Loss and Gain of Natural Killer Cell Receptor Function in an African Hunter-Gatherer Population

PLoS Genetics

Volumn 11, Issue 8, 2015, Pages

  Hilton, Hugo G ^a   Norman, Paul J ^a   Nemat Gorgani, Neda ^a   Goyos, Ana ^a   Hollenbach, Jill A ^b   Henn, Brenna M ^c   Gignoux, Christopher R ^a   Guethlein, Lisbeth A ^a   Parham, Peter ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HLA B ANTIGEN; HLA C ANTIGEN; HLA C1 ANTIGEN; HLA C2 ANTIGEN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL2; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL3; NATURAL KILLER CELL RECEPTOR; UNCLASSIFIED DRUG; KIR2DL1 PROTEIN, HUMAN;

ALLELE; ALLOTYPE; ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; CELL SURFACE; CONTROLLED STUDY; DNA POLYMORPHISM; GAIN OF FUNCTION MUTATION; GENE FREQUENCY; GENE FUNCTION; GENE INTERACTION; GENE LINKAGE DISEQUILIBRIUM; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; HUNTER GATHERER; INDIGENOUS PEOPLE; KHOISAN; KIR2DL1 GENE; LOSS OF FUNCTION MUTATION; NATURAL KILLER CELL; POINT MUTATION; PROTEIN FUNCTION; RECEPTOR BINDING; SOUTH AFRICAN; ZULU (PEOPLE); GENETIC ASSOCIATION STUDY; GENETIC POLYMORPHISM; GENETICS; HELA CELL LINE; IMMUNOLOGY; MEDICAL GENETICS; METABOLISM; MOLECULAR EVOLUTION; SIGNAL TRANSDUCTION; SOUTH AFRICA;

ALLELES; EVOLUTION, MOLECULAR; GENETIC ASSOCIATION STUDIES; GENETICS, MEDICAL; HAPLOTYPES; HELA CELLS; HUMANS; KILLER CELLS, NATURAL; LINKAGE DISEQUILIBRIUM; POLYMORPHISM, GENETIC; RECEPTORS, KIR2DL1; SIGNAL TRANSDUCTION; SOUTH AFRICA;

EID: 84939525443     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005439     Document Type: Article

References (57)

