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PMID: 24292667 Published · ppublish English Journal Article Review

Prediction of aquaporin function by integrating evolutionary and functional analyses.

The Journal of membrane biology ·Vol. 247 ·No. 2 ·2014-02-00 ·Pages 107-25

Perez Di Giorgio J, Soto G, Alleva K, Jozefkowicz C, Amodeo G, Muschietti JP, Ayub ND

Abstract

Aquaporins (AQPs) are a family of channel proteins, which transport water and/or small solutes across cell membranes. AQPs are present in Bacteria, Eukarya, and Archaea. The classical AQP evolution paradigm explains the inconsistent phylogenetic trees by multiple transfer events and emphasizes that the assignment of orthologous AQPs is not possible, making it difficult to integrate functional information. Recently, a novel phylogenetic framework of eukaryotic AQP evolution showed congruence between eukaryotic AQPs and organismal trees identifying 32 orthologous clusters in plants and animals (Soto et al. Gene 503:165-176, 2012). In this article, we discuss in depth the methodological strength, the ability to predict functionality and the AQP community perception about the different paradigms of AQP evolution. Moreover, we show an updated review of AQPs transport functions in association with phylogenetic analyses. Finally, we discuss the possible effect of AQP data integration in the understanding of water and solute transport in eukaryotic cells.

MeSH Terms
Animals Aquaporins/classification,physiology Bacteria Biological Transport Eukaryota Evolution, Molecular Humans Multigene Family Phylogeny Plants Protein Conformation Protein Interaction Domains and Motifs
Chemicals
Aquaporins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Perez Di Giorgio Juliana
Instituto de Investigaciones en Ingeniería Genética y Biología Molecular, Dr. Hector Torres (INGEBI-CONICET), Vuelta de Obligado 2490, C1428ADN, Buenos Aires, Argentina.
Soto Gabriela
Alleva Karina
Jozefkowicz Cintia
Amodeo Gabriela
Muschietti Jorge Prometeo
Ayub Nicolás Daniel
References (153)
153 references, click to expand
  1. Water channel properties of major intrinsic protein of lens.
    J Biol Chem. 1995 Apr 14;270(15):9010-16 PMID: 7536742
  2. Phylogenomics and the reconstruction of the tree of life.
    Nat Rev Genet. 2005 May;6(5):361-75 PMID: 15861208
  3. Design and characterization of genetically engineered zebrafish aquaporin-3 mutants highly permeable to the cryoprotectant ethylene glycol.
    BMC Biotechnol. 2011 Apr 08;11:34 PMID: 21477270
  4. Cloning of a new aquaporin (AQP10) abundantly expressed in duodenum and jejunum.
    Biochem Biophys Res Commun. 2001 Oct 5;287(4):814-9 PMID: 11573934
  5. The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation.
    Plant Cell. 2006 Jun;18(6):1498-509 PMID: 16679457
  6. ER membrane aquaporins in plants.
    Pflugers Arch. 2008 Jul;456(4):709-16 PMID: 17924135
  7. Tetrameric assembly of CHIP28 water channels in liposomes and cell membranes: a freeze-fracture study.
    J Cell Biol. 1993 Nov;123(3):605-18 PMID: 7693713
  8. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein.
    Science. 1992 Apr 17;256(5055):385-7 PMID: 1373524
  9. The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol.
    Plant J. 1999 Jun;18(5):565-70 PMID: 10417707
  10. Substitution of a single amino acid residue in the aromatic/arginine selectivity filter alters the transport profiles of tonoplast aquaporin homologs.
