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Published in: Malaria Journal 1/2013

Open Access 01-12-2013 | Review

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

Authors: Lauren Gong, Sunil Parikh, Philip J Rosenthal, Bryan Greenhouse

Published in: Malaria Journal | Issue 1/2013

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Abstract

Sickle cell trait (HbAS) is the best-characterized genetic polymorphism known to protect against falciparum malaria. Although the protective effect of HbAS against malaria is well known, the mechanism(s) of protection remain unclear. A number of biochemical and immune-mediated mechanisms have been proposed, and it is likely that multiple complex mechanisms are responsible for the observed protection. Increased evidence for an immune component of protection as well as novel mechanisms, such as enhanced tolerance to disease mediated by HO-1 and reduced parasitic growth due to translocation of host micro-RNA into the parasite, have recently been described. A better understanding of relevant mechanisms will provide valuable insight into the host-parasite relationship, including the role of the host immune system in protection against malaria.
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Literature
1.
go back to reference Williams TN: Human red blood cell polymorphisms and malaria. Curr Opin Microbiol. 2006, 9: 388-394.PubMed Williams TN: Human red blood cell polymorphisms and malaria. Curr Opin Microbiol. 2006, 9: 388-394.PubMed
2.
go back to reference Kwiatkowski DP, Luoni G: Host genetic factors in resistance and susceptibility to malaria. Parassitologia. 2006, 48: 450-467.PubMed Kwiatkowski DP, Luoni G: Host genetic factors in resistance and susceptibility to malaria. Parassitologia. 2006, 48: 450-467.PubMed
3.
4.
go back to reference Taylor SM, Cerami C, Fairhurst RM: Hemoglobinopathies: slicing the Gordian knot of Plasmodium falciparum malaria pathogenesis. PLoS Pathog. 2013, 9: e1003327-PubMedCentralPubMed Taylor SM, Cerami C, Fairhurst RM: Hemoglobinopathies: slicing the Gordian knot of Plasmodium falciparum malaria pathogenesis. PLoS Pathog. 2013, 9: e1003327-PubMedCentralPubMed
5.
go back to reference Piel FB, Patil AP, Howes RE, Nyangiri OA, Gething PW, Williams TN, Weatherall DJ, Hay SI: Global distribution of the sickle cell gene and geographical confirmation of the malaria hypothesis. Nat Commun. 2010, 1: 104-PubMedCentralPubMed Piel FB, Patil AP, Howes RE, Nyangiri OA, Gething PW, Williams TN, Weatherall DJ, Hay SI: Global distribution of the sickle cell gene and geographical confirmation of the malaria hypothesis. Nat Commun. 2010, 1: 104-PubMedCentralPubMed
6.
go back to reference Beet E: Sickle cell disease in the Balovale District of Northern Rhodesia. East Afr Med J. 1946, 23: 75-86.PubMed Beet E: Sickle cell disease in the Balovale District of Northern Rhodesia. East Afr Med J. 1946, 23: 75-86.PubMed
7.
8.
go back to reference Brain P: The sickle cell trait; its clinical significance. S Afr Med J. 1952, 26: 925-928.PubMed Brain P: The sickle cell trait; its clinical significance. S Afr Med J. 1952, 26: 925-928.PubMed
9.
go back to reference Ingram VM: Abnormal human haemoglobins. III. The chemical difference between normal and sickle cell haemoglobins. Biochim Biophys Acta. 1959, 36: 402-411.PubMed Ingram VM: Abnormal human haemoglobins. III. The chemical difference between normal and sickle cell haemoglobins. Biochim Biophys Acta. 1959, 36: 402-411.PubMed
10.
go back to reference Bunn HF: Pathogenesis and treatment of sickle cell disease. N Engl J Med. 1997, 337: 762-769.PubMed Bunn HF: Pathogenesis and treatment of sickle cell disease. N Engl J Med. 1997, 337: 762-769.PubMed
11.
go back to reference Haldane JBS: Disease and evolution. Ric Sci Suppl. 1949, 19: 68-76. Haldane JBS: Disease and evolution. Ric Sci Suppl. 1949, 19: 68-76.
12.
go back to reference Gilles HM, Fletcher KA, Hendrickse RG, Lindner R, Reddy S, Allan N: Glucose-6-phosphate-dehydrogenase deficiency, sickling, and malaria in African children in South Western Nigeria. Lancet. 1967, 1: 138-140.PubMed Gilles HM, Fletcher KA, Hendrickse RG, Lindner R, Reddy S, Allan N: Glucose-6-phosphate-dehydrogenase deficiency, sickling, and malaria in African children in South Western Nigeria. Lancet. 1967, 1: 138-140.PubMed
13.
go back to reference Hill AV, Allsopp CE, Kwiatkowski D, Anstey NM, Twumasi P, Rowe PA, Bennett S, Brewster D, McMichael AJ, Greenwood BM: Common west African HLA antigens are associated with protection from severe malaria. Nature. 1991, 352: 595-600.PubMed Hill AV, Allsopp CE, Kwiatkowski D, Anstey NM, Twumasi P, Rowe PA, Bennett S, Brewster D, McMichael AJ, Greenwood BM: Common west African HLA antigens are associated with protection from severe malaria. Nature. 1991, 352: 595-600.PubMed
14.
go back to reference May J, Evans JA, Timmann C, Ehmen C, Busch W, Thye T, Agbenyega T, Horstmann RD: Hemoglobin variants and disease manifestations in severe falciparum malaria. JAMA. 2007, 297: 2220-2226.PubMed May J, Evans JA, Timmann C, Ehmen C, Busch W, Thye T, Agbenyega T, Horstmann RD: Hemoglobin variants and disease manifestations in severe falciparum malaria. JAMA. 2007, 297: 2220-2226.PubMed
15.
go back to reference Williams TN, Mwangi TW, Roberts DJ, Alexander ND, Weatherall DJ, Wambua S, Kortok M, Snow RW, Marsh K: An immune basis for malaria protection by the sickle cell trait. PLoS Med. 2005, 2: e128-PubMedCentralPubMed Williams TN, Mwangi TW, Roberts DJ, Alexander ND, Weatherall DJ, Wambua S, Kortok M, Snow RW, Marsh K: An immune basis for malaria protection by the sickle cell trait. PLoS Med. 2005, 2: e128-PubMedCentralPubMed
16.
go back to reference 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: Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat Genet. 2009, 41: 657-665.PubMedCentralPubMed 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: Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat Genet. 2009, 41: 657-665.PubMedCentralPubMed
17.