1. Parham P, Moffett A, (2013) Variable NK cell receptors and their MHC class I ligands in immunity, reproduction and human evolution. Nat Rev Immunol 13: 133–144. doi: 10.1038/nri3370 23334245
2. Cooper MA, Colonna M, Yokoyama WM, (2009) Hidden talents of natural killers: NK cells in innate and adaptive immunity. EMBO Rep 10: 1103–1110. doi: 10.1038/embor.2009.203 19730434
3. Bashirova AA, Martin MP, McVicar DW, Carrington M, (2006) The killer immunoglobulin-like receptor gene cluster: tuning the genome for defense. Annu Rev Genomics Hum Genet 7: 277–300. 16824023
4. Parham P, Norman PJ, Abi-Rached L, Guethlein LA, (2012) Human-specific evolution of killer cell immunoglobulin-like receptor recognition of major histocompatibility complex class I molecules. Philos Trans R Soc Lond B Biol Sci 367: 800–811. doi: 10.1098/rstb.2011.0266 22312047
5. Boyington JC, Motyka SA, Schuck P, Brooks AG, Sun PD, (2000) Crystal structure of an NK cell immunoglobulin-like receptor in complex with its class I MHC ligand. Nature 405: 537–543. 10850706
6. Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, et al. (1987) The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329: 512–518. 2443855
7. Winter CC, Long EO, (1997) A single amino acid in the p58 killer cell inhibitory receptor controls the ability of natural killer cells to discriminate between the two groups of HLA-C allotypes. J Immunol 158: 4026–4028. 9126959
8. Uhrberg M, Valiante NM, Shum BP, Shilling HG, Lienert-Weidenbach K, et al. (1997) Human diversity in killer cell inhibitory receptor genes. Immunity 7: 753–763. 9430221
9. Abi-Rached L, Moesta AK, Rajalingam R, Guethlein LA, Parham P, (2010) Human-specific evolution and adaptation led to major qualitative differences in the variable receptors of human and chimpanzee natural killer cells. PLoS Genet 6: e1001192. doi: 10.1371/journal.pgen.1001192 21079681
10. Henn BM, Gignoux CR, Jobin M, Granka JM, Macpherson JM, et al. (2011) Hunter-gatherer genomic diversity suggests a southern African origin for modern humans. Proc Natl Acad Sci U S A 108: 5154–5162. doi: 10.1073/pnas.1017511108 21383195
11. Petersen DC, Libiger O, Tindall EA, Hardie RA, Hannick LI, et al. (2013) Complex patterns of genomic admixture within southern Africa. PLoS Genet 9: e1003309. doi: 10.1371/journal.pgen.1003309 23516368
12. Tishkoff SA, Reed FA, Friedlaender FR, Ehret C, Ranciaro A, et al. (2009) The genetic structure and history of Africans and African Americans. Science 324: 1035–1044. doi: 10.1126/science.1172257 19407144
13. Nakimuli A, Chazara O, Byamugisha J, Elliott AM, Kaleebu P, et al. (2014) Pregnancy, parturition and preeclampsia in women of African ancestry. Am J Obstet Gynecol 210: 510–520 e511. doi: 10.1016/j.ajog.2013.10.879 24184340
14. Norman PJ, Hollenbach JA, Nemat-Gorgani N, Guethlein LA, Hilton HG, et al. (2013) Co-evolution of human leukocyte antigen (HLA) class I ligands with killer-cell immunoglobulin-like receptors (KIR) in a genetically diverse population of sub-Saharan Africans. PLoS Genet 9: e1003938. doi: 10.1371/journal.pgen.1003938 24204327
15. Bryc K, Auton A, Nelson MR, Oksenberg JR, Hauser SL, et al. (2010) Genome-wide patterns of population structure and admixture in West Africans and African Americans. Proc Natl Acad Sci U S A 107: 786–791. doi: 10.1073/pnas.0909559107 20080753
16. Schuster SC, Miller W, Ratan A, Tomsho LP, Giardine B, et al. (2010) Complete Khoisan and Bantu genomes from southern Africa. Nature 463: 943–947. doi: 10.1038/nature08795 20164927
17. Lachance J, Vernot B, Elbers CC, Ferwerda B, Froment A, et al. (2012) Evolutionary history and adaptation from high-coverage whole-genome sequences of diverse African hunter-gatherers. Cell 150: 457–469. doi: 10.1016/j.cell.2012.07.009 22840920
18. Chimusa ER, Meintjies A, Tchanga M, Mulder N, Seioghe C, et al. (2015) A genomic portrait of haplotype diversity and signatures of selection in indigenous southern African populations. PLoS Genet 11: e1005052. doi: 10.1371/journal.pgen.1005052 25811879
