Immune effector mechanisms in malaria

Parasite Immunology

Volumn 28, Issue 1-2, 2006, Pages 51-60

  Marsh, K ^a,b   Kinyanjui, S ^a,c  

^a CGMRC KEMRI   (Kenya)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Immunity; Malaria; Vaccines

Indexed keywords

INTERLEUKIN 12; MEROZOITE SURFACE PROTEIN 1; MEROZOITE SURFACE PROTEIN 2; MALARIA VACCINE; PARASITE ANTIGEN;

ALLELE; COST BENEFIT ANALYSIS; DISEASE PREDISPOSITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTE; GENE TARGETING; GENETIC POLYMORPHISM; HUMAN; IMMUNE RESPONSE; MALARIA; METHODOLOGY; MORTALITY; NONHUMAN; POPULATION RESEARCH; PRIORITY JOURNAL; REVIEW; SPOROZOITE; ADOLESCENT; ADULT; ANIMAL; ANTIGENIC VARIATION; CHILD; IMMUNOLOGY; INFANT; MALARIA FALCIPARUM; MIDDLE AGED; PARASITOLOGY; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD;

ADOLESCENT; ADULT; ANIMALS; ANTIGENIC VARIATION; ANTIGENS, PROTOZOAN; CHILD; CHILD, PRESCHOOL; ERYTHROCYTES; HUMANS; INFANT; MALARIA VACCINES; MALARIA, FALCIPARUM; MIDDLE AGED; PLASMODIUM FALCIPARUM; POLYMORPHISM, GENETIC;

EID: 33644871833     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2006.00808.x     Document Type: Review

References (124)