go back to reference Taylor SM, Parobek CM, Fairhurst RM: Haemoglobinopathies and the clinical epidemiology of malaria: a systematic review and meta-analysis. Lancet Infect Dis. 2012, 12: 457-468.PubMedCentralPubMed Taylor SM, Parobek CM, Fairhurst RM: Haemoglobinopathies and the clinical epidemiology of malaria: a systematic review and meta-analysis. Lancet Infect Dis. 2012, 12: 457-468.PubMedCentralPubMed
18.
go back to reference Wambua S, Mwangi TW, Kortok M, Uyoga SM, Macharia AW, Mwacharo JK, Weatherall DJ, Snow RW, Marsh K, Williams TN: The effect of alpha + −thalassaemia on the incidence of malaria and other diseases in children living on the coast of Kenya. PLoS Med. 2006, 3: e158-PubMedCentralPubMed Wambua S, Mwangi TW, Kortok M, Uyoga SM, Macharia AW, Mwacharo JK, Weatherall DJ, Snow RW, Marsh K, Williams TN: The effect of alpha + −thalassaemia on the incidence of malaria and other diseases in children living on the coast of Kenya. PLoS Med. 2006, 3: e158-PubMedCentralPubMed
19.
go back to reference Williams TN, Wambua S, Uyoga S, Macharia A, Mwacharo JK, Newton CRJC, Maitland K: Both heterozygous and homozygous alpha + thalassemias protect against severe and fatal Plasmodium falciparum malaria on the coast of Kenya. Blood. 2005, 106: 368-371.PubMed Williams TN, Wambua S, Uyoga S, Macharia A, Mwacharo JK, Newton CRJC, Maitland K: Both heterozygous and homozygous alpha + thalassemias protect against severe and fatal Plasmodium falciparum malaria on the coast of Kenya. Blood. 2005, 106: 368-371.PubMed
20.
go back to reference Allen SJ, O’Donnell A, Alexander ND, Alpers MP, Peto TE, Clegg JB, Weatherall DJ: alpha + −Thalassemia protects children against disease caused by other infections as well as malaria. Proc Natl Acad Sci USA. 1997, 94: 14736-14741.PubMedCentralPubMed Allen SJ, O’Donnell A, Alexander ND, Alpers MP, Peto TE, Clegg JB, Weatherall DJ: alpha + −Thalassemia protects children against disease caused by other infections as well as malaria. Proc Natl Acad Sci USA. 1997, 94: 14736-14741.PubMedCentralPubMed
21.
go back to reference Mockenhaupt FP, Ehrhardt S, Gellert S, Otchwemah RN, Dietz E, Anemana SD, Bienzle U: Alpha(+)-thalassemia protects African children from severe malaria. Blood. 2004, 104: 2003-2006.PubMed Mockenhaupt FP, Ehrhardt S, Gellert S, Otchwemah RN, Dietz E, Anemana SD, Bienzle U: Alpha(+)-thalassemia protects African children from severe malaria. Blood. 2004, 104: 2003-2006.PubMed
22.
go back to reference Krause MA, Diakite SAS, Lopera-Mesa TM, Amaratunga C, Arie T, Traore K, Doumbia S, Konate D, Keefer JR, Diakite M, Fairhurst RM: α-Thalassemia impairs the cytoadherence of Plasmodium falciparum-infected erythrocytes. PLoS One. 2012, 7: e37214-PubMedCentralPubMed Krause MA, Diakite SAS, Lopera-Mesa TM, Amaratunga C, Arie T, Traore K, Doumbia S, Konate D, Keefer JR, Diakite M, Fairhurst RM: α-Thalassemia impairs the cytoadherence of Plasmodium falciparum-infected erythrocytes. PLoS One. 2012, 7: e37214-PubMedCentralPubMed
23.
go back to reference 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: Reduced risk of Plasmodium vivax malaria in Papua New Guinean children with Southeast Asian ovalocytosis in two cohorts and a case–control study. PLoS Med. 2012, 9: e1001305-PubMedCentralPubMed 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: Reduced risk of Plasmodium vivax malaria in Papua New Guinean children with Southeast Asian ovalocytosis in two cohorts and a case–control study. PLoS Med. 2012, 9: e1001305-PubMedCentralPubMed
24.
go back to reference Hutagalung R, Wilairatana P, Looareesuwan S, Brittenham GM, Aikawa M, Gordeuk VR: Influence of hemoglobin E trait on the severity of Falciparum malaria. J Infect Dis. 1999, 179: 283-286.PubMed Hutagalung R, Wilairatana P, Looareesuwan S, Brittenham GM, Aikawa M, Gordeuk VR: Influence of hemoglobin E trait on the severity of Falciparum malaria. J Infect Dis. 1999, 179: 283-286.PubMed
25.
go back to reference Chotivanich K, Udomsangpetch R, Pattanapanyasat K, Chierakul W, Simpson J, Looareesuwan S, White N: Hemoglobin E: a balanced polymorphism protective against high parasitemias and thus severe P falciparum malaria. Blood. 2002, 100: 1172-1176.PubMed Chotivanich K, Udomsangpetch R, Pattanapanyasat K, Chierakul W, Simpson J, Looareesuwan S, White N: Hemoglobin E: a balanced polymorphism protective against high parasitemias and thus severe P falciparum malaria. Blood. 2002, 100: 1172-1176.PubMed
26.
go back to reference Mockenhaupt FP, Ehrhardt S, Cramer JP, Otchwemah RN, Anemana SD, Goltz K, Mylius F, Dietz E, Eggelte TA, Bienzle U: Hemoglobin C and resistance to severe malaria in Ghanaian children. J Infect Dis. 2004, 190: 1006-1009.PubMed Mockenhaupt FP, Ehrhardt S, Cramer JP, Otchwemah RN, Anemana SD, Goltz K, Mylius F, Dietz E, Eggelte TA, Bienzle U: Hemoglobin C and resistance to severe malaria in Ghanaian children. J Infect Dis. 2004, 190: 1006-1009.PubMed
27.
go back to reference 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: Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature. 2001, 414: 305-308.PubMed 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: Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature. 2001, 414: 305-308.PubMed
28.
