Aquaporin evolution in fishes

Frontiers in Physiology

Volumn JUL, Issue , 2011, Pages

  Finn, Roderick Nigel ^a,b   Cerdà, Joan ^c  

^a UNIVERSITY OF BERGEN   (Norway)

^b INSTITUTE OF MARINE RESEARCH   (Norway)

^c INSTITUT DE CIÈNCIES DEL MAR   (Spain)

Author keywords

Aquaporin; Evolution; Gene duplication; Neofunctionalization; Water transport

Indexed keywords

EID: 84864990396     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2011.00044     Document Type: Review

References (56)

1. Agre, P. (2005). Aquaporin water channels. Biosci. Rep. 24, 127-163.
2. Agre, P., Borgnia, M. J., Yasui, M., Neely, J. D., Carbrey, J., Kozono, D., Beitz, E., Hoffert, J., Leitch, V., and King, L. S. (2001). "Discovery of the aqua-porins and their impact on basic and clinical physiology," in Aquaporins, eds S. Hohmann, S. Nielsen, and P. Agre (New York: Academic Press), 1-39.
3. Agre, P., Sasaki, S., and Chrispeels, M. J. (1993). Aquaporins, a family of membrane water channel proteins. Am. J.Physiol. 265, F461.
4. Amores, A., Force, A., Yan, Y. L., Joly, L., Amemiya, C., Fritz, A., Ho, R. K., Langeland, J., Prince, V., Wang, Y. L., Westerfield, M., Ekker, M., and Postlethwait, J. H. (1998). Zebrafish hox clusters and vertebrate genome evolution. Science 282, 1711-1714.
5. Beitz, E., Liu, K., Ikeda, M., Guggino, W. B., Agre, P., and Yasui, M. (2006). Determinants of AQP6 trafficking to intracellular sites versus the plasma membrane in transfected mammalian cells. Biol. Cell 98, 101-109.
6. Benga, G., Popescu, O., Borza, V., Pop, V. I., Muresan, A., Mocsy, I., Brain, A.,and Wrigglesworth,J.M. (1986a). Water permeability of human erythrocytes. Identification of membrane proteins involved in water transport. Eur. J. Cell Biol. 1986, 41, 252-262.
7. Benga, G., Popescu, O., Borza, V., Pop, V. I., and Holmes, R. E. (1986b). Chloromercuribenzenesul-fonate binding by membrane proteins and the inhibition of water transport in human erythrocytes. Biochemistry 25, 1535-1538.
8. Bloemendal, H., Vermorken, Z. F., Dunia, I., and Benedetti, E. L. (1972). The plasma membranes of eye lens fibres. Biochemical and structural characterization. Cell Differ. 1, 91-106.
9. Broekhuyse, R. M., and Kuhlmann, F. D. (1974). Lens membranes 1. Composition of urea-treated plasma membranes from calf lens. Exp. Eye Res. 19, 297-302.
10. Broekhuyse, R. M., Kuhlmann, F. D., and Stols, L. H. (1976). Lens membranes II. Isolation and characterization of the main intrinsic polypeptide (MIP) of bovine lens fiber membranes. Exp. Eye Res. 23, 365-371.
11. Cerdà, J. (2009). Molecular pathways during marine fish egg hydration: the role of aquaporins. J. Fish Biol. 75,2175-2196.
12. Cerdà, J., and Finn, R. N. (2010). Piscine aquaporins: an overview of recent advances. J. Exp. Zool. 313A, 623-650.
13. Chaube, R., Chauvigné, F., Tingaud-Sequeira, A., Joy, K. P., Acharjee, A., Singh, V., and Cerdà, J. (2011). Molecular and functional characterization of catfish (Heteropneustes fossilis) aquaporin-1b: changes in expression during ovarian development and hormone-induced follicular maturation. Gen. Comp. Endocrinol. 170, 162-171.
