Malaria and the Red Blood Cell Membrane

Seminars in Hematology

Volumn 41, Issue 2, 2004, Pages 173-188

  Cooke, Brian M ^a   Mohandas, Narla ^b   Coppel, Ross L ^b  

^a MONASH UNIVERSITY   (Australia)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

ANEMIA; BLOOD CELL; CYTOPLASM; CYTOSKELETON; ERYTHROCYTE ADHESIVENESS; ERYTHROCYTE MEMBRANE; GENOME; HOST CELL; HOST PARASITE INTERACTION; HUMAN; MALARIA; MEMBRANE FLUIDITY; NONHUMAN; PATHOGENESIS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; ROSETTE FORMATION; VASCULAR ENDOTHELIUM;

EID: 1942477417     PISSN: 00371963     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.seminhematol.2004.01.004     Document Type: Article

References (186)

1. Sachs J, Malaney P: The economic and social burden of malaria. Nature 415:680-685, 2002
2. Nagel RL, Roth EF Jr: Malaria and red cell genetic defects. Blood 74:1213-1221, 1989
3. Sherman IW: Membrane structure and function of malaria parasites and the infected erythrocyte. Parasitology 91:609-645, 1985
4. Cooke BM, Mohandas N, Coppel RL: The malaria-infected red blood cell: Structural and functional changes. Adv Parasitol 50:1-86, 2001
5. MacPherson GG, Warrell MJ, White NJ, Looareesuwan S, Warrell DA: Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am J Pathol 119:385-401, 1985
6. Miller LH, Baruch DI, Marsh K, Doumbo OK: The pathogenic basis of malaria. Nature 415:673-679, 2002
7. Bannister L, Mitchell G: The ins, outs and roundabouts of malaria. Trends Parasitol 19:209-213, 2003
8. Bannister LH, Mitchell GH, Butcher GA, Dennis ED, Cohen S: Structure and development of the surface coat of erythrocytic merozoites of Plasmodium knowlesi. Cell Tissue Res 245:281-290, 1986
9. Roggwiller E, Betoulle ME, Blisnick T, Braun Breton C: A role for erythrocyte band 3 degradation by the parasite gp76 serine protease in the formation of the parasitophorous vacuole during invasion of erythrocytes by Plasmodium falciparum. Mol Biochem Parasitol 82:13-24, 1996
10. Wilson R: Biochemistry of red cell invasion. Blood Cells 16:237-252, 1990
11. Rangachari K, Dluzewski A, Wilson RJ, Gratzer WB: Control of malarial invasion by phosphorylation of the host cell membrane cytoskeleton. Nature 324:364-365, 1986
12. Pinder JC, Fowler RE, Dluzewski AR, Bannister LH, Lavin FM, Mitchell GH, et al: Actomyosin motor in the merozoite of the malaria parasite, Plasmodium falciparum: Implications for red cell invasion. J Cell Sci 111:1831-1839, 1998
13. Reed MB, Caruana SR, Batchelor AH, Thompson JK, Crabb BS, Cowman AF: Targeted disruption of an erythrocyte binding antigen in Plasmodium falciparum is associated with a switch toward a sialic acid-independent pathway of invasion. Proc Natl Acad Sci USA 97:7509-7514, 2000
14. Dolan SA, Miller LH, Wellems TE: Evidence for a switching mechanism in the invasion of erythrocytes by Plasmodium falciparum. J Clin Invest 86:618-624, 1990
15. k). Strain differences indicate receptor heterogeneity and two pathways for invasion. J Clin Invest 80:1190-1193, 1987
16. Perkins ME, Holt EH: Erythrocyte receptor recognition varies in Plasmodium falciparum isolates. Mol Biochem Parasitol 27:23-34, 1988
17. Mayer DC, Mu JB, Feng X, Su XZ, Miller LH: Polymorphism in a Plasmodium falciparum erythrocyte-binding ligand changes its receptor specificity. J Exp Med 196:1523-1528, 2002
18. Topolska AE, Wang L, Black CG, Coppel RL: Merozoite cell biology, in Waters AP, Janse CJ (eds): Genomes and the Molecular Cell Biology of Malaria Parasites. Norfolk, UK, Horizon Scientific Press, 2004
19. Rayner JC, Vargas-Serrato E, Huber CS, Galinski MR, Barnwell JW: A Plasmodium falciparum homologue of Plasmodium vivax reticulocyte binding protein (PvRBP1) defines a trypsin-resistant erythrocyte invasion pathway. J Exp Med 194:1571-1581, 2001
20. Duraisingh MT, Triglia T, Ralph SA, Rayner JC, Barnwell JW, McFadden GI, et al: Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes. EMBO J 22:1047-1057, 2003
21. Horuk R, Chitnis CE, Darbonne WC, Colby TJ, Rybicki A, Hadley TJ, et al: A receptor for the malarial parasite Plasmodium vivax: The erythrocyte chemokine receptor. Science 261:1182-1184, 1993
22. Haynes JD, Dalton JP, Klotz FW, McGinniss MH, Hadley TJ, Hudson DE, et al: Receptor-like specificity of a Plasmodium knowlesi malarial protein that binds to Duffy antigen ligands on erythrocytes. J Exp Med 167:1873-1881, 1988
23. Miller LH, Mason SJ, Clyde DF, McGinniss MH: The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med 295:302-304, 1976
