Plasmodium permeomics: Membrane transport proteins in the malaria parasite

Current Topics in Microbiology and Immunology

Volumn 295, Issue , 2005, Pages 325-356

  Kirk, Kiaran ^a   Martin, R E ^a   Broer S ^a   Howitt, S M ^a   Saliba, K J ^a,b  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b The Australian National University   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; XENOBIOTIC AGENT;

CELL FUNCTION; CELL MEMBRANE; CELL VACUOLE; CELLULAR DISTRIBUTION; ERYTHROCYTE; GENE MUTATION; GENOME; HOST CELL; MALARIA; MEMBRANE ELECTROPHYSIOLOGY; NONHUMAN; NUTRIENT UPTAKE; OOCYTE; PARASITE ISOLATION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; RNA INTERFERENCE; XENOPUS LAEVIS; YEAST;

PLASMODIUM FALCIPARUM; XENOPUS LAEVIS;

EID: 24144442901     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/3-540-29088-5_13     Document Type: Review

References (129)

1. Agre P, Preston GM, Smith BL, Jung JS, Raina S, Moon C, Guggino WB, Nielsen S (1993) Aquaporin CHIP: the archetypal molecular water channel. Am J Physiol 265:F463-F476
2. Alkhalil A, Cohn JV, Wagner MA, Cabrera JS, Rajapandi T, Desai SA (2004) Plasmodium falciparum likely encodes the principal anion channel on infected human erythrocytes. Blood 104:4279-4286
3. Allen RJW, Kirk K (2004) The membrane potential of the intraerythrocytic malaria parasite Plasmodium falciparum. J Biol Chem 279:11264-11272
4. Allen RJW, Kirk K (2004) Cell volume control in the Plasmodium-infected erythrocyte. Trends Parasitol 20:7-10
5. Alleva LM, Kirk K (2001) Calcium regulation in the intraerythrocytic malaria parasite Plasmodium falciparum. Mol Biochem Parasitol 117:121-128
6. Ansorge I, Benting J, Bhakdi S, Lingelbach K (1996) Protein sorting in Plasmodium falciparum-infected red blood cells permeabilized with the pore-forming protein streptolysin O. Biochem J 315:307-314
7. Ansorge I, Paprotka K, Bhakdi S, Lingelbach K (1997) Permeabilization of the erythrocyte membrane with streptolysin O allows access to the vacuolar membrane of Plasmodium falciparum and a molecular analysis of membrane topology. Mol Biochem Parasitol 84:259-261
8. Bhaduri-McIntosh S, Vaidya AB (1998) Plasmodium falciparum: import of a phosphate carrier protein into heterologous mitochondria. Exp Parasitol 88:252-254
9. 2+ store. J Biol Chem 278:27910J. Biol. Chem. 27915
10. Biagini GA, Pasini EM, Hughes RH, De Koning H, Vial HJ, O'Neill PM, Ward SA, Bray PG (2004) Characterization of the choline carrier of Plasmodium falciparum: a route for the selective delivery of novel antimalarial drugs. Blood 104:3372-3377
11. Bozdech Z, Llinas M, Pulliam BL, Wong ED, Zhu J, DeRisi JL (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 1:85-100
12. Bray PG, Saliba KJ, Davies JD, Spiller DG, White MR, Kirk K, Ward SA (2002) Distribution of acridine orange fluorescence in Plasmodium falciparum-infected erythrocytes and its implications for the evaluation of digestive vacuole pH. Mol Biochem Parasitol 119:301-304; discussion 307-309, 311-313
13. Caldas ML, Wasserman M (2001) Cytochemical localisation of calcium ATPase activity during the erythrocytic cell cycle of Plasmodium falciparum. Int J Parasitol 31:776-782
14. Carter NS, Ben Mamoun C, Liu W, Silva EO, Landfear, SM, Goldberg DE, Ullman B (2000) Isolation and functional characterization of the PfNT1 nucleoside transporter gene from Plasmodium falciparum. J Biol Chem 275:10683-10691
15. Cereghino GP, Cregg JM (1999) Applications of yeast in biotechnology: protein production and genetic analysis. Curr Opin Biotechnol 10:422-427
16. Choi I, Mikkelsen RB (1990) Plasmodium falciparum: ATP/ADP transport across the parasitophorous vacuolar and plasma membranes. Exp Parasitol 71:452-462
17. Clements JD, Martin RE (2002) Identification of novel membrane proteins by searching for patterns in hydropathy profiles. Eur J Biochem 269:2101-2107
