Abstract
Aquaporins (AQPs) are multifunctional transmembrane channel proteins permeable to water and an expanding array of solutes. AQP-mediated ion channel activity was first observed when purified AQP0 from bovine lens was incorporated into lipid bilayers. Electrophysiological properties of ion-conducting AQPs since discovered in plants, invertebrates, and mammals have been assessed using native, reconstituted, and heterologously expressed channels. Accumulating evidence is defining amino acid residues that govern differential solute permeability through intrasubunit and central pores of AQP tetramers. Rings of charged and hydrophobic residues around pores influence AQP selectivity, and are candidates for further work to define motifs that distinguish ion conduction capability, versus strict water and glycerol permeability. Similarities between AQP ion channels thus far include large single channel conductances and long open times, but differences in ionic selectivity, permeability to divalent cations, and mechanisms of gating (e.g., by voltage, pH, and cyclic nucleotides) are unique to subtypes. Effects of lipid environments in modulating parameters such as single channel amplitude could explain in part the variations in AQP ion channel properties observed across preparations. Physiological roles of the ion-conducting AQP classes span diverse processes including regulation of cell motility, organellar pH, neural development, signaling, and nutrient acquisition. Advances in computational methods can generate testable predictions of AQP structure–function relationships, which combined with innovative high-throughput assays could revolutionize the field in defining essential properties of ion-conducting AQPs, discovering new AQP ion channels, and understanding the effects of AQP interactions with proteins, signaling cascades, and membrane lipids.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agre P, Sasaki S, Chrispeels MJ (1993) Aquaporins: a family of water channel proteins. Am J Physiol 265(3 Pt 2):F461. https://doi.org/10.1152/ajprenal.1993.265.3.F461
Alexandersson E, Fraysse L, Sjövall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59(3):469–484. https://doi.org/10.1007/s11103-005-0352-1
Angladon M-A, Fossépré M, Leherte L, Vercauteren DP (2019) Interaction of POPC, DPPC, and POPE with the μ opioid receptor: a coarse-grained molecular dynamics study. PLoS One 14(3):e0213646. https://doi.org/10.1371/journal.pone.0213646
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(3):576–588. https://doi.org/10.1124/mol.57.3.576
Aponte-Santamaría C, Briones R, Schenk AD, Walz T, de Groot BL (2012) Molecular driving forces defining lipid positions around aquaporin-0. Proc Natl Acad Sci 109(25):9887–9892. https://doi.org/10.1073/pnas.1121054109
Arai H, Pink S, Forgac M (1989) Interaction of anions and ATP with the coated vesicle proton pump. Biochemistry 28(7):3075–3082. https://doi.org/10.1021/bi00433a051
Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284(5415):770–776. https://doi.org/10.1126/science.284.5415.770
Aung T, Nourmohammadi S, Qu Z, Harata-Lee Y, Cui J, Shen H, Yool A, Pukala T, Du H, Kortschak R (2019) fractional Deletion of compound Kushen injection indicates cytokine signaling pathways are critical for its perturbation of the cell cycle. Sci Rep 9(1):1–16. https://doi.org/10.1038/s41598-019-50271-4
Bagriantsev SN, Chatelain FC, Clark KA, Alagem N, Reuveny E, Minor DL Jr (2014) Tethered protein display identifies a novel Kir3. 2 (GIRK2) regulator from protein scaffold libraries. ACS Chem Neurosci 5(9):812–822. https://doi.org/10.1021/cn5000698
Beitz E, Liu K, Ikeda M, Guggino WB, Agre P, Yasui M (2006a) Determinants of AQP6 trafficking to intracellular sites versus the plasma membrane in transfected mammalian cells. Biol Cell 98(2):101–109. https://doi.org/10.1042/BC20050025
Beitz E, Wu B, Holm LM, Schultz JE, Zeuthen T (2006b) Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons. Proc Natl Acad Sci U S A 103(2):269–274. https://doi.org/10.1073/pnas.0507225103
Bernardi M, Marracino P, Liberti M, Gárate J-A, Burnham CJ, Apollonio F, English NJ (2019) Controlling ionic conductivity through transprotein electropores in human aquaporin 4: a non-equilibrium molecular-dynamics study. Phys Chem Chem Phys 21(6):3339–3346. https://doi.org/10.1039/C8CP06643D
Bernstein JD, Okamoto Y, Kim M, Shikano S (2013) Potential use of potassium efflux-deficient yeast for studying trafficking signals and potassium channel functions. FEBS Open Biol 3:196–203. https://doi.org/10.1016/j.fob.2013.04.002
Berry V, Francis P, Kaushal S, Moore A, Bhattacharya S (2000) Missense mutations in MIP underlie autosomal dominant ‘polymorphic’and lamellar cataracts linked to 12q. Nat Genet 25(1):15–17. https://doi.org/10.1038/75538