24. Sim BKL, Carter JM, Deal CD, Holland C, Haynes JD, Gross M: Plasmodium falciparum: Further characterization of a functionally active region of the merozoite invasion ligand EBA-175. Exp Parasitol 78:259-268, 1994
25. Dolan SA, Proctor JL, Alling DW, Okubo Y, Wellems TE, Miller LH: Glycophorin B as an EBA-175 independent Plasmodium falciparum receptor of human erythrocytes. Mol Biochem Parasitol 64:55-63, 1994
26. Gilberger TW, Thompson JK, Triglia T, Good RT, Duraisingh MT, Cowman AF: A novel EBA-175 paralogue from Plasmodium falciparum defines a new trypsin-resistant receptor on human erythrocytes. J Biol Chem 278:14480-14486, 2003
27. Mayer DC, Kaneko O, Hudson-Taylor DE, Reid ME, Miller LH: Characterization of a Plasmodium falciparum erythrocyte-binding protein paralogous to EBA-175. Proc Natl Acad Sci USA 98:5222-5227, 2001
28. Lobo CA, Rodriguez M, Reid M, Lustigman S: Glycophorin C is the receptor for the Plasmodium falciparum erythrocyte binding ligand PfEBP-2 (baebl). Blood 101:4628-4631, 2003
29. Duraisingh MT, Maier AG, Triglia T, Cowman AF: Erythrocyte-binding antigen 175 mediates invasion in Plasmodium falciparum utilizing sialic acid-dependent and -independent pathways. Proc Natl Acad Sci USA 100:4796-801, 2003
30. Goel VK, Li X, Chen H, Liu SC, Chishti AH, Oh SS: Band 3 is a host receptor binding merozoite surface protein 1 during the Plasmodium falciparum invasion of erythrocytes. Proc Natl Acad Sci USA 100:5164-5169, 2003
31. Li X, Chen H, Oo TH, Daly TM, Bergman LW, Liu S-C, et al: A co-ligand complex anchors Plasmodium falciparum merozoites to the erythrocyte invasion receptor band 3. J Biol Chem 279:5765-5771, 2004
32. Kushwaha A, Perween A, Mukund S, Majumdar S, Bhardwaj D, Chowdhury NR, et al: Amino terminus of Plasmodium falciparum acidic basic repeat antigen interacts with the erythrocyte membrane through band 3 protein. Mol Biochem Parasitol 122:45-54, 2002
33. Okoyeh JN, Pillai CR, Chitnis CE: Plasmodium falciparum field isolates commonly use erythrocyte invasion pathways that are independent of sialic acid residues of glycophorin A. Infect Immun 67:5784-5791, 1999
34. Haldar K, Mohandas N, Samuel BU, Harrison T, Hiller NL, Akompong T, et al: Protein and lipid trafficking induced in erythrocytes infected by malaria parasites. Cell Microbiol 4:383-395, 2002
35. Haldar K, Samuel BU, Mohandas N, Harrison T, Hiller NL: Transport mechanisms in Plasmodium-infected erythrocytes: Lipid rafts and a tubovesicular network. Int J Parasitol 31:1393-1401, 2001
36. Haldar K, Samuel BU, Mohandas N, Harrison T, Hiller NL: Erythrocytic vacuolar rafts induced by malaria parasites. Curr Opin Hematol 8:92-97, 2001
37. Samuel BU, Mohandas N, Harrison T, McManus H, Rosse W, Reid M, et al: The role of cholesterol and glycosylphosphatidylinositol-anchored proteins of erythrocyte rafts in regulating raft protein content and malarial infection. J Biol Chem 276:29319-29329, 2001
38. Harrison T, Samuel BU, Akompong T, Hamm H, Mohandas N, Lomasney JW, et al: Erythrocyte G protein-coupled receptor signaling in malarial infection. Science 301:1734-1736, 2003
39. Wang L, Mohandas N, Thomas A, Coppel RL: Detection of detergent-resistant membranes in asexual blood-stage parasites of Plasmodium falciparum. Mol Biochem Parasitol 130:149-153, 2003
40. Mattei D, Berzins K, Wahlgren M, Udomsangpetch R, Perlmann P, Griesser HW, et al: Cross-reactive antigenic determinants present on different Plasmodium falciparum blood-stage antigens. Parasite Immunol 11:15-29, 1989
41. Wahlin B, Sjolander A, Ahlborg N, Udomsangpetch R, Scherf A, Mattei D, et al: Involvement of Pf155/RESA and cross-reactive antigens in Plasmodium falciparum merozoite invasion in vitro. Infect Immun 60:443-449, 1992
42. Waller KL, Cooke BM, Nunomura W, Mohandas N, Coppel RL: Mapping the binding domains involved in the interaction between the Plasmodium falciparum knob-associated histidine-rich protein (KAHRP) and the cytoadherence ligand P falciparum erythrocyte membrane protein 1 (PfEMP1). J Biol Chem 274:23808-23813, 1999
43. Waller KL, Nunomura W, Cooke BM, Mohandas N, Coppel RL: Mapping the domains of the cytoadherence ligand Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) that bind to the knob-associated histidine-rich protein (KAHRP). Mol Biochem Parasitol 119:125-129, 2002
44. Przyborski JM, Wickert H, Krohne G, Lanzer M: Maurer's clefts - A novel secretory organelle? Mol Biochem Parasitol 132:17-26, 2003
45. Wickham ME, Rug M, Ralph SA, Klonis N, McFadden GI, Tilley L, et al: Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes. EMBO J 20:5636-5649, 2001