14. Chauvigne, E, Lubzens, E., and Cerdà, J. (2011). Design and characterization of genetically engineered zebrafish aquaporin-3 mutants highly permeable to the cryoprotectant ethylene glycol. BMC Biotechnol. 11, 34. doi: 10.1186/1472-6750-11-34
15. Cutler, C. P., and Cramb, G. (2000). "Water transport and aquaporin expression in fish," in Molecular Biology and Physiology of Water and Solute Transport, eds S. Hohmann and S. N. Neilsen (New York: Kluwer Academic/Plenum Publishers), 433-441.
16. de Groot, B. L., and Grubmüller, H. (2005). The dynamics and energetics of water permeation and proton exclusion in aquaporins. Curr. Opin. Struct. Biol. 15, 176-183.
17. Deen, P. M. T., Verdijk, D. M. A., Knoers, N. V. A. A., Wieringa, B., Monnens, L. A. H., van Os, C. H., and van Oost, B. A. (1994). Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine. Science 264, 92-95.
18. Denker, B. M., Smith, B. L., Kuhajda, F. P.,andAgre, P. (1988). Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J. Biol. Chem. 263,15634-15642.
19. Eto, K., Noda, Y., Horikawa, S., Uchida, S., and Sasaki, S. (2011). Phosphorylation of aquaporin-2 regulates its water permeability. J. Biol. Chem. 285,40777-40784.
20. Fabra, M., Raldúa, D., Bozzo, M. G., Deen, P. M. T., Lubzens, E., and Cerdà, J. (2006). Yolk proteolysis and aquaporin-1o play essential roles to regulate fish oocyte hydration during meiosis resumption. Dev. Biol. 295,250-262.
21. Fabra, M., Raldúa, D., Power, D. M., Deen, P. M. T., and Cerdà, J. (2005). Marine fish egg hydration is aquaporin-mediated. Science 307, 545.
22. Finn, R. N. (2007). The maturational disassembly and differential proteolysis of paralogous vitellogenins in a marine pelagophil teleost: a conserved mechanism of oocyte hydration. Biol. Reprod. 76, 936-948.
23. Finn, R. N., and Fyhn, H. J. (2010). Requirement for amino acids in ontogeny of fish. Aquac. Res. 41, 684-716.
24. Finn, R. N., and Kristoffersen, B. A. (2007). Vertebrate vitellogenin gene duplication in relation to the "3R hypothesis": correlation to the pelagic egg and the oceanic radiation of teleosts. PLoS ONE 2, e169. doi: 10.1371/journal.pone.0000169
25. Finn, R. N., Østby, G. C., Norberg, B., and Fyhn, H. J. (2002). In vivo oocyte hydration in Atlantic halibut (Hippoglossus hippoglossus): proteolytic liberation of free amino acids, and ion transport, are driving forces for osmotic water influx. J. Exp. Biol. 205,211-224.
26. Froger, A., Clemens, D., Kalman, K., Németh-Cahalan, K.-L., Schilling, T. E, and Hall, J. E. (2010). Two distinct aquaporin 0s are required for development and transparency of the zebrafish Lens. Invest. Ophthalmol. Vis.Sci. 51,6582-6589.
27. Gorin, M. B., Yancey, S. B., Cline, J., Revel, J. P., and Horwitz, J. (1984). The major intrinsic protein (MIP) of the bovine lens fiber membrane: characterization and structure based on cDNA cloning. Cell 39, 49-59.
28. Hamdi, M., Sanchez, M. A., Beene, L. C., Liu, Q., Landfear, S. M., Rosen, B. P., and Liu, Z. (2010). Arsenic transport by zebrafish aquaglyceroporins. BMCMol. Biol. 10, 104. doi: 10.1186/1471-2199-10-104
