Reappraisal of known malaria resistance loci in a large multicenter study

Nature Genetics

Volumn 46, Issue 11, 2014, Pages 1197-1204

  Rockett, Kirk A ^a,b,c   Clarke, Geraldine M ^a,c   Fitzpatrick, Kathryn ^a   Hubbart, Christina ^a   Jeffreys, Anna E ^a   Rowlands, Kate ^a   Craik, Rachel ^a   Jallow, Muminatou ^d,e   Conway, David J ^d,f   Bojang, Kalifa A ^d   Pinder, Margaret ^d   Usen, Stanley ^d   Sisay Joof, Fatoumatta ^d   Sirugo, Giorgio ^d   Toure, Ousmane ^g   Thera, Mahamadou A ^g   Konate, Salimata ^g   Sissoko, Sibiry ^g   Niangaly, Amadou ^g   Poudiougou, Belco ^g   Mangano, Valentina D ^h   Bougouma, Edith C ⁱ   Sirima, Sodiomon B ⁱ   Modiano, David ^h   Amenga Etego, Lucas N ^j   Ghansah, Anita ^k   Koram, Kwadwo A ^k   Wilson, Michael D ^k   Enimil, Anthony ^l   Evans, Jennifer ^m,n   Amodu, Olukemi ^o   Olaniyan, Subulade ^o   Apinjoh, Tobias ^p   Mugri, Regina ^p   Ndi, Andre ^p   Ndila, Carolyne M ^q   Uyoga, Sophie ^q   Macharia, Alexander ^q   Peshu, Norbert ^q   Williams, Thomas N ^q,r   Manjurano, Alphaxard ^f,s   Riley, Eleanor ^f   Drakeley, Chris ^s,w   Reyburn, Hugh ^f,s   Nyirongo, Vysaul ^t   Kachala, David ^u   Molyneux, Malcolm ^v   Dunstan, Sarah J ^u,v   Phu, Nguyen Hoan ^u   Quyen, Nguyen Thi Ngoc ^u   Thai, Cao Quang ^u   Hien, Tran Tinh ^u   Manning, Laurens ^x,y   Laman, Moses ^x   Siba, Peter ^x   Karunajeewa, Harin ^y   Allen, Steve ^z   Allen, Angela ^aa   Davis, Timothy M E ^y   Michon, Pascal ^x,ab   Mueller, Ivo ^x,ac,ad   Green, Angie ^a   Molloy, Sile ^a   Johnson, Kimberly J ^a   Kerasidou, Angeliki ^a,ae   Cornelius, Victoria ^a   Hart, Lee ^a   Vanderwal, Aaron ^a   Joaquin, Miguelsan ^a   Band, Gavin ^a   Le, Si Quang ^a   Pirinen, Matti ^a   Sepúlveda, Nuno ^f   Spencer, Chris C A ^a,c   Clark, Taane G ^f   Agbenyega, Tsiri ^l,af   Achidi, Eric ^p   Doumbo, Ogobara ^g   Farrar, Jeremy ^u,v   Marsh, Kevin ^q   Taylor, Terrie ^t   Kwiatkowski, Dominic P ^a,b,c   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d MEDICAL RESEARCH COUNCIL LABORATORIES   (Gambia)

^e Royal Victoria Teaching Hospital Gambia   (Gambia)

^f LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^g UNIVERSITY OF BAMAKO   (Mali)

^h SAPIENZA UNIVERSITY OF ROME   (Italy)

ⁱ Burkina Faso   (Burkina Faso)

^j NAVRONGO HEALTH RESEARCH CENTRE   (Ghana)

^k University of Ghana   (Ghana)

^l KOMFO ANOKYE TEACHING HOSPITAL   (Ghana)

^m BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

ⁿ KUMASI CENTRE FOR COLLABORATIVE RESEARCH IN TROPICAL MEDICINE   (Ghana)

^o UNIVERSITY OF IBADAN   (Nigeria)

