Haptoglobin (HP) and Haptoglobin-related protein (HPR) copy number variation, natural selection, and trypanosomiasis

Human Genetics

Volumn 133, Issue 1, 2014, Pages 69-83

  Hardwick, Robert J ^a   Ménard, Anne ^a   Sironi, Manuela ^b   Milet, Jacqueline ^c   Garcia, André ^d,e   Sese, Claude ^f   Yang, Fengtang ^g   Fu, Beiyuan ^g   Courtin, David ^c   Hollox, Edward J ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b SCIENTIFIC INSTITUTE   (Italy)

^c UNIVERSITY OF ABOMEY CALAVI   (Benin)

^d INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f Programme National de Lutte Contre la Trypanosomose Humaine Africaine (PNLTHA)   (Congo)

^g WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HAPTOGLOBIN;

AFRICAN TRYPANOSOMIASIS; APOLIPOPROTEIN 1 GENE; ARTICLE; CENTRAL AFRICA; CONGO; CONTROLLED STUDY; COPY NUMBER VARIATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE DUPLICATION; GENE FREQUENCY; GENETIC PROCEDURES; GEOGRAPHIC DISTRIBUTION; HAPLOTYPE; HAPLOTYPE MAP; HAPTOGLOBIN GENE; HAPTOGLOBIN RELATED GENE; HOMOZYGOSITY; HUMAN; MAJOR CLINICAL STUDY; NATURAL SELECTION; PARALOG RATIO TEST; PARALOGY; PARENT; PRIORITY JOURNAL; TRYPANOSOMA;

EID: 84891856920     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-013-1352-x     Document Type: Article

References (56)

