1932

Abstract

In pigs, the major histocompatibility complex (MHC), or swine leukocyte antigen (SLA) complex, maps to chromosome 7. It consists of three regions, the class I and class III regions mapping to 7p1.1 and the class II region mapping to 7q1.1. The swine MHC is divided by the centromere, which is unique among mammals studied to date. The SLA complexspans between 2.4 and 2.7 Mb, depending on haplotype, and encodes approximately 150 loci, with at least 120 genes predicted to be functional. Here we update the whole SLA complex based on the Sscrofa11.1 build and annotate the organization for all recognized SLA genes and their allelic sequences. We present SLA nomenclature and typing methods and discuss the expression of SLA proteins, as well as their role in antigen presentation and immune, disease, and vaccine responses. Finally, we explore the role of SLA genes in transplantation and xenotransplantation and their importance in swine biomedical models.

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2020-02-15
2024-04-19
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Literature Cited

  1. 1. 
    Renard C, Hart E, Sehra H, Beasley H, Coggill P et al. 2006. The genomic sequence and analysis of the swine major histocompatibility complex. Genomics 88:96–110First full-length sequencing and annotation of the complete SLA complex (haplotype Hp-1.1).
    [Google Scholar]
  2. 2. 
    Danchin E, Vitiello V, Vienne A, Richard O, Gouret P et al. 2004. The major histocompatibility complex origin. Immunol. Rev. 198:216–32
    [Google Scholar]
  3. 3. 
    Hu R, Lemonnier G, Bourneuf E, Vincent-Naulleau S, Rogel-Gaillard C 2011. Transcription variants of SLA-7, a swine non classical MHC class I gene. BMC Proc 5:Suppl. 4S10 https://doi.org/10.1186/1753-6561-5-S4-S10
    [Crossref] [Google Scholar]
  4. 4. 
    Ho CS, Lunney JK, Ando A, Rogel-Gaillard C, Lee J-H et al. 2009. Nomenclature for factors of the SLA system, update 2008. Tissue Antigens 73:307–15 https://doi.org/10.1111/j.1399-0039.2009.01213.x
    [Crossref] [Google Scholar]
  5. 5. 
    Gao Y, Wahlberg P, Marthey S, Esquerré D, Jaffrézic F et al. 2012. Analysis of porcine MHC using microarrays. Vet. Immunol. Immunopathol. 148:78–84 https://doi.org/10.1016/j.vetimm.2011.04.007
    [Crossref] [Google Scholar]
  6. 6. 
    Maroilley T, Lemonnier G, Lecardonnel J, Esquerré D, Ramayo-Caldas Y et al. 2017. Deciphering the genetic regulation of peripheral blood transcriptome in pigs through expression genome-wide association study and allele-specific expression analysis. BMC Genom 18:967 https://doi.org/10.1186/s12864-017-4354-6 Examples of genomic regulation of SLA genes by noncoding RNAs and regulatory variants.
    [Crossref] [Google Scholar]
  7. 7. 
    Ellis SA, Hammond JA. 2014. The functional significance of cattle major histocompatibility complex class I genetic diversity. Annu. Rev. Anim. Biosci. 2:285–306 https://doi.org/10.1146/annurev-animal-022513-114234
    [Crossref] [Google Scholar]
  8. 8. 
    Tanaka-Matsuda M, Ando A, Rogel-Gaillard C, Chardon P, Uenishi H 2009. Difference in number of loci of swine leukocyte antigen classical class I genes among haplotypes. Genomics 93:261–73 https://doi.org/10.1016/j.ygeno.2008.10.004
    [Crossref] [Google Scholar]
  9. 9. 
    Rogel-Gaillard C, Vaiman M, Renard C, Chardon P, Yerle M 1997. Localization of the beta 2-microglobulin gene to pig chromosome 1q17. Mamm. Genome 8:948
    [Google Scholar]
  10. 10. 
    Kusza S, Flori L, Gao Y, Teillaud A, Hu R et al. 2011. Transcription specificity of the class Ib genes SLA-6, SLA-7 and SLA-8 of the swine major histocompatibility complex and comparison with class Ia genes. Anim. Genet. 42:510–20 https://doi.org/10.1111/j.1365-2052.2010.02170.x
    [Crossref] [Google Scholar]
  11. 11. 
    Crew MD, Phanavanh B, Garcia-Borges CN 2004. Sequence and mRNA expression of nonclassical SLA class I genes SLA-7 and SLA-8. Immunogenetics 56:111–14
    [Google Scholar]
  12. 12. 
    Smith DM, Lunney JK, Ho CS, Martens GW, Ando A et al. 2005. Nomenclature for factors of the swine leukocyte antigen class II system. Tissue Antigens 66:623–39
    [Google Scholar]
  13. 13. 
    Horton R, Gibson R, Coggill P, Miretti M, Allcock RJ et al. 2008. Variation analysis and gene annotation of eight MHC haplotypes: the MHC Haplotype Project. Immunogenetics 60:1–18
    [Google Scholar]
  14. 14. 
    Horton R, Wilming L, Rand V, Lovering RC, Bruford EA et al. 2004. Gene map of the extended human MHC. Nat. Rev. Genet. 5:889–99
    [Google Scholar]
  15. 15. 
    Ballingall KT, Bontrop RE, Ellis SA, Grimholt U, Hammond JA et al. 2018. Comparative MHC nomenclature: report from the ISAG/IUIS-VIC committee. Immunogenetics 70:625–32. https://doi.org/10.1007/s00251-018-1073-3Role of comparative MHC nomenclature committee for dissemination of MHC-related information to the scientific community.
    [Crossref] [Google Scholar]
  16. 16. 
    Maccari G, Robinson J, Ballingall K, Guethlein LA, Grimholt U et al. 2017. IPD-MHC 2.0: an improved inter-species database for the study of the major histocompatibility complex. Nucleic Acids Res 45:D860–D64
    [Google Scholar]
  17. 17. 
