Skip to main content

The Evolutionary Aspects of Aquaporin Family

  • Chapter
  • First Online:

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 969))

Abstract

Aquaporins (AQPs ) are a family of transmembrane proteins present in almost all species including virus. They are grossly divided into three subfamilies based on the sequence around a highly conserved pore-forming NPA motif: (1) classical water -selective AQP (CAQP), (2) glycerol -permeable aquaglyceroporin (AQGP) and (3) AQP super-gene channel, superaquaporin (SAQP). AQP is composed of two tandem repeats of conserved three transmembrane domains and a NPA motif. AQP ancestors probably started in prokaryotes by the duplication of half AQP genes to be diversified into CAQPs or AQGPs by evolving a subfamily-specific carboxyl-terminal NPA motif. Both AQP subfamilies may have been carried over to unicellular eukaryotic ancestors, protists and further to multicellular organisms. Although fungus lineage has kept both AQP subfamilies, the plant lineage has lost AQGP after algal ancestors with extensive diversifications of CAQPs into PIP, TIP, SIP, XIP, HIP and LIP with a possible horizontal transfer of NIP from bacteria. Interestingly, the animal lineage has obtained new SAQP subfamily with highly deviated NPA motifs, especially at the amino-terminal halves in both prostomial and deuterostomial animals. The prostomial lineage has lost AQGP after hymenoptera, while the deuterostomial lineage has kept all three subfamilies up to the vertebrate with diversified CAQPs (AQP0, 1, 2, 4, 5, 6, 8) and AQGPs (AQP3, 7, 9, 10) with limited SAQPs (AQP11, 12) in mammals. Whole-genome duplications, local gene duplications and horizontal gene transfers may have produced the AQP diversity with adaptive selections and functional alternations in response to environment changes. With the above evolutionary perspective in mind, the function of each AQP could be speculated by comparison among species to get new insights into physiological roles of AQPs . This evolutionary guidance in AQP research will lead to deeper understandings of water and solute homeostasis.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  1. Abascal F, Irisarri I, Zardoya R (2014) Diversity and evolution of membrane intrinsic proteins. Biochim Biophys Acta 1840(5):1468–1481

    Article  CAS  PubMed  Google Scholar 

  2. Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141

    Article  CAS  PubMed  Google Scholar 

  3. Agre P (2004) Aquaporin water channels (Nobel lecture). Angew Chem-Int Ed 43:4278–4290

    Article  CAS  Google Scholar 

  4. Ahmadpour D, Geijer C, Tamas MJ, Lindkvist-Petersson K, Hohmann S (2014) Yeast reveals unexpected roles and regulatory features of aquaporins and aquaglyceroporins. Biochim Biophys Acta 1840:1482–1491

    Article  CAS  PubMed  Google Scholar 

  5. Amores A, Catchen J, Ferrara A, Fontenot Q, Postlethwaite JH (2011) Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics 188:799–808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Andersson JO (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62:1182–1197

    Article  CAS  PubMed  Google Scholar 

  7. Bahamontes-Rosa N, Wu B, Beitz E, Kremsner PG, Kun JF (2007) Limited genetic diversity of the Plasmodium falciparum aquaglyceroporin gene. Mol Biochem Parasitol 156:255–257

    Article  CAS  PubMed  Google Scholar 

  8. 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  10. Beitz E, Wu B, 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 U S A 103:269–274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Benga G (2012) On the definition, nomenclature and classification of water channel proteins (aquaporins and relatives). Mol Asp Med 33(5–6):514–517

    Article  CAS  Google Scholar 

  12. Benoit JB, Hansen IA, Szuter EM, Drake LL, Burnett DL, Attardo GM (2014) Emerging roles of aquaporins in relation to the physiology of blood-feeding arthropods. J Comp Physiol B 184:811–825

    Article  PubMed  Google Scholar 

  13. Berthelot C, Brunet F, Chalopin D, Juanchich A, Bernard M, Noel B, Bento P, Da Silva C, Labadie K, Alberti A et al (2014) The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun 5:3657