46. Crabb BS, Cooke BM, Reeder JC, Waller RF, Caruana SR, Davern KM, et al: Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 89:287-296, 1997
47. Waterkeyn JG, Wickham ME, Davern KM, Cooke BM, Coppel RL, Reeder JC, et al: Targeted mutagenesis of Plasmodium falciparum erythrocyte membrane protein 3 (PfEMP3) disrupts cytoadherence of malaria-infected red blood cells. EMBO J 19:2813-2823, 2000
48. Magowan C, Coppel RL, Lau AO, Moronne MM, Tchernia G, Mohandas N: Role of the Plasmodium falciparum mature-parasite-infected erythrocyte surface antigen (MESA/ PfEMP-2) in malarial infection of erythrocytes. Blood 86:3196-3204, 1995
49. Lustigman S, Anders RF, Brown GV, Coppel RL: The mature-parasite-infected erythrocyte surface antigen (MESA) of Plasmodium falciparum associates with the erythrocyte membrane skeletal protein, band 4.1. Mol Biochem Parasitol 38:261-270, 1990
50. Foley M, Corcoran L, Tilley L, Anders R: Plasmodium falciparum: Mapping the membrane-binding domain in the ring-infected erythrocyte surface antigen. Exp Parasitol 79:340-350, 1994
51. Kilejian A, Rashid MA, Aikawa M, Aji T, Yang YF: Selective association of a fragment of the knob protein with spectrin, actin and the red cell membrane. Mol Biochem Parasitol 44:175-182, 1991
52. Waller KL, Nunomura W, An X, Cooke BM, Mohandas N, Coppel RL: Mature parasite-infected erythrocyte surface antigen (MESA) of Plasmodium falciparum binds to the 30-kDa domain of protein 4.1 in malaria-infected red blood cells. Blood 102:1911-1914, 2003
53. Manno S, Takakuwa Y, Nagao K, Mohandas N: Modulation of erythrocyte membrane mechanical function by beta-spectrin phosphorylation and dephosphorylation. J Biol Chem 270:5659-5665, 1995
54. Yuthavong Y, Limpaiboon T: The relationship of phosphorylation of membrane proteins with the osmotic fragility and filterability of Plasmodium berghei-infected mouse erythrocytes. Biochim Biophys Acta 929:278-287, 1987
55. Murray MC, Perkins ME: Phosphorylation of erythrocyte membrane and cytoskeleton proteins in cells infected with Plasmodium falciparum. Mol Biochem Parasitol 34:229-236, 1989
56. Ling E, Danilov YN, Cohen CM: Modulation of red cell band 4.1 function by cAMP-dependent kinase and protein kinase C phosphorylation. J Biol Chem 263:2209-2216, 1988
57. Chishti AH, Maalouf GJ, Marfatia S, Palek J, Wang W, Fisher D, et al: Phosphorylation of protein 4.1 in Plasmodium falciparum-infected human red blood cells. Blood 83:3339-3345, 1994
58. Kun JF, Hibbs AR, Saul A, McColl DJ, Coppel RL, Anders RF: A putative Plasmodium falciparum exported serine/threonine protein kinase. Mol Biochem Parasitol 85:41-51, 1997
59. Dua M, Raphael P, Sijwali PS, Rosenthal PJ, Hanspal M: Recombinant falcipain-2 cleaves erythrocyte membrane ankyrin and protein 4.1. Mol Biochem Parasitol 116:95-99, 2001
60. Raphael P, Takakuwa Y, Manno S, Liu SC, Chishti AH, Hanspal M: A cysteine protease activity from Plasmodium falciparum cleaves human erythrocyte ankyrin. Mol Biochem Parasitol 110:259-272, 2000
61. Le Bonniec S, Deregnaucourt C, Redeker V, Banerjee R, Grellier P, Goldberg DE, et al: Plasmepsin II, an acidic hemoglobinase from the Plasmodium falciparum food vacuole, is active at neutral pH on the host erythrocyte membrane skeleton. J Biol Chem 274:14218-14223, 1999
62. Suwanarusk R, Cooke BM, Dondorp AM, Silamut K, Sattabongkot J, White NJ, et al: The deformability of red blood cells parasitized by Plasmodium falciparum and P. vivax. J Infect Dis 189:190-194, 2004
63. Barnwell JW, Ingravallo P, Galinski MR, Matsumoto Y, Aikawa M: Plasmodium vivax: Malarial proteins associated with the membrane-bound caveola-vesicle complexes and cytoplasmic cleft structures of infected erythrocytes. Exp Parasitol 70:85-99, 1990
64. Taraschi TF, O'Donnell M, Martinez S, Schneider T, Trelka D, Fowler VM, et al: Generation of an erythrocyte vesicle transport system by Plasmodium falciparum malaria parasites. Blood 102:3420-3426, 2003
65. Haldar K: Intracellular trafficking in Plasmodium-infected erythrocytes. Curr Opin Microbiol 1:466-471, 1998
66. Lauer SA, Rathod PK, Ghori N, Haldar K: A membrane network for nutrient import in red cells infected with the malaria parasite. Science 276:1122-1125, 1997
67. Waller RF, Reed MB, Cowman AF, McFadden GI: Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J 19:1794-1802, 2000
68. Bozdech Z, VanWye J, Haldar K, Schurr E: The human malaria parasite Plasmodium falciparum exports the ATP-binding cassette protein PFGCN20 to membrane structures in the host red blood cell. Mol Biochem Parasitol 97:81-95, 1998
