Biochemical and immunological mechanisms by which sickle cell trait protects against malaria

Malaria Journal

Volumn 12, Issue 1, 2013, Pages

  Gong, Lauren ^a   Parikh, Sunil ^b   Rosenthal, Philip J ^c   Greenhouse, Bryan ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b YALE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Genetics; Immunology; Immunopathogenesis; Malaria; Plasmodium falciparum; Protection; Red blood cell polymorphisms; Sickle cell trait; Sickle haemoglobin

Indexed keywords

HEMOGLOBIN;

ADAPTIVE IMMUNITY; CELLULAR IMMUNITY; CHEMICAL ANALYSIS; HOST PARASITE INTERACTION; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOPATHOGENESIS; INNATE IMMUNITY; MALARIA FALCIPARUM; PLASMODIUM FALCIPARUM; PROTECTION; REVIEW; SICKLE CELL TRAIT;

HOST-PATHOGEN INTERACTIONS; HUMANS; MALARIA, FALCIPARUM; SICKLE CELL TRAIT;

EID: 84883628670     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-12-317     Document Type: Review

References (104)

1. Human red blood cell polymorphisms and malaria. Williams TN, Curr Opin Microbiol 2006 9 388 394 (Pubitemid 44108720)
2. Host genetic factors in resistance and susceptibility to malaria. Kwiatkowski DP, Luoni G, Parassitologia 2006 48 450 467
3. Heritability of malaria in Africa. Mackinnon MJ, Mwangi TW, Snow RW, Marsh K, Williams TN, PLoS Med 2005 2 340
4. Hemoglobinopathies: slicing the Gordian knot of Plasmodium falciparum malaria pathogenesis. Taylor SM, Cerami C, Fairhurst RM, PLoS Pathog 2013 9 1003327
5. Global distribution of the sickle cell gene and geographical confirmation of the malaria hypothesis. Piel FB, Patil AP, Howes RE, Nyangiri OA, Gething PW, Williams TN, Weatherall DJ, Hay SI, Nat Commun 2010 1 104
6. Sickle cell disease in the Balovale District of Northern Rhodesia. Beet E, East Afr Med J 1946 23 75 86
7. Protection afforded by sickle-cell trait against subtertian malareal infection. Allison A, Br Med J 1954 1 290 294
8. The sickle cell trait; its clinical significance. Brain P, S Afr Med J 1952 26 925 928
9. Abnormal human haemoglobins. III. The chemical difference between normal and sickle cell haemoglobins. Ingram VM, Biochim Biophys Acta 1959 36 402 411
10. Pathogenesis and treatment of sickle cell disease. Bunn HF, N Engl J Med 1997 337 762 769 (Pubitemid 27417977)
11. Disease and evolution. Haldane JBS, Ric Sci Suppl 1949 19 68 76
12. Glucose-6-phosphate-dehydrogenase deficiency, sickling, and malaria in African children in South Western Nigeria. Gilles HM, Fletcher KA, Hendrickse RG, Lindner R, Reddy S, Allan N, Lancet 1967 1 138 140
13. Common west African HLA antigens are associated with protection from severe malaria. Hill AV, Allsopp CE, Kwiatkowski D, Anstey NM, Twumasi P, Rowe PA, Bennett S, Brewster D, McMichael AJ, Greenwood BM, Nature 1991 352 595 600 (Pubitemid 21912384)
14. Hemoglobin variants and disease manifestations in severe falciparum malaria. May J, Evans JA, Timmann C, Ehmen C, Busch W, Thye T, Agbenyega T, Horstmann RD, JAMA 2007 297 2220 2226 (Pubitemid 47010879)
15. An immune basis for malaria protection by the sickle cell trait. Williams TN, Mwangi TW, Roberts DJ, Alexander ND, Weatherall DJ, Wambua S, Kortok M, Snow RW, Marsh K, PLoS Med 2005 2 128
16. Genome-wide and fine-resolution association analysis of malaria in West Africa. Jallow M, Teo YY, Small KS, Rockett KA, Deloukas P, Clark TG, Kivinen K, Bojang KA, Conway DJ, Pinder M, Sirugo G, Sisay-Joof F, Usen S, Auburn S, Bumpstead SJ, Campino S, Coffey A, Dunham A, Fry AE, Green A, Gwilliam R, Hunt SE, Inouye M, Jeffreys AE, Mendy A, Palotie A, Potter S, Ragoussis J, Rogers J, Rowlands K, et al. Nat Genet 2009 41 657 665
