Haemoglobinopathies and resistance to malaria

REFERENCES

• Beet EA. Sickle cell disease in the Balovale district of Northern Rhodesia. East Afr Med J 1946; 23: 75–86.
   PubMedGoogle Scholar
• Allison AC. Protection afforded by sickle cell trait against subtertian malarial infection. BMJ 1954; 1: 290–295.
   PubMed Web of Science ®Google Scholar
• Haldane JB S. The rate of mutation of human genes. Hereditas, 1949; Suppl 35: 267-273.
   Google Scholar
• 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 Web of Science ®Google Scholar
• 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 Web of Science ®Google Scholar
• Jakobsen PH, Riley EM, Allen SJ et al. Differential antibody response of Gambian donors to soluble Plasmodium falciparum antigens. Trans R Soc Trop Med Hyg 1991; 85: 26–32.
   PubMed Web of Science ®Google Scholar
• Weatherall DJ, Clegg J. The Thalassaemias. Oxford: Oxford University Press, 2002.
   Google Scholar
• Allen SJ, O'Donnell A, Alexander ND et al. alphatThalassemia protects children against disease caused by other infections as well as malaria. Proc Nail Acad Sci USA 1997; 94: 14736–14741.
   PubMed Web of Science ®Google Scholar
• Willcox M, Bjorkman A, Brohult J, Pehrson PO, Rombo L, Bengtsson E. A case-control study in northern Liberia of Plasmodium falciparum malaria in haemoglobin S and beta-thalassaemia traits. Ann Trop Med Parasitol 1983; 77: 239–246.
   PubMed Web of Science ®Google Scholar
• Oppenheimer SJ, Hill AV, Gibson FD, Macfarlane SB, Moody JB, Pringle J. The interaction of alpha thalassaemia with malaria. Trans R Soc Trop Med Hyg 1987; 81: 322–326.
   PubMed Web of Science ®Google Scholar
• Williams TN, Maitland K, Bennett S et al. High incidence of malaria in alpha-thalassaemic children. Nature 1996; 383: 522–525.
   PubMed Web of Science ®Google Scholar
• Williams TN, Maitland K, Ganczakowski M et al. Red blood cell phenotypes in the alpha thalassaemias from early childhood to maturity. Br J Haematol 1996; 95: 266–272.
   PubMed Web of Science ®Google Scholar
• Fairhurst RM, Fujioka H, Hayton K, Collins KF, Wellems TE. Aberrant development of Plasmodium falciparum in hemoglobin CC red cells: implications for the malaria protective effect of the homozygous state. Blood 2003; 101: 3309–3315.
   PubMed Web of Science ®Google Scholar
• Schrier SL. Pathophysiology of thalassemia. Curr Opin Hematol 2002; 9: 123–126.
   PubMed Web of Science ®Google Scholar
• Akide-Ndunge OB, Ayi K, Arese P. The Haldane malaria hypothesis. Facts, artifacts, and a prophecy. Redox Report 2003; 8: 301–306.
   Web of Science ®Google Scholar
• Ho M, White NJ. Molecular mechanisms of cytoadherence in malaria. Am J Physiol 1999; 276: C1231–C1242.
   PubMed Web of Science ®Google Scholar
• Craig A, Scherf A. Molecules on the surface of the Plasmodium falciparum infected erythrocyte and their role in malaria pathogenesis and immune evasion. Mol Biochem Parasitol 2001; 115: 129–143.
   PubMed Web of Science ®Google Scholar
• Bunyaratvej A, Butthep P, Yuthavong Y et al. Increased phagocytosis of Plasmodium falciparum-infected erythrocytes with haemoglobin E by peripheral blood monocytes. Ada Haematol 1986; 76: 155–158.
   Web of Science ®Google Scholar
• Yuthavong Y, Butthep P, Bunyaratvej A, Fucharoen S, Khusmith S. Impaired parasite growth and increased susceptibility to phagocytosis of Plasmodium falciparum infected alpha-thalassemia or hemoglobin Constant Spring red blood cells. Am J Clin Pathol 1988; 89: 521–525.
   PubMed Web of Science ®Google Scholar
• Shear HL, Roth Jr EF, Fabry ME et al. Transgenic mice expressing human sickle hemoglobin are partially resistant to rodent malaria. Blood 1993; 81: 222–226.
   PubMed Web of Science ®Google Scholar
• Cappadoro M, Giribaldi G, O'Brien E et al. 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 Web of Science ®Google Scholar
• Schwarzer E, Turrini F, Giribaldi G, Cappadoro M, Arese P. Phagocytosis of P. falciparum malarial pigment hemozoin by human monocytes inactivates monocyte protein kinase C. Biochim Biophys Acta 1993; 1181: 51–54.
