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Immunogenetics

, Volume 69, Issue 5, pp 325–339 | Cite as

Improved full-length killer cell immunoglobulin-like receptor transcript discovery in Mauritian cynomolgus macaques

  • Trent M. Prall
  • Michael E. Graham
  • Julie A. Karl
  • Roger W. Wiseman
  • Adam J. Ericsen
  • Muthuswamy Raveendran
  • R. Alan Harris
  • Donna M. Muzny
  • Richard A. Gibbs
  • Jeffrey Rogers
  • David H. O’ConnorEmail author
Original Article

Abstract

Killer cell immunoglobulin-like receptors (KIRs) modulate disease progression of pathogens including HIV, malaria, and hepatitis C. Cynomolgus and rhesus macaques are widely used as nonhuman primate models to study human pathogens, and so, considerable effort has been put into characterizing their KIR genetics. However, previous studies have relied on cDNA cloning and Sanger sequencing that lack the throughput of current sequencing platforms. In this study, we present a high throughput, full-length allele discovery method utilizing Pacific Biosciences circular consensus sequencing (CCS). We also describe a new approach to Macaque Exome Sequencing (MES) and the development of the Rhexome1.0, an adapted target capture reagent that includes macaque-specific capture probe sets. By using sequence reads generated by whole genome sequencing (WGS) and MES to inform primer design, we were able to increase the sensitivity of KIR allele discovery. We demonstrate this increased sensitivity by defining nine novel alleles within a cohort of Mauritian cynomolgus macaques (MCM), a geographically isolated population with restricted KIR genetics that was thought to be completely characterized. Finally, we describe an approach to genotyping KIRs directly from sequence reads generated using WGS/MES reads. The findings presented here expand our understanding of KIR genetics in MCM by associating new genes with all eight KIR haplotypes and demonstrating the existence of at least one KIR3DS gene associated with every haplotype.

Keywords

Killer cell immunoglobulin-like receptors Mauritian cynomolgus macaques Whole Genome and Macaque Exome Sequencing PacBio long-amplicon sequencing 

Notes

Acknowledgements

This research was supported by contracts HHSN272201600007C and HHSN272201100013C from the National Institute of Allergy and Infectious Diseases of the National Institutes of Health and was conducted at a facility constructed with support from the Research Facilities Improvement Program (RR15459-01, RR20141-01).

Supplementary material

251_2017_977_MOESM1_ESM.pdf (61 kb)
Supplementary Fig. 1 Mafa-KIR3DL and Mafa -KIR3DS phylogenetic trees. Phylogenetic analysis of MCM KIR3DL and KIR3DS sequences. Both phylogenetic trees contain the human KIR3DL1*00701 allele as an outgroup (AF262973). Bootstrapping values are shown to the left of nodes. Novel sequences are highlighted in bold font. A, the tree contains KIR3DL sequences. Vertical bars denote lineages. B, the tree contains KIR3DS sequences. (PDF 61 kb).
251_2017_977_MOESM2_ESM.docx (62 kb)
Supplementary Table 1 (DOCX 62 kb).
251_2017_977_MOESM3_ESM.docx (90 kb)
Supplementary Table 2 (DOCX 89 kb).
251_2017_977_MOESM4_ESM.docx (40 kb)
Supplementary Table 3 (DOCX 40 kb).
251_2017_977_MOESM5_ESM.docx (36 kb)
Supplementary Table 4 (DOCX 35 kb).
251_2017_977_MOESM6_ESM.docx (18 kb)
Supplementary Table 5 (DOCX 17 kb).
251_2017_977_MOESM7_ESM.docx (84 kb)
Supplementary Table 6 Comparison of sequences identified by PacBio CCS versus WGS/MES. (DOCX 84 kb).