    Maccari G, Robinson J, Bontrop RE, Otting N, De Groot NG et al. 2018. IPD-MHC: nomenclature requirements for the non-human major histocompatibility complex in the next-generation sequencing era. Immunogenetics 70:619–23 https://doi.org/10.1007/s00251-018-1072-4
    [Crossref] [Google Scholar]
  18. 18. 
    Abraham JP, Barker DJ, Robinson J, Maccari G, Marsh SGE 2018. The IPD databases: cataloguing and understanding allele variants. Methods Mol. Biol. 1802:31–48 https://doi.org/10.1007/978-1-4939-8546-3_3
    [Crossref] [Google Scholar]
  19. 19. 
    Ho CS, Lunney JK, Franzo-Romain MH, Martens GW, Lee YJ et al. 2009. Molecular characterization of swine leucocyte antigen class I genes in outbred pig populations. Anim. Genet. 40:468–78 https://doi.org/10.1111/j.1365-2052.2009.01860.x
    [Crossref] [Google Scholar]
  20. 20. 
    Ho CS, Lunney JK, Franzo-Romain MH, Martens GW, Lee YJ et al. 2010. Molecular characterization of swine leucocyte antigen class II genes in outbred pig populations. Anim. Genet. 41:428–32 https://doi.org/10.1111/j.1365-2052.2010.02019.x
    [Crossref] [Google Scholar]
  21. 21. 
    Cho HO, Ho CS, Lee YJ, Cho IC, Lee SS et al. 2010. Establishment of a resource population of SLA haplotype-defined Korean native pigs. Mol. Cells 29:493–99
    [Google Scholar]
  22. 22. 
    Yeom SC, Park CG, Lee BC, Lee WJ 2010. SLA typing using the PCR-SSP method and establishment of the SLA homozygote line in pedigreed SNU miniature pigs. Anim. Sci. J. 81:158–64 https://doi.org/10.1111/j.1740-0929.2009.00727.x
    [Crossref] [Google Scholar]
  23. 23. 
    Gao C, Jiang Q, Guo D, Liu J, Han L, Qu L 2014. Characterization of swine leukocyte antigen (SLA) polymorphism by sequence-based and PCR-SSP methods in Chinese Bama miniature pigs. Dev. Comp. Immunol. 45:87–96 https://doi.org/10.1016/j.dci.2014.02.006
    [Crossref] [Google Scholar]
  24. 24. 
    Gao C, Quan J, Jiang X, Li C, Lu X, Chen H 2017. Swine leukocyte antigen diversity in Canadian specific pathogen-free Yorkshire and Landrace pigs. Front. Immunol. 8:282 https://doi.org/10.3389/fimmu.2017.00282
    [Crossref] [Google Scholar]
  25. 25. 
    Ando A, Shigenari A, Ota M, Sada M, Kawata H et al. 2011. SLA-DRB1 and -DQB1 genotyping by the PCR-SSOP-Luminex method. Tissue Antigens 78:49–55 https://doi.org/10.1111/j.1399-0039.2011.01669.x
    [Crossref] [Google Scholar]
  26. 26. 
    Ando A, Imaeda N, Ohshima S, Miyamoto A, Kaneko N et al. 2014. Characterization of swine leukocyte antigen alleles and haplotypes on a novel miniature pig line, Microminipig. Anim. Genet. 45:791–98 https://doi.org/10.1111/age.12199
    [Crossref] [Google Scholar]
  27. 27. 
    Jung WY, Choi NR, Seo DW, Lim HT, Ho CS, Lee JH 2014. Sequence-based characterization of five SLA loci in Asian wild boars. Int. J. Immunogenet. 41:397–400 https://doi.org/10.1111/iji.12141
    [Crossref] [Google Scholar]
  28. 28. 
    Le M, Choi H, Choi MK, Cho H, Kim JH et al. 2015. Development of a simultaneous high resolution typing method for three SLA class II genes, SLA-DQA,. SLA-DQB1 , and SLA-DRB1 and the analysis of SLA class II haplotypes. Gene 564:228–32 https://doi.org/10.1016/j.gene.2015.03.049
    [Crossref] [Google Scholar]
  29. 29. 
    Ho CS, Martens GW, Amoss MS Jr., Gomez-Raya L, Beattie CW, Smith DM 2010. Swine leukocyte antigen (SLA) diversity in Sinclair and Hanford swine. Dev. Comp. Immunol 34:250–57 https://doi.org/10.1016/j.dci.2009.09.006
    [Crossref] [Google Scholar]
  30. 30. 
    Essler SE, Ertl W, Deutsch J, Ruetgen BC, Groiss S et al. 2013. Molecular characterization of swine leukocyte antigen gene diversity in purebred Pietrain pigs. Anim. Genet. 44:202–5 https://doi.org/10.1111/j.1365-2052.2012.02375.x
    [Crossref] [Google Scholar]
  31. 31. 
    Pedersen LE, Jungersen G, Sorensen MR, Ho CS, Vadekær DF 2014. Swine leukocyte antigen (SLA) class I allele typing of Danish swine herds and identification of commonly occurring haplotypes using sequence specific low and high resolution primers. Vet. Immunol. Immunopathol. 162:108–16 https://doi.org/10.1016/j.vetimm.2014.10.007
    [Crossref] [Google Scholar]
  32. 32. 
    Gimsa U, Ho CS, Hammer SE 2017. Preferred SLA class I/class II haplotype combinations in German Landrace pigs. Immunogenetics 69:39–47 https://doi.org/10.1007/s00251-016-0946-6
    [Crossref] [Google Scholar]
  33. 33. 
    Schwartz JC, Hemmink JD, Graham SP, Tchilian E, Charleston B et al. 2018. The major histocompatibility complex homozygous inbred Babraham pig as a resource for veterinary and translational medicine. HLA 92:40–43 https://doi.org/10.1111/tan.13281
    [Crossref] [Google Scholar]
  34. 34. 
