Signatures of historical demography and pathogen richness on MHC class i genes

Immunogenetics

Volumn 64, Issue 3, 2012, Pages 165-175

  Qutob, Nouar ^a   Balloux, Francois ^b   Raj, Towfique ^c,d   Liu, Hua ^a   Marion De Procé, Sophie ^e   Trowsdale, John ^a   Manica, Andrea ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Dempography; MHC; MHC diversity; Natural selection; Pathogen richness

Indexed keywords

HLA A ANTIGEN; HLA B ANTIGEN; HLA C ANTIGEN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

AFRICA SOUTH OF THE SAHARA; ALLOTYPE; ARTICLE; BACTERIUM; DEMOGRAPHY; GENE FREQUENCY; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HETEROZYGOSITY; HISTOCOMPATIBILITY GENE; HUMAN; MICROORGANISM; MOLECULAR EVOLUTION; PATHOGEN RICHNESS; PRIORITY JOURNAL; SPECIES RICHNESS; VIRUS;

ALLELES; DATABASES, GENETIC; DEMOGRAPHY; EVOLUTION, MOLECULAR; GENE FREQUENCY; GENES, MHC CLASS I; GENETIC VARIATION; GENETICS, POPULATION; HLA-B ANTIGENS; HLA-C ANTIGENS; HOST-PATHOGEN INTERACTIONS; HUMANS; REGRESSION ANALYSIS; SELECTION, GENETIC;

EID: 84857357877     PISSN: 00937711     EISSN: 14321211     Source Type: Journal    
DOI: 10.1007/s00251-011-0576-y     Document Type: Article

References (70)

