Genetic variation and susceptibility to infection: The red cell and malaria

British Journal of Haematology

Volumn 141, Issue 3, 2008, Pages 276-286

  Weatherall, D J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Genetics; Malaria; Red cells

Indexed keywords

HEMOGLOBIN; HEMOGLOBIN C; HEMOGLOBIN E; HEMOGLOBIN S;

ALPHA THALASSEMIA; BETA THALASSEMIA; BLOOD GROUP; CONFERENCE PAPER; DISEASE PREDISPOSITION; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; ERYTHROCYTE METABOLISM; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GLUCOSE 6 PHOSPHATE DEHYDROGENASE DEFICIENCY; HUMAN; MALARIA; PRIORITY JOURNAL;

BLOOD GROUP ANTIGENS; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; GENETIC PREDISPOSITION TO DISEASE; GLYCOGEN STORAGE DISEASE TYPE I; HEMOGLOBINOPATHIES; HUMANS; MALARIA; VARIATION (GENETICS);

EID: 42049110421     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2008.07085.x     Document Type: Conference Paper

References (85)

1. Aidoo, M., Terlouw, D.J., Kolczak, M.S., McElroy, P.D., ter Kuile, F.O., Kariuki, S., Nahlen, B.L., Lal, A.A. Udhayakumar, V. (2002) Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet, 359, 1311 1312.
2. Aitman, T.J., Cooper, L.D., Norsworthy, P.J., Wahid, F.N., Gray, J.K., Curtis, B.R., McKeigue, P.M., Kwiatkowski, D., Greenwood, B.M., Snow, R.W., Hill, A.V. Scott, J. (2000) Malaria susceptibility and CD36 mutation. Nature, 405, 1015 1016.
3. +-Thalassaemia protects children against disease due to malaria and other infections. Proceedings of the National Academy of Sciences of the United States of America, 94, 14736 14741.
4. Allen, S.J., O'Donnell, A., Alexander, N.D.E., Mgone, C.S., Peto, T.E.A., Clegg, J.B., Alpers, M.P. Weatherall, D.J. (1999) Prevention of cerebral malaria in children in Papua New Guinea by southeast Asian ovalocytosis band 3. American Journal of Tropical Medicine and Hygiene, 60, 1056 1060.
5. Allison, A.C. (1965) Population genetics of abnormal haemoglobins and glucose-6-phosphate dehydrogenase deficiency. In : Abnormal Haemoglobins in Africa (ed. by J.H.P. Jonxis pp. 365. Blackwell Scientific Publications, Oxford.
6. Barragan, A., Kremsner, P.G., Wahlgren, M. Carlson, J. (2000) Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infection and Immunity, 68, 2971 2975.
7. Bellamy, R., Kwiatkowski, D. Hill, A.V. (1998) Absence of an association between intercellular adhesion molecule 1, complement receptor 1 and interleukin 1 receptor antagonist gene polymorphisms and severe malaria in a West African population. Transaction of the Royal Society of Tropical Medicine and Hygiene, 92, 312 316.
8. Bruce-Chwatt, L.J. de Zulueta, J. (1980) The Rise and Fall of Malaria in Europe. A Historico-Epidemiological Study. Oxford University Press, Oxford.
9. Cabrera, G., Cot, M., Migot-Nabias, F., Kremsner, P.G., Deloron, P. Luty, A.J. (2005) The sickle cell trait is associated with enhanced immunoglobulin G antibody responses to Plasmodium falciparum variant surface antigens. Journal of Infectious Diseases, 191, 1631 1638.
10. Cappadoro, M., Giribaldi, G., O'Brien, E., Turrini, F., Mannu, F., Ulliers, D., Simula, G., Luzzatto, L. Arese, P. (1998) Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood, 92, 2527 2534.
11. Carter, R. Mendis, K.N. (2002) Evolutionary and historical aspects of the burden of malaria. Clinical Microbiology Reviews, 15, 564 594.