    Dunkelberger JR, Ho CS, Hess AS, Serão NVL, Lunney JK, Dekkers JCM 2014. Predicting MHC haplotypes from high-density SNP genotypes in pigs. Proceedings of the World Congress on Genetics Applied to Livestock Production (WCGALP), Volume Genetics of Trait Complexes: Disease Resistance (Posters) 532: http://www.wcgalp.org/proceedings/2014/predicting-mhc-haplotypes-high-density-snp-genotypes-pigs
    [Google Scholar]
  35. 35. 
    Shiina T, Suzuki S, Kulski JK 2016. MHC genotyping in human and non-human species by PCR-based next-generation sequencing. Next Generation Sequencing: Advances, Applications and Challenges JK Kulski 81–109 London: IntechOpen Ltd.
    [Google Scholar]
  36. 36. 
    Kita YF, Ando A, Tanaka K, Suzuki S, Ozaki Y et al. 2012. Application of high-resolution, massively parallel pyrosequencing for estimation of haplotypes and gene expression levels of swine leukocyte antigen (SLA) class I genes. Immunogenetics 64:187–99 https://doi.org/10.1007/s00251-011-0572-2
    [Crossref] [Google Scholar]
  37. 37. 
    Rathmann Sørensen M, Ilsøe M, Strube ML, Bishop R, Erbs G et al. 2017. Sequence-based genotyping of expressed swine leukocyte antigen class I alleles by next-generation sequencing reveal novel swine leukocyte antigen class I haplotypes and alleles in Belgian, Danish, and Kenyan fattening pigs and Göttingen minipigs. Front. Immunol. 8:701 https://doi.org/10.3389/fImmu.2017.00701
    [Crossref] [Google Scholar]
  38. 38. 
    Lee C, Moroldo M, Perdomo-Sabogal A, Mach N, Marthey S et al. 2018. Inferring the evolution of the major histocompatibility complex of wild pigs and peccaries using hybridisation DNA capture-based sequencing. Immunogenetics 70:401–17 https://doi.org/10.1007/s00251-017-1048-9
    [Crossref] [Google Scholar]
  39. 39. 
    Petersdorf EW, O'hUigin C. 2019. The MHC in the era of next-generation sequencing: implications for bridging structure with function. Hum. Immunol. 80:67–78 https://doi.org/10.1016/j.humimm.2018.10.002
    [Crossref] [Google Scholar]
  40. 40. 
    Fuselli S, Baptista RP, Panziera A, Magi A, Guglielmi S et al. 2018. A new hybrid approach for MHC genotyping: high-throughput NGS and long read MinION nanopore sequencing, with application to the non-model vertebrate Alpine chamois (Rupicapra rupicapra). Heredity 121:293–303 https://doi.org/10.1038/s41437-018-0070-5
    [Crossref] [Google Scholar]
  41. 41. 
    Lang K, Surendranath V, Quenzel P, Schöfl G, Schmidt AH, Lange V 2018. Full-length HLA class I genotyping with the MinION Nanopore sequencer. Methods Mol. Biol. 1802:155–62 https://doi.org/10.1007/978-1-4939-8546-3_10
    [Crossref] [Google Scholar]
  42. 42. 
    Liu C, Xiao F, Hoisington-Lopez J, Lang K, Quenzel P et al. 2018. Accurate typing of human leukocyte antigen class I genes by oxford nanopore sequencing. J. Mol. Diagn. 20:428–35 https://doi.org/10.1016/j.jmoldx.2018.02.006
    [Crossref] [Google Scholar]
  43. 43. 
    Lunney JK, Ho CS, Wysocki M, Smith DM 2009. Molecular genetics of the swine major histocompatibility complex, the SLA complex. Dev. Comp. Immunol. 33:362–74
    [Google Scholar]
  44. 44. 
    Nambiar M, Smith GR. 2016. Repression of harmful meiotic recombination in centromeric regions. Semin. Cell Dev. Biol. 54:188–97
    [Google Scholar]
  45. 45. 
    Carrington M. 1999. Recombination within the human MHC. Immunol. Rev. 167:245–56
    [Google Scholar]
  46. 46. 
    Kwiatkowski P, Artrip JH, John R, Edwards NM, Wang SF et al. 1999. Induction of swine major histocompatibility complex class I molecules on porcine endothelium by tumor necrosis factor-α reduces lysis by human natural killer cells. Transplantation 67:211–18
    [Google Scholar]
  47. 47. 
    Tennant LM, Renard C, Chardon P, Powell PP 2007. Regulation of porcine classical and nonclassical MHC class I expression. Immunogenetics 59:377–89
    [Google Scholar]
  48. 48. 
    Pescovitz MD, Popitz F, Sachs DH, Lunney JK 1985. Expression of Ia antigens on resting porcine T cells: a marker of functional T cells subsets. Advances in Gene Technology: Molecular Biology of the Immune System JW Streilein, F Ahmad, S Black, B Blomberg, RW Voellmy 271–72 Int. Counc. Sci. Short Rep Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  49. 49. 
    Saalmüller A, Weiland F, Reddehase MJ 1991. Resting porcine T lymphocytes expressing class II major histocompatibility antigen. Immunobiology 183:102–14
    [Google Scholar]
  50. 50. 
    Saalmüller A, Maurer S. 1994. Major histocompatibility antigen class II expressing resting porcine T lymphocytes are potent antigen-presenting cells in mixed leukocyte culture. Immunobiology 190:23–34
    [Google Scholar]
  51. 51. 
    Takamatsu HH, Denyer MS, Wileman TE 2002. A subpopulation of circulating porcine γδ T cells can act as professional antigen presenting cells.. Vet. Immunol. Immunopathol. 87:223–24
    [Google Scholar]
  52. 52. 
    Takamatsu HH, Denyer MS, Stirling C, Cox S, Aggarwal N et al. 2006. Porcine γδ T cells: possible roles on the innate and adaptive immune responses following virus infection. Vet. Immunol. Immunopathol. 112:49–61
    [Google Scholar]
  53. 53. 
    Seebach JD, Schneider MK, Comrack CA, LeGuern A, Kolb SA et al. 2001. Immortalized bone-marrow derived pig endothelial cells. Xenotransplantation 8:48–61
    [Google Scholar]
  54. 54. 
