Abstract
Aquaporins (AQPs) are proteins that span plasma membranes allowing the movement of water and small solutes into or out of cells. The type, expression levels and activity of AQPs play a major role in the relative permeability of each cell to water or other solutes. Research on arthropod AQPs has expanded in the last 10 years due to the completion of several arthropod genome projects and the increased availability of genetic information accessible through other resources such as de novo transcriptome assemblies. In particular, there has been significant advancement in elucidating the roles that AQPs serve in relation to the physiology of blood-feeding arthropods of medical importance. The focus of this review is upon the significance of AQPs in relation to hematophagy in arthropods. This will be accomplished via a narrative describing AQP functions during the life history of hematophagic arthropods that includes the following critical phases: (1) Saliva production necessary to blood feeding, (2) Intake and excretion of water during blood digestion, (3) Reproduction and egg development and (4) Off-host environmental stress tolerance. The concentration on these phases will highlight known vulnerabilities in the biology of hematophagic arthropods that could be used to develop novel control strategies as well as research topics that have yet to be examined.
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Adamson ML, Caira JN (1994) Evolutionary factors influencing the nature of parasite specificity. Parasitology 109:S85–S95
Agre P (2006) The aquaporin water channels. Proc Am Thorac Soc 3:5–13
Alves-Silva J, Ribeiro JMC, Van Den Abbeele J, Attardo GM, Hao ZR, Haines LR, Soares MB, Berriman M, Aksoy S, Lehane MJ (2010) An insight into the sialome of Glossina morsitans morsitans. BMC Genomics 11:213
Attardo GM et al. (2014) Genome sequence of the tsetse fly (Glossina morsitans): vector of African trypanosomiasis. Science 344:380–386
Azuma M, Nagae T, Maruyama M, Kataoka N, Miyake S (2012) Two water-specific aquaporins at the apical and basal plasma membranes on insect epithelia: molecular basis for water recycling through the cryptonephric rectal complex of lepidopteran larvae. J Insect Physiol 58:523–533
Ball A, Campbell EM, Jacob J, Hoppler S, Bowman AS (2009) Identification, functional characterization and expression patterns of a water-specific aquaporin in the brown dog tick, Rhipicephalus sanguineus. Insect Biochem Mol Biol 39:105–112
Beitz E, Pavlovic-Djuranovic S, Yasui M, Arge P, Schultz JE (2004) Molecular dissection of water and glycerol permeability of the aquaglyceroproin from Plasmodium falciparum by mutational analysis. Proc Nat Acad Sci USA 101:1153–1158
Beitz E, Wu B, Holm LM, Schultz JE, Zeuthen T (2006) Point mutations in the aromatic/arginine region in aquaporin 1 allows passage or urea, glycerol, ammonia and protons. Proc Nat Acad Sci USA 103:269–274
Benoit JB (2010) Water management by dormant insects: comparisons between dehydration resistance during summer aestivation and winter diapause. In: Navas CA, de Carvalho JE (eds) Aestivation: molecular and physiological aspects. Springer, Berlin, pp 209–229
Benoit JB, Denlinger DL (2007) Suppression of water loss during adult diapause in the northern house mosquito, Culex pipiens. J Exp Biol 210:217–226
Benoit JB, Denlinger DL (2010) Meeting the challenges of on-host and off-host water balance in blood-feeding arthropods. J Insect Physiol 56:1366–1376
Benoit JB, Yoder JA, Lopez-Martinez G, Elnitsky MA, Lee RE Jr, Denlinger DL (2007) Habitat requirements of the seabird tick, Ixodes uriae (Acari: Ixodidae), from the Antarctic Peninsula in relation to water balance characteristics of eggs, nonfed and engorged stages. J Comp Physiol B 177:205–215