    Biochim Biophys Acta. 2012 Jan;1818(1):1-11 PMID: 21963407
  11. Horizontal gene transfer in prokaryotes: quantification and classification.
    Annu Rev Microbiol. 2001;55:709-42 PMID: 11544372
  12. NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana.
    J Biol Chem. 2009 Jan 23;284(4):2114-20 PMID: 19029297
  13. Effect of expressing the water channel aquaporin-1 on the CO2 permeability of Xenopus oocytes.
    Am J Physiol. 1998 Feb;274(2):C543-8 PMID: 9486145
  14. Purification and functional characterization of aquaporin-8.
    Biol Cell. 2006 Mar;98(3):153-61 PMID: 15948717
  15. Functional identification of the glycerol permease activity of Arabidopsis thaliana NLM1 and NLM2 proteins by heterologous expression in Saccharomyces cerevisiae.
    FEBS Lett. 2000 Sep 22;481(3):293-8 PMID: 11007982
  16. Relative CO(2)/NH(3) selectivities of mammalian aquaporins 0-9.
    Am J Physiol Cell Physiol. 2013 May 15;304(10):C985-94 PMID: 23485707
  17. Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens.
    BMC Plant Biol. 2008 Apr 22;8:45 PMID: 18430224
  18. Transport functions and expression analysis of vacuolar membrane aquaporins in response to various stresses in rice.
    J Plant Physiol. 2008 Dec;165(18):1879-88 PMID: 18707797
  19. Isolation and characterization of three maize aquaporin genes, ZmNIP2;1, ZmNIP2;4 and ZmTIP4;4 involved in urea transport.
    BMB Rep. 2012 Feb;45(2):96-101 PMID: 22360887
  20. Ammonia detoxification via ureagenesis in rat hepatocytes involves mitochondrial aquaporin-8 channels.
    Hepatology. 2013 May;57(5):2061-71 PMID: 23299935
  21. 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. 1994 Jul 5;91(14):6269-73 PMID: 7517548
  22. Ser123 is essential for the water channel activity of McPIP2;1 from Mesembryanthemum crystallinum.
    J Biol Chem. 2010 May 28;285(22):16739-47 PMID: 20332086
  23. A phylogenetic framework for the aquaporin family in eukaryotes.
    J Mol Evol. 2001 May;52(5):391-404 PMID: 11443343
  24. Aquaporins are multifunctional water and solute transporters highly divergent in living organisms.
    Biochim Biophys Acta. 2009 Jun;1788(6):1213-28 PMID: 19327343
  25. Homology assessment and molecular sequence alignment.
    J Biomed Inform. 2006 Feb;39(1):18-33 PMID: 16380300
  26. An aquaglyceroporin is abundantly expressed early in the development of the suspensor and the embryo proper of loblolly pine.
    Plant Physiol. 2001 Dec;127(4):1556-67 PMID: 11743100
  27. A defect in the yeast plasma membrane urea transporter Dur3p is complemented by CpNIP1, a Nod26-like protein from zucchini (Cucurbita pepo L.), and by Arabidopsis thaliana delta-TIP or gamma-TIP.
    FEBS Lett. 2003 Jul 17;547(1-3):69-74 PMID: 12860388
  28. Cloning and identification of a new member of water channel (AQP10) as an aquaglyceroporin.
    Biochim Biophys Acta. 2002 Jul 19;1576(3):335-40 PMID: 12084581
  29. Identification of maize silicon influx transporters.
    Plant Cell Physiol. 2009 Jan;50(1):5-12 PMID: 18676379
  30. Lateral gene transfer in eukaryotes.
    Cell Mol Life Sci. 2005 Jun;62(11):1182-97 PMID: 15761667
  31. Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana.