18. Cooper RA, Ferdig MT, Su XZ, Ursos LM, Mu J, Nomura T, Fujioka H, Fidock DA, Roepe PD, Wellems TE (2002) Alternative mutations at position 76 of the vacuolar transmembrane protein PfCRT are associated with chloroquine resistance and unique stereospecific quinine and quinidine responses in Plasmodium falciparum. Mol Pharmacol 61:35-42
19. Cowman AF, Karcz S, Galatis D, Culvenor JG (1991) A P-glycoprotein homologue of Plasmodium falciparum is localized on the digestive vacuole. J Cell Biol 113:1033-1042
20. Cranmer SL, Conant AR, Gutteridge WE, Halestrap AP (1995) Characterization of the enhanced transport of L- and D-lactate into human red blood cells infected with Plasmodium falciparum suggests the presence of a novel saturable lactate proton cotransporter. J Biol Chem 270:15045-15052
21. Desai SA, Krogstad DJ, McCleskey EW (1993) A nutrient-permeable channel on the intraerythrocytic malaria parasite. Nature 362:643-646
22. Desai SA, Rosenberg RL (1997) Pore size of the malaria parasite's nutrient channel. Proc Natl Acad Sci USA 94:2045-2049
23. Desai SA, Bezrukov SM, Zimmerberg J (2000) A voltage-dependent channel involved in nutrient uptake by red blood cells infected with the malaria parasite. Nature 406:1001-1005
24. Divo AA, Geary TG, Davis NL, Jensen JB (1985) Nutritional requirements of Plasmodium falciparum in culture. I. Exogenously supplied dialyzable components necessary for continuous growth. J Protozool 32:59-64
25. Duraisingh MT, Triglia T, Cowman AF (2002) Negative selection of Plasmodium falciparum reveals targeted gene deletion by double crossover recombination. Int J Parasitol 32:81-89
26. --dependent cation conductance in human red blood cells. J Physiol 539:847-855
27. Duranton C, Huber S, Tanneur V, Lang K, Brand V, Sandu C, Lang F (2003) Electrophysiological properties of the Plasmodium falciparum-induced cation conductance of human erythrocytes. Cell Physiol Biochem 13:189-198
28. Duranton C, Huber SM, Tanneur V, Brand VB, Akkaya C, Shumilina EV, Sandu CD, Lang F (2004) Organic osmolyte permeabilities of the malaria-induced anion conductances in human erythrocytes. J Gen Physiol 123:417-426
29. Dyer M, Jackson M, McWhinney C, Zhao G, Mikkelsen R (1996) Analysis of a cation-transporting ATPase of Plasmodium falciparum. Mol Biochem Parasitol 78:1-12
30. Dzekunov SM, Ursos LM, Roepe PD (2000) Digestive vacuolar pH of intact intraerythrocytic P. falciparum either sensitive or resistant to chloroquine. Mol Biochem Parasitol 110:107-124
31. Eckstein-Ludwig U, Webb RJ, Van Goethem ID, East JM, Lee AG, Kimura M, O'Neill PM, Bray PG, Ward SA, Krishna S (2003) Artemisinins target the SERCA of Plasmodium falciparum. Nature 424:957-961
32. Egée S, Lapaix F, Decherf G, Staines HM, Ellory JC, Doerig C, Thomas SL (2002) A stretch-activated anion channel is up-regulated by the malaria parasite Plasmodium falciparum. J Physiol 542:795-801
33. El Tahir A, Malhotra P, Chauhan VS (2003) Uptake of proteins and degradation of human serum albumin by Plasmodium falciparum-infected human erythrocytes. Malaria J 2:11
34. + channel from the malaria parasite Plasmodium falciparum. Biochem Biophys Res Commun 318:477-484
35. Elliott JL, Saliba KJ, Kirk K (2001) Transport of lactate and pyruvate in the intraerythrocytic malaria parasite, Plasmodium falciparum. Biochem J 355:733-739
36. Fidock DA, Nomura T, Talley AK, Cooper RA, Dzekunov SM, Ferdig MT, Ursos LM, Sidhu AB, Naude B, Deitsch KW, Su XZ, Wootton JC, Roepe PD, Wellems, TE (2000) Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol Cell 6:861-871
37. Foote SJ, Thompson JK, Cowman AF, Kemp DJ (1989) Amplification of the multidrug resistance gene in some chloroquine-resistant isolates of P. falciparum. Cell 57:921-930
38. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511