    Article  PubMed  PubMed Central  Google Scholar 

  14. Bienert GP, Bienert MD, Jahn TP, Boutry M, Chaumont F (2011) Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates. Plant J 66:306–317

    Article  CAS  PubMed  Google Scholar 

  15. Bienert GP, Desguin B, Chaumont F, Hols P (2013) Channel-mediated lactic acid transport: a novel function for aquaglyceroporins in bacteria. Biochemist J454:559–570

    Article  CAS  Google Scholar 

  16. Brunet FG, Crollius HR, Paris M, Aury JM, Gibert P, Jaillon O, Laudet V, Robinson-Rechavi M (2006) Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. Mol Biol Evol 23:1808–1816

    Article  CAS  PubMed  Google Scholar 

  17. 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  CAS  PubMed  Google Scholar 

  18. Campbell EM, Ball A, Hoppler S, Bowman AS (2008) Invertebrate aquaporins: a review. J Comp Physiol B 178(8):935–955

    Article  CAS  PubMed  Google Scholar 

  19. Canestro C, Albalat R, Irimia M, Garcia-Fernandez J (2013) Impact of gene gains, losses and duplication modes on the origin and diversification of vertebrates. Semin Cell Dev Biol 24:83–94

    Article  PubMed  Google Scholar 

  20. Cavalier-Smith T (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52:297–354

    Article  CAS  PubMed  Google Scholar 

  21. Czyzewski BK, Wang DN (2012) Identification and characterization of a bacterial hydrosulphide ion channel. Nature 483(7390):494–497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Danielson JA, Johanson U (2008) Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 8:45

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Danielson JA, Johanson U (2010) Phylogeny of major intrinsic proteins. Adv Exp Med Biol 679:9–31

    Google Scholar 

  24. Donoghue PC, Purnell MA (2005) Genome duplication, extinction and vertebrate evolution. Trends Ecol Evol 20:312–319

    Article  PubMed  Google Scholar 

  25. Drake LL, Rodriguez SD, Hansen IA (2015) Functional characterization of aquaporins and aquaglyceroporins of the yellow fever mosquito, Aedes aegypti. Sci Rep 5:7795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Fadiel A, Isokpehi RD, Stambouli N, Hamza A, Benammar-Elgaaied A, Scalise TJ (2009) Protozoan parasite aquaporins. Expert Rev Proteomics 6:199–211

    Article  CAS  PubMed  Google Scholar 

  27. Finn RN, Cerda J (2015) Evolution and functional diversity of aquaporins. Biol Bull 229:6–23

    Article  CAS  PubMed  Google Scholar 

  28. Finn RN, Chauvigne F, Hlidberg JB, Cutler CP, Cerda J (2014) The lineage-specific evolution of aquaporin gene clusters facilitated tetrapod terrestrial adaptation. PLoS One 9(11):e113686

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Finn RN, Chauvigne F, Stavang JA, Belles X, Cerda J (2015) Insect glycerol transporters evolved by functional co-option and gene replacement. Nat Commun 6:7814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Froger A, Clemens D, Kalman K, Nemeth-Cahalan KL, Schilling TF, Hall JE (2010) Two distinct aquaporin 0 s required for development and transparency of the zebrafish lens. Invest Ophthalmol Vis Sci 51:6582–6592

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  32. 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 290:481–486

    Article  CAS  PubMed  Google Scholar 

  33. 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 U S A 103(14):5355–5360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Gomes D, Agasse A, Thiebaud P, Delrot S, Geros H, Chaumont F (2009) Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim Biophys Acta 1788(6):1213–1228

    Article  CAS  PubMed  Google Scholar 

  35. Gonen T, Sliz P, Kistler J, Cheng Y, Walz T (2004) Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 429:193–197

    Article  CAS  PubMed  Google Scholar 

  36. Grohme MA, Mali B, Wełnicz W, Michel S, Schill RO, Frohme M (2013) The aquaporin channel repertoire of the tardigrade Milnesium tardigradum. Bioinf Biol Insight 7:153–165

