Functional characterization of a novel aquaporin from Dictyostelium discoideum amoebae implies a unique gating mechanism

Journal of Biological Chemistry

Volumn 287, Issue 10, 2012, Pages 7487-7494

  Von Bülow, Julia ^a   Müller Lucks, Annika ^a   Kais, Lei ^b   Bernhards, Frank ^b   Beitz, Eric ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORINS; BASIC FUNCTIONS; CELL MOTILITY; CHANNEL GATING; CYSTEINE RESIDUES; DEVELOPMENTAL STAGE; DICTYOSTELIUM DISCOIDEUM; FUNCTIONAL CHARACTERIZATION; GATING MECHANISMS; GLYCOSYLATED; INTRACELLULAR LOOP; LOCALIZATION PATTERNS; MERCURIC CHLORIDE; MODEL ORGANISMS; POINT MUTATIONS; SELECTIVITY FILTER; STRUCTURE MODELS; WATER CHANNELS; WATER PERMEABILITY; WESTERN-BLOT ANALYSIS; WILD TYPES; XENOPUS LAEVIS OOCYTES;

AMINO ACIDS; CELL MEMBRANES; CHLORINE COMPOUNDS; CLONING; ENZYME ACTIVITY; GLYCEROL; MERCURY COMPOUNDS; OSMOSIS; TOBACCO; UREA;

CYTOLOGY;

AQUAPORIN; AQUAPORIN B; CYSTEINE; GLYCEROL; GREEN FLUORESCENT PROTEIN; MERCURIC CHLORIDE; UNCLASSIFIED DRUG; UREA;

AMINO TERMINAL SEQUENCE; AMOEBA (LIFE CYCLE STAGE); ARTICLE; CELL MOTILITY; CHANNEL GATING; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DICTYOSTELIUM DISCOIDEUM; DORMANCY; MOLECULAR CLONING; NONHUMAN; OOCYTE; OSMOREGULATION; POINT MUTATION; PREDICTION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; WATER PERMEABILITY; WESTERN BLOTTING; WILD TYPE; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; AQUAPORINS; CLONING, MOLECULAR; DICTYOSTELIUM; MOLECULAR SEQUENCE DATA; OOCYTES; PROTEIN STRUCTURE, SECONDARY; PROTOZOAN PROTEINS; SEQUENCE DELETION; WATER; WATER-ELECTROLYTE BALANCE; XENOPUS LAEVIS;

DICTYOSTELIUM DISCOIDEUM; METAZOA; PROTOZOA; XENOPUS LAEVIS;

EID: 84857692588     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.329102     Document Type: Article

References (46)