^p UNIVERSITY OF BUEA   (Cameroon)

^q KEMRI WELLCOME TRUST RESEARCH PROGRAMME   (Kenya)

^r IMPERIAL COLLEGE LONDON   (United Kingdom)

^s KILIMANJARO CHRISTIAN MEDICAL CENTRE   (Tanzania)

^t UNIVERSITY OF MALAWI   (Malawi)

^u OXFORD UNIVERSITY CLINICAL RESEARCH UNIT   (Viet Nam)

^v UNIVERSITY OF OXFORD   (United Kingdom)

^w UNIVERSITY OF MELBOURNE   (Australia)

^x PAPUA NEW GUINEA INSTITUTE OF MEDICAL RESEARCH   (Papua New Guinea)

^y UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^z SWANSEA UNIVERSITY   (United Kingdom)

^aa UNIVERSITY OF OXFORD   (United Kingdom)

^ab Divine Word University   (Papua New Guinea)

^ac WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^ad CENTRE FOR RESEARCH IN ENVIRONMENTAL EPIDEMIOLOGY CREAL   (Spain)

^ae UNIVERSITY OF OXFORD   (United Kingdom)

^af KWAME NKRUMAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Ghana)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ATP2B4 PROTEIN, HUMAN; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE;

AFRICA SOUTH OF THE SAHARA; CASE CONTROL STUDY; CLINICAL TRIAL; DISEASE RESISTANCE; GENE LOCUS; GENETIC ASSOCIATION; GENETICS; GLUCOSE 6 PHOSPHATE DEHYDROGENASE DEFICIENCY; HUMAN; MALARIA FALCIPARUM; MULTICENTER STUDY; PAPUA NEW GUINEA; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL MODEL; VIET NAM;

AFRICA SOUTH OF THE SAHARA; CASE-CONTROL STUDIES; DISEASE RESISTANCE; GENETIC ASSOCIATION STUDIES; GENETIC LOCI; GLUCOSEPHOSPHATE DEHYDROGENASE; GLUCOSEPHOSPHATE DEHYDROGENASE DEFICIENCY; HUMANS; LOGISTIC MODELS; MALARIA, FALCIPARUM; PAPUA NEW GUINEA; PLASMA MEMBRANE CALCIUM-TRANSPORTING ATPASES; POLYMORPHISM, SINGLE NUCLEOTIDE; VIETNAM;

EID: 84908885451     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3107     Document Type: Article

References (56)

