Nutrient transport and pathogenesis in selected parasitic protozoa

Eukaryotic Cell

Volumn 10, Issue 4, 2011, Pages 483-493

  Landfear, Scott M ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBOXYLIC ACID; CARRIER PROTEIN; IRON; POLYAMINE; PURINE DERIVATIVE;

ANIMAL; ARTICLE; GENETICS; HUMAN; LEISHMANIA; METABOLISM; PARASITE; PATHOGENICITY; PHYSIOLOGY; PLASMODIUM; TOXOPLASMA; TRANSPORT AT THE CELLULAR LEVEL; TRYPANOSOMA;

AMINO ACIDS; ANIMALS; BIOLOGICAL TRANSPORT; CARBOXYLIC ACIDS; CARRIER PROTEINS; HUMANS; IRON; LEISHMANIA; PARASITES; PLASMODIUM; POLYAMINES; PURINES; TOXOPLASMA; TRYPANOSOMA;

PROTOZOA;

EID: 79955430195     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00287-10     Document Type: Article

References (107)

1. Akerman, M., P. Shaked-Mishan, S. Mazareb, H. Volpin, and D. Zilber-stein. 2004. Novel motifs in amino acid permease genes from Leishmania. Biochem. Biophys. Res. Commun. 325:353-366.
2. Antoine, J. C., E. Prina, C. Jouanne, and P. Bongrand. 1990. Parasito-phorous vacuoles of Leishmania amazonensis-infected macrophages maintain an acidic pH. Infect. Immun. 58:779-787.
3. Arastu-Kapur, S., C. S. Arendt, T. Purnat, N. S. Carter, and B. Ullman. 2005. Second-site suppression of a nonfunctional mutation within the Leish-mania donovani inosine-guanosine transporter. J. Biol. Chem. 280:2213-2219.
4. Arastu-Kapur, S., E. Ford, B. Ullman, and N. S. Carter. 2003. Functional analysis of an inosine-guanosine transporter from Leishmania donovani: the role of conserved residues, aspartate 389 and arginine 393. J. Biol. Chem. 278:33327-33333.
5. Arendt, C. S., and B. Ullman. 2010. Role of transmembrane domain 4 in ligand permeation by Crithidia fasciculata equilibrative nucleoside transporter 2 (CfNT2). J. Biol. Chem. 285:6024-6035.
6. Aslett, M., C. Aurrecoechea, M. Berriman, J. Brestelli, B. P. Brunk, M. Carrington, D. P. Depledge, S. Fischer, B. Gajria, X. Gao, M. J. Gardner, A. Gingle, G. Grant, O. S. Harb, M. Heiges, C. Hertz-Fowler, R. Houston, F. Innamorato, J. Iodice, J. C. Kissinger, E. Kraemer, W. Li, F. J. Logan, J. A. Miller, S. Mitra, P. J. Myler, V. Nayak, C. Pennington, I. Phan, D. F. Pinney, G. Ramasamy, M. B. Rogers, D. S. Roos, C. Ross, D. Sivam, D. F. Smith, G. Srinivasamoorthy, C. J. Stoeckert, Jr. S. Subramanian, R. Thi-bodeau, A. Tivey, C. Treatman, G. Velarde, and H. Wang. 2010. TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res. 38:D457-D462.
7. Azema, L., et al. 2004. Interaction of substituted hexose analogues with the Trypanosoma brucei hexose transporter. Biochem. Pharmacol. 67:459-467.
8. Bakker, B. M., H. V. Westerhoff, F. R. Opperdoes, and P. A. Michels. 2000. Metabolic control analysis of glycolysis in trypanosomes as an approach to improve selectivity and effectiveness of drugs. Mol. Biochem. Parasitol. 106:1-10.
9. Baldwin, S. A., G. A. McConkey, C. E. Cass, and J. D. Young. 2007. Nucleoside transport as a potential target for chemotherapy in malaria. Curr. Pharm. Des. 13:569-580.