    J Plant Res. 2012 Jan;125(1):147-53 PMID: 21390558
  32. Reconstituted aquaporin 1 water channels transport CO2 across membranes.
    J Biol Chem. 1998 Dec 11;273(50):33123-6 PMID: 9837877
  33. Localization and functional analysis of CHIP28k water channels in stably transfected Chinese hamster ovary cells.
    J Biol Chem. 1993 Oct 25;268(30):22756-64 PMID: 8226786
  34. Structural basis of water-specific transport through the AQP1 water channel.
    Nature. 2001 Dec 20-27;414(6866):872-8 PMID: 11780053
  35. Aquaporins: Phylogeny, Structure, and Physiology of Water Channels.
    News Physiol Sci. 1999 Oct;14:187-193 PMID: 11390849
  36. Intracellular pH sensing is altered by plasma membrane PIP aquaporin co-expression.
    Plant Mol Biol. 2010 Sep;74(1-2):105-18 PMID: 20593222
  37. Chemokine-dependent T cell migration requires aquaporin-3-mediated hydrogen peroxide uptake.
    J Exp Med. 2012 Sep 24;209(10):1743-52 PMID: 22927550
  38. PIP1 and PIP2 aquaporins are differentially expressed during tobacco anther and stigma development.
    J Exp Bot. 2005 Jan;56(409):113-21 PMID: 15520027
  39. Cloning, functional characterization and heterologous expression of TaLsi1, a wheat silicon transporter gene.
    Plant Mol Biol. 2012 May;79(1-2):35-46 PMID: 22351076
  40. The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO₂ transport facilitator.
    Plant J. 2011 Sep;67(5):795-804 PMID: 21564354
  41. Rapid gating and anion permeability of an intracellular aquaporin.
    Nature. 1999 Nov 11;402(6758):184-7 PMID: 10647010
  42. Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane.
    FASEB J. 2006 Oct;20(12):1974-81 PMID: 17012249
  43. Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system.
    Plant J. 1994 Aug;6(2):187-99 PMID: 7920711
  44. The polyhydroxyalkanoate genes of a stress resistant Antarctic Pseudomonas are situated within a genomic island.
    Plasmid. 2007 Nov;58(3):240-8 PMID: 17629557
  45. Evidence for a glycerol pathway through aquaporin 1 (CHIP28) channels.
    Pflugers Arch. 1995 Jul;430(3):447-58 PMID: 7491270
  46. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes.
    J Biol Chem. 2007 Jan 12;282(2):1183-92 PMID: 17105724
  47. Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501.
    Proc Natl Acad Sci U S A. 2008 May 27;105(21):7564-9 PMID: 18495935
  48. Arabidopsis NIP2;1, a major intrinsic protein transporter of lactic acid induced by anoxic stress.
    J Biol Chem. 2007 Aug 17;282(33):24209-18 PMID: 17584741
  49. Ion permeation of AQP6 water channel protein. Single channel recordings after Hg2+ activation.
    J Biol Chem. 2002 Aug 9;277(32):29224-30 PMID: 12034750
  50. Horizontal gene transfer: the path to maturity.
    Mol Microbiol. 2003 Nov;50(3):725-7 PMID: 14617135
  51. FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization.
    Proc Natl Acad Sci U S A. 2007 Jul 24;104(30):12359-64 PMID: 17636130
  52. Isolation and characterization of the urease gene (URE) from the pathogenic fungus Coccidioides immitis.
    Gene. 1997 Oct 1;198(1-2):387-91 PMID: 9370306
  53. Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation.
    Plant Cell. 1998 Mar;10(3):451-9 PMID: 9501117
  54. Aquaporin NIP2;1 is mainly localized to the ER membrane and shows root-specific accumulation in Arabidopsis thaliana.
    Plant Cell Physiol. 2006 Oct;47(10):1420-6 PMID: 16954136
  55. Ammonia permeability of the soybean nodulin 26 channel.
    FEBS Lett. 2010 Oct 22;584(20):4339-43 PMID: 20875821
  56. Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance.
    Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):13052-6 PMID: 7528931
  57. Purification and functional reconstitution of soybean nodulin 26. An aquaporin with water and glycerol transport properties.
    Biochemistry. 1999 Jan 5;38(1):347-53 PMID: 9890916
  58. Enhancement of proton conductance by mutations of the selectivity filter of aquaporin-1.
    J Mol Biol. 2011 Apr 8;407(4):607-20 PMID: 21277313
  59. Differential water permeability and regulation of three aquaporin 4 isoforms.
    Cell Mol Life Sci. 2010 Mar;67(5):829-40 PMID: 20013023
  60. Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes.