go back to reference Agarwal A, Guindo A, Cissoko Y, Taylor JG, Coulibaly D, Koné A, Kayentao K, Djimde A, Plowe CV, Doumbo O, Wellems TE, Diallo D: Hemoglobin C associated with protection from severe malaria in the Dogon of Mali, a West African population with a low prevalence of hemoglobin S. Blood. 2000, 96: 2358-2363.PubMed Agarwal A, Guindo A, Cissoko Y, Taylor JG, Coulibaly D, Koné A, Kayentao K, Djimde A, Plowe CV, Doumbo O, Wellems TE, Diallo D: Hemoglobin C associated with protection from severe malaria in the Dogon of Mali, a West African population with a low prevalence of hemoglobin S. Blood. 2000, 96: 2358-2363.PubMed
29.
go back to reference Williams TN, Mwangi TW, Wambua S, Alexander ND, Kortok M, Snow RW, Marsh K: Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. J Infect Dis. 2005, 192: 178-186.PubMedCentralPubMed Williams TN, Mwangi TW, Wambua S, Alexander ND, Kortok M, Snow RW, Marsh K: Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. J Infect Dis. 2005, 192: 178-186.PubMedCentralPubMed
30.
go back to reference Aidoo M, Terlouw DJ, Kolczak MS, McElroy PD, ter Kuile FO, Kariuki S, Nahlen BL, Lal AA, Udhayakumar V: Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet. 2002, 359: 1311-1312.PubMed Aidoo M, Terlouw DJ, Kolczak MS, McElroy PD, ter Kuile FO, Kariuki S, Nahlen BL, Lal AA, Udhayakumar V: Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet. 2002, 359: 1311-1312.PubMed
31.
go back to reference Marsh K, Otoo L, Hayes RJ, Carson DC, Greenwood BM: Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Trans R Soc Trop Med Hyg. 1989, 83: 293-303.PubMed Marsh K, Otoo L, Hayes RJ, Carson DC, Greenwood BM: Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Trans R Soc Trop Med Hyg. 1989, 83: 293-303.PubMed
32.
go back to reference Clark TD, Greenhouse B, Njama-Meya D, Nzarubara B, Maiteki-Sebuguzi C, Staedke SG, Seto E, Kamya MR, Rosenthal PJ, Dorsey G: Factors determining the heterogeneity of malaria incidence in children in Kampala, Uganda. J Infect Dis. 2008, 198: 393-400.PubMed Clark TD, Greenhouse B, Njama-Meya D, Nzarubara B, Maiteki-Sebuguzi C, Staedke SG, Seto E, Kamya MR, Rosenthal PJ, Dorsey G: Factors determining the heterogeneity of malaria incidence in children in Kampala, Uganda. J Infect Dis. 2008, 198: 393-400.PubMed
33.
go back to reference 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: Sickle cell trait is associated with a delayed onset of malaria: implications for time-to-event analysis in clinical studies of malaria. J Infect Dis. 2008, 198: 1265-1275.PubMedCentralPubMed 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: Sickle cell trait is associated with a delayed onset of malaria: implications for time-to-event analysis in clinical studies of malaria. J Infect Dis. 2008, 198: 1265-1275.PubMedCentralPubMed
34.
go back to reference Kreuels B, Kreuzberg C, Kobbe R, Ayim-Akonor M, Apiah-Thompson P, Thompson B, Ehmen C, Adjei S, Langefeld I, Adjei O, May J: Differing effects of HbS and HbC traits on uncomplicated falciparum malaria, anemia, and child growth. Blood. 2010, 115: 4551-4558.PubMed Kreuels B, Kreuzberg C, Kobbe R, Ayim-Akonor M, Apiah-Thompson P, Thompson B, Ehmen C, Adjei S, Langefeld I, Adjei O, May J: Differing effects of HbS and HbC traits on uncomplicated falciparum malaria, anemia, and child growth. Blood. 2010, 115: 4551-4558.PubMed
35.
go back to reference Gong L, Maiteki-Sebuguzi C, Rosenthal PJ, Hubbard AE, Drakeley CJ, Dorsey G, Greenhouse B: Evidence for both innate and acquired mechanisms of protection from Plasmodium falciparum in children with sickle cell trait. Blood. 2012, 119: 3808-3814.PubMedCentralPubMed Gong L, Maiteki-Sebuguzi C, Rosenthal PJ, Hubbard AE, Drakeley CJ, Dorsey G, Greenhouse B: Evidence for both innate and acquired mechanisms of protection from Plasmodium falciparum in children with sickle cell trait. Blood. 2012, 119: 3808-3814.PubMedCentralPubMed
36.
go back to reference Parikh S, Dorsey G, Rosenthal PJ: Host polymorphisms and the incidence of malaria in Ugandan children. Am J Trop Med Hyg. 2004, 71: 750-753.PubMed Parikh S, Dorsey G, Rosenthal PJ: Host polymorphisms and the incidence of malaria in Ugandan children. Am J Trop Med Hyg. 2004, 71: 750-753.PubMed
37.
go back to reference Motulsky AG, Vandepitte J, Fraser GR: Population genetic studies in the Congo. I. Glucose-6-phosphate dehydrogenase deficiency, hemoglobin S, and malaria. Am J Hum Genet. 1966, 18: 514-537.PubMedCentralPubMed Motulsky AG, Vandepitte J, Fraser GR: Population genetic studies in the Congo. I. Glucose-6-phosphate dehydrogenase deficiency, hemoglobin S, and malaria. Am J Hum Genet. 1966, 18: 514-537.PubMedCentralPubMed
38.
go back to reference Fleming AF, Storey J, Molineaux L, Iroko EA, Attai ED: Abnormal haemoglobins in the Sudan savanna of Nigeria. I. Prevalence of haemoglobins and relationships between sickle cell trait, malaria and survival. Ann Trop Med Parasitol. 1979, 73: 161-172.PubMed Fleming AF, Storey J, Molineaux L, Iroko EA, Attai ED: Abnormal haemoglobins in the Sudan savanna of Nigeria. I. Prevalence of haemoglobins and relationships between sickle cell trait, malaria and survival. Ann Trop Med Parasitol. 1979, 73: 161-172.PubMed
39.
go back to reference Jakobsen PH, Riley EM, Allen SJ, Larsen SO, Bennett S, Jepsen S, Greenwood BM: Differential antibody response of Gambian donors to soluble Plasmodium falciparum antigens. Trans R Soc Trop Med Hyg. 1991, 85: 26-32.PubMed Jakobsen PH, Riley EM, Allen SJ, Larsen SO, Bennett S, Jepsen S, Greenwood BM: Differential antibody response of Gambian donors to soluble Plasmodium falciparum antigens. Trans R Soc Trop Med Hyg. 1991, 85: 26-32.PubMed
40.