10. Barrett, M. P., E. Tetaud, A. Seyfang, F. Brignaud, and T. Baltz. 1998. Trypanosome glucose transporters. Mol. Biochem. Parasitol. 91:195-205.
11. Bayele, H. K. 2001. Triazinyl derivatives that are potent inhibitors of glucose transport in Trypanosoma brucei. Parasitol. Res. 87:911-914.
12. Beitz, E., S. Pavlovic-Djuranovic, M. Yasui, P. Agre, and J. E. Schultz. 2004. Molecular dissection of water and glycerol permeability of the aquaglyc-eroporin from Plasmodium falciparum by mutational analysis. Proc. Natl. Acad. Sci. U. S. A. 101:1153-1158.
13. Blume, M., et al. 2009. Host-derived glucose and its transporter in the obligate intracellular pathogen Toxoplasma gondii are dispensable by glu-taminolysis. Proc. Natl. Acad. Sci. U. S. A. 106:12998-13003.
14. Blume, M., et al. 17 December 2010, posting date. A constitutive pan-hexose permease for the Plasmodium life cycle and transgenic models for screening of antimalarial sugar analogs. FASEB J. doi:10.1096/fj.10-173278.
15. Bringaud, F., and T. Baltz. 1993. Differential regulation of two distinct families of glucose transporter genes in Trypanosoma brucei. Mol. Cell. Biol. 13:1146-1154.
16. Burchmore, R. J., and M. P. Barrett. 2001. Life in vacuoles-nutrient acquisition by Leishmania amastigotes. Int. J. Parasitol. 31:1311-1320.
17. Burchmore, R. J. S., and S. M. Landfear. 1998. Differential regulation of multiple glucose transporter genes in the parasitic protozoan Leishmania mexicana. J. Biol. Chem. 273:29118-29126.
18. Burchmore, R. J. S., et al. 2003. Genetic characterization of glucose transporter function in Leishmania mexicana. Proc. Natl. Acad. Sci. U. S. A. 100:3901-3906.
19. Burri, C., and R. Brun. 2003. Eflornithine for the treatment of human African trypanosomiasis. Parasitol. Res. 90(Supp. 1):S49-S52.
20. Capul, A. A., S. Hickerson, T. Barron, S. J. Turco, and S. M. Beverley. 2007. Comparisons of mutants lacking the Golgi UDP-galactose or GDP-man-nose transporters establish that phosphoglycans are important for promas-tigote but not amastigote virulence in Leishmania major. Infect. Immun. 75:4629-4637.
21. Carter, N. S., et al. 2000. Isolation and functional characterization of the PfNT1 nucleoside transporter gene from Plasmodium falciparum. J. Biol. Chem. 275:10683-10691.
22. Carter, N. S., B. J. Berger, and A. H. Fairlamb. 1995. Uptake of diamidine drugs by the P2 transporter in melarsen-sensitive and -resistant Trypano-soma brucei brucei. J. Biol. Chem. 270:28153-28157.
23. Carter, N. S., et al. 2000. Cloning of a novel inosine-guanosine transporter gene from Leishmania donovani by functional rescue of a transport-deficient mutant. J. Biol. Chem. 275:20935-20941.
24. Carter, N. S., and A. H. Fairlamb. 1993. Arsenical-resistant trypanosomes lack an unusual adenine/adenosine transporter. Nature 361:173-175.
25. Carter, N. S., et al. 2010. Adaptive responses to purine starvation in Leish-mania donovani. Mol. Microbiol. 78:92-107.
26. Cunningham, M. L., and S. M. Beverley. 2001. Pteridine salvage throughout the Leishmania infectious cycle: implications for antifolate chemotherapy. Mol. Biochem. Parasitol. 113:199-213.
27. Daily, J. P., et al. 2005. In vivo transcriptome of Plasmodium falciparum reveals overexpression of transcripts that encode surface proteins. J. Infect. Dis. 191:1196-1203.
28. Darlyuk, I., et al. 2009. Arginine homeostasis and transport in the human pathogen Leishmania donovani. J. Biol. Chem. 284:19800-19807.