1. M Alcaide SV Edwards JJ Negro D Serrano JL Tella 2008 Extensive polymorphism and geographical variation at a positively selected MHC class II B gene of the lesser kestrel (Falco naumanni) Mol Ecol 17 2652 2665 18489548 10.1111/j.1365-294X.2008.03791.x 1:CAS:528:DC%2BD1cXotlCksLg%3D
2. M Alcaide JA Lemus G Blanco JL Tella D Serrano JJ Negro A Rodríguez M García-Montijano 2010 MHC diversity and differential exposure to pathogens in kestrels (Aves: Falconidae) Mol Ecol 19 691 705 20074317 10.1111/j.1365-294X.2009.04507.x 1:CAS:528:DC%2BC3cXjsFekur0%3D
3. FW Allendorf 1986 Genetic drift and the loss of alleles versus heterozygosity Zoo Biology 5 181 190 10.1002/zoo.1430050212
4. N Anfossi P Andre S Guia CS Falk S Roetnynck CA Stewart V Breso C Frassati D Reviron D Middleton F Romagne S Ugolini E Vivier 2006 Human NK cell education by inhibitory receptors for MHC class I Immunity 25 331 342 16901727 10.1016/j.immuni.2006.06.013 1:CAS:528:DC%2BD28XpvVGjsrc%3D
5. V Apanius D Penn PR Slev LR Ruff WK Potts 1997 The nature of selection on the major histocompatibility complex Crit Rev Immunol 17 179 224 9094452 1:CAS:528:DyaK2sXivVaqtr8%3D
6. Appanna R, Ponnampalavanar S, Lum Chai See L, Sekaran S (2010) Susceptible and protective HLA class 1 alleles against dengue fever and dengue hemorrhagic fever patients in a Malaysian population. 5(9):e13029
7. J Arnaiz-Villena JI Moscoso J Serrano-Vela Martinez-Laso 2006 The uniqueness of Amerindians according to HLA genes and the peopling of the Americas Inmunología 25 13 24
8. L Betti F Balloux W Amos T Hanihara A Manica 2009 Distance from Africa, not climate, explains within-population phenotypic diversity in humans Proc Roy Soc B 276 809 814 10.1098/rspb.2008.1563
9. JG Bodmer SGE Marsh P Parham HA Erlich E Albert WF Bodmer B Dupont B Mach WR Mayr T Sasazuki GMT Schreuder JL Strominger A Svejgaard PI Terasaki 1990 Nomenclature for factors of the HLA system Tissue Antigens 35 1 8 2305394 10.1111/j.1399-0039.1990.tb01749.x 1:STN:280:DyaK3c7mt1Kltw%3D%3D
10. RJ Boyton DM Altmann 2007 Natural killer cells, killer immunoglobulin-like receptors and human leukocyte antigen class I in disease Clin Exp Immunol 149 1 8 17521317 10.1111/j.1365-2249.2007.03424.x 1:CAS:528:DC%2BD2sXovFKksbw%3D
11. M Carrington MP Martin 2006 The impact of variation at the KIR gene cluster on human disease Curr Top Microbiol Immunol 298 225 257 16329188 10.1007/3-540-27743-9-12 1:CAS:528:DC%2BD28XhtFyrs7Y%3D
12. M Carrington GW Nelson MP Martin T Kissner D Vlahov JJ Goedert R Kaslow S Buchbinder K Hoots J O'Brian 1999 HLA and HIV I: heterozygote advantage and B*35-Cw*04 disadvantage Science 283 5408 1748 1752 10073943 10.1126/science.283.5408.1748 1:CAS:528:DyaK1MXhvFSnu7s%3D
13. M Cella A Longo GB Ferrara JL Strominger M Colonna 1994 NK3-specific natural killer cells are selectively inhibited by Bw4-positive HLA alleles with isoleucine 80 J Exp Med 180 1235 1242 7931060 10.1084/jem.180.4.1235 1:CAS:528:DyaK2cXlslOltb4%3D
14. V Coetzee L Barrett JM Greeff SP Henzi DI Perrett I David AA Wadee 2007 Common HLA alleles associated with health, but not with facial attractivenss PLoS One 2 e640 17653267 10.1371/journal.pone.0000640
15. PC Doherty RM Zinkernagel 1975 Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex Nature 256 50 52 1079575 10.1038/256050a0 1:STN:280:DyaE2M7nsFarug%3D%3D
16. S Duhamel S Jacquet 2005 Flow cytometric analysis of bacteria- and virus-like particles in lake sediments J Microbiol Meth 64 3 316 323 10.1016/j.mimet.2005.05.008
17. QR Fan DC Wiley 1999 Structure of human histocompatibility leukocyte antigen (HLA)-Cw4, a ligand for the KIR2D natural killer cell inhibitory receptor J Exp Med 190 113 10429675 10.1084/jem.190.1.113 1:CAS:528: DyaK1MXksVeiu7w%3D
18. X Gao TR O'Brien TM Welzel D Marti Y Qi JJ Goedert J Phair R Pfeiffer M Carrington 2010 HLA-B alleles associate consistently with HIV heterosexual transmission, viral load, and progression to AIDS, but not susceptibility to infection AIDS 24 12 1835 1840 20588164 10.1097/QAD.0b013e32833c3219 1:CAS:528:DC%2BC3cXos1Wqtrs%3D