1. Marsh K Malaria - a neglected disease? Parasitology 1992 104 Suppl. S53 S69
2. Gupta S Snow RW Donnelly CA et al. Immunity to non-cerebral severe malaria is acquired after one or two infections Nat Med 1999 5 340 343
3. Bull PC Lowe BS Kaleli N et al. Plasmodium falciparum infections are associated with agglutinating antibodies to parasite-infected erythrocyte surface antigens among healthy Kenyan children J Infect Dis 2002 185 1688 1691
4. Kinyanjui SM Mwangi T Bull PC et al. Protection against clinical malaria by heterologous immunoglobulin G antibodies against malaria-infected erythrocyte variant surface antigens requires interaction with asymptomatic infections J Infect Dis 2004 190 1527 1533
5. Polley SD Mwangi T Kocken CH et al. Human antibodies to recombinant protein constructs of Plasmodium falciparum Apical Membrane Antigen 1 (AMA1) and their associations with protection from malaria Vaccine 2004 23 718 728
6. Collins WE Jeffery GM A retrospective examination of mosquito infection on humans infected with Plasmodium falciparum Am J Trop Med Hyg 2003 68 366 371
7. Day KP Marsh K Naturally acquired immunity to Plasmodium falciparum Immunol Today 1991 12 A68 A71
8. Anders RF McColl DJ Coppel RL Molecular variation in Plasmodium falciparum: polymorphic antigens of asexual erythrocytic stages Acta Trop 1993 53 239 253
9. Kyes S Horrocks P Newbold C Antigenic variation at the infected red cell surface in malaria Annu Rev Microbiol 2001 55 673 707
10. Sokhna CS Rogier C Dieye A et al. Host factors affecting the delay of reappearance of Plasmodium falciparum after radical treatment among a semi-immune population exposed to intense perennial transmission Am J Trop Med Hyg 2000 62 266 270
11. Owusu-Agyei S Koram KA Baird JK et al. Incidence of symptomatic and asymptomatic Plasmodium falciparum infection following curative therapy in adult residents of northern Ghana Am J Trop Med Hyg 2001 65 197 203
12. Nardin E Zavala F Nussenzweig V et al. Pre-erythrocytic malaria vaccine: mechanisms of protective immunity and human vaccine trials Parasitologia 1999 41 397 402
13. Beier JC Onyango FK Koros JK et al. Quantitation of malaria sporozoites transmitted in vitro during salivation by wild Afrotropical Anopheles Med Vet Entomol 1991 5 71 79
14. Hoffman SL Goh LM Luke TC et al. Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites J Infect Dis 2002 185 1155 1164
15. Scheller LF Azad AF Maintenance of protective immunity against malaria by persistent hepatic parasites derived from irradiated sporozoites Proc Natl Acad Sci USA 1995 92 4066 4068
16. Leiriao P Mota MM Rodriguez A Apoptotic Plasmodium-infected hepatocytes provide antigens to liver dendritic cells J Infect Dis 2005 191 1576 1581
17. James E Apoptosis: key to the attenuated malaria vaccine? J Infect Dis 2005 191 1573 1575
18. Esposito F Lombardi S Modiano D et al. Prevalence and levels of antibodies to the circumsporozoite protein of Plasmodium falciparum in an endemic area and their relationship to resistance against malaria infection Trans R Soc Trop Med Hyg 1988 82 827 832
19. Calle JM Nardin EH Clavijo P et al. Recognition of different domains of the Plasmodium falciparum CS protein by the sera of naturally infected individuals compared with those of sporozoite-immunized volunteers J Immunol 1992 149 2695 2701
20. John CC Zickafoose JS Sumba PO et al. Antibodies to the Plasmodium falciparum antigens circumsporozoite protein, thrombospondin-related adhesive protein, and liver-stage antigen 1 vary by ages of subjects and by season in a highland area of Kenya Infect Immun 2003 71 4320 4325
21. Pasquetto V Fidock DA Gras H et al. Plasmodium falciparum sporozoite invasion is inhibited by naturally acquired or experimentally induced polyclonal antibodies to the STARP antigen Eur J Immunol 1997 27 2502 2513
22. Silvie O Franetich JF Charrin S et al. A role for apical membrane antigen 1 during invasion of hepatocytes by Plasmodium falciparum sporozoites J Biol Chem 2004 279 9490 9496
23. Schwenk R Asher LV Chalom I et al. Opsonization by antigen-specific antibodies as a mechanism of protective immunity induced by Plasmodium falciparum circumsporozoite protein-based vaccine Parasite Immunol 2003 25 17 25
24. Tsuji M Zavala F T cells as mediators of protective immunity against liver stages of Plasmodium Trends Parasitol 2003 19 88 93
25. Doolan DL Hoffman SL The complexity of protective immunity against liver-stage malaria J Immunol 2000 165 1453 1462
26. Reece WH Pinder M Gothard PK et al. A CD4(+) T-cell immune response to a conserved epitope in the circumsporozoite protein correlates with protection from natural Plasmodium falciparum infection and disease Nat Med 2004 10 406 410