69. Hinterberg K, Scherf A, Gysin J, Toyoshima T, Aikawa M, Mazie JC, et al: Plasmodium falciparum: The Pf332 antigen is secreted from the parasite by a brefeldin A-dependent pathway and is translocated to the erythrocyte membrane via the Maurer's clefts. Exp Parasitol 79:279-291, 1994
70. Kriek N, Tilley L, Horrocks P, Pinches R, Elford BC, Ferguson DJP, et al: Characterisation 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, 2003
71. a. Haeggstrom M, Kironde F, Berzins K, Chen Q, Wahlgren M, Fernandez V: Common trafficking pathway for variant antigens destined for the surface of the Plasmodium falciparum-infected erythrocyte. Mol Biochem Parasitol 133:1-14, 2004
72. b. Blisnick T, Morales-Betoulle ME, Barale J-C, Uzureau P, Berry L, Desroses S, et al: Pfsbp1, a Maurer's cleft Plasmodium falciparum protein, is associated with the erythrocyte skeleton. Mol Biochem Parasitol 111:107-121, 2000
73. Atkinson CT, Aikawa M, Perry G, Fujino T, Bennett V, Davidson EA, et al: Ultrastructural localization of erythrocyte cytoskeletal and integral membrane proteins in Plasmodium falciparum-infected erythrocytes. Eur J Cell Biol 45:192-199, 1988
74. Etzion Z, Perkins ME: Localization of a parasite encoded protein to erythrocyte cytoplasmic vesicles of Plasmodium falciparum-infected cells. Eur J Cell Biol 48:174-179, 1989
75. Cooke BM, Coppel RL: Cytoadhesion and falciparum malaria - Going with the flow. Parasitol Today 11:282-287, 1995
76. Beeson JG, Brown GV: Pathogenesis of Plasmodium falciparum malaria: The roles of parasite adhesion and antigenic variation. Cell Mol Life Sci 59:258-271, 2002
77. Cooke B, Coppel R, Wahlgren M: Falciparum malaria: Sticking up, standing out and out-standing. Parasitol Today 16:416-420, 2000
78. Baruch DI, Rogerson SJ, Cooke BM: Asexual blood stages of malaria antigens: Cytoadherence. Chem Immunol 80:144-162, 2002
79. Ockenhouse CF, Klotz FW, Tandon NN, Jamieson GA: Sequestrin, a CD36 recognition protein on Plasmodium falciparum malaria-infected erythrocytes identified by anti-idiotype antibodies. Proc Natl Acad Sci USA 88:3175-3179, 1991
80. Fernandez V, Hommel M, Chen Q, Hagblom P, Wahlgren M: Small, clonally variant antigens expressed on the surface of the Plasmodium falciparum-infected erythrocyte are encoded by the rif gene family and are the target of human immune responses. J Exp Med 190:1393-1404, 1999
81. Udomsangpetch R, Aikawa M, Berzins K, Wahlgren M, Perlmann P: Cytoadherence of knobless Plasmodium falciparum-infected erythrocytes and its inhibition by a human monoclonal antibody. Nature 338:763-765, 1989
82. Trenholme KR, Gardiner DL, Holt DC, Thomas EA, Cowman AF, Kemp DJ: clag9: A cytoadherence gene in Plasmodium falciparum essential for binding of parasitized erythrocytes to CD36. Proc Natl Acad Sci USA 97:4029-4033, 2000
83. Kaneko O, Tsuboi T, Ling IT, Howell S, Shirano M, Tachibana M, et al: 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, 2001
84. Baruch DI, Ma XC, Singh HB, Bi X, Pasloske BL, Howard RJ: Identification of a region of PfEMP1 that mediates adherence of Plasmodium falciparum infected erythrocytes to CD36: Conserved function with variant sequence. Blood 90:3766-3775, 1997
85. Cooke BM, Nicoll CL, Baruch DI, Coppel RL: A recombinant peptide based on PfEMP-1 blocks and reverses adhesion of malaria-infected red blood cells to CD36 under flow. Mol Microbiol 30:83-90, 1998
86. Treutiger CJ, Heddini A, Fernandez V, Muller WA, Wahlgren M: PECAM-1/CD31, an endothelial receptor for binding Plasmodium falciparum-infected erythrocytes. Nat Med 3:1405-1408, 1997
87. Glenister FK, Coppel RL, Cowman AF, Mohandas N, Cooke BM: Contribution of parasite proteins to altered mechanical properties of malaria-infected red blood cells. Blood 99:1060-1063, 2002
88. Clough B, Atilola FA, Pasvoi G: The role of rosetting in the multiplication of Plasmodium falciparum: Rosette formation neither enhances nor targets parasite invasion into uninfected red cells. Br J Haematol 100:99-104, 1998
89. Cooke BM, Morris-Jones S, Greenwood BM, Nash GB: Adhesion of parasitized red blood cells to cultured endothelial cells: A flow-based study of isolates from Gambian children with falciparum malaria. Parasitology 107:359-368, 1993
90. Kaul DK, Roth E Jr, Nagel RL, Howard RJ, Handunnetti SM: Rosetting of Plasmodium falciparum-infected red blood cells with uninfected red blood cells enhances microvascular obstruction under flow conditions. Blood 78:812-819, 1991
91. Moulds JM, Kassambara L, Middleton JJ, Baby M, Sagara I, Guindo A, et al: Identification of complement receptor one (CR1) polymorphisms in west Africa. Genes Immun 1:325-329, 2000