39. Gazarini ML, Thomas AP, Pozzan T, Garcia CR (2003) Calcium signaling in a low calcium environment: how the intracellular malaria parasite solves the problem. J Cell Biol 161:103-110
40. Gero AM, Dunn CG, Brown DM, Pulenthiran K, Gorovits EL, Bakos T, Weis AL (2003) New malaria chemotherapy developed by utilization of a unique parasite transport system. Curr Pharm Des 9:867-877
41. Ginsburg H, Kutner S, Krugliak M, Cabantchik ZI (1985) Characterization of permeation pathways appearing in the host membrane of Plasmodium falciparum infected red blood cells. Mol Biochem Parasitol 14:313-322
42. Ginsburg H, Stein WD (2004) The new permeability pathways induced by the malaria parasite in the membrane of the infected erythrocyte: comparison of results using different experimental techniques. J Membr Biol 197:113-134
43. Goodyer ID, Hayes DJ, Eisenthal R (1997) Efflux of 6-deoxy-D-glucose from Plasmodium falciparum-infected erythrocytes via two saturable carriers. Mol Biochem Parasitol 84:229-239
44. Griffith DA, Delipala C, Leadsham J, Jarvis SM, Oesterhelt D (2003) A novel yeast expression system for the overproduction of quality-controlled membrane proteins. FEBS Lett 553:45-50
45. Hansen M, Kun JF, Schultz JE, Beitz E (2002) A single, bi-functional aquaglyceroporin in blood-stage Plasmodium falciparum malaria parasites. J Biol Chem 277:4874-4882
46. +-ATPase localized in plasma membranes of malaria parasite cells, Plasmodium falciparum, is involved in regional acidification of parasitised erythrocytes. J Biol Chem 275:34353-34358
47. +/glucose co-transporter. Nature 330:379-381
48. Hong W, Tang BL (1993) Protein trafficking along the exocytotic pathway. Bioessays 15:231-238
49. - channels of human erythrocytes by membrane oxidation. EMBO J. 21:22-30
50. Huber SM, Duranton C, Henke G, Van De Sand C, Heussler V, Shumilina E, Sandu CD, Tanneur V, Brand V, Kasinathan RS, Lang KS, Kremsner PG, Hubner CA, Rust MB, Dedek K, Jentsch TJ, Lang F (2004) Plasmodium induces swelling-activated ClC-2 anion channels in the host erythrocyte. J Biol Chem
51. Huestis R, Fischer K (2001) Prediction of many new exons and introns in Plasmodium falciparum chromosome 2. Mol Biochem Parasitol 118:187-199
52. Joet T, Holterman L, Stedman TT, Kocken CH, Van Der Wel A, Thomas AW, Krishna S (2002) Comparative characterization of hexose transporters of Plasmodium knowlesi, Plasmodium yoelii and Toxoplasma gondii highlights functional differences within the apicomplexan family. Biochem J 368:923-929
53. Joet T, Eckstein-Ludwig U, Morin C, Krishna S (2003) Validation of the hexose transporter of Plasmodium falciparum as a novel drug target. Proc Natl Acad Sci USA 100:7476-7479
54. Joet T, Chotivanich K, Silamut K, Patel AP, Morin C, KrishnaS (2004) Analysis of Plasmodium vivax hexose transporters and characterization of a parasitocidal inhibitor. Biochem J 381:905-909
55. Kanaani J, Ginsburg H (1989) Metabolic interconnection between the human malarial parasite Plasmodium falciparum and its host erythrocyte. Regulation of ATP levels by means of an adenylate translocator and adenylate kinase. J Biol Chem 264:3194-3199
56. Kanaani J, Ginsburg H (1991) Transport of lactate in Plasmodium falciparum-infected human erythrocytes. J Cell Physiol 149:469-476
57. Karcz SR, Herrmann VR, Cowman AF (1993) Cloning and characterization of a vacuolar ATPase A subunit homologue from Plasmodium falciparum. Mol Biochem Parasitol 58:333-344
58. Karcz SR, Herrmann VR, Trottein F, Cowman AF (1994) Cloning and characterization of the vacuolar ATPase B subunit from Plasmodium falciparum. Mol Biochem Parasitol 65:123-133
59. Kirk K, Horner HA, Elford BC, Ellory JC, Newbold CI (1994) Transport of diverse substrates into malaria-infected erythrocytes via a pathway showing functional characteristics of a chloride channel. J Biol Chem 269:3339-3347