Bienert GP, Thorsen M, Schüssler MD, Nilsson HR, Wagner A, Tamás MJ, Jahn TP (2008) A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biol 6(1):26. https://doi.org/10.1186/1741-7007-6-26
Bloemendal H, Hockwin O (1982) Lens protein. Crit Rev Biochem 12(1):1–38. https://doi.org/10.3109/10409238209105849
Boassa D, Yool AJ (2002) A fascinating tail: cGMP activation of aquaporin-1 ion channels. Trends Pharmacol Sci 23(12):558–562. https://doi.org/10.1016/S0165-6147(02)02112-0
Boassa D, Stamer WD, Yool AJ (2006) Ion Channel Function of Aquaporin-1 Natively Expressed in Choroid Plexus. J Neurosci 26(30):7811–7819. https://doi.org/10.1523/jneurosci.0525-06.2006
Boursiac Y, Chen S, Luu D-T, Sorieul M, van den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139(2):790–805. https://doi.org/10.1104/pp.105.065029
Brand M, Campos-Ortega JA (1988) Two groups of interrelated genes regulate early neurogenesis in Drosophila melanogaster. Rouxs Arch Dev Biol 197(8):457–470. https://doi.org/10.1007/BF00385679
Byrt CS, Zhao M, Kourghi M, Bose J, Henderson SW, Qiu J, Gilliham M, Schultz C, Schwarz M, Ramesh SA, Yool A, Tyerman S (2017) Non-selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH. Plant Cell Environ 40(6):802–815. https://doi.org/10.1111/pce.12832
Campbell EM, Birdsell DN, Yool AJ (2012) The Activity of Human Aquaporin 1 as a cGMP-Gated Cation Channel Is Regulated by Tyrosine Phosphorylation in the Carboxyl-Terminal Domain. Mol Pharmacol 81(1):97–105. https://doi.org/10.1124/mol.111.073692
Chakrabarti N, Tajkhorshid E, Bt Roux, Pomès R (2004) Molecular basis of proton blockage in aquaporins. Structure 12(1):65–74. https://doi.org/10.1016/j.str.2003.11.017
Chandy G, Zampighi G, Kreman M, Hall J (1997) Comparison of the water transporting properties of MIP and AQP1. J Membr Biol 159(1):29–39. https://doi.org/10.1007/s002329900266
Chen Y, Tachibana O, Oda M, Xu R, Hamada J-i, Yamashita J, Hashimoto N, Takahashi JA (2006) Increased expression of aquaporin 1 in human hemangioblastomas and its correlation with cyst formation. J Neurooncol 80(3):219–225. https://doi.org/10.1007/s11060-005-9057-1
Chepelinsky AB (2009) Structural function of MIP/aquaporin 0 in the eye lens; genetic defects lead to congenital inherited cataracts. Handb Exp Pharmacol 190:265–297. https://doi.org/10.1007/978-3-540-79885-9_14
Chow PH, Kourghi M, Pei JV, Nourmohammadi S, Yool AJ (2020) 5-hydroxymethyl-furfural and structurally related compounds block the ion conductance in human aquaporin-1 channels and slow cancer cell migration and invasion. Mol Pharmacol 98(1):38–48. https://doi.org/10.1124/mol.119.119172
Conde A, Diallinas G, Chaumont F, Chaves M, Geros H (2010) Transporters, channels, or simple diffusion? Dogmas, atypical roles and complexity in transport systems. Int J Biochem Cell Biol 42(6):857–868. https://doi.org/10.1016/j.biocel.2009.12.012
De Almeida A, Mósca AF, Wragg D, Wenzel M, Kavanagh P, Barone G, Leoni S, Soveral G, Casini A (2017) The mechanism of aquaporin inhibition by gold compounds elucidated by biophysical and computational methods. Chem Commun 53(27):3830–3833. https://doi.org/10.1039/C7CC00318H
De Ieso ML, Pei JV, Nourmohammadi S, Smith E, Chow PH, Kourghi M, Hardingham JE, Yool AJ (2019) Combined pharmacological administration of AQP1 ion channel blocker AqB011 and water channel blocker Bacopaside II amplifies inhibition of colon cancer cell migration. Sci Rep 9(1):12635. https://doi.org/10.1038/s41598-019-49045-9
De Ieso ML, Yool AJ (2018) Mechanisms of aquaporin-facilitated cancer invasion and metastasis. Front Chem 6(135). https://doi.org/10.3389/fchem.2018.00135
Dean RM, Rivers RL, Zeidel ML, Roberts DM (1999) Purification and functional reconstitution of soybean nodulin 26. An aquaporin with water and glycerol transport properties. Biochemistry 38(1):347–353. https://doi.org/10.1021/bi982110c
Demidchik V, Tester M (2002) Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol 128(2):379–387. https://doi.org/10.1104/pp.010524%JPlantPhysiology
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(19):3881–3893. https://doi.org/10.1242/dev.124.19.3881
Ehring GR, Zampighi G, Horwitz J, Bok D, Hall JE (1990) Properties of channels reconstituted from the major intrinsic protein of lens fiber membranes. J Gen Physiol 96(3):631–664. https://doi.org/10.1085/jgp.96.3.631
Ehring GR, Lagos N, Zampighi GA, Hall JE (1992) Phosphorylation modulates the voltage dependence of channels reconstituted from the major intrinsic protein of lens fiber membranes. J Membr Biol 126(1):75–88. https://doi.org/10.1007/bf00233462
Eisenberg D, Gill HS, Pfluegl GM, Rotstein SH (2000) Structure–function relationships of glutamine synthetases. Biochim Biophys Acta 1477(1–2):122–145. https://doi.org/10.1016/S0167-4838(99)00270-8