12. Cavalli-Sforza, L.L. Feldman, M.W. (2003) The application of molecular genetic approaches to the study of human evolution. Nature Genetics, 33 (Suppl. 266 275.
13. Chitnis, C.E. Miller, L.H. (1994) Identification of the erythrocyte binding domains of Plasmodium vivax and Plasmodium knowlesi proteins involved in erythrocyte invasion. Journal of Experimental Medicine, 180, 497 506.
14. Chotivanich, K., Udomsangpetch, R., Pattanapanyasat, K., Chierakul, W., Simpson, J., Looareesuwan, S. White, N. (2002) Hemoglobin E: a balanced polymorphism protective against high parasitemias and thus severe P. falciparum malaria. Blood, 100, 1172 1176.
15. Cockburn, I.A., Mackinnon, M.J., O'Donnell, A., Allen, S.J., Moulds, J.M., Baisor, M., Bockarie, M., Reeder, J.C. Rowe, J.A. (2004) A human complement receptor 1 polymorphism that reduces Plasmodium falciparum rosetting confers protection against severe malaria. Proceedings of the National Academy of Sciences of the United States of America, 101, 272 277.
16. Cooke, G.S. Hill, A.V.S. (2001) Genetics of susceptibility to human infectious disease. Nature Reviews Genetics, 2, 967 977.
17. Cserti, C.M. Dzik, W.H. (2007) The ABO blood group system and Plasmodium falciparum malaria. Blood, 110, 2250 2258.
18. Dronamraju, K.R. Arese, P. (2006) In : Malaria: Genetic and Evolutionary Aspects. Chapter 6, Evolutionary Origins of Human Malaria Parasites (ed. by S.M. Rich, F.J. Ayala). Springer, New York.
19. Facer, C.A. (1995) Erythrocytes carrying mutations in spectrin and protein 4.1 show differing sensitivities to invasion by Plasmodium falciparum. Parasitology Research, 81, 52 57.
20. Fairhurst, R.M., Fujioka, H., Hayton, K., Collins, K.F. Wellems, T.E. (2003) Aberrant development of Plasmodium falciparum in hemoglobin CC red cells: implications for the malaria protective effect of the homozygous state. Blood, 101, 3309 3315.
21. Fairhurst, R.M., Baruch, D.I., Brittain, N.J., Ostera, G.R., Wallach, J.S., Hoang, H.L., Hayton, K., Guindo, A., Makobongo, M.O., Schwartz, O.M., Tounkara, A., Doumbo, O.K., Diallo, D.A., Fujioka, H., Ho, M. Wellems, T.E. (2005) Abnormal display of PfEMP-1 on erythrocytes carrying haemoglobin C may protect against malaria. Nature, 435, 1117 1121.
22. Fernandez-Reyes, D., Craig, A.G., Kyes, S.A., Peshu, N., Snow, R.W., Berendt, A.R., Marsh, K. Newbold, C.I. (1997) A high frequency African coding polymorphism in the N-terminal domain of ICAM-1 predisposing to cerebral malaria in Kenya. Human Molecular Genetics, 6, 1357 1360.
23. Fischer, P.R. Boone, P. (1998) Short report: severe malaria associated with blood group. American Journal of Tropical Medicine and Hygiene, 58, 122 123.
24. Flint, J., Hill, A.V.S., Bowden, D.K., Oppenheimer, S.J., Sill, P.R., Serjeantson, S.W., Bana-Koiri, J., Bhatia, K., Alpers, M.P., Boyce, A.J., Weatherall, D.J. Clegg, J.B. (1986) High frequencies of α thalassaemia are the result of natural selection by malaria. Nature, 321, 744 749.
25. Flint, J., Harding, R.M., Boyce, A.J. Clegg, J.B. (1998) The population genetics of the haemoglobinopathies. In : Baillière's Clinical Haematology; 'Haemoglobinopathies', Vol. 11 (ed. by D.R. Higgs D.J. Weatherall pp. 1 51. Baillière Tindall and W.B. Saunders, London.