1. Haldane, J.B.S. Disease and evolution. Ric. Sci. Suppl. A 19, 68-76 (1949).
2. Allison, A.C. Protection afforded by sickle-cell trait against subtertian malarial infection. BMJ 1, 290-294 (1954).
3. Allison, A.C. Genetic factors in resistance to malaria. Ann. NY Acad. Sci. 91, 710-729 (1961).
4. Bienzle, U., Ayeni, O., Lucas, A.O. & Luzzatto, L. Glucose-6-phosphate dehydrogenase and malaria. Greater resistance of females heterozygous for enzyme deficiency and of males with non-deficient variant. Lancet 1, 107-110 (1972).
5. Ruwende, C. et al. Natural selection of hemi- and heterozygotes for G6PD deficiency in Africa by resistance to severe malaria. Nature 376, 246-249 (1995).
6. Tishkoff, S.A. et al. Haplotype diversity and linkage disequilibrium at human G6PD: recent origin of alleles that confer malarial resistance. Science 293, 455-462 (2001).
7. Kwiatkowski, D.P. How malaria has affected the human genome and what human genetics can teach us about malaria. Am. J. Hum. Genet. 77, 171-192 (2005).
8. Verra, F., Mangano, V.D. & Modiano, D. Genetics of susceptibility to Plasmodium falciparum: from classical malaria resistance genes towards genome-wide association studies. Parasite Immunol. 31, 234-253 (2009).
9. Hedrick, P.W. Population genetics of malaria resistance in humans. Heredity (Edinb.) 107, 283-304 (2011).
10. Malaria Genomic Epidemiology Network. A global network for investigating the genomic epidemiology of malaria. Nature 456, 732-737 (2008).
11. World Health Organization. Severe falciparum malaria. Trans. R. Soc. Trop. Med. Hyg. 94 (suppl. 1), S1-S90 (2000).
12. World Health Organization. Guidelines for the Treatment of Malaria 2nd edn. (World Health Organization, Geneva, 2010).
13. Marsh, K. et al. Indicators of life-threatening malaria in African children. N. Engl. J. Med. 332, 1399-1404 (1995).
14. Taylor, T. et al. Standardized data collection for multi-center clinical studies of severe malaria in African children: establishing the SMAC network. Trans. R. Soc. Trop. Med. Hyg. 100, 615-622 (2006).
15. Jallow, M. et al. Clinical features of severe malaria associated with death: a 13-year observational study in The Gambia. PLoS ONE 7, e45645 (2012).
16. Chokshi, D.A. et al. Valid consent for genomic epidemiology in developing countries. PLoS Med. 4, e95 (2007).
17. Parker, M. et al. Ethical data release in genome-wide association studies in developing countries. PLoS Med. 6, e1000143 (2009).
18. Snow, R.W. et al. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 349, 1650-1654 (1997).
19. Reyburn, H. et al. Association of transmission intensity and age with clinical manifestations and case fatality of severe Plasmodium falciparum malaria. J. Am. Med. Assoc. 293, 1461-1470 (2005).
20. Yamamoto, F., Clausen, H., White, T., Marken, J. & Hakomori, S. Molecular genetic basis of the histo-blood group ABO system. Nature 345, 229-233 (1990).
21. Ogasawara, K. et al. Molecular genetic analysis of variant phenotypes of the ABO blood group system. Blood 88, 2732-2737 (1996).
22. Fry, A.E. et al. Common variation in the ABO glycosyltransferase is associated with susceptibility to severe Plasmodium falciparum malaria. Hum. Mol. Genet. 17, 567-576 (2008).
23. Cappellini, M.D. & Fiorelli, G. Glucose-6-phosphate dehydrogenase deficiency. Lancet 371, 64-74 (2008).
24. Hirono, A. & Beutler, E. Molecular cloning and nucleotide sequence of cDNA for human glucose-6-phosphate dehydrogenase variant A. Proc. Natl. Acad. Sci. USA 85, 3951-3954 (1988).
25. Clark, T.G. et al. Allelic heterogeneity of G6PD deficiency in West Africa and severe malaria susceptibility. Eur. J. Hum. Genet. 17, 1080-1085 (2009).
26. Timmann, C. et al. Genome-wide association study indicates two novel resistance loci for severe malaria. Nature 489, 443-446 (2012).
27. Sabeti, P. et al. CD40L association with protection from severe malaria. Genes Immun. 3, 286-291 (2002).
28. Hirschhorn, J.N., Lohmueller, K., Byrne, E. & Hirschhorn, K. A comprehensive review of genetic association studies. Genet. Med. 4, 45-61 (2002).