References

  1. Albrecht C, Malzahn D, Brameier M, Hermes M, Ansari AA, Walter L (2014) Progression to AIDS in SIV-infected rhesus macaques is associated with distinct KIR and MHC class I polymorphisms and NK cell dysfunction. Front Immunol 5:600CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alter G, Martin MP, Teigen N, Carr WH, Suscovich TJ, Schneidewind A, Streeck H, Waring M, Meier A, Brander C, Lifson JD, Allen TM, Carrington M, Altfeld M (2007) Differential natural killer cell-mediated inhibition of HIV-1 replication based on distinct KIR/HLA subtypes. J Exp Med 204:3027–3036CrossRefPubMedPubMedCentralGoogle Scholar
  3. Anderson DJ, Kirk AD (2013) Primate models in organ transplantation. Cold Spring Harb Perspect Med 3:a015503CrossRefPubMedPubMedCentralGoogle Scholar
  4. Antony JM, MacDonald KS (2015) A critical analysis of the cynomolgus macaque, Macaca fascicularis, as a model to test HIV-1/SIV vaccine efficacy. Vaccine 33:3073–3083CrossRefPubMedGoogle Scholar
  5. Bainbridge MN, Wang M, Wu Y, Newsham I, Muzny DM, Jefferies JL, Albert TJ, Burgess DL, Gibbs RA (2011) Targeted enrichment beyond the consensus coding DNA sequence exome reveals exons with higher variant densities. Genome Biol 12:R68CrossRefPubMedPubMedCentralGoogle Scholar
  6. Biassoni R, Falco M, Cambiaggi A, Costa P, Verdiani S, Pende D, Conte R, Di Donato C, Parham P, Moretta L (1995) Amino acid substitutions can influence the natural killer (NK)-mediated recognition of HLA-C molecules. Role of serine-77 and lysine-80 in the target cell protection from lysis mediated by “group 2” or “group 1” NK clones. J Exp Med 182:605–609CrossRefPubMedGoogle Scholar
  7. Bimber BN, Evans DT (2015) The killer-cell immunoglobulin-like receptors of macaques. Immunol Rev 267:246–258CrossRefPubMedGoogle Scholar
  8. Bimber BN, Moreland AJ, Wiseman RW, Hughes AL, O’Connor DH (2008) Complete characterization of killer Ig-like receptor (KIR) haplotypes in Mauritian cynomolgus macaques: novel insights into nonhuman primate KIR gene content and organization. J Immunol 181:6301–6308CrossRefPubMedPubMedCentralGoogle Scholar
  9. Blokhuis JH, Doxiadis GG, Bontrop RE (2009) A splice site mutation converts an inhibitory killer cell Ig-like receptor into an activating one. Mol Immunol 46:640–648CrossRefPubMedGoogle Scholar
  10. Blokhuis JH, van der Wiel MK, Doxiadis GG, Bontrop RE (2010) The mosaic of KIR haplotypes in rhesus macaques. Immunogenetics 62:295–306CrossRefPubMedPubMedCentralGoogle Scholar
  11. Blokhuis JH, van der Wiel MK, Doxiadis GG, Bontrop RE (2011) The extreme plasticity of killer cell Ig-like receptor (KIR) haplotypes differentiates rhesus macaques from humans. Eur J Immunol 41:2719–2728CrossRefPubMedGoogle Scholar
  12. Bonagura VR, Du Z, Ashouri E, Luo L, Hatam LJ, DeVoti JA, Rosenthal DW, Steinberg BM, Abramson AL, Gjertson DW, Reed EF, Rajalingam R (2010) Activating killer cell immunoglobulin-like receptors 3DS1 and 2DS1 protect against developing the severe form of recurrent respiratory papillomatosis. Hum Immunol 71:212–219CrossRefPubMedGoogle Scholar
  13. Carr WH, Pando MJ, Parham P (2005) KIR3DL1 polymorphisms that affect NK cell inhibition by HLA-Bw4 ligand. J Immunol 175:5222–5229CrossRefPubMedGoogle Scholar
  14. Carrillo-Bustamante P, Keşmir C, de Boer RJ (2016) The evolution of natural killer cell receptors. Immunogenetics 68:3–18CrossRefPubMedGoogle Scholar
  15. Carrington M, Norman P. (2003) The KIR Gene ClusterGoogle Scholar