26. Friedman, M.J. (1978) Erythrocytic mechanism of sickle cell resistance to malaria. Proceedings of the National Academy of Sciences of the United States of America, 75, 1994.
27. Friedman, M.J., Roth, E.F., Nagel, R.L. Trager, W. (1979) Plasmodium falciparum: physiological interactions with the human sickle cell. Experimental Parasitology, 47, 73.
28. Ganczakowski, M., Town, M., Bowden, D.K., Vulliamy, T.J., Kaneko, A., Clegg, J.B., Weatherall, D.J. Luzzatto, L. (1995) Multiple glucose 6-phosphate dehydrogenase-deficient variants correlate with malaria endemicity in the Vanuatu archipelago (southwestern Pacific). American Journal of Human Genetics, 56, 294 301.
29. Genton, B., Al-Yaman, F., Mgone, C.S., Alexander, N., Paniu, M.M. Alpers, M.P. (1995) Ovalocytosis and cerebral malaria. Nature, 378, 564 565.
30. Haldane, J.B.S. (1949) The rate of mutation of human genes. Proceedings of the VIII International Congress of Genetics. Hereditas, 35, 267 273.
31. Hill, A.V.S., Bowden, D.K., O'Shaughnessy, D.F., Weatherall, D.J. Clegg, J.B. (1988) β-Thalassemia in Melanesia: association with malaria and characterization of a common variant (IVSI nt 5 G-C). Blood, 72, 9 14.
32. Hill, A.V.S., Allsopp, C.E.M., Kwiatkowski, D., Anstey, N.M., Twunmasi, P., Rowe, P.A., Bennett, S., Brewster, D., McMichael, A.J. Greenwood, B.M. (1991) Common west African HLA antigens are associated with protection from severe malaria. Nature, 352, 595 600.
33. Huisman, T.H.J., Carver, M.F.H. Efremov, G.D. (1998) A Syllabus of Human Hemoglobin Variants. Sickle Cell Foundation, Augusta, GA.
34. Hutagalung, R., Wilairatana, P., Looareesuwan, S., Brittenham, G.M., Aikawa, M. Gordeuk, V.R. (1999) Influence of hemoglobin E trait on the severity of falciparum malaria. Journal of Infectious Diseases, 179, 283 286.
35. Kikuchi, M., Looareesuwan, S., Ubalee, R., Tasanor, O., Suzuki, F., Wattanagoon, Y., Na-Bangchang, K., Kimura, A., Aikawa, M. Hirayama, K. (2001) Association of adhesion molecule PECAM-1/CD31 polymorphism with susceptibility to cerebral malaria in Thais. Parasitology International, 50, 235 239.
36. Kun, J.F., Klabunde, J., Lell, B., Luckner, D., Alpers, M., May, J., Meyer, C. Kremsner, P.G. (1999) Association of the ICAM-1Kilifi mutation with protection against severe malaria in Lambarene, Gabon. American Journal of Tropical Medicine and Hygiene, 61, 776 779.
37. Kwiatkowski, D.P. (2005) How malaria has affected the human genome and what human genetics can teach us about malaria. American Journal of Human Genetics, 77, 171 192.
38. Lederberg, J. (1999) J.B.S. Haldane (1949) on infectious disease and evolution. Genetics, 153, 1 3.
39. Lell, B., May, J., Schmidt-Ott, R.J., Lehman, L.G., Luckner, D., Greve, B., Matousek, P., Schmid, D., Herbich, K., Mockenhaupt, F.P., Meyer, C.G., Bienzle, U. Kremsner, P.G. (1999) The role of red blood cell polymorphisms in resistance and susceptibility to malaria. Clinical Infectious Diseases, 28, 794 799.
40. Livingstone, F.B. (1985) Frequencies of Hemoglobin Variants. Oxford University Press, New York, Oxford.
41. Luzzatto, L., Nwachiku-Jarrett, E.S. Reddy, S. (1970) Increased sickling of parasitised erythrocytes as mechanism of resistance against malaria in the sickle-cell trait. Lancet, i, 319.