    Article  CAS  Google Scholar 

  37. Gupta AB, Sankararamakrishnan R (2009) Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biol 9:Art. no. 134

    Google Scholar 

  38. Gupta AB, Verma RK, Agarwal V, Vajpai M, Bansal V, Sankararamakrishnan R (2012) MIPModDB: a central resource for the superfamily of major intrinsic proteins. Nucleic Acids Res 40:D362–D369

    Article  CAS  PubMed  Google Scholar 

  39. Gustavsson S, Lebrun AS, Norden K, Chaumont F, Johanson U (2005) A novel plant major intrinsic protein in Physcomitrella patens most similar to bacterial glycerol channels. Plant Physiol 139(1):287–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Hara-Chikuma M, Verkman AS (2006) Physiological roles of glycerol-transporting aquaporins: the aquaglyceroporins. Cell Mol Life Sci 63:1386–1392

    Article  CAS  PubMed  Google Scholar 

  41. Hedfalk K, Bill RM, Mullins JG, Karlgren S, Filipsson C, Bergstrom J, Tamás MJ, Rydström J, Hohmann S (2004) A regulatory domain in the C-terminal extension of the yeast glycerol channel Fps1p. J Biol Chem 279:14954–14960

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  43. Hub JS, de Groot BL (2008) Mechanism of selectivity in aquaporins and aquaglyceroporins. Proc Natl Acad Sci U S A 105:1198–1203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Innan H, Kondrashov F (2010) The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 11:97–108

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  46. Ishibashi K (2009) New members of mammalian aquaporins: AQP10-AQP12. Handb Exp Pharmacol 190:251–262

    Article  CAS  Google Scholar 

  47. Ishibashi K, Sasaki S (1998) The dichotomy of MIP family suggests two separate origins of water channels. News Physiol Sci 13:137–142

    CAS  PubMed  Google Scholar 

  48. Ishibashi K, Kuwahara M, Sasaki S (2000) Molecular biology of aquaporins. Rev Physiol Biochem Pharmacol 141:1–32

    Article  CAS  PubMed  Google Scholar 

  49. Ishibashi K, Hara S, Kondo S (2009) Aquaporin water channels in mammals. Clin Exp Nephrol 13:107–117

    Article  CAS  PubMed  Google Scholar 

  50. Ishibashi K, Kondo S, Hara S, Morishita Y (2011) The evolutionary aspects of aquaporin family. Am J Phys Regul Integr Comp Phys 300:R566–R576

    CAS  Google Scholar 

  51. Ishibashi K, Koike S, Kondo S, Hara S, Tanaka Y (2009) The role of a group III AQP, AQP11 in intracellular organelle homeostasis. J Med Investig 56(Suppl):312–317

    Article  Google Scholar 

  52. Itoh T, Rai T, Kuwahara M, Ko SB, Uchida S, Sasaki S, Ishibashi K (2005) Identification of a novel aquaporin, AQP12, expressed in pancreatic acinar cells. Biochem Biophys Res Commun 330:832–838

    Article  CAS  PubMed  Google Scholar 

  53. 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  CAS  PubMed  Google Scholar 

  54. Kataoka N, Miyake S, Azuma M (2009) Aquaporin and aquaglyceroporin in silkworms, differently expressed in the hindgut and midgut of Bombyx mori. Insect Mol Biol 18:303–314

    Article  CAS  PubMed  Google Scholar 

  55. 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 Phys Cell Phys 289:C397–C407

    Article  CAS  Google Scholar 

  56. Kayingo G, Sirotkin V, Hohmann S, Prior BA (2004) Accumulation and release of the osmolyte glycerol is independent of the putative MIP channel Spac977.17p in Schizosaccharomyces pombe. Antonie Van Leeuwenhoek 85:85–92

    Article  CAS  PubMed  Google Scholar 

  57. Keeling PJ, Palmer JD (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9:605–618

    Article  CAS  PubMed  Google Scholar 

  58. Khabudaev KV, Petrova DP, Grachev MA, Likhoshway YV (2014) A new subfamily LIP of the major intrinsic proteins. BMC Genomics 15:173

