The malaria parasite Plasmodium falciparum: Cell biological peculiarities and nutritional consequences

Protoplasma

Volumn 240, Issue 1, 2010, Pages 3-12

  Baumeister, Stefan ^a   Winterberg, Markus ^a,b   Przyborski, Jude M ^a   Lingelbach, Klaus ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Apicomplexa; Erythrocyte; Malaria; New permeability pathways; Plasmodium falciparum

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; BLOOD; CELL COMPARTMENTALIZATION; CELL MEMBRANE PERMEABILITY; CELL ORGANELLE; CELL VACUOLE; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; HUMAN; MALARIA FALCIPARUM; METABOLISM; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; PLASMODIUM FALCIPARUM; REVIEW; ULTRASTRUCTURE;

ANIMALS; CELL COMPARTMENTATION; CELL MEMBRANE PERMEABILITY; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; HOST-PARASITE INTERACTIONS; HUMANS; MALARIA, FALCIPARUM; MODELS, BIOLOGICAL; ORGANELLES; PLASMODIUM FALCIPARUM; VACUOLES;

ALGAE; APICOMPLEXA; EUKARYOTA; MAMMALIA; PLASMODIUM (APICOMPLEXA); PLASMODIUM FALCIPARUM;

EID: 77949539756     PISSN: 0033183X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00709-009-0090-3     Document Type: Review

References (75)