42. Luzzatto, L., Mehta, A. Vulliamy, T. (2001) Glucose 6-phosphate dehydrogenase. In : The Metabolic and Molecular Basis of Inherited Disease (ed. by C.R. Scriver, A.L. Beaudet, W.S. Sly, D. Valle, B. Childs B. Vogelstein pp. 4517 4554. McGraw Hill, New York.
43. Luzzi, G.A., Merry, A.H., Newbold, C.I., Marsh, K., Pasvol, G. Weatherall, D.J. (1991) Surface antigen expression on Plasmodium falciparum-infected erythrocytes is modified in α- and β-thalassemia. Journal of Experimental Medicine, 173, 785 791.
44. Maier, A.G., Duraisingh, M.T., Reeder, J.C., Patel, S.S., Kazura, J.W., Zimmerman, P.A. Cowman, A.F. (2003) Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nature Medicine, 9, 87 92.
45. Marsh, K., Otoo, L., Hayes, R.J., Carson, D.C. Greenwood, B.M. (1989) Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Transactions of the Royal Society of Tropical Medicine and Hygiene, 83, 293 303.
46. Miller, L.H., Mason, S.J., Clyde, D.F. McGinniss, M.H. (1976) The resistance factor to Plasmodium vivax in Blacks. New England Journal of Medicine, 295, 302 304.
47. Miller, L.H., Haynes, J.D., McAuliffe, F.M., Shiroishi, T., Durocher, J.R. McGinniss, M.H. (1977) Evidence for differences in erythrocyte surface receptors for the malarial parasites, Plasmodium falciparum and Plasmodium knowlesi. Journal of Experimental Medicine, 146, 277 281.
48. Min-Oo, G., Fortin, A., Tam, M.F., Nantel, A., Stevenson, M.M. Gros, P. (2003) Pyruvate kinase deficiency in mice protects against malaria. Nature Genetics, 35, 357 362.
49. Mockenhaupt, F.P., Ehrhardt, S., Gellert, S., Otchwemah, R.N., Dietz, E., Anemana, S.D. Bienzle, U. (2004) Alpha(+)-thalassemia protects African children from severe malaria. Blood, 104, 2003 2006.
50. Modiano, D., Luoni, G., Sirima, B.S., Simporé, J., Verra, F., Konaté, A., Rastrelli, E., Olivieri, A., Calissano, C., Paganotti, G.M., D'Urbano, L., Sanou, I., Sawadogo, A., Modano, G. Coluzzi, M. (2001) Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature, 414, 305 308.
51. Morle, L., Morle, F., Roux, A.F., Godet, J., Forget, B.G., Denoroy, L., Garbarz, M., Dhermy, D., Kastally, R. Delaunay, J. (1989) Spectrin Tunis (Sp alpha I/78), an elliptocytogenic variant, is due to the CGG - - TGG codon change (Arg - - Trp) at position 35 of the alpha I domain. Blood, 74, 828 832.
52. Mourant, A.E. (1968) Genetical polymorphisms and the incidence of disease. Proceedings of the Royal Society of Medicine, 61, 163.
53. O'Shaughnessy, D.F., Hill, A.V.S., Bowden, D.K., Weatherall, D.J. Clegg, J.B., with Collaborators (1990) Globin genes in Micronesia: origins and affinities of Pacific Island peoples. American Journal of Human Genetics, 46, 144 155.
54. Ohashi, J., Naka, I., Patarapotikul, J., Hananantachai, H., Brittenham, G., Looareesuwan, S., Clark, A.G. Tokunaga, K. (2004) Extended linkage disequilibrium surrounding the hemoglobin E variant due to malarial selection. American Journal of Human Genetics, 74, 1198 1208.
55. Pain, A., Urban, B.C., Kai, O., Casals-Pascual, C., Shafi, J., Marsh, K. Roberts, D.J. (2001) A non-sense mutation in Cd36 gene is associated with protection from severe malaria. Lancet, 357, 1502 1503.
56. Pasvol, G., Weatherall, D.J. Wilson, R.J. (1977) Effects of foetal haemoglobin on susceptibility of red cells to Plasmodium falciparum. Nature, 270, 171 173.
