Population genetics of GYPB and association study between GYPB*S/s polymorphism and susceptibility to P. falciparum infection in the Brazilian Amazon

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Tarazona Santos, Eduardo ^a   Castilho, Lilian ^b   Amaral, Daphne R T ^b   Costa, Daiane C ^b   Furlani, Natália G ^c   Zuccherato, Luciana W ^a   Machado, Moara ^a   Reid, Marion E ^d   Zalis, Mariano G ^e   Rossit, Andréa R ^c,g   Santos, Sidney E B ^f   Machado, Ricardo L ^c   Lustigman, Sara ^d  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b Laboratório de Pesquisa em Hemoterapia Hemocentro Campinas   (Brazil)

^c FACULDADE DE MEDICINA DE SÃO JOSÉ DO RIO PRETO   (Brazil)

^d NEW YORK BLOOD CENTER   (United States)

^e FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^f FEDERAL UNIVERSITY OF PARÁ   (Brazil)

^g FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPHORIN B; GLYCOPHORIN; GYPB PROTEIN, HUMAN;

ADULT; ARTICLE; BRAZIL; COEVOLUTION; CONTROLLED STUDY; ETHNICITY; EXON; FEMALE; GENE FREQUENCY; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOTYPE; HOST PARASITE INTERACTION; HUMAN; INFECTION RISK; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; MALE; NATURAL SELECTION; NUCLEOTIDE SEQUENCE; POPULATION GENETICS; SEQUENCE HOMOLOGY; ALLELE; CASE CONTROL STUDY; ENDEMIC DISEASE; GENETIC MARKER; GENETIC PREDISPOSITION; GENETICS; PHYSIOLOGY; PLASMODIUM FALCIPARUM;

PLASMODIUM FALCIPARUM;

ALLELES; BRAZIL; CASE-CONTROL STUDIES; ENDEMIC DISEASES; GENE FREQUENCY; GENETIC MARKERS; GENETIC PREDISPOSITION TO DISEASE; GENETICS, POPULATION; GLYCOPHORIN; HUMANS; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; POLYMORPHISM, GENETIC;

EID: 79551505789     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016123     Document Type: Article

References (90)