19. K Gendzekhadze PJ Norman L Abi-Rached T Graef AK Moesta Z Layrisse P Parham 2001 Co-evolution of KIR2DL3 with HLA-C in a human population retaining minimal essential diversity of KIR and HLA class I ligands Proc Nati Acad Sci USA 106 44 18692 18697 10.1073/pnas.0906051106
20. K Gendzekhadze PJ Norman L Abi-Rached T Graef AK Moesta Z Layrisse P Parham 2009 Co-evolution of KIR2DL3 with HLA-C in a human population retaining minimal essential diversity of KIR and HLA class I ligands Proc Natl Acad Sci USA 106 18692 18697 19837691 10.1073/pnas.0906051106 1:CAS:528: DC%2BD1MXhsVKms7jK
21. V Godot S Harraga I Beurton M Deschaseaux E Sarciron B Gottstein DA Vuitton 2000 Resistance/susceptibility to Echinococcus multilocularis infection and cytokine profile in humans. I. Comparison of patients with progressive and abortive lesions Clin Exp Immunol 121 484 490 10971515 10.1046/j.1365-2249.2000. 01308.x 1:CAS:528:DC%2BD3cXmslSgsbc%3D
22. T Graef AK Moesta PJ Norman L Abi-Rached L Vago AM Older Aguilar M Gleimer JA Hammond LA Guethlein DA Bushnell PJ Robinson P Parham 2009 KIR2DS4 is a product of gene conversion with KIR3DL2 that introduced specificity for HLA-A*11 while diminishing avidity for HLA-C J Exp Med 206 11 2557 2572 19858347 10.1084/jem.20091010 1:CAS:528:DC%2BD1MXhtlCltrbJ
23. V Guernier ME Hochberg JF Guégan 2004 Ecology drives the worldwide distribution of human diseases PLoS Biol 2 740 746 10.1371/journal.pbio.0020141 1:CAS:528:DC%2BD2cXltVCksrs%3D
24. E Guivier M Galan P Male E Kallio L Voutilainen H Henttonen G Olsson A Lundkvist K Tersago D Augot J Cosson N Charbonnel 2010 Associations between MHC genes and Puumala virus infection in Myodes glareolus are detected in wild populations, but not from experimental infection data J Gen Virol 91 10 2507 2512 2510.1099/vir.2500.021600-021600 20573856 10.1099/vir.0.021600-0 1:CAS:528:DC%2BC3cXht12qs7rL
25. P Hansasuta T Dong H Thananchai M Weekes C Willberg H Aldemir S Rowland-Jones VM Braud 2004 Recognition of HLA-A3 and HLA-A11 by KIR3DL2 is peptide-specific Mol Immunol 34 1673 1679 1:CAS:528:DC%2BD2cXltFKru7k%3D
26. SE Hiby JJ Walker KM O'shaughnessy CWG Redman M Carrington J Trowsdale A Moffett 2004 Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success J Exp Med 200 8 957 965 15477349 10.1084/jem.20041214 1:CAS:528:DC%2BD2cXovVensL0%3D
27. SE Hiby R Apps AM Sharkey LE Farrell L Gardner A Mulder FH Claas JJ Walker CW Redman L Morgan C Tower L Regan GE Moore M Carrington A Moffett 2010 Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2 J Clin Invest 120 11 4102 4010 20972337 10.1172/JCI43998 1:CAS:528:DC%2BC3cXhsVWgtbjF
28. AV Hill CEM Allsopp DK Kwiatkowski NM Anstey P Twumasi PA Rowe S Bennett D Brewster AJ McMichael BM Greenwood 1991 Common west African HLA antigens are associated with protection from severe malaria Nature 352 595 600 1865923 10.1038/352595a0 1:STN:280:DyaK3Mzis1Sqtw%3D%3D
29. P Hoglund P Brodin 2009 Current perspectives of natural killer cell education by MHC class I molecules Nat Rev Immunol 10 724 734 10.1038/nri2835
30. DT Jones WR Taylor JM Thornton 1992 The rapid generation of mutation data matrices from protein sequences Comput Appl Biosci 8 275 282 1633570 1:CAS:528:DyaK38Xlt1Okt7w%3D
31. SI Khakoo M Carrington 2006 KIR and disease: a model system or system of models Immunol Rev 214 186 201 17100885 10.1111/j.1600-065X.2006.00459.x 1:CAS:528:DC%2BD28XhtlClsrzM
32. KK Kidd AJ Pakstis WC Speed JR Kidd 2004 Understanding human DNA sequence variation J Hered 95 5 406 420 15388768 10.1093/jhered/esh060 1:CAS:528:DC%2BD2cXnvVOmsb4%3D
33. RN Koehler AM Walsh E Saathoff S Tovanabutra MA Arroyo JR Currier L Maboko M Hoelsher ML Robb NL Michael F McCutchan J Kim G Kijak 2010 Class I HLA-A*7401 is associated with protection from HIV-1 acquisition and disease progression in Mbeya, Tanzania J Infect Dis 202 1562 1566 20923372 10.1086/656913 1:CAS:528:DC%2BC3cXhsFOns73L