19. Howell N, (2007) Demography of the Dobe! Kung. New Brunswick, N.J.: AldineTransaction.
20. Gendzekhadze K, Norman PJ, Abi-Rached L, Graef T, Moesta AK, et al. (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 U S A 106: 18692–18697. doi: 10.1073/pnas.0906051106 19837691
21. Middleton D, Meenagh A, Gourraud PA, (2007) KIR haplotype content at the allele level in 77 Northern Irish families. Immunogenetics 59: 145–158. 17200871
22. Nemat-Gorgani N, Edinur HA, Hollenbach JA, Traherne JA, Dunn PP, et al. (2014) KIR diversity in Maori and Polynesians: populations in which HLA-B is not a significant KIR ligand. Immunogenetics 66: 597–611. doi: 10.1007/s00251-014-0794-1 25139336
23. Vierra-Green C, Roe D, Hou L, Hurley CK, Rajalingam R, et al. (2012) Allele-level haplotype frequencies and pairwise linkage disequilibrium for 14 KIR loci in 506 European-American individuals. PLoS One 7: e47491. doi: 10.1371/journal.pone.0047491 23139747
24. Yawata M, Yawata N, Draghi M, Little AM, Partheniou F, et al. (2006) Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function. J Exp Med 203: 633–645. 16533882
25. Abecasis GR, Auton A, Brooks LD, DePristo MA, Durbin RM, et al. (2012) An integrated map of genetic variation from 1,092 human genomes. Nature 491: 56–65. doi: 10.1038/nature11632 23128226
26. Kidd JM, Sharpton TJ, Bobo D, Norman PJ, Martin AR, et al. (2014) Exome capture from saliva produces high quality genomic and metagenomic data. BMC Genomics 15: 262. doi: 10.1186/1471-2164-15-262 24708091
27. Gurdasani D, Carstensen T, Tekola-Ayele F, Pagani L, Tachmazidou I, et al. (2015) The African Genome Variation Project shapes medical genetics in Africa. Nature 517: 327–332. doi: 10.1038/nature13997 25470054
28. Gronau I, Hubisz MJ, Gulko B, Danko CG, Siepel A, (2011) Bayesian inference of ancient human demography from individual genome sequences. Nat Genet 43: 1031–1034. doi: 10.1038/ng.937 21926973
29. Schlebusch CM, Skoglund P, Sjodin P, Gattepaille LM, Hernandez D, et al. (2012) Genomic variation in seven Khoe-San groups reveals adaptation and complex African history. Science 338: 374–379. doi: 10.1126/science.1227721 22997136
30. Burshtyn DN, Scharenberg AM, Wagtmann N, Rajagopalan S, Berrada K, et al. (1996) Recruitment of tyrosine phosphatase HCP by the killer cell inhibitor receptor. Immunity 4: 77–85. 8574854
31. Moesta AK, Norman PJ, Yawata M, Yawata N, Gleimer M, et al. (2008) Synergistic polymorphism at two positions distal to the ligand-binding site makes KIR2DL2 a stronger receptor for HLA-C than KIR2DL3. J Immunol 180: 3969–3979. 18322206
32. Hilton HG, Vago L, Older Aguilar AM, Moesta AK, Graef T, et al. (2012) Mutation at positively selected positions in the binding site for HLA-C shows that KIR2DL1 is a more refined but less adaptable NK cell receptor than KIR2DL3. J Immunol 189: 1418–1430. doi: 10.4049/jimmunol.1100431 22772445
33. Abi-Rached L, Jobin MJ, Kulkarni S, McWhinnie A, Dalva K, et al. (2011) The shaping of modern human immune systems by multiregional admixture with archaic humans. Science 334: 89–94. doi: 10.1126/science.1209202 21868630
34. Gonzalez-Galarza FF, Christmas S, Middleton D, Jones AR, (2011) Allele frequency net: a database and online repository for immune gene frequencies in worldwide populations. Nucleic Acids Res 39: D913–919. doi: 10.1093/nar/gkq1128 21062830
35. VandenBussche CJ, Mulrooney TJ, Frazier WR, Dakshanamurthy S, Hurley CK, (2009) Dramatically reduced surface expression of NK cell receptor KIR2DS3 is attributed to multiple residues throughout the molecule. Genes Immun 10: 162–173. doi: 10.1038/gene.2008.91 19005473
36. Pando MJ, Gardiner CM, Gleimer M, McQueen KL, Parham P, (2003) The protein made from a common allele of KIR3DL1 (3DL1*004) is poorly expressed at cell surfaces due to substitution at positions 86 in Ig domain 0 and 182 in Ig domain 1. J Immunol 171: 6640–6649. 14662867