1. McGhee RB (1953) The infection by Plasmodium lophurae of duck erythrocytes in the chicken embryo. J Exp Med 97(6): 773-82.
2. Cowman AF, Crabb BS (2006) Invasion of red blood cells by malaria parasites. Cell 124(4): 755-66.
3. Okoyeh JN, Pillai CR, Chitnis CE (1999) Plasmodium falciparum field isolates commonly use erythrocyte invasion pathways that are independent of sialic acid residues of glycophorin A. Infect Immun 67(11): 5784-91.
4. Baum J, Pinder M, Conway DJ (2003) Erythrocyte invasion phenotypes of Plasmodium falciparum in The Gambia. Infect Immun 71(4): 1856-63.
5. Baum J, Thomas AW, Conway DJ (2003) Evidence for diversifying selection on erythrocyte-binding antigens of Plasmodium falciparum and P. vivax. Genetics 163(4): 1327-36.
6. Lobo CA, de Frazao K, Rodriguez M, Reid M, Zalis M, et al. (2004) Invasion profiles of Brazilian field isolates of Plasmodium falciparum: phenotypic and genotypic analyses. Infect Immun 72(10): 5886-91.
7. Bei AK, Membi CD, Rayner JC, Mubi M, Ngasala B, et al. (2007) Variant merozoite protein expression is associated with erythrocyte invasion phenotypes in Plasmodium falciparum isolates from Tanzania. Mol Biochem Parasitol 153(1): 66-71.
8. Deans AM, Nery S, Conway DJ, Kai O, Marsh K, et al. (2007) Invasion Pathways and Malaria Severity in Kenyan Plasmodium falciparum Clinical Isolates. Infect Immun 75(6): 3014-20.
9. Jennings CV, Ahouidi AD, Zilversmit M, Bei AK, Rayner J, et al. (2007) Molecular analysis of erythrocyte invasion in Plasmodium falciparum isolates from Senegal. Infect Immun 75(7): 3531-8.
10. Pasvol G, Wainscoat JS, Weatherall DJ (1982) Erythrocytes deficiency in glycophorin resist invasion by the malarial parasite Plasmodium falciparum. Nature 297(5861): 64-6.
11. Pasvol G, Jungery M, Weatherall DJ, Parsons SF, Anstee DJ, et al. (1982) Glycophorin as a possible receptor for Plasmodium falciparum. Lancet 2(8305): 947-50.
12. Hadley TJ (1986) Invasion of erythrocytes by malaria parasites: a cellular and molecular overview. Annu Rev Microbiol 40: 451-77.
13. Booth PB, Albrey JA, Whittaker J, Sanger R (1970) Gerbich blood group system: a useful genetic marker in certain Melanesians of Papua and New Guinea. Nature 228(270): 462.
14. Booth PB, McLoughlin K, Hornabrook RW, Macgregor A, Malcolm LA (1972) The Gerbich blood group system in New Guinea. II. The Morobe District and North Papuan Coast. Hum Biol Oceania 1(4): 259-66.
15. Macgregor A, Booth PB (1973) A second example of anti-Ge1, and some observations on Gerbich subgroups. Vox Sang 25(5): 474-8.
16. Booth PB, Tills D, Warlow A, Kopec AC, Mourant AE, et al. (1982) Red cell antigen, serum protein and red cell enzyme polymorphisms in Karkar Islanders and inhabitants of the adjacent North Coast of New Guinea. Hum Hered 32(6): 385-403.
17. Serjeantson SW, White BS, Bhatia K, Trent RJ (1994) A 3.5 kb deletion in the glycophorin C gene accounts for the Gerbich-negative blood group in Melanesians. Immunol Cell Biol 72(1): 23-7.
18. Patel SS, King CL, Mgone CS, Kazura JW, Zimmerman PA (2004) Glycophorin C (Gerbich antigen blood group) and band 3 polymorphisms in two malaria holoendemic regions of Papua New Guinea. Am J Hematol 75(1): 1-5.
19. Allen SJ, O'Donnell A, Alexander ND, Mgone CS, Peto TE, et al. (1999) Prevention of cerebral malaria in children in Papua New Guinea by southeast Asian ovalocytosis band 3. Am J Trop Med Hyg 60(6): 1056-60.
20. Miller LH, Haynes JD, McAuliffe FM, Shiroishi T, Durocher JR, et al. (1977) Evidence for differences in erythrocyte surface receptors for the malarial parasites, Plasmodium falciparum and Plasmodium knowlesi. J Exp Med 146(1): 277-81.
21. Facer CA (1983) Merozoites of P. falciparum require glycophorin for invasion into red cells. Bull Soc Pathol Exot Filiales 76(5): 463-9.
