Solute restriction reveals an essential role for clag3-associated channels in malaria parasite nutrient acquisition

Molecular Pharmacology

Volumn 82, Issue 6, 2012, Pages 1104-1114

  Pillai, Ajay D ^a,c   Nguitragool, Wang ^a,d   Lyko, Brian ^a,e   Dolinta, Keithlee ^a,f   Butler, Michelle M ^b   Nguyen, Son T ^b   Peet, Norton P ^b   Bowlin, Terry L ^b   Desai, Sanjay A ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b MICROBIOTIX INC   (United States)

^c Wellcome Trust/DBT India Alliance   (India)

^d MAHIDOL UNIVERSITY   (Thailand)

^e TOWSON UNIVERSITY   (United States)

^f UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANION CHANNEL; ANTIMALARIAL AGENT; CLAG3 PROTEIN; ISPA 28; PLASMODIAL SURFACE ANION CHANNEL; PLASMODIAL SURFACE ANION CHANNEL INHIBITOR; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ANTIMALARIAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; FEMALE; GENE EXPRESSION; GENE MAPPING; GENE SWITCHING; GENETIC LINKAGE; GROWTH INHIBITION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; NUTRIENT UPTAKE; PHENOTYPE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SOLUTE;

ANIMALS; ANIONS; ANTIMALARIALS; BIOLOGICAL TRANSPORT; CELL MEMBRANE PERMEABILITY; EPIGENOMICS; ERYTHROCYTES; HELA CELLS; HUMANS; ION CHANNELS; MALARIA; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; TRANSFECTION;

EID: 84869846744     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.081224     Document Type: Article

References (59)

