins: a review. J Comp Physiol B 178, 935–955 (2008). https://doi.org/10.1007/s00360-008-0288-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-008-0288-2

Keywords

Navigation