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Konno N, Hyodo S, Yamaguchi Y, Matsuda K, Uchiyama M (2010) Vasotocin/V2-type receptor/aquaporin axis exists in African lungfish kidney but is functional only in terrestrial condition. Endocrinology 151:1089–1096

    Article  CAS  PubMed  Google Scholar 

  60. Kozono D, Ding X, Iwasaki I, Meng X, Kamagata Y, Agre P, Kitagawa Y (2003) Functional expression and characterization of an archaeal aquaporin AqpM from Methanothermobacter marburgensis. J Biol Chem 278:10649–10656

    Article  CAS  PubMed  Google Scholar 

  61. Kuraku S, Meyer A, Kuratani S (2009) Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after? Mol Biol Evol 26:47–59

    Article  CAS  PubMed  Google Scholar 

  62. Laize V, Tacnet F, Ripoche P, Hohmann S (2000) Polymorphism of Saccharomyces cerevisiae aquaporins. Yeast 16:897–903

    Article  CAS  PubMed  Google Scholar 

  63. Lee JK, Kozono D, Remis J, Kitagawa Y, Agre P, Stroud RM (2005) Structural basis for conductance by the archaeal aquaporin AqpM at 1.68 A. Proc Natl Acad Sci U S A 102:18932–18937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Lee SJ, Murphy CT, Kenyon C (2009) Glucose shortens the life span of C. elegans by downregulating DAF-16/FOXO activity and aquaporin gene expression. Cell Metab 10:379–391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Li G, Santoni V, Maurel C (2014) Plant aquaporins: roles in plant physiology. Biochim Biophys Acta 1840:1574–1582

    Article  CAS  PubMed  Google Scholar 

  66. Lin X, Hong T, Mu Y, Torres J (2012) Identification of residues involved in water versus glycerol selectivity in aquaporins by differential residue pair co-evolution. Biochim Biophys Acta 1818:907–914

    Article  CAS  PubMed  Google Scholar 

  67. Liu Y, Promeneur D, Rojek A, Kumar N, Frøkiaer 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 U S A 104:12560–12564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Macqueen DJ, Johnston IA (2014) A well-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification. Proc Biol Soc B 281:20132881

    Article  Google Scholar 

  69. Marjanovic Z, Uehlein N, Kaldenhoff R, Zwiazek JJ, Weiss M, Hampp R, Nehls U (2005) Aquaporins in poplar: what a difference a symbiont makes! Planta 222:258–268

    Article  CAS  PubMed  Google Scholar 

  70. Martos-Sitcha JA, Campinho MA, Mancera JM, Martínez-Rodríguez G, Fuentes J (2015) Vasotocin and isotocin regulate aquaporin 1 function in the sea bream. J Exp Biol 218:684–693

    Article  PubMed  Google Scholar 

  71. Meyers LA, Levin DA (2006) On the abundance of polyploids in flowering plants. Evolution 60:1198–1206

    Article  PubMed  Google Scholar 

  72. Meyer A, Schart M (1999) Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr Opin Cell Biol 11:699–704

    Article  CAS  PubMed  Google Scholar 

  73. Morinaga T, Nakakoshi M, Hirao A, Imai M, Ishibashi K (2002) Mouse aquaporin 10 gene (AQP10) is a pseudogene. Biochem Biophys Res Commun 294:630–634

    Article  CAS  PubMed  Google Scholar 

  74. Morishita Y, Sakube Y, Sasaki S, Ishibashi K (2004) Aquaporin superfamily (superaquaporins): expansion of aquaporins restricted to multicellular organisms. J Pharmacol Sci 96:276–279

    Article  CAS  PubMed  Google Scholar 

  75. Morishita Y, Matsuzaki T, Hara-chikuma M, Andoo A, Shimono M, Matsuki A, Kobayashi K, Ikeda M, Yamamoto T, Verkman AS, Kusano E, Ookawara S, Takata K, Sasaki S, Ishibashi K (2005) Disruption of aquaporin-11 produces polycystic kidneys following vacuolization of the proximal tubule. Mol Cell Biol 25:7770–7779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Mukhopadhyay R, Bhattacharjee H, Rosen BP (2014) Aquaglyceroporins: generalized metalloid channels. Biochim Biophys Acta 1840:1583–1591