El Hindy N, Bankfalvi A, Herring A, Adamzik M, Lambertz N, Zhu Y, Siffert W, Sure U, Sandalcioglu IE (2013) Correlation of aquaporin-1 water channel protein expression with tumor angiogenesis in human astrocytoma. Anticancer Res 33(2):609–613
Endo M, Jain RK, Witwer B, Brown D (1999) Water channel (aquaporin 1) expression and distribution in mammary carcinomas and glioblastomas. Microvasc Res 58(2):89–98. https://doi.org/10.1006/mvre.1999.2158
Epstein W, Buurman E, McLaggan D, Naprstek J (1993) Multiple mechanisms, roles and controls of K+ transport in Escherichia coli. Biochem Soc Trans 21(4):1006–1010. https://doi.org/10.1042/bst0211006
Fairbairn DJ, Liu W, Schachtman DP, Gomez-Gallego S, Day SR, Teasdale RD (2000) Characterisation of two distinct HKT1-like potassium transporters from Eucalyptus camaldulensis. Plant Mol Biol 43(4):515–525. https://doi.org/10.1023/A:1006496402463
Fischer G, Kosinska-Eriksson U, Aponte-Santamaría C, Palmgren M, Geijer C, Hedfalk K, Hohmann S, De Groot BL, Neutze R, Lindkvist-Petersson K (2009) Crystal structure of a yeast aquaporin at 1.15 Å reveals a novel gating mechanism. PLoS Biol 7(6):e1000130. https://doi.org/10.1371/journal.pbio.1000130
Fortin MG, Morrison NA, Verma DP (1987) Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res 15(2):813–824. https://doi.org/10.1093/nar/15.2.813
Fu D, Libson A, Miercke LJ, Weitzman C, Nollert P, Krucinski J, Stroud RM (2000) Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290(5491):481–486. https://doi.org/10.1126/science.290.5491.481
Girsch SJ, Peracchia C (1985) Lens cell-to-cell channel protein: I. Self-assembly into liposomes and permeability regulation by calmodulin. J Membr Biol 83(3):217–225. https://doi.org/10.1007/BF01868696
Gorin MB, Yancey SB, Cline J, Revel J-P, Horwitz J (1984) The major intrinsic protein (MIP) of the bovine lens fiber membrane: Characterization and structure based on cDNA cloning. Cell 39(1):49–59. https://doi.org/10.1016/0092-8674(84)90190-9
Gotfryd K, Mósca AF, Missel JW, Truelsen SF, Wang K, Spulber M, Krabbe S, Hélix-Nielsen C, Laforenza U, Soveral G, Pedersen PA, Gourdon P (2018) Human adipose glycerol flux is regulated by a pH gate in AQP10. Nat Commun 9(1):4749. https://doi.org/10.1038/s41467-018-07176-z
Gu R-X, Ingólfsson HI, De Vries AH, Marrink SJ, Tieleman DP (2017) Ganglioside-lipid and ganglioside-protein interactions revealed by coarse-grained and atomistic molecular dynamics simulations. J Phys Chem B 121(15):3262–3275. https://doi.org/10.1021/acs.jpcb.6b07142
Guenther JF, Chanmanivone N, Galetovic MP, Wallace IS, Cobb JA, Roberts DM (2003) Phosphorylation of soybean nodulin 26 on serine 262 enhances water permeability and is regulated developmentally and by osmotic signals. Plant Cell 15(4):981–991. https://doi.org/10.1105/tpc.009787
Günther W, Lüchow A, Cluzeaud F, Vandewalle A, Jentsch TJ (1998) ClC-5, the chloride channel mutated in Dent’s disease, colocalizes with the proton pump in endocytotically active kidney cells. Proc Natl Acad Sci 95(14):8075–8080. https://doi.org/10.1073/pnas.95.14.8075
Hachez C, Chaumont F (2010) Aquaporins: a family of highly regulated multifunctional channels. Adv Exp Med Biol 679:1–17. https://doi.org/10.1007/978-1-4419-6315-4_1
Hadidi H, Kamali R (2021) Molecular dynamics study of water transport through AQP5-R188C mutant causing palmoplantar keratoderma (PPK) using the gating mechanism concept. Biophys Chem 277:106655. https://doi.org/10.1016/j.bpc.2021.106655
Hara-Chikuma M, Satooka H, Watanabe S, Honda T, Miyachi Y, Watanabe T, Verkman AS (2015) Aquaporin-3-mediated hydrogen peroxide transport is required for NF-κB signalling in keratinocytes and development of psoriasis. Nat Commun 6(1):7454. https://doi.org/10.1038/ncomms8454
Hazama A, Kozono D, Guggino WB, Agre P, Yasui M (2002) Ion permeation of AQP6 water channel protein: single-channel recordings after Hg2+ activation. J Biol Chem 277(32):29224–29230. https://doi.org/10.1074/jbc.M204258200
Holm LM, Klaerke DA, Zeuthen T (2004) Aquaporin 6 is permeable to glycerol and urea. Pflugers Arch 448(2):181–186. https://doi.org/10.1007/s00424-004-1245-x
Hoque MO, Soria J-C, Woo J, Lee T, Lee J, Jang SJ, Upadhyay S, Trink B, Monitto C, Desmaze C (2006) Aquaporin 1 is overexpressed in lung cancer and stimulates NIH-3T3 cell proliferation and anchorage-independent growth. Am J Pathol 168(4):1345–1353. https://doi.org/10.2353/ajpath.2006.050596
Hub JS, De Groot BL (2008) Mechanism of selectivity in aquaporins and aquaglyceroporins. Proc Natl Acad Sci 105(4):1198–1203. https://doi.org/10.1073/pnas.0707662104
Hub JS, Aponte-Santamaría C, Grubmüller H, de Groot BL (2010) Voltage-regulated water flux through aquaporin channels in silico. Biophys J 99(12):L97–L99. https://doi.org/10.1016/j.bpj.2010.11.003