    Plant J. 1999 Jun;18(6):577-87 PMID: 10417709
  61. Aquaporins with selectivity for unconventional permeants.
    Cell Mol Life Sci. 2007 Sep;64(18):2413-21 PMID: 17571212
  62. Aquaporin-11 containing a divergent NPA motif has normal water channel activity.
    Biochim Biophys Acta. 2007 Mar;1768(3):688-93 PMID: 17178102
  63. Purified lens junctional protein forms channels in planar lipid films.
    Proc Natl Acad Sci U S A. 1985 Dec;82(24):8468-72 PMID: 2417221
  64. Aquaporins constitute a large and highly divergent protein family in maize.
    Plant Physiol. 2001 Mar;125(3):1206-15 PMID: 11244102
  65. Phylogenetic characterization of the MIP family of transmembrane channel proteins.
    J Membr Biol. 1996 Oct;153(3):171-80 PMID: 8849412
  66. Detecting lateral gene transfers by statistical reconciliation of phylogenetic forests.
    BMC Bioinformatics. 2010 Jun 15;11:324 PMID: 20550700
  67. Plasma membrane aquaporins in the motor cells of Samanea saman: diurnal and circadian regulation.
    Plant Cell. 2002 Mar;14(3):727-39 PMID: 11910017
  68. The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic.
    J Exp Bot. 2011 Aug;62(12):4391-8 PMID: 21586431
  69. TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana.
    Plant J. 2010 Dec;64(6):1038-47 PMID: 21143683
  70. A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes.
    BMC Biol. 2008 Jun 10;6:26 PMID: 18544156
  71. The NPC motif of aquaporin-11, unlike the NPA motif of known aquaporins, is essential for full expression of molecular function.
    J Biol Chem. 2011 Feb 4;286(5):3342-50 PMID: 21118806
  72. Water and glycerol permeabilities of aquaporins 1-5 and MIP determined quantitatively by expression of epitope-tagged constructs in Xenopus oocytes.
    J Biol Chem. 1997 Jun 27;272(26):16140-6 PMID: 9195910
  73. Subcellular localization of selectively permeable aquaporins in the male germ line of a marine teleost reveals spatial redistribution in activated spermatozoa.
    Biol Reprod. 2013 Aug 15;89(2):37 PMID: 23782838
  74. Boron toxicity tolerance in barley through reduced expression of the multifunctional aquaporin HvNIP2;1.
    Plant Physiol. 2010 Aug;153(4):1706-15 PMID: 20581256
  75. Novel type aquaporin SIPs are mainly localized to the ER membrane and show cell-specific expression in Arabidopsis thaliana.
    FEBS Lett. 2005 Oct 24;579(25):5814-20 PMID: 16223486
  76. The zebrafish genome encodes the largest vertebrate repertoire of functional aquaporins with dual paralogy and substrate specificities similar to mammals.
    BMC Evol Biol. 2010 Feb 11;10:38 PMID: 20149227
  77. Pentavalent methylated arsenicals are substrates of human AQP9.
    Biometals. 2010 Feb;23(1):119-27 PMID: 19802720
  78. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.
    Mol Biol Evol. 2011 Oct;28(10):2731-9 PMID: 21546353
  79. Cloning and expression of apical membrane water channel of rat kidney collecting tubule.
    Nature. 1993 Feb 11;361(6412):549-52 PMID: 8429910
  80. Molecular cloning and characterization of an aquaporin cDNA from salivary, lacrimal, and respiratory tissues.
    J Biol Chem. 1995 Jan 27;270(4):1908-12 PMID: 7530250
  81. Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9.
    Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6053-8 PMID: 11972053
  82. From genome to function: the Arabidopsis aquaporins.
    Genome Biol. 2002;3(1):RESEARCH0001 PMID: 11806824
  83. Members of the aquaporin family in the developing pea seed coat include representatives of the PIP, TIP, and NIP subfamilies.