29. Dean, S., R. Marchetti, K. Kirk, and K. R. Matthews. 2009. A surface transporter family conveys the trypanosome differentiation signal. Nature 459:213-217.
30. de Koning, H. P., D. J. Bridges, and R. J. Burchmore. 2005. Purine and pyrimidine transport in pathogenic protozoa: from biology to therapy. FEMS Microbiol. Rev. 29:987-1020.
31. Desai, S. A., S. M. Bezrukov, and J. Zimmerberg. 2000. A voltage-dependent channel involved in nutrient uptake by red blood cells infected with the malaria parasite. Nature 406:1001-1005.
32. Desai, S. A., D. J. Krogstad, and E. W. McCleskey. 1993. A nutrient-permeable channel on the intraerythrocytic malaria parasite. Nature 362: 643-646.
33. Detke, S. 1997. Identification of a transcription factor like protein at the TOR locus in Leishmania mexicana amazonensis. Mol. Biochem. Parasitol. 90:505-511.
34. Detke, S. 2007. TOR-induced resistance to toxic adenosine analogs in Leishmania brought about by the internalization and degradation of the adenosine permease. Exp. Cell Res. 313:1963-1978.
35. Downie, M. J., et al. 2010. PfNT2, a permease of the equilibrative nucleo-side transporter family in the endoplasmic reticulum of Plasmodium falcip-arum. J. Biol. Chem. 285:20827-20833.
36. + sym-porter from Leishmania donovani. Mol. Cell. Biol. 15:5508-5515.
37. El Bissati, K., et al. 2006. The plasma membrane permease PfNT1 is essential for purine salvage in the human malaria parasite Plasmodium falciparum. Proc. Natl. Acad. Sci. U. S. A. 103:9286-9291.
38. Feng, X., et al. 2009. Amplification of an alternate transporter gene suppresses the avirulent phenotype of glucose transporter null mutants in Leishmania mexicana. Mol. Microbiol. 71:369-381.
39. Fortier, A., G. Min-Oo, J. Forbes, S. Lam-Yuk-Tseung, and P. Gros. 2005. Single gene effects in mouse models of host:pathogen interactions. J. Leu-koc. Biol. 77:868-877.
40. Gardner, M. J., et al. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511.
41. Gottlieb, M. 1985. Enzyme regulation in a trypanosomatid: effect of purine starvation on levels of 3'-nucleotidase activity. Science 227:72-74.
42. Gourbal, B., et al. 2004. Drug uptake and modulation of drug resistance in Leishmania by an aquaglyceroporin. J. Biol. Chem. 279:31010-31017.
43. Griffiths, M., et al. 1997. Cloning of a human nucleoside transporter implicated in the cellular uptake of adenosine and chemotherapeutic drugs. Nat. Med. 3:89-93.
44. Hammond, D. J., and W. E. Gutteridge. 1984. Purine and pyrimidine metabolism in the Trypanosomatidae. Mol. Biochem. Parasitol. 13:243-261.
45. Hasne, M. P., I. Coppens, R. Soysa, and B. Ullman. 2010. A high-affinity putrescine-cadaverine transporter from Trypanosoma cruzi. Mol. Microbiol. 76:78-91.
46. Hasne, M. P., and B. Ullman. 2005. Identification and characterization of a polyamine permease from the protozoan parasite Leishmania major. J. Biol. Chem. 280:15188-15194.
47. Heby, O., S. C. Roberts, and B. Ullman. 2003. Polyamine biosynthetic enzymes as drug targets in parasitic protozoa. Biochem. Soc. Trans. 31:415-419.
48. Huynh, C, and N. W. Andrews. 2008. Iron acquisition within host cells and the pathogenicity of Leishmania. Cell Microbiol. 10:293-300.
49. Huynh, C, D. L. Sacks, and N. W. Andrews. 2006. A Leishmania ama-zonensis ZIP family iron transporter is essential for parasite replication within macrophage phagolysosomes. J. Exp. Med. 203:2363-2375.
50. Igoillo-Esteve, M., M. Mazet, G. Deumer, P. Wallemacq, and P. A. Michels. 2011. Glycosomal ABC transporters of Trypanosoma brucei: characterization of their expression, topology and substrate specificity. Int. J. Parasitol. 41:429-438.