Benoit JB, Hansen IA, Attardo GM, Mireji PO, Bargul JL, Drake LL, Masiga DK, Aksoy S (2014a) Aquaporins are critical for provision of water during lactation and intrauterine progeny hydration to maintain tsetse fly reproductive success. PLoS Neg Trop Dis 8:e2517
Benoit JB, Attardo GM, Michalkova V, Bohova J, Zhang Q, Baumann A, Mireji PO, Takac P, Denlinger DL, Ribeiro JM, Aksoy S (2014b) A novel highly divergent protein family from a viviparous insect identified by RNA-seq analysis: a potential target for tsetse fly-specific abortifacients. PLoS Genet 10:e1003874
Beyenbach KW, Piermarini PM (2011) Transcellular and paracellular pathways of transepithelial fluid secretion in Malpighian (renal) tubules of the yellow fever mosquito Aedes aegypti. Acta Physiol 202:387–407
Beyenbach KW, Skaer H, Dow JA (2010) The developmental, molecular, and transport biology of Malpighian tubules. Ann Rev Entomol 55:351–374
Borgnia M, Nielsen S, Engel A, Agre P (1999) Cellular and molecular biology of the aquaporin water channels. Ann Rev Biochem 68:425–458
Briegel H, Gut T, Lea AO (2003) Sequential deposition of yolk components during oogenesis in an insect, Aedes aegypti (Diptera: Culicidae). J Insect Physiol 49:249–260
Campbell EM, Ball A, Hoppler S, Bowman AS (2008) Invertebrate aquaporins: a review. J Comp Physiol B 178:935–955
Campbell EM, Burdin M, Hoppler S, Bowman AS (2010) Role of an aquaporin in the sheep tick Ixodes ricinus: assessment as a potential control target. Int J Parasitol 40:15–23
Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Biol Cell 97:749–764
Clements AN (1992) The Biology of Mosquitoes: Development, nutrition, and reproduction. Chapman and Hall, London
Cmelik SHW, Bursell E, Slack E (1969) Composition of the gut contents of third-instar tsetse larvae (Glossina morsitans Westwood). Comp Biochem Physiol 29:447–453
Cohen E (2012) Role of aquaporins in osmoregulation, desiccation and cold hardiness in insects Entomol. Ornithol Herpetol S1:1–17
Connolly DL, Shanahan CM, Weissberg PL (1998) The aquaporins. A family of water channel proteins. Int J Biochem Cell Biol 30:169–172
Das S, Radtke A, Choi YJ, Mendes AM, Valenzuela JG, Dimopoulos G (2010) Transcriptomic and functional analysis of the Anopheles gambiae salivary gland in relation to blood feeding. BMC Genom 11:566
de Groot BL, Grubmüller H (2001) Water permeation across biological membranes: mechanism and dynamics of Aquaporin-1 and GlpF. Science 294:2353–2357
Delporte C (2013) Aquaporins in salivary glands and pancreas. Biochim Biophys Acta (In press)
Delporte C, Steinfeld S (2006) Distribution and roles of aquaporins in salivary glands. Biochim Biophys Acta 1758:1061–1070
Denlinger DL, Armbruster PA (2014) Mosqutio diapause. Ann Rev Entomol 59:73–93
Denlinger DL, Lee RE Jr (2010) Low temperature biology of insects. Cambridge University Press, Cambridge
Denlinger DL, Ma W-C (1974) Dynamics of the pregnancy cycle in the tsetse Glossina morsitans. J Insect Physiol 20:1015–1026
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
Drake LL (2014) Expression and functional characterization of aquaporins of the yellow fever mosquito, Aedes aegypti (Unpublished, personal results)
Drake LL, Boudko DY, Marinotti O, Carpenter VK, Dawe AL, Hansen IA (2010) The aquaporin gene family of the yellow fever mosquito, Aedes aegypti. PloS One 5:e15578
Drake LL, Price DP, Aguirre SE, Hansen IA (2012) RNAi-mediated gene knockdown and in vivo diuresis assay in adult female Aedes aegypti mosquitoes. J Vis Exp 65:e3479
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. FEBS 270:422–429
Fabrick JA, Pei J, Hull JJ, Yool AJ (2014) Molecular and functional characterization of multiple auqaporin water channel proteins from the western tarnished plant bug, Lygus hesperus. Insect Biochem Mol Biol 45:125–140
Francischetti IM, Calvo E, Andersen JF, Pham VM, Favreau AJ, Barbian KD, Romero A, Valenzuela JG, Ribeiro JM (2010) Insight into the sialome of the bed bug, Cimex lectularius. J Proteome Res 9:3820–3831