17. Haemoglobinopathies and the clinical epidemiology of malaria: a systematic review and meta-analysis. Taylor SM, Parobek CM, Fairhurst RM, Lancet Infect Dis 2012 12 457 468
18. The effect of alpha + -thalassaemia on the incidence of malaria and other diseases in children living on the coast of Kenya. Wambua S, Mwangi TW, Kortok M, Uyoga SM, Macharia AW, Mwacharo JK, Weatherall DJ, Snow RW, Marsh K, Williams TN, PLoS Med 2006 3 158
19. Both heterozygous and homozygous alpha + thalassemias protect against severe and fatal Plasmodium falciparum malaria on the coast of Kenya. Williams TN, Wambua S, Uyoga S, Macharia A, Mwacharo JK, Newton CRJC, Maitland K, Blood 2005 106 368 371 (Pubitemid 40967215)
20. alpha + -Thalassemia protects children against disease caused by other infections as well as malaria. Allen SJ, O'Donnell A, Alexander ND, Alpers MP, Peto TE, Clegg JB, Weatherall DJ, Proc Natl Acad Sci USA 1997 94 14736 14741 (Pubitemid 28041443)
21. Alpha(+)-thalassemia protects African children from severe malaria. Mockenhaupt FP, Ehrhardt S, Gellert S, Otchwemah RN, Dietz E, Anemana SD, Bienzle U, Blood 2004 104 2003 2006 (Pubitemid 39297850)
22. α-Thalassemia impairs the cytoadherence of Plasmodium falciparum-infected erythrocytes. Krause MA, Diakite SAS, Lopera-Mesa TM, Amaratunga C, Arie T, Traore K, Doumbia S, Konate D, Keefer JR, Diakite M, Fairhurst RM, PLoS One 2012 7 37214
23. Reduced risk of Plasmodium vivax malaria in Papua New Guinean children with Southeast Asian ovalocytosis in two cohorts and a case-control study. Rosanas-Urgell A, Lin E, Manning L, Rarau P, Laman M, Senn N, Grimberg BT, Tavul L, Stanisic DI, Robinson LJ, Aponte JJ, Dabod E, Reeder JC, Siba P, Zimmerman PA, Davis TME, King CL, Michon P, Mueller I, PLoS Med 2012 9 1001305
24. Influence of hemoglobin E trait on the severity of Falciparum malaria. Hutagalung R, Wilairatana P, Looareesuwan S, Brittenham GM, Aikawa M, Gordeuk VR, J Infect Dis 1999 179 283 286 (Pubitemid 29028372)
25. Hemoglobin E: a balanced polymorphism protective against high parasitemias and thus severe P falciparum malaria. Chotivanich K, Udomsangpetch R, Pattanapanyasat K, Chierakul W, Simpson J, Looareesuwan S, White N, Blood 2002 100 1172 1176 (Pubitemid 34864268)
26. Hemoglobin C and resistance to severe malaria in Ghanaian children. Mockenhaupt FP, Ehrhardt S, Cramer JP, Otchwemah RN, Anemana SD, Goltz K, Mylius F, Dietz E, Eggelte TA, Bienzle U, J Infect Dis 2004 190 1006 1009 (Pubitemid 39120981)
27. Haemoglobin C protects against clinical Plasmodium falciparum malaria. Modiano D, Luoni G, Sirima BS, Simporé J, Verra F, Konaté A, Rastrelli E, Olivieri A, Calissano C, Paganotti GM, D'Urbano L, Sanou I, Sawadogo A, Modiano G, Coluzzi M, Nature 2001 414 305 308 (Pubitemid 33097806)
28. Hemoglobin C associated with protection from severe malaria in the Dogon of Mali, a West African population with a low prevalence of hemoglobin S. Agarwal A, Guindo A, Cissoko Y, Taylor JG, Coulibaly D, Koné A, Kayentao K, Djimde A, Plowe CV, Doumbo O, Wellems TE, Diallo D, Blood 2000 96 2358 2363
29. Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. Williams TN, Mwangi TW, Wambua S, Alexander ND, Kortok M, Snow RW, Marsh K, J Infect Dis 2005 192 178 186 (Pubitemid 40863872)