  16. Chaichompoo P, Bostik P, Stephenson S, Udompunturuk S, Kobkitjaroen J, Pattanapanyasat K, Ansari AA (2010) Multiple KIR gene polymorphisms are associated with plasma viral loads in SIV-infected rhesus macaques. Cell Immunol 263:176–187CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cirocco RE, Mathew JM, Burke GW, Esquenazi V, Miller J (2007) Killer cell immunoglobulin-like receptor polymorphisms in HLA-identical kidney transplant recipients: lack of 2DL2 and 2DS2 may be associated with poor graft function. Tissue Antigens 69(Suppl 1):123–124CrossRefPubMedGoogle Scholar
  18. Dunphy SE, Guinan KJ, Chorcora CN, Jayaraman J, Traherne JA, Trowsdale J, Pende D, Middleton D, Gardiner CM (2015) 2DL1, 2DL2 and 2DL3 all contribute to KIR phenotype variability on human NK cells. Genes Immun 16:301–310CrossRefPubMedGoogle Scholar
  19. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefPubMedGoogle Scholar
  20. Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, Peluso P, Rank D, Baybayan P, Bettman B, Bibillo A, Bjornson K, Chaudhuri B, Christians F, Cicero R, Clark S, Dalal R, Dewinter A, Dixon J, Foquet M, Gaertner A, Hardenbol P, Heiner C, Hester K, Holden D, Kearns G, Kong X, Kuse R, Lacroix Y, Lin S, Lundquist P, Ma C, Marks P, Maxham M, Murphy D, Park I, Pham T, Phillips M, Roy J, Sebra R, Shen G, Sorenson J, Tomaney A, Travers K, Trulson M, Vieceli J, Wegener J, Wu D, Yang A, Zaccarin D, Zhao P, Zhong F, Korlach J, Turner S (2009) Real-time DNA sequencing from single polymerase molecules. Science 323:133–138CrossRefPubMedGoogle Scholar
  21. Ericsen AJ, Starrett GJ, Greene JM, Lauck M, Raveendran M, Deiros DR, Mohns MS, Vince N, Cain BT, Pham NH, Weinfurter JT, Bailey AL, Budde ML, Wiseman RW, Gibbs R, Muzny D, Friedrich TC, Rogers J, O’Connor DH (2014) Whole genome sequencing of SIV-infected macaques identifies candidate loci that may contribute to host control of virus replication. Genome Biol 15:478CrossRefPubMedPubMedCentralGoogle Scholar
  22. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  23. Gardiner CM (2008) Killer cell immunoglobulin-like receptors on NK cells: the how, where and why. Int J Immunogenet 35:1–8CrossRefPubMedGoogle Scholar
  24. González-Galarza FF, Takeshita LY, Santos EJ, Kempson F, Maia MH, da Silva AL, Silva ALT e, Ghattaoraya GS, Alfirevic A, Jones AR, Middleton D (2015) Allele frequency net 2015 update: new features for HLA epitopes, KIR and disease and HLA adverse drug reaction associations. Nucleic Acids Res 43:D784–D788CrossRefPubMedGoogle Scholar
  25. Hansen DS, D’Ombrain MC, Schofield L (2007) The role of leukocytes bearing natural killer complex receptors and killer immunoglobulin-like receptors in the immunology of malaria. Curr Opin Immunol 19:416–423CrossRefPubMedGoogle Scholar
  26. Hellmann I, Lim SY, Gelman RS, Letvin NL (2011) Association of activating KIR copy number variation of NK cells with containment of SIV replication in rhesus monkeys. PLoS Pathog 7:e1002436CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hellmann I, Letvin NL, Schmitz JE (2013) KIR2DL4 copy number variation is associated with CD4+ T-cell depletion and function of cytokine-producing NK cell subsets in SIV-infected Mamu-A*01-negative rhesus macaques. J Virol 87:5305–5310CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hershberger KL, Shyam R, Miura A, Letvin NL (2001) Diversity of the killer cell Ig-like receptors of rhesus monkeys. J Immunol 166:4380–4390CrossRefPubMedGoogle Scholar
  29. Hershberger KL, Kurian J, Korber BT, Letvin NL (2005) Killer cell immunoglobulin-like receptors (KIR) of the African-origin sabaeus monkey: evidence for recombination events in the evolution of KIR. Eur J Immunol 35:922–935CrossRefPubMedGoogle Scholar
