Epistasis between the haptoglobin common variant and α +thalassemia influences risk of severe malaria in Kenyan children

Blood

Volumn 123, Issue 13, 2014, Pages 2008-2016

  Atkinson, Sarah H ^a,b,c   Uyoga, Sophie M ^c   Nyatichi, Emily ^c   Macharia, Alex W ^c   Nyutu, Gideon ^c   Ndila, Carolyne ^c   Kwiatkowski, Dominic P ^d,e   Rockett, Kirk A ^d,e   Williams, Thomas N ^c,f  

^a OXFORD UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HAPTOGLOBIN; HAPTOGLOBIN 2 2; HEMOGLOBIN S; PLASMA PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ALPHA THALASSEMIA; ANEMIA; ARTICLE; BRAIN MALARIA; CASE CONTROL STUDY; CHILD; CHILDHOOD DISEASE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; EPISTASIS; FEMALE; GENE INTERACTION; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOTYPE; GLOBIN GENE; HETEROZYGOTE; HOMOZYGOTE; HUMAN; INFANT; KENYA; LABORATORY TEST; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; MALE; MEDLINE; META ANALYSIS (TOPIC); NEWBORN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; RISK ASSESSMENT; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM;

ALPHA-THALASSEMIA; CASE-CONTROL STUDIES; CHILD; CHILD, PRESCHOOL; EPISTASIS, GENETIC; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HAPTOGLOBINS; HUMANS; INFANT; INFANT, NEWBORN; KENYA; MALARIA, FALCIPARUM; MALE; META-ANALYSIS AS TOPIC; RISK FACTORS; SEVERITY OF ILLNESS INDEX;

EID: 84897510008     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-10-533489     Document Type: Article

References (57)