30. Protective effects of the sickle cell gene against malaria morbidity and mortality. Aidoo M, Terlouw DJ, Kolczak MS, McElroy PD, ter Kuile FO, Kariuki S, Nahlen BL, Lal AA, Udhayakumar V, Lancet 2002 359 1311 1312 (Pubitemid 34310639)
31. Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Marsh K, Otoo L, Hayes RJ, Carson DC, Greenwood BM, Trans R Soc Trop Med Hyg 1989 83 293 303 (Pubitemid 19163208)
32. Factors determining the heterogeneity of malaria incidence in children in Kampala, Uganda. Clark TD, Greenhouse B, Njama-Meya D, Nzarubara B, Maiteki-Sebuguzi C, Staedke SG, Seto E, Kamya MR, Rosenthal PJ, Dorsey G, J Infect Dis 2008 198 393 400
33. Sickle cell trait is associated with a delayed onset of malaria: implications for time-to-event analysis in clinical studies of malaria. Crompton PD, Traore B, Kayentao K, Doumbo S, Ongoiba A, Diakite SAS, Krause MA, Doumtabe D, Kone Y, Weiss G, Huang C-Y, Doumbia S, Guindo A, Fairhurst RM, Miller LH, Pierce SK, Doumbo OK, J Infect Dis 2008 198 1265 1275
34. Differing effects of HbS and HbC traits on uncomplicated falciparum malaria, anemia, and child growth. Kreuels B, Kreuzberg C, Kobbe R, Ayim-Akonor M, Apiah-Thompson P, Thompson B, Ehmen C, Adjei S, Langefeld I, Adjei O, May J, Blood 2010 115 4551 4558
35. Evidence for both innate and acquired mechanisms of protection from Plasmodium falciparum in children with sickle cell trait. Gong L, Maiteki-Sebuguzi C, Rosenthal PJ, Hubbard AE, Drakeley CJ, Dorsey G, Greenhouse B, Blood 2012 119 3808 3814
36. Host polymorphisms and the incidence of malaria in Ugandan children. Parikh S, Dorsey G, Rosenthal PJ, Am J Trop Med Hyg 2004 71 750 753 (Pubitemid 40075624)
37. Population genetic studies in the Congo. I. Glucose-6-phosphate dehydrogenase deficiency, hemoglobin S, and malaria. Motulsky AG, Vandepitte J, Fraser GR, Am J Hum Genet 1966 18 514 537
38. Abnormal haemoglobins in the Sudan savanna of Nigeria. I. Prevalence of haemoglobins and relationships between sickle cell trait, malaria and survival. Fleming AF, Storey J, Molineaux L, Iroko EA, Attai ED, Ann Trop Med Parasitol 1979 73 161 172 (Pubitemid 10226902)
39. Differential antibody response of Gambian donors to soluble Plasmodium falciparum antigens. Jakobsen PH, Riley EM, Allen SJ, Larsen SO, Bennett S, Jepsen S, Greenwood BM, Trans R Soc Trop Med Hyg 1991 85 26 32
40. Red blood cell polymorphisms in relation to Plasmodium falciparum asymptomatic parasite densities and morbidity in Senegal. Migot-Nabias F, Pelleau S, Watier L, Guitard J, Toly C, De Araujo C, Ngom MI, Chevillard C, Gaye O, Garcia A, Microbes Infect 2006 8 2352 2358 (Pubitemid 44499042)
41. Influence of haemoglobins S and C on predominantly asymptomatic Plasmodium infections in northern Ghana. Danquah I, Ziniel P, Eggelte TA, Ehrhardt S, Mockenhaupt FP, Trans R Soc Trop Med Hyg 2010 104 713 719
42. Malaria in patients with sickle cell anemia: burden, risk factors, and outcome at the outpatient clinic and during hospitalization. Makani J, Komba AN, Cox SE, Oruo J, Mwamtemi K, Kitundu J, Magesa P, Rwezaula S, Meda E, Mgaya J, Pallangyo K, Okiro E, Muturi D, Newton CR, Fegan G, Marsh K, Williams TN, Blood 2010 115 215 220
43. Sickle cell trait protects against Plasmodium falciparum infection. Billo MA, Johnson ES, Doumbia SO, Poudiougou B, Sagara I, Diawara SI, Diakité M, Diallo M, Doumbo OK, Tounkara A, Rice J, James MA, Krogstad DJ, Am J Epidemiol 2012 176 Suppl 7 175 185