go back to reference Migot-Nabias F, Pelleau S, Watier L, Guitard J, Toly C, De Araujo C, Ngom MI, Chevillard C, Gaye O, Garcia A: Red blood cell polymorphisms in relation to Plasmodium falciparum asymptomatic parasite densities and morbidity in Senegal. Microbes Infect. 2006, 8: 2352-2358.PubMed Migot-Nabias F, Pelleau S, Watier L, Guitard J, Toly C, De Araujo C, Ngom MI, Chevillard C, Gaye O, Garcia A: Red blood cell polymorphisms in relation to Plasmodium falciparum asymptomatic parasite densities and morbidity in Senegal. Microbes Infect. 2006, 8: 2352-2358.PubMed
41.
go back to reference Danquah I, Ziniel P, Eggelte TA, Ehrhardt S, Mockenhaupt FP: Influence of haemoglobins S and C on predominantly asymptomatic Plasmodium infections in northern Ghana. Trans R Soc Trop Med Hyg. 2010, 104: 713-719.PubMed Danquah I, Ziniel P, Eggelte TA, Ehrhardt S, Mockenhaupt FP: Influence of haemoglobins S and C on predominantly asymptomatic Plasmodium infections in northern Ghana. Trans R Soc Trop Med Hyg. 2010, 104: 713-719.PubMed
42.
go back to reference 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: Malaria in patients with sickle cell anemia: burden, risk factors, and outcome at the outpatient clinic and during hospitalization. Blood. 2010, 115: 215-220.PubMedCentralPubMed 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: Malaria in patients with sickle cell anemia: burden, risk factors, and outcome at the outpatient clinic and during hospitalization. Blood. 2010, 115: 215-220.PubMedCentralPubMed
43.
go back to reference 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: Sickle cell trait protects against Plasmodium falciparum infection. Am J Epidemiol. 2012, 176 (Suppl 7): S175-185.PubMedCentralPubMed 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: Sickle cell trait protects against Plasmodium falciparum infection. Am J Epidemiol. 2012, 176 (Suppl 7): S175-185.PubMedCentralPubMed
44.
go back to reference Ntoumi F, Rogier C, Dieye A, Trape JF, Millet P, Mercereau-Puijalon O: Imbalanced distribution of Plasmodium falciparum MSP-1 genotypes related to sickle-cell trait. Mol Med. 1997, 3: 581-592.PubMedCentralPubMed Ntoumi F, Rogier C, Dieye A, Trape JF, Millet P, Mercereau-Puijalon O: Imbalanced distribution of Plasmodium falciparum MSP-1 genotypes related to sickle-cell trait. Mol Med. 1997, 3: 581-592.PubMedCentralPubMed
45.
go back to reference Konaté L, Zwetyenga J, Rogier C, Bischoff E, Fontenille D, Tall A, Spiegel A, Trape JF, Mercereau-Puijalon O: Variation of Plasmodium falciparum msp1 block 2 and msp2 allele prevalence and of infection complexity in two neighbouring Senegalese villages with different transmission conditions. Trans R Soc Trop Med Hyg. 1999, 93 (Suppl 1): 21-28.PubMed Konaté L, Zwetyenga J, Rogier C, Bischoff E, Fontenille D, Tall A, Spiegel A, Trape JF, Mercereau-Puijalon O: Variation of Plasmodium falciparum msp1 block 2 and msp2 allele prevalence and of infection complexity in two neighbouring Senegalese villages with different transmission conditions. Trans R Soc Trop Med Hyg. 1999, 93 (Suppl 1): 21-28.PubMed
46.
go back to reference Guggenmoos-Holzmann I, Bienzle U, Luzzatto L: Plasmodium falciparum malaria and human red cells. II. Red cell genetic traits and resistance against malaria. Int J Epidemiol. 1981, 10: 16-22.PubMed Guggenmoos-Holzmann I, Bienzle U, Luzzatto L: Plasmodium falciparum malaria and human red cells. II. Red cell genetic traits and resistance against malaria. Int J Epidemiol. 1981, 10: 16-22.PubMed
47.
go back to reference Luzzatto L, Nwachuku-Jarrett ES, Reddy S: Increased sickling of parasitised erythrocytes as mechanism of resistance against malaria in the sickle-cell trait. Lancet. 1970, 1: 319-321.PubMed Luzzatto L, Nwachuku-Jarrett ES, Reddy S: Increased sickling of parasitised erythrocytes as mechanism of resistance against malaria in the sickle-cell trait. Lancet. 1970, 1: 319-321.PubMed
48.
go back to reference Roth EF, Friedman M, Ueda Y, Tellez I, Trager W, Nagel RL: Sickling rates of human AS red cells infected in vitro with Plasmodium falciparum malaria. Science. 1978, 202: 650-652.PubMed Roth EF, Friedman M, Ueda Y, Tellez I, Trager W, Nagel RL: Sickling rates of human AS red cells infected in vitro with Plasmodium falciparum malaria. Science. 1978, 202: 650-652.PubMed
49.
50.
go back to reference Pasvol G, Weatherall DJ, Wilson RJ: Cellular mechanism for the protective effect of haemoglobin S against P. falciparum malaria. Nature. 1978, 274: 701-703.PubMed Pasvol G, Weatherall DJ, Wilson RJ: Cellular mechanism for the protective effect of haemoglobin S against P. falciparum malaria. Nature. 1978, 274: 701-703.PubMed
51.
go back to reference Orjih AU, Chevli R, Fitch CD: Toxic heme in sickle cells: an explanation for death of malaria parasites. Am J Trop Med Hyg. 1985, 34: 223-227.PubMed Orjih AU, Chevli R, Fitch CD: Toxic heme in sickle cells: an explanation for death of malaria parasites. Am J Trop Med Hyg. 1985, 34: 223-227.PubMed
52.
go back to reference Ginsburg H, Handeli S, Friedman S, Gorodetsky R, Krugliak M: Effects of red blood cell potassium and hypertonicity on the growth of Plasmodium falciparum in culture. Z Parasitenkd. 1986, 72: 185-199.PubMed Ginsburg H, Handeli S, Friedman S, Gorodetsky R, Krugliak M: Effects of red blood cell potassium and hypertonicity on the growth of Plasmodium falciparum in culture. Z Parasitenkd. 1986, 72: 185-199.PubMed
53.
go back to reference Ayi K, Turrini F, Piga A, Arese P: Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Blood. 2004, 104: 3364-3371.PubMed Ayi K, Turrini F, Piga A, Arese P: Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Blood. 2004, 104: 3364-3371.PubMed
54.
