Worldwide genetic variation at the 3′ untranslated region of the HLA-G gene: Balancing selection influencing genetic diversity

Genes and Immunity

Volumn 15, Issue 2, 2014, Pages 95-106

  Sabbagh, A ^a,b   Luisi, P ^c   Castelli, E C ^d   Gineau, L ^a,b   Courtin, D ^e   Milet, J ^e   Massaro, J D ^f   Laayouni, H ^c   Moreau, P ^g,h   Donadi, E A ^f   Garcia, A ^a,b  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^e UNIVERSITY OF ABOMEY CALAVI   (Benin)

^f UNIVERSITY OF SÃO PAULO   (Brazil)

^g SAINT LOUIS HOSPITAL   (France)

^h UNIVERSITÉ PARIS DIDEROT   (France)

Author keywords

30UTR; Balancing selection; Evolution; Haplotype; HLA G; Linkage disequilibrium

Indexed keywords

HLA G ANTIGEN; NUCLEOTIDE;

3' UNTRANSLATED REGION; AFRICA SOUTH OF THE SAHARA; ARTICLE; BALANCING SELECTION; CONTROLLED STUDY; DEMOGRAPHY; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; HUMAN EXPERIMENT; HUMAN GENOME; INDEL MUTATION; MALE; POPULATION DIFFERENTIATION; POPULATION GENETICS; PRIORITY JOURNAL; PROTEIN PROCESSING; SEQUENCE ANALYSIS;

3' UNTRANSLATED REGIONS; AFRICA; AMERICAS; ASIA; BASE SEQUENCE; ETHNIC GROUPS; EUROPE; FEMALE; GENE FREQUENCY; HAPLOTYPES; HLA-G ANTIGENS; HUMANS; IMMUNE TOLERANCE; INDEL MUTATION; LINKAGE DISEQUILIBRIUM; MALE; POLYMORPHISM, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 84895876454     PISSN: 14664879     EISSN: 14765470     Source Type: Journal    
DOI: 10.1038/gene.2013.67     Document Type: Article

References (79)