    Plant Mol Biol. 2003 Nov;53(5):633-45 PMID: 15010602
  84. Aquaporin gating.
    Curr Opin Struct Biol. 2006 Aug;16(4):447-56 PMID: 16837191
  85. Secretin promotes osmotic water transport in rat cholangiocytes by increasing aquaporin-1 water channels in plasma membrane. Evidence for a secretin-induced vesicular translocation of aquaporin-1.
    J Biol Chem. 1997 May 16;272(20):12984-8 PMID: 9148905
  86. Bidirectional water fluxes and specificity for small hydrophilic molecules in aquaporins 0-5.
    J Biol Chem. 1998 Dec 4;273(49):32446-51 PMID: 9829975
  87. Tissue and cell-specific localization of rice aquaporins and their water transport activities.
    Plant Cell Physiol. 2008 Jan;49(1):30-9 PMID: 18037610
  88. A silicon transporter in rice.
    Nature. 2006 Mar 30;440(7084):688-91 PMID: 16572174
  89. Loop A is critical for the functional interaction of two Beta vulgaris PIP aquaporins.
    PLoS One. 2013;8(3):e57993 PMID: 23483963
  90. Water permeability and characterization of aquaporin-11.
    J Struct Biol. 2011 May;174(2):315-20 PMID: 21251984
  91. Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels.
    Biochemistry. 2005 Dec 27;44(51):16826-34 PMID: 16363796
  92. Comparison of the water transporting properties of MIP and AQP1.
    J Membr Biol. 1997 Sep 1;159(1):29-39 PMID: 9309208
  93. Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis.
    Plant Physiol. 2003 Nov;133(3):1220-8 PMID: 14576283
  94. Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole.
    Plant Physiol. 2005 Feb;137(2):671-80 PMID: 15665250
  95. The vacuolar membrane protein gamma-TIP creates water specific channels in Xenopus oocytes.
    EMBO J. 1993 Jun;12(6):2241-7 PMID: 8508761
  96. Genome-wide molecular clock and horizontal gene transfer in bacterial evolution.
    J Bacteriol. 2004 Oct;186(19):6575-85 PMID: 15375139
  97. The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants.
    Plant Physiol. 2001 Aug;126(4):1358-69 PMID: 11500536
  98. 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. 1996 Aug 1;35(3):543-50 PMID: 8812490
  99. Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter.
    Plant Physiol. 2004 Jun;135(2):1059-68 PMID: 15181215
  100. Arabidopsis NIP1;1 transports antimonite and determines antimonite sensitivity.
    Plant Cell Physiol. 2009 Nov;50(11):1977-81 PMID: 19783540
  101. Heterotetrameric composition of aquaporin-4 water channels.
    Biochemistry. 1999 Aug 24;38(34):11156-63 PMID: 10460172
  102. Cloning and expression of AQP3, a water channel from the medullary collecting duct of rat kidney.
    Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10997-1001 PMID: 7526388
  103. Molecular cloning of a new aquaporin from rat pancreas and liver.
    J Biol Chem. 1997 Nov 28;272(48):30329-33 PMID: 9374520
  104. The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions.
    Nature. 2003 Oct 16;425(6959):734-7 PMID: 14520414
  105. Aquaporin tetramer composition modifies the function of tobacco aquaporins.
    J Biol Chem. 2010 Oct 8;285(41):31253-60 PMID: 20657033
  106. Molecular mechanisms of urea transport in plants.
    J Membr Biol. 2006;212(2):83-91 PMID: 17264988
  107. Carrier-mediated urea transport across the mitochondrial membrane of an elasmobranch (Raja erinacea) and a teleost (Oncorhynchus mykiss) fish.