27. Holder AA Proteins on the surface of the malaria parasite and cell invasion Parasitology 1994 108 Suppl. S5 S18
28. Black CG Wu T Wang L et al. Merozoite surface protein 8 of Plasmodium falciparum contains two epidermal growth factor-like domains Mol Biochem Parasitol 2001 114 217 226
29. Mello K Daly TM Morrisey J et al. A multigene family that interacts with the amino terminus of plasmodium MSP-1 identified using the yeast two-hybrid system Eukaryot Cell 2002 1 915 925
30. Li X Chen H Oo TH et al. A co-ligand complex anchors Plasmodium falciparum merozoites to the erythrocyte invasion receptor band 3 J Biol Chem 2004 279 5765 5771
31. Mitchell GH Thomas AW Margos G et al. Apical membrane antigen 1, a major malaria vaccine candidate, mediates the close attachment of invasive merozoites to host red blood cells Infect Immun 2004 72 154 158
32. Triglia T Healer J Caruana SR et al. Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species Mol Microbiol 2000 38 706 718
33. Adams JH Blair PL Kaneko O et al. An expanding ebl family of Plasmodium falciparum Trends Parasitol 2001 17 297 299
34. Taylor HM Grainger M Holder AA Variation in the expression of a Plasmodium falciparum protein family implicated in erythrocyte invasion Infect Immun 2002 70 5779 5789
35. Holder AA Blackman MJ Burghaus PA et al. A malaria merozoite surface protein (MSP1) - structure, processing and function Mem Inst Oswaldo Cruz 1992 87 Suppl. 3 37 42
36. Blackman MJ Holder AA Secondary processing of the Plasmodium falciparum merozoite surface protein-1 (MSP1) by a calcium-dependent membrane-bound serine protease: shedding of MSP133 as a noncovalently associated complex with other fragments of the MSP1 Mol Biochem Parasitol 1992 50 307 315
37. Druilhe P Khusmith S Epidemiological correlation between levels of antibodies promoting merozoite phagocytosis of Plasmodium falciparum and malaria-immune status Infect Immun 1987 55 888 891
38. Kumaratilake LM Ferrante A Opsonization and phagocytosis of Plasmodium falciparum merozoites measured by flow cytometry Clin Diagn Lab Immunol 2000 7 9 13
39. Egan AF Morris J Barnish G et al. Clinical immunity to Plasmodium falciparum malaria is associated with serum antibodies to the 19-kDa C-terminal fragment of the merozoite surface antigen, PfMSP-1 J Infect Dis 1996 173 765 769
40. Conway DJ Cavanagh DR Tanabe K et al. A principal target of human immunity to malaria identified by molecular population genetic and immunological analyses Nat Med 2000 6 689 692
41. Metzger WG Okenu DM Cavanagh DR et al. Serum IgG3 to the Plasmodium falciparum merozoite surface protein 2 is strongly associated with a reduced prospective risk of malaria Parasite Immunol 2003 25 307 312
42. Dodoo D Theander TG Kurtzhals JA et al. Levels of antibody to conserved parts of Plasmodium falciparum merozoite surface protein 1 in Ghanaian children are not associated with protection from clinical malaria Infect Immun 1999 67 2131 2137
43. Okech BA Corran PH Todd J et al. Fine specificity of serum antibodies to Plasmodium falciparum merozoite surface protein, PfMSP-1(19), predicts protection from malaria infection and high-density parasitemia Infect Immun 2004 72 1557 1567
44. Corran PH O'Donnell RA Todd J et al. The fine specificity, but not the invasion inhibitory activity, of 19-kilodalton merozoite surface protein 1-specific antibodies is associated with resistance to malarial parasitemia in a cross-sectional survey in The Gambia Infect Immun 2004 72 6185 6189
45. Verra F Hughes AL Natural selection on apical membrane antigen-1 of Plasmodium falciparum Parasitologia 1999 41 93 95
46. Polley SD Conway DJ Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene Genetics 2001 158 1505 1512
47. Quin SJ Langhorne J Different regions of the malaria merozoite surface protein 1 of Plasmodium chabaudi elicit distinct T-cell and antibody isotype responses Infect Immun 2001 69 2245 2251
48. Cavanagh DR Dobano C Elhassan IM et al. Differential patterns of human immunoglobulin G subclass responses to distinct regions of a single protein, the merozoite surface protein 1 of Plasmodium falciparum Infect Immun 2001 69 1207 1211
49. Diallo TO Spiegel A Diouf A et al. Short report: differential evolution of immunoglobulin G1/G3 antibody responses to Plasmodium falciparum MSP1(19) over time in malaria-immune adult Senegalese patients Am J Trop Med Hyg 2002 66 137 139
50. Al-Yaman F Genton B Reeder JC et al. Humoral response to defined Plasmodium falciparum antigens in cerebral and uncomplicated malaria and their relationship to parasite genotype Am J Trop Med Hyg 1997 56 430 435