   PubMed Web of Science ®Google Scholar
• Taramelli D, Basilico N, De Palma AM et al. The effect of synthetic malaria pigment (beta-haematin) on adhesion molecule expression and interleukin-6 production by human endothelial cells. Trans R Soc Trop Med Hyg 1998; 92: 57–62.
   PubMed Web of Science ®Google Scholar
• Omodeo-Sale MF, Motti A, Basilico N, Parapini S, O11iaro P, Taramelli D. Accelerated senescence of human erythrocytes cultured with Plasmodium falciparum. Blood 2003; 196: 190–195.
   Google Scholar
• McGilvray ID, Serghides 1, Kapus A, Rotstein OD, Kain KC. Non-opsonic monocyte/macrophage phagocytosis of Plasmodium falciparum-parasitized erythrocytes: a role for CD36 in malarial clearance. Blood 2000; 96: 3231–3240.
   PubMed Web of Science ®Google Scholar
• Urban BC, Ferguson DJ, Pain A et al. Plasmodium falciparum- infected erythrocytes modulate the maturation of dendritic cells. Nature 1999; 400: 73–77.
   PubMed Web of Science ®Google Scholar
• Urban BC, Roberts DJ. Malaria, monocytes, macrophages and myeloid dendritic cells: sticking of infected erythrocytes switches off host cells. Curr Opin Immunol 2002; 14: 458–465.
   PubMed Web of Science ®Google Scholar
• 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 Web of Science ®Google Scholar
• Bayoumi RA. The sickle-cell trait modifies the intensity and specificity of the immune response against P. falciparum malaria and leads to acquired protective immunity. Med Hypotheses 1987; 22: 287–298.
   PubMed Web of Science ®Google Scholar
• Abu-Zeid YA, Abdulhadi NH, Theander TG et al. Seasonal changes in cell mediated immune responses to soluble antigens in children with haemoglobin AA and haemoglobin AS. Trans R Soc Trop Med Hyg 1992; 86: 20–22.
   PubMed Web of Science ®Google Scholar
• Aidoo M, Terlouw DJ, Kolczak MS et al. Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet 2002; 359: 1311–1312.
   PubMed Web of Science ®Google Scholar
• Allen SJ, Bennett S, Riley EM et al. 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 Web of Science ®Google Scholar
• Hill AV, Allsopp CE, Kwiatkowski D et al. Common west African HLA antigens are associated with protection from severe malaria. Nature 1991; 352: 595–600.
   PubMed Web of Science ®Google Scholar
• Marsh K. Malaria - a neglected disease? Parasitology 1992; 104 ( Suppl): S53-S69.
   Google Scholar
• Flint J, Hill AV, Bowden DK et al. High frequencies of alpha-thalassaemia are the result of natural selection by malaria. Nature 1986; 321: 744–750.
   PubMed Web of Science ®Google Scholar
• Yenchitsomanus P, Summers KM, Board PG et al. Alpha-thalassemia in Papua New Guinea. Hum Genet 1986; 74: 432–437.
   PubMed Web of Science ®Google Scholar
• Siniscalco M, Bernini L, Latte B, Motulski AG. Favism and thalassaemia in Sardinia and their relationship to malaria. Nature 1961; 190: 1179–1180.
   Web of Science ®Google Scholar
• Hill AV, Bowden DK, O'Shaughnessy DF, Weatherall DJ, Clegg JB. Beta thalassemia in Melanesia: association with malaria and characterization of a common variant (IVS-1 nt 5 G-C). Blood 1988; 72: 9–14.
   PubMed Web of Science ®Google Scholar
• Flatz G, Pik C, Sringam S. Haemoglobin E and beta-thalassaemia: their distribution in Thailand. Ann Hum Genet 1965; 29: 151–170.
   PubMed Web of Science ®Google Scholar
• Agarwal A, Guindo A, Cissoko Y et al. 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 Web of Science ®Google Scholar
• Modiano D, Luoni G, Sirima BS et al. Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature 2001; 414: 305–308.
   PubMed Web of Science ®Google Scholar
• Nagel RL, Raventos-Suarez C, Fabry ME, Tanowitz H, Sicard D, Labie D. Impairment of the growth of Plasmodium falciparum in HbEE erythrocytes. J Clin Invest 1981; 68: 303–305.
   PubMed Web of Science ®Google Scholar
• Ifediba TC, Stem A, Ibrahim A, Rieder RF. Plasmodium falciparum in vitro: diminished growth in hemoglobin H disease erythrocytes. Blood 1985; 65: 452–455.