    Carrillo A, Chamorro S, Rodríguez-Gago M, Álvarez B, Molina MJ et al. 2002. Isolation and characterization of immortalized porcine aortic endothelial cell lines. Vet. Immunol. Immunopathol. 89:91–98
    [Google Scholar]
  55. 55. 
    Kim D, Kim JY, Koh HS, Lee JP, Kim YT et al. 2005. Establishment and characterization of endothelial cell lines from the aorta of miniature pig for the study of xenotransplantation. Cell Biol. Int. 29:638–46
    [Google Scholar]
  56. 56. 
    Park K-M, Cha S-H, Ahn C, Woo H-M 2013. Generation of porcine induced pluripotent stem cells and evaluation of their major histocompatibility complex protein expression in vitro. Vet. Res. Commun. 37:293–301 https://doi.org/10.1007/s11259-013-9574-x
    [Crossref] [Google Scholar]
  57. 57. 
    Wilson AD, Haverson K, Southgate K, Bland PW, Stokes CR, Bailey M 1996. Expression of major histocompatibility complex class II antigens on normal porcine intestinal endothelium. Immunology 88:98–103
    [Google Scholar]
  58. 58. 
    Pescovitz MD, Sachs DH, Lunney JK, Hsu SM 1984. Localization of class II MHC antigens on porcine renal vascular endothelium. Transplantation 37:627–31
    [Google Scholar]
  59. 59. 
    Summerfield A, Ruggli N. 2015. Immune responses against classical swine fever virus: between ignorance and lunacy. Front. Vet. Sci. 2:10 https://doi.org/10.3389/fvets.2015.00010
    [Crossref] [Google Scholar]
  60. 60. 
    Kim M, Seo H, Choi Y, Shim J, Bazer FW, Ka H 2012. Swine leukocyte antigen-DQ expression and its regulation by interferon-gamma at the maternal-fetal interface in pigs. Biol. Reprod. 86: 43: https://doi.org/10.1095/biolreprod.111.094011
    [Crossref] [Google Scholar]
  61. 61. 
    Basta S, Carrasco CP, Knoetig SM, Rigden RC, Gerber H et al. 2000. Porcine alveolar macrophages: poor accessory or effective suppressor cells for T-lymphocytes. Vet. Immunol. Immunopathol. 77:177–90
    [Google Scholar]
  62. 62. 
    Summerfield A, Guzylack-Piriou L, Schaub A, Carrasco CP, Tâche V et al. 2003. Porcine peripheral blood dendritic cells and natural interferon-producing cells. Immunology 110:440–49
    [Google Scholar]
  63. 63. 
    Auray G, Keller I, Python S, Gerber M, Bruggmann R et al. 2016. Characterization and transcriptomic analysis of porcine blood conventional and plasmacytoid dendritic cells reveals striking species-specific differences. J. Immunol. 197:4791–806
    [Google Scholar]
  64. 64. 
    Edwards JC, Everett HE, Pedrera M, Mokhtar H, Marchi E et al. 2017. CD1 and CD1+ porcine blood dendritic cells are enriched for the orthologues of the two major mammalian conventional subsets. Sci. Rep. 7:40942 https://doi.org/10.1038/srep40942
    [Crossref] [Google Scholar]
  65. 65. 
    Gerner W, Denyer MS, Takamatsu H-H, Wileman TE, Wiesmüller K-H et al. 2006. Identification of novel foot-and-mouth disease virus specific T-cell epitopes in c/c and d/d haplotype miniature swine. Virus Res 121:223–28
    [Google Scholar]
  66. 66. 
    Talker SC, Koinig HC, Stadler M, Graage R, Klingler E et al. 2015. Magnitude and kinetics of multifunctional CD4+ and CD8β+ T cells in pigs infected with swine influenza A virus. Vet. Res. 46:52 https://doi.org/10.1186/s13567-015-0182-3
    [Crossref] [Google Scholar]
  67. 67. 
    Gutiérrez AH, Loving C, Moise L, Terry FE, Brockmeier SL et al. 2016. In vivo validation of predicted and conserved T cell epitopes in a swine influenza model. PLOS ONE 11:e0159237 https://doi.org/10.1371/journal.pone.0159237
    [Crossref] [Google Scholar]
  68. 68. 
    Holzer B, Martini V, Edmans M, Tchilian E 2019. T and B cell immune responses to influenza viruses in pigs. Front. Immunol. 10:98
    [Google Scholar]
  69. 69. 
    Franzoni G, Kurkure NV, Essler SE, Everett HE, Bodman-Smith K et al. 2013. Proteome-wide screening reveals immunodominance in the CD8 T cell response against classical swine fever virus with antigen-specificity dependent on MHC class I haplotype. PLOS ONE 8:e84246
    [Google Scholar]
  70. 70. 
    Franzoni G, Graham SP, Sanna G, Angioi P, Fiori MS et al. 2018. Interaction of porcine monocyte-derived dendritic cells with African swine fever viruses of diverse virulence. Vet. Microbiol. 216:190–97 https://doi.org/10.1016/j.vetmic.2018.02.021
    [Crossref] [Google Scholar]
  71. 71. 
    Van Chanh Le Q, Le TM, Cho HS, Kim WI, Hong K et al. 2018. Analysis of peptide-SLA binding by establishing immortalized porcine alveolar macrophage cells with different SLA class II haplotypes. Vet. Res. 49:96 https://doi.org/10.1186/s13567-018-0590-2
    [Crossref] [Google Scholar]
  72. 72. 
    Mokhtar H, Eck M, Morgan SB, Essler SE, Frossard JP et al. 2014. Proteome-wide screening of the European porcine reproductive and respiratory syndrome virus reveals a broad range of T cell antigen reactivity. Vaccine 32:6828–37
    [Google Scholar]
  73. 73. 