    Am J Physiol Regul Integr Comp Physiol. 2008 Jun;294(6):R1947-57 PMID: 18385468
  108. Piscine aquaporins: an overview of recent advances.
    J Exp Zool A Ecol Genet Physiol. 2010 Dec 1;313(10):623-50 PMID: 20717996
  109. Structure of a glycerol-conducting channel and the basis for its selectivity.
    Science. 2000 Oct 20;290(5491):481-6 PMID: 11039922
  110. The evolutionary aspects of aquaporin family.
    Am J Physiol Regul Integr Comp Physiol. 2011 Mar;300(3):R566-76 PMID: 21148473
  111. Aquaporin-1 transports NO across cell membranes.
    Hypertension. 2006 Jul;48(1):157-64 PMID: 16682607
  112. Aquaporin adipose, a putative glycerol channel in adipocytes.
    J Biol Chem. 2000 Jul 7;275(27):20896-902 PMID: 10777495
  113. Regulation of statoconia mineralization in Aplysia californica in vitro.
    Connect Tissue Res. 1996;35(1-4):317-23 PMID: 9084670
  114. Cloned human aquaporin-1 is a cyclic GMP-gated ion channel.
    Mol Pharmacol. 2000 Mar;57(3):576-88 PMID: 10692499
  115. Acyrthosiphon pisum AQP2: a multifunctional insect aquaglyceroporin.
    Biochim Biophys Acta. 2012 Mar;1818(3):627-35 PMID: 22166843
  116. Insights into plant plasma membrane aquaporin trafficking.
    Trends Plant Sci. 2013 Jun;18(6):344-52 PMID: 23291163
  117. Interactions between plasma membrane aquaporins modulate their water channel activity.
    Plant Cell. 2004 Jan;16(1):215-28 PMID: 14671024
  118. The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is a homolog of the tonoplast water channel protein TIP.
    Plant Physiol. 1994 Dec;106(4):1325-33 PMID: 7846153
  119. Aquaporin evolution in fishes.
    Front Physiol. 2011 Jul 26;2:44 PMID: 21886623
  120. Aquaporin homologues in plants and mammals transport ammonia.
    FEBS Lett. 2004 Sep 10;574(1-3):31-6 PMID: 15358535
  121. Functional and molecular characterization of the human neutral solute channel aquaporin-9.
    Am J Physiol. 1999 Nov;277(5):F685-96 PMID: 10564231
  122. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain.
    Proc Natl Acad Sci U S A. 2008 Jul 22;105(29):9931-5 PMID: 18626020
  123. Arginine degradation by arginase in mitochondria of soybean seedling cotyledons.
    Planta. 2000 Mar;210(4):652-8 PMID: 10787060
  124. CDD: conserved domains and protein three-dimensional structure.
    Nucleic Acids Res. 2013 Jan;41(Database issue):D348-52 PMID: 23197659
  125. Characterization of aquaporin-6 as a nitrate channel in mammalian cells. Requirement of pore-lining residue threonine 63.
    J Biol Chem. 2002 Oct 18;277(42):39873-9 PMID: 12177001
  126. Role of the aquaporin PIP1 subfamily in the chilling tolerance of rice.
    Plant Cell Physiol. 2009 Feb;50(2):216-29 PMID: 19098326
  127. Phylogeny and evolution of the major intrinsic protein family.
    Biol Cell. 2005 Jun;97(6):397-414 PMID: 15850454
  128. Triiodothyronine modulates the expression of aquaporin-8 in rat liver mitochondria.
    J Endocrinol. 2007 Jan;192(1):111-20 PMID: 17210748
  129. Characterization of four plasma membrane aquaporins in tulip petals: a putative homolog is regulated by phosphorylation.