go back to reference 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: Translocation of sickle cell erythrocyte microRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell Host Microbe. 2012, 12: 187-199.PubMedCentralPubMed 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: Translocation of sickle cell erythrocyte microRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell Host Microbe. 2012, 12: 187-199.PubMedCentralPubMed
55.
go back to reference Trager W, Rudzinska MA, Bradbury PC: The fine structure of Plasmodium falciparum and its host erythrocytes in natural malarial infections in man. Bull World Health Organ. 1966, 35: 883-885.PubMedCentralPubMed Trager W, Rudzinska MA, Bradbury PC: The fine structure of Plasmodium falciparum and its host erythrocytes in natural malarial infections in man. Bull World Health Organ. 1966, 35: 883-885.PubMedCentralPubMed
56.
go back to reference Udomsangpetch R, Wåhlin B, Carlson J, Berzins K, Torii M, Aikawa M, Perlmann P, Wahlgren M: Plasmodium falciparum-infected erythrocytes form spontaneous erythrocyte rosettes. J Exp Med. 1989, 169: 1835-1840.PubMed Udomsangpetch R, Wåhlin B, Carlson J, Berzins K, Torii M, Aikawa M, Perlmann P, Wahlgren M: Plasmodium falciparum-infected erythrocytes form spontaneous erythrocyte rosettes. J Exp Med. 1989, 169: 1835-1840.PubMed
57.
go back to reference Carlson J, Helmby H, Hill AV, Brewster D, Greenwood BM, Wahlgren M: Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet. 1990, 336: 1457-1460.PubMed Carlson J, Helmby H, Hill AV, Brewster D, Greenwood BM, Wahlgren M: Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet. 1990, 336: 1457-1460.PubMed
58.
go back to reference Treutiger CJ, Hedlund I, Helmby H, Carlson J, Jepson A, Twumasi P, Kwiatkowski D, Greenwood BM, Wahlgren M: Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. Am J Trop Med Hyg. 1992, 46: 503-510.PubMed Treutiger CJ, Hedlund I, Helmby H, Carlson J, Jepson A, Twumasi P, Kwiatkowski D, Greenwood BM, Wahlgren M: Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. Am J Trop Med Hyg. 1992, 46: 503-510.PubMed
59.
go back to reference Aikawa M, Iseki M, Barnwell JW, Taylor D, Oo MM, Howard RJ: The pathology of human cerebral malaria. Am J Trop Med Hyg. 1990, 43: 30-37.PubMed Aikawa M, Iseki M, Barnwell JW, Taylor D, Oo MM, Howard RJ: The pathology of human cerebral malaria. Am J Trop Med Hyg. 1990, 43: 30-37.PubMed
60.
go back to reference 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: Impaired cytoadherence of Plasmodium falciparum-infected erythrocytes containing sickle hemoglobin. Proc Natl Acad Sci USA. 2008, 105: 991-996.PubMedCentralPubMed 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: Impaired cytoadherence of Plasmodium falciparum-infected erythrocytes containing sickle hemoglobin. Proc Natl Acad Sci USA. 2008, 105: 991-996.PubMedCentralPubMed
61.
go back to reference Ockenhouse CF, Tandon NN, Magowan C, Jamieson GA, Chulay JD: Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor. Science. 1989, 243: 1469-1471.PubMed Ockenhouse CF, Tandon NN, Magowan C, Jamieson GA, Chulay JD: Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor. Science. 1989, 243: 1469-1471.PubMed
62.
go back to reference Ockenhouse CF, Shear HL: Malaria-induced lymphokines: stimulation of macrophages for enhanced phagocytosis. Infect Immun. 1983, 42: 733-739.PubMedCentralPubMed Ockenhouse CF, Shear HL: Malaria-induced lymphokines: stimulation of macrophages for enhanced phagocytosis. Infect Immun. 1983, 42: 733-739.PubMedCentralPubMed
63.
go back to reference McGilvray ID, Serghides L, Kapus A, Rotstein OD, Kain KC: Nonopsonic monocyte/macrophage phagocytosis of Plasmodium falciparum-parasitized erythrocytes: a role for CD36 in malarial clearance. Blood. 2000, 96: 3231-3240.PubMed McGilvray ID, Serghides L, Kapus A, Rotstein OD, Kain KC: Nonopsonic monocyte/macrophage phagocytosis of Plasmodium falciparum-parasitized erythrocytes: a role for CD36 in malarial clearance. Blood. 2000, 96: 3231-3240.PubMed
64.
go back to reference Yazdani SS, Mukherjee P, Chauhan VS, Chitnis CE: Immune responses to asexual blood-stages of malaria parasites. Curr Mol Med. 2006, 6: 187-203.PubMed Yazdani SS, Mukherjee P, Chauhan VS, Chitnis CE: Immune responses to asexual blood-stages of malaria parasites. Curr Mol Med. 2006, 6: 187-203.PubMed
65.
go back to reference Kaul DK, Roth EF, 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. 1991, 78: 812-819.PubMed Kaul DK, Roth EF, 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. 1991, 78: 812-819.PubMed
66.
go back to reference Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, Buley ID, Gatter KC, Newbold CI, Pukritayakamee S, Nagachinta B: 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. Am J Pathol. 1994, 145: 1057-1069.PubMedCentralPubMed Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, Buley ID, Gatter KC, Newbold CI, Pukritayakamee S, Nagachinta B: 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. Am J Pathol. 1994, 145: 1057-1069.PubMedCentralPubMed
67.
go back to reference Miller LH, Baruch DI, Marsh K, Doumbo OK: The pathogenic basis of malaria. Nature. 2002, 415: 673-679.PubMed Miller LH, Baruch DI, Marsh K, Doumbo OK: The pathogenic basis of malaria. Nature. 2002, 415: 673-679.PubMed
68.
go back to reference Dondorp AM, Pongponratn E, White NJ: Reduced microcirculatory flow in severe falciparum malaria: pathophysiology and electron-microscopic pathology. Acta Trop. 2004, 89: 309-317.PubMed Dondorp AM, Pongponratn E, White NJ: Reduced microcirculatory flow in severe falciparum malaria: pathophysiology and electron-microscopic pathology. Acta Trop. 2004, 89: 309-317.PubMed
69.
go back to reference 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: Abnormal display of PfEMP-1 on erythrocytes carrying haemoglobin C may protect against malaria. Nature. 2005, 435: 1117-1121.PubMed 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: Abnormal display of PfEMP-1 on erythrocytes carrying haemoglobin C may protect against malaria. Nature. 2005, 435: 1117-1121.PubMed
70.