    Mokhtar H, Pedrera M, Frossard JP, Biffar L, Choudhury B et al. 2016. The non-structural protein 5 and matrix protein are major antigenic targets of T cell immunity to porcine reproductive and respiratory syndrome virus. Front. Immunol. 7:40 https://doi.org/10.3389/fimmu.2016.00040
    [Crossref] [Google Scholar]
  74. 74. 
    Burgara-Estrella A, Díaz I, Rodríguez-Gómez I, Essler SE, Hernández J, Mateu E 2013. Predicted peptides from non-structural proteins of porcine reproductive and respiratory syndrome virus are able to induce INF-γ and IL-10. Viruses 5:663–77
    [Google Scholar]
  75. 75. 
    Ramachandran S, Jaramillo A, Xu XC, McKane BW, Chapman WC, Mohanakumar T 2004. Human immune responses to porcine endogenous retrovirus-derived peptides presented naturally in the context of porcine and human major histocompatibility complex class I molecules: implications in xenotransplantation of porcine organs. Transplantation 77:1580–88
    [Google Scholar]
  76. 76. 
    Pan X, Qi J, Zhang N, Li Q, Yin C et al. 2011. Complex assembly, crystallization and preliminary X-ray crystallographic studies of the swine major histocompatibility complex molecule SLA-1*1502. Acta Crystallogr. F 67:5568–71 https://doi.org/10.1107/S174430911100741X
    [Crossref] [Google Scholar]
  77. 77. 
    Zhang N, Qi J, Feng S, Gao F, Liu J et al. 2011. Crystal structure of swine major histocompatibility complex class I SLA-1 0401 and identification of 2009 pandemic swine-origin influenza A H1N1 virus cytotoxic T lymphocyte epitope peptides. J. Virol. 85:11709–24 https://doi.org/10.1128/JVI.05040-11
    [Crossref] [Google Scholar]
  78. 78. 
    Fan S, Wu Y, Wang S, Wang Z, Jiang B et al. 2016. Structural and biochemical analyses of swine major histocompatibility complex class I complexes and prediction of the epitope map of important influenza A virus strains. J. Virol. 90:6625–41 https://doi.org/10.1128/JVI.00119-16
    [Crossref] [Google Scholar]
  79. 79. 
    Gao FS, Zhai XX, Jiang P, Zhang Q, Gao H et al. 2018. Identification of two novel foot-and-mouth disease virus cytotoxic T lymphocyte epitopes that can bind six SLA-I proteins. Gene 653:91–101 https://doi.org/10.1016/j.gene.2018.02.025
    [Crossref] [Google Scholar]
  80. 80. 
    Fan S, Wang Y, Wang S, Wang X, Wu Y et al. 2018. Polymorphism and peptide-binding specificities of porcine major histocompatibility complex (MHC) class I molecules. Mol. Immunol. 93:236–45 https://doi.org/10.1016/j.molimm.2017.06.024
    [Crossref] [Google Scholar]
  81. 81. 
    Feng L, Sun MW, Jiang P, Li ZB, Gao H et al. 2018. Purification, crystallization and preliminary X-ray crystallographic studies of swine MHC class I complexed with an FMDV CTL epitope Hu64. Res. Vet. Sci. 119:205–8. https://doi.org/10.1016/j.rvsc.2018.06.018Alternative method to identify antigen-specific SLA class I binding motifs.
    [Crossref] [Google Scholar]
  82. 82. 
    Pedersen LE, Rasmussen M, Harndahl M, Nielsen M, Buus S, Jungersen G 2016. A combined prediction strategy increases identification of peptides bound with high affinity and stability to porcine MHC class I molecules SLA-1*04:01, SLA-2*04:01, and SLA-3*04:01. Immunogenetics 68:157–65 https://doi.org/10.1007/s00251-015-0883-9 One of the first papers describing the generation of SLA class I tetramers in swine.
    [Crossref] [Google Scholar]
  83. 83. 
    Baratelli M, Pedersen LE, Trebbien R, Larsen LE, Jungersen G et al. 2017. Identification of cross-reacting T-cell epitopes in structural and non-structural proteins of swine and pandemic H1N1 influenza A virus strains in pigs. J. Gen. Virol. 98:895–99 https://doi.org/10.1099/jgv.0.000748
    [Crossref] [Google Scholar]
  84. 84. 
    Tungatt K, Dolton G, Morgan SB, Attaf M, Fuller A et al. 2018. Induction of influenza-specific local CD8 T-cells in the respiratory tract after aerosol delivery of vaccine antigen or virus in the Babraham inbred pig. PLOS Pathog 14:e1007017 https://doi.org/10.1371/journal.ppat.1007017
    [Crossref] [Google Scholar]
  85. 85. 
    Imaeda N, Ando A, Takasu M, Matsubara T, Nishii N et al. 2018. Influences of swine leukocyte antigen haplotypes on serum antigen titers against swine erysipelas vaccine and traits of reproductive ability and meat production in a SLA-defined Duroc pigs. J. Vet. Med. Sci. 80:1662–68
    [Google Scholar]
  86. 86. 
    Bohórquez JA, Defaus S, Muñoz-González S, Perez-Simó M, Rosell R et al. 2017. A bivalent dendrimeric peptide bearing a T-cell epitope from foot-and-mouth disease virus protein 3A improves humoral response against classical swine fever virus. Virus Res 238:8–12 https://doi.org/10.1016/j.virusres.2017.05.020 Development of a novel vaccination strategy based on viral-specific peptides.
    [Crossref] [Google Scholar]
  87. 87. 
    Blanco E, Guerra B, de la Torre BG, Defaus S, Dekker A et al. 2016. Full protection of swine against foot-and-mouth disease by a bivalent B-cell epitope dendrimer peptide. Antiviral Res 129:74–80 https://doi.org/10.1016/j.antiviral.2016.03.005
    [Crossref] [Google Scholar]
  88. 88. 
    Cortey M, Arocena G, Ait-Ali T, Vidal A, Li Y et al. 2018. Analysis of the genetic diversity and mRNA expression level in porcine reproductive and respiratory syndrome virus vaccinated pigs that developed short or long viremias after challenge. Vet. Res. 49:19 https://doi.org/10.1186/s13567-018-0514-1
    [Crossref] [Google Scholar]
  89. 89. 