29. Hiraoki, Y., Tani, K., Kamagawa, A., Gyobu, N., Nishikawa, K., Suzuki, H., Walz, T., Sasaki, S., Mitsuoki, K., Kimura, K., Mizoguchi, A., and Fujiyoshi, Y (2006). Implications of the aquaporin-4 structure on array formation and cell adhesion. J. Mol. Biol. 355, 628-639.
30. Ikeda, M., Andoo, A., Shimono, M., Takamatsu, N., Taki, A., Muta, K., Matsushita, W., Uechi, T., Matsuzaki, T., Kenmochi, N., Takata, K., Sasaki, S., Ito, K., and Ishibasji, K. (2011). The NPC motif of aquaporin-11, unlike the NPA motif of known aquaporins, is essential for full expression of molecular function. J. Biol. Chem. 286, 3342-3350.
31. Itoh, T., Rai, T., Kuwahara, M., Ko, S. B., Uchida, S., Sasaki, S.,snd Ishibashi, K. (2005). Identification of a novel aquaporin, AQP12, expressed in pancreatic acinar cells. Biochem. Biophys. Res. Commun. 330,832-838.
32. Jaillon, O., Aury, J. M., Brunet, F., Petit, J. L., Stange-Thomann, N., Mauceli, E., Bouneau, L., Fischer, C., Ozouf-Costaz, C., Bernot, A., Nicaud, S., Jaffe, D., Fisher, S., Lutfalla, G., Dossat, C., Segurens, B., Dasilva, C., Salanoubat, M., Levy, M., Boudet, N., Castellano, S., Anthouard, V., Jubin, C., Castelli, V., Katinka, M., Vacherie, B., Biémont, C., Skalli, Z., Cattolico, L., Poulain, J., De Berardinis, V., Cruaud, C., Duprat, S., Brottier, P., Coutanceau, J. P., Gouzy, J., Parra, G., Lardier, G., Chapple, C., McKernan, K. J., McE-wan, P., Bosak, S., Kellis, M., Volff, J. N., Guigó, R., Zody, M. C., Mesirov, J., Lindblad-Toh, K., Birren, B., Nusbaum, C., Kahn, D., Robinson-Rechavi, M., Laudet, V., Schachter, V., Quétier, F., Saurin, W., Scarpelli, C., Wincker, P., Lander, E. S., Weis-senbach, J.,Roest Crollius, H. (2004). Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431, 946-957.
33. King, L. S., Kozono, D., and Agre, P. (2004). From structure to disease: the evolving tale of aquaporin biology. Nat. Rev. Mol. Cell Biol. 5, 687-698.
34. MacIver, B., Cutler, C. P., Yin, J., Hill, M. G., Zeidel, M. L., and Hill, W. G. (2009). Expression and functional characterization of four aquaporin water channels from the European eel (Anguilla anguilla). J. Exp. Biol. 212,2856-2863.
35. Neely, J. D., Christensen, B. M., Nielsen, S., and Agre, P. (1999). Heterotetrameric composition of aquaporin-4 water channels. Biochemistry 38, 11156-11163.
36. Park, W., Scheffler, B. E., Bauer, P. J., and Campbell, P. T. (2010). Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biol. 10, 142. doi: 10.1186/1471-2229-10-142
37. Preston, G. M., andAgre, P. (1991). Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc. Natl. Acad. Sci. U.S.A. 88, 11110-11114.
38. Preston, G. M., Carroll, T. P., Guggino, W B., and Agre, P. (1992). Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256, 385-387.
39. Stahlberg, H., Heymann, B., Mitsuoka, K., Fuyijoshi, Y., and Engel, A. (2001). "The aquaporin superfamily: structure and function," in Aquaporins, eds S. Hohmann, S. Nielsen, and P. Agre (New York: Academic Press), 40-119.
40. Sun, Y., Zhang, Q., Qi, J., Chen, Y., Zhong, Q., Li, C., Yu, Y., Li, S., and Wang, Z. (2010). Identification of differential genes in the ovary relative to the testis and their expression patterns in half-smooth tongue sole (Cynoglossus semilaevis). J. Genet. Genomics 37,137-145.