go back to reference Cyrklaff M, Sanchez CP, Kilian N, Bisseye C, Simpore J, Frischknecht F, Lanzer M: Hemoglobins S and C interfere with actin remodeling in Plasmodium falciparum-infected erythrocytes. Science. 2011, 334: 1283-1286.PubMed Cyrklaff M, Sanchez CP, Kilian N, Bisseye C, Simpore J, Frischknecht F, Lanzer M: Hemoglobins S and C interfere with actin remodeling in Plasmodium falciparum-infected erythrocytes. Science. 2011, 334: 1283-1286.PubMed
71.
go back to reference Cappadoro M, Giribaldi G, O’Brien E, Turrini F, Mannu F, Ulliers D, Simula G, Luzzatto L, Arese P: Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood. 1998, 92: 2527-2534.PubMed Cappadoro M, Giribaldi G, O’Brien E, Turrini F, Mannu F, Ulliers D, Simula G, Luzzatto L, Arese P: Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood. 1998, 92: 2527-2534.PubMed
72.
go back to reference Arese P, Turrini F, Schwarzer E: Band 3/complement-mediated recognition and removal of normally senescent and pathological human erythrocytes. Cell Physiol Biochem. 2005, 16: 133-146.PubMed Arese P, Turrini F, Schwarzer E: Band 3/complement-mediated recognition and removal of normally senescent and pathological human erythrocytes. Cell Physiol Biochem. 2005, 16: 133-146.PubMed
73.
go back to reference 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: Accelerated clearance of Plasmodium-infected erythrocytes in sickle cell trait and annexin-A7 deficiency. Cell Physiol Biochem. 2009, 24: 415-428.PubMed 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: Accelerated clearance of Plasmodium-infected erythrocytes in sickle cell trait and annexin-A7 deficiency. Cell Physiol Biochem. 2009, 24: 415-428.PubMed
74.
go back to reference Tanaka Y, Schroit AJ: Insertion of fluorescent phosphatidylserine into the plasma membrane of red blood cells. Recognition by autologous macrophages. J Biol Chem. 1983, 258: 11335-11343.PubMed Tanaka Y, Schroit AJ: Insertion of fluorescent phosphatidylserine into the plasma membrane of red blood cells. Recognition by autologous macrophages. J Biol Chem. 1983, 258: 11335-11343.PubMed
75.
go back to reference Schroit AJ, Madsen JW, Tanaka Y: In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membranes. J Biol Chem. 1985, 260: 5131-5138.PubMed Schroit AJ, Madsen JW, Tanaka Y: In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membranes. J Biol Chem. 1985, 260: 5131-5138.PubMed
76.
go back to reference Boas FE, Forman L, Beutler E: Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia. Proc Natl Acad Sci USA. 1998, 95: 3077-3081.PubMedCentralPubMed Boas FE, Forman L, Beutler E: Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia. Proc Natl Acad Sci USA. 1998, 95: 3077-3081.PubMedCentralPubMed
77.
go back to reference Hoffmann PR, de Cathelineau AM, Ogden CA, Leverrier Y, Bratton DL, Daleke DL, Ridley AJ, Fadok VA, Henson PM: Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J Cell Biol. 2001, 155: 649-659.PubMedCentralPubMed Hoffmann PR, de Cathelineau AM, Ogden CA, Leverrier Y, Bratton DL, Daleke DL, Ridley AJ, Fadok VA, Henson PM: Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J Cell Biol. 2001, 155: 649-659.PubMedCentralPubMed
78.
go back to reference Urban BC, Shafi MJ, Cordery DV, Macharia A, Lowe B, Marsh K, Williams TN: Frequencies of peripheral blood myeloid cells in healthy Kenyan children with alpha + thalassemia and the sickle cell trait. Am J Trop Med Hyg. 2006, 74: 578-584.PubMedCentralPubMed Urban BC, Shafi MJ, Cordery DV, Macharia A, Lowe B, Marsh K, Williams TN: Frequencies of peripheral blood myeloid cells in healthy Kenyan children with alpha + thalassemia and the sickle cell trait. Am J Trop Med Hyg. 2006, 74: 578-584.PubMedCentralPubMed
79.
go back to reference Jepsen S, Andersen BJ: Immunoadsorbent isolation of antigens from the culture medium of in vitro cultivated Plasmodium falciparum. Acta Pathol Microbiol Scand C. 1981, 89: 99-103.PubMed Jepsen S, Andersen BJ: Immunoadsorbent isolation of antigens from the culture medium of in vitro cultivated Plasmodium falciparum. Acta Pathol Microbiol Scand C. 1981, 89: 99-103.PubMed
80.
go back to reference Bygbjerg IC, Jepsen S, Theander TG, Odum N: Specific proliferative response of human lymphocytes to purified soluble antigens from Plasmodium falciparum in vitro cultures and to antigens from malaria patients’ sera. Clin Exp Immunol. 1985, 59: 421-426.PubMedCentralPubMed Bygbjerg IC, Jepsen S, Theander TG, Odum N: Specific proliferative response of human lymphocytes to purified soluble antigens from Plasmodium falciparum in vitro cultures and to antigens from malaria patients’ sera. Clin Exp Immunol. 1985, 59: 421-426.PubMedCentralPubMed
81.
go back to reference Riley EM, Andersson G, Otoo LN, Jepsen S, Greenwood BM: Cellular immune responses to Plasmodium falciparum antigens in Gambian children during and after an acute attack of falciparum malaria. Clin Exp Immunol. 1988, 73: 17-22.PubMedCentralPubMed Riley EM, Andersson G, Otoo LN, Jepsen S, Greenwood BM: Cellular immune responses to Plasmodium falciparum antigens in Gambian children during and after an acute attack of falciparum malaria. Clin Exp Immunol. 1988, 73: 17-22.PubMedCentralPubMed
82.
go back to reference Bayoumi RA, Abu-Zeid YA, Abdulhadi NH, Saeed BO, Theander TG, Hviid L, Ghalib HW, Nugud AH, Jepsen S, Jensen JB: Cell-mediated immune responses to Plasmodium falciparum purified soluble antigens in sickle-cell trait subjects. Immunol Lett. 1990, 25: 243-249.PubMed Bayoumi RA, Abu-Zeid YA, Abdulhadi NH, Saeed BO, Theander TG, Hviid L, Ghalib HW, Nugud AH, Jepsen S, Jensen JB: Cell-mediated immune responses to Plasmodium falciparum purified soluble antigens in sickle-cell trait subjects. Immunol Lett. 1990, 25: 243-249.PubMed
83.