22. Facer CA (1983) Erythrocyte sialoglycoproteins and Plasmodium falciparum invasion. Trans R Soc Trop Med Hyg 77(4): 524-30.
23. Pasvol G (1984) Receptors on red cells for Plasmodium falciparum and their interaction with merozoites. Philos Trans R Soc Lond B Biol Sci 307(1131): 189-200.
24. Weatherall DJ (1996) Host genetics and infectious disease. Parasitology 112 Suppl: S23-9.
25. Miller LH (1994) Impact of malaria on genetic polymorphism and genetic diseases in Africans and African Americans. Proc Natl Acad Sci U S A 91(7): 2415-9.
26. Wang HY, Tang H, Shen CK, Wu CI (2003) Rapidly evolving genes in human. I. The glycophorins and their possible role in evading malaria parasites. Mol Biol Evol 20(11): 1795-804.
27. Reid ME, Lomas-Francis C (2004) The Blood Group Antigen. 2nd ed. FactBook Seriers Elsevier, Academic Press.
28. Huang CH, Blumenfeld OO (1988) Characterization of a genomic hybrid specifying the human erythrocyte antigen Dantu: Dantu gene is duplicated and linked to a delta glycophorin gene deletion. Proc Natl Acad Sci U S A 85(24): 9640-4.
29. Storry JR, Reid ME, Fetics S, Huang CH (2003) Mutations in GYPB exon 5 drive the S2s2U+(var) phenotype in persons of African descent: implications for transfusion. Transfusion 43(12): 1738-47.
30. Unger P, Procter JL, Moulds JJ, Moulds M, Blanchard D, et al. (1987) The Dantu erythrocyte phenotype of the NE variety. II. Serology, immunochemistry, genetics, and frequency. Blut 55(1): 33-43.
31. Contreras M, Green C, Humphreys J, Tippett P, Daniels G, et al. (1984) Serology and genetics of an MNSs-associated antigen Dantu. Vox Sang 46(6): 377-86.
32. Field SP, Hempelmann E, Mendelow BV, Fleming AF (1994) Glycophorin variants and Plasmodium falciparum: protective effect of the Dantu phenotype in vitro. Hum Genet 93(2): 148-50.
33. Storry JR, Reid ME, MacLennan S, Lubenko A, Nortman P (2001) The lowincidence MNS antigens M(v), s(D), and Mit arise from single amino acid substitutions on GPB. Transfusion 41(2): 269-75.
34. Dahr W, Moulds JJ (1987) High-frequency antigens of human erythrocyte membrane sialoglycoproteins, IV. Molecular properties of the U antigen. Biol Chem Hoppe Seyler 368(6): 659-67.
35. Blumenfeld OO, Huang CH (1997) Molecular genetics of glycophorin MNS variants. Transfus Clin Biol 4(4): 357-65.
36. Reid ME, Storry JR, Ralph H, Blumenfeld OO, Huang CH (1996) Expression and quantitative variation of the low-incidence blood group antigen He on some S2s2red cells. Transfusion 36(8): 719-24.
37. Huang CH, Blumenfeld OO, Reid ME, Chen Y, Daniels GL, et al. (1997) Alternative splicing of a novel glycophorin allele GPHe(GL) generates two protein isoforms in the human erythrocyte membrane. Blood 90(1): 391-7.
38. Fraser GR, Giblett ER, Motulsky AG (1966) Population genetic studies in the Congo. 3. Blood groups (ABO, MNSs, Rh, Jsa). Am J Hum Genet 18(6): 546-52.
39. Vos GH, Moores P, Lowe RF (1971) A comparative study between the S2s2U2phenotype found in Central African Negroes and the S2s+U2penotype in Rhnull individuals. S Afr J Med Sci 36(1): 1-6.
40. Lowe RF, Moores PP (1972) S2s2U2red cell factor in Africans of Rhodesia, Malawi, Mozambique and Natal. Hum Hered 22(4): 344-50.
41. Issitt PD, Anstee DJ (1998) Applied blood group serology. 4th ed, ed. N.C. Durham Montgomery Scientific Publications.
42. Patel SS, Katsnelson S, McNamara D, Reeder JC, Kazura JW, et al. (2004) Multiple Erythrocyte Polymorphisms Including a Glycophorin B Variant in a malaria endemic area of Papua New Guinea. ASTMH Abstract #913 2004.
43. Conrad DF, Pinto D, Redon R, Feuk L, Gokcumen O, et al. Origins and functional impact of copy number variation in the human genome. Nature 464(7289): 704-12.
44. Mayer DC, Cofie J, Jiang L, Hartl DL, Tracy E, et al. (2009) Glycophorin B is the erythrocyte receptor of Plasmodium falciparum erythrocyte-binding ligand, EBL-1. Proc Natl Acad Sci U S A 106(13): 5348-52.