44. Imbalanced distribution of Plasmodium falciparum MSP-1 genotypes related to sickle-cell trait. Ntoumi F, Rogier C, Dieye A, Trape JF, Millet P, Mercereau-Puijalon O, Mol Med 1997 3 581 592 (Pubitemid 27465229)
45. Variation of Plasmodium falciparum msp1 block 2 and msp2 allele prevalence and of infection complexity in two neighbouring Senegalese villages with different transmission conditions. Konaté L, Zwetyenga J, Rogier C, Bischoff E, Fontenille D, Tall A, Spiegel A, Trape JF, Mercereau-Puijalon O, Trans R Soc Trop Med Hyg 1999 93 Suppl 1 21 28 (Pubitemid 29123571)
46. Plasmodium falciparum malaria and human red cells. II. Red cell genetic traits and resistance against malaria. Guggenmoos-Holzmann I, Bienzle U, Luzzatto L, Int J Epidemiol 1981 10 16 22 (Pubitemid 11095376)
47. Increased sickling of parasitised erythrocytes as mechanism of resistance against malaria in the sickle-cell trait. Luzzatto L, Nwachuku-Jarrett ES, Reddy S, Lancet 1970 1 319 321
48. Sickling rates of human AS red cells infected in vitro with Plasmodium falciparum malaria. Roth EF Jr, Friedman M, Ueda Y, Tellez I, Trager W, Nagel RL, Science 1978 202 650 652 (Pubitemid 9055627)
49. Erythrocytic mechanism of sickle cell resistance to malaria. Friedman MJ, Proc Natl Acad Sci USA 1978 75 1994 1997 (Pubitemid 8335470)
50. Cellular mechanism for the protective effect of haemoglobin S against P. falciparum malaria. Pasvol G, Weatherall DJ, Wilson RJ, Nature 1978 274 701 703 (Pubitemid 8405068)
51. Toxic heme in sickle cells: an explanation for death of malaria parasites. Orjih AU, Chevli R, Fitch CD, Am J Trop Med Hyg 1985 34 223 227 (Pubitemid 15085211)
52. Effects of red blood cell potassium and hypertonicity on the growth of Plasmodium falciparum in culture. Ginsburg H, Handeli S, Friedman S, Gorodetsky R, Krugliak M, Z Parasitenkd 1986 72 185 199 (Pubitemid 16154383)
53. Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Ayi K, Turrini F, Piga A, Arese P, Blood 2004 104 3364 3371 (Pubitemid 39507160)
54. Translocation of sickle cell erythrocyte microRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. LaMonte G, Philip N, Reardon J, Lacsina JR, Majoros W, Chapman L, Thornburg CD, Telen MJ, Ohler U, Nicchitta CV, Haystead T, Chi J-T, Cell Host Microbe 2012 12 187 199
55. The fine structure of Plasmodium falciparum and its host erythrocytes in natural malarial infections in man. Trager W, Rudzinska MA, Bradbury PC, Bull World Health Organ 1966 35 883 885
56. Plasmodium falciparum-infected erythrocytes form spontaneous erythrocyte rosettes. Udomsangpetch R, Wåhlin B, Carlson J, Berzins K, Torii M, Aikawa M, Perlmann P, Wahlgren M, J Exp Med 1989 169 1835 1840 (Pubitemid 19126838)
57. Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Carlson J, Helmby H, Hill AV, Brewster D, Greenwood BM, Wahlgren M, Lancet 1990 336 1457 1460
58. Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. Treutiger CJ, Hedlund I, Helmby H, Carlson J, Jepson A, Twumasi P, Kwiatkowski D, Greenwood BM, Wahlgren M, Am J Trop Med Hyg 1992 46 503 510
59. The pathology of human cerebral malaria. Aikawa M, Iseki M, Barnwell JW, Taylor D, Oo MM, Howard RJ, Am J Trop Med Hyg 1990 43 30 37 (Pubitemid 20259480)
60. Impaired cytoadherence of Plasmodium falciparum-infected erythrocytes containing sickle hemoglobin. Cholera R, Brittain NJ, Gillrie MR, Lopera-Mesa TM, Diakité SAS, Arie T, Krause MA, Guindo A, Tubman A, Fujioka H, Diallo DA, Doumbo OK, Ho M, Wellems TE, Fairhurst RM, Proc Natl Acad Sci USA 2008 105 991 996 (Pubitemid 351282069)
61. Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor. Ockenhouse CF, Tandon NN, Magowan C, Jamieson GA, Chulay JD, Science 1989 243 1469 1471 (Pubitemid 19087130)
62. Malaria-induced lymphokines: stimulation of macrophages for enhanced phagocytosis. Ockenhouse CF, Shear HL, Infect Immun 1983 42 733 739 (Pubitemid 14230273)
63. Nonopsonic monocyte/macrophage phagocytosis of Plasmodium falciparum-parasitized erythrocytes: a role for CD36 in malarial clearance. McGilvray ID, Serghides L, Kapus A, Rotstein OD, Kain KC, Blood 2000 96 3231 3240
64. Immune responses to asexual blood-stages of malaria parasites. Yazdani SS, Mukherjee P, Chauhan VS, Chitnis CE, Curr Mol Med 2006 6 187 203
65. Rosetting of Plasmodium falciparum-infected red blood cells with uninfected red blood cells enhances microvascular obstruction under flow conditions. Kaul DK, Roth EF Jr, Nagel RL, Howard RJ, Handunnetti SM, Blood 1991 78 812 819
66. An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, Buley ID, Gatter KC, Newbold CI, Pukritayakamee S, Nagachinta B, Am J Pathol 1994 145 1057 1069 (Pubitemid 24345654)
67. The pathogenic basis of malaria. Miller LH, Baruch DI, Marsh K, Doumbo OK, Nature 2002 415 673 679 (Pubitemid 34136400)
68. Reduced microcirculatory flow in severe falciparum malaria: pathophysiology and electron-microscopic pathology. Dondorp AM, Pongponratn E, White NJ, Acta Trop 2004 89 309 317 (Pubitemid 38117067)
69. Abnormal display of PfEMP-1 on erythrocytes carrying haemoglobin C may protect against malaria. Fairhurst RM, Baruch DI, Brittain NJ, Ostera GR, Wallach JS, Hoang HL, Hayton K, Guindo A, Makobongo MO, Schwartz OM, Tounkara A, Doumbo OK, Diallo DA, Fujioka H, Ho M, Wellems TE, Nature 2005 435 1117 1121 (Pubitemid 40910520)
70. Hemoglobins S and C interfere with actin remodeling in Plasmodium falciparum-infected erythrocytes. Cyrklaff M, Sanchez CP, Kilian N, Bisseye C, Simpore J, Frischknecht F, Lanzer M, Science 2011 334 1283 1286
71. Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Cappadoro M, Giribaldi G, O'Brien E, Turrini F, Mannu F, Ulliers D, Simula G, Luzzatto L, Arese P, Blood 1998 92 2527 2534 (Pubitemid 28452997)
72. Band 3/complement-mediated recognition and removal of normally senescent and pathological human erythrocytes. Arese P, Turrini F, Schwarzer E, Cell Physiol Biochem 2005 16 133 146 (Pubitemid 41643014)
73. Accelerated clearance of Plasmodium-infected erythrocytes in sickle cell trait and annexin-A7 deficiency. Lang PA, Kasinathan RS, Brand VB, Duranton C, Lang C, Koka S, Shumilina E, Kempe DS, Tanneur V, Akel A, Lang KS, Foller M, Kun JFJ, Kremsner PG, Wesselborg S, Laufer S, Clemen CS, Herr C, Noegel AA, Wieder T, Gulbins E, Lang F, Huber SM, Cell Physiol Biochem 2009 24 415 428
74. Insertion of fluorescent phosphatidylserine into the plasma membrane of red blood cells. Recognition by autologous macrophages. Tanaka Y, Schroit AJ, J Biol Chem 1983 258 11335 11343 (Pubitemid 13021283)
75. In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membranes. Schroit AJ, Madsen JW, Tanaka Y, J Biol Chem 1985 260 5131 5138 (Pubitemid 15031516)
76. Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia. Boas FE, Forman L, Beutler E, Proc Natl Acad Sci USA 1998 95 3077 3081 (Pubitemid 28135857)
77. Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. Hoffmann PR, de Cathelineau AM, Ogden CA, Leverrier Y, Bratton DL, Daleke DL, Ridley AJ, Fadok VA, Henson PM, J Cell Biol 2001 155 649 659 (Pubitemid 34289322)
78. Frequencies of peripheral blood myeloid cells in healthy Kenyan children with alpha + thalassemia and the sickle cell trait. Urban BC, Shafi MJ, Cordery DV, Macharia A, Lowe B, Marsh K, Williams TN, Am J Trop Med Hyg 2006 74 578 584 (Pubitemid 46774436)
79. Immunoadsorbent isolation of antigens from the culture medium of in vitro cultivated Plasmodium falciparum. Jepsen S, Andersen BJ, Acta Pathol Microbiol Scand C 1981 89 99 103 (Pubitemid 11145708)
80. Specific proliferative response of human lymphocytes to purified soluble antigens from Plasmodium falciparum in vitro cultures and to antigens from malaria patients' sera. Bygbjerg IC, Jepsen S, Theander TG, Odum N, Clin Exp Immunol 1985 59 421 426 (Pubitemid 15174435)
81. Cellular immune responses to Plasmodium falciparum antigens in Gambian children during and after an acute attack of falciparum malaria. Riley EM, Andersson G, Otoo LN, Jepsen S, Greenwood BM, Clin Exp Immunol 1988 73 17 22
82. Cell-mediated immune responses to Plasmodium falciparum purified soluble antigens in sickle-cell trait subjects. Bayoumi RA, Abu-Zeid YA, Abdulhadi NH, Saeed BO, Theander TG, Hviid L, Ghalib HW, Nugud AH, Jepsen S, Jensen JB, Immunol Lett 1990 25 243 249 (Pubitemid 20260876)
83. Lymphoproliferative responses to Plasmodium falciparum antigens in children with and without the sickle cell trait. Abu-Zeid YA, Abdulhadi NH, Hviid L, Theander TG, Saeed BO, Jepsen S, Jensen JB, Bayoumi RA, Scand J Immunol 1991 34 237 242
84. Modulation of the cellular immune response during Plasmodium falciparum infections in sickle cell trait individuals. Abu-Zeid YA, Theander TG, Abdulhadi NH, Hviid L, Saeed BO, Jepsen S, Jensen JB, Bayoumi RA, Clin Exp Immunol 1992 88 112 118
85. Longitudinal study of Plasmodium falciparum infection and immune responses in infants with or without the sickle cell trait. Le Hesran JY, Personne I, Personne P, Fievet N, Dubois B, Beyemé M, Boudin C, Cot M, Deloron P, Int J Epidemiol 1999 28 793 798 (Pubitemid 29401344)
86. Impaired cell-mediated immunity in Plasmodium falciparum-infected patients with high-parasitemia and cerebral malaria. Brasseur P, Agrapart M, Ballet JJ, Druilhe P, Warrell MJ, Tharavanij S, Clin Immunol Immunopathol 1983 27 38 50 (Pubitemid 13120950)
87. Antigen-specific immunosuppression in human malaria due to Plasmodium falciparum. Ho M, Webster HK, Looareesuwan S, Supanaranond W, Phillips RE, Chanthavanich P, Warrell DA, J Infect Dis 1986 153 763 771 (Pubitemid 16133760)
88. Suppression of parasite-specific response in Plasmodium falciparum malaria. A longitudinal study of blood mononuclear cell proliferation and subset composition. Theander TG, Bygbjerg IC, Andersen BJ, Jepsen S, Kharazmi A, Odum N, Scand J Immunol 1986 24 73 81 (Pubitemid 16048867)
89. Cytokines in the pathogenesis of and protection against malaria. Angulo I, Fresno M, Clin Diagn Lab Immunol 2002 9 1145 1152 (Pubitemid 35283273)
90. The relationship of serum gamma-globulin concentration to malaria and sickling. Edozien JC, Boyo AE, Morley DC, J Clin Pathol 1960 13 118 123
91. Abnormal haemoglobins in the Sudan savanna of Nigeria. II. Immunological response to malaria in normals and subjects with sickle cell trait. Cornille-Brøgger R, Fleming AF, Kagan I, Matsushima T, Molineaux L, Ann Trop Med Parasitol 1979 73 173 183 (Pubitemid 10226903)