1. Aikawa M, Hepler PK, Huff CG, Sprinz H (1966) The feeding mechanism of avian malarial parasites. J Cell Biol 28: 355-373.
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. doi: 10. 1182/blood-2004-05-2047.
3. 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.
4. Bannister LH, Butcher GA, Dennis ED, Mitchell GH (1975) Structure and invasive behaviour of Plasmodium knowlesi merozoites in vitro. Parasitology 71: 483-491.
5. Baumeister S, Endermann T, Charpian S, Nyalwidhe J, Duranton C, Huber S, Kirk K, Lang F, Lingelbach K (2003) A biotin derivative blocks parasite induced novel permeation pathways in Plasmodium falciparum-infected erythrocytes. Mol Biochem Parasitol 132: 35-45. doi: 10. 1016/j. molbiopara. 2003. 08. 003.
6. Baumeister S, Winterberg M, Duranton C, Huber SM, Lang F, Kirk K, Lingelbach K (2006) Evidence for the involvement of Plasmodium falciparum proteins in the formation of new permeability pathways in the erythrocyte membrane. Mol Microbiol 60: 493-504. doi: 10. 1111/j. 1365-2958. 2006. 05112. x.
7. Bietz S, Montilla I, Külzer S, Przyborski JM, Lingelbach K (2009) Recruitment of human aquaporin 3 to internal membranes in the Plasmodium falciparum infected erythrocyte. Mol Biochem Parasitol 167: 48-53. doi: 10. 1016/j. molbiopara. 2009. 04. 006.
8. Blackman J (2008) Malarial proteases and host cell egress: an 'emerging' cascade. Cell Microbiol 10: 1925-1934. doi: 10. 1111/j. 1462-5822. 2008. 01176. x.
9. Boddey JA, Moritz RL, Simpson RJ, Cowman AF (2009) Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Traffic 10: 285-299. doi: 10. 1111/j. 1600-0854. 2008. 00864. x.
10. Burchmore RJS, Barrett MP (2001) Life in vacuoles-nutrient acquisition by Leishmania amastigotes. Int J Parasitol 31: 1311-1320. doi: 10. 1016/S0020-7519(01)00259-4.
11. Chang HH, Falick AM, Carlton PM, Sedat JW, DeRisi JL, Marletta MA (2008) N-terminal processing of proteins exported by malaria parasites. Mol Biochem Parasitol 160: 107-115. doi: 10. 1016/j. molbiopara. 2008. 04. 011.
12. Charpian S, Przyborski JM (2008) Protein transport across the parasitophorous vacuole of Plasmodium falciparum: into the great wide open. Traffic 9: 157-165. doi: 10. 1111/j. 1600-0854. 2007. 00648. x.
13. Cohn JV, Alkhalil A, Wagner MA, Rajapandi T, Desai SA (2003) Extracellular lysines on the plasmodial surface anion channel involved in Na + exclusion. Mol Biochem Parasitol 132: 27-34. doi: 10. 1016/j. molbiopara. 2003. 08. 001.
14. Coppens I, Dunn JD, Romano JD, Pypaert M, Zhang H, Boothroyd JC, Joiner KA (2006) Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell 125: 261-274. doi: 10. 1016/j. cell. 2006. 01. 056.
15. Crabb BS, Cooke BM, Reeder JC, Waller RF, Caruana SR, Davern KM, Wickham ME, Brown GV, Coppel RL, Cowman AF (1997) Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 89: 287-296. doi: 10. 1016/S0092-8674(00)80207-X.
16. de Koning-Ward TF, Gilson PR, Boddey JA, Rug M, Smith BJ, Papenfuss AT, Sanders PR, Lundie RJ, Maier AG, Cowman AF, Crabb BS (2009) A newly discovered protein export machine in malaria parasites. Nature 459: 945-949. doi: 10. 1038/nature08104.
17. Desai SA, Krogstad DJ, McCleskey EW (1993) A nutrient-permeable channel on the intraerythrocytic malaria parasite. Nature 362: 643-646. doi: 10. 1038/362643a0.
18. 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. doi: 10. 1038/35023000.
19. 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. doi: 10. 1113/jphysiol. 2002. 022970.
20. Elliott DA, McIntosh MT, Hosgood HD 3rd, Chen S, Zhang G, Baevova P, Joiner KA (2008) Four distinct pathways of hemoglobin uptake in the malaria parasite Plasmodium falciparum. Proc Natl Acad Sci U S A 105: 2463-2468. doi: 10. 1073/pnas. 0711067105.
21. Fichera ME, Roos DS (1997) A plastid organelle as a drug target in apicomplexan parasites. Nature 390: 407-409. doi: 10. 1038/37132.
22. Foth BJ, Ralph SA, Tonkin CJ, Struck NS, Fraunholz M, Roos DS, Cowman AF, McFadden GI (2003) Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299: 705-708. doi: 10. 1126/science. 1078599.
23. Gehde N, Hinrichs C, Montilla I, Charpian S, Lingelbach K, Przyborski JM (2009) Protein unfolding is an essential requirement for transport across the parasitophorous vacuolar membrane of Plasmodium falciparum. Mol Microbiol 71: 613-628. doi: 10. 1111/j. 1365-2958. 2008. 06552. x.
24. Gero AM, Kirk K (1994) Nutrient transport pathways in Plasmodium-infected erythrocytes: what and where are they? Parasitol Today 10: 395-399. doi: 10. 1016/0169-4758(94)90231-3.
25. Ginsburg H (2002) Oxidative permeabilization? Trends Parasitol 18: 346. doi: 10. 1016/S1471-4922(02)02322-X.
26. 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.