go back to reference Abu-Zeid YA, Abdulhadi NH, Hviid L, Theander TG, Saeed BO, Jepsen S, Jensen JB, Bayoumi RA: Lymphoproliferative responses to Plasmodium falciparum antigens in children with and without the sickle cell trait. Scand J Immunol. 1991, 34: 237-242.PubMed Abu-Zeid YA, Abdulhadi NH, Hviid L, Theander TG, Saeed BO, Jepsen S, Jensen JB, Bayoumi RA: Lymphoproliferative responses to Plasmodium falciparum antigens in children with and without the sickle cell trait. Scand J Immunol. 1991, 34: 237-242.PubMed
84.
go back to reference Abu-Zeid YA, Theander TG, Abdulhadi NH, Hviid L, Saeed BO, Jepsen S, Jensen JB, Bayoumi RA: Modulation of the cellular immune response during Plasmodium falciparum infections in sickle cell trait individuals. Clin Exp Immunol. 1992, 88: 112-118.PubMedCentralPubMed Abu-Zeid YA, Theander TG, Abdulhadi NH, Hviid L, Saeed BO, Jepsen S, Jensen JB, Bayoumi RA: Modulation of the cellular immune response during Plasmodium falciparum infections in sickle cell trait individuals. Clin Exp Immunol. 1992, 88: 112-118.PubMedCentralPubMed
85.
go back to reference Le Hesran JY, Personne I, Personne P, Fievet N, Dubois B, Beyemé M, Boudin C, Cot M, Deloron P: Longitudinal study of Plasmodium falciparum infection and immune responses in infants with or without the sickle cell trait. Int J Epidemiol. 1999, 28: 793-798.PubMed Le Hesran JY, Personne I, Personne P, Fievet N, Dubois B, Beyemé M, Boudin C, Cot M, Deloron P: Longitudinal study of Plasmodium falciparum infection and immune responses in infants with or without the sickle cell trait. Int J Epidemiol. 1999, 28: 793-798.PubMed
86.
go back to reference Brasseur P, Agrapart M, Ballet JJ, Druilhe P, Warrell MJ, Tharavanij S: Impaired cell-mediated immunity in Plasmodium falciparum-infected patients with high-parasitemia and cerebral malaria. Clin Immunol Immunopathol. 1983, 27: 38-50.PubMed Brasseur P, Agrapart M, Ballet JJ, Druilhe P, Warrell MJ, Tharavanij S: Impaired cell-mediated immunity in Plasmodium falciparum-infected patients with high-parasitemia and cerebral malaria. Clin Immunol Immunopathol. 1983, 27: 38-50.PubMed
87.
go back to reference Ho M, Webster HK, Looareesuwan S, Supanaranond W, Phillips RE, Chanthavanich P, Warrell DA: Antigen-specific immunosuppression in human malaria due to Plasmodium falciparum. J Infect Dis. 1986, 153: 763-771.PubMed Ho M, Webster HK, Looareesuwan S, Supanaranond W, Phillips RE, Chanthavanich P, Warrell DA: Antigen-specific immunosuppression in human malaria due to Plasmodium falciparum. J Infect Dis. 1986, 153: 763-771.PubMed
88.
go back to reference Theander TG, Bygbjerg IC, Andersen BJ, Jepsen S, Kharazmi A, Odum N: Suppression of parasite-specific response in Plasmodium falciparum malaria. A longitudinal study of blood mononuclear cell proliferation and subset composition. Scand J Immunol. 1986, 24: 73-81.PubMed Theander TG, Bygbjerg IC, Andersen BJ, Jepsen S, Kharazmi A, Odum N: Suppression of parasite-specific response in Plasmodium falciparum malaria. A longitudinal study of blood mononuclear cell proliferation and subset composition. Scand J Immunol. 1986, 24: 73-81.PubMed
89.
go back to reference Angulo I, Fresno M: Cytokines in the pathogenesis of and protection against malaria. Clin Diagn Lab Immunol. 2002, 9: 1145-1152.PubMedCentralPubMed Angulo I, Fresno M: Cytokines in the pathogenesis of and protection against malaria. Clin Diagn Lab Immunol. 2002, 9: 1145-1152.PubMedCentralPubMed
90.
go back to reference Edozien JC, Boyo AE, Morley DC: The relationship of serum gamma-globulin concentration to malaria and sickling. J Clin Pathol. 1960, 13: 118-123.PubMedCentralPubMed Edozien JC, Boyo AE, Morley DC: The relationship of serum gamma-globulin concentration to malaria and sickling. J Clin Pathol. 1960, 13: 118-123.PubMedCentralPubMed
91.
go back to reference Cornille-Brøgger R, Fleming AF, Kagan I, Matsushima T, Molineaux L: Abnormal haemoglobins in the Sudan savanna of Nigeria. II. Immunological response to malaria in normals and subjects with sickle cell trait. Ann Trop Med Parasitol. 1979, 73: 173-183.PubMed Cornille-Brøgger R, Fleming AF, Kagan I, Matsushima T, Molineaux L: Abnormal haemoglobins in the Sudan savanna of Nigeria. II. Immunological response to malaria in normals and subjects with sickle cell trait. Ann Trop Med Parasitol. 1979, 73: 173-183.PubMed
92.
go back to reference Dziegiel M, Rowe P, Bennett S, Allen SJ, Olerup O, Gottschau A, Borre M, Riley EM: Immunoglobulin M and G antibody responses to Plasmodium falciparum glutamate-rich protein: correlation with clinical immunity in Gambian children. Infect Immun. 1993, 61: 103-108.PubMedCentralPubMed Dziegiel M, Rowe P, Bennett S, Allen SJ, Olerup O, Gottschau A, Borre M, Riley EM: Immunoglobulin M and G antibody responses to Plasmodium falciparum glutamate-rich protein: correlation with clinical immunity in Gambian children. Infect Immun. 1993, 61: 103-108.PubMedCentralPubMed
93.
go back to reference Aluoch JR: Higher resistance to Plasmodium falciparum infection in patients with homozygous sickle cell disease in western Kenya. Trop Med Int Health. 1997, 2: 568-571.PubMed Aluoch JR: Higher resistance to Plasmodium falciparum infection in patients with homozygous sickle cell disease in western Kenya. Trop Med Int Health. 1997, 2: 568-571.PubMed
94.