45. Baleotti W, Jr., Rios M, Reid ME, Fabron A, Jr., Pellegrino J, Jr., et al. (2003) A novel DI*A allele without the Band 3-Memphis mutation in Amazonian Indians. Vox Sang 84(4): 326-30.
46. Castilho L, Rios M, Pellegrino J, Jr., Saad ST, Costa FF, et al. (2004) A Novel FY Allele in Brazilians. Vox Sang 87(3): 190-5.
47. Baleotti W, Jr., Rios M, Reid ME, Hashmi G, Fabron A, Jr., et al. (2006) Dombrock gene analysis in Brazilian people reveals novel alleles. Vox Sang 91(1): 81-7.
48. Montoya F, Restrepo M, Montoya AE, Rojas W (1994) Blood groups and malaria. Rev Inst Med Trop Sao Paulo 36(1): 33-8.
49. Beiguelman B, Alves FP, Moura MM, Engracia V, Nunes AC, et al. (2003) The association of genetic markers and malaria infection in the Brazilian Western Amazonian region. Mem Inst Oswaldo Cruz 98(4): 455-60.
50. Cavasini CE, De Mattos LC, Alves RT, Couto AA, Calvosa VS, et al. (2006) Frequencies of ABO, MNSs, and Duffy phenotypes among blood donors and malaria patients from four Brazilian Amazon areas. Hum Biol 78(2): 215-9.
51. Kimura M, Kaneko O, Liu Q, Zhou M, Kawamoto F, et al. (1997) Identification of the four species of human malaria parasites by nested PCR that targets variant sequences in the small subunit rRNA gene. Parasitology International 46: 91-95.
52. Hashmi G, Shariff T, Seul M, Vissavajjhala P, Hue-Roye K, et al. (2005) A flexible array format for large-scale, rapid blood group DNA typing. Transfusion 45(5): 680-8.
53. Hashmi G, Shariff T, Zhang Y, Cristobal J, Chau C, et al. (2007) Determination of 24 minor red blood cell antigens for more than 2000 blood donors by highthroughput DNA analysis. Transfusion 47(4): 736-47.
54. Montgomery KT, Iartchouck O, Li L, Loomis S, Obourn V, et al. (2008) PolyPhred analysis software for mutation detection from fluorescence-based sequence data. Curr Protoc Hum Genet Chapter 7: Unit 7 16.
55. Machado M, Magalhães WCS, Sene A, Araújo B, Faria-Campos A, et al. (2010) Phred-Phrap-Consed-Polyphred to analyses tools: a pipeline to facilitate population genetics re-sequencing studies. Investigative Genetics In Press.
56. da Silva MC, Zuccherato LW, Soares-Souza GB, Vieira ZM, Cabrera L, et al. (2010) Development of two flexible multiplex mini-sequencing panels of ancestry informative SNPs for admixture studies in Latin Americans and their application to populations of the state of Minas Gerais in Brazil. Genetics and Molecular Research 9(4): 2069-85.
57. Santos NP, Ribeiro-Rodrigues EM, Ribeiro-Dos-Santos AK, Pereira R, Gusmao L, et al. (2010) Assessing individual interethnic admixture and population substructure using a 48-insertion-deletion (INSEL) ancestry-informative marker (AIM) panel. Hum Mutat 31(2): 184-90.
58. Schaid DJ, Rowland CM, Tines DE, Jacobson RM, Poland GA (2002) Score tests for association between traits and haplotypes when linkage phase is ambiguous. Am J Hum Genet 70(2): 425-34.
59. Lake SL, Lyon H, Tantisira K, Silverman EK, Weiss ST, et al. (2003) Estimation and tests of haplotype-environment interaction when linkage phase is ambiguous. Hum Hered 55(1): 56-65.
60. Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67(1): 170-81.
61. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2): 945-59.
62. Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet 76(3): 449-62.
63. Li N, Stephens M (2003) Modeling linkage disequilibrium and identifying recombination hotspots using single-nucleotide polymorphism data. Genetics 165(4): 2213-33.
64. Hill WG, Robertson AR (1968) Linkage disequilibrium in finite populations. Theor Appl Genet 38: 226-231.
65. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21(2): 263-5.
66. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105(2): 437-60.
67. Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7(2): 256-76.
68. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3): 585-95.
69. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133(3): 693-709.
70. Omoto R, Reid ME, Castilho L (2008) Molecular analyses of GYPB in African Brazilians. Immunohematology 24(4): 148-53.
71. Miller LH, Mason SJ, Dvorak JA, McGinniss MH, Rothman IK (1975) Erythrocyte receptors for (Plasmodium knowlesi) malaria: Duffy blood group determinants. Science 189(4202): 561-3.
72. Michon P, Woolley I, Wood EM, Kastens W, Zimmerman PA, et al. (2001) Duffy-null promoter heterozygosity reduces DARC expression and abrogates adhesion of the P. vivax ligand required for blood-stage infection. FEBS Lett 495(1-2): 111-4.
73. Cavasini CE, de Mattos LC, Couto AA, Couto VS, Gollino Y, et al. (2007) Duffy blood group gene polymorphisms among malaria vivax patients in four areas of the Brazilian Amazon region. Malar J 6: 167.
74. Lell B, May J, Schmidt-Ott RJ, Lehman LG, Luckner D, et al. (1999) The role of red blood cell polymorphisms in resistance and susceptibility to malaria. Clin Infect Dis 28(4): 794-9.
75. Carter R, Mendis KN (2002) Evolutionary and historical aspects of the burden of malaria. Clin Microbiol Rev 15(4): 564-94.
76. Zimmerman PA, Patel SS, Maier AG, Bockarie MJ, Kazura JW (2003) Erythrocyte polymorphisms and malaria parasite invasion in Papua New Guinea. Trends Parasitol 19(6): 250-2.
77. Dahr W (1986) Recent Advances in Blood Group Biochemistry VVengelen-Tyler, WJJudd, eds. ArlingtonVA: American Association of Blood Banks. pp 23-65.
78. Ramensky V, Bork P, Sunyaev S (2002) Human non-synonymous SNPs: server and survey. Nucleic Acids Res 30(17): 3894-900.
79. Williamson SH, Hernandez R, Fledel-Alon A, Zhu L, Nielsen R, et al. (2005) Simultaneous inference of selection and population growth from patterns of variation in the human genome. Proc Natl Acad Sci U S A 102(22): 7882-7.
80. Sabeti PC (2008) Natural selection: Uncovering mechanisms of evolutionary adaptation to infectious disease. Nature Education 1(1).
81. Ayodo G, Price AL, Keinan A, Ajwang A, Otieno MF, et al. (2007) Combining evidence of natural selection with association analysis increases power to detect malaria-resistance variants. Am J Hum Genet 81(2): 234-42.
82. Akey JM, Eberle MA, Rieder MJ, Carlson CS, Shriver MD, et al. (2004) Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol 2(10): e286.
83. Haldane JBS (1949) Disease and evolution. Ricerca Science Supplement 19: 3-10.
84. Escalante AA, Barrio E, Ayala FJ (1995) Evolutionary origin of human and primate malarias: evidence from the circumsporozoite protein gene. Mol Biol Evol 12(4): 616-26.
85. Neafsey DE, Schaffner SF, Volkman SK, Park D, Montgomery P, et al. (2008) Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence. Genome Biol 9(12): R171.
86. Campbell MC, Tishkoff SA (2008) African genetic diversity: implications for human demographic history, modern human origins, and complex disease mapping. Annu Rev Genomics Hum Genet 9: 403-33.
87. Grossman SR, Shylakhter I, Karlsson EK, Byrne EH, Morales S, et al. (2010) A composite of multiple signals distinguishes causal variants in regions of positive selection. Science 327(5967): 883-6.
88. International HapMap 3 Consortium, Altshuler DM, Gibbs RA, Peltonen L, Dermitzakis E, et al. (2010) Integrating common and rare genetic variation in diverse human populations. Nature 467(7311): 52-8.
89. 1000 Genomes Project Consortium, Durbin RM, Abecasis GR, Altshuler DL, Auton A, et al. (2010) A map of human genome variation from population-scale sequencing. Nature 467(7319): 1061-73.
90. Machado RLD, Povoa MM, Calvosa VSP, Ferreira MU, Rossit ARB, et al. (2004) Genetic Structure of Plasmodium falciparum populations in the Brazilian Amazon Region. The Journal of Infectious Disease 190(9): 1547-1555.