Genetic diversity of the HLA-G coding region in Amerindian populations from the Brazilian Amazon: A possible role of natural selection

Genes and Immunity

Volumn 14, Issue 8, 2013, Pages 518-526

  Mendes Junior, C T ^a   Castelli, E C ^b   Meyer, D ^a   Simoes A L ^a   Donadi, E A ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Amerindians; evolution; HLA G; MHC; natural selection; South America

Indexed keywords

HLA G ANTIGEN;

ALLELE; AMERICAN INDIAN; ARTICLE; BRAZIL; CONTROLLED STUDY; CROSSING OVER; DNA FLANKING REGION; EXON; GENE FREQUENCY; GENETIC ALGORITHM; GENETIC VARIABILITY; HAPLOTYPE; HETEROZYGOSITY; HUMAN; NATURAL SELECTION; NONHUMAN; PRIMATE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM;

ALLELES; BRAZIL; CROSSING OVER, GENETIC; EXONS; HAPLOTYPES; HLA-G ANTIGENS; HUMANS; INDIANS, CENTRAL AMERICAN; OPEN READING FRAMES; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC;

EID: 84889654213     PISSN: 14664879     EISSN: 14765470     Source Type: Journal    
DOI: 10.1038/gene.2013.47     Document Type: Article

References (78)

