Rapid identification of bovine MHCI haplotypes in genetically divergent cattle populations using next-generation sequencing

Immunogenetics - Tập 68 - Trang 765-781 - 2016
Deepali Vasoya1, Andy Law1, Paolo Motta1, Mingyan Yu2, Adrian Muwonge1, Elizabeth Cook2, Xiaoying Li3, Karen Bryson3,4, Amanda MacCallam3, Tatjana Sitt5, Philip Toye2, Barend Bronsvoort1, Mick Watson1, W. Ivan Morrison3, Timothy Connelley3
1Division of Genetics and Genomics, The Roslin Institute, The University of Edinburgh, Midlothian, UK
2International Livestock Research Institute, Nairobi, Kenya
3Division of Infection and Immunity, The Roslin Institute, The University of Edinburgh, Midlothian, UK
4Trinity College Dublin, Dublin, Ireland
5Department of Animal and Veterinary Sciences, The University of Vermont, Burlington, USA

Tóm tắt

The major histocompatibility complex (MHC) region contains many genes that are key regulators of both innate and adaptive immunity including the polymorphic MHCI and MHCII genes. Consequently, the characterisation of the repertoire of MHC genes is critical to understanding the variation that determines the nature of immune responses. Our current knowledge of the bovine MHCI repertoire is limited with only the Holstein-Friesian breed having been studied in any depth. Traditional methods of MHCI genotyping are of low resolution and laborious and this has been a major impediment to a more comprehensive analysis of the MHCI repertoire of other cattle breeds. Next-generation sequencing (NGS) technologies have been used to enable high throughput and much higher resolution MHCI typing in a number of species. In this study we have developed a MiSeq platform approach and requisite bioinformatics pipeline to facilitate typing of bovine MHCI repertoires. The method was validated initially on a cohort of Holstein-Friesian animals and then demonstrated to enable characterisation of MHCI repertoires in African cattle breeds, for which there was limited or no available data. During the course of these studies we identified >140 novel classical MHCI genes and defined 62 novel MHCI haplotypes, dramatically expanding the known bovine MHCI repertoire.