92. Immunoglobulin M and G antibody responses to Plasmodium falciparum glutamate-rich protein: correlation with clinical immunity in Gambian children. Dziegiel M, Rowe P, Bennett S, Allen SJ, Olerup O, Gottschau A, Borre M, Riley EM, Infect Immun 1993 61 103 108 (Pubitemid 23015405)
93. Higher resistance to Plasmodium falciparum infection in patients with homozygous sickle cell disease in western Kenya. Aluoch JR, Trop Med Int Health 1997 2 568 571 (Pubitemid 27304336)
94. High immunoglobulin G2 (IgG2) and low IgG4 levels are associated with human resistance to Plasmodium falciparum malaria. Aucan C, Traoré Y, Tall F, Nacro B, Traoré-Leroux T, Fumoux F, Rihet P, Infect Immun 2000 68 1252 1258 (Pubitemid 30108518)
95. Antibody responses to Plasmodium falciparum: evolution according to the severity of a prior clinical episode and association with subsequent reinfection. Luty AJ, Ulbert S, Lell B, Lehman L, Schmidt-Ott R, Luckner D, Greve B, Matousek P, Schmid D, Herbich K, Dubois B, Deloron P, Kremsner PG, Am J Trop Med Hyg 2000 62 566 572 (Pubitemid 32210476)
96. Relationship between malaria incidence and IgG levels to Plasmodium falciparum merozoite antigens in Malian children: impact of hemoglobins S and C. Miura K, Diakite M, Diouf A, Doumbia S, Konate D, Keita AS, Moretz SE, Tullo G, Zhou H, Lopera-Mesa TM, Anderson JM, Fairhurst RM, Long CA, PLoS ONE 2013 8 60182
97. Hemoglobin S and C heterozygosity enhances neither the magnitude nor breadth of antibody responses to a diverse array of Plasmodium falciparum antigens. Tan X, Traore B, Kayentao K, Ongoiba A, Doumbo S, Waisberg M, Doumbo OK, Felgner PL, Fairhurst RM, Crompton PD, J Infect Dis 2011 204 1750 1761
98. Haemoglobin C and S role in acquired immunity against Plasmodium falciparum malaria. Verra F, Simpore J, Warimwe GM, Tetteh KK, Howard T, Osier FHA, Bancone G, Avellino P, Blot I, Fegan G, Bull PC, Williams TN, Conway DJ, Marsh K, Modiano D, PLoS ONE 2007 2 978
99. Impact of red blood cell polymorphisms on the antibody response to Plasmodium falciparum in Senegal. Sarr JB, Pelleau S, Toly C, Guitard J, Konaté L, Deloron P, Garcia A, Migot-Nabias F, Microbes Infect 2006 8 1260 1268 (Pubitemid 43842006)
100. Relationship of binding of immunoglobulin G to Plasmodium falciparum-infected erythrocytes with parasite endemicity and antibody responses to conserved antigen in immune individuals. Diatta A-M, Marrama L, Tall A, Trape J-F, Dieye A, Garraud O, Mercereau-Puijalon O, Perraut R, Clin Diagn Lab Immuno 2004 11 6 11 (Pubitemid 38090645)
101. The sickle cell trait is associated with enhanced immunoglobulin G antibody responses to Plasmodium falciparum variant surface antigens. Cabrera G, Cot M, Migot-Nabias F, Kremsner PG, Deloron P, Luty AJF, J Infect Dis 2005 191 1631 1638 (Pubitemid 40656750)
102. Morbidity from malaria and immune responses to defined Plasmodium falciparum antigens in children with sickle cell trait in The Gambia. Allen SJ, Bennett S, Riley EM, Rowe PA, Jakobsen PH, O'Donnell A, Greenwood BM, Trans R Soc Trop Med Hyg 1992 86 494 498
103. Immunity to malaria: more questions than answers. Langhorne J, Ndungu FM, Sponaas A-M, Marsh K, Nat Immunol 2008 9 725 732 (Pubitemid 351859155)
104. Sickle hemoglobin confers tolerance to Plasmodium infection. Ferreira A, Marguti I, Bechmann I, Jeney V, Chora A, Palha NR, Rebelo S, Henri A, Beuzard Y, Soares MP, Cell 2011 145 398 409