1. Akkaya C, Shumilina E, Bobballa D, Brand VB, Mahmud H, Lang F, and Huber SM (2009) The Plasmodium falciparum-induced anion channel of human erythrocytes is an ATP-release pathway. Pflugers Arch 457:1035-1047.
2. Alkhalil A, Cohn JV, Wagner MA, Cabrera JS, Rajapandi T, and Desai SA (2004) Plasmodium falciparum likely encodes the principal anion channel on infected human erythrocytes. Blood 104:4279-4286. (Pubitemid 39620183)
3. Alkhalil A, Hill DA, and Desai SA (2007) Babesia and plasmodia increase host erythrocyte permeability through distinct mechanisms. Cell Microbiol 9:851-860. (Pubitemid 46394898)
4. Alkhalil A, Hong L, Nguitragool W, and Desai SA (2012) Voltage-dependent inactivation of the plasmodial surface anion channel via a cleavable cytoplasmic component. Biochim Biophys Acta 1818:367-374.
5. Alkhalil A, Pillai AD, Bokhari AA, Vaidya AB, and Desai SA (2009) Complex inheritance of the plasmodial surface anion channel in a Plasmodium falciparum genetic cross. Mol Microbiol 72:459-469.
6. Armstrong MD and Stave U (1973) A study of plasma free amino acid levels. II. Normal values for children and adults. Metabolism 22:561-569.
7. Asahi H, Kanazawa T, Kajihara Y, Takahashi K, and Takahashi T (1996) Hypoxanthine: a low molecular weight factor essential for growth of erythrocytic Plasmodium falciparum in a serum-free medium. Parasitology 113:19-23. (Pubitemid 26228364)
8. Boddey JA, Hodder AN, Günther S, Gilson PR, Patsiouras H, Kapp EA, Pearce JA, de Koning-Ward TF, Simpson RJ, Crabb BS, et al. (2010) An aspartyl protease directs malaria effector proteins to the host cell. Nature 463:627-631.
9. Brand VB, Sandu CD, Duranton C, Tanneur V, Lang KS, Huber SM, and Lang F (2003) Dependence of Plasmodium falciparum in vitro growth on the cation permeability of the human host erythrocyte. Cell Physiol Biochem 13:347-356. (Pubitemid 37465150)
10. Broman KW, Wu H, Sen S, and Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889-890. (Pubitemid 36582406)
11. Chung WY, Gardiner DL, Anderson KA, Hyland CA, Kemp DJ, and Trenholme KR (2007) The CLAG/RhopH1 locus on chromosome 3 of Plasmodium falciparum: two genes or two alleles of the same gene? Mol Biochem Parasitol 151:229-232. (Pubitemid 46054216)
12. Comeaux CA, Coleman BI, Bei AK, Whitehurst N, and Duraisingh MT (2011) Functional analysis of epigenetic regulation of tandem RhopH1/clag genes reveals a role in Plasmodium falciparum growth. Mol Microbiol 80:378-390.
13. Cortés A, Carret C, Kaneko O, Yim Lim BY, Ivens A, and Holder AA (2007) Epigenetic silencing of Plasmodium falciparum genes linked to erythrocyte invasion. PLoS Pathog 3:e107.
14. Deitsch KW, Lukehart SA, and Stringer JR (2009) Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens. Nat Rev Microbiol 7:493-503.
15. Desai SA (2012) Ion and nutrient uptake by malaria parasite-infected erythrocytes. Cell Microbiol 14:1003-1009.
16. Desai SA, Bezrukov SM, and Zimmerberg J (2000) A voltage-dependent channel involved in nutrient uptake by red blood cells infected with the malaria parasite. Nature 406:1001-1005.
17. Freitas-Junior LH, Bottius E, Pirrit LA, Deitsch KW, Scheidig C, Guinet F, Nehrbass U, Wellems TE, and Scherf A (2000) Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407:1018-1022.
18. Gamo FJ, Sanz LM, Vidal J, de Cozar C, Alvarez E, Lavandera JL, Vanderwall DE, Green DV, Kumar V, Hasan S, et al. (2010) Thousands of chemical starting points for antimalarial lead identification. Nature 465:305-310.
19. Gero AM and Wood AM (1991) New nucleoside transport pathways induced in the host erythrocyte membrane of malaria and Babesia infected cells. Adv Exp Med Biol 309A:169-172.
20. Ginsburg H, Krugliak M, Eidelman O, and Cabantchik ZI (1983) New permeability pathways induced in membranes of Plasmodium falciparum infected erythrocytes. Mol Biochem Parasitol 8:177-190. (Pubitemid 13061833)