    Hess AS, Trible BR, Hess MK, Rowland RRR, Lunney JK et al. 2018. Genetic relationships of antibody response, viremia level and weight gain in pigs experimentally infected with porcine reproductive and respiratory syndrome virus. J. Anim. Sci. 96:3565–81 https://doi.org/10.1093/jas/sky229
    [Crossref] [Google Scholar]
  90. 90. 
    Walker LR, Jobman EE, Sutton KM, Wittler J, Johnson RK, Ciobanu DC 2019. Genome-wide association analysis for porcine reproductive and respiratory syndrome virus susceptibility traits in two genetic populations of pigs. J. Anim. Sci. 97:83253–61
    [Google Scholar]
  91. 91. 
    Yang N, Li J, Yang Q, Qiao J, Cui D et al. 2018. Reduced antigen presentation capability and modified inflammatory/immunosuppressive cytokine expression of induced monocyte-derived dendritic cells from peripheral blood of piglets infected with porcine circovirus type 2. Arch. Virol. 163:1231–39 https://doi.org/10.1007/s00705-018-3735-8
    [Crossref] [Google Scholar]
  92. 92. 
    Walker LR, Engle TB, Vu H, Tosky ER, Nonneman DJ et al. 2018. Synaptogyrin-2 influences replication of porcine circovirus 2. PLOS Genet 14:e1007750 https://doi.org/10.1371/journal.pgen.1007750
    [Crossref] [Google Scholar]
  93. 93. 
    Ando A, Shigenari A, Kojima-Shibata C, Nakajoh M, Suzuki K et al. 2016. Association of swine leukocyte antigen class II haplotypes and immune-related traits in a swine line selected for resistance to mycoplasmal pneumonia. Comp. Immunol. Microbiol. Infect. Dis. 48:33–40
    [Google Scholar]
  94. 94. 
    Zhang S, Yang J, Wang L, Li Z, Pang P, Li F 2018. SLA-11 mutations are associated with litter size traits in Large White and Chinese DIV pigs. Anim. Biotechnol. 30:212–18 https://doi.org/10.1080/10495398.2018.1471401
    [Crossref] [Google Scholar]
  95. 95. 
    Matsubara T, Takasu M, Imaeda N, Nishii N, Takashima S et al. 2018. Genetic association of swine leukocyte antigen class II haplotypes and body weight in Microminipigs. Asian-Australas. J. Anim. Sci. 3:163–66
    [Google Scholar]
  96. 96. 
    Demeure O, Sanchez MP, Riquet J, Iannuccelli N, Demars J et al. 2005. Exclusion of the swine leukocyte antigens as candidate region and reduction of the position interval for the Sus scrofa chromosome 7 QTL affecting growth and fatness. J. Anim. Sci. 83:1979–87
    [Google Scholar]
  97. 97. 
    Wei WH, Skinner TM, Anderson JA, Southwood OI, Plastow G et al. 2011. Mapping QTL in the porcine MHC region affecting fatness and growth traits in a Meishan/Large White composite population. Anim. Genet. 42:83–85
    [Google Scholar]
  98. 98. 
    Swindle MM, Makin A, Herron AJ, Clubb FJ Jr., Frazier KS 2012. Swine as models in biomedical research and toxicology testing. Vet. Pathol. 49:344–56
    [Google Scholar]
  99. 99. 
    Sachs DH, Leight G, Cone J, Schwarz S, Stuart L, Rosenberg S 1976. Transplantation in miniature swine. I. Fixation of the major histocompatibility complex. Transplantation 22:559–67
    [Google Scholar]
  100. 100. 
    Sykes M. 2018. IXA Honorary Member Lecture, 2017: the long and winding road to tolerance. Xenotransplantation 25:e12419 https://doi.org/10.1111/xen.12419
    [Crossref] [Google Scholar]
  101. 101. 
    Lee JH, Simond D, Hawthorne WJ, Walters SN, Patel AT et al. 2005. Characterization of the swine major histocompatibility complex alleles at eight loci in Westran pigs. Xenotransplantation 12:303–7
    [Google Scholar]
  102. 102. 
    Smith DM, Martens GW, Ho CS, Asbury JM 2005. DNA sequence based typing of swine leukocyte antigens in Yucatan miniature pigs. Xenotransplantation 12:481–88
    [Google Scholar]
  103. 103. 
    Miura K, Sahara H, Waki S, Kawai A, Sekijima M et al. 2016. Development of the intestinal transplantation model with major histocompatibility complex inbred CLAWN miniature swine. Transpl. Proc. 48:1315–19 https://doi.org/10.1016/j.transproceed.2016.01.023
    [Crossref] [Google Scholar]
  104. 104. 
    Figueiredo C, Carvalho Oliveira M, Chen-Wacker C, Jansson K, Höffler K et al. 2019. Immunoengineering of the vascular endothelium to silence MHC expression during normothermic ex vivo lung perfusion. Hum. Gene Ther. 30:485–96
    [Google Scholar]
  105. 105. 
    Zinne N, Krueger M, Hoeltig D, Tuemmler B, Boyle EC et al. 2018. Treatment of infected lungs by ex vivo perfusion with high dose antibiotics and autotransplantation: a pilot study in pigs. PLOS ONE 13:e0193168 https://doi.org/10.1371/journal.pone.0193168
    [Crossref] [Google Scholar]
  106. 106. 
    Lassiter R, Wang Y, Fang X, Winn M, Ghaffari A et al. 2017. A model of acute renal allograft rejection in outbred Yorkshire piglets. Transpl. Immunol. 42:40–46
    [Google Scholar]
  107. 107. 
    Wang Y, Merchen TD, Fang X, Lassiter R, Ho CS et al. 2018. Regulation of indoleamine 2,3 dioxygenase and its role in a porcine model of acute kidney allograft rejection. J. Investig. Med. 66:1109–17
    [Google Scholar]
  108. 108. 