1. Black RE, Cousens S, Johnson HL, et al. Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet. 2009;375(9730):1969-1987.
2. Rother RP, Bell L, Hillmen P, Gladwin MT. The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: a novel mechanism of human disease. JAMA. 2005;293(13):1653-1662. (Pubitemid 40471796)
3. Pamplona A, Hanscheid T, Epiphanio S, Mota MM, Vigário AM. Cerebral malaria and the hemolysis/methemoglobin/heme hypothesis: shedding new light on an old disease. Int J Biochem Cell Biol. 2009;41(4):711-716.
4. Langlois MR, Delanghe JR. Biological and clinical significance of haptoglobin polymorphism in humans. Clin Chem. 1996;42(10):1589-1600. (Pubitemid 26354735)
5. Kristiansen M, Graversen JH, Jacobsen C, et al. Identification of the haemoglobin scavenger receptor. Nature. 2001;409(6817):198-201. (Pubitemid 32144285)
6. Asleh R, Guetta J, Kalet-Litman S, Miller-Lotan R, Levy AP. Haptoglobin genotype- and diabetes-dependent differences in iron-mediated oxidative stress in vitro and in vivo. Circ Res. 2005;96(4):435-441. (Pubitemid 40354537)
7. Bamm VV, Tsemakhovich VA, Shaklai M, Shaklai N. Haptoglobin phenotypes differ in their ability to inhibit heme transfer from hemoglobin to LDL. Biochemistry. 2004;43(13):3899-3906. (Pubitemid 38437056)
8. Melamed-Frank M, Lache O, Enav BI, et al. Structure-function analysis of the antioxidant properties of haptoglobin. Blood. 2001;98(13):3693-3698.
9. Tseng CF, Lin CC, Huang HY, Liu HC, Mao SJ. Antioxidant role of human haptoglobin. Proteomics. 2004;4(8):2221-2228. (Pubitemid 39025321)
10. Guetta J, Strauss M, Levy NS, Fahoum L, Levy AP. Haptoglobin genotype modulates the balance of Th1/Th2 cytokines produced by macrophages exposed to free hemoglobin. Atherosclerosis. 2007;191(1):48-53. (Pubitemid 46227428)
11. Dayan L, Levy AP, Blum S, et al. Haptoglobin genotype and endothelial function in diabetes mellitus: a pilot study. Eur J Appl Physiol. 2009;106(4):639-644.
12. Purushothaman M, Krishnan P, Purushothaman KR, et al. Genotype-dependent impairment of hemoglobin clearance increases oxidative and inflammatory response in human diabetic atherosclerosis. Arterioscler Thromb Vasc Biol. 2012;32(11):2769-2775.
13. Chaichana KL, Levy AP, Miller-Lotan R, Shakur S, Tamargo RJ. Haptoglobin 2-2 genotype determines chronic vasospasm after experimental subarachnoid hemorrhage. Stroke. 2007;38(12):3266-3271. (Pubitemid 350175747)
14. Ohnishi H, Iihara K, Kaku Y, et al. Haptoglobin phenotype predicts cerebral vasospasm and clinical deterioration after aneurysmal subarachnoid hemorrhage. J Stroke Cerebrovasc Dis. 2013;22(4):520-526.
15. Elagib AA, Kider AO, Akerström B, Elbashir MI. Association of the haptoglobin phenotype (1-1) with falciparum malaria in Sudan. Trans R Soc Trop Med Hyg. 1998;92(3):309-311. (Pubitemid 28286932)
16. Quaye IK, Ekuban FA, Goka BQ, et al. Haptoglobin 1-1 is associated with susceptibility to severe Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg. 2000;94(2):216-219. (Pubitemid 30307300)
17. Aucan C, Walley AJ, Greenwood BM, Hill AV. Haptoglobin genotypes are not associated with resistance to severe malaria in The Gambia. Trans R Soc Trop Med Hyg. 2002;96(3):327-328. (Pubitemid 34785076)
18. Bienzle U, Eggelte TA, Adjei LA, et al. Limited influence of haptoglobin genotypes on severe malaria in Ghanaian children. Trop Med Int Health. 2005;10(7):668-671. (Pubitemid 40933940)
19. Mendonça VR, Luz NF, Santos NJ, et al. Association between the haptoglobin and heme oxygenase 1 genetic profiles and soluble CD163 in susceptibility to and severity of human malaria. Infect Immun. 2012;80(4):1445-1454.
20. Atkinson SH, Mwangi TW, Uyoga SM, et al. The haptoglobin 2-2 genotype is associated with a reduced incidence of Plasmodium falciparum malaria in children on the coast of Kenya. Clin Infect Dis. 2007;44(6):802-809. (Pubitemid 46365304)
21. Cox SE, Doherty C, Atkinson SH, et al. Haplotype association between haptoglobin (Hp2) and Hp promoter SNP (A-61C) may explain previous controversy of haptoglobin and malaria protection. PLoS ONE. 2007;2(4):e362.
22. Minang JT, Gyan BA, Anchang JK, Troye-Blomberg M, Perlmann H, Achidi EA. Haptoglobin phenotypes and malaria infection in pregnant women at delivery in western Cameroon. Acta Trop. 2004;90(1):107-114. (Pubitemid 38117060)
23. Imrie H, Ferguson DJ, Day KP. Human serum haptoglobin is toxic to Plasmodium falciparum in vitro. Mol Biochem Parasitol. 2004;133(1):93-98. (Pubitemid 37510312)
24. Hunt NH, Driussi C, Sai-Kiang L. Haptoglobin and malaria. Redox Rep. 2001;6(6):389-392. (Pubitemid 34134334)
25. Grant DJ, Maeda N. A base substitution in the promoter associated with the human haptoglobin 2-1 modified phenotype decreases transcriptional activity and responsiveness to interleukin-6 in human hepatoma cells. Am J Hum Genet. 1993;52(5):974-980. (Pubitemid 23313719)
26. Teye K, Quaye IK, Koda Y, et al. A-61C and C-101G Hp gene promoter polymorphisms are, respectively, associated with ahaptoglobinaemia and hypohaptoglobinaemia in Ghana. Clin Genet. 2003;64(5):439-443. (Pubitemid 37406895)
27. Maeda N, Yang F, Barnett DR, Bowman BH, Smithies O. Duplication within the haptoglobin Hp2 gene. Nature. 1984;309(5964):131-135. (Pubitemid 14142780)