34. S Kulkarni R Savan Y Qi X Gao Y Yuki SE Bass MP Martin P Hunt SG Deeks A Telenti F Pereyra D Goldstein S Wolinsky B Walker HA Young M Carrington 2011 Differential microRNA regulation of HLA-C expression and its association with HIV control Nature 472 7344 495 498 21499264 10.1038/nature09914 1:CAS:528:DC%2BC3MXkslCmurY%3D
35. Lechler R (1994) HLA and diseases. Academic press limited, London, pp 1-186
36. H Liu F Prugnolle A Manica F Balloux 2006 A geography explicit genetic model of worldwide human-settelment history Am J Hum Genet 79 230 237 16826514 10.1086/505436 1:CAS:528:DC%2BD28XnsVOksbc%3D
37. O Mandelboim HT Reyburn EG Sheu M Vales-Gomez DM Davis L Pazmany JL Strominger 1997 The binding site of NK receptors on HLA-C molecules Immunity 6 3 341 350 9075934 10.1016/S1074-7613(00)80336-2 1:CAS:528:DyaK2sXit1Wlu7Y%3D
38. A Manica F Prugnolle F Balloux 2005 Geography is a better determinant of human genetic differentiation than ethnicity Hum Genet 118 366 371 16189711 10.1007/s00439-005-0039-3
39. A Manica W Amos F Balloux T Hanihara 2007 The effect of ancient bottenecks on human phenotype variation Nature 448 346 348 17637668 10.1038/nature05951 1:CAS:528:DC%2BD2sXnvVeqsb0%3D
40. SN McAdam JE Boyson X Liu TL Garber AL Hughes RE Bontrop DI Watkins 1994 A uniquely high level of recombination at the HLA-B locus Proc Natl Acad Sci USA 91 5893 5897 8016085 10.1073/pnas.91.13.5893 1:CAS:528:DyaK2cXlt1Krs7w%3D
41. EE McClelland DJ Penn WK Potts 2003 Major histocompatibility complex heterozygote superiority during coinfection Infect Immun 71 4 2079 2086 12654829 10.1128/IAI.71.4.2079-2086.2003 1:CAS:528:DC%2BD3sXislOhtrg%3D
42. Meyer D, Mack SJ (2006) Major histocompatibility complex (MHC) genes: polymorphism. Encyclopedia of Life Sciences
43. D Meyer G Thomson 2001 How selection shapes variation of the human major histocompatibility complex: a review Ann Hum Genet 65 1 26 11415519 10.1046/j.1469-1809.2001.6510001.x 1:CAS:528:DC%2BD3MXkt1Srtbc%3D
44. M Nei 1978 Estimation of average heterozygosity and genetic distance from a small number of individuals Genetics 89 583 590 17248844 1:STN:280: DC%2BC3crpt1Kqtg%3D%3D
45. P Parham 2005 MHC I molecules and KIRs in human history, healthy and survival Nat Rev Immunol 5 201 214 15719024 10.1038/nri1570 1:CAS:528: DC%2BD2MXhslSju78%3D
46. P Parham LA Guethlein 2010 Pregnancy immunogenetics: NK cell education in the womb? J Clin Invest 1 120 3801 3804 10.1172/JCI44559
47. S Paterson K Wilson JM Pemberton 1998 Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population Proc Natl Acad Sci USA 95 3714 3719 9520432 10.1073/pnas.95.7.3714 1:CAS:528:DyaK1cXitlKjt74%3D
48. DJ Penn K Damjanovich WK Potts 2002 MHC heterozygosity confers a selective advantage against multiple-strain infections Proc Nati Acad Sci USA 99 11260 11264 10.1073/pnas.162006499 1:CAS:528:DC%2BD38XmslSmtbw%3D
49. SB Piertney MK Oliver 2006 The evolutionary ecology of the major histocompatibility complex Heredity 96 7 21 16094301 1:CAS:528: DC%2BD28XjsFOrsLY%3D
50. F Prugnolle A Manica F Balloux 2005 Geography predicts neutral genetic diversity of human populations Curr Biol 15 R159 R160 15753023 10.1016/j.cub.2005.02.038 1:CAS:528:DC%2BD2MXitVCntrw%3D
51. F Prugnolle A Manica M Charpentier J Guegan F Balloux 2005 Pathogen-driven selection and worldwide HLA class 1 diversity Curr Biol 15 1022 1027 15936272 10.1016/j.cub.2005.04.050 1:CAS:528:DC%2BD2MXltVOms7Y%3D
52. R Development Core Team (2005) R: A language and environment for statistical computing. R Foundation for Statistical Computing.
53. S Rajagopalan EO Long 2005 Understanding how combinations of HLA and KIR genes influence disease J Exp Med 201 7 1025 1029 15809348 10.1084/jem.20050499 1:CAS:528:DC%2BD2MXjtFWlsr0%3D