    Zachary AA, Leffell MS. 2016. HLA mismatching strategies for solid organ transplantation—a balancing act. Front. Immunol. 7:575
    [Google Scholar]
  109. 109. 
    Hernandez-Fuentes MP, Franklin C, Rebollo-Mesa I, Mollon J, Delaney F et al. 2018. Long- and short-term outcomes in renal allografts with deceased donors: a large recipient and donor genome-wide association study. Am. J. Transplant. 18:1370–79
    [Google Scholar]
  110. 110. 
    Kirkman RL, Colvin RB, Flye MW, Leight GS, Rosenberg SA et al. 1979. Transplantation in miniature swine. VI. Factors influencing survival of renal allografts. Transplantation 28:18–23
    [Google Scholar]
  111. 111. 
    Scalea JR, Okumi M, Villani V, Shimizu A, Nishimura H et al. 2014. Abrogation of renal allograft tolerance in MGH miniature swine: the role of intra-graft and peripheral factors in long-term tolerance. Am. J. Transplant. 14:2001–10 https://doi.org/10.1111/ajt.12816
    [Crossref] [Google Scholar]
  112. 112. 
    Fishman JA, Sachs DH, Yamada K, Wilkinson RA 2018. Absence of interaction between porcine endogenous retrovirus and porcine cytomegalovirus in pig-to-baboon renal xenotransplantation in vivo. Xenotransplantation 25:e12395 https://doi.org/10.1111/xen.12395
    [Crossref] [Google Scholar]
  113. 113. 
    Schenk M, Matar AJ, Hanekamp I, Hawley RJ, Huang CA, Duran-Struuck R 2019. Development of a transplantable GFP+ B-cell lymphoma tumor cell line from MHC-defined miniature swine: potential for a large animal tumor model. Front. Oncol. 9:209 https://doi.org/10.3389/fonc.2019.00209
    [Crossref] [Google Scholar]
  114. 114. 
    Smith DM, Newhouse M, Naziruddin B, Kresie L 2006. Blood groups and transfusions in pigs. Xenotransplantation 13:186–94
    [Google Scholar]
  115. 115. 
    Kwak HH, Park KM, Teotia PK, Lee GS, Lee ES et al. 2013. Acute rejection after swine leukocyte antigen-matched kidney allo-transplantation in cloned miniature pigs with different mitochondrial DNA-encoded minor histocompatibility antigen. Transplant. Proc. 45:1754–60
    [Google Scholar]
  116. 116. 
    Tiercy JM. 2016. How to select the best available related or unrelated donor of hematopoietic stem cells. Haematologica 101:680–87
    [Google Scholar]
  117. 117. 
    Bertaina A, Andreani M. 2018. Major histocompatibility complex and hematopoietic stem cell transplantation: beyond the classical HLA polymorphism. Int. J. Mol. Sci. 19:2621 https://doi.org/10.3390/ijms19020621
    [Crossref] [Google Scholar]
  118. 118. 
    Pennington LR, Sakamoto K, Popitz-Bergez FA, Pescovitz MD, McDonough MA et al. 1988. Bone marrow transplantation in miniature swine. I. Development of the model. Transplantation 45:21–26
    [Google Scholar]
  119. 119. 
    Duran-Struuck R, Huang CA, Orf K, Bronson RT, Sachs DH, Spitzer TR 2015. Miniature swine as a clinically relevant model of graft-versus-host disease. Comp. Med. 65:429–43
    [Google Scholar]
  120. 120. 
    Powell EJ, Graham J, Ellinwood NM, Hostetter J, Yaeger M et al. 2017. T cell lymphoma and leukemia in severe combined immunodeficiency pigs following bone marrow transplantation: a case report. Front. Immunol. 8:813
    [Google Scholar]
  121. 121. 
    Kueckelhaus M, Fischer S, Seyda M, Bueno EM, Aycart MA et al. 2016. Vascularized composite allotransplantation: current standards and novel approaches to prevent acute rejection and chronic allograft deterioration. Transpl. Int. 29:655–62
    [Google Scholar]
  122. 122. 
    Ng ZY, Lellouch AG, Rosales IA, Geoghegan L, Gama AR et al. 2019. Graft vasculopathy of vascularized composite allografts in humans: a literature review and retrospective study. Transpl. Int. 32:831–38 https://doi.org/10.1111/tri.13421
    [Crossref] [Google Scholar]
  123. 123. 
    Cetrulo CL Jr., Torabi R, Scalea JR, Shimizu A, Leto Barone AA et al. 2013. Vascularized composite allograft transplant survival in miniature swine: Is MHC tolerance sufficient for acceptance of epidermis. Transplantation 96:966–74
    [Google Scholar]
  124. 124. 
    Ibrahim Z, Cooney DS, Shores JT, Sacks JM, Wimmers EG et al. 2013. A modified heterotopic swine hind limb transplant model for translational vascularized composite allotransplantation (VCA) research. J. Vis. Exp. 2013:8050475 https://doi.org/10.3791/50475
    [Crossref] [Google Scholar]
  125. 125. 
    Leonard DA, Kurtz JM, Mallard C, Albritton A, Duran-Struuck R et al. 2014. Vascularized composite allograft tolerance across MHC barriers in a large animal model. Am. J. Transplant. 14:343–55
    [Google Scholar]
  126. 126. 
    Shanmugarajah K, Powell H, Leonard DA, Mallard C, Albritton A et al. 2017. The effect of MHC antigen matching between donors and recipients on skin tolerance of vascularized composite allografts. Am. J. Transplant. 17:1729–41
    [Google Scholar]
  127. 127. 
    Fries CA, Lawson SD, Wang LC, Spencer JR, Roth M et al. 2019. composite graft pretreatment with hydrogen sulfide delays the onset of acute rejection. Ann. Plast. Surg. 82:452–58
    [Google Scholar]
  128. 128. 
