Ammonia permeability of the aquaglyceroporins from Plasmodium falciparum, Toxoplasma gondii and Trypansoma brucei

Molecular Microbiology

Volumn 61, Issue 6, 2006, Pages 1598-1608

  Zeuthen, Thomas ^a   Wu, Binghua ^b   Pavlovic Djuranovic, Slavica ^b   Holm, Lars M ^a   Uzcategui, Nestor L ^b   Duszenko, Michael ^b   Kun, Jürgen F J ^b   Schultz, Joachim E ^b   Beitz, Eric ^b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETAMIDE; AMMONIA; AQUAGLYCEROPORIN; AQUAPORIN; FORMAMIDE; METHYLAMINE;

ACIDIFICATION; ARTICLE; CLAMP; EFFUSION; ERYTHROCYTE; IC 50; OOCYTE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; RADIOACTIVITY; TOXOPLASMA GONDII; WATER PERMEABILITY; YEAST;

AMMONIA; ANIMALS; AQUAGLYCEROPORINS; GENETIC COMPLEMENTATION TEST; MEMBRANE PROTEINS; METHYLAMINES; OOCYTES; PERMEABILITY; PLASMODIUM FALCIPARUM; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TOXOPLASMA; TRYPANOSOMA BRUCEI BRUCEI; XENOPUS LAEVIS;

PLASMODIUM FALCIPARUM; TOXOPLASMA GONDII; TRYPANOSOMA BRUCEI; XENOPUS LAEVIS;

EID: 33748490735     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05325.x     Document Type: Article

References (40)