92. a. Cockburn IA, Mackinnon MJ, O'Donnell A, Allen SJ, Moulds JM, Baisor M, et al: A human complement receptor 1 polymorphism that reduces Plasmodium falciparum rosetting confers protection against severe malaria. Proc Natl Acad Sci USA 101:272-277, 2004
93. Somner EA, Black J, Pasvol G: Multiple human serum components act as bridging molecules in rosette formation by Plasmodium falciparum-infected erythrocytes. Blood 95:674-682, 2000
94. Crandall I, Collins WE, Gysin J, Sherman IW: Synthetic peptides based on motifs present in human band 3 protein inhibit cytoadherence/sequestration of the malaria parasite Plasmodium falciparum. Proc Natl Acad Sci USA 90:4703-4707, 1993
95. Eda S, Lawler J, Sherman IW: Plasmodium falciparum-infected erythrocyte adhesion to the type 3 repeat domain of thrombospondin-1 is mediated by a modified band 3 protein. Mol Biochem Parasitol 100:195-205, 1999
96. Thevenin BJM, Crandall I, Ballas SK, Sherman IW, Shohet SB: Band 3 peptides block the adherence of sickle cells to endothelial cells in vitro. Blood 90:4172-4179, 1997
97. Menendez C, Fleming AF, Alonso PL: Malaria-related anaemia. Parasitol Today 16:469-476, 2000
98. Wickramasinghe SN, Abdalla SH: Blood and bone marrow changes in malaria. Baillieres Best Pract Res Clin Haematol 13:277-299, 2000
99. Dondorp AM, Kager PA, Vreeken J, White NJ: Abnormal blood flow and red blood cell deformability in severe malaria. Parasitol Today 16:228-232, 2000
100. Joshi P, Alam A, Chandra R, Puri SK, Gupta CM: Possible basis for membrane changes in nonparasitized erythrocytes of malaria-infected animals. Biochim Biophys Acta 862:220-222, 1986
101. Waitumbi JN, Opollo MO, Muga RO, Misore AO, Stoute JA: Red cell surface changes and erythrophagocytosis in children with severe Plasmodium falciparum anemia. Blood 95:1481-1486, 2000
102. Pasvol G, Anstee D, Tanner MJ: Glycophorin C and the invasion of red cells by Plasmodium falciparum. Lancet 1:907-908, 1984
103. Maier AG, Duraisingh MT, Reeder JC, Patel SS, Kazura JW, Zimmerman PA, et al: Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nat Med 9:87-92, 2003
104. Fairhurst RM, Fujioka H, Hayton K, Collins KF, Wellems TE: Aberrant development of Plasmodium falciparum in hemoglobin CC red cells: Implications for the malaria protective effect of the homozygous state. Blood 101:3309-3315, 2003
105. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, et al: Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511, 2002
106. Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, Haynes JD, et al: Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301:1503-1508, 2003
107. Leech JH, Barnwell JW, Miller LH, Howard RJ: Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes. J Exp Med 159:1567-1575, 1984
108. Howard RF, Stanley HA, Reese RT: Characterization of a high-molecular-weight phosphoprotein synthesized by the human malarial parasite Plasmodium falciparum. Gene 64:65-75, 1988
109. Baruch DI, Pasloske BL, Singh HB, Bi XH, Ma XC, Feldman M, et al: Cloning the P. falciparum gene encoding PfEMP-1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82:77-87, 1995
110. Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE, Peterson DS, et al: Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82:101-110, 1995
111. Su XZ, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, Peterson DS, et al: The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82:89-100, 1995
112. Wickert H, Wissing F, Andrews KT, Stich A, Krohne G, Lanzer M: Evidence for trafficking of PfEMP1 to the surface of P. falciparum-infected erythrocytes via a complex membrane network. Eur J Cell Biol 82:271-284, 2003
113. Newbold CI: Antigenic variation in Plasmodium falciparum: Mechanisms and consequences. Curr Opin Microbiol 2:420-425, 1999
114. Robinson BA, Welch TL, Smith JD: Widespread functional specialization of Plasmodium falciparum erythrocyte membrane protein 1 family members to bind CD36 analysed across a parasite genome. Mol Microbiol 47:1265-1278, 2003
115. Cheng Q, Cloonan N, Fischer K, Thompson J, Waine G, Lanzer M, et al: Stevor and rif are Plasmodium falciparum-multicopy gene families which potentially encode variant antigens. Mol Biochem Parasitol 97:161-176, 1998
116. Kyes SA, Rowe JA, Kriek N, Newbold CI: Rifins: A second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum. Proc Natl Acad Sci USA 96:9333-9338, 1999