51. Inbar, E., et al. Lysine transporters in human trypanosomatid pathogens. Amino Acids, in press.
52. Jacques, I., N. W. Andrews, and C. Huynh. 2010. Functional characterization of LIT1, the Leishmania amazonensis ferrous iron transporter. Mol. Biochem. Parasitol. 170:28-36.
53. Joet, T., U. Eckstein-Ludwig, C. Morin, and S. Krishna. 2003. Validation of the hexose transporter of Plasmodium falciparum as a novel drug target. Proc. Natl. Acad. Sci. U. S. A. 100:7476-7479.
54. Kerby, D. R., and S. Detke. 1993. Reduced purine accumulation is encoded on an amplified DNA in Leishmania mexicana amazonensis resistant to toxic nucleosides. Mol. Biochem. Parasitol. 60:171-185.
55. Kirk, K., and K. J. Saliba. 2007. Targeting nutrient uptake mechanisms in Plasmodium. Curr. Drug Targets 8:75-88.
56. Landfear, S. M. 2010. Glucose transporters in parasitic protozoa. Methods Mol. Biol. 637:245-262.
57. Landfear, S. M., B. Ullman, N. Carter, and M. Sanchez. 2004. Nucleoside and nucleobase transporters in parasitic protozoa. Eukaryot. Cell 3:245-254.
58. Ligtenberg, M. J. L., et al. 1994. Reconstitution of a surface transferrin binding complex in insect form Trypanosoma brucei. EMBO J. 13:2565-2573.
59. Liu, W., et al. 2006. Functional characterization of nucleoside transporter gene replacements in Leishmania donovani. Mol. Biochem. Parasitol. 150: 300-307.
60. +2 pool content and signaling and expression of a calcium pump are linked to virulence in Leishmania mexicana amazonensis amastigotes. J. Biol. Chem. 272:9464-9473.
61. Luo, S., M. Vieira, J. Graves, L. Zhong, and S. N. Moreno. 2001. A plasma membrane-type Ca(2+)-ATPase co-localizes with a vacuolar H(+)-pyro-phosphatase to acidocalcisomes of Toxoplasma gondii. EMBO J. 20:55-64.
62. Marchesini, N., M. Vieira, S. Luo, S. N. Moreno, and R. Docampo. 2005. A malaria parasite-encoded vacuolar H(+)-ATPase is targeted to the host erythrocyte. J. Biol. Chem. 280:36841-36847.
63. Maser, P., C. Sutterlin, A. Kralli, and R. Kaminsky. 1999. A nucleoside transporter from Trypanosoma brucei involved in drug resistance. Science 285:242-244.
64. Matovu, E., et al. 2001. Genetic variants of the TbAT1 adenosine transporter from African trypanosomes in relapse infections following melar-soprol therapy. Mol. Biochem. Parasitol. 117:73-81.
65. Matovu, E., et al. 2003. Mechanisms of arsenical and diamidine uptake and resistance in Trypanosoma brucei. Eukaryot. Cell 2:1003-1008.
66. McConville, M. J., D. de Souza, E. Saunders, V. A. Likic, and T. Naderer. 2007. Living in a phagolysosome; metabolism of Leishmania amastigotes. Trends Parasitol. 23:368-375.
67. Meade, J. C., G. H. Coombs, J. C. Mottram, P. E. Steele, and J. R. Stringer. 1991. Conservation of cation-transporting ATPase genes in Leishmania. Mol. Biochem. Parasitol. 45:29-38.
68. Montalvetti, A., P. Rohloff, and R. Docampo. 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.
69. Mullin, K. A., et al. 2006. Membrane transporters in the relict plastid of malaria parasites. Proc. Natl. Acad. Sci. U. S. A. 103:9572-9577.
70. Naderer, T., and M. J. McConville. 2008. The Leishmania-macrophage interaction: a metabolic perspective. Cell Microbiol. 10:301-308.