1. Armour JAL, Palla R, Zeeuwen PLJM, den Heijer M, Schalkwijk J, Hollox EJ (2007) Accurate, high-throughput typing of copy number variation using paralogue ratios from dispersed repeats. Nucleic Acids Res 35:e19 (Pubitemid 46344733)
2. Atkinson SH, Mwangi TW, Uyoga SM, Ogada E, Macharia AW, Marsh K, Prentice AM, Williams TN (2007) 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 44:802-809 (Pubitemid 46365304)
3. Aucan C, Walley AJ, Greenwood BM, Hill AVS (2002) Haptoglobin genotypes are not associated with resistance to severe malaria in The Gambia. Trans R Soc Trop Med Hyg 96:327-328 (Pubitemid 34785076)
4. Barnes C, Plagnol V, Fitzgerald T, Redon R, Marchini J, Clayton D, Hurles ME (2008) A robust statistical method for case-control association testing with copy number variation. Nat Genet 40:1245-1252
5. Barrett MP, Burchmore RJS, Stich A, Lazzari JO, Frasch AC, Cazzulo JJ, Krishna S (2003) The trypanosomiases. Lancet 362:1469-1480 (Pubitemid 37352887)
6. Bienzle U, Eggelte TA, Adjei LA, Dietz E, Ehrhardt S, Cramer JP, Otchwemah RN, Mockenhaupt FP (2005) Short Communication: limited influence of haptoglobin genotypes on severe malaria in Ghanaian children. Tropical Med Int Health 10:668-671 (Pubitemid 40933940)
7. Cann HM, de Toma C, Cazes L, Legrand MF, Morel V, Piouffre L, Bodmer J, Bodmer WF, Bonne-Tamir B, Cambon-Thomsen A, Chen Z, Chu J, Carcassi C, Contu L, Du R, Excoffier L, Ferrara GB, Groot H, Gurwitz D, Jenkins T, Herrera RJ, Huang X, Kidd J, Kidd KK, Langaney A, Lin AA, Mehdi SQ, Parham P, Piazza A, Pistillo MP, Qian Y, Shu Q, Xu J, Zhu S, Weber JL, Greely HT, Feldman MW, Thomas G, Dausset J, Cavalli-Sforza LL (2002) A human genome diversity cell line panel. Science (New York, NY) 296:261
8. Carter K, Worwood M (2007) Haptoglobin: a review of the major allele frequencies worldwide and their association with diseases. Int J Lab Hematol 29:92-110 (Pubitemid 46911165)
9. Conrad DF, Pinto D, Redon R, Feuk L, Gokcumen O, Zhang Y, Aerts J, Andrews TD, Barnes C, Campbell P, Fitzgerald T, Hu M, Ihm C, Kristiansson K, Macarthur D, Macdonald J, Onyiah I, Pang A, Robson S, Stirrups K, Valsesia A, Walter K, Wei J, Consortium" WTCC, Tyler-Smith C, Carter N, Lee C, Scherer S, Hurles M (2009) Origins and functional impact of copy number variation in the human genome. Nature 464:704-712
10. Courtin D, Milet J, Jamonneau V, Yeminanga CS, Kumeso VKB, Bilengue CMM, Betard C, Garcia A (2007) Association between human African trypanosomiasis and the IL6 gene in a Congolese population. Infect Genet Evol 7:60-68 (Pubitemid 44888580)
11. De G, Yip W-K, Ionita-Laza I, Laird N (2013) Rare variant analysis for family-based design. PLoS ONE 8:e48495
12. Drain J, Bishop JR, Hajduk SL (2001) Haptoglobin-related protein mediates trypanosome lytic factor binding to trypanosomes. J Biol Chem 276:30254-30260
13. Ekwanzala M, Pépin J, Khonde N, Molisho S, Bruneel H, De Wals P (1996) In the heart of darkness: sleeping sickness in Zaire. Lancet 348:1427 (Pubitemid 26395241)
14. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564-567
15. Fenner JN (2005) Cross-cultural estimation of the human generation interval for use in genetics-based population divergence studies. Am J Phys Anthropol 128:415-423 (Pubitemid 41407413)
16. Fumagalli M, Pozzoli U, Cagliani R, Comi GP, Riva S, Clerici M, Bresolin N, Sironi M (2009) Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions. J Exp Med 206:1395-1408
17. Gautier M, Vitalis R (2012) rehh: an R package to detect footprints of selection in genome-wide SNP data from haplotype structure. Bioinformatics 28:1176-1177
18. Genovese G, Friedman DJ, Ross MD, Lecordier L, Uzureau P, Freedman BI, Bowden DW, Langefeld CD, Oleksyk TK, Uskinski Knob AL, Bernhardy AJ, Hicks PJ, Nelson G, Vanhollebeke B, Winkler C, Kopp J, Pays E, MR P (2010) Association of trypanolytic ApoL1 variants with kidney disease in African Americans. Science 329:841-845