Huber VJ, Tsujita M, Yamazaki M, Sakimura K, Nakada T (2007) Identification of arylsulfonamides as aquaporin 4 inhibitors. Bioorg Med Chem Lett 17(5):1270–1273. https://doi.org/10.1016/j.bmcl.2006.12.010
Hwang JH, Ellingson SR, Roberts DM (2010) Ammonia permeability of the soybean nodulin 26 channel. FEBS Lett 584(20):4339–4343. https://doi.org/10.1016/j.febslet.2010.09.033
Ikeda M, Beitz E, Kozono D, Guggino WB, Agre P, Yasui M (2002) Characterization of aquaporin-6 as a nitrate channel in mammalian cells: requirement of pore-lining residue threonine 63. J Biol Chem 277(42):39873–39879. https://doi.org/10.1074/jbc.M207008200
Ishibashi K, Sasaki S, Fushimi K, Uchida S, Kuwahara M, Saito H, Furukawa T, Nakajima K, Yamaguchi Y, Gojobori T 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 U S A 91(14):6269–6273. https://doi.org/10.1073/pnas.91.14.6269
Jahn TP, Møller ALB, Zeuthen T, Holm LM, Klærke DA, Mohsin B, Kühlbrandt W, Schjoerring JK (2004) Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett 574(1):31–36. https://doi.org/10.1016/j.febslet.2004.08.004
Kapilan R, Vaziri M, Zwiazek JJ (2018) Regulation of aquaporins in plants under stress. Biol Res 51(1):1–11. https://doi.org/10.1186/s40659-018-0152-0
Kawada H, Inanobe A, Kurachi Y (2016) Isolation of proflavine as a blocker of G protein-gated inward rectifier potassium channels by a cell growth-based screening system. Neuropharmacology 109:18–28. https://doi.org/10.1016/j.neuropharm.2016.05.016
Kourghi M, Pei JV, De Ieso ML, Flynn G, Yool AJ (2016) Bumetanide derivatives AqB007 and AqB011 selectively block the aquaporin-1 ion channel conductance and slow cancer cell migration. Mol Pharmacol 89(1):133–140. https://doi.org/10.1124/mol.115.101618
Kourghi M, Nourmohammadi S, Pei JV, Qiu J, McGaughey S, Tyerman SD, Byrt CS, Yool AJ (2017) Divalent cations regulate the ion conductance properties of diverse classes of aquaporins. Int J Mol Sci 18(11):2323. https://doi.org/10.3390/ijms18112323
Kourghi M, Pei JV, De Ieso ML, Nourmohammadi S, Chow PH, Yool AJ (2017b) Fundamental structural and functional properties of aquaporin ion channels found across the kingdoms of life. Clin Exp Pharmacol Physiol. https://doi.org/10.1111/1440-1681.12900
Kwon T-H, Hager H, Nejsum LN, Andersen M-LE, Føkiær J, Nielsen S (2001) Physiology and pathophysiology of renal aquaporins. Semin Nephrol 21(3):231–238. https://doi.org/10.1053/snep.2001.21647
Laganowsky A, Reading E, Allison TM, Ulmschneider MB, Degiacomi MT, Baldwin AJ, Robinson CV (2014) Membrane proteins bind lipids selectively to modulate their structure and function. Nature 510(7503):172–175. https://doi.org/10.1038/nature13419
Lee AG (2004) How lipids affect the activities of integral membrane proteins. Biochim Biophys Acta Biomembr 1666(1):62–87. https://doi.org/10.1016/j.bbamem.2004.05.012
Lee JW, Zhang Y, Weaver CD, Shomer NH, Louis CF, Roberts DM (1995) Phosphorylation of nodulin 26 on serine 262 affects its voltage-sensitive channel activity in planar lipid bilayers. J Biol Chem 270(45):27051–27057. https://doi.org/10.1074/jbc.270.45.27051
Lehmann R, Jiménez F, Dietrich U, Campos-Ortega JA (1983) On the phenotype and development of mutants of early neurogenesis in Drosophila melanogaster. Wilhelm Roux Arch Dev Biol 192(2):62–74. https://doi.org/10.1007/BF00848482
Liu K, Kozono D, Kato Y, Agre P, Hazama A, Yasui M (2005) Conversion of aquaporin 6 from an anion channel to a water-selective channel by a single amino acid substitution. Proc Natl Acad Sci U S A 102(6):2192–2197. https://doi.org/10.1073/pnas.0409232102
Locascio A, Andrés-Colás N, Mulet JM, Yenush L (2019) Saccharomyces cerevisiae as a tool to investigate plant potassium and sodium transporters. Int J Mol Sci 20(9):2133. https://doi.org/10.3390/ijms20092133
Longatti P, Basaldella L, Orvieto E, Dei Tos A, Martinuzzi A (2006) Aquaporin (s) expression in choroid plexus tumours. Pediatr Neurosurg 42(4):228–233. https://doi.org/10.1159/000092359
Luu DT, Martiniere A, Sorieul M, Runions J, Maurel C (2012) Fluorescence recovery after photobleaching reveals high cycling dynamics of plasma membrane aquaporins in Arabidopsis roots under salt stress. Plant J 69(5):894–905. https://doi.org/10.1111/j.1365-313X.2011.04841.x
Ma TH, Frigeri A, Skach W, Verkman AS (1993) Cloning of a novel rat kidney cDNA homologous to CHIP28 and WCH-CD water channels. Biochem Biophys Res Commun 197(2):654–659. https://doi.org/10.1006/bbrc.1993.2529
Ma T, Yang B, Kuo W-L, Verkman AS (1996) cDNA cloning and gene structure of a novel water channel expressed exclusively in human kidney: evidence for a gene cluster of aquaporins at chromosome locus 12q13. Genomics 35(3):543–550. https://doi.org/10.1006/geno.1996.0396