117. Abdel-Latif MS, Khattab A, Lindenthal C, Kremsner PG, Klinkert MQ: Recognition of variant Rifin antigens by human antibodies induced during natural Plasmodium falciparum-infections. Infect Immun 70:7013-7021, 2002
118. Kaviratne M, Khan SM, Jarra W, Preiser PR: Small variant STEVOR antigen is uniquely located within Maurer's clefts in Plasmodium falciparum-infected red blood cells. Eukaryot Cell 1:926-935, 2002
119. Coppel RL, Cowman AF, Anders RF, Bianco AE, Saint RB, Lingelbach KR, et al: Immune sera recognize on erythrocytes Plasmodium falciparumantigen composed of repeated amino acid sequences. Nature 310:789-792, 1984
120. Perlmann H, Berzins K, Wahlgren M, Carlsson J, Bjorkman A, Patarroyo ME, et al: Antibodies in malarial sera to parasite antigens in the membrane of erythrocytes infected with early asexual stages of Plasmodium falciparum. J Exp Med 159:1686-1704, 1984
121. Favaloro JM, Coppel RL, Corcoran LM, Foote SJ, Brown GV, Anders RF, et al: Structure of the RESA gene of Plasmodium falciparum. Nucleic Acids Res 14:8265-8277, 1986
122. Foley M, Murray LJ, Anders RF: The ring-infected erythrocyte surface antigen protein of Plasmodium falciparum is phosphorylated upon association with the host cell membrane. Mol Biochem Parasitol 38:69-75, 1990
123. Foley M, Tilley L, Sawyer WH, Anders RF: The ring-infected erythrocyte surface antigen of Plasmodium falciparum associates with spectrin in the erythrocyte membrane. Mol Biochem Parasitol 46:137-147, 1991
124. Coppel RL, Lustigman S, Murray L, Anders RF: MESA is a Plasmodium falciparum phosphoprotein associated with the erythrocyte membrane skeleton. Mol Biochem Parasitol 31:223-231, 1988
125. Coppel RL: Repeat structures in a Plasmodium falciparum protein (MESA) that binds human erythrocyte protein 4.1. Mol Biochem Parasitol 50:335-347, 1992
126. Kilejian A: Characterization of a protein correlated with the production of knob-like protrusions on membranes of erythrocytes infected with Plasmodium falciparum. Proc Natl Acad Sci USA 76:4650-4653, 1979
127. Magowan C, Nunomura W, Waller KL, Yeung J, Liang J, Van Dort H, et al: Plasmodium falciparum histidine-rich protein 1 associates with the band 3 binding domain of ankyrin in the infected red cell membrane. Biochim Biophys Acta 1502:461-470, 2000
128. Oh SS, Voigt S, Fisher D, Yi SJ, LeRoy PJ, Derick LH, et al: Plasmodium falciparum erythrocyte membrane protein 1 is anchored to the actin-spectrin junction and knob-associated histidine-rich protein in the erythrocyte skeleton. Mol Biochem Parasitol 108:237-247, 2000
129. Pasloske BL, Baruch DI, van Schravendijk MR, Handunnetti SM, Aikawa M, Fujioka H, et al: Cloning and characterization of a Plasmodium falciparum gene encoding a novel high-molecular weight host membrane-associated protein, PfEMP3. Mol Biochem Parasitol 59:59-72, 1993
130. Stahl HD, Crewther PE, Anders RF, Kemp DJ: Structure of the FIRA gene of Plasmodium falciparum. Mol Biol Med 4:199-211, 1987
131. Spycher C, Klonis N, Spielmann T, Kump E, Steiger S, Tilley L, et al: MAHRP-1, a novel Plasmodium falciparum histidinerich protein, binds ferriprotoporphyrin IX and loocalizes to the Maurer's clefts. J Biol Chem 278:35373-35383, 2003
132. Albano FR, Berman A, La Greca N, Hibbs AR, Wickham M, Foley M, et al: A homologue of Sarlp localises to a novel trafficking pathway in malaria-infected erythrocytes. Eur J Cell Biol 78:453-462, 1999
133. de Castro FA, Ward GE, Jambou R, Attal G, Mayau V, Jaureguiberry G, et al: Identification of a family of Rab G-proteins in Plasmodium falciparum and a detailed characterisation of pfrab6. Mol Biochem Parasitol 80:77-88, 1996
134. Chen Q, Heddini A, Barragan A, Fernandez V, Pearce SF, Wahlgren M: The semiconserved head structure of Plasmodium falciparum erythrocyte membrane protein 1 mediates binding to multiple independent host receptors. J Exp Med 192:1-10, 2000
135. Baruch DI, Gormely JA, Ma C, Howard RJ, Pasloske BL: Plasmodium falciparumerythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule 1. Proc Natl Acad Sci USA 93:3497-3502, 1996
136. Oquendo P, Hundt E, Lawler J, Seed B: CD36 directly mediates cytoadherence of Plasmodium falciparum parasitized erythrocytes. Cell 58:95-101, 1989
137. Cooke BM, Berendt AR, Craig AG, MacGregor J, Newbold CI, Nash GB: Rolling and stationary cytoadhesion of red blood cells parasitized by Plasmodium falciparum: Separate roles for ICAM-1, CD36 and thrombospondin. Br J Haematol 87:162-170, 1994
138. Cooke BM, Morris-Jones S, Greenwood BM, Nash GB: Mechanisms of cytoadhesion of flowing, parasitized red blood cells from Gambian children with falciparum malaria. Am J Trop Med Hyg 53:29-35, 1995