1. Preston, G. M., Smith, B. L., Zeidel, M. L., Moulds, J. J., and Agre, P. (1994) Mutations in aquaporin-1 in phenotypically normal humans without functional CHIP water channels. Science 265, 1585-1587 (Pubitemid 24308974)
2. Fu, D., Libson, A., Miercke, L. J., Weitzman, C., Nollert, P., Krucinski, J., and Stroud, R. M. (2000) Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290, 481-486
3. Pavlovic-Djuranovic, S., Kun, J. F., Schultz, J. E., and Beitz, E. (2006) Dihydroxyacetone and methylglyoxal as permeants of the Plasmodium aquaglyceroporin inhibit parasite proliferation. Biochim. Biophys. Acta 1758, 1012-1017 (Pubitemid 44373850)
4. Echevarria, M., Windhager, E. E., Tate, S. S., and Frindt, G. (1994) Cloning and expression of AQP3, a water channel from the medullary collecting duct of rat kidney. Proc. Natl. Acad. Sci. U.S.A. 91, 10997-11001 (Pubitemid 24349612)
5. Holm, L. M., Jahn, T. P., Møller, A. L., Schjoerring, J. K., Ferri, D., Klaerke, D. A., and Zeuthen, T. (2005) NH3 and NH4+ permeability in aquaporin-expressing Xenopus oocytes. Pflueger's Arch. 450, 415-428
6. Beitz, E., Wu, B., Holm, L. M., Schultz, J. E., and 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 (Pubitemid 43122390)
7. Wu, B., Steinbronn, C., Alsterfjord, M., Zeuthen, T., and Beitz, E. (2009) Concerted action of two cation filters in the aquaporin water channel. EMBO J. 28, 2188-2194
8. de Groot, B. L., and Grubmüller, H. (2001) Water permeation across biological membranes. Mechanism and dynamics of aquaporin-1 and GlpF. Science 294, 2353-2357
9. Thrane, A. S., Rappold, P. M., Fujita, T., Torres, A., Bekar, L. K., Takano, T., Peng, W., Wang, F., Thrane, V. R., Enger, R., Haj-Yasein, N. N., Skare, Ø., Holen, T., Klungland, A., Ottersen, O. P., Nedergaard, M., and Nagelhus, E. A. (2011) Critical role of aquaporin-4 (AQP4) in astrocytic Ca2+signaling events elicited by cerebral edema. Proc. Natl. Acad. Sci. U.S.A. 108, 846-851
10. Huang, C. G., Lamitina, T., Agre, P., and Strange, K. (2007) Functional analysis of the aquaporin gene family in Caenorhabditis elegans. Am. J. Physiol. Cell Physiol. 292, C1867-1873 (Pubitemid 47080543)
11. Luyten, K., Albertyn, J., Skibbe, W. F., Prior, B. A., Ramos, J., Thevelein, J. M., and Hohmann, S. (1995) Fps1, a yeast member of the MIP family of channel proteins, is a facilitator for glycerol uptake and efflux and is inactive under osmotic stress. EMBO J. 14, 1360-1371
12. Zeuthen, T., Wu, B., Pavlovic-Djuranovic, S., Holm, L. M., Uzcategui, N. L., Duszenko, M., Kun, J. F., Schultz, J. E., and Beitz, E. (2006) Ammonia permeability of the aquaglyceroporins from Plasmodium falciparum, Toxoplasma gondii and Trypansoma brucei. Mol. Microbiol. 61, 1598-1608 (Pubitemid 44359386)
13. Wu, B., Song, J., and Beitz, E. (2010) Novel channel enzyme fusion proteins confer arsenate resistance. J. Biol. Chem. 285, 40081-40087
14. Saadoun, S., Papadopoulos, M. C., Hara-Chikuma, M., and Verkman, A. S. (2005) Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434, 786-792 (Pubitemid 44739524)
15. Langridge, P. D., and Kay, R. R. (2006) Blebbing of Dictyostelium cells in response to chemoattractant. Exp. Cell Res. 312, 2009-2017 (Pubitemid 43850926)
16. Annesley, S. J., and Fisher, P. R. (2009) Dictyostelium discoideum. A model for many reasons. Mol. Cell Biochem. 329, 73-91
17. Raper, K. B. (1950) Stalk formation in Dictyostelium. Science 112, 450
18. Mitra, B. N., Yoshino, R., Morio, T., Yokoyama, M., Maeda, M., Urushihara, H., and Tanaka, Y. (2000) Loss of a member of the aquaporin gene family, aqpA affects spore dormancy in Dictyostelium. Gene 251, 131-139 (Pubitemid 30394264)