21. Ginsburg H, Kutner S, Krugliak M, and 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. (Pubitemid 15140562)
22. Guiguemde WA, Shelat AA, Bouck D, Duffy S, Crowther GJ, Davis PH, Smithson DC, Connelly M, Clark J, Zhu F, et al. (2010) Chemical genetics of Plasmodium falciparum. Nature 465:311-315.
23. Hill DA, Pillai AD, Nawaz F, Hayton K, Doan L, Lisk G, and Desai SA (2007) A blasticidin S-resistant Plasmodium falciparum mutant with a defective plasmodial surface anion channel. Proc Natl Acad Sci USA 104:1063-1068. (Pubitemid 46154736)
24. Homewood CA and Neame KD (1974) Malaria and the permeability of the host erythrocyte. Nature 252:718-719.
25. Istvan ES, Dharia NV, Bopp SE, Gluzman I, Winzeler EA, and Goldberg DE (2011) Validation of isoleucine utilization targets in Plasmodium falciparum. Proc Natl Acad Sci USA 108:1627-1632.
26. Kaneko O, Tsuboi T, Ling IT, Howell S, Shirano M, Tachibana M, Cao YM, Holder AA, and Torii M (2001) The high molecular mass rhoptry protein, RhopH1, is encoded by members of the clag multigene family in Plasmodium falciparum and Plasmodium yoelii. Mol Biochem Parasitol 118:223-231. (Pubitemid 34001685)
27. Kirk K, Horner HA, Elford BC, Ellory JC, and 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. (Pubitemid 24237649)
28. Kraemer SM and Smith JD (2003) Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family. Mol Microbiol 50:1527-1538. (Pubitemid 38010450)
29. Kutner S, Breuer WV, Ginsburg H, and Cabantchik ZI (1987) On the mode of action of phlorizin as an antimalarial agent in in vitro cultures of Plasmodium falciparum. Biochem Pharmacol 36:123-129. (Pubitemid 17227220)
30. Lavazec C, Sanyal S, and Templeton TJ (2007) Expression switching in the stevor and Pfmc-2TM superfamilies in Plasmodium falciparum. Mol Microbiol 64:1621-1634. (Pubitemid 46889912)
31. Lew VL, Macdonald L, Ginsburg H, Krugliak M, and Tiffert T (2004) Excess haemoglobin digestion by malaria parasites: a strategy to prevent premature host cell lysis. Blood Cells Mol Dis 32:353-359. (Pubitemid 38581853)
32. Lisk G and Desai SA (2005) The plasmodial surface anion channel is functionally conserved in divergent malaria parasites. Eukaryot Cell 4:2153-2159. (Pubitemid 41798320)
33. Lisk G, Kang M, Cohn JV, and Desai SA (2006) Specific inhibition of the plasmodial surface anion channel by dantrolene. Eukaryot Cell 5:1882-1893.
34. Lisk G, Pain M, Gluzman IY, Kambhampati S, Furuya T, Su XZ, Fay MP, Goldberg DE, and Desai SA (2008) Changes in the plasmodial surface anion channel reduce leupeptin uptake and can confer drug resistance in P. falciparum-infected erythrocytes. Antimicrob Agents Chemother 52:2346-2354. (Pubitemid 351915661)
35. Liu J, Istvan ES, Gluzman IY, Gross J, and Goldberg DE (2006) Plasmodium falciparum ensures its amino acid supply with multiple acquisition pathways and redundant proteolytic enzyme systems. Proc Natl Acad Sci USA 103:8840-8845. (Pubitemid 43878106)
36. Lyko B, Hammershaimb EA, Nguitragool W, Wellems TE, and Desai SA (2012) A high-throughput method to detect Plasmodium falciparum clones in limiting dilution microplates. Malar J 11:124.
37. Marshall NJ, Goodwin CJ, and Holt SJ (1995) A critical assessment of the use of microculture tetrazolium assays to measure cell growth and function. Growth Regul 5:69-84.
38. Martin RE and Kirk K (2007) Transport of the essential nutrient isoleucine in human erythrocytes infected with the malaria parasite Plasmodium falciparum. Blood 109:2217-2224. (Pubitemid 46348226)
39. Matsuhisa S, Takesawa S, and Sakai K (1987) Binary-solute adsorption of dosed drugs on serum-albumin. Chem Eng J Biochem Eng J 34:B21-B27. (Pubitemid 17553721)
40. Milsom JP, Morgan MY, and Sherlock S (1979) Factors affecting plasma amino acid concentrations in control subjects. Metabolism 28:313-319. (Pubitemid 9144327)