57. Pasvol, G., Weatherall, D.J. Wilson, R.J.M. (1978) A mechanism for the protective effect of haemoglobin S against P. falciparum. Nature, 274, 701 703.
58. Pasvol, G., Wainscoat, J.S. Weatherall, D.J. (1982) Erythrocytes deficiency in glycophorin resist invasion by the malarial parasite Plasmodium falciparum. Nature, 297, 64 66.
59. Perkins, M. (1981) Inhibitory effects of erythrocyte membrane proteins on the in vitro invasion of the human malarial parasite (Plasmodium falciparum) into its host cell. Journal of Cell Biology, 90, 563 567.
60. Rees, D.C., Williams, T.N., Maitland, K., Clegg, J.B. Weatherall, D.J. (1998) Alpha thalassemia is associated with increased soluble transferrin receptor levels. British Journal of Haematology, 103, 365 370.
61. Roberts, D.J., Harris, T. Williams, T.N. (2004) The influence of inherited traits on malaria infection. In : Susceptibility to Infectious Diseases: The Importance of Host Genetics (ed. by R. Bellamy pp. 139 184. Cambridge University Press, Cambridge.
62. Roth, Jr., E.F., Friedman, M., Ueda, Y., Tellez, L., Trager, W. Nagel, R.L. (1978) Sickling rates of human AS red cells infected in vitro with Plasmodium falciparum malaria. Science, 202, 650 652.
63. Ruwende, C., Khoo, S.C., Snow, R.W., Yates, S.N.R., Kwiatkowski, D., Gupta, S., Warn, P., Allsopp, C.E.M., Gilbert, S.C., Peschu, N., Newbold, C.I., Greenwood, B.M., Marsh, K. Hill, A.V.S. (1995) Natural selection of hemi- and heterozygotes for G6PD deficiency in Africa by resistance to severe malaria. Nature, 376, 246 249.
64. Shear, H.L., Grinberg, L., Gilman, J., Fabry, M.E., Stamatoyannopoulos, G., Goldberg, D.E. Nagel, R.L. (1998) Transgenic mice expressing human fetal globin are protected from malaria by a novel mechanism. Blood, 92, 2520 2526.
65. Silvestroni, E. Bianco, I. (1947) Sulla frequenza dei porta tori di malatia di morbo di Codey e primi observazioni sulla frequenza dei portatore di microcitemia nel Ferrarese e inakune regioni limitrofe. Bollettino Atti Academy of Medicine, 72, 32.
66. Siniscalco, M., Bernini, L., Latte, B. Motulsky, A.G. (1961) Favism and thalassaemia in Sardinia and their relationship to malaria. Nature, 190, 1179 1180.
67. Steinberg, M.H., Forget, B.G., Higgs, D.R. Nagel, R.L. (eds) (2001) Disorders of Hemoglobin. Cambridge University Press, New York.
68. Tishkoff, S.A., Varkonyi, R., Cahinhinan, N., Abbes, S., Argyropoulos, G., Destro-Bisol, G., Drousiotou, A., Dangerfield, B., Lefranc, G., Loiselet, J., Piro, A., Stoneking, M., Tagarelli, A., Tagarelli, G., Touma, E.H., Williams, S.M. Clark, A.G. (2001) Haplotype diversity and linkage disequilibrium at human G6PD: recent origin of alleles that confer malarial resistance. Science, 293, 455 462.
69. Udomsangpetch, R., Todd, J., Carlson, J. Greenwood, B.M. (1993) The effects of hemoglobin genotype and ABO blood group on the formation of rosettes by Plasmodium falciparum-infected red blood cells. American Journal of Tropical Medicine and Hygiene, 48, 149 153.
70. Valentine, W.N. Neel, J.V. (1944) Hematologic and genetic study of transmission of thalassemia (Cooley's anemia: Mediterranean anemia). Archives of Internal Medicine, 74, 185 196.