19. Flick, K. M., Shaulsky, G., and Loomis, W. F. (1997) The wacA gene of Dictyostelium discoideum is a developmentally regulated member of the MIP family. Gene 195, 127-130 (Pubitemid 27354688)
20. Watts, D. J., and Ashworth, J. M. (1970) Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem. J. 119, 171-174
21. Hansen, M., Kun, J. F., Schultz, J. E., and Beitz, E. (2002) A single, bifunctional aquaglyceroporin in blood-stage Plasmodium falciparum malaria parasites. J. Biol. Chem. 277, 4874-4882 (Pubitemid 34968523)
22. Klammt, C., Löhr, F., Schäfer, B., Haase, W., Dötsch, V., Rüterjans, H., Glaubitz, C., and Bernhard, F. (2004) High level cell-free expression and specific labeling of integral membrane proteins. Eur. J. Biochem. 271, 568-580 (Pubitemid 38183631)
23. Klammt, C., Schwarz, D., Fendler, K., Haase, W., Dötsch, V., and Bernhard, F. (2005) Evaluation of detergents for the soluble expression of α-helical and β-barrel-type integral membrane proteins by a preparative scale individual cell-free expression system. FEBS J. 272, 6024-6038 (Pubitemid 41713694)
24. Schneider, B., Junge, F., Shirokov, V. A., Durst, F., Schwarz, D., Dötsch, V., and Bernhard, F. (2010) Membrane protein expression in cell-free systems. Methods Mol. Biol. 601, 165-186
25. Zeidel, M. L., Nielsen, S., Smith, B. L., Ambudkar, S. V., Maunsbach, A. B., and Agre, P. (1994) Ultrastructure, pharmacologic inhibition, and transport selectivity of aquaporin channel-forming integral protein in proteoliposomes. Biochemistry 33, 1606-1615 (Pubitemid 24093712)
26. Kai, L., Kaldenhoff, R., Lian, J., Zhu, X., Dötsch, V., Bernhard, F., Cen, P., and Xu, Z. (2010) Preparative scale production of functional mouse aquaporin 4 using different cell-free expression modes. PLoS ONE 5, e12972
27. Grimbleby, F. H., and Ntailianas, H. A. (1961) Binding of trichloroacetic acid by protein. Nature 189, 835-836
28. Eichinger, L., Pachebat, J. A., Glöckner, G., Rajandream, M. A., Sucgang, R., Berriman, M., Song, J., Olsen, R., Szafranski, K., Xu, Q., Tunggal, B., Kummerfeld, S., Madera, M., Konfortov, B. A., Rivero, F., Bankier, A. T., Lehmann, R., Hamlin, N., Davies, R., Gaudet, P., Fey, P., Pilcher, K., Chen, G., Saunders, D., Sodergren, E., Davis, P., Kerhornou, A., Nie, X., Hall, N., Anjard, C., Hemphill, L., Bason, N., Farbrother, P., Desany, B., Just, E., Morio, T., Rost, R., Churcher, C., Cooper, J., Haydock, S., van Driessche, N., Cronin, A., Goodhead, I., Muzny, D., Mourier, T., Pain, A., Lu, M., Harper, D., Lindsay, R., Hauser, H., James, K., Quiles, M., Madan Babu, M., Saito, T., Buchrieser, C., Wardroper, A., Felder, M., Thangavelu, M., Johnson, D., Knights, A., Loulseged, H., Mungall, K., Oliver, K., Price, C., Quail, M. A., Urushihara, H., Hernandez, J., Rabbinowitsch, E., Steffen, D., Sanders, M., Ma, J., Kohara, Y., Sharp, S., Simmonds, M., Spiegler, S., Tivey, A., Sugano, S., White, B., Walker, D., Woodward, J., Winckler, T., Tanaka, Y., Shaulsky, G., Schleicher, M., Weinstock, G., Rosenthal, A., Cox, E. C., Chisholm, R. L., Gibbs, R., Loomis, W. F., Platzer, M., Kay, R. R., Williams, J., Dear, P. H., Noegel, A. A., Barrell, B., and Kuspa, A. (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435, 43-57 (Pubitemid 40655903)
29. Liu, L. H., Ludewig, U., Gassert, B., Frommer, W. B., and von Wirén, N. (2003) Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis. Plant Physiol. 133, 1220-1228 (Pubitemid 37458020)