139. Baruch DI, Ma XC, Pasloske B, Howard RJ, Miller LH: CD36 peptides that block cytoadherence define the CD36 binding region for Plasmodium falciparum-infected erythrocytes. Blood 94:2121-2127, 1999
140. Yipp BG, Baruch DI, Brady C, Murray AG, Looareesuwan S, Kubes P, et al: Recombinant PfEMP1 peptide inhibits and reverses cytoadherence of clinical Plasmodium falciparum isolates in vivo. Blood 101:331-337, 2003
141. Handunnetti SM, van Schravendijk MR, Hasler T, Barnwell JW, Greenwalt DE, Howard RJ: Involvement of CD36 on eryihrocytes as a rosetting receptor for Plasmodium falciparum-infected erythrocytes. Blood 80:2097-2104, 1992
142. Berendt AR, McDowall A, Craig AG, Bates PA, Sternberg MJ, Marsh K, et al: The binding site on ICAM-1 for Plasmodium falciparum-infected erythrocytes overlaps, but is distinct from, the LFA-1-binding site. Cell 68:71-81, 1992
143. Berendt AR, Simmons DL, Tansey J, Newbold CI, Marsh K: Intercellular adhesion molecule-1 is an endothelial cell adhesion receptor for Plasmodium falciparum. Nature 341:57-59, 1989
144. Smith JD, Craig AG, Kriek N, Hudson-Taylor D, Kyes S, Fagen T, et al: Identification of a Plasmodium falciparum intercellular adhesion molecule-1 binding domain: A parasite adhesion trait implicated in cerebral malaria. Proc Natl Acad Sci USA 97:1766-1771, 2000
145. Craig A, Fernandez-Reyes D, Mesri M, McDowall A, Altieri DC, Hogg N, et al: A functional analysis of a natural variant of intercellular adhesion molecule-1 (ICAM-1Kilifi). Hum Mol Genet 9:525-530, 2000
146. Gray C, McCormick C, Turner G, Craig A: ICAM-1 can play a major role in mediating P. falciparum adhesion to endothelium under flow. Mol Biochem Parasitol 128:187-193, 2003
147. Gray C, Craig A: Fibrinogen binding to intercellular adhesion molecule 1: Implications for Plasmodium falciparum adhesion. Infect Immun 70:3962-3964, 2002
148. Roberts DD, SherwoodJA, Spitalnik SL, Panton LJ, Howard RJ, Dixit VM, et al: Thrombospondin binds falciparum malaria parasitized erythrocytes and may mediate cytoadherence. Nature 318:64-66, 1985
149. Sherwood JA, Roberts DD, Marsh K, Harvey EB, Spitalnik SL, Miller LH, et al: Thrombospondin binding by parasitized erythrocyte isolates in falciparum malaria. Am J Trop Med Hyg 36:228-233, 1987
150. Newbold C, Warn P, Black G, Berendt A, Craig A, Snow B, et al: Receptor-specific adhesion and clinical disease in Plasmodium falciparum. Am J Trop Med Hyg 57:389-398, 1997
151. Rogerson SJ, Chaiyaroj SC, Ng K, Reeder JC, Brown GV: Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparum-infected erythrocytes. J Exp Med 182:15-20, 1995
152. Fried M, Duffy PE: Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272:1502-1504, 1996
153. Buffet PA, Gamain B, Scheidig C, Baruch D, Smith JD, Hemandez-Rivas R, et al: Plasmodium falciparum domain mediating adhesion to chondroitin sulfate A: A receptor for human placental infection. Proc Natl Acad Sci USA 96:12743-12748, 1999
154. Reeder JC, Cowman AF, Davern KM, BeesonJG, Thompson JK, Rogerson SJ, et al: The adhesion of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A is mediated by P. falciparum erythrocyte membrane protein 1. Proc Natl Acad Sci USA 96:5198-5202, 1999
155. Maubert B, Fievet N, Tami G, Boudin C, Deloron P: Cytoadherence of Plasmodium falciparum-infected erythrocytes in the human placenta. Parasite Immunol 22:191-199, 2000
156. Beeson JG, Rogerson SJ, Cooke BM, Reeder JC, Chai W, Lawson AM, et al: Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nat Med 6:86-90, 2000
157. Rowe A, Moulds JM, Newbold CI, Miller LH: P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388:292-295, 1997
158. Rowe JA, Rogerson SJ, Raza A, Moulds JM, Kazatchkine MD, Marsh K, et al: Mapping of the region of complement receptor (CR) 1 required for Plasmodium falciparum rosetting and demonstration of the importance of CR1 in rosetting in field isolates. J Immunol 165:6341-6346, 2000
159. Zimmerman PA, Fitness J, Moulds JM, McNamara DT, Kasehagen LJ, Rowe JA, et al: CR1 Knops blood group alleles are not associated with severe malaria in the Gambia. Genes Immun 4:368-373, 2003
160. Chen Q, Barragan A, Fernandez V, Sundstrom A, Schlichtherle M, Sahlen A, et al: Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. J Exp Med 187:15-23, 1998
161. Barragan A, Fernandez V, Chen Q, von Euler A, Wahlgren M, Spillmann D: The Duffy-binding-like domain 1 of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) is a heparan sulfate ligand that requires 12 mers for binding. Blood 95:3594-3599, 2000