51. Dolan SA Miller LH Wellems TE Evidence for a switching mechanism in the invasion of erythrocytes by Plasmodium falciparum J Clin Invest 1990 86 618 624
52. 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 1999 67 5784 5791
53. Baum J Pinder M Conway DJ Erythrocyte invasion phenotypes of Plasmodium falciparum in The Gambia Infect Immun 2003 71 1856 1863
54. Duraisingh MT Triglia T Ralph SA et al. Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes Embo J 2003 22 1047 1057
55. Nkuo TK Deas JE Sera from Cameroon induce crisis forms during Plasmodium falciparum growth inhibition studies in vitro Trans R Soc Trop Med Hyg 1988 82 380 383
56. Perlaza BL Herrera MA Villegas A et al. Antibody-independent inhibition of Plasmodium falciparum in vitro cultures J Clin Microbiol 1990 28 1172 1176
57. Sy NE Oberst RB Macalagay PS et al. In vitro growth inhibition of Plasmodium falciparum by sera from different regions of the Philippines Am J Trop Med Hyg 1990 43 243 247
58. Shi YP Udhayakumar V Oloo AJ et al. Differential effect and interaction of monocytes, hyperimmune sera, and immunoglobulin G on the growth of asexual stage Plasmodium falciparum parasites Am J Trop Med Hyg 1999 60 135 141
59. Tebo AE Kremsner PG Luty AJ Plasmodium falciparum: a major role for IgG3 in antibody-dependent monocyte-mediated cellular inhibition of parasite growth in vitro Exp Parasitol 2001 98 20 28
60. Brown GV Anders RF Mitchell GF et al. Target antigens of purified human immunoglobulins which inhibit growth of Plasmodium falciparum in vitro Nature 1982 297 591 593
61. Brown GV Anders RF Knowles G Differential effect of immunoglobulin on the in vitro growth of several isolates of Plasmodium falciparum Infect Immun 1983 39 1228 1235
62. Butcher GA Clark IA Crane G Inhibition of intra-erythrocytic growth of Plasmodium falciparum by human sera from Papua New Guinea Trans R Soc Trop Med Hyg 1987 81 568 572
63. Bolad A Nebie I Cuzin-Ouattara N et al. Antibody-mediated in vitro growth inhibition of field isolates of Plasmodium falciparum from asymptomatic children in Burkina Faso Am J Trop Med Hyg 2003 68 728 733
64. Marsh K Otoo L Hayes R et al. Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection Trans Roy Soc Trop Med Hyg 1989 83 293 303
65. Perraut R Marrama L Diouf B et al. Antibodies to the conserved C-terminal domain of the Plasmodium falciparum merozoite surface protein 1 and to the merozoite extract and their relationship with in vitro inhibitory antibodies and protection against clinical malaria in a Senegalese village J Infect Dis 2005 191 264 271
66. Bouharoun-Tayoun H Attanath P Sabchareon A et al. Antibodies that protect humans against Plasmodium falciparum blood stages do not on their own inhibit parasite growth and invasion in vitro, but act in cooperation with monocytes J Exp Med 1990 172 1633 1641
67. Chappel JA Holder AA Monoclonal antibodies that inhibit Plasmodium falciparum invasion in vitro recognise the first growth factor-like domain of merozoite surface protein-1 Mol Biochem Parasitol 1993 60 303 311
68. Blackman MJ Scott-Finnigan TJ Shai S et al. Antibodies inhibit the protease-mediated processing of a malaria merozoite surface protein J Exp Med 1994 180 389 393
69. Uthaipibull C Aufiero B Syed SE et al. Inhibitory and blocking monoclonal antibody epitopes on merozoite surface protein 1 of the malaria parasite Plasmodium falciparum J Mol Biol 2001 307 1381 1394
70. Dutta S Haynes JD Moch JK et al. Invasion-inhibitory antibodies inhibit proteolytic processing of apical membrane antigen 1 of Plasmodium falciparum merozoites Proc Natl Acad Sci USA 2003 100 12295 12300
71. Dekker C Uthaipibull C Calder LJ et al. Inhibitory and neutral antibodies to Plasmodium falciparum MSP119 form ring structures with their antigen Mol Biochem Parasitol 2004 137 143 149
72. Guevara Patino JA Holder AA McBride JS et al. Antibodies that inhibit malaria merozoite surface protein-1 processing and erythrocyte invasion are blocked by naturally acquired human antibodies J Exp Med 1997 186 1689 1699
73. Nwuba RI Sodeinde O Anumudu CI et al. The human immune response to Plasmodium falciparum includes both antibodies that inhibit merozoite surface protein 1 secondary processing and blocking antibodies Infect Immun 2002 70 5328 5331
74. Druilhe P Perignon J A hypothesis about the chronicity of malaria infection Parasitol Today 1997 13 9 353 355
75. Bouharoun-Tayoun H Druilhe P Antibodies in falciparum malaria: what matters most, quantity or quality? Mem Inst Oswaldo Cruz 1992 87 Suppl. 3 229 234