19. Goudet J (2004) hierfstat, a package for r to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184-186 (Pubitemid 40350918)
20. Handley LJL, Manica A, Goudet J, Balloux F (2007) Going the distance: human population genetics in a clinal world. Trends Genet 23:432-439 (Pubitemid 47259574)
21. Hardwick RJ, Machado LR, Zuccherato LW, Antolinos S, Xue Y, Shawa N, Gilman RH, Cabrera L, Berg DE, Tyler-Smith C, Tarazona-Santos E, Hollox EJ (2011) A worldwide analysis of beta-defensin copy number variation suggests recent selection of a high-expressing DEFB103 gene copy in East Asia. Hum Mutat 32:743-750
22. Hardwick RJ, Amogne W, Mugusi S, Yimer G, Ngaimisi E, Habtewold A, Minzi O, Makonnen E, Janabi M, Machado LR, Viskaduraki M, Mugusi F, Aderaye G, Lindquist L, Hollox EJ, Aklillu E (2012) β-defensin Genomic Copy Number Is Associated With HIV Load and Immune Reconstitution in Sub-Saharan Africans. J Infect Dis 206:1012-1019
23. Horvath S, Xu X, Laird NM (2001) The family based association test method: strategies for studying general genotype-phenotype associations. Eur J Human Genet 9:301 (Pubitemid 32366699)
24. Iskow RC, Gokcumen O, Lee C (2012) Exploring the role of copy number variants in human adaptation. Trends Genet 28:245-257
25. Jolly D, Prentice IC, Bonnefille R, Ballouche A, Bengo M, Brenac P, Buchet G, Burney D, Cazet JP, Cheddadi R, Edorh T, Elenga H, Elmoutaki S, Guiot J, Laarif F, Lamb H, Lezine A-M, Maley J, Mbenza M, Peyron O, Reille M, Reynaud-Ferrara I, Riollet G, Ritchie J, Roche E, Scott L, Ssemmanda I, Straka H, Umer M, Van Campo E, Vilimumbalo S, Vincens A, Waller M (2008) Biome reconstruction from pollen and plant macrofossil data for Africa and the Arabian peninsula at 0 and 6000 years. J Biogeogr 25:1007-1027
26. Jorge A, Antonio S, Ángel C (2008) SPSmart: adapting population based SNP genotype databases for fast and comprehensive web access. BMC Bioinformatics 9:428
27. Kieft R, Capewell P, Turner CMR, Veitch NJ, MacLeod A, Hajduk S (2010) Mechanism of Trypanosoma brucei gambiense (group 1) resistance to human trypanosome lytic factor. Proc Natl Acad Sci 107:16137-16141
28. Ko W-Y, Rajan P, Gomez F, Scheinfeldt L, Froment A, Nyambo TB, Omar SA, Wambebe C, Ranciaro A, Hirbo JB, Tishkoff SA (2013) Identifying Darwinian Selection Acting on Different Human APOL1 Variants among Diverse African Populations. Am J Human Genet 93:54-66
29. Koch W, Latz W, Eichinger M, Roguin A, Levy AP, Schömig A, Kastrati A (2002) Genotyping of the common haptoglobin Hp 1/2 polymorphism based on PCR. Clin Chem 48:1377-1382 (Pubitemid 34925770)
30. Koda Y, Soejima M, Yoshioka N, Kimura H (1998) The haptoglobin-gene deletion responsible for anhaptoglobinemia. Am J Human Genet 62:245-252 (Pubitemid 28110765)
31. Langlois MR, Delanghe JR (1996) Biological and clinical significance of haptoglobin polymorphism in humans. Clin Chem 42:1589-1600 (Pubitemid 26354735)
32. Li JZ, Absher DM, Tang H, Southwick AM, Casto AM, Ramachandran S, Cann HM, Barsh GS, Feldman M, Cavalli-Sforza LL (2008) Worldwide human relationships inferred from genome-wide patterns of variation. Science 319:1100-1104 (Pubitemid 351300793)
33. Maeda N, Yang F, Barnett DR, Bowman BH, Smithies O (1984) Duplication within the haptoglobin Hp2 gene. Nature 309:131
34. Maeda N, McEvoy SM, Harris HF, Huisman T, Smithies O (1986) Polymorphisms in the human haptoglobin gene cluster: chromosomes with multiple haptoglobin-related (Hpr) genes. Proc Natl Acad Sci 83:7395-7399 (Pubitemid 16000528)
35. Matise TC, Chen F, Chen W, Francisco M, Hansen M, He C, Hyland FC, Kennedy GC, Kong X, Murray SS, Ziegle J, Stewart W, Buyske S (2007) A second-generation combined linkage-physical map of the human genome. Genome Res 17:1783-1786 (Pubitemid 351360002)
36. Mockenhaupt FP, Ehrhardt S, Gellert S, Otchwemah RN, Dietz E, Anemana SD, Bienzle U (2004) α+ -thalassemia protects African children from severe malaria. Blood 104:2003-2006 (Pubitemid 39297850)