54. R Rajalingam P Krausa HG Shilling JB Stein A Balamurugan MD McGinnis NW Cheng NK Mehra P Parham 2002 Distinctive KIR and HLA diversity in a panel of North Indian Hindus Immunogenetics 53 1009 1019 11904677 10.1007/s00251-001- 0425-5 1:CAS:528:DC%2BD38XhvVCnu7s%3D
55. S Ramachandran O Deshpande CC Roseman NA Rosenberg MW Feldman LL Cavalli-Sforza 2005 Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa Proc Natl Acad Sci USA 102 15942 15947 16243969 10.1073/pnas.0507611102 1:CAS:528:DC%2BD2MXht1Wru7fL
56. J Robinson MJ Waller P Parham N de Groot R Bontrop LJ Kennedy P Stoehr SG Marsh 2003 IMGT/HLA and IMGT/MHC: sequence databases for the study of the major histocompatibility complex Nucleic Acids Res 31 311 314 12520010 10.1093/nar/gkg070 1:CAS:528:DC%2BD3sXhvFSmsb0%3D
57. IG Romero A Manica J Goudet LL Handley F Balloux 2009 How accurate is the current picture of human genetic variation? Heredity 102 120 126 18766200 10.1038/hdy.2008.89 1:CAS:528:DC%2BD1MXotVChtQ%3D%3D
58. MJ Simmonds JM Howson JM Heward J Carr-Smith JA Franklyn JA Todd SC Gough 2007 A novel and major association of HLA-C in Graves' disease that eclipses the classical HLA-DRB1 effect Hum Mol Genet 16 18 2149 2153 17597093 10.1093/hmg/ddm165 1:CAS:528:DC%2BD2sXpvVaitrY%3D
59. RM Single MP Martin X Ga D Meyer M Yeager JR Kidd KK Kidd M Carrington 2007 Global diversity and evidence for coevolution of KIR and HLA Nat Genet 39 9 1114 1119 17694058 10.1038/ng2077 1:CAS:528:DC%2BD2sXps12gtLw%3D
60. S Sommer 2005 The importance of immune gene variability in evolutionary ecology and evolution Frontiers in Zoology 2 16 16242022 10.1186/1742-9994-2-16
61. JO Stephen X Gao M Carrington 2001 HLA and AIDS: a cautionary tale Trends Mol Med 7 9 379 381 10.1016/S1471-4914(01)02131-1
62. M Stern L Ruggeri M Capanni A Mancusi A Velardi 2008 Human leukocyte antigens A23, A24, and A32 but not A25 are ligands for KIR3DL1 Blood 112 3 708 710 18502829 10.1182/blood-2008-02-137521 1:CAS:528:DC%2BD1cXpsVaisrw%3D
63. K Tamura J Dudley M Nei S Kumar 2007 MEGA4: molecular evolutionary genetics analysis, version 4.0 Mol Biol Evol 24 8 1596 1599 17488738 10.1093/molbev/msm092 1:CAS:528:DC%2BD2sXpsVGrsL8%3D
64. H Thananchai G Gillespie MP Martin A Bashirova N Yawata M Yawata P Easterbrook DW McVicar K Maenaka P Parham M Carrington T Dong S Rowland-Jones 2007 Cutting edge: allele specific and peptide-dependent interactions between KIR3DL1 and HLA-A and HLA-B J Immunol 178 33 37 17182537 1:CAS:528: DC%2BD2sXnslyh
65. R Thomas R Apps Y Qi X Gao V Male C O'hUigin G O'Connor D Ge J Fellay JN Martin J Margolick JJ Goedert S Buchbinder GD Kirk MP Martin A Telenti SG Deeks BD Walker D Goldstein DW McVicar A Moffett M Carrington 2009 HLA-C cell surface expression and control of HIV/AIDS correlate with a variant upstream of HLA-C Nat Genet 41 12 1290 1294 19935663 10.1038/ng.486 1:CAS:528:DC%2BD1MXhsVGlurvL
66. MR Thursz D Kwiatkowski CEM Allsopp BM Greenwood HC Thomas AVS Hill 1995 Association between an MHC class II allele and clearance of hepatitis B virus in the Gambia N Engl J Med 332 1065 1069 7898524 10.1056/NEJM199504203321604 1:STN:280:DyaK2M3gs1egsQ%3D%3D
67. MR Thursz HC Thomas BM Greenwood AV Hill 1997 Heterozygote advantage for HLA-class II type in hepatitis B virus infection Nat Genet 17 1 11 12 9288086 10.1038/ng0997-11 1:CAS:528:DyaK2sXlvVCktbk%3D
68. E Trachtenberg B Korber C Sollars TB Kepler PT Hraber E Hayes R Funkhouser M Fugate J Theiler YS Hsu K Kunstman S Wu J Phair H Erlich S Wolinsky 2003 Advantage of rare HLA supertype in HIV disease progression Nat Med 9 928 935 12819779 10.1038/nm893 1:CAS:528:DC%2BD3sXkvFOjsb0%3D
69. AP Williams AR Bateman SI Khakoo 2005 Hanging in the balance: KIR and their role in disease Mol Interv 5 226 240 16123537 10.1124/mi.5.4.6 1:CAS:528:DC%2BD2MXhtVGntrfE
70. Z Yang 1996 Among-site variation and its impact of phylogenetic analysis Trends Ecol Evol 11 367 372 21237881 10.1016/0169-5347(96)10041-0 1:STN:280:DC%2BC3M7itFGjtw%3D%3D