60. Kirk K, Horner HA, Kirk J (1996) Glucose uptake in Plasmodium falciparum-infected erythrocytes is an equilibrative not an active process. Mol Biochem Parasitol 82:195-205
61. Kirk K, Staines HM, Martin RE, Saliba KJ. (1999) In: Transport and trafficking in the malaria-infected erythrocyte. Novartis Foundation Symposium 226. Novartis Foundation, Wiley, Chichester, pp 55-73
62. Kirk K (2001) Membrane transport in the malaria-infected erythrocyte. Physiol Rev 81:495-537
63. Kozak M (1986) Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44:283-292
64. Krishna S, Webb R, Woodrow C (2001) Transport proteins of Plasmodium falciparum: defining the limits of metabolism. Int J Parasitol 31:1331-1342
65. 2+-ATPase (PfATP4) belonging to a subclass unique to apicomplexan organisms. J Biol Chem 276:10782-10787
66. Krogstad DJ, Schlesinger PH, Gluzman IY (1985) Antimalarials increase vesicle pH in Plasmodium falciparum. J Cell Biol 101:2302-2309
67. Krugliak M, Zhang J, Ginsburg H (2002) Intraerythrocytic Plasmodium falciparum utilizes only a fraction of the amino acids derived from the digestion of host cell cytosol for the biosynthesis of its proteins. Mol Biochem Parasitol 119:249-256
68. Kumar R, Adams B, Oldenburg A, Musiyenko A, Barik S (2002) Characterisation and expression of a PP1 serine/threonine protein phosphatase (PfPP1) from the malaria parasite, Plasmodium falciparum: demonstration of its essential role using RNA interference. Malaria J 1:5
69. Lambros C, Vanderberg JP (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65:418-420
70. Lehane AM, Saliba KJ, Allen RJW, Kirk K (2004) Choline uptake into the malaria parasite is energised by the membrane potential. Biochem Biophys Res Commun 320:311-317
71. Malhotra P, Dasaradhi PV, Kumar A, Mohmmed A, Agrawal N, Bhatnagar RK, Chauhan VS (2002) Double-stranded RNA-mediated gene silencing of cysteine proteases (falcipain-1 and -2) of Plasmodium falciparum. Mol Microbiol 45:1245-1254
72. +-pyrophosphatase in malaria parasites. Biochem J 347:243-253
73. Martin RE, Henry RI, Abbey JL, Clements JD, Kirk K (2005) The 'permeome' of the malaria parasite: an overview of the membrane transport proteins of Plasmodium falciparum. Genome Biol 6:R26
74. Martin RE, Kirk K (2004) The malaria parasite's chloroquine resistance transporter is a member of the drug/metabolite transporter superfamily. Mol Biol Evol 21:1938-1949
75. +-pyrophosphatases in malaria parasites. Mol Biochem Parasitol 114:183-195
76. McRobert L, McConkey GA (2002) RNA interference (RNAi) inhibits growth of Plasmodium falciparum. Mol Biochem Parasitol 119:273-278
77. Milek RL, Stunnenberg HG, Konings RN (2000) Assembly and expression of a synthetic gene encoding the antigen Pfs48/45 of the human malaria parasite Plasmodium falciparum in yeast. Vaccine 18:1402-1411
78. Mohmmed A, Dasaradhi PV, Bhatnagar RK, Chauhan VS, Malhotra P (2003) In vivo gene silencing in Plasmodium berghei - a mouse malaria model. Biochem Biophys Res Commun 309:506-511
79. Nessler S, Friedrich O, Bakouh N, Fink RH, Sanchez CP, Planelles G, Lanzer M (2004) Evidence for activation of endogenous transporters in Xenopus laevis oocytes expressing the Plasmodium falciparum chloroquine resistance transporter PfCRT. J Biol Chem 279:39438-39446
80. Nyalwidhe J, Baumeister S, Hibbs AR, Tawill S, Papakrivos J, Volker U, Lingelbach K (2002) A nonpermeant biotin derivative gains access to the parasitophorous vacuole in Plasmodium falciparum-infected erythrocytes permeabilized with streptolysin O. J Biol Chem 277:40005-40011
81. Parker MD, Hyde RJ, Yao SY, McRobert L, Cass CE, Young JD, McConkey GA, Baldwin SA (2000) Identification of a nucleoside/nucleobase transporter from Plasmodium falciparum, a novel target for anti-malarial chemotherapy. Biochem J 349:67-75
82. Pasvol G, Wilson RJ, Smalley ME, Brown J (1978) Separation of viable schizont-infected red cells of Plasmodium falciparum from human blood. Ann Trop Med Parasitol 72:87-88