    Article  CAS  PubMed  Google Scholar 

  77. Nozaki K, Ishii D, Ishibashi K (2008) Intracellular aquaporins: clues for intracellular water transport? Pflugers Arch 456:701–707

    Article  CAS  PubMed  Google Scholar 

  78. Ohta E, Itoh T, Nemoto T, Kumagai J, Ko SB, Ishibashi K, Ohno M, Uchida K, Ohta A, Sohara E, Uchida S, Sasaki S, Rai T (2009) Pancreas-specific aquaporin 12 null mice showed increased susceptibility to caerulein-induced acute pancreatitis. Am J Phys Cell Phys 297:C1368–C1378

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  80. Park JH, Saier MH Jr (1996) Phylogenetic characterization of the MIP family of transmembrane channel proteins. J Membr Biol 153:171–180

    Article  CAS  PubMed  Google Scholar 

  81. 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  CAS  PubMed  Google Scholar 

  82. Perez Di Giorgio J, Soto G, Alleva K, Jozefkowicz C, Amodeo G, Muschietti JP, Ayub ND (2014) Prediction of aquaporin function by integrating evolutionary and functional analyses. J Membr Biol 247(2):107–125

    Article  CAS  PubMed  Google Scholar 

  83. 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

    Article  CAS  PubMed  Google Scholar 

  84. Philips J, Herskowitz I (1997) Osmotic balance regulates cell fusion during mating in Saccharomyces cerevisiae. J Cell Biol 138:961–974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Pommerrenig B, Diehn TA, Bienert GP (2015) Metalloido-porins: essentiality of Nodulin 26-like intrinsic proteins in metalloid transport. Plant Sci 238:212–227

    Article  CAS  PubMed  Google Scholar 

  86. Prak S, Hem S, Boudet J, Viennois G, Sommerer N, Rossignol M, Maurel C, Santoni V (2008) Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins: role in subcellular trafficking of AtPIP2;1 in response to salt stress. Mol Cell Proteomics 7:1019–1037

    Article  CAS  PubMed  Google Scholar 

  87. Promeneur D, Liu Y, Maciel J, Agre P, King LS, Kumar N (2007) Aquaglyceroporin PbAQP during intraerythrocytic development of the malaria parasite Plasmodium berghei. Proc Natl Acad Sci U S A 104:2211–2216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. 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

    Article  CAS  PubMed  Google Scholar 

  89. Rivera MC, Lake LA (2004) The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431:152–155

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  91. Sabir F, Loureiro-Dias MC, Prista C (2016) Comparative analysis of sequences, polymorphisms and topology of yeasts aquaporins and aquaglyceroporins. FEMS Yeast Res 16:fow025

    Article  PubMed  Google Scholar 

  92. Soto G, Alleva K, Amodeo G, Muschietti J, Ayub ND (2012) New insight into the evolution of aquaporins from flowering plants and vertebrates: orthologous identification and functional transfer is possible. Gene 503:165–176

    Article  CAS  PubMed  Google Scholar 

  93. Soupene E, King N, Lee H, Kustu S (2002) Aquaporin Z of Escherichia coli: reassessment of its regulation and physiological role. J Bacteriol 84:4304–4307

    Article  CAS  Google Scholar 

  94. Stavang J, Chauvigne C, Kongshaug H, Cerda J, Nilsen F, Finn RN (2015) Phylogenomic and functional analyses of salmon lice aquaporins uncover the molecular diversity of the superfamily in Arthropoda. BMC Genomics 16:618

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. Suzuki M, Shibata Y, Ogushi Y, Okada R (2015) Molecular machinery for vasotocin-dependent transepithelial water movement in amphibians: aquaporins and evolution. Biol Bull 229:109–119

    Article  CAS  PubMed  Google Scholar 

  96. Takano J, Wada M, Ludewig U, Schaaf G, von Wiren N, Fujiwara T (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18:1498–1509

    Article  PubMed  PubMed Central  Google Scholar 

  97. Tanaka Y, Morishita Y, Ishibashi K (2015) Aquaporin10 is a pseudogene in cattle and their relatives. Biochem Biophys Rep 1:16–21