Tài liệu tham khảo

Apps R, Meng Z, Del Prete GQ, Lifson JD, Zhou M, Carrington M (2015) Relative expression levels of the HLA class-I proteins in normal and HIV-infected cells. J Immunol 194:3594–3600 Apps R, Qi Y, Carlson JM, Chen H, Gao X, Thomas R, Yuki Y, Del Prete GQ, Goulder P, Brumme ZL, Brumme CJ, John M, Mallal S, Nelson G, Bosch R, Heckerman D, Stein JL, Soderberg KA, Moody MA, Denny TN, Zeng X, Fang J, Moffett A, Lifson JD, Goedert JJ, Buchbinder S, Kirk GD, Fellay J, McLaren P, Deeks SG, Pereyra F, Walker B, Michael NL, Weintrob A, Wolinsky S, Liao W, Carrington M (2013) Influence of HLA-C expression level on HIV control. Science 340:87–91 Babiuk S, Horseman B, Zhang C, Bickis M, Kusalik A, Schook LB, Abrahamsen MS, Pontarollo R (2007) BoLA class I allele diversity and polymorphism in a herd of cattle. Immunogenetics 59:167–176 Birch J, Murphy L, MacHugh ND, Ellis SA (2006) Generation and maintenance of diversity in the cattle MHC class I region. Immunogenetics 58:670–679 Bradley DG, MacHugh DE, Cunningham P, Loftus RT (1996) Mitochondrial diversity and the origins of African and European cattle. Proc Natl Acad Sci U S A 93:5131–5135 Brown P, Spooner RL, Clark AJ (1989) Cloning and characterization of a BoLA class I cDNA clone. Immunogenetics 29:58–60 Cereb N, Kim HR, Ryu J, Yang SY (2015) Advances in DNA sequencing technologies for high resolution HLA typing. Hum Immunol 76:923–927 Chappell P, el Meziane K, Harrison M, Magiera L, Hermann C, Mears L, Wrobel AG, Durant C, Nielsen LL, Buus S, Ternette N, Mwangi W, Butter C, Nair V, Ahyee T, Duggleby R, Madrigal A, Roversi P, Lea SM, Kaufman J (2015) Expression levels of MHC class I molecules are inversely correlated with promiscuity of peptide binding. Elife 4:e05345 Codner GF, Stear MJ, Reeve R, Matthews L, Ellis SA (2012) Selective forces shaping diversity in the class I region of the major histocompatibility complex in dairy cattle. Anim Genet 43:239–249 Davies CJ, Eldridge JA, Fisher PJ, Schlafer DH (2006) Evidence for expression of both classical and non-classical major histocompatibility complex class I genes in bovine trophoblast cells. Am J Reprod Immunol 55:188–200 De Santis D, Dinauer D, Duke J, Erlich HA, Holcomb CL, Lind C, Mackiewicz K, Monos D, Moudgil A, Norman P, Parham P, Sasson A, Allcock RJ (2013) 16(th) IHIW: review of HLA typing by NGS. Int J Immunogenet 40:72–76 Decker JE, McKay SD, Rolf MM, Kim J, Molina Alcala A, Sonstegard TS, Hanotte O, Gotherstrom A, Seabury CM, Praharani L, Babar ME, Correia de Almeida Regitano L, Yildiz MA, Heaton MP, Liu WS, Lei CZ, Reecy JM, Saif-Ur-Rehman M, Schnabel RD, Taylor JF (2014) Worldwide patterns of ancestry, divergence, and admixture in domesticated cattle. PLoS Genet 10:e1004254 Dudley DM, Karl JA, Creager HM, Bohn PS, Wiseman RW, O’Connor DH (2014) Full-length novel MHC class I allele discovery by next-generation sequencing: two platforms are better than one. Immunogenetics 66:15–24 Ellis SA, Holmes EC, Staines KA, Smith KB, Stear MJ, McKeever DJ, MacHugh ND, Morrison WI (1999) Variation in the number of expressed MHC genes in different cattle class I haplotypes. Immunogenetics 50:319–328 Ellis SA, Morrison WI, MacHugh ND, Birch J, Burrells A, Stear MJ (2005) Serological and molecular diversity in the cattle MHC class I region. Immunogenetics 57:601–606 Ellis SA, Staines KA, Morrison WI (1996) cDNA sequence of cattle MHC class I genes transcribed in serologically defined haplotypes A18 and A31. Immunogenetics 43:156–159 Ellis SA, Staines KA, Stear MJ, Hensen EJ, Morrison WI (1998) DNA typing for BoLA class I using sequence-specific primers (PCR-SSP). Eur J Immunogenet 25:365–370 Erlich H (2012) HLA DNA typing: past, present, and future. Tissue Antigens 80:1–11 Gabriel C, Furst D, Fae I, Wenda S, Zollikofer C, Mytilineos J, Fischer GF (2014) HLA typing by next-generation sequencing–getting closer to reality. Tissue Antigens 83:65–75 Gaddum RM, Cook RS, Furze JM, Ellis SA, Taylor G (2003) Recognition of bovine respiratory syncytial virus proteins by bovine CD8+ T lymphocytes. Immunology 108:220–229 Graham SP, Pelle