162. Vogt AM, Barragan A, Chen Q, Kironde F, Spillmann D, Wahlgren M: Heparan sulfate on endothelial cells mediates the binding of Plasmodium falciparum-infected erythrocytes via the DBL1a domain of PfEMP1. Blood 101:2405-2411, 2003
163. Barragan A, Kremsner PG, Wahlgren M, Carlson J: Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infect Immun 68:2971-2975, 2000
164. Carlson J, Wahlgren M: Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. J Exp Med 176:1311-1317, 1992
165. Ho M, Schollaardt T, Niu X, Looareesuwan S, Patel KD, Kubes P: Characterization of Plasmodium falciparum-infected erythrocyte and P-selectin interaction under flow conditions. Blood 91:4803-4809, 1998
166. Senczuk AM, Reeder JC, Kosmala MM, Ho M: Plasmodium falciparum erythrocyte membrane protein 1 functions as a ligand for P-selectin. Blood 98:3132-3135, 2001
167. Ockenhouse CF, Tegoshi T, Maeno Y, Benjamin C, Ho M, Kan KE, et al: Human vascular endothelial cell adhesion receptors for Plasmodium falciparum-infected erythrocytes: Roles for endothelial leukocyte adhesion molecule 1 and vascular cell adhesion molecule 1. J Exp Med 176:1183-1189, 1992
168. Siano JP, Grady KK, Millet P, Wick TM: Short report: Plasmodium falciparum: Cytoadherence to a v b3 on human microvascular endothelial cells. Am J Trop Med Hyg 59:77-99, 1998
169. Barnwell JW, Nichols ME, Rubinstein P: In vitro evaluation of the role of the Duffy blood group in erythrocyte invasion by Plasmodium vivax. J Exp Med 169:1795-802, 1989
170. Pasvol G, Wainscoat JS, Weatherall DJ: Erythrocytes deficiency in glycophorin resist invasion by the malarial parasite Plasmodium falciparum. Nature 297:64-66, 1982
171. Pasvol G, Wilson RJ: The interaction of malaria parasites with red blood cells. Br Med Bull 38:133-140, 1982
172. Bunyaratvej A, Butthep P, Kaewkettong P, Yuthavong Y: Malaria protection in hereditary ovalocytosis: relation to red cell deformability, red cell parameters and degree of ovalocytosis. Southeast Asian J Trop Med Public Health 28:38-42, 1997(suppl 3)
173. Hadley TJ, Miller LH: Invasion of erythrocytes by malaria parasites: Erythrocyte ligands and parasite receptors. Prog Allergy 41:49-71, 1988
174. Facer CA: Erythrocytes carrying mutations in spectrin and protein 4.1 show differing sensitivities to invasion by Plasmodium falciparum. Parasitol Res 81:52-57, 1995
175. Pasvol G: The interaction between sickle haemoglobin and the malarial parasite Plasmodium falciparum. Trans R Soc Trop Med Hyg 74:701-705, 1980
176. Friedman MJ: Ultrastructural damage to the malaria parasite in the sickled cell. J Protozool 26:195-199, 1979
177. Chotivanich K, Udomsangpetch R, Pattanapanyasat K, Chierakul W, Simpson J, Looareesuwan S, et al: Hemoglobin E: A balanced polymorphism protective against high parasitemias and thus severe P falciparum malaria. Blood 100:1172-1176, 2002
178. Nagel RL, Raventos-Suarez C, Fabry ME, Tanowitz H, Sicard D, Labie D: Impairment of the growth of Plasmodium falciparum in HbEE erythrocytes. J Clin Invest 68:303-305, 1981
179. Friedman MJ, Roth EF, Nagel RL, Trager W: The role of hemoglobins C, S, and Nbalt in the inhibition of malaria parasite development in vitro. Am J Trop Med Hyg 28:777-780, 1979
180. Luzzi GA, Merry AH, Newbold CI, Marsh K, Pasvol G: Protection by alpha-thalassaemia against Plasmodium falciparum malaria: Modified surface antigen expression rather than impaired growth or cytoadherence. Immunol Lett 30:233-240, 1991
181. Flint J, Hill AV, Bowden DK, Oppenheimer SJ, Sill PR, Serjeantson SW, et al: High frequencies of alpha-thalassaemia are the result of natural selection by malaria. Nature 321:744-750, 1986
182. Udomsangpetch R, Sueblinvong T, Pattanapanyasat K, Dharmkrong-at A, Kittikalayawong A, Webster HK: Alteration in cytoadherence and rosetting of Plasmodium falciparum-infected thalassemic red blood cells. Blood 82:3752-3759, 1993
183. Carlson J, Nash GB, Gabutti V, al-Yaman F, Wahlgren M: Natural protection against severe Plasmodium falciparum malaria due to impaired rosette formation. Blood 84:3909-3914, 1994
184. Willcox M, Bjorkman A, Brohult J, Pehrson PO, Rombo L, Bengtsson E: A case-control study in northern Liberia of Plasmodium falciparum malaria in haemoglobin S and beta-thalassaemia traits. Ann Trop Med Parasitol 77:239-246, 1983
185. Ifediba TC, Stern A, Ibrahim A, Rieder RF: Plasmodium falciparum in vitro: Diminished growth in hemoglobin H disease erythrocytes. Blood 65:452-455, 1984
186. Friedman MJ: Oxidant damage mediates variant red cell resistance to malaria. Nature 280:245-247, 1979