30. Sui, H., Han, B. G., Lee, J. K., Walian, P., and Jap, B. K. (2001) Structural basis of water-specific transport through the AQP1 water channel. Nature 414, 872-878 (Pubitemid 34024731)
31. 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 (Pubitemid 43237610)
32. Gupta, R., Jung, E., Gooley, A. A., Williams, K. L., Brunak, S., and Hansen, J. (1999) Scanning the available Dictyostelium discoideum proteome for O-linked GlcNAc glycosylation sites using neural networks. Glycobiology 9, 1009-1022 (Pubitemid 29473958)
33. Yasui, M., Hazama, A., Kwon, T. H., Nielsen, S., Guggino, W. B., and Agre, P. (1999) Rapid gating and anion permeability of an intracellular aquaporin. Nature 402, 184-187
34. Beitz, E., Pavlovic-Djuranovic, S., Yasui, M., Agre, P., and Schultz, J. E. (2004) Molecular dissection of water and glycerol permeability of the aquaglyceroporin from Plasmodium falciparum by mutational analysis. Proc. Natl. Acad. Sci. U.S.A. 101, 1153-1158 (Pubitemid 38182658)
35. Haynes, P. A. (1998) Phosphoglycosylation. A new structural class of glycosylation? Glycobiology 8, 1-5
36. Uzcategui, N. L., Szallies, A., Pavlovic-Djuranovic, S., Palmada, M., Figarella, K., Boehmer, C., Lang, F., Beitz, E., and Duszenko, M. (2004) Cloning, heterologous expression, and characterization of three aquaglyceroporins from Trypanosoma brucei. J. Biol. Chem. 279, 42669-42676 (Pubitemid 39372152)
37. Beitz, E. (2005) Aquaporins from pathogenic protozoan parasites. Structure, function and potential for chemotherapy. Biol. Cell 97, 373-383
38. Bapteste, E., Brinkmann, H., Lee, J. A., Moore, D. V., Sensen, C. W., Gordon, P., Duruflé, L., Gaasterland, T., Lopez, P., Müller, M., and Philippe, H. (2002) The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba. Proc. Natl. Acad. Sci. U.S.A. 99, 1414-1419 (Pubitemid 34136507)
39. Tamás, M. J., Karlgren, S., Bill, R. M., Hedfalk, K., Allegri, L., Ferreira, M., Thevelein, J. M., Rydström, J., Mullins, J. G., and Hohmann, S. (2003) A short regulatory domain restricts glycerol transport through yeast Fps1p. J. Biol. Chem. 278, 6337-6345 (Pubitemid 36800892)
40. Fischer, G., Kosinska-Eriksson, U., Aponte-Santamaría, C., Palmgren, M., Geijer, C., Hedfalk, K., Hohmann, S., de Groot, B. L., Neutze, R., and Lindkvist-Petersson, K. (2009) Crystal structure of a yeast aquaporin at 1.15 ångstrom reveals a novel gating mechanism. PLoS Biol. 7, e1000130
41. Marchesini, N., Ruiz, F. A., Vieira, M., and Docampo, R. (2002) Acidocalcisomes are functionally linked to the contractile vacuole of Dictyostelium discoideum. J. Biol. Chem. 277, 8146-8153 (Pubitemid 34968269)
42. Nishihara, E., Yokota, E., Tazaki, A., Orii, H., Katsuhara, M., Kataoka, K., Igarashi, H., Moriyama, Y., Shimmen, T., and Sonobe, S. (2008) Presence of aquaporin and V-ATPase on the contractile vacuole of Amoeba proteus. Biol. Cell 100, 179-188 (Pubitemid 351372676)
43. Montalvetti, A., Rohloff, P., and Docampo, R. (2004) A functional aquaporin co-localizes with the vacuolar proton pyrophosphatase to acidocalcisomes and the contractile vacuole complex of Trypanosoma cruzi. J. Biol. Chem. 279, 38673-38682 (Pubitemid 39296024)
44. Zhang, Z., Chen, Z., Song, Y., Zhang, P., Hu, J., and Bai, C. (2010) Expression of aquaporin 5 increases proliferation and metastasis potential of lung cancer. J. Pathol. 221, 210-220
45. Habermann, B. (2004) The BAR-domain family of proteins: a case of bending and binding? EMBO Rep. 5, 250-255
46. Beitz, E. (2000) T(E)Xtopo. Shaded membrane protein topology plots in LAT(E)X2epsilon. Bioinformatics 16, 1050-1051