28. Jallow M, Teo YY, Small KS, et al Wellcome Trust Case Control Consortium; Malaria Genomic Epidemiology Network. Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat Genet. 2009;41(6):657-665.
29. Cahill LE, Jensen MK, Chasman DI, Hazra A, Levy AP, Rimm EB. Currently available versions of genome-wide association studies cannot be used to query the common haptoglobin copy number variant. J Am Coll Cardiol. 2013;62(9):860-861.
30. Marsh K, Forster D, Waruiru C, et al. Indicators of life-threatening malaria in African children. N Engl J Med. 1995;332(21):1399-1404.
31. Snow RW, Omumbo JA, Lowe B, et al. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet. 1997;349(9066):1650-1654. (Pubitemid 27234806)
32. Scott JA, Bauni E, Moisi JC, et al. Profile: The Kilifi Health and Demographic Surveillance System (KHDSS). Int J Epidemiol. 2012;41(3):650-657.
33. Maitland K, Pamba A, Newton CR, Levin M. Response to volume resuscitation in children with severe malaria. Pediatr Crit Care Med. 2003;4(4):426-431.
34. Williams TN, Uyoga S, Macharia A, et al. Bacteraemia in Kenyan children with sickle-cell anaemia: a retrospective cohort and case-control study. Lancet. 2009;374(9698):1364-1370.
35. Atkinson SH, Rockett K, Sirugo G, et al. Seasonal childhood anaemia in West Africa is associated with the haptoglobin 2-2 genotype. PLoS Med. 2006;3(5):e172.
36. Chong SS, Boehm CD, Higgs DR, Cutting GR. Single-tube multiplex-PCR screen for common deletional determinants of alpha-thalassemia. Blood. 2000;95(1):360-362. (Pubitemid 30017265)
37. Griffin TJ, Smith LM. Single-nucleotide polymorphism analysis by MALDI-TOF mass spectrometry. Trends Biotechnol. 2000;18(2):77-84. (Pubitemid 30084699)
38. Carlborg O, Haley CS. Epistasis: too often neglected in complex trait studies? Nat Rev Genet. 2004;5(8):618-625. (Pubitemid 39005756)
39. Allen SJ, Rowe P, Allsopp CE, et al. A prospective study of the influence of alpha thalassaemia on morbidity from malaria and immune responses to defined Plasmodium falciparum antigens in Gambian children. Trans R Soc Trop Med Hyg. 1993;87(3):282-285.
40. Mockenhaupt FP, Ehrhardt S, Gellert S, et al. Alpha(+)-thalassemia protects African children from severe malaria. Blood. 2004;104(7):2003-2006. (Pubitemid 39297850)
41. Cheng ML, Ho HY, Tseng HC, Lee CH, Shih LY, Chiu DT. Antioxidant deficit and enhanced susceptibility to oxidative damage in individuals with different forms of alpha-thalassaemia. Br J Haematol. 2005;128(1):119-127.
42. Weatherall DJ, Clegg JB. The Thalassaemia Syndromes, 4th ed. Oxford, UK: Blackwell Science Ltd.; 2001.
43. Awadallah SM. Haptoglobin 2-2 phenotype is associated with decreased ferroxidase activity in smokers. Clin Chim Acta. 2003;334(1-2):71-76. (Pubitemid 36836059)
44. Langlois MR, Delanghe JR, De Buyzere ML, Bernard DR, Ouyang J. Effect of haptoglobin on the metabolism of vitamin C. Am J Clin Nutr. 1997;66(3):606-610. (Pubitemid 27366784)
45. Delanghe JR, Langlois MR, De Buyzere ML, Torck MA. Vitamin C deficiency and scurvy are not only a dietary problem but are codetermined by the haptoglobin polymorphism. Clin Chem. 2007;53(8):1397-1400. (Pubitemid 47206335)
46. Allen A, Fisher C, Premawardhena A, et al. Methemoglobinemia and ascorbate deficiency in hemoglobin E β thalassemia: metabolic and clinical implications. Blood. 2012;120(15):2939-2944.
47. Chamoun V, Zeman A, Blennow K, et al. Haptoglobins as markers of blood-CSF barrier dysfunction: the findings in normal CSF. J Neurol Sci. 2001;182(2):117-121. (Pubitemid 33786707)
48. Borsody M, Burke A, Coplin W, Miller-Lotan R, Levy A. Haptoglobin and the development of cerebral artery vasospasm after subarachnoid hemorrhage. Neurology. 2006;66(5):634-640. (Pubitemid 43739814)
49. Cockburn IA, Mackinnon MJ, O'Donnell A, et al. A human complement receptor 1 polymorphism that reduces Plasmodium falciparum rosetting confers protection against severe malaria. Proc Natl Acad Sci USA. 2004;101(1):272-277. (Pubitemid 38084240)
50. 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(11):3909-3914. (Pubitemid 24362492)
51. 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(12):3752-3759. (Pubitemid 24006060)
52. Luzzi GA, Merry AH, Newbold CI, Marsh K, Pasvol G, Weatherall DJ. Surface antigen expression on Plasmodium falciparum-infected erythrocytes is modified in alpha- and beta-thalassemia. J Exp Med. 1991;173(4):785-791.
53. Williams TN, Weatherall DJ, Newbold CI. The membrane characteristics of Plasmodium falciparum-infected and -uninfected heterozygous alpha(0)thalassaemic erythrocytes. Br J Haematol. 2002;118(2):663-670. (Pubitemid 34994679)
54. 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(10):3364-3371.
55. Zakaria-Meehan Z, Massad G, Simpson LM, Travis JC, Oliver JD. Ability of Vibrio vulnificus to obtain iron from hemoglobin-haptoglobin complexes. Infect Immun. 1988;56(1):275-277. (Pubitemid 18032165)
56. Speeckaert R, Colebunders B, Boelaert JR, et al. Association of haptoglobin phenotypes with the development of Kaposi's sarcoma in HIV patients. Arch Dermatol Res. 2011;303(10):763-769.
57. McDermid JM, van der Loeff MF, Jaye A, et al. Mortality in HIV infection is independently predicted by host iron status and SLC11A1 and HP genotypes, with new evidence of a gene-nutrient interaction. Am J Clin Nutr. 2009;90(1):225-233.