1. Hviid TV. HLA-G in human reproduction: Aspects of genetics, function and pregnancy complications. Hum Reprod Update 2006; 12: 209-232.
2. Rizzo R, Vercammen M, van de Velde H, Horn PA, Rebmann V. The importance of HLA-G expression in embryos, trophoblast cells, and embryonic stem cells. Cell Mol Life Sci 2011; 68: 341-352.
3. Larsen MH, Bzorek M, Pass MB, Larsen LG, Nielsen MW, Svendsen SG et al. Human leukocyte antigen-G in the male reproductive system and in seminal plasma. Mol Hum Reprod 2011; 17: 727-738.
4. Crisa L, McMaster MT, Ishii JK, Fisher SJ, Salomon DR. Identification of a thymic epithelial cell subset sharing expression of the class Ib HLA-G molecule with fetal trophoblasts. J Exp Med 1997; 186: 289-298.
5. Le Discorde M, Moreau P, Sabatier P, Legeais JM, Carosella ED. Expression of HLA-G in human cornea, an immune-privileged tissue. Hum Immunol 2003; 64: 1039-1044.
6. Menier C, Rabreau M, Challier JC, Le Discorde M, Carosella ED, Rouas-Freiss N. Erythroblasts secrete the nonclassical HLA-G molecule from primitive to definitive hematopoiesis. Blood 2004; 104: 3153-3160.
7. Larsen MH, Hviid TV. Human leukocyte antigen-G polymorphism in relation to expression, function, and disease. Hum Immunol 2009; 70: 1026-1034.
8. Donadi EA, Castelli EC, Arnaiz-Villena A, Roger M, Rey D, Moreau P. Implications of the polymorphism of HLA-G on its function, regulation, evolution and disease association. Cell Mol Life Sci 2011; 68: 369-395.
9. Carosella ED. The tolerogenic molecule HLA-G. Immunol Lett 2011; 138: 22-24.
10. Deschaseaux F, Delgado D, Pistoia V, Giuliani M, Morandi F, Durrbach A. HLA-G in organ transplantation: Towards clinical applications. Cell Mol Life Sci 2011; 68: 397-404.
11. Yie SM, Hu Z. Human leukocyte antigen-G (HLA-G) as a marker for diagnosis, prognosis and tumor immune escape in human malignancies. Histol Histopathol 2011; 26: 409-420.
12. González A, Rebmann V, LeMaoult J, Horn PA, Carosella ED, Alegre E. The immunosuppressive molecule HLA-G and its clinical implications. Crit Rev Clin Lab Sci 2012; 49: 63-84.
13. Castelli EC, Mendes-Junior CT, Veiga-Castelli LC, Roger M, Moreau P, Donadi EA. A comprehensive study of polymorphic sites along the HLA-G gene: Implication for gene regulation and evolution. Mol Biol Evol 2011; 28: 3069-3086.
14. Tan Z, Shon AM, Ober C. Evidence of balancing selection at the HLA-G promoter region. Hum Mol Genet 2005; 14: 3619-3628.
15. Hviid TV, Rizzo R, Melchiorri L, Stignani M, Baricordi OR. Polymorphism in the 5' upstream regulatory and 3' untranslated regions of the HLA-G gene in relation to soluble HLA-G and IL-10 expression. Hum Immunol 2006; 67: 53-62.
16. Alvarez M, Piedade J, Balseiro S, Ribas G, Regateiro F. HLA-G 3'-UTR SNP and 14-bp deletion polymorphisms in Portuguese and Guinea-Bissau populations. Int J Immunogenet 2009; 36: 361-366.
17. Castelli EC, Mendes-Junior CT, Deghaide NH, de Albuquerque RS, Muniz YC, Simö es RT et al. The genetic structure of 3'untranslated region of the HLA-G gene: Polymorphisms and haplotypes. Genes Immun 2010; 11: 134-141.
18. Lucena-Silva N, Monteiro AR, de Albuquerque RS, Gomes RG, Mendes-Junior CT, Castelli EC et al. Haplotype frequencies based on eight polymorphic sites at the 3' untranslated region of the HLA-G gene in individuals from two different geographical regions of Brazil. Tissue Antigens 2012; 79: 272-278.
19. Tan Z, Randall G, Fan J, Camoretti-Mercado B, Brockman-Schneider R, Pan L et al. Allele-specific targeting of microRNAs to HLA-G and risk of asthma. Am J Hum Genet 2007; 81: 829-834.
20. Yie SM, Li LH, Xiao R, Librach CL. A single base-pair mutation in the 3'-untranslated region of HLA-G mRNA is associated with pre-eclampsia. Mol Hum Reprod 2008; 14: 649-653.
21. Castelli EC, Moreau P, Oya E, Chiromatzo A, Mendes-Junior CT, Veiga-Castelli LC et al. In silico analysis of microRNAS targeting the HLA-G 3' untranslated region alleles and haplotypes. Hum Immunol 2009; 70: 1020-1025.
22. Svendsen SG, Hantash BM, Zhao L, Faber C, Bzorek M, Nissen MH et al. The expression and functional activity of membrane-bound human leukocyte antigen-G1 are influenced by the 3'-untranslated region. Hum Immunol 2013; 74: 818-827.
23. Courtin D, Milet J, Sabbagh A, Massaro JD, Castelli EC, Jamonneau V et al. HLA-G 3' UTR-2 haplotype is associated with Human African trypanosomiasis susceptibility. Infect Genet Evol 2013; 17: 1-7.
24. Garcia A, Milet J, Courtin D, Sabbagh A, Massaro JD, Castelli EC et al. Association of HLA-G 3'UTR polymorphisms with response to malaria infection: A first insight. Infect Genet Evol 2013; 16: 263-269.