71. Nasser, M. I. A., and S. M. Landfear. 2004. Sequences required for the flagellar targeting of an integral membrane protein. Mol. Biochem. Para-sitol. 135:89-100.
72. Naula, C. M., F. J. Logan, P. E. Wong, M. P. Barrett, and R. J. Burchmore. 2010. A glucose transporter can mediate ribose uptake: definition of residues that confer substrate specificity in a sugar transporter. J. Biol. Chem. 285:29721-29728.
73. Opperdoes, F. R., and G. H. Coombs. 2007. Metabolism of Leishmania: proven and predicted. Trends Parasitol. 23:149-158.
74. Ortiz, D., M. A. Sanchez, H. P. Koch, H. P. Larsson, and S. M. Landfear. 2009. An acid-activated nucleobase transporter from Leishmania major. J. Biol. Chem. 284:16164-16169.
75. Ortiz, D., et al. 2007. Molecular genetic analysis of purine nucleobase transport in Leishmania major. Mol. Microbiol. 64:1228-1243.
76. Ortiz, D., M. A. Sanchez, P. Quecke, and S. M. Landfear. 2009. Two novel nucleobase/pentamidine transporters from Trypanosoma brucei. Mol. Biochem. Parasitol. 163:67-76.
77. Ortiz, D., et al. 2010. Purine restriction induces pronounced translational upregulation of the NT1 adenosine/pyrimidine nucleoside transporter in Leishmania major. Mol. Microbiol. 78:108-118.
78. Ouameur, A. A., I. Girard, D. Legare, and M. Ouellette. 2008. Functional analysis and complex gene rearrangements of the folate/biopterin transporter (FBT) gene family in the protozoan parasite Leishmania. Mol. Biochem. Parasitol. 162:155-164.
79. Papageorgiou, I., H. P. De Koning, K. Soteriadou, and G. Diallinas. 2008. Kinetic and mutational analysis of the Trypanosoma brucei NBT1 nucleo-base transporter expressed in Saccharomyces cerevisiae reveals structural similarities between ENT and MFS transporters. Int. J. Parasitol. 38:641-653.
80. Parker, M. D., et al. 2000. Identification of a nucleoside/nucleobase transporter from Plasmodium falciparum, a novel target for anti-malarial chemotherapy. Biochem. J. 349:67-75.
81. Perez-Victoria, J. M., et al. 2001. Alkyl-lysophospholipid resistance in mul-tidrug-resistant Leishmania tropica and chemosensitization by a novel P-glycoprotein-like transporter modulator. Antimicrob. Agents Chemother. 45:2468-2474.
82. Piper, R. C., X. Xu, D. G. Russell, B. M. Little, and S. M. Landfear. 1995. Differential targeting of two glucose transporters from Leishmania enriettii is mediated by an NH2-terminal domain. J. Cell Biol. 128:499-508.
83. Quashie, N. B., et al. 2008. A comprehensive model of purine uptake by the malaria parasite Plasmodium falciparum: identification of four purine transport activities in intraerythrocytic parasites. Biochem. J. 411:287-295.
84. Rager, N., C. Ben Mamoun, N. S. Carter, D. E. Goldberg, and B. Ullman. 2001. Localization of the Plasmodium falciparum PfNT1 nucleoside transporter to the parasite plasma membrane. J. Biol. Chem. 276:41095-41099.
85. Revelard, P., and E. Pays. 1991. Structure and transcription of a P-ATPase gene from Trypanosoma brucei. Mol. Biochem. Parasitol. 46:241-252.
86. Roberts, S. C., et al. 2004. Arginase plays a pivotal role in polyamine precursor metabolism in Leishmania. Characterization of gene deletion mutants. J. Biol. Chem. 279:23668-23678.
87. Rodriguez-Contreras, D., X. Feng, K. M. Keeney, H. G. Bouwer, and S. M. Landfear. 2007. Phenotypic characterization of a glucose transporter null mutant in Leishmania mexicana. Mol. Biochem. Parasitol. 153:9-18.