29. Williams, T.N. et al. Negative epistasis between the malaria-protective effects of α+-thalassemia and the sickle cell trait. Nat. Genet. 37, 1253-1257 (2005).
30. Atkinson, S.H. et al. Epistasis between the haptoglobin common variant and α+thalassemia influences risk of severe malaria in Kenyan children. Blood 123, 2008-2016 (2014).
31. Steinberg, M.H., Eaton, J.W., Berger, E., Coleman, M.B. & Oelshlegel, F.J. Erythrocyte calcium abnormalities and the clinical severity of sickling disorders. Br. J. Haematol. 40, 533-539 (1978).
32. Band, G. et al. Imputation-based meta-analysis of severe malaria in three African populations. PLoS Genet. 9, e1003509 (2013).
33. Fairhurst, R.M. et al. Abnormal display of PfEMP-1 on erythrocytes carrying haemoglobin C may protect against malaria. Nature 435, 1117-1121 (2005).
34. Bunn, H.F. The triumph of good over evil: protection by the sickle gene against malaria. Blood 121, 20-25 (2013).
35. Cserti, C.M. & Dzik, W.H. The ABO blood group system and Plasmodium falciparum malaria. Blood 110, 2250-2258 (2007).
36. Rowe, J.A. et al. Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc. Natl. Acad. Sci. USA 104, 17471-17476 (2007).
37. Teo, Y.Y., Small, K.S. & Kwiatkowski, D.P. Methodological challenges of genome-wide association analysis in Africa. Nat. Rev. Genet. 11, 149-160 (2010).
38. Teo, Y.Y. et al. Genome-wide comparisons of variation in linkage disequilibrium. Genome Res. 19, 1849-1860 (2009).
39. Luzzatto, L. G6PD deficiency and malaria selection. Heredity 108, 456 (2012).
40. Menendez, C., Fleming, A.F. & Alonso, P.L. Malaria-related anaemia. Parasitol. Today 16, 469-476 (2000).
41. Weatherall, D.J. & Kwiatkowski, D. Hematologic disorders of children in developing countries. Pediatr. Clin. North Am. 49, 1149-1164 (2002).
42. Calis, J.C. et al. Severe anemia in Malawian children. N. Engl. J. Med. 358, 888-899 (2008).
43. Howes, R.E., Battle, K.E., Satyagraha, A.W., Baird, J.K. & Hay, S.I. G6PD deficiency: global distribution, genetic variants and primaquine therapy. Adv. Parasitol. 81, 133-201 (2013).
44. Price, R.N. et al. Vivax malaria: neglected and not benign. Am. J. Trop. Med. Hyg. 77, 79-87 (2007).
45. Louicharoen, C. et al. Positively selected G6PD-Mahidol mutation reduces Plasmodium vivax density in Southeast Asians. Science 326, 1546-1549 (2009).
46. Guerra, C.A. et al. The international limits and population at risk of Plasmodium vivax transmission in 2009. PLoS Negl. Trop. Dis. 4, e774 (2010).
47. Liu, W. et al. African origin of the malaria parasite Plasmodium vivax. Nat. Commun. 5, 3346 (2014).
48. Miller, L.H., Mason, S.J., Clyde, D.F. & McGinniss, M.H. The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N. Engl. J. Med. 295, 302-304 (1976).
49. Hamblin, M.T., Thompson, E.E. & Di Rienzo, A. Complex signatures of natural selection at the Duffy blood group locus. Am. J. Hum. Genet. 70, 369-383 (2002).
50. Apinjoh, T.O. et al. Association of cytokine and Toll-like receptor gene polymorphisms with severe malaria in three regions of Cameroon. PLoS ONE 8, e81071 (2013).
51. Manjurano, A. et al. Candidate human genetic polymorphisms and severe malaria in a Tanzanian population. PLoS ONE 7, e47463 (2012).
52. Dunstan, S.J. et al. Variation in human genes encoding adhesion and proinflammatory molecules are associated with severe malaria in the Vietnamese. Genes Immun. 13, 503-508 (2012).
53. Toure, O. et al. Candidate polymorphisms and severe malaria in a Malian population. PLoS ONE 7, e43987 (2012).
54. Vallone, P.M., Decker, A.E. & Butler, J.M. Allele frequencies for 70 autosomal SNP loci with U.S. Caucasian, African-American, and Hispanic samples. Forensic Sci. Int. 149, 279-286 (2005).
55. Clayton, D. Testing for association on the X chromosome. Biostatistics 9, 593-600 (2008).
56. Cordell, H.J. Detecting gene-gene interactions that underlie human diseases. Nat. Rev. Genet. 10, 392-404 (2009).