76. Theisen M Soe S Oeuvray C et al. The glutamate-rich protein (GLURP) of Plasmodium falciparum is a target for antibody-dependent monocyte-mediated inhibition of parasite growth in vitro Infect Immun 1998 66 11 17
77. Singh S Soe S Roussilhon C et al. Plasmodium falciparum merozoite surface protein 6 displays multiple targets for naturally occurring antibodies that mediate monocyte-dependent parasite killing Infect Immun 2005 73 1235 1238
78. O'Donnell RA Saul A Cowman AF et al. Functional conservation of the malaria vaccine antigen MSP-119 across distantly related Plasmodium species Nat Med 2000 6 91 95
79. O'Donnell RA de Koning-Ward TF Burt RA et al. Antibodies against merozoite surface protein (MSP)-1(19) are a major component of the invasion-inhibitory response in individuals immune to malaria J Exp Med 2001 193 1403 1412
80. De Koning-Ward TF O'Donnell RA Drew DR et al. A new rodent model to assess blood stage immunity to the Plasmodium falciparum antigen merozoite surface protein 119 reveals a protective role for invasion inhibitory antibodies J Exp Med 2003 198 869 875
81. John CC O'Donnell RA Sumba PO et al. Evidence that invasion-inhibitory antibodies specific for the 19-kDa fragment of merozoite surface protein-1 (MSP-1 19) can play a protective role against blood-stage Plasmodium falciparum infection in individuals in a malaria endemic area of Africa J Immunol 2004 173 666 672
82. Healer J Murphy V Hodder AN et al. Allelic polymorphisms in apical membrane antigen-1 are responsible for evasion of antibody-mediated inhibition in Plasmodium falciparum Mol Microbiol 2004 52 159 168
83. Marsh K Howard R Antigens induced on erythrocytes by Plasmodium falciparum: expression of diverse and conserved determinants Science 1986 231 150 153
84. Kyes SA Rowe JA Kriek N et al. Rifins: a second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum Proc Natl Acad Sci USA 1999 96 9333 9338
85. Cheng Q Cloonan N Fischer K et al. stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens Mol Biochem Parasitol 1998 97 161 176
86. Sherwood JA Marsh K Howard RJ et al. Antibody mediated strain-specific agglutination of Plasmodium falciparum- parasitized erythrocytes visualized by ethidium bromide staining Parasite Immunol 1985 7 659 663
87. Staalsoe T Giha HA Dodoo D et al. Detection of antibodies to variant antigens on Plasmodium falciparum-infected erythrocytes by flow cytometry Cytometry 1999 35 329 336
88. Piper KP Roberts DJ Day KP Plasmodium falciparum: analysis of the antibody specificity to the surface of the trophozoite-infected erythrocyte Exp Parasitol 1999 91 161 169
89. Newbold C Pinches R Roberts D et al. Plasmodium falciparum: the human agglutinating antibody response to the infected red cell surface is predominantly variant specific Exp Parasitol 1992 75 281 292
90. Ofori MF Dodoo D Staalsoe T et al. Malaria-induced acquisition of antibodies to Plasmodium falciparum variant surface antigens Infect Immun 2002 70 2982 2988
91. Kinyanjui SM Bull P Newbold CI et al. Kinetics of antibody responses to Plasmodium falciparum-infected erythrocyte variant surface antigens J Infect Dis 2003 187 667 674
92. Bull PC Lowe BS Kortok M et al. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria Nat Med 1998 4 358 360
93. Giha HA Staalsoe T Dodoo D et al. Antibodies to variable Plasmodium falciparum-infected erythrocyte surface antigens are associated with protection from novel malaria infections Immunol Lett 2000 71 117 126
94. Dodoo D Staalsoe T Giha H et al. Antibodies to variant antigens on the surfaces of infected erythrocytes are associated with protection from malaria in Ghanaian children Infect Immun 2001 69 3713 3718
95. Bull PC Kortok M Kai O et al. Plasmodium falciparum-infected erythrocytes: agglutination by diverse Kenyan plasma is associated with severe disease and young host age J Infect Dis 2000 182 252 259
96. Nielsen MA Staalsoe T Kurtzhals JA et al. Plasmodium falciparum variant surface antigen expression varies between isolates causing severe and nonsevere malaria and is modified by acquired immunity J Immunol 2002 168 3444 3450
97. Lindenthal C Kremsner PG Klinkert MQ Commonly recognised Plasmodium falciparum parasites cause cerebral malaria Parasitol Res 2003 91 363 368
98. Kraemer SM Smith JD Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family Mol Microbiol 2003 50 1527 1538
99. Lavstsen T Salanti A Jensen AT et al. Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions Malar J 2003 2 27
100. Jensen AT Magistrado P Sharp S et al. Plasmodium falciparum associated with severe childhood malaria preferentially expresses PfEMP1 encoded by group A var genes J Exp Med 2004 199 1179 1190