   PubMed Web of Science ®Google Scholar
• Brockelman CR, Wongsattayanont B, Tan-ariya P. Fucharoen S. Thalassemic erythrocytes inhibit in vitro growth of Plasmodium falciparum. J Clin Microbiol 1987; 25: 56–60.
   Google Scholar
• Bunyaratvej A, Butthep P, Sae-Ung N, Fucharoen S, Yuthavong Y. Reduced deformability of thalassemic erythrocytes and erythrocytes with abnormal hemoglobins and relation with susceptibility to Plasmodium falciparum invasion. Blood 1992; 79: 2460–2463.
   PubMed Web of Science ®Google Scholar
• Friedman MJ, Roth EF, Nagel RL, Trager W. The role of hemoglobins C, S, and Nbalt in the inhibition of malaria parasite development in vitro. Am J Trop Med Hyg 1979; 28: 777–780.
   PubMed Web of Science ®Google Scholar
• Kaminsky R, Kruger N, Hempelmann E, Bommer W. Reduced development of Plasmodium falciparum in beta-thalassaemic erythrocytes. Z Parasitenkd 1986; 72: 553–556.
   PubMed Web of Science ®Google Scholar
• Luzzi GA, Toni M, Aikawa M, Pasvol G. Unrestricted growth of Plasmodium falciparum in microcytic erythrocytes in iron deficiency and thalassaemia. Br J Haematol 1990; 74: 519–524.
   PubMed Web of Science ®Google Scholar
• Williams TN, Weatherall DJ, Newbold CI. The membrane characteristics of Plasmodium falciparum-infected and - uninfected heterozygous alpha() thalassaemic erythrocytes. Br J Haematol 2002; 118: 663–670.
   PubMed Web of Science ®Google Scholar
• Udomsangpetch R, Sueblinvong T, Pattanapanyasat K, Dharmkrong-at A, Kittikalayawong A, Webster HK. Alteration in cytoadherence and rosetting of Plasmodium falciparum-infected thalassemic red blood cells. Blood 1993; 82: 3752–3759.
   PubMed Web of Science ®Google Scholar
• Senok AC, Li K, Nelson EA, Yu LM, Tian LP, Oppenheimer SJ.Invasion and growth of Plasmodium falciparum is inhibited in fractionated thalassaemic erythrocytes. Trans R Soc Trop Med Hyg 1997; 91: 138–143.
   PubMed Web of Science ®Google Scholar
• Roth Jr 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 Web of Science ®Google Scholar
• 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 Web of Science ®Google Scholar
• Friedman MJ. Erythrocytic mechanism of sickle cell resistance to malaria. Proc Natl Acad Sci USA 1978; 75: 1994–1997.
   PubMed Web of Science ®Google Scholar
• Carlson J, Nash GB, Gabutti V. al-Yaman F, Wahlgren M. Natural protection against severe Plasmodium falciparum malaria due to impaired rosette formation. Blood 1994; 84: 3909–3914.
   PubMed Web of Science ®Google Scholar
• Udomsangpetch R, Todd J, Carlson J, Greenwood BM. The effects of hemoglobin genotype and ABO blood group on the formation of rosettes by Plasmodium falciparum-infected red blood cells. Am J Trop Med Hyg 1993; 48: 149–153.
   PubMed Web of Science ®Google Scholar
• Luzzi GA, Merry AH, Newbold C, Marsh K, Pasvol G.Protection by alpha-thalassaemia against Plasmodium falciparum malaria: modified surface antigen expression rather than impaired growth or cytoadherence. Immunol Lett 1991; 30: 233–240.
   PubMed Web of Science ®Google Scholar
• Lutz HU, Bussolino F, Flepp R, Fasler S, Stammler P. Kazatchkine MD, Arese P Naturally occurring anti-band-3 antibodies and complement together mediate phagocytosis of oxidatively stressed human erythrocytes. Proc Natl Acad Sci USA 1987; 84: 7368–7372.
   PubMed Web of Science ®Google Scholar
• Luzzatto L, Usanga FA, Reddy S. Glucose-6-phosphate dehydrogenase deficient red cells: resistance to infection by malarial parasites. Science 1969; 164: 839–842.
   PubMed Web of Science ®Google Scholar
• Ocana-Morgner C, Mota MM, Rodriguez A. Malaria blood stage suppression of liver stage immunity by dendritic cells. J Exp Med 2003; 197: 143–151.
   PubMed Web of Science ®Google Scholar
• Urban BC, Willcox N, Roberts DJ. A role for CD36 in the regulation of dendritic cell function. Proc Natl Acad Sci USA 2001; 98: 8750–8755.
   PubMed Web of Science ®Google Scholar