Ma J, Zhou C, Yang J, Ding X, Zhu Y, Chen X (2016) Expression of AQP6 and AQP8 in epithelial ovarian tumor. J Mol Histol 47(2):129–134. https://doi.org/10.1007/s10735-016-9657-4
Martinac B, Rohde PR, Battle AR, Petrov E, Pal P, Foo AFW, Vásquez V, Huynh T, Kloda A (2010) Studying mechanosensitive ion channels using liposomes. In: Weissig V (ed) Liposomes: Methods and Protocols, Volume 2: Biological Membrane Models. Humana Press, Totowa, pp 31–53. https://doi.org/10.1007/978-1-60761-447-0_4
Masalkar P, Wallace IS, Hwang JH, Roberts DM (2010) Interaction of cytosolic glutamine synthetase of soybean root nodules with the C-terminal domain of the symbiosome membrane nodulin 26 aquaglyceroporin. J Biol Chem 285(31):23880–23888. https://doi.org/10.1074/jbc.M110.135657
McGaughey SA, Qiu J, Tyerman SD, Byrt CS (2018) Regulating root aquaporin function in response to changes in salinity. Ann Plant Rev Online 1:381–416. https://doi.org/10.1002/9781119312994.apr0626
McLennan R, McKinney MC, Teddy JM, Morrison JA, Kasemeier-Kulesa JC, Ridenour DA, Manthe CA, Giniunaite R, Robinson M, Baker RE, Maini PK, Kulesa PM (2020) Neural crest cells bulldoze through the microenvironment using Aquaporin 1 to stabilize filopodia. Development 147 (1). https://doi.org/10.1242/dev.185231
Miao GH, Verma DP (1993) Soybean nodulin-26 gene encoding a channel protein is expressed only in the infected cells of nodules and is regulated differently in roots of homologous and heterologous plants. Plant Cell 5(7):781–794. https://doi.org/10.1105/tpc.5.7.781
Modesto E, Barcellos L, Campos-de-Carvalho AC (1990) MIP 28 forms channels in planar lipid bilayers. Braz J Med Biol Res 23(10):1029–1032
Modesto E, Lampe PD, Ribeiro MC, Spray DC, Campos de Carvalho AC (1996) Properties of chicken lens MIP channels reconstituted into planar lipid bilayers. J Membr Biol 154(3):239–249. https://doi.org/10.1007/s002329900148
Molinas A, Mirazimi A, Holm A, Loitto VM, Magnusson K-E, Vikström E (2016) Protective role of host aquaporin 6 against Hazara virus, a model for Crimean–Congo hemorrhagic fever virus infection. FEMS Microbiol Lett 363(8):fnw058. https://doi.org/10.1093/femsle/fnw058
Mom R, Muries B, Benoit P, Robert-Paganin J, Réty S, Js V, Pádua A, Label P, Auguin D (2021) Voltage-gating of aquaporins, a putative conserved safety mechanism during ionic stresses. FEBS Lett 595(1):41–57. https://doi.org/10.1002/1873-3468.13944
Moon C, Soria J-C, Jang SJ, Lee J, Hoque MO, Sibony M, Trink B, Chang YS, Sidransky D, Mao L (2003) Involvement of aquaporins in colorectal carcinogenesis. Oncogene 22(43):6699–6703. https://doi.org/10.1038/sj.onc.1206762
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(15):9010–9016. https://doi.org/10.1074/jbc.270.15.9010
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(6804):599–605. https://doi.org/10.1038/35036519
Nagashima G, Fujimoto T, Suzuki R, Asai J-i, Itokawa H, Noda M (2006) Dural invasion of meningioma: a histological and immunohistochemical study. Brain Tumor Pathol 23(1):13–17. https://doi.org/10.1007/s10014-006-0193-x
Németh-Cahalan KL, Clemens DM, Hall JE (2013) Regulation of AQP0 water permeability is enhanced by cooperativity. J Gen Physiol 141(3):287–295. https://doi.org/10.1085/jgp.201210884
Obermeyer G, Tyerman SD (2005) NH4+ currents across the peribacteroid membrane of soybean. Macroscopic and microscopic properties, inhibition by Mg2+, and temperature dependence indicate a subpicoSiemens channel finely regulated by divalent cations. Plant Physiol 139(2):1015–1029. https://doi.org/10.1104/pp.105.066670
Oster GF, Perelson AS (1987) The physics of cell motility. J Cell Sci 1987(Supplement_8):35–54. https://doi.org/10.1242/jcs.1987.Supplement_8.3
Papadopoulos MC, Verkman AS (2013) Aquaporin water channels in the nervous system. Nat Rev Neurosci 14(4):265–277. https://doi.org/10.1038/nrn3468
Papadopoulos M, Saadoun S, Verkman A (2008) Aquaporins and cell migration. Pflügers Arch Eur J Physiol 456(4):693–700. https://doi.org/10.1007/s00424-007-0357-5
Pei JV, Burton JL, Kourghi M, De Ieso ML, Yool AJ (2016) Drug discovery and therapeutic targets for pharmacological modulators of aquaporin channels. In: Soveral G, Casinin A, Nielsen S (eds) Aquaporins in Health and Disease: New Molecular Targets For Drug Discovery. CRC Press, Oxfordshire, pp 275–297
Pei JV, Heng S, De Ieso ML, Sylvia G, Kourghi M, Nourmohammadi S, Abell AD, Yool AJ (2019) Development of a photoswitchable lithium-sensitive probe to analyze nonselective cation channel activity in migrating cancer cells. Mol Pharmacol 95(5):573–583. https://doi.org/10.1124/mol.118.115428