R, Yamage M, Mwangi DM, Honda Y, Mwakubambanya RS, de Villiers EP, Abuya E, Awino E, Gachanja J, Mbwika F, Muthiani AM, Muriuki C, Nyanjui JK, Onono FO, Osaso J, Riitho V, Saya RM, Ellis SA, McKeever DJ, MacHugh ND, Gilbert SC, Audonnet JC, Morrison WI, van der Bruggen P, Taracha EL (2008) Characterization of the fine specificity of bovine CD8 T-cell responses to defined antigens from the protozoan parasite Theileria parva. Infect Immun 76:685–694 Guethlein LA, Norman PJ, Hilton HH, Parham P (2015) Co-evolution of MHC class I and variable NK cell receptors in placental mammals. Immunol Rev 267:259–282 Guzman E, Taylor G, Charleston B, Ellis SA (2010) Induction of a cross-reactive CD8(+) T cell response following foot-and-mouth disease virus vaccination. J Virol 84:12375–12384 Guzman E, Taylor G, Charleston B, Skinner MA, Ellis SA (2008) An MHC-restricted CD8+ T-cell response is induced in cattle by foot-and-mouth disease virus (FMDV) infection and also following vaccination with inactivated FMDV. J Gen Virol 89:667–675 Hammond JA, Marsh SG, Robinson J, Davies CJ, Stear MJ, Ellis SA (2012) Cattle MHC nomenclature: is it possible to assign sequences to discrete class I genes? Immunogenetics 64:475–480 Heimbruch KE, Karl JA, Wiseman RW, Dudley DM, Johnson Z, Kaur A, O’Connor DH (2015) Novel MHC class I full-length allele and haplotype characterization in sooty mangabeys. Immunogenetics 67:437–445 Holmes EC, Roberts AF, Staines KA, Ellis SA (2003) Evolution of major histocompatibility complex class I genes in Cetartiodactyls. Immunogenetics 55:193–202 Hosomichi K, Shiina T, Tajima A, Inoue I (2015) The impact of next-generation sequencing technologies on HLA research. J Hum Genet 60:665–673 Lange V, Bohme I, Hofmann J, Lang K, Sauter J, Schone B, Paul P, Albrecht V, Andreas JM, Baier DM, Nething J, Ehninger U, Schwarzelt C, Pingel J, Ehninger G, Schmidt AH (2014) Cost-efficient high-throughput HLA typing by MiSeq amplicon sequencing. BMC Genomics 15:63 Loftus RT, MacHugh DE, Bradley DG, Sharp PM, Cunningham P (1994) Evidence for two independent domestications of cattle. Proc Natl Acad Sci U S A 91:2757–2761 Macdonald IK, Harkiolaki M, Hunt L, Connelley T, Carroll AV, MacHugh ND, Graham SP, Jones EY, Morrison WI, Flower DR, Ellis SA (2010) MHC class I bound to an immunodominant Theileria parva epitope demonstrates unconventional presentation to T cell receptors. PLoS Pathog 6:e1001149 MacHugh DE, Shriver MD, Loftus RT, Cunningham P, Bradley DG (1997) Microsatellite DNA variation and the evolution, domestication and phylogeography of taurine and zebu cattle (Bos taurus and Bos indicus). Genetics 146:1071–1086 Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963 Oomen RA, Gillett RM, Kyle CJ (2013) Comparison of 454 pyrosequencing methods for characterizing the major histocompatibility complex of nonmodel species and the advantages of ultra deep coverage. Mol Ecol Resour 13:103–116 Promerova M, Babik W, Bryja J, Albrecht T, Stuglik M, Radwan J (2012) Evaluation of two approaches to genotyping major histocompatibility complex class I in a passerine-CE-SSCP and 454 pyrosequencing. Mol Ecol Resour 12:285–292 Robinson J, Halliwell JA, McWilliam H, Lopez R, Parham P, Marsh SG (2013) The IMGT/HLA database. Nucleic Acids Res 41:D1222–D1227 Schwartz JC, Hammond JA (2015) The assembly and characterisation of two structurally distinct cattle MHC class I haplotypes point to the mechanisms driving diversity. Immunogenetics 67:539–544 Sepil I, Moghadam HK, Huchard E, Sheldon BC (2012) Characterization and 454 pyrosequencing of major histocompatibility complex class I genes in the great tit reveal complexity in a passerine system. BMC Evol Biol 12:68 Snary D, Barnstable CJ, Bodmer WF, Crumpton MJ (1977) Molecular structure of human histocompatibility antigens: the HLA-C series. Eur J Immunol 7:580–585 Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 Troy CS, MacHugh DE, Bailey JF, Magee DA, Loftus RT, Cunningham P, Chamberlain AT, Sykes BC, Bradley DG (2001) Genetic evidence for Near-Eastern origins of European cattle. Nature 410:1088–1091