101. Fried F Nosten F Brockman A et al. Maternal antibodies block malaria Nature 1998 395 852 852
102. Ricke CH Staalsoe T Koram K et al. Plasma antibodies from malaria-exposed pregnant women recognize variant surface antigens on Plasmodium falciparum-infected erythrocytes in a parity-dependent manner and block parasite adhesion to chondroitin sulfate A J Immunol 2000 165 3309 3316
103. Beeson JG Reeder JC Rogerson SJ et al. Parasite adhesion and immune evasion in placental malaria Trends Parasitol 2001 17 331 337
104. Rowe JA Kyes SA The role of Plasmodium falciparum var genes in malaria in pregnancy Mol Microbiol 2004 53 1011 1019
105. Deitsch KW Hviid L Variant surface antigens, virulence genes and the pathogenesis of malaria Trends Parasitol 2004 20 562 566
106. Udeinya I Miller L McGregor I et al. Plasmodium falciparum strain-specific antibody blocks binding of infected erythrocytes to amelanotic melanoma cells Nature 1983 303 429 431
107. Singh B Ho M Looareesuwan S et al. Plasmodium falciparum: inhibition/reversal of cytoadherence of Thai isolates to melanoma cells by local immune sera Clin Exp Immunol 1988 72 145 150
108. Beeson JG Mann EJ Elliott SR et al. Antibodies to variant surface antigens of Plasmodium falciparum-infected erythrocytes and adhesion inhibitory antibodies are associated with placental malaria and have overlapping and distinct targets J Infect Dis 2004 189 540 551
109. Carlson J Helmby H Hill A et al. Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies Lancet 1990 336 1457 1460
110. Staalsoe T Megnekou R Fievet N et al. Acquisition and decay of antibodies to pregnancy-associated variant antigens on the surface of Plasmodium falciparum-infected erythrocytes that protect against placental parasitemia J Infect Dis 2001 184 618 626
111. Taylor DW Zhou A Marsillio LE et al. Antibodies that inhibit binding of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A and to the C terminus of merozoite surface protein 1 correlate with reduced placental malaria in Cameroonian women Infect Immun 2004 72 1603 1607
112. Duffy PE Fried M Antibodies that inhibit Plasmodium falciparum adhesion to chondroitin sulfate A are associated with increased birth weight and the gestational age of newborns Infect Immun 2003 71 6620 6623
113. Staalsoe T Shulman CE Bulmer JN et al. Variant surface antigen-specific IgG and protection against clinical consequences of pregnancy-associated Plasmodium falciparum malaria Lancet 2004 363 283 289
114. Salanti A Dahlback M Turner L et al. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria J Exp Med 2004 200 1197 1203
115. Khattab A Reinhardt C Staalsoe T et al. Analysis of IgG with specificity for variant surface antigens expressed by placental Plasmodium falciparum isolates Malar J 2004 3 21
116. Tuikue Ndam NG Fievet N Bertin G et al. Variable adhesion abilities and overlapping antigenic properties in placental Plasmodium falciparum isolates J Infect Dis 2004 190 2001 2009
117. Perraut R Mercereau-Puijalon O Mattei D et al. Induction of opsonizing antibodies after injection of recombinant Plasmodium falciparum vaccine candidate antigens in preimmune Saimiri sciureus monkeys Infect Immun 1995 63 554 562
118. Mota MM Brown KN Holder AA et al. Acute Plasmodium chabaudi chabaudi malaria infection induces antibodies which bind to the surfaces of parasitized erythrocytes and promote their phagocytosis by macrophages in vitro Infect Immun 1998 66 4080 4086
119. Yoneto T Waki S Takai T et al. A critical role of Fc receptor-mediated antibody-dependent phagocytosis in the host resistance to blood-stage Plasmodium berghei XAT infection J Immunol 2001 166 6236 6241
120. Celada A Cruchaud A Perrin LH Opsonic activity of human immune serum on in vitro phagocytosis of Plasmodium falciparum infected red blood cells by monocytes Clin Exp Immunol 1982 47 635 644
121. Tebo AE Kremsner PG Luty AJ Fcgamma receptor-mediated phagocytosis of Plasmodium falciparum-infected erythrocytes in vitro Clin Exp Immunol 2002 130 300 306
122. Stanley HA Mayes JT Cooper NR et al. Complement activation by the surface of Plasmodium falciparum infected erythrocytes Mol Immunol 1984 21 145 150
123. Wiesner J Jomaa H Wilhelm M et al. Host cell factor CD59 restricts complement lysis of Plasmodium falciparum-infected erythrocytes Eur J Immunol 1997 27 2708 2713
124. Pombo DJ Lawrence G Hirunpetcharat C et al. Immunity to malaria after administration of ultra-low doses of red cells infected with Plasmodium falciparum Lancet 2002 360 610 617