Poveda JA, Giudici AM, Renart ML, Molina ML, Montoya E, Fernández-Carvajal A, Fernández-Ballester G, Encinar JA (1838) González-Ros JM (2014) Lipid modulation of ion channels through specific binding sites. Biochim Biophys Acta Biomembr 6:1560–1567. https://doi.org/10.1016/j.bbamem.2013.10.023
Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256(5055):385–387. https://doi.org/10.1126/science.256.5055.385
Qiu J, McGaughey SA, Groszmann M, Tyerman SD, Byrt CS (2020) Phosphorylation influences water and ion channel function of AtPIP2;1. Plant Cell Environ 43(10):2428–2442. https://doi.org/10.1111/pce.13851
Rambow J, Wu B, Rönfeldt D, Beitz E (2014) Aquaporins with anion/monocarboxylate permeability: mechanisms, relevance for pathogen–host interactions. Front Pharmacol 5(199). https://doi.org/10.3389/fphar.2014.00199
Rao Y, Jan LY, Jan YN (1990) Similarity of the product of the Drosophila neurogenic gene big brain to transmembrane channel proteins. Nature 345(6271):163–167. https://doi.org/10.1038/345163a0
Reizer J, Reizer A, Saier MH Jr (1993) 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 28(3):235–257. https://doi.org/10.3109/10409239309086796
Rivers RL, Dean RM, Chandy G, Hall JE, Roberts DM, Zeidel ML (1997) Functional analysis of nodulin 26, an aquaporin in soybean root nodule symbiosomes. J Biol Chem 272(26):16256–16261. https://doi.org/10.1074/jbc.272.26.16256
Roberts DM, Tyerman SD (2002) Voltage-dependent cation channels permeable to NH4+, K+, and Ca2+ in the symbiosome membrane of the model legume Lotus japonicus. Plant Physiol 128(2):370–378. https://doi.org/10.1104/pp.010568
Ros R, Lemaillet G, Fonrouge A, Daram P, Enjuto M, Salmon J-M, Thibaud J-B, Sentenac H (1999) Molecular determinants of the Arabidopsis AKT1 K+ channel ionic selectivity investigated by expression in yeast of randomly mutated channels. Physiol Plant 105(3):459–468. https://doi.org/10.1034/j.1399-3054.1999.105310.x
Rubio F, Gassmann W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270(5242):1660–1663. https://doi.org/10.1126/science.270.5242.1660
Saadoun S, Papadopoulos M, Davies D, Bell B, Krishna S (2002) Increased aquaporin 1 water channel expression inhuman brain tumours. Br J Cancer 87(6):621–623. https://doi.org/10.1038/sj.bjc.6600512
Sachdeva R, Singh B (2014) Phosphorylation of Ser-180 of rat aquaporin-4 shows marginal affect on regulation of water permeability: molecular dynamics study. J Biomol Struct Dyn 32(4):555–566. https://doi.org/10.1080/07391102.2013.780981
Saparov SM, Kozono D, Rothe U, Agre P, Pohl P (2001) Water and ion permeation of aquaporin-1 in planar lipid bilayers: major differences in structural determinants and stoichiometry. J Biol Chem 276(34):31515–31520. https://doi.org/10.1074/jbc.M104267200
Saparov SM, Liu K, Agre P, Pohl P (2007) Fast and selective ammonia transport by aquaporin-8. J Biol Chem 282(8):5296–5301. https://doi.org/10.1074/jbc.M609343200
Schwab A, Stock C (2014) Ion channels and transporters in tumour cell migration and invasion. Philos Trans R Soc B Biol Sci 369(1638):20130102. https://doi.org/10.1098/rstb.2013.0102
Sentenac H, Bonneaud N, Minet M, Lacroute F, Salmon J-M, Gaymard F, Grignon C (1992) Cloning and expression in yeast of a plant potassium ion transport system. Science 256(5057):663–665. https://doi.org/10.1126/science.1585180
Shen L, Shrager P, Girsch SJ, Donaldson PJ, Peracchia C (1991) Channel reconstitution in liposomes and planar bilayers with HPLC-purified MIP26 of bovine lens. J Membr Biol 124(1):21–32. https://doi.org/10.1007/BF01871361
Sindhu Kumari S, Gupta N, Shiels A, FitzGerald PG, Menon AG, Mathias RT, Varadaraj K (2015) Role of Aquaporin 0 in lens biomechanics. Biochem Biophys Res Commun 462(4):339–345. https://doi.org/10.1016/j.bbrc.2015.04.138
Smith BL, Agre P (1991) Erythrocyte Mr 28,000 transmembrane protein exists as a multisubunit oligomer similar to channel proteins. J Biol Chem 266(10):6407–6415. https://doi.org/10.1016/S0021-9258(18)38133-X
Stautz J, Hellmich Y, Fuss MF, Silberberg JM, Devlin JR, Stockbridge RB, Hänelt I (2021) Molecular mechanisms for bacterial potassium homeostasis. J Mol Biol 433(16):166968. https://doi.org/10.1016/j.jmb.2021.166968
Stock C, Schwab A (2015) Ion channels and transporters in metastasis. Biochim Biophys Acta Biomembr 10:2638–2646. https://doi.org/10.1016/j.bbamem.2014.11.012
Stroka KM, Jiang H, Chen S-H, Tong Z, Wirtz D, Sun SX, Konstantopoulos K (2014) Water permeation drives tumor cell migration in confined microenvironments. Cell 157(3):611–623. https://doi.org/10.1016/j.cell.2014.02.052
Sui H, Han B-G, Lee JK, Walian P, Jap BK (2001) Structural basis of water-specific transport through the AQP1 water channel. Nature 414(6866):872–878. https://doi.org/10.1038/414872a
Tajkhorshid E, Nollert P, Jensen MØ, Miercke LJ, O’Connell J, Stroud RM, Schulten K (2002) Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296(5567):525–530. https://doi.org/10.1126/science.1067778