83. Penny JI, Hall ST, Woodrow CJ, Cowan GM, Gero AM, Krishna S (1998) Expression of substrate-specific transporters encoded by Plasmodium falciparum in Xenopus laevis oocytes. Mol Biochem Parasitol 93:81-89
84. +-dependent multivitamin transporter. Arch Biochem Biophys 366:95-106
85. Prasad PD, Srinivas SR, Wang H, Leibach FH, Devoe LD, Ganapathy V (2000) Electrogenic nature of rat sodium-dependent multivitamin transport. Biochem Biophys Res Commun 270:836-840
86. Rager N, Mamoun CB, Carter NS, Goldberg DE, Ullman B (2001) Localization of the Plasmodium falciparum PfNT1 nucleoside transporter to the parasite plasma membrane. J Biol Chem 276:41095-41099
87. Rasoloson D, Shi L, Chong CR, Kafsack BF, Sullivan DJ (2004) Copper pathways in Plasmodium falciparum infected erythrocytes indicate an efflux role for the copper P-ATPase. Biochem J 381:803-811
88. Raymond M, Gros P, Whiteway M, Thomas DY (1992) Functional complementation of yeast ste6 by a mammalian multidrug resistance mdr gene. Science 256:232-234
89. Reed MB, Saliba KJ, Caruana SR, Kirk, K, Cowman AF (2000) Pgh1 modulates sensitivity and resistance to multiple antimalarials in Plasmodium falciparum. Nature 403:906-909
90. Rothman JE (1987) Protein sorting by selective retention in the endoplasmic reticulum and Golgi stack. Cell 50:521-522
91. Saier MH Jr (2000) A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol Mol Biol Rev 64:354-411
92. Saliba KJ, Folb PI, Smith PJ (1998) Role for the Plasmodium falciparum digestive vacuole in chloroquine resistance. Biochem Pharmacol 56:313-320
93. Saliba KJ, Horner HA, Kirk K (1998) Transport and metabolism of the essential vitamin pantothenic acid in human erythrocytes infected with the malaria parasite Plasmodium falciparum. J Biol Chem 273:10190-10195
94. Saliba KJ, Kirk K (1998) Uptake of an antiplasmodial protease inhibitor into Plasmodium falciparum-infected human erythrocytes via a parasite-induced pathway. Mol Biochem Parasitol 94:297-301
95. +-ATPase. J Biol Chem 274:33213-33219
96. +-coupled pantothenate transport in the intracellular malaria parasite. J Biol Chem 276:18115-18121
97. +-pyrophosphatase. J Biol Chem 278:5605-5612
98. Saliba KJ, Krishna S, Kirk K (2004) Inhibition of hexose transport and abrogation of pH homeostasis in the intraerythrocytic malaria parasite by an O-3-hexose derivative. FEBS Lett 16:93-96
99. Santiago TC, Zufferey R, Mehra RS, Coleman RA, Mamoun CB (2004) The Plasmodium falciparum PfGatp is an endoplasmic reticulum membrane protein important for the initial step of malarial glycerolipid synthesis. J Biol Chem 279:9222-9232
100. Sidhu AB, Verdier-Pinard D, Fidock DA (2002) Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by PfCRT mutations. Science 298:210-213
101. Spiller DG, Bray PG, Hughes RH, Ward SA, White MR (2002) The pH of the Plasmodium falciparum digestive vacuole: holy grail or dead-end trail? Trends Parasitol 18:441-444
102. + transport in Plasmodium falciparum-infected red cells. J Membr Biol 172:13-24
103. Staines HM, Rae C, Kirk K (2000) Increased permeability of the malaria-infected erythrocyte to organic cations. Biochim Biophys Acta 1463:88-98
104. + in malaria-infected erythrocytes. Am J Physiol 280: C1576-C1587
105. Staines HM, Powell T, Ellory JC, Egee S, Lapaix F, Decherf G, Thomas SL, Duranton C, Lang F, Huber SM (2003) Modulation of whole-cell currents in Plasmodium falciparum-infected human red blood cells by holding potential and serum. J Physiol 552:177-183
106. Staines HM, Powell T, Thomas SL, Ellory JC (2004) Plasmodium falciparum-induced channels. Int J Parasitol 34:665-673
107. Stead AM, Bray PG, Edwards IG, DeKoning HP, Elford BC, Stocks PA, Ward SA (2001) Diamidine compounds: selective uptake and targeting in Plasmodium falciparum. Mol Pharmacol 59:1298-1306