Gaede K, Knulle W (1997) On the mechanism of water vapor sorption from unsaturated atmospheres by ticks. J Exp Biol 200:1491–1498
Gonen T, Walz T (2006) The structure of aquaporins. Q Rev Biophys 39:361–396
Goto SG, Philip BN, Teets NM, Kawarasaki Y, Lee RE Jr, Denlinger DL (2011) Functional characterization of an aquaporin in the Antarctic midge Belgica antarctica. J Insect Physiol 57:1106–1114
Hachez C, Chaumont F (2010) Aquaporins: a family of highly regulated multifunctional channels. Adv Exp Med Biol 679:1–17
Hadley NF (1994) Water relations of terrestrial arthropods. Academic, New York
Harlow HJ, Braun EJ (1997) Gastric Na+K+ATPase activity and intestinal urea hydrolysis of the common vampire bat, Desmodus rotundus. Comp Biochem Physiol A Physiol 118:665–669
Herraiz A, Chauvigne F, Cerda J, Belles X, Piulachs M-D (2011) Identification and functional characterization of an ovarian aquaporin from the cockroach Blattella germanica L. (Dictyoptera, Blattellidae). J Exp Biol 214:3630–3638
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
Hub JS, de Groot BL (2008) Mechanism of selectivity in aquaporins and aquaglyceroproins. Proc Nat Acad Sci USA 105:1198–1203
Ishibashi K, Kondo S, Hara S, Morishita Y (2011) The evolutionary aspects of aquaporin family. Am J Physiology Reg Int Comp Physiol 300:R566–R576
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
Jochim RC, Teixeira CR, Laughinghouse A, Mu J, Oliveira F, Gomes RB, Elnaiem DE, Valenzuela JG (2008) The midgut transcriptome of Lutzomyia longipalpis: comparative analysis of cDNA libraries from sugar-fed, blood-fed, post-digested and Leishmania infantum chagasi-infected sand flies. BMC Genom 9:15
Jung JS, Preston GM, Smith BL, Guggino WB, Agre P (1994) Molecular structure of the water channel through aquaporin CHIP-the hour glass model. J Biol Chem 269:14648–14654
Kaldenhoff R, Fischer M (2006a) Aquaporins in plants. Acta Physiol 187:169–176
Kaldenhoff R, Fischer M (2006b) Functional aquaporin diversity in plants. Biochim Biophys Acta 1758:1134–1141
Kanwar R, Fortini ME (2008) The big brain aquaporin is required for endosome maturation and notch receptor trafficking. Cell 133:852–863
Kataoka N, Miyake S, Azuma M (2009a) Aquaporin and aquaglyceroporin in silkworms, differentially expressed in the hindgut and midgut of Bombyx mori. Insect Mol Biol 18:303–314
Kataoka N, Miyake S, Azuma M (2009b) Molecular characterization of aquaporin and aquaglyceroporin in the alimentry canal of Grapholita molesta (the oriental fruit moth)—comparison with Bombyx mori aquaporins. J Insect Biotech Sericol 78:81–90
Kaufman WR, Phillips JE (1973) Ion and water balance in the ixodid tick Dermacentor andersoni. I. routes of ion and water excretion. J Exp Biol 58:523–536
Kaufmann N, Mathai JC, Hill WG, Dow JA, Zeidel ML, Brodsky JL (2005) Developmental expression and biophysical characterization of a Drosophila melanogaster aquaporin. Am J Physiol Cell Physiol 289:C397–C407
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
Kortenoeven MLA, Fenton RA (2014) Renal aquaporins and water balance disorders. Biochim Biophys Acta 1840:1459–1533
Lagrée V, Froger A, Deschamp S, Hubert JF, Delamarche C, Bonnec G, Thomas D, Gouranton J, Pellerin I (1999) Switch from an aquaporin to glycerol channel by two amino acid substitution. J Biol Chem 274:6817–6819
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Lawson D, Arensburger P, Atkinson P, Besansky NJ, Bruggner RV, Butler R, Campbell KS, Christophides GK, Christley S, Dialynas E, Emmert D, Hammond M, Hill CA, Kennedy RC, Lobo NF, MacCallum MR, Madey G, Megy K, Redmond S, Russo S, Severson DW, Stinson EO, Topalis P, Zdobnov EM, Birney E, Gelbart WM, Kafatos FC, Louis C, Collins FH (2007) VectorBase: a home for invertebrate vectors of human pathogens. Nucleic Acids Res 35:D503–D505