41. Mok BW, Ribacke U, Winter G, Yip BH, Tan CS, Fernandez V, Chen Q, Nilsson P, and Wahlgren M (2007) Comparative transcriptomal analysis of isogenic Plasmodium falciparum clones of distinct antigenic and adhesive phenotypes. Mol Biochem Parasitol 151:184-192. (Pubitemid 46054214)
42. Nguitragool W, Bokhari AA, Pillai AD, Rayavara K, Sharma P, Turpin B, Aravind L, and Desai SA (2011) Malaria parasite clag3 genes determine channel-mediated nutrient uptake by infected red blood cells. Cell 145:665-677.
43. Pillai AD, Pain M, Solomon T, Bokhari AA, and Desai SA (2010) A cell-based high-throughput screen validates the plasmodial surface anion channel as an antimalarial target. Mol Pharmacol 77:724-733.
44. Plouffe D, Brinker A, McNamara C, Henson K, Kato N, Kuhen K, Nagle A, Adrián F, Matzen JT, Anderson P, et al. (2008) In silico activity profiling reveals the mechanism of action of antimalarials discovered in a high-throughput screen. Proc Natl Acad Sci USA 105:9059-9064.
45. Quashie NB, Ranford-Cartwright LC, and de Koning HP (2010) Uptake of purines in Plasmodium falciparum-infected human erythrocytes is mostly mediated by the human equilibrative nucleoside transporter and the human facilitative nucleobase transporter. Malar J 9:36.
46. Russo I, Babbitt S, Muralidharan V, Butler T, Oksman A, and Goldberg DE (2010) Plasmepsin V licenses Plasmodium proteins for export into the host erythrocyte. Nature 463:632-636.
47. Saliba KJ, Horner HA, and 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. (Pubitemid 28227619)
48. Sato JD and Kan M (2001) Media for culture of mammalian cells. Curr Protoc Cell Biol Unit 1.2.
49. Saunders SJ, Truswell AS, Barbezat GO, Wittman W, and Hansen JD (1967) Plasma free aminoacid pattern in protein-calorie malnutrition: reappraisal of its diagnostic value. Lancet 2:795-797.
50. Scherf A, Hernandez-Rivas R, Buffet P, Bottius E, Benatar C, Pouvelle B, Gysin J, and Lanzer M (1998) Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. EMBO J 17:5418-5426. (Pubitemid 28427055)
51. Scherf A, Lopez-Rubio JJ, and Riviere L (2008) Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol 62:445-470.
52. Staines HM, Alkhalil A, Allen RJ, De Jonge HR, Derbyshire E, Egée S, Ginsburg H, Hill DA, Huber SM, Kirk K, et al. (2007) Electrophysiological studies of malaria parasite-infected erythrocytes: current status. Int J Parasitol 37:475-482. (Pubitemid 46399711)
53. Staines HM, Dee BC, O'Brien M, Lang HJ, Englert H, Horner HA, Ellory JC, and Kirk K (2004) Furosemide analogues as potent inhibitors of the new permeability pathways of Plasmodium falciparum-infected human erythrocytes. Mol Biochem Parasitol 133:315-318. (Pubitemid 38032879)
54. + in malaria-infected erythrocytes. Am J Physiol Cell Physiol 280: C1576-C1587.
55. Tamez PA, Bhattacharjee S, van Ooij C, Hiller NL, Llinás M, Balu B, Adams JH, and Haldar K (2008) An erythrocyte vesicle protein exported by the malaria parasite promotes tubovesicular lipid import from the host cell surface. PLoS Pathog 4:e1000118.
56. Tonkin CJ, Carret CK, Duraisingh MT, Voss TS, Ralph SA, Hommel M, Duffy MF, Silva LM, Scherf A, Ivens A, et al. (2009) Sir2 paralogues cooperate to regulate virulence genes and antigenic variation in Plasmodium falciparum. PLoS Biol 7:e84.
57. Vincensini L, Fall G, Berry L, Blisnick T, and Braun Breton C (2008) The RhopH complex is transferred to the host cell cytoplasm following red blood cell invasion by Plasmodium falciparum. Mol Biochem Parasitol 160:81-89.
58. Wellems TE, Panton LJ, Gluzman IY, do Rosario VE, Gwadz RW, Walker-Jonah A, and Krogstad DJ (1990) Chloroquine resistance not linked to mdr-like genes in a Plasmodium falciparum cross. Nature 345:253-255.
59. Winterberg M, Rajendran E, Baumeister S, Bietz S, Kirk K, and Lingelbach K (2012) Chemical activation of a high-affinity glutamate transporter in human erythrocytes and its implications for malaria-parasite-induced glutamate uptake. Blood 119:3604-3612.