27. Ginsburg H, Krugliak M, Eidelman O, Cabantchik ZI (1983) New permeability pathways induced in membranes of Plasmodium falciparum infected erythrocytes. Mol Biochem Parasitol 8: 177-190. doi: 10. 1016/0166-6851(83)90008-7.
28. Goldberg DE (2005) Hemoglobin degradation. Curr Top Microbiol Immunol 295: 275-291. doi: 10. 1007/3-540-29088-5_11.
29. Goodman CD, McFadden GI (2007) Fatty acid biosynthesis as a drug target in apicomplexan parasites. Curr Drug Targets 8: 15-30.
30. Günther K, Tümmler M, Arnold HH, Ridley R, Goman M, Scaife JG, Lingelbach K (1991) An exported protein of Plasmodium falciparum is synthesized as an integral membrane protein. Mol Biochem Parasitol 46: 149-157. doi: 10. 1016/0166-6851(91)90208-N.
31. Hanssen E, Sougrat R, Frankland S, Deed S, Klonis N, Lippincott-Schwartz J, Tilley L (2008) Electron tomography of the Maurer's cleft organelles of Plasmodium falciparum-infected erythrocytes reveals novel structural features. Mol Microbiol 67: 703-718. doi: 10. 1111/j. 1365-2958. 2007. 06063. x.
32. Hiller NL, Akompong T, Morrow JS, Holder AA, Haldar K (2003) Identification of a stomatin orthologue in vacuoles induced in human erythrocytes by malaria parasites. A role for microbial raft proteins in apicomplexan vacuole biogenesis. J Biol Chem 278: 48413-48421. doi: 10. 1074/jbc. M307266200.
33. Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T, Lopez-Estrano C, Haldar K (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306: 1934-1937. doi: 10. 1126/science. 1102737.
34. Huber SM, Uhlemann AC, Gamper NL, Duranton C, Kremsner PG, Lang F (2002a) Plasmodium falciparum activates endogenous Cl(-) channels of human erythrocytes by membrane oxidation. EMBO J 21: 22-30. doi: 10. 1093/emboj/21. 1. 22.
35. Huber S, Uhlemann A, Gamper N, Duranton C, Lang F, Kremsner P (2002b) Oxidative permeabilization? Trends Parasitol 18: 346. doi: 10. 1016/S1471-4922(02)02323-1.
36. Joiner KA, Fuhrman SA, Miettinen HM, Kasper LH, Mellman I (1990) Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249: 641-646.
37. Kirk K (2001) Membrane transport in the malaria-infected erythrocyte. Physiol Rev 81: 495-537.
38. Kirk K, Saliba KJ (2007) Targeting nutrient uptake mechanisms in Plasmodium. Curr Drug Targets 8: 75-88.
39. Klemba M, Goldberg DE (2002) Biological roles of proteases in parasitic protozoa. Annu Rev Biochem 71: 275-305. doi: 10. 1146/annurev. biochem. 71. 090501. 145453.
40. Kriek N, Tilley L, Horrocks P, Pinches R, Elford BC, Ferguson DJ, Lingelbach K, Newbold CI (2003) Characterization of the pathway for transport of the cytoadherence-mediating protein, PfEMP1, to the host cell surface in malaria parasite-infected erythrocytes. Mol Microbiol 50: 1215-1227. doi: 10. 1046/j. 1365-2958. 2003. 03784. x.
41. Lauer SA, Rathod PK, Ghori N, Haldar K (1997) A membrane network for nutrient import in red cells infected with the malaria parasite. Science 5315: 1122-1125. doi: 10. 1126/science. 276. 5315. 1122.
42. Lev S, Moreno H, Martinez R, Canoll P, Peles E, Musacchio JM, Plowman GD, Rudy B, Schlessinger J (1995) Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions. Nature 376: 737-745. doi: 10. 1038/376737a0.
43. Levitan IB (1994) Modulation of ion channels by protein phosphorylation and dephosphorylation. Annu Rev Physiol 56: 193-212. doi: 10. 1146/annurev. ph. 56. 030194. 001205.
44. Lingelbach K, Joiner KA (1998) The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells. J Cell Sci 111: 1467-1475.
45. Lingelbach K, Przyborski JM (2006) The long and winding road: protein trafficking mechanisms in the Plasmodium falciparum infected erythrocyte. Mol Biochem Parasitol 147: 1-8. doi: 10. 1016/j. molbiopara. 2006. 01. 014.
46. Lizundia R, Werling D, Langsley G, Ralph SA (2009) Theileria apicoplast as a target for chemotherapy. Antimicrob Agents Chemother 53: 1213-1217. doi: 10. 1128/AAC. 00126-08.
47. Maier AG, Cooke BM, Cowman AF, Tilley L (2009) Malaria parasite proteins that remodel the host erythrocyte. Nat Rev Microbiol 7: 341-354. doi: 10. 1038/nrmicro2110.
48. Marti M, Baum J, Rug M, Tilley L, Cowman AF (2005) Signal-mediated export of proteins from the malaria parasite to the host erythrocyte. J Cell Biol 171: 587-592. doi: 10. 1083/jcb. 200508051.
49. Martin RE, Kirk K (2007) Transport of the essential nutrient isoleucine in human erythrocytes infected with the malaria parasite Plasmodium falciparum. Blood 109: 2217-2224. doi: 10. 1182/blood-2005-11-026963.
50. McFadden GI, Reith ME, Munholland J, Lang-Unnasch N (1996) Plastid in human parasite. Nature 381: 482. doi: 10. 1038/381482a0.
51. Merckx A, Nivez MP, Bouyer G, Alano P, Langsley G, Deitsch K, Thomas S, Doerig C, Egée S (2008) Plasmodium falciparum regulatory subunit of cAMP-dependent PKA and anion channel conductance. PLoS Pathog 4: e19.