Lee KS, Park HJ, Bae JS, Goo TW, Kim I, Sohn HD, Jin BR (2001) Molecular cloning and expression of a cDNA encoding the luciferase from the firefly, Pyrocoelia rufa. J Biotechnol 92:9–19
Lee S, Chung G, Steudle E (2005) Gating of aquaporins by low temperature in roots of chilling-sensitive cucumber and chilling-tolerant figleaf gourd. J Exp Bot 56:985–995
Lehane MJ (2005) Biology of blood-sucking insects, 2nd edn. Cambridge University Press, Cambridge
Liu K, Tsujimoto H, Cha SJ, Agre P, Rasgon JL (2011) Aquaporin water channel AgAQP1 in the malaria vector mosquito Anopheles gambiae during blood feeding and humidity adaptation. Proc Nat Acad Sci USA 108:6062–6066
Megy K, Emrich SJ, Lawson D, Campbell D, Dialynas E, Hughes DS, Koscielny G, Louis C, Maccallum RM, Redmond SN, Sheehan A, Topalis P, Wilson D, VectorBase C (2012) VectorBase: improvements to a bioinformatics resource for invertebrate vector genomics. Nucleic Acids Res 40:D729–D734
Michaud MR, Benoit JB, Lopez-Martinez G, Elnitsky MA, Lee RE Jr, Denlinger DL (2008) Metabolomics reveals unique and shared metabolic changes in response to heat shock, freezing and desiccation in the Antarctic midge, Belgica antarctica. J Insect Physiol 54:645–655
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
Needham GR, Teel PD (1991) Off-host physiological ecology of ticks. Ann Rev Entomol 36:659–681
Neafsey DE, Christophides GK, Collins FH, Emrich SJ, Fontaine MC, Gelbart W, Hahn MW, Howell PI, Kafatos FC, Lawson D, Muskavitch MA, Waterhouse RM, Williams LJ, Besansky NJ (2013) The evolution of the Anopheles 16 genomes project. G3 3:1191–1194
Palli SR, Bai H, Wigginton J (2011) Insect biochemistry and molecular biology. In: Gilbert LI (ed) Insect genomics and beyond. Springer Science, New York
Pei J (2008) Multiple protein sequence alignment. Curr Opin Struct Biol 18:382–386
Pei J, Tang M, Grishin NV (2008) PROMALS3D web server for accurate multiple protein sequence and structure alignments. Nucleic Acids Res 36:W30–W34
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
Philip BN, Kiss AJ, Lee RE Jr (2011) The protective role of aquaporins in the freeze-tolerant insect Eurosta solidaginis: functional characterization and tissue abundance of EsAQP1. J Exp Biol 214:848–857
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
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 116:31–40
Ribeiro JM (1987) Role of saliva in blood-feeding by arthropods. Ann Rev Entomol 32:463–478
Ribeiro JMC, Francischetti IMB (2003) Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Ann Rev Entomol 48:73–88
Ribeiro JM, Arca B, Lombardo F, Calvo E, Phan VM, Chandra PK, Wikel SK (2007) An annotated catalogue of salivary gland transcripts in the adult female mosquito, Aedes aegypti. BMC Genomics 8:6
Sauer JR, Hair JA (1972) Quanity of blood ingested by lone star tick (Acarina: Ixodidae). Ann Entomol Soc Am 65:1065
Serrao JE, Fialho MCQ, Azevedo DO, Zanuncio JC (2014) Aquaporins in the honeybee crop - a new function for an old organ. Protoplasma In press (10.1007/s00709-014-0645-9)
Sonenshine DE, Roe MR (2014) Biology of ticks. Oxford University Press, Oxford
Spring JH, Robichaux SR, Hamlin JA (2009) The role of aquaporins in excretion in insects. J Exp Biol 212:358–362
Staniscuaski F, Paluzzi JP, Real-Guerra R, Carlini CR, Orchard I (2013) Expression analysis and molecular characterization of aquaporins in Rhodnius prolixus. J Insect Physiol 59:1140–1150
Stoffolano JG Jr, Haselton AT (2013) The adult diptern crop: a unique and overlooked organ. Ann Rev Entomol 58:205–225
Stutzer C, van Zyl WA, Olivier NA, Richards S, Maritz-Oliver C (2013) Gene expression profiling of adult female tissues in feeding Rhipicephalus microplus cattle ticks. Int J Parasitol 43:541–554
Sugimoto N, Matsuzaki K, Ishibashi H, Tanaka M, Sawaki T, Fujita Y, Kawanami T, Masaki Y, Okazaki T, Sekine J, Koizumi S, Yachie A, Umehara H, Shido O (2013) Upregulation of aquaporin expression in the salivary glands of heat-acclimated rats. Sci Rep 3:1763
Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tatsumi K, Tsuji S, Miwa H, Morisaku T, Nuriya M et al (2009) Drosophila big brain does not act as a water channel, but mediates cell adhesion. FEBS Lett 583:2077–2082
Teets NM, Peyton JT, Ragland GJ, Colinet H, Renault D, Hahn DA, Denlinger DL (2012) Combined transcriptomic and metabolomic approach uncovers the molecular mechanisms of cold tolerance in a temperate flesh fly. Physiol Genomics 44:764–777
Telleria EL, Benoit JB, Zhao X, Savage AF, Regmi S, Silva TLA, O’Neill M, Aksoy S (2014) Insights into the trypanosome transmission process revealed through transcriptomic analysis of parasitized tsetse salivary glands. PLoS Neg Trop Dis 8:e2649
Tobe SS, Langley PA (1978) Reproductive physiology of Glossina. Ann Rev Entomol 23:283–307
Tomkowiak E, Pienkowska JR (2010) The current knowledge of invertebrate aquaporin water channels with particular emphasis on insect AQPs. Adv Cell Biol 2:90–103
Tsujimoto H, Liu K, Linser PJ, Agre P, Rasgon JL (2013) Organ-specific splice variants of aquaporin water channel AgAQP1 in the malaria vector Anopheles gambiae. PLoS One 8:e75888
Valenzuela JG, Francischetti IMB, Pham VM, Garfield MK, Ribeiro JMC (2003) Exploring the salivary gland transcriptome and proteome of the Anopheles stephensi mosquito. Insect Biochem Mol Biol 33:717–732
Verkman AS (2005a) More than just water channels: unexpected cellular roles of aquaporins. J Cell Sci 118:3225–3232
Verkman AS (2005b) Novel roles of aquaporins revealed by phenotype analysis of knockout mice. Rev Physiol Biochem Pharmacol 155:31–55
Wallace IS, Shakesby AJ, Hwang JH, Choi WG, Martinkova N, Douglas AE, Roberts DM (2012) Acyrthosiphon pisum AQP2: a multifunctional insect aquaglyceroporin. Biochim Biophys Acta 1818:627–635
Wang Y, Tajkhorshid E (2007) Molecular mechanisms of conduction and selectivity in aquaporin water channels. J Nut 137:1509S–1515S
Wharton GA (1985) Water balance of insects. In: Kerkut GA, Gilbert LM (eds) Comprehensive insect physiology, biochemistry and pharmacology. Pergamon, Oxford, pp 565–603
Yanochko GM, Yool AJ (2002) Regulated cationic channel function in Xenopus oocytes expressing Drosophila big brain. J Neurosci 22:2530–2540
Yi SX, Benoit JB, Elnitsky MA, Kaufmann N, Brodsky JL, Zeidel ML, Denlinger DL, Lee RE Jr (2011) Function and immuno-localization of aquaporins in the Antarctic midge Belgica antarctica. J Insect Physiol 57:1096–1105
Yoder JA, Benoit JB, Rellinger EJ, Tank JL (2006a) Developmental profiles in tick water balance with a focus on the new Rocky Mountain spotter fever vector, Rhipicephalus sanguineus. Med Vet Entomol 20:365–372
Yoder JA, Benoit JB, Denlinger DL, Rivers DB (2006b) Stress-induced accumulation of glycerol in the flesh fly, Sarcophaga bullata: Evidence indicating anti-desiccant and cryoprotectant functions of this polyol and a role for the brain in coordinating the response. J Insect Physiol 52:202-214
Yoder JA, Hedges BZ, Benoit JB (2012) Water balance of the American dog tick, Dermacentor variabilis, throughout its development with comparative observations between field-collected and laboratory-reared ticks. Int J Acarol 38:334–343
Zardoya R (2005) Phylogeny and evolution of the major intrinsic protein family. Biol Cell 97:397–414
Zhang R, Logee KA, Verkman AS (1990) Expression of messenger-RNA coding for kidney and red-cell water channels in Xenopus. J Biol Chem 265:15375-15378
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Benoit, J.B., Hansen, I.A., Szuter, E.M. et al. Emerging roles of aquaporins in relation to the physiology of blood-feeding arthropods. J Comp Physiol B 184, 811–825 (2014). https://doi.org/10.1007/s00360-014-0836-x
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DOI: https://doi.org/10.1007/s00360-014-0836-x