108. +-pantothenate symporter. J Biol Chem 274:18747-18752
109. Stolz J, Caspari T, Carr AM, Sauer N (2004) Cell division defects of Schizosaccharomyces pombe liz1- mutants are caused by defects in pantothenate uptake. Eukaryot Cell 3:406-412
110. Tan W, Tai E, Chow LMC (2003) Expression and characterisation of PfCRT in yeast. Exp Parasitol 105:34
111. Teasdale RD, Jackson MR (1996) Signal-mediated sorting of membrane proteins between the endoplasmic reticulum and the golgi apparatus. Ann Rev Cell Dev Biol. 12:27-54
112. Thomas SL, Lew VL (2004) Plasmodium falciparum and the permeation pathway of the host red blood cell. Trends Parasitol 20:122-125
113. Tran CV, Saier MH Jr (2004) The principal chloroquine resistance protein of Plasmodium falciparum is a member of the drug/metabolite transporter superfamily. Microbiology 150:1-3
114. Ullu E, Tschudi C, Chakraborty T (2004) RNA interference in protozoan parasites. Cell Microbiol 6:509-519
115. Verloo P, Kocken CH, Van der Wel A, Tilly BC, Hogema BM, Sinaasappel M, Thomas AW, De Jonge HR (2004) Plasmodium falciparum-activated chloride channels are defective in erythrocytes from cystic fibrosis patients. J Biol Chem 279:10316-10322
116. Volkman SK, Cowman AF, Wirth DF (1995) Functional complementation of the ste6 gene of Saccharomyces cerevisiae with the PfMDR1 gene of Plasmodium falciparum. Proc Natl Acad Sci. USA 92:8921-8925
117. Wagner MA, Andemariam B, Desai SA (2003) A two-compartment model of osmotic lysis in Plasmodium falciparum-infected erythrocytes. Biophys J 84:116-123
118. Waller KL, Muhle RA, Ursos LM, Horrocks P, Verdier-Pinard D, Sidhu AB, Fujioka H, Roepe PD, Fidock DA (2003) Chloroquine resistance modulated in vitro by expression levels of the Plasmodium falciparum chloroquine resistance transporter. J Biol Chem 278:33593-33601
119. Waller RF, Keeling PJ, Donald RG, Striepen B, Handman E, Lang-Unnasch N, Cowman AF, Besra GS, Roos DS, McFadden GI (1998) Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc Natl Acad SciUSA 95:12352-12357
120. +-dependent multivitamin transporter. Cloning, functional expression, gene structure, and chromosomal localization. J Biol Chem 274:14875-14883
121. Weber JH, Vishnyakov A, Hambach K, Schultz A, Schultz JE, Linder JU (2004) Adenylyl cyclases from Plasmodium, Paramecium and Tetrahymena are novel ion channel/enzyme fusion proteins. Cell Signal 16:115-125
122. Wilson CM, Serrano AE, Wasley A, Bogenschutz MP, Shankar AH, Wirth DF (1989) Amplification of a gene related to mammalian mdr genes in drug-resistant Plasmodium falciparum. Science 244:1184-1186
123. Withers-Martinez C, Carpenter EP, Hackett F, Ely B, Sajid M, Grainger M, Blackman MJ (1999) PCR-based gene synthesis as an efficient approach for expression of the A+T-rich malaria genome. Protein Eng 12:1113-1120
124. Woodrow CJ, Penny JI, Krishna S (1999) Intraerythrocytic Plasmodium falciparum expresses a high affinity facilitative hexose transporter. J Biol Chem 274:7272-7277
125. Woodrow CJ, Burchmore RJ, Krishna S (2000) Hexose permeation pathways in Plasmodium falciparum-infected erythrocytes. Proc Natl Acad Sci USA 97:9931-9936
126. + exchanger determines chloroquine uptake in Plasmodium falciparum. J Cell Biol 140:335-345
127. Yadava A, Ockenhouse CF (2003) Effect of codon optimization on expression levels of a functionally folded malaria vaccine candidate in prokaryotic and eukaryotic expression systems. Infect Immun 71:4961-4969
128. Zhang H, Howard EM, Roepe PD (2002) Analysis of the antimalarial drug resistance protein PfCRT expressed in yeast. J Biol Chem 277:49767-49775
129. Zuegge J, Ralph S, Schmuker M, McFadden GI, Schneider G (2001) Deciphering apicoplast targeting signals-feature extraction from nuclear-encoded precursors of Plasmodium falciparum apicoplast proteins. Gene 280:19-26