  30. Hilton HG, Guethlein LA, Goyos A, Nemat-Gorgani N, Bushnell DA, Norman PJ, Parham P (2015) Polymorphic HLA-C receptors balance the functional characteristics of KIR haplotypes. J Immunol 195:3160–3170CrossRefPubMedPubMedCentralGoogle Scholar
  31. Jiang Y, Chen O, Cui C, Zhao B, Han X, Zhang Z, Liu J, Xu J, Hu Q, Liao C, Shang H (2013) KIR3DS1/L1 and HLA-Bw4-80I are associated with HIV disease progression among HIV typical progressors and long-term nonprogressors. BMC Infect Dis 13:405CrossRefPubMedPubMedCentralGoogle Scholar
  32. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282PubMedGoogle Scholar
  33. Karl JA, Graham ME, Wiseman RW, Heimbruch KE, Gieger SM, Doxiadis GG, Bontrop RE, O’Connor DH (2017) Major histocompatibility complex haplotyping and long-amplicon allele discovery in cynomolgus macaques from Chinese breeding facilities. Immunogenetics 69:211–229Google Scholar
  34. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  35. Khakoo SI, Thio CL, Martin MP, Brooks CR, Gao X, Astemborski J, Cheng J, Goedert JJ, Vlahov D, Hilgartner M, Cox S, Little AM, Alexander GJ, Cramp ME, O’Brien SJ, Rosenberg WM, Thomas DL, Carrington M (2004) HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 305:872–874CrossRefPubMedGoogle Scholar
  36. Knapp S, Warshow U, Hegazy D, Brackenbury L, Guha IN, Fowell A, Little AM, Alexander GJ, Rosenberg WM, Cramp ME, Khakoo SI (2010) Consistent beneficial effects of killer cell immunoglobulin-like receptor 2DL3 and group 1 human leukocyte antigen-C following exposure to hepatitis C virus. Hepatology 51:1168–1175CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kochetov AV (2008) Alternative translation start sites and hidden coding potential of eukaryotic mRNAs. BioEssays 30:683–691CrossRefPubMedGoogle Scholar
  38. Kruse PH, Rosner C, Walter L (2010) Characterization of rhesus macaque KIR genotypes and haplotypes. Immunogenetics 62:281–293CrossRefPubMedGoogle Scholar
  39. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefPubMedGoogle Scholar
  40. Kunert K, Seiler M, Mashreghi MF, Klippert K, Schönemann C, Neumann K, Pratschke J, Reinke P, Volk HD, Kotsch K (2007) KIR/HLA ligand incompatibility in kidney transplantation. Transplantation 84:1527–1533CrossRefPubMedGoogle Scholar
  41. Kuśnierczyk P (2013) Are killer cell immunoglobulin-like receptor genes important for the prediction of kidney graft rejection. Arch Immunol Ther Exp 61:321–325CrossRefGoogle Scholar
  42. La Manna G, Corsini S, Iannelli S, Cappuccilli ML, Comai G, Iorio M, Todeschini P, Carretta E, Scolari MP, Bontadini A, Stefoni S (2013) Influence of the immunogenetic KIR and HLA systems on long-term renal transplant outcome. Ann Transplant 18:611–621CrossRefPubMedGoogle Scholar
  43. Lanier LL (2005) NK cell recognition. Annu Rev Immunol 23:225–274CrossRefPubMedGoogle Scholar
  44. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefPubMedGoogle Scholar
  45. Legaz I, López-Álvarez MR, Campillo JA, Moya-Quiles MR, Bolarín JM, de la Peña J, Salgado G, Gimeno L, García-Alonso AM, Muro M, Miras M, Alonso C, Álvarez-López MR, Minguela A (2013) KIR gene mismatching and KIR/C ligands in liver transplantation: consequences for short-term liver allograft injury. Transplantation 95:1037–1044CrossRefPubMedGoogle Scholar
  46. Lodoen MB, Lanier LL (2006) Natural killer cells as an initial defense against pathogens. Curr Opin Immunol 18:391–398CrossRefPubMedGoogle Scholar
  47. Long EO, Rajagopalan S (2000) HLA class I recognition by killer cell Ig-like receptors. Semin Immunol 12:101–108CrossRefPubMedGoogle Scholar