88. Rodriguez-Contreras, D., and S. M. Landfear. 2006. Metabolic changes in glucose transporter-deficient Leishmania mexicana and parasite virulence. J. Biol. Chem. 281:20068-20076.
89. Russell, D. G., S. Xu, and P. Chakraborty. 1992. Intracellular trafficking and the parasitorphorous vacuole of Leishmania mexicana-infected macro-phages. J. Cell Sci. 103:1193-1210.
90. Saliba, K. J., et al. 2006. Sodium-dependent uptake of inorganic phosphate by the intracellular malaria parasite. Nature 443:582-585.
91. Schlein, Y. 1986. Sandfly diet and Leishmania. Parasitol. Today 2:175-177.
92. Shaked-Mishan, P., et al. 2006. A novel high-affinity arginine transporter from the human parasitic protozoan Leishmania donovani. Mol. Microbiol. 60:30-38.
93. Slavic, K., et al. 2010. Life cycle studies of the hexose transporter of Plasmodium species and genetic validation of their essentiality. Mol. Mi-crobiol. 75:1402-1413.
94. Stein, A., et al. 2003. Equilibrative nucleoside transporter family members from Leishmania donovani are electrogenic proton symporters. J. Biol. Chem. 278:35127-35134.
95. ter Kuile, B. H. 1993. Glucose and proline transport in kinetoplastids. Parasitol. Today 9:206-210.
96. ter Kuile, B. H. 1991. Glucose uptake mechanisms as potential targets for drugs against trypanosomatids, p. 635. In G. H. Coombs and M. North (ed.), Biochemical protozoology. Taylor and Francis, London, United Kingdom.
97. Tetaud, E., M. P. Barrett, F. Bringaud, and T. Baltz. 1997. Kinetoplastid glucose transporters. Biochem. J. 325:569-580.
98. Tetaud, E., F. Bringaud, S. Chabas, M. P. Barrett, and T. Baltz. 1994. Characterization of glucose transport and cloning of a hexose transporter gene in Trypanosoma cruzi. Proc. Natl. Acad. Sci. U. S. A. 91:8278-8282.
99. Uzcategui, N. L., et al. 2004. Cloning, heterologous expression, and characterization of three aquaglyceroporins from Trypanosoma brucei. J. Biol. Chem. 279:42669-42676.
100. Valdes, R., W. Liu, B. Ullman, and S. M. Landfear. 2006. Comprehensive examination of charged intramembrane residues in a nucleoside transporter. J. Biol. Chem. 281:22647-22655.
101. Valdes, R., G. Vasudevan, D. Conklin, and S. M. Landfear. 2004. Transmembrane domain 5 of the LdNT1.1 nucleoside transporter is an amphi-pathic helix that forms part of the nucleoside translocation pathway. Biochemistry 43:6793-6802.
102. Valdes, R. M., S. A. Arastu-Kapur, S. M. Landfear, and U. Shinde. 2009. An ab initio structural model of a nucleoside permease predicts functionally important residues. J. Biol. Chem. 284:19067-19076.
103. Vasudevan, G., et al. 1998. Cloning of Leishmania nucleoside transporter genes by rescue of a transport-deficient mutant. Proc. Natl. Acad. Sci. U. S. A. 95:9873-9878.
104. Vasudevan, G., B. Ullman, and S. M. Landfear. 2001. Point mutations in a nucleoside transporter gene from Leishmania donovani confer drug resistance and alter substrate selectivity. Proc. Natl. Acad. Sci. U. S. A. 98:6092-6097.
105. Vickerman, K. 1985. Developmental cycles and biology of pathogenic try-panosomes. Br. Med. Bull. 41:105-114.
106. Wilson, M. E., T. S. Lewis, M. A. Miller, M. L. McCormick, and B. E. Britigan. 2002. Leishmania chagasi: uptake of iron bound to lactoferrin or transferrin requires an iron reductase. Exp. Parasitol. 100:196-207.
107. Woodrow, C. J., J. I. Penny, and S. Krishna. 1999. Intraerythrocytic Plas-modium falciparum expresses a high affinity facilitative hexose transporter. J. Biol. Chem. 274:7272-7277.