Tang W, Ruknudin A, Yang WP, Shaw S-Y, Knickerbocker A, Kurtz S (1995) Functional expression of a vertebrate inwardly rectifying K+ channel in yeast. Mol Biol Cell 6(9):1231–1240. https://doi.org/10.1091/mbc.6.9.1231
Tillman TS, Cascio M (2003) Effects of membrane lipids on ion channel structure and function. Cell Biochem Biophys 38(2):161–190. https://doi.org/10.1385/CBB:38:2:161
Tomita Y, Dorward H, Yool AJ, Smith E, Townsend AR, Price TJ, Hardingham JE (2017) Role of Aquaporin 1 signalling in cancer development and progression. Int J Mol Sci 18(2):299. https://doi.org/10.3390/ijms18020299
Tong J, Briggs MM, McIntosh TJ (2012) Water permeability of aquaporin-4 channel depends on bilayer composition, thickness, and elasticity. Biophys J 103(9):1899–1908. https://doi.org/10.1016/j.bpj.2012.09.025
Tong J, Canty JT, Briggs MM, McIntosh TJ (2013) The water permeability of lens aquaporin-0 depends on its lipid bilayer environment. Exp Eye Res 113:32–40. https://doi.org/10.1016/j.exer.2013.04.022
Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R, Kjellbom P (2006) Structural mechanism of plant aquaporin gating. Nature 439(7077):688–694. https://doi.org/10.1038/nature04316
Tran STH, Horie T, Imran S, Qiu J, McGaughey S, Byrt CS, Tyerman SD, Katsuhara M (2020) A survey of barley PIP aquaporin ionic conductance reveals Ca2+-sensitive HvPIP2;8 Na+ and K+ conductance. Int J Mol Sci 21(19):7135. https://doi.org/10.3390/ijms21197135
Tyerman SD, Whitehead LF, Day DA (1995) A channel-like transporter for NH4+ on the symbiotic interface of N2-fixing plants. Nature 378(6557):629–632. https://doi.org/10.1038/378629a0
Tyerman SD, McGaughey SA, Qiu J, Yool AJ, Byrt CS (2021) Adaptable and multifunctional ion-conducting aquaporins. Annu Rev Plant Biol 72(1):703–736. https://doi.org/10.1146/annurev-arplant-081720-013608
Udvardi MK, Day DA (1997) Metabolite transport across symbiotic membranes of legume nodules. Annu Rev Plant Biol 48(1):493–523. https://doi.org/10.1146/annurev.arplant.48.1.493
Ueda M, Tsutsumi N, Fujimoto M (2016) Salt stress induces internalization of plasma membrane aquaporin into the vacuole in Arabidopsis thaliana. Biochem Biophys Res Commun 474(4):742–746. https://doi.org/10.1016/j.bbrc.2016.05.028
Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425(6959):734–737. https://doi.org/10.1038/nature02027
Vacca A, Frigeri A, Ribatti D, Nicchia GP, Nico B, Ria R, Svelto M, Dammacco F (2001) Microvessel overexpression of aquaporin 1 parallels bone marrow angiogenesis in patients with active multiple myeloma. Br J Haematol 113(2):415–421. https://doi.org/10.1046/j.1365-2141.2001.02738.x
Varadaraj K, Kushmerick C, Baldo G, Bassnett S, Shiels A, Mathias R (1999) The role of MIP in lens fiber cell membrane transport. J Membr Biol 170(3):191–203. https://doi.org/10.1007/s002329900549
Varadaraj K, Kumari SS, Mathias RT (2010) Transgenic expression of AQP1 in the fiber cells of AQP0 knockout mouse: effects on lens transparency. Exp Eye Res 91(3):393–404. https://doi.org/10.1016/j.exer.2010.06.013
Verdoucq L, Grondin A, Maurel C (2008) Structure–function analysis of plant aquaporin At PIP2;1 gating by divalent cations and protons. Biochem J 415(3):409–416. https://doi.org/10.1042/BJ20080275
Verkman A, Hara-Chikuma M, Papadopoulos MC (2008) Aquaporins—new players in cancer biology. J Mol Med 86(5):523–529. https://doi.org/10.1007/s00109-008-0303-9
Wagner K, Unger L, Salman MM, Kitchen P, Bill RM, Yool AJ (2021) Signaling mechanisms and pharmacological modulators governing diverse aquaporin functions in human health and disease. Biochim Biophys Acta Biomembr in press
Wang Y, Tajkhorshid E (2007) Molecular mechanisms of conduction and selectivity in aquaporin water channels. J Nutr 137(6):1509S-1515S. https://doi.org/10.1093/jn/137.6.1509S
Wang Y, Cohen J, Boron WF, Schulten K, Tajkhorshid E (2007) Exploring gas permeability of cellular membranes and membrane channels with molecular dynamics. J Struct Biol 157(3):534–544. https://doi.org/10.1016/j.jsb.2006.11.008
Wang Z, Wang Y, He Y, Zhang N, Chang W, Niu Y (2020) Aquaporin-1 facilitates proliferation and invasion of gastric cancer cells via GRB7-mediated ERK and Ras activation. Anim Cells Syst 24(5):253–259. https://doi.org/10.1080/19768354.2020.1833985
Weaver CD, Shomer NH, Louis CF, Roberts DM (1994) Nodulin 26, a nodule-specific symbiosome membrane protein from soybean, is an ion channel. J Biol Chem 269(27):17858–17862. https://doi.org/10.1016/S0021-9258(17)32388-8
Wei X, Dong J (2015) Aquaporin 1 promotes the proliferation and migration of lung cancer cell in vitro. Oncol Rep 34(3):1440–1448. https://doi.org/10.3892/or.2015.4107