1. Pyo CW, Williams LM, Moore Y, Hyodo H, Li SS, Zhao LP et al. HLA-E, HLA-F, and HLA-G polymorphism: genomic sequence defines haplotype structure and variation spanning the nonclassical class I genes. Immunogenetics 2006; 58: 241-251.
2. Hviid TV. HLA-G in human reproduction: aspects of genetics, function and pregnancy complications. Hum Reprod Update 2006; 12: 209-232.
3. 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.
4. 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.
5. Carosella ED, Gregori S, Rouas-Freiss N, LeMaoult J, Menier C, Favier B. The role of HLA-G in immunity and hematopoiesis. Cell Mol Life Sci 2011; 68: 353-368.
6. Amiot L, Ferrone S, Grosse-Wilde H, Seliger B. Biology of HLA-G in cancer: a candidate molecule for therapeutic intervention? Cell Mol Life Sci 2011; 68: 417-431.
7. Fujii T, Ishitani A, Geraghty DE. A soluble form of the HLA-G antigen is encoded by a messenger ribonucleic acid containing intron 4. J Immunol 1994; 153: 5516-5524.
8. LeMaoult J, Krawice-Radanne I, Dausset J, Carosella ED. HLA-G1-expressing antigen-presenting cells induce immunosuppressive CD4\+ T cells. Proc Natl Acad Sci USA 2004; 101: 7064-7069.
9. Rouas-Freiss N, Goncalves RM, Menier C, Dausset J, Carosella ED. Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc Natl Acad Sci USA 1997; 94: 11520-11525.
10. Ristich V, Liang S, Zhang W, Wu J, Horuzsko A. Tolerization of dendritic cells by HLA-G. Eur J Immunol 2005; 35: 1133-1142.
11. 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.
12. Ober C, Aldrich CL, Chervoneva I, Billstrand C, Rahimov F, Gray HL et al. Variation in the HLA-G promoter region influences miscarriage rates. Am J Hum Genet 2003; 72: 1425-1435.
13. 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.
14. Solier C, Mallet V, Lenfant F, Bertrand A, Huchenq A, Le Bouteiller P. HLA-G unique promoter region: functional implications. Immunogenetics 2001; 53: 617-625.
15. Castelli EC, Mendes-Junior CT, Deghaide NH, de Albuquerque RS, Muniz YC, Simoes RT et al. The genetic structure of 30untranslated region of the HLA-G gene: polymorphisms and haplotypes. Genes Immun 2010; 11: 134-141.
16. Castelli EC, Moreau P, Oya e Chiromatzo A, Mendes-Junior CT, Veiga-Castelli LC, Yaghi L et al. In silico analysis of microRNAS targeting the HLA-G 30 untranslated region alleles and haplotypes. Hum Immunol 2009; 70: 1020-1025.
17. Tan Z, Shon AM, Ober C. Evidence of balancing selection at the HLA-G promoter region. Hum Mol Genet 2005; 14: 3619-3628.
18. 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.
19. Meyer D, Thomson G. How selection shapes variation of the human major histocompatibility complex: a review. Ann Hum Genet 2001; 65(Pt 1): 1-26.
20. Mendes-Junior CT, Castelli EC, Moreau P, Simoes AL, Donadi EA. Absence of the HLA-G*0113N allele in Amerindian populations from the Brazilian Amazon region. Hum Immunol 2010; 71: 428-431.
21. Mendes-Junior CT, Castelli EC, Simoes AL, Donadi EA. Absence of the HLAG* 0105N allele in Amerindian populations from the Brazilian Amazon Region: a possible role of natural selection. Tissue Antigens 2007; 70: 330-334.
22. Ober C, Aldrich CL. HLA-G polymorphisms: neutral evolution or novel function? J Reprod Immunol 1997; 36: 1-21.
23. Suarez MB, Morales P, Castro MJ, Fernandez V, Varela P, Alvarez M et al. A new HLA-G allele (HLA-G*0105N) and its distribution in the Spanish population. Immunogenetics 1997; 45: 464-465.
24. Lajoie J, Jeanneau A, Faucher MC, Moreau P, Roger M. Characterisation of five novel HLA-G alleles with coding DNA base changes. Tissue Antigens 2008; 72: 502-504.
25. Pfeiffer KA, Fimmers R, Engels G, van der Ven H, van der Ven K. The HLA-G genotype is potentially associated with idiopathic recurrent spontaneous abortion. Mol Hum Reprod 2001; 7: 373-378.
26. Aldrich CL, Stephenson MD, Karrison T, Odem RR, Branch DW, Scott JR et al. HLA-G genotypes and pregnancy outcome in couples with unexplained recurrent miscarriage. Mol Hum Reprod 2001; 7: 1167-1172.
27. Moreau P, Contu L, Alba F, Lai S, Simoes R, Orru S et al. HLA-G gene polymorphism in human placentas: possible association of G*0106 allele with preeclampsia and miscarriage. Biol Reprod 2008; 79: 459-467.
28. Berger DS, Hogge WA, Barmada MM, Ferrell RE. Comprehensive analysis of HLA-G: implications for recurrent spontaneous abortion. Reprod Sci 2010; 17: 331-338.
29. Aldrich C, Wambebe C, Odama L, Di Rienzo A, Ober C. Linkage disequilibrium and age estimates of a deletion polymorphism (1597DeltaC) in HLA-G suggest nonneutral evolution. Hum Immunol 2002; 63: 405-412.
30. Ober C, Aldrich C, Rosinsky B, Robertson A, Walker MA, Willadsen S et al. HLA-G1 protein expression is not essential for fetal survival. Placenta 1998; 19: 127-132.
31. Mendes-Junior CT, Castelli EC, Simoes RT, Simoes AL, Donadi EA. HLA-G 14-bp polymorphism at exon 8 in Amerindian populations from the Brazilian Amazon. Tissue Antigens 2007; 69: 255-260.
32. 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(4 (suppl)): 919-923.
33. Salzano FM, Callegari-Jacques SM. South American Indians: a case study in evolution. Oxford University Press: New York, 1988.
34. Atay GA, Arsan S, Atasay B, Ensari A, Aysev D. The possible role of intrauterine infections in unexplained second trimester abortions and macerated stillbirths: a study from a single center. J Perinatol 2004; 24: 679-685.
35. Petersson K, Norbeck O, Westgren M, Broliden K. Detection of parvovirus B19, cytomegalovirus and enterovirus infections in cases of intrauterine fetal death. J Perinat Med 2004; 32: 516-521.
36. Harrison GA, Humphrey KE, Jakobsen IB, Cooper DW. A 14 bp deletion polymorphism in the HLA-G gene. Hum Mol Genet 1993; 2: 2200.