1. Khademi, S., O'Connell, J., 3rd, Remis, J., Robles-Colmenares, Y., Miercke, L.J., and Stroud, R.M. (2004) Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 Å. Science 305: 1587-1594.
2. Beitz, E. (2005) Aquaporins from pathogenic protozoan parasites: structure, function and potential for chemotherapy. Biol Cell 97: 373-383.
3. 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 USA 101: 1153-1158.
4. 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 USA 103: 269-274.
5. Bergmeyer, H.U., and Beutler, H.O. (1990) Methods of Enzymatic Analysis: Ammonia, Vol. 8, 3rd edn. Cambridge, UK: VCH Publishers (UK).
6. Desai, S.A., Krogstad, D.J., and McCleskey, E.W. (1993) A nutrient-permeable channel on the intraerythrocytic malaria parasite. Nature 362: 463-466.
7. Elford, B.C., and Pinches, R.A. (1992) Inducible transport systems in the regulation of parasite growth in malaria-infected red blood cells. Biochem Soc Trans 20: 790-796.
8. Elford, B.C., Haynes, J.D., Chulay, J.D., and Wilson, R.J.M. (1985) Selective stage-specific changes in the permeability to small hydrophilic solutes of human erythrocytes infected with Plasmodium falciparum. Mol Biochem Parasitol 16: 43-60.
9. Garvin, J.L., Burg, M.B., and Knepper, M.A. (1985) Ammonium replaces potassium in supporting sodium transport by the Na-K-ATPase of renal proximal straight tubules. Am J Physiol 249: F785-F788.
10. Geary, T.G., Divo, A.A., Bonanni, L.C., and Jensen, J.B. (1985) Nutritional requirements of Plasmodium falciparum in culture. III. Further observations on essential nutrients and antimetabolites. J Protozool 32: 608-613.
11. Ginsburg, H. (2002) Abundant proton pumping in Plasmodium falciparum, but why? Trends Parasitol 18: 483-486.
12. Goldberg, D.E. (2005) Hemoglobin degradation. Curr Top Microbiol Immunol 295: 275-291.
13. Hansen, M., Kun, J.F.J., Schultz, J.E., and Beitz, E. (2002) A single, bi-functional aquaglyceroporin in blood-stage Plasmodium falciparum malaria parasites. J Biol Chem 277: 4874-4882.
14. +-ATPase localized in plasma membranes of malaria parasite cells, Plasmodium falciparum, is involved in regional acidification of parasitized erythrocytes. J Biol Chem 275: 34353-34358.
15. Hemker, M.B., Cheroutre, G., van Zwieten, R., Maaskant-van Wijk, P.A., Roos, D., Loos, J.A., et al. (2003) The Rh complex exports ammonium from human red blood cells. Br J Haematol 122: 333-140.
16. + permeability in aquaporin-expressing Xenopus oocytes. Pflüger's Arch 450: 415-428.
17. Jahn, T.P., Møller, A.L., Zeuthen, T., Holm, L.M., Klærke, D.A., Mohsin, B., et al. (2004) Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett 574: 31-36.
18. Krogstad, D.J., Schlesinger, P.H., and Gluzman, I.Y. (1985) Antimalarials increase vesicle pH in Plasmodium falciparum. J Cell Biol 101: 2302-2309.
19. Lambros, C., and Vanderberg, J.P. (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65: 418-420.
20. Loque, D., Ludewig, U., Yuan, L., and von Wiren, N. (2005) Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol 137: 671-680.
21. 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.
22. Marini, A.M., Vissers, S., Urrestarazu, A., and André, B. (1994) Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J 13: 3456-3463.
23. Marti, M., Baum, J., Rug, M., Tilley, L., and Cowman, A.F. (2005) Signal-mediated export of proteins from the malaria parasite to the host erythrocyte. J Cell Biol 171: 587-592.
24. Meinild, A.K., Klærke, D.A., and Zeuthen, T. (1998) Bidirectional water fluxes and specificity for small hydrophilic molecules in aquaporins 0-5. J Biol Chem 273: 32446-32451.
25. Müller, I.B., Walter, R.D., and Wrenger, C. (2005) Structural metal dependency of the arginase from the human malaria parasite Plasmodium falciparum. Biol Chem 386: 117-126.
26. Noedl, H., Wernsdorfer, W.H., Miller, R.S., and Wongsrichanalai, C. (2002) Histidine-rich protein II: a novel approach to malaria drug sensitivity testing. Antimicrob Agents Chemother 46: 1658-1664.
27. Pavlovic-Djuranovic, S., Schultz, J.E., and 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.
28. 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 (in press).
29. 3 into red blood cells. Proc Natl Acad Sci USA 101: 17222-17227.
30. Rosenthal, P.J. (2002) Hydrolysis of erythrocyte proteins by proteases of malaria parasites. Curr Opinion Hematol 9: 140-145.
31. 14C-amino acids by malarial plasmodia (Plasmodium iophurae). VI. Changes in the kinetic constants of amino acid transport during infection. Exp Parasitol 35: 369-373.
32. Träger, W., and Jensen, J.B. (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
33. Uzcategui, N.L., Szallies, A., Pavlovic-Djuranovic, S., Palmada, M., Figarella, K., Boehmer, C., et al. (2004) Cloning, heterologous expression and characterization of three aquaglyceroporins from Trypanosoma brucei. J Biol Chem 279: 42669-42676.
34. Wagner, J.T., Ludemann, H., Farber, P.M., Lottspeich, F., and Krauth-Siegel, R.L. (1998) Glutamate dehydrogenase, the marker protein of Plasmodium falciparum - cloning, expression and characterization of the malarial enzyme. Eur J Biochem 258: 813-819.
35. Werner, C., Stubbs, M.T., Krauth-Siegel, R.L., and Klebe, G. (2005) The crystal structure of Plasmodium falciparum glutamate dehydrogenase, a putative target for novel antimalarial drugs. J Mol Biol 349: 597-607.
36. Westhoff, C.M., Ferreri-Jacobia, M., Mak, D.O., and Foskett, J.K. (2002) Identification of the erythrocyte Rh blood group glycoprotein as a mammalian ammonium transporter. J Biol Chem 277: 12499-12502.
37. Yang, B., Zhao, D., Solenov, E., and Verkman, A.S. (2006) Evidence from knockout mice against physiologically significant aquaporin-8 facilitated ammonia transport. Am J Physiol Cell Physiol (in press).
38. Yayon, A., Cabantchik, Z.I., and Ginsburg, H. (1985) Susceptibility of human malaria parasites to chloroquine is pH dependent. Proc Natl Acad Sci USA 82: 2784-2788.
39. Zarchin, S., Krugliak, M., and Ginsburg, H. (1986) Digestion of the host erythrocyte by malaria parasites is the primary target for quinoline-containing antimalarials. Biochem Pharmacol 35: 2435-2442.
40. +-coupled sugar transporters (SGLT1). J Physiol 542: 71-87.