52. Merckx A, Bouyer G, Thomas SL, Langsley G, Egée S (2009) Anion channels in Plasmodium-falciparum-infected erythrocytes and protein kinase A. Trends Parasitol 25: 139-144. doi: 10. 1016/j. pt. 2008. 12. 005.
53. Miller LH, Baruch DI, Marsh K, Doumbo OK (2002) The pathogenic basis of malaria. Nature 415: 673-679. doi: 10. 1038/415673a.
54. Mullin KA, Lim L, Ralph SA, Spurck TP, Handman E, McFadden GI (2006) Membrane transporters in the relict plastid of malaria parasites. Proc Natl Acad Sci U S A 103: 9572-9577. doi: 10. 1073/pnas. 0602293103.
55. Murphy SC, Samuel BU, Harrison T, Speicher KD, Speicher DW, Reid ME, Prohaska R, Low PS, Tanner MJ, Mohandas N, Haldar K (2004) Erythrocyte detergent-resistant membrane proteins: their characterization and selective uptake during malarial infection. Blood 103: 1920-1928. doi: 10. 1182/blood-2003-09-3165.
56. Murphy SC, Fernandez-Pol S, Chung PH, Prasanna Murthy SN, Milne SB, Salomao M, Brown HA, Lomasney JW, Mohandas N, Haldar K (2007) Cytoplasmic remodeling of erythrocyte raft lipids during infection by the human malaria parasite Plasmodium falciparum. Blood 110: 2132-2139. doi: 10. 1182/blood-2007-04-083873.
57. Nunes MC, Goldring JP, Doerig C, Scherf A (2007) A novel protein kinase family in Plasmodium falciparum is differentially transcribed and secreted to various cellular compartments of the host cell. Mol Microbiol 63: 391-403. doi: 10. 1111/j. 1365-2958. 2006. 05521. x.
58. Nyalwidhe J, Lingelbach K (2006) Proteases and chaperones are the most abundant proteins in the parasitophorous vacuole of Plasmodium falciparum-infected erythrocytes. Proteomics 6: 1563-1573. doi: 10. 1002/pmic. 200500379.
59. 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. doi: 10. 1074/jbc. M207077200.
60. Nyalwidhe J, Maier UG, Lingelbach K (2003) Intracellular parasitism: cell biological adaptations of parasitic protozoa to a life inside cells. Zoology (Jena) 106: 341-348. doi: 10. 1078/0944-2006-00127.
61. Pouvelle B, Spiegel R, Hsiao L, Howard RJ, Morris RL, Thomas AP, Taraschi TF (1991) Direct access to serum macromolecules by intraerythrocytic malaria parasites. Nature 353: 73-75. doi: 10. 1038/353073a0.
62. Ralph SA, van Dooren GG, Waller RF, Crawford MJ, Fraunholz MJ, Foth BJ, Tonkin CJ, Roos DS, McFadden GI (2004) Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol 2: 203-216. doi: 10. 1038/nrmicro843.
63. 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. doi: 10. 1074/jbc. 273. 17. 10190.
64. Schneider AG, Mercereau-Puijalon O (2005) A new Apicomplexa-specific protein kinase family: multiple members in Plasmodium falciparum, all with an export signature. BMC Genomics 6: 30. doi: 10. 1186/1471-2164-6-30.
65. Sinai AP, Joiner KA (1997) Safe Haven: the cell biology of nonfusogenic pathogen vacuoles. Annu Rev Microbiol 51: 415-462. doi: 10. 1146/annurev. micro. 51. 1. 415.
66. Slater AF (1992) Malaria pigment. Exp Parasitol 74: 362-365. doi: 10. 1016/0014-4894(92)90162-4.
67. Slomianny C (1990) Three-dimensional reconstruction of the feeding process of the malaria parasite. Blood Cells 16: 369-378.
68. Soldati D, Meissner M (2004) Toxoplasma as a novel system for motility. Curr Opin Cell Biol 16: 32-40. doi: 10. 1016/j. ceb. 2003. 11. 013.
69. Soldati D (1999) The apicoplast as a potential therapeutic target in toxoplasma and other apicomplexan parasites. Parasitol Today 15: 5-7. doi: 10. 1016/S0169-4758(98)01363-5.
70. Staines HM, Alkhalil A, Allen RJ, De Jonge HR, Derbyshire E, Egée S, Ginsburg H, Hill DA, Huber SM, Kirk K, Lang F, Lisk G, Oteng E, Pillai AD, Rayavara K, Rouhani S, Saliba KJ, Shen C, Solomon T, Thomas SL, Verloo P, Desai SA (2007) Electrophysiological studies of malaria parasite-infected erythrocytes: current status. Int J Parasitol 37: 475-482. doi: 10. 1016/j. ijpara. 2006. 12. 013.
71. Surolia N, Padmanaban G (1992) De novo biosynthesis of heme offers a new chemotherapeutic target in the human malarial parasite. Biochem Biophys Res Commun 187: 744-750.
72. 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. doi: 10. 1074/jbc. M311540200.
73. WHO (2009) Fact sheet N°94. http://www.who.int/mediacentre/factsheets/fs094/en/index.html.
74. Wickert H, Krohne G (2007) The complex morphology of Maurer's clefts: from discovery to three-dimensional reconstructions. Trends Parasitol 23: 502-509. doi: 10. 1016/j. pt. 2007. 08. 008.
75. Wickert H, Göttler W, Krohne G, Lanzer M (2004) Maurer's cleft organization in the cytoplasm of Plasmodium falciparum-infected erythrocytes: new insights from three-dimensional reconstruction of serial ultrathin sections. Eur J Cell Biol 83: 567-582.