37. Rousseau P, Le Discorde M, Mouillot G, Marcou C, Carosella ED, Moreau P. The 14 bp deletion-insertion polymorphism in the 30 UT region of the HLA-G gene influences HLA-G mRNA stability. Hum Immunol 2003; 64: 1005-1010.
38. Excoffier L, Slatkin M. Maximum-likelihood estimation of molecular haplotype frequencies in a diploid population. Mol Biol Evol 1995; 12: 921-927.
39. Stephens M, Smith NJ, Donnelly P. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 2001; 68: 978-989.
40. Castelli EC, Mendes-Junior CT, Donadi EA. HLA-G alleles and HLA-G 14 bp polymorphisms in a Brazilian population. Tissue Antigens 2007; 70: 62-68.
41. Neel JV, Gershowitz H, Mohrenweiser HW, Amos B, Kostyu DD, Salzano FM et al. Genetic studies on the Ticuna, an enigmatic tribe of Central Amazonas. Ann Hum Genet 1980; 44: 37-54.
42. Mendes-Junior CT, Simoes AL. Mitochondrial DNA variability among eight Tikuna villages: evidence for an intratribal genetic heterogeneity pattern. Am J Phys Anthropol 2009; 140: 526-531.
43. Salzano FM, Callegari-Jacques SM, Neel JV. Genetic demography of the Amazonian Ticuna Indians. J Hum Evol 1980; 9: 179-191.
44. Mestriner MA, Simoes AL, Salzano FM. New studies on the esterase D polymorphism in South American Indians. Am J Phys Anthropol 1980; 52: 95-101.
45. Mohrenweiser H, Neel JV, Mestriner MA, Salzano FM, Migliazza E, Simoes AL et al. Electrophoretic variants in three Amerindian tribes: the Baniwa, Kanamari, and Central Pano of western Brazil. Am J Phys Anthropol 1979; 50: 237-246.
46. Salzano FM, Jacques SM. Genetic demography of the Central Pano and Kanamari Indians of Brazil. Hum Biol 1979; 51: 551-564.
47. Salzano FM. Molecular variability in Amerindians: widespread but uneven information. An Acad Bras Cienc 2002; 74: 223-263.
48. Parham P, Arnett KL, Adams EJ, Little AM, Tees K, Barber LD et al. Episodic evolution and turnover of HLA-B in the indigenous human populations of the Americas. Tissue Antigens 1997; 50: 219-232.
49. Tsuneto LT, Probst CM, Hutz MH, Salzano FM, Rodriguez-Delfin LA, Zago MA et al. HLA class II diversity in seven Amerindian populations. Clues about the origins of the Ache. Tissue Antigens 2003; 62: 512-526.
50. Moreau P, Dausset J, Carosella ED, Rouas-Freiss N. Viewpoint on the functionality of the human leukocyte antigen-G null allele at the fetal-maternal interface. Biol Reprod 2002; 67: 1375-1378.
51. Bamshad MJ, Mummidi S, Gonzalez E, Ahuja SS, Dunn DM, Watkins WS et al. A strong signature of balancing selection in the 50 cis-regulatory region of CCR5. Proc Natl Acad Sci USA 2002; 99: 10539-10544.
52. Nei M, Kumar S. Molecular Evolution and Phylogenetics. Oxford University Press: New York, USA, 2000.
53. Harris EE, Meyer D. The molecular signature of selection underlying human adaptations. Am J Phys Anthropol 2006; Suppl 43: 89-130.
54. Stephens JC, Schneider JA, Tanguay DA, Choi J, Acharya T, Stanley SE et al. Haplotype variation and linkage disequilibrium in 313 human genes. Science 2001; 293: 489-493.
55. Simonsen KL, Churchill GA, Aquadro CF. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 1995; 141: 413-429.
56. Zhai W, Nielsen R, Slatkin M. An investigation of the statistical power of neutrality tests based on comparative and population genetic data. Mol Biol Evol 2009; 26: 273-283.
57. Ptak SE, Przeworski M. Evidence for population growth in humans is confounded by fine-scale population structure. Trends Genet 2002; 18: 559-563.
58. Fagundes NJ, Ray N, Beaumont M, Neuenschwander S, Salzano FM, Bonatto SL et al. Statistical evaluation of alternative models of human evolution. Proc Natl Acad Sci USA 2007; 104: 17614-17619.
59. Amos W, Hoffman JI. Evidence that two main bottleneck events shaped modern human genetic diversity. Proc Biol Sci 2010; 277: 131-137.
60. Flajollet S, Poras I, Carosella ED, Moreau P. RREB-1 is a transcriptional repressor of HLA-G. J Immunol 2009; 183: 6948-6959.
61. Moreau P, Flajollet S, Carosella ED. Non-classical transcriptional regulation of HLAG: an update. J Cell Mol Med 2009; 13: 2973-2989.
62. Higuchi R. Simple and rapid preparation of samples for PCR. In: Erlich HA (ed) PCR Technology: Principles and Applications for DNA Amplification. Stockton Press: New York, NY, USA, 1989, pp 31-38.
63. Hviid TV, Hylenius S, Hoegh AM, Kruse C, Christiansen OB. HLA-G polymorphisms in couples with recurrent spontaneous abortions. Tissue Antigens 2002; 60: 122-132.
64. Guo SW, Thompson EA. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 1992; 48: 361-372.
65. Rousset F. genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 2008; 8: 103-106.
66. Raymond M, Rousset F. An exact test for population differentiation. Evolution 1995; 49: 1280-1283.
67. Excoffier L, Lischer HE. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 2010; 10: 564-567.
68. Excoffier L, Slatkin M. Incorporating genotypes of relatives into a test of linkage disequilibrium. Am J Hum Genet 1998; 62: 171-180.
69. 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.
70. Ewens WJ. The sampling theory of selectively neutral alleles. Theor Popul Biol 1972; 3: 87-112.
71. Watterson GA. The homozygosity test of neutrality. Genetics 1978; 88: 405-417.
72. Slatkin M. An exact test for neutrality based on the Ewens sampling distribution. Genet Res 1994; 64: 71-74.
73. Lancaster A, Nelson MP, Meyer D, Thomson G, Single RM. PyPop: a software framework for population genomics: analyzing large-scale multi-locus genotype data. Pac Symp Biocomput 2003; 8: 514-525.
74. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989; 123: 585-595.
75. Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986; 3: 418-426.
76. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28: 2731-2739.
77. McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 1991; 351: 652-654.
78. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009; 25: 1451-1452.