37. Thomas R, Yamada E, Alter G, Martin MP, Bashirova AA, et al. (2008) Novel KIR3DL1 alleles and their expression levels on NK cells: convergent evolution of KIR3DL1 phenotype variation? J Immunol 180: 6743–6750. 18453594
38. Bari R, Bell T, Leung WH, Vong QP, Chan WK, et al. (2009) Significant functional heterogeneity among KIR2DL1 alleles and a pivotal role of arginine 245. Blood 114: 5182–5190. doi: 10.1182/blood-2009-07-231977 19828694
39. Klitz W, Thomson G, (1987) Disequilibrium pattern analysis. II. Application to Danish HLA A and B locus data. Genetics 116: 633–643. 3476350
40. Frazier WR, Steiner N, Hou L, Dakshanamurthy S, Hurley CK, (2013) Allelic Variation in KIR2DL3 Generates a KIR2DL2-like Receptor with Increased Binding to its HLA-C Ligand. J Immunol.
41. Hiby SE, Walker JJ, O'Shaughnessy K M, Redman CW, Carrington M, et al. (2004) Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J Exp Med 200: 957–965. 15477349
42. Nakimuli A, Chazara O, Hiby SE, Farrell L, Tukwasibwe S, et al. (2015) A KIR B centromeric region present in Africans but not Europeans protects pregnant women from pre-eclampsia. Proc Natl Acad Sci U S A 112: 845–850. doi: 10.1073/pnas.1413453112 25561558
43. Kim HL, Ratan A, Perry GH, Montenegro A, Miller W, et al. (2014) Khoisan hunter-gatherers have been the largest population throughout most of modern-human demographic history. Nat Commun 5: 5692. doi: 10.1038/ncomms6692 25471224
44. Oppenheimer S, (2012) Out-of-Africa, the peopling of continents and islands: tracing uniparental gene trees across the map. Philos Trans R Soc Lond B Biol Sci 367: 770–784. doi: 10.1098/rstb.2011.0306 22312044
45. Hollenbach JA, Nocedal I, Ladner MB, Single RM, Trachtenberg EA, (2012) Killer cell immunoglobulin-like receptor (KIR) gene content variation in the HGDP-CEPH populations. Immunogenetics 64: 719–737. doi: 10.1007/s00251-012-0629-x 22752190
46. Norman PJ, Abi-Rached L, Gendzekhadze K, Korbel D, Gleimer M, et al. (2007) Unusual selection on the KIR3DL1/S1 natural killer cell receptor in Africans. Nat Genet 39: 1092–1099. 17694054
47. Robinson J, Halliwell JA, McWilliam H, Lopez R, Marsh SG, (2013) IPD—the Immuno Polymorphism Database. Nucleic Acids Res 41: D1234–1240. doi: 10.1093/nar/gks1140 23180793
48. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943
49. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25. doi: 10.1186/gb-2009-10-3-r25 19261174
50. Hilton HG, Moesta AK, Guethlein LA, Blokhuis J, Parham P, et al. (2015) The production of KIR-Fc fusion proteins and their use in a multiplex HLA class I binding assay. Journal of Immunological Methods doi: 10.1016/j.jim.2015.06.012
51. Shilling HG, Guethlein LA, Cheng NW, Gardiner CM, Rodriguez R, et al. (2002) Allelic polymorphism synergizes with variable gene content to individualize human KIR genotype. J Immunol 168: 2307–2315. 11859120
52. Wilson MJ, Torkar M, Haude A, Milne S, Jones T, et al. (2000) Plasticity in the organization and sequences of human KIR/ILT gene families. Proc Natl Acad Sci U S A 97: 4778–4783. 10781084
53. Norman PJ, Cook MA, Carey BS, Carrington CV, Verity DH, et al. (2004) SNP haplotypes and allele frequencies show evidence for disruptive and balancing selection in the human leukocyte receptor complex. Immunogenetics 56: 225–237. 15185041
54. Hancock AM, Rienzo AD, (2008) Detecting the Genetic Signature of Natural Selection in Human Populations: Models, Methods, and Data. Annu Rev Anthropol 37: 197–217. 20622977
55. Nielsen R, (2005) Molecular signatures of natural selection. Annu Rev Genet 39: 197–218. 16285858
56. Oleksyk TK, Smith MW, O'Brien SJ, (2010) Genome-wide scans for footprints of natural selection. Philos Trans R Soc Lond B Biol Sci 365: 185–205. doi: 10.1098/rstb.2009.0219 20008396
57. Thomson G, Klitz W, (1987) Disequilibrium pattern analysis. I. Theory. Genetics 116: 623–632. 3623083