    Google Scholar 

  98. Tanghe A, Van Dijck P, Thevelein JM (2006) Why do microorganisms have aquaporins? Trends Microbiol 14:78–85

    Article  PubMed  CAS  Google Scholar 

  99. Tchekneva EE, Khuchua Z, Davis LS, Kadkina V, Dunn SR, Bachman S, Ishibashi K, Rinchik EM, Harris RC, Dikov MM, Breyer MD (2008) A newly identified ENU-induced single amino acid mutation in aquaporin-11 resulting in perinatal kidney failure in mice. J Am Nephrol Soc 19:1955–1964

    Article  CAS  Google Scholar 

  100. Tingaud-Sequeira A, Calusinska M, Finn RN, Chauvigne F, Lozano J, Cerda J (2010) The zebrafish genome encodes the largest vertebrate repertoire of functional aquaporins with dual paralogy and substrate specificities similar to mammals. BMC Evol Biol 10:38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  101. Verma RK, Prabh ND, Sankararamakrishnan R (2014) New subfamilies of major intrinsic proteins in fungi suggest novel transport properties in fungal channels: implications for the host-fungal interactions. BMC Evol Biol 14:173

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. Verma RK, Prabh ND, Sankararamakrishnan R (2015) Intra-helical salt-bridge and helix destabilizing residues within the same helical turn: role of functionally important loop E half-helix in channel regulation of major intrinsic proteins. Biochim Biophys Acta 1848(6):1436–1449

    Article  CAS  PubMed  Google Scholar 

  103. Viadiu H, Gonen T, Walz T (2007) Projection map of aquaporin-9 at 7 A resolution. J Mol Biol 367:80–88

    Article  CAS  PubMed  Google Scholar 

  104. von Bulow J, Beitz E (2015) Number and regulation of protozoan aquaporins reflect environmental complexity. Biol Bull 229:38–46

    Article  Google Scholar 

  105. Wallace IS, Shakesby AJ, Hwang JH, Choi WG, Martínková N, Douglas AE, Roberts DM (2012) Acyrthosiphon pisum AQP2: a multifunctional insect aquaglyceroporin. Biochim Biophys Acta 1818:627–635

    Article  CAS  PubMed  Google Scholar 

  106. Wang Y, Huang Y, Wang J, Cheng C, Huang W, Lu P, Xu YN, Wang P, Yan N, Shi Y (2009) Structure of the formate transporter FocA reveals a pentameric aquaporin-like channel. Nature 462:467–472

    Article  CAS  PubMed  Google Scholar 

  107. 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  CAS  PubMed  Google Scholar 

  108. Yakata K, Tani K, Fujiyoshi F (2011) Water permeability and characterization of aquaporin-11. J Struct Biol 174:315–320

    Article  CAS  PubMed  Google Scholar 

  109. Zardoya R (2005) Phylogeny and evolution of the major intrinsic protein family. Biol Cell 97(6):397–414

    Article  CAS  PubMed  Google Scholar 

  110. Zardoya R, Villalba S (2001) A phylogenetic framework for the aquaporin family in eukaryotes. J Mol Evol 52(5):391–404

    Article  CAS  PubMed  Google Scholar 

  111. Zardoya R, Ding X, Kitagawa Y, Chrispeels MJ (2002) Origin of plant glycerol transporters by horizontal gene transfer and functional recruitment. Proc Natl Acad Sci U S A 99:14893–14896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Zeuthen T (2010) Water-transporting proteins. J Membr Biol 234:57–73

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by JSPS KAKENHI Grant Number 24591243 and 15K09302.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kenichi Ishibashi M.D., Ph.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Ishibashi, K., Morishita, Y., Tanaka, Y. (2017). The Evolutionary Aspects of Aquaporin Family. In: Yang, B. (eds) Aquaporins. Advances in Experimental Medicine and Biology, vol 969. Springer, Dordrecht. https://doi.org/10.1007/978-94-024-1057-0_2

Download citation

Publish with us

Policies and ethics