25. Sabbagh A, Courtin D, Milet J, Massaro JD, Castelli EC, Migot-Nabias F et al. Association of HLA-G 3' untranslated region polymorphisms with antibody response against Plasmodium falciparum antigens: Preliminary results. Tissue Antigens 2013; 82: 53-58.
26. Goldstein DB, Chikhi L. Human migrations and population structure: What we know and why it matters. Annu Rev Genomics Hum Genet 2002; 3: 129-152.
27. Campbell MC, Tishkoff SA. African genetic diversity: Implications for human demographic history, modern human origins, and complex disease mapping. Annu Rev Genomics Hum Genet 2008; 9: 403-433.
28. The 1000 Genomes Project Consortium, Abecasis GR, Auton A, Brooks LD, DePristo MA, Durbin RM et al. An integrated map of genetic variation from 1,092 human genomes. Nature 2012; 491: 56-65.
29. Castro MJ, Morales P, Martinez-Laso J, Allende L, Rojo-Amigo R, Gonzalez-Hevilla M et al. Evolution of MHC-G in humans and primates based on three new 3'UT polymorphisms. Hum Immunol 2000; 61: 1157-1163.
30. Akey JM, Zhang G, Zhang K, Jin L, Shriver MD. Interrogating a high-density SNP map for signatures of natural selection. Genome Res 2002; 12: 1805-1814.
31. Elhaik E. Empirical distributions of FST from large-scale human polymorphism data. PLoS One 2012; 7: E49837.
32. Mu XJ, Lu ZJ, Kong Y, Lam HY, Gerstein MB. Analysis of genomic variation in non-coding elements using population-scale sequencing data from the 1000 Genomes Project. Nucleic Acids Res 2011; 39: 7058-7076.
33. Maruyama T, Fuerst PA. Population bottlenecks and non-equilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 1985; 111: 675-689.
34. Tishkoff SA, Reed FA, Friedlaender FR, Ehret C, Ranciaro A, Froment A et al. The genetic structure and history of Africans and African Americans. Science 2009; 324: 1035-1044.
35. Henn BM, Cavalli-Sforza LL, Feldman MW. The great human expansion. Proc Natl Acad Sci USA 2012; 109: 17758-17764.
36. Nielsen R. Statistical tests of selective neutrality in the age of genomics. Heredity 2001; 86: 641-647.
37. Teshima KM, Coop G, Przeworski M. How reliable are empirical genomic scans for selective sweeps? Genome Res 2006; 16: 702-712.
38. Yu F, Keinan A, Chen H, Ferland RJ, Hill RS, Mignault AA et al. Detecting natural selection by empirical comparison to random regions of the genome. Hum Mol Genet 2009; 18: 4853-4867.
39. Akey JM. Constructing genomic maps of positive selection in humans: Where do we go from here? Genome Res 2009; 19: 711-722.
40. Laval G, Patin E, Barreiro LB, Quintana-Murci L. Formulating a historical and demographic model of recent human evolution based on resequencing data from noncoding regions. PLoS One 2010; 5: E10284.
41. McEvoy BP, Powell JE, Goddard ME, Visscher PM. Human population dispersal 'Out of Africa' estimated from linkage disequilibrium and allele frequencies of SNPs. Genome Res 2011; 21: 821-829.
42. Pritchard JK. Whole-genome sequencing data offer insights into human demography. Nat Genet 2011; 43: 923-925.
43. Pluzhnikov A, Donnelly P. Optimal sequencing strategies for surveying molecular genetic diversity. Genetics 1996; 144: 1247-1262.
44. Martelli-Palomino G, Pancoto JA, Muniz YCN, Mendes-Junior CT, Castelli EC, Massaro JD et al. Polymorphic sites at the 3' untranslated region of the HLA-G gene are associated with differential HLA-G soluble levels in the Brazilian and French population. PLoS One 2013; 8: E71742.
45. Larsen MH, Hylenius S, Andersen AM, Hviid TV. The 3'-untranslated region of the HLA-G gene in relation to pre-eclampsia: Revisited. Tissue Antigens 2010; 75: 253-261.
46. O'Brien M, McCarthy T, Jenkins D, Paul P, Dausset J, Carosella ED et al. Altered HLA-G transcription in pre-eclampsia is associated with allele specific inheritance: Possible role of the HLA-G gene in susceptibility to the disease. Cell Mol Life Sci 2001; 58: 1943-1949.
47. Hviid TV, Hylenius S, Rorbye C, Nielsen LG. HLA-G allelic variants are associated with differences in the HLA-G mRNA isoform profile and HLA-G mRNA levels. Immunogenetics 2003; 55: 63-79.
48. Rousseau P, Le Discorde M, Mouillot G, Marcou C, Carosella ED, Moreau P. The 14-bp Deletion-Insertion polymorphism in the 3' UT region of the HLA-G gene influences HLA-G mRNA stability. Hum Immunol 2003; 64: 1005-1010.
49. Gonzalez A, Alegre E, Torres MI, Díaz-Lagares A, Lorite P, Palomeque T et al. Evaluation of HLA-G5 plasmatic levels during pregnancy and relationship with the 14-bp polymorphism. Am J Reprod Immunol 2010; 64: 367-374.