Wu B, Steinbronn C, Alsterfjord M, Zeuthen T, Beitz E (2009) Concerted action of two cation filters in the aquaporin water channel. EMBO J 28(15):2188–2194. https://doi.org/10.1038/emboj.2009.182
Yanochko GM, Yool AJ (2002) Regulated cationic channel function in Xenopus oocytes expressing Drosophila big brain. J Neurosci 22(7):2530–2540. https://doi.org/10.1523/jneurosci.22-07-02530.2002
Yanochko GM, Yool AJ (2004) Block by extracellular divalent cations of Drosophila big brain channels expressed in Xenopus oocytes. Biophys J 86(3):1470–1478. https://doi.org/10.1016/S0006-3495(04)74215-0
Yasui M, Hazama A, Kwon T-H, Nielsen S, Guggino WB, Agre P (1999a) Rapid gating and anion permeability of an intracellular aquaporin. Nature 402(6758):184–187. https://doi.org/10.1038/46045
Yasui M, Kwon T-H, Knepper MA, Nielsen S, Agre P (1999) Aquaporin-6: an intracellular vesicle water channel protein in renal epithelia. Proc Natl Acad Sci 96(10):5808–5813. https://doi.org/10.1073/pnas.96.10.5808
Yenush L (2016) Potassium and sodium transport in yeast. In: Ramos J, Sychrová H, Kschischo M (eds) Yeast Membrane Transport. Springer International Publishing, Cham, pp 187–228. (https://doi.org/10.1007/978-3-319-25304-6_8)
Yool AJ (2007) Dominant-negative suppression of big brain ion channel activity by mutation of a conserved glutamate in the first transmembrane domain. Gene Expr 13(6):329–337. https://doi.org/10.3727/000000006781510688
Yool AJ, Campbell EM (2012) Structure, function and translational relevance of aquaporin dual water and ion channels. Mol Aspects Med 33(5):553–561. https://doi.org/10.1016/j.mam.2012.02.001
Yool AJ, Weinstein AM (2002) New roles for old holes: ion channel function in aquaporin-1. News Physiol Sci 17:68–72
Yool AJ, Stamer WD, Regan JW (1996) Forskolin stimulation of water and cation permeability in aquaporin1 water channels. Science 273(5279):1216–1218. https://doi.org/10.1126/science.273.5279.1216
Yool AJ, Stamer WD (2004) Novel roles for aquaporins as gated ion channels. In: Maui RA (eds) Molecular and cellular insights to ion channel biology. Elsevier, Amsterdam, pp 351–379. https://doi.org/10.1016/S1569-2558(03)32015-6
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(9):1411–1423. https://doi.org/10.1016/j.str.2006.07.006
Yusupov M, Yan D, Cordeiro RM, Bogaerts A (2018) Atomic scale simulation of H2O2 permeation through aquaporin: toward the understanding of plasma cancer treatment. J Phys D Appl Phys 51(12):125401. https://doi.org/10.1088/1361-6463/aaae7a
Zaks-Makhina E, Kim Y, Aizenman E, Levitan ES (2004) Novel neuroprotective K+ channel inhibitor identified by high-throughput screening in yeast. Mol Pharmacol 65(1):214–219. https://doi.org/10.1124/mol.65.1.214
Zampighi GA, Hall JE, Kreman M (1985) Purified lens junctional protein forms channels in planar lipid films. Proc Natl Acad Sci 82(24):8468–8472. https://doi.org/10.1073/pnas.82.24.8468
Zhang JX, Xie C, Zhu Z, Huang H, Zeng Z (2012) Potential role of AQP1 and VEGF in the development of malignant pleural effusion in mice. Med Oncol 29(2):656–662. https://doi.org/10.1007/s12032-011-9960-6
Zhao Y, Vararattanavech A, Li X, Hélixnielsen C, Vissing T, Torres J, Wang R, Fane AG, Tang CY (2013) Effects of proteoliposome composition and draw solution types on separation performance of aquaporin-based proteoliposomes: implications for seawater desalination using aquaporin-based biomimetic membranes. Environ Sci Technol 47(3):1496–1503. https://doi.org/10.1021/es304306t
Zhou X, Su Z, Anishkin A, Haynes WJ, Friske EM, Loukin SH, Kung C, Saimi Y (2007) Yeast screens show aromatic residues at the end of the sixth helix anchor transient receptor potential channel gate. Proc Natl Acad Sci 104(39):15555–15559. https://doi.org/10.1073/pnas.0704039104
Acknowledgements
We thank Boris Martinac and Yoshitaka Nakayama for assistance with patch-clamp electrophysiology data and methods.
Funding
This work was supported by the Australian Research Council (19ARC_DP190101745), and the Medical Advances Without Animals (MAWA) Trust.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval and consent to participate
This study did not use animals or human subjects and did not require ethics approval. This study did not involve human participants. Informed consent is not applicable.
Consent for publication
This manuscript does not contain any individual person’s data in any form. Informed consent is not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Henderson, S.W., Nourmohammadi, S., Ramesh, S.A. et al. Aquaporin ion conductance properties defined by membrane environment, protein structure, and cell physiology. Biophys Rev 14, 181–198 (2022). https://doi.org/10.1007/s12551-021-00925-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12551-021-00925-3