71. Weatherall, D.J. (2008) Red cell polymorphisms and malaria. In : Genetic Susceptibility to Infectious Diseases (ed. by R.A. Kaslow, J.M. McNicholl A.V.S. Hill pp. 107 119. Oxford University Press, New York.
72. Weatherall, D.J. Clegg, J.B. (2001a) The Thalassaemia Syndromes. Blackwell Science, Oxford.
73. Weatherall, D.J. Clegg, J.B. (2001b) Inherited haemoglobin disorders: an increasing global health problem. Bulletin of the World Health Organisation, 79, 704 712.
74. Weatherall, D.J. Clegg, J.B. (2002) Genetic variability in response to infection. Malaria and after. Genes and Immunity, 3, 331 337.
75. Weatherall, D.J., Miller, L.H., Baruch, D.I., Marsh, K., Doumbo, O.K., Casals-Pascual, C. Roberts, D.J. (2002) Malaria and the red cell. Hematology/American Society for Hematology. Education Program, 35 57.
76. Willcox, M.C., Bjorkman, A., Brohult, J., Persson, P.-O., Rombo, L. Bengtsson, E. (1983) A case-control study in northern Liberia of Plasmodium falciparummalaria in haemoglobin S and β-thalassaemia traits. Annals of Tropical Medicine and Parasitology, 77, 239 246.
77. Williams, T.N. (2006) Red blood cell defects and malaria. Molecular and Biochemical Parasitology, 149, 121 127.
78. Williams, T.N., Maitland, K., Bennett, S., Ganczakowski, M., Peto, T.E.A., Newbold, C.I., Bowden, D.K., Weatherall, D.J. Clegg, J.B. (1996) High incidence of malaria in α-thalassaemic children. Nature, 383, 522 525.
79. Williams, T.N., Weatherall, D.J. Newbold, C.I. (2002) The membrane characteristics of Plasmodium falciparum-infected and -uninfected heterozygous alpha(0)thalassaemic erythrocytes. British Journal Haematology, 118, 663 670.
80. Williams, T.N., Mwangi, T.W., Wambua, S., Alexander, N.D., Kortok, M., Snow, R.W. Marsh, K. (2005a) Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. Journal of Infectious Diseases, 192, 178 186.
81. Williams, T.N., Mwangi, T.W., Roberts, D.J., Alexander, N.D., Weatherall, D.J., Wambua, S., Kortok, M., Snow, R.W. Marsh, K. (2005b) An immune basis for malaria protection by the sickle cell trait. PLoS Medicine, 2, e128.
82. Williams, T.N., Wambua, S., Uyoga, S., Macharia, A., Mwacharo, J.K., Newton, C.R. Maitland, K. (2005c) Both heterozygous and homozygous alpha+ thalassemias protect against severe and fatal Plasmodium falciparum malaria on the coast of Kenya. Blood, 106, 368 371.
83. Williams, T.N., Mwangi, T.W., Wambua, S., Peto, T.E., Weatherall, D.J., Gupta, S., Recker, M., Penman, B.S., Uyoga, S., Macharia, A., Mwacharo, J.K., Snow, R.W. Marsh, K. (2005d) Negative epistasis between the malaria-protective effects of alpha+-thalassemia and the sickle cell trait. Nature Genetics, 37, 1253 1257.
84. Yuthavong, Y., Butthep, P., Bunyaratvej, A., Fucharoen, S. Khurmith, S. (1988) Impaired parasite growth and increased susceptibility to phagocytosis of Plasmodium falciparum infected alpha-thalassemia and hemoglobin Constant Spring red blood cells. American Journal of Clinical Pathology, 89, 521 525.
85. Zimmerman, P.A., Woolley, I., Masinde, G.L., Miller, S.M., McNamara, D.T., Hazlett, F., Mgone, C.S., Alpers, M.P., Genton, B., Boatin, B.A. Kazura, J.W. (1999) Emergence of FY*A(null) in a Plasmodium vivax-endemic region of Papua New Guinea. Proceedings of the National Academy of Sciences of the United States of America, 96, 13973 13977.