  48. Lupski JR, Gonzaga-Jauregui C, Yang Y, Bainbridge MN, Jhangiani S, Buhay CJ, Kovar CL, Wang M, Hawes AC, Reid JG, Eng C, Muzny DM, Gibbs RA (2013) Exome sequencing resolves apparent incidental findings and reveals further complexity of SH3TC2 variant alleles causing Charcot-Marie-Tooth neuropathy. Genome Med 5:57CrossRefPubMedPubMedCentralGoogle Scholar
  49. Marras F, Bozzano F, Ascierto ML, De Maria A (2014) Baseline and dynamic expression of activating NK cell receptors in the control of chronic viral infections: the paradigm of HIV-1 and HCV. Front Immunol 5. doi: 10.3389/fimmu.2014.00305
  50. Martin MP, Gao X, Lee JH, Nelson GW, Detels R, Goedert JJ, Buchbinder S, Hoots K, Vlahov D, Trowsdale J, Wilson M, O’Brien SJ, Carrington M (2002) Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat Genet 31:429–434PubMedGoogle Scholar
  51. Messaoudi I, Estep R, Robinson B, Wong SW (2011) Nonhuman primate models of human immunology. Antioxid Redox Signal 14:261–273CrossRefPubMedPubMedCentralGoogle Scholar
  52. Middleton D, Gonzelez F (2010) The extensive polymorphism of KIR genes. Immunology 129:8–19CrossRefPubMedPubMedCentralGoogle Scholar
  53. Moreland AJ, Guethlein LA, Reeves RK, Broman KW, Johnson RP, Parham P, O’Connor DH, Bimber BN (2011) Characterization of killer immunoglobulin-like receptor genetics and comprehensive genotyping by pyrosequencing in rhesus macaques. BMC Genomics 12:295CrossRefPubMedPubMedCentralGoogle Scholar
  54. Ponte M, Cantoni C, Biassoni R, Tradori-Cappai A, Bentivoglio G, Vitale C, Bertone S, Moretta A, Moretta L, Mingari MC (1999) Inhibitory receptors sensing HLA-G1 molecules in pregnancy: decidua-associated natural killer cells express LIR-1 and CD94/NKG2A and acquire p49, an HLA-G1-specific receptor. Proc Natl Acad Sci U S A 96:5674–5679CrossRefPubMedPubMedCentralGoogle Scholar
  55. Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842CrossRefPubMedPubMedCentralGoogle Scholar
  56. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277CrossRefPubMedGoogle Scholar
  57. Robinson J, Waller MJ, Stoehr P, Marsh SG (2005) IPD—the immuno polymorphism database. Nucleic Acids Res 33:D523–D526CrossRefPubMedGoogle Scholar
  58. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  59. Sambrook JG, Bashirova A, Palmer S, Sims S, Trowsdale J, Abi-Rached L, Parham P, Carrington M, Beck S (2005) Single haplotype analysis demonstrates rapid evolution of the killer immunoglobulin-like receptor (KIR) loci in primates. Genome Res 15:25–35CrossRefPubMedPubMedCentralGoogle Scholar
  60. Sambrook JG, Bashirova A, Andersen H, Piatak M, Vernikos GS, Coggill P, Lifson JD, Carrington M, Beck S (2006) Identification of the ancestral killer immunoglobulin-like receptor gene in primates. BMC Genomics 7:209CrossRefPubMedPubMedCentralGoogle Scholar
  61. Schmitz JE, Korioth-Schmitz B (2013) Immunopathogenesis of simian immunodeficiency virus infection in nonhuman primates. Curr Opin HIV AIDS 8:273–279PubMedGoogle Scholar
  62. Shilling HG, Young N, Guethlein LA, Cheng NW, Gardiner CM, Tyan D, Parham P (2002) Genetic control of human NK cell repertoire. J Immunol 169:239–247CrossRefPubMedGoogle Scholar
  63. Sussman RW, Tattersall I (1986) Distribution, abundance, and putative ecological strategy of Macaca fascicularis on the island of Mauritius, southwestern Indian Ocean. Folia Primatol 46:28–43CrossRefGoogle Scholar
  64. Travers KJ, Chin CS, Rank DR, Eid JS, Turner SW (2010) A flexible and efficient template format for circular consensus sequencing and SNP detection. Nucleic Acids Res 38:e159CrossRefPubMedPubMedCentralGoogle Scholar
  65. Trowsdale J, Barten R, Haude A, Stewart CA, Beck S, Wilson MJ (2001) The genomic context of natural killer receptor extended gene families. Immunol Rev 181:20–38CrossRefPubMedGoogle Scholar