go back to reference Aucan C, Traoré Y, Tall F, Nacro B, Traoré-Leroux T, Fumoux F, Rihet P: High immunoglobulin G2 (IgG2) and low IgG4 levels are associated with human resistance to Plasmodium falciparum malaria. Infect Immun. 2000, 68: 1252-1258.PubMedCentralPubMed Aucan C, Traoré Y, Tall F, Nacro B, Traoré-Leroux T, Fumoux F, Rihet P: High immunoglobulin G2 (IgG2) and low IgG4 levels are associated with human resistance to Plasmodium falciparum malaria. Infect Immun. 2000, 68: 1252-1258.PubMedCentralPubMed
95.
go back to reference 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: Antibody responses to Plasmodium falciparum: evolution according to the severity of a prior clinical episode and association with subsequent reinfection. Am J Trop Med Hyg. 2000, 62: 566-572.PubMed 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: Antibody responses to Plasmodium falciparum: evolution according to the severity of a prior clinical episode and association with subsequent reinfection. Am J Trop Med Hyg. 2000, 62: 566-572.PubMed
96.
go back to reference 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: Relationship between malaria incidence and IgG levels to Plasmodium falciparum merozoite antigens in Malian children: impact of hemoglobins S and C. PLoS ONE. 2013, 8: e60182-PubMedCentralPubMed 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: Relationship between malaria incidence and IgG levels to Plasmodium falciparum merozoite antigens in Malian children: impact of hemoglobins S and C. PLoS ONE. 2013, 8: e60182-PubMedCentralPubMed
97.
go back to reference Tan X, Traore B, Kayentao K, Ongoiba A, Doumbo S, Waisberg M, Doumbo OK, Felgner PL, Fairhurst RM, Crompton PD: Hemoglobin S and C heterozygosity enhances neither the magnitude nor breadth of antibody responses to a diverse array of Plasmodium falciparum antigens. J Infect Dis. 2011, 204: 1750-1761.PubMedCentralPubMed Tan X, Traore B, Kayentao K, Ongoiba A, Doumbo S, Waisberg M, Doumbo OK, Felgner PL, Fairhurst RM, Crompton PD: Hemoglobin S and C heterozygosity enhances neither the magnitude nor breadth of antibody responses to a diverse array of Plasmodium falciparum antigens. J Infect Dis. 2011, 204: 1750-1761.PubMedCentralPubMed
98.
go back to reference 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: Haemoglobin C and S role in acquired immunity against Plasmodium falciparum malaria. PLoS ONE. 2007, 2: e978-PubMedCentralPubMed 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: Haemoglobin C and S role in acquired immunity against Plasmodium falciparum malaria. PLoS ONE. 2007, 2: e978-PubMedCentralPubMed
99.
go back to reference Sarr JB, Pelleau S, Toly C, Guitard J, Konaté L, Deloron P, Garcia A, Migot-Nabias F: Impact of red blood cell polymorphisms on the antibody response to Plasmodium falciparum in Senegal. Microbes Infect. 2006, 8: 1260-1268.PubMed Sarr JB, Pelleau S, Toly C, Guitard J, Konaté L, Deloron P, Garcia A, Migot-Nabias F: Impact of red blood cell polymorphisms on the antibody response to Plasmodium falciparum in Senegal. Microbes Infect. 2006, 8: 1260-1268.PubMed
100.
go back to reference Diatta A-M, Marrama L, Tall A, Trape J-F, Dieye A, Garraud O, Mercereau-Puijalon O, Perraut R: Relationship of binding of immunoglobulin G to Plasmodium falciparum-infected erythrocytes with parasite endemicity and antibody responses to conserved antigen in immune individuals. Clin Diagn Lab Immuno. 2004, 11: 6-11. Diatta A-M, Marrama L, Tall A, Trape J-F, Dieye A, Garraud O, Mercereau-Puijalon O, Perraut R: Relationship of binding of immunoglobulin G to Plasmodium falciparum-infected erythrocytes with parasite endemicity and antibody responses to conserved antigen in immune individuals. Clin Diagn Lab Immuno. 2004, 11: 6-11.
101.
go back to reference Cabrera G, Cot M, Migot-Nabias F, Kremsner PG, Deloron P, Luty AJF: The sickle cell trait is associated with enhanced immunoglobulin G antibody responses to Plasmodium falciparum variant surface antigens. J Infect Dis. 2005, 191: 1631-1638.PubMed Cabrera G, Cot M, Migot-Nabias F, Kremsner PG, Deloron P, Luty AJF: The sickle cell trait is associated with enhanced immunoglobulin G antibody responses to Plasmodium falciparum variant surface antigens. J Infect Dis. 2005, 191: 1631-1638.PubMed
102.
go back to reference Allen SJ, Bennett S, Riley EM, Rowe PA, Jakobsen PH, O’Donnell A, Greenwood BM: Morbidity from malaria and immune responses to defined Plasmodium falciparum antigens in children with sickle cell trait in The Gambia. Trans R Soc Trop Med Hyg. 1992, 86: 494-498.PubMed Allen SJ, Bennett S, Riley EM, Rowe PA, Jakobsen PH, O’Donnell A, Greenwood BM: Morbidity from malaria and immune responses to defined Plasmodium falciparum antigens in children with sickle cell trait in The Gambia. Trans R Soc Trop Med Hyg. 1992, 86: 494-498.PubMed
103.
go back to reference Langhorne J, Ndungu FM, Sponaas A-M, Marsh K: Immunity to malaria: more questions than answers. Nat Immunol. 2008, 9: 725-732.PubMed Langhorne J, Ndungu FM, Sponaas A-M, Marsh K: Immunity to malaria: more questions than answers. Nat Immunol. 2008, 9: 725-732.PubMed
104.
go back to reference Ferreira A, Marguti I, Bechmann I, Jeney V, Chora A, Palha NR, Rebelo S, Henri A, Beuzard Y, Soares MP: Sickle hemoglobin confers tolerance to Plasmodium infection. Cell. 2011, 145: 398-409.PubMed Ferreira A, Marguti I, Bechmann I, Jeney V, Chora A, Palha NR, Rebelo S, Henri A, Beuzard Y, Soares MP: Sickle hemoglobin confers tolerance to Plasmodium infection. Cell. 2011, 145: 398-409.PubMed
Metadata
Title
Biochemical and immunological mechanisms by which sickle cell trait protects against malaria
Authors
Lauren Gong
Sunil Parikh
Philip J Rosenthal
Bryan Greenhouse
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2013
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-12-317

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