41. Suzuki, M., and Tanaka, S. (2009). Molecular and cellular regulation of water homeostasis in anuran amphibians by aquaporins. Comp. Biochem. Physiol. 153A: 231-241.
42. Takata, K., Matsuzaki, T., and Tajika, Y. (2004). Aquaporins: water channel proteins of the cell membrane. Prog. Histochem. Cytochem. 39,1-83.
43. Tamma, G., Robben, J. H., Trimpert, C., Boon, M., and Deen, P. M. T. (2011). Regulation of AQP2 localization by S256 and S261 phosphorylation and ubiquitination.Am.J. Physiol., Cell Physiol. 300, C636-C646.
44. Tatsumi, K., Tsuji, S., Miwa, H., Morisaku, T., Nuriya, M., Orihara, M., Kaneko, K., Okano, H., and Yasui, M. (2009). Drosophila big brain does not act as a water channel, but mediates cell adhesion. FEBS Lett. 583, 2077-2082.
45. Thoroddsen, A., Dahm-Kähler, P., Lind, A. K., Weijdegård, B., Lindenthal, B., Müller, J., and Bränstrøm, M. (2011). The water permeability channels aquaporins 1-4 are differentially expressed in granulosa and theca cells of the preovulatory follicle during precise stages of human ovula-tion. J. Clin. Endocrinol. Metab. 96, 1021-1028.
46. Tingaud-Sequeira, A., Calusinska, M., Finn, R. N., Chauvigne, E, Lozano, J., and Cerdà, 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. doi: 10.1186/1471-2148-10-38
47. Tingaud-Sequeira, A., Chauvigne, R, Fabra, M., Lozano, J., Raldúa, D., and Cerdà, J. (2008). Structural and functional divergence of two fish aquaporin-1 water channels following teleost-specific gene duplication. BMC Evol. Biol. 8, 259. doi: 10.1186/1471-2148-8-259
48. Tipsmark, C. K., Sørensen, K. J., and Madsen, S. S. (2010). Aquaporin expression dynamics in osmoregulatory tissues of Atlantic salmon during smoltification and seawater acclimation. J. Exp. Biol. 213, 368-379.
49. Törnroth-Horsefield, S., Wang, Y., Hedfalk, K., Johanson, U., Karlsson, M., Tajkhorshid, E., Neutze, R., and Kjellbom, P. (2006). Structural mechanism of plant aquaporin gating. Nature 439, 688-694.
50. Vermorken, A. J. M., Hildernink, J. M. H. C., Benedetti, E. L., and Bloemendal, H. (1977). Changes in membrane protein pattern in relation to lens cell differentiation. FEBS Lett. 83,301-306.
51. Virkki, L. V., Franke, C., Somieski, P., and Boron, W. E (2002). Cloning and functional characterization of a novel aquaporin from Xenopus laevis oocytes. J. Biol. Chem. 277, 40610-40616.
52. Volff, J. N. (2005). Genome evolution and biodiversity in teleost fish. Heredity 94,280-294.
53. Wu, B., and Beitz, E. (2007). Aquaporins with selectivity for unconventional permeants. Cell. Mol. Life Sci.64 2005 2413-2421
54. Zapater, C., Chauvigne, E, Norberg, B., Finn, R. N., and Cerdà, J. (2011). Dual neofunctionalization of a rapidly evolving aquaporin-1 paralog reveals constrained and relaxed traits controlling channel function during meiosis resumption in marine teleosts. Mol. Biol. Evol. doi: 10.1093/molbev/msr146. [Epub ahead of print].
55. Zardoya, R. (2005). Phylogeny and evolution of the major intrinsic protein family. Biol. Cell 97, 397-414.
56. Zichichi, R., Magnoli, D., Montalbano, G., Laurà, R., Vega, J. A., Ciriaco, E., and Germanà, A. (2011). Aquaporin 4 in the sensory organs of adult zebrafish (Danio rerio). Brain Res. 1384,23-28.