37. Muranjan M, Nussenzweig V, Tomlinson S (1998) Characterization of the human serum trypanosome toxin, haptoglobin-related protein. J Biol Chem 273:3884-3887 (Pubitemid 28103245)
38. Nielsen MJ, Moestrup SK (2009) Receptor targeting of hemoglobin mediated by the haptoglobins: roles beyond heme scavenging. Blood 114:764-771
39. Nielsen MJ, Petersen SV, Jacobsen C, Oxvig C, Rees D, Møller HJ, Moestrup SK (2006) Haptoglobin-related protein is a high-affinity hemoglobin-binding plasma protein. Blood 108:2846-2849
40. Pelak K, Need AC, Fellay J, Shianna KV, Feng S, Urban TJ, Ge D, De Luca A, Martinez-Picado J, Wolinsky SM, Martinson J, Jamieson B, Bream J, Martin M, Borrow P, McMichael A, Haynes B, Telenti A, Carrington M, Goldstein D, Alter G, Immunology NCfHAV (2011) Copy number variation of KIR genes influences HIV-1 control. PLoS Biology 9:e1001208
41. Perry GH, Dominy NJ, Claw KG, Lee AS, Fiegler H, Redon R, Werner J, Villanea FA, Mountain JL, Misra R, Carter N, Lee C, Stone A (2007) Diet and the evolution of human amylase gene copy number variation. Nat Genet 39:1256-1260 (Pubitemid 47482688)
42. Perry GH, Yang F, Marques-Bonet T, Murphy C, Fitzgerald T, Lee AS, Hyland C, Stone AC, Hurles ME, Tyler-Smith C, Carter N, Eichler E, Lee C, Redon R (2008) Copy number variation and evolution in humans and chimpanzees. Genome Res 18:1698-1710
43. Pozzoli U, Fumagalli M, Cagliani R, Comi GP, Bresolin N, Clerici M, Sironi M (2010) The role of protozoa-driven selection in shaping human genetic variability. Trends Genet 26:95-99
44. Quaye IKE, Ekuban FA, Goka BQ, Adabayeri V, Kurtzhals JAL, Gyan B, Ankrah NA, Hviid L, Akanmori BD (2000) Haptoglobin 1-1 is associated with susceptibility to severe Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg 94:216-219 (Pubitemid 30307300)
45. Raper J, Fung R, Ghiso J, Nussenzweig V, Tomlinson S (1999) Characterization of a novel trypanosome lytic factor from human serum. Infect Immun 67:1910-1916 (Pubitemid 29144414)
46. Rodriguez S, Williams DM, Guthrie PAI, McArdle WL, Smith GD, Evans DM, Gaunt TR, Day INM (2012) Molecular and population analysis of natural selection on the human haptoglobin duplication. Ann Hum Genet 76:352-362
47. Rosenberg NA (2006) Standardized subsets of the HGDP-CEPH Human Genome Diversity Cell Line Panel, accounting for atypical and duplicated samples and pairs of close relatives. Ann Hum Genet 70:841-847 (Pubitemid 44530648)
48. Sabeti PC, Reich DE, Higgins JM, Levine HZP, Richter DJ, Schaffner SF, Gabriel SB, Platko JV, Patterson NJ, McDonald GJ, Ackerman H, Campbell S, Altshuler D, Cooper R, Kwiatkowski D, Ward R, Lander ES (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419:832-837 (Pubitemid 35238568)
49. Smith AB, Esko JD, Hajduk SL (1995) Killing of trypanosomes by the human haptoglobin-related protein. Science-New York Then Washington 268:284-286
50. Smithies O (1955) Zone electrophoresis in starch gels: group variations in the serum proteins of normal human adults. Biochem J 61:629-641
51. Smithies O, Connell G, Dixon G (1962) Chromosomal rearrangements and the evolution of haptoglobin genes. Nature 196:232
52. Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Human Genet 73:1162-1169 (Pubitemid 37414228)
53. Steverding D (2008) The history of African trypanosomiasis. Parasit Vectors 1
54. Vanhollebeke B, De Muylder G, Nielsen MJ, Pays A, Tebabi P, Dieu M, Raes M, Moestrup SK, Pays E (2008) A haptoglobin-hemoglobin receptor conveys innate immunity to Trypanosoma brucei in humans. Sci Signal 320:677
55. Voight BF, Kudaravalli S, Wen X, Pritchard JK (2006) A map of recent positive selection in the human genome. PLoS Biol 4:e72
56. Walker S, Janyakhantikul S, Armour JAL (2009) Multiplex Paralogue Ratio Tests for accurate measurement of multiallelic CNVs. Genomics 93:98-103