  66. Uhrberg M, Valiante NM, Shum BP, Shilling HG, Lienert-Weidenbach K, Corliss B, Tyan D, Lanier LL, Parham P (1997) Human diversity in killer cell inhibitory receptor genes. Immunity 7:753–763CrossRefPubMedGoogle Scholar
  67. Valiante NM, Uhrberg M, Shilling HG, Lienert-Weidenbach K, Arnett KL, D’Andrea A, Phillips JH, Lanier LL, Parham P (1997) Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 7:739–751CrossRefPubMedGoogle Scholar
  68. Vallender EJ (2011) Expanding whole exome resequencing into non-human primates. Genome Biol 12:R87CrossRefPubMedPubMedCentralGoogle Scholar
  69. Van Bergen J, Thompson A, Haasnoot GW, Roodnat JI, de Fijter JW, Claas FH, Koning F, Doxiadis II (2011) KIR-ligand mismatches are associated with reduced long-term graft survival in HLA-compatible kidney transplantation. Am J Transplant 11:1959–1964CrossRefPubMedGoogle Scholar
  70. Wende H, Volz A, Ziegler A (2000) Extensive gene duplications and a large inversion characterize the human leukocyte receptor cluster. Immunogenetics 51:703–713CrossRefPubMedGoogle Scholar
  71. Westbrook CJ, Karl JA, Wiseman RW, Mate S, Koroleva G, Garcia K, Sanchez-Lockhart M, O’Connor DH, Palacios G (2015) No assembly required: full-length MHC class I allele discovery by PacBio circular consensus sequencing. Hum Immunol 76:891–896CrossRefPubMedGoogle Scholar
  72. Wilson MJ, Torkar M, Haude A, Milne S, Jones T, Sheer D, Beck S, Trowsdale J (2000) Plasticity in the organization and sequences of human KIR/ILT gene families. Proc Natl Acad Sci U S A 97:4778–4783CrossRefPubMedPubMedCentralGoogle Scholar
  73. Wiseman RW, Karl JA, Bimber BN, O’Leary CE, Lank SM, Tuscher JJ, Detmer AM, Bouffard P, Levenkova N, Turcotte CL, Szekeres E, Wright C, Harkins T, O’Connor DH (2009) Major histocompatibility complex genotyping with massively parallel pyrosequencing. Nat Med 15:1322–1326CrossRefPubMedPubMedCentralGoogle Scholar
  74. Wiseman RW, Karl JA, Bohn PS, Nimityongskul FA, Starrett GJ, O’Connor DH (2013) Haplessly hoping: macaque major histocompatibility complex made easy. ILAR J 54:196–210CrossRefPubMedPubMedCentralGoogle Scholar
  75. Yan WH, Lin A, Chen BG, Zhou MY, Dai MZ, Chen XJ, Gan LH, Zhu M, Shi WW, Li BL (2007) Possible roles of KIR2DL4 expression on uNK cells in human pregnancy. Am J Reprod Immunol 57:233–242CrossRefPubMedGoogle Scholar
  76. Yawata M, Yawata N, Draghi M, Little AM, Partheniou F, Parham P (2006) Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function. J Exp Med 203:633–645CrossRefPubMedPubMedCentralGoogle Scholar
  77. Zipperlen K, Gallant M, Stapleton S, Heath J, Barrett L, Grant M (2015) Protective genotypes in HIV infection reflect superior function of KIR3DS1+ over KIR3DL1+ CD8+ T cells. Immunol Cell Biol 93:67–76CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Trent M. Prall
    • 1
  • Michael E. Graham
    • 2
  • Julie A. Karl
    • 2
  • Roger W. Wiseman
    • 1
    • 2
  • Adam J. Ericsen
    • 1
  • Muthuswamy Raveendran
    • 3
  • R. Alan Harris
    • 3
  • Donna M. Muzny
    • 3
  • Richard A. Gibbs
    • 3
  • Jeffrey Rogers
    • 3
    • 4
  • David H. O’Connor
    • 1
    • 2
    Email author
  1. 1.Wisconsin National Primate Research CenterUniversity of WisconsinMadisonUSA
  2. 2.Department of Pathology and Laboratory MedicineUniversity of WisconsinMadisonUSA
  3. 3.Human Genome Sequencing CenterBaylor College of MedicineHoustonUSA
  4. 4.Department of Molecular and Human GeneticsBaylor College of MedicineHoustonUSA

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