    Plant Cell Physiol. 2008 Aug;49(8):1196-208 PMID: 18567892
  130. Relative CO2/NH3 selectivities of AQP1, AQP4, AQP5, AmtB, and RhAG.
    Proc Natl Acad Sci U S A. 2009 Mar 31;106(13):5406-11 PMID: 19273840
  131. Gene family content-based phylogeny of prokaryotes: the effect of criteria for inferring homology.
    Syst Biol. 2005 Apr;54(2):268-76 PMID: 16012097
  132. Abiotic stresses modulate expression of major intrinsic proteins in barley (Hordeum vulgare).
    C R Biol. 2011 Feb;334(2):127-39 PMID: 21333943
  133. Function of a separate NH3-pore in Aquaporin TIP2;2 from wheat.
    FEBS Lett. 2007 Nov 27;581(28):5413-7 PMID: 17967420
  134. Arsenic trioxide uptake by human and rat aquaglyceroporins.
    Biochem Biophys Res Commun. 2004 Apr 16;316(4):1178-85 PMID: 15044109
  135. Two distinct aquaporin 0s required for development and transparency of the zebrafish lens.
    Invest Ophthalmol Vis Sci. 2010 Dec;51(12):6582-92 PMID: 20671274
  136. Members of rice plasma membrane intrinsic proteins subfamily are involved in arsenite permeability and tolerance in plants.
    Transgenic Res. 2012 Dec;21(6):1265-77 PMID: 22350764
  137. Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins.
    Nature. 2003 Sep 25;425(6956):393-7 PMID: 14508488
  138. Plant plasma membrane water channels conduct the signalling molecule H2O2.
    Biochem J. 2008 Aug 15;414(1):53-61 PMID: 18462192
  139. New insight into the evolution of aquaporins from flowering plants and vertebrates: orthologous identification and functional transfer is possible.
    Gene. 2012 Jul 15;503(1):165-76 PMID: 22561693
  140. NH3 and NH4+ permeability in aquaporin-expressing Xenopus oocytes.
    Pflugers Arch. 2005 Sep;450(6):415-28 PMID: 15988592
  141. Molecular biology of microbial ureases.
    Microbiol Rev. 1995 Sep;59(3):451-80 PMID: 7565414
  142. Origin of plant glycerol transporters by horizontal gene transfer and functional recruitment.
    Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14893-6 PMID: 12397183
  143. A look inside: localization patterns and functions of intracellular plant aquaporins.
    New Phytol. 2009 Oct;184(2):289-302 PMID: 19674338
  144. Water-selective and multifunctional aquaporins from Lotus japonicus nodules.
    Planta. 2000 Apr;210(5):741-8 PMID: 10805445
  145. Water transport by the Na+/glucose cotransporter under isotonic conditions.
    Biol Cell. 1997 Aug;89(5-6):307-12 PMID: 9468601
  146. Functional analysis of nodulin 26, an aquaporin in soybean root nodule symbiosomes.
    J Biol Chem. 1997 Jun 27;272(26):16256-61 PMID: 9195927
  147. Aquaporin 6 is permeable to glycerol and urea.
    Pflugers Arch. 2004 May;448(2):181-6 PMID: 14985982
  148. NIP6;1 is a boric acid channel for preferential transport of boron to growing shoot tissues in Arabidopsis.
    Plant Cell. 2008 Oct;20(10):2860-75 PMID: 18952773
  149. Water permeability of rat liver mitochondria: A biophysical study.
    Biochim Biophys Acta. 2006 Aug;1758(8):1018-24 PMID: 16934743
  150. Characterization of substrate specificity of a rice silicon transporter, Lsi1.
    Pflugers Arch. 2008 Jul;456(4):679-86 PMID: 18214526
  151. Cloning and functional expression of a new water channel abundantly expressed in the testis permeable to water, glycerol, and urea.
    J Biol Chem. 1997 Aug 15;272(33):20782-6 PMID: 9252401
  152. AtTIP1;3 and AtTIP5;1, the only highly expressed Arabidopsis pollen-specific aquaporins, transport water and urea.
    FEBS Lett. 2008 Dec 10;582(29):4077-82 PMID: 19022253
  153. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide.
    Biochim Biophys Acta. 2014 May;1840(5):1596-604 PMID: 24060746
Article Info
Journal
The Journal of membrane biology
Abbr.
J Membr Biol
ISSN
1432-1424
DOI
10.1007/s00232-013-9618-8
Published
2014-02-00
Epub
2013-00-29
Pages
107-25
Language
English
Region
United States
NLM ID
0211301
Subset
IM
External Links
PubMed source DOI: 10.1007/s00232-013-9618-8 View journal details
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