50. Mendes-Junior CT, Castelli EC, Simö es RT, Simö es AL, Donadi EA. HLA-G 14-bp polymorphism at exon 8 in Amerindian populations from the Brazilian Amazon. Tissue Antigens 2007; 69: 255-260.
51. Veit TD, Cazarolli J, Salzano FM, Schiengold M, Chies JA. New evidence for balancing selection at the HLA-G locus in South Amerindians. Genet Mol Biol 2012; 35: 919-923.
52. Hviid TV, Rizzo R, Christiansen OB, Melchiorri L, Lindhard A, Baricordi OR. HLA-G and IL-10 in serum in relation to HLA-G genotype and polymorphisms. Immunogenetics 2004; 56: 135-141.
53. Santos KE, Lima THA, Felício LP, Massaro JD, Palomino GM, Silva ACA et al. Insights on the HLA-G evolutionary history provided by a nearby Alu insertion. Mol Biol Evol 2013; 30: 2423-2434.
54. Ober C, Rosinsky B, Grimsley C, van der Ven K, Robertson A, Runge A. Population genetic studies of HLA-G: Allele frequencies and linkage disequilibrium with HLAA1. J Reprod Immunol 1996; 32: 111-123.
55. van der Ven K, Skrablin S, Engels G, Krebs D. HLA-G polymorphisms and allele frequencies in Caucasians. Hum Immunol 1998; 59: 302-312.
56. Hviid TV, Christiansen OB. Linkage disequilibrium between human leukocyte antigen (HLA) class II and HLA-G-possible implications for human reproduction and autoimmune disease. Hum Immunol 2005; 66: 688-699.
57. Castelli EC, Mendes-Junior CT, Viana de Camargo JL, Donadi EA. HLA-G polymorphism and transitional cell carcinoma of the bladder in a Brazilian population. Tissue Antigens 2008; 72: 149-157.
58. Park Y, Park Y, Kim YS, Kwon OJ, Kim HS. Allele frequencies of human leukocyte antigen-G in a Korean population. Int J Immunogenet 2012; 39: 39-45.
59. Courtin D, Milet J, Jamonneau V, Yeminanga CS, Kumeso VK, Bilengue CM et al. Association between human African trypanosomiasis and the IL6 gene in a Congolese population. Infect Genet Evol 2007; 7: 60-68.
60. Milet J, Nuel G, Watier L, Courtin D, Slaoui Y, Senghor P et al. Genome wide linkage study, using a 250K SNP map, of Plasmodium falciparum infection and mild malaria attack in a Senegalese population. PLoS One 2010; 5: E11616.
61. Le Port A, Cottrell G, Martin-Prevel Y, Migot-Nabias F, Cot M, Garcia A. First malaria infections in a cohort of infants in Benin: Biological, environmental and genetic determinants. Description of the study site, population methods and preliminary results. BMJ Open 2012; 2: E000342.
62. Hill WG, Robertson A. Linkage disequilibrium in finite populations. Theor Appl Genet 1968; 38: 226-231.
63. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics 2005; 21: 263-265.
64. Stephens M, Donnelly P. A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 2003; 73: 1162-1169.
65. Excoffier L, Smouse PE, Quattro JM. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 1992; 131: 479-491.
66. Excoffier L, Laval G, Schneider S. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 2005; 1: 47-50.
67. Li Y, Willer CJ, Ding J, Scheet P, Abecasis GR. MaCH: Using sequence and genotype data to estimate haplotypes and unobserved genotypes. Genet Epidemiol 2010; 34: 816-834.
68. Wright S. The genetical structure of populations. Ann Eug 1951; 15: 323-354.
69. Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, Dagdigian C et al. The Bioperl toolkit: Perl modules for the life sciences. Genome Res 2002; 12: 1611-1618.
70. Kelley JL, Madeoy J, Calhoun JC, Swanson W, Akey JM. Genomic signatures of positive selection in humans and the limits of outlier approaches. Genome Res 2006; 16: 980-989.
71. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D et al. PLINK: A toolset for whole-genome association and population-based linkage analysis. Am J Hum Genet 2007; 81: 559-575.
72. Barreiro LB, Laval G, Quach H, Patin E, Quintana-Murci L. Natural selection has driven population differentiation in modern humans. Nat Genet 2008; 40: 340-345.
73. Beaumont MA, Nichols RA. Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B 1996; 263: 1619-1626.
74. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989; 123: 585-595.
75. Fu YX, Li WH. Statistical tests of neutrality of mutations. Genetics 1993; 133: 693-709.
76. Librado P, Rozas J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009; 25: 1451-1452.
77. Watterson GA. On the number of segregating sites in genetical models without recombination. Theor Popul Biol 1975; 7: 256-276.
78. Woolfe A, Goode DK, Cooke J, Callaway H, Smith S, Snell P et al. CONDOR: A database resource of developmentally associated conserved non-coding elements. BMC Dev Biol 2007; 7: 100.
79. Nei M. Molecular Evolutionary Genetics. Columbia University Press: New York, 1987.