    Kotsougiani D, Hundepool CA, Willems JI, Friedrich P, Shin AY, Bishop AT 2017. Surgical angiogenesis in porcine tibial allotransplantation: a new large animal bone vascularized composite allotransplantation model. J. Vis. Exp. 126:e55238 https://doi.org/10.3791/55238
    [Crossref] [Google Scholar]
  129. 129. 
    Kotsougiani D, Willems JI, Shin AY, Friedrich PF, Hundepool CA, Bishop AT 2018. A new porcine vascularized tibial bone allotransplantation model. Anatomy and surgical technique. Microsurgery 38:195–202
    [Google Scholar]
  130. 130. 
    Fries CA, Lawson SD, Wang LC, Slaughter KV, Vemula PK et al. 2019. Graft-implanted, enzyme responsive, tacrolimus-eluting hydrogel enables long-term survival of orthotopic porcine limb vascularized composite allografts: a proof of concept study. PLOS ONE 14:e0210914
    [Google Scholar]
  131. 131. 
    Malliaras K, Smith RR, Kanazawa H, Yee K, Seinfeld J et al. 2013. Validation of contrast-enhanced magnetic resonance imaging to monitor regenerative efficacy after cell therapy in a porcine model of convalescent myocardial infarction. Circulation 128:2764–75
    [Google Scholar]
  132. 132. 
    Yee K, Malliaras K, Kanazawa H, Tseliou E, Cheng K et al. 2014. Allogeneic cardiospheres delivered via percutaneous transendocardial injection increase viable myocardium, decrease scar size, and attenuate cardiac dilatation in porcine ischemic cardiomyopathy. PLOS ONE 9:e113805
    [Google Scholar]
  133. 133. 
    Kanazawa H, Tseliou E, Dawkins JF, De Couto G, Gallet R et al. 2016. Durable benefits of cellular postconditioning: long-term effects of allogeneic cardiosphere-derived cells infused after reperfusion in pigs with acute myocardial infarction. J. Am. Heart Assoc. 5:2e002796
    [Google Scholar]
  134. 134. 
    Hickey RD, Mao SA, Glorioso J, Elgilani F, Amiot B et al. 2016. Curative ex vivo liver-directed gene therapy in a pig model of hereditary tyrosinemia type 1. Sci. Transl. Med. 8:349ra99
    [Google Scholar]
  135. 135. 
    Strnadel J, Carromeu C, Bardy C, Navarro M, Platoshyn O et al. 2018. Survival of syngeneic and allogeneic iPSC-derived neural precursors after spinal grafting in minipigs. Sci. Transl. Med. 10:440eaam6651Illustrates the potential of porcine-derived induced pluripotent stem cells in allogeneic transplantation research.
    [Google Scholar]
  136. 136. 
    Tambur AR, Campbell P, Claas FH, Feng S, Gebel HM et al. 2018. Sensitization in transplantation: assessment of risk (STAR) 2017 working group meeting report. Am. J. Transplant. 18:71604–14
    [Google Scholar]
  137. 137. 
    Tinckam KJ, Chandraker A. 2006. Mechanisms and role of HLA and non-HLA alloantibodies. Clin. J. Am. Soc. Nephrol. 1:404–14
    [Google Scholar]
  138. 138. 
    Fischer K, Kind A, Schnieke A 2018. Assembling multiple xenoprotective transgenes in pigs. Xenotransplantation 25:e12431 https://doi.org/10.1111/xen.12431
    [Crossref] [Google Scholar]
  139. 139. 
    Reyes LM, Estrada JL, Wang ZY, Blosser RJ, Smith RF et al. 2014. Creating class I MHC-null pigs using guide RNA and the Cas9 endonuclease. J. Immunol. 193:5751–57
    [Google Scholar]
  140. 140. 
    Martens GR, Reyes LM, Li P, Butler JR, Ladowski JM et al. 2017. Humoral reactivity of renal transplant-waitlisted patients to cells from GGTA1/CMAH/B4GalNT2, and SLA class I knockout pigs. Transplantation 101:e86–e92
    [Google Scholar]
  141. 141. 
    Abicht JM, Sfriso R, Reichart B, Längin M, Gahle K et al. 2018. Multiple genetically modified GTKO/hCD46/HLA-E/hβ2-mg porcine hearts are protected from complement activation and natural killer cell infiltration during ex vivo perfusion with human blood. Xenotransplantation 25:e12390 https://doi.org/10.1111/xen.12390 Potential for genetically engineered pigs in xenogeneic transplantation.
    [Crossref] [Google Scholar]
  142. 142. 
    Estrada JL, Martens G, Li P, Adams A, Newell KA et al. 2015. Evaluation of human and non-human primate antibody binding to pig cells lacking GGTA1/CMAH/β4GalNT2 genes. Xenotransplantation 22:194–202
    [Google Scholar]
  143. 143. 
    Issa N, Cosio FG, Gloor JM, Sethi S, Dean PG et al. 2008. Transplant glomerulopathy: risk and prognosis related to anti-human leukocyte antigen class II antibody levels. Transplantation 86:681–85
    [Google Scholar]
  144. 144. 
    Tambur AR, Rosati J, Roitberg S, Glotz D, Friedewald JJ, Leventhal JR 2014. Epitope analysis of HLA-DQ antigens: What does the antibody see. Transplantation 98:157–66
    [Google Scholar]
  145. 145. 
    Tambur AR. 2016. HLA-DQ antibodies: Are they real? Are they relevant? Why so many?. Curr. Opin. Organ Transplant. 21:441–46
    [Google Scholar]
  146. 146. 
    Díaz Varela I, Sánchez Mozo P, Centeno Cortés A, Alonso Blanco C, Valdés Cañedo F 2003. Cross-reactivity between swine leukocyte antigen and human anti-HLA-specific antibodies in sensitized patients awaiting renal transplantation. J. Am. Soc. Nephrol. 14:2677–83
    [Google Scholar]
  147. 147. 
    Ladowski JM, Martens GR, Reyes LM, Wang ZY, Eckhoff DE et al. 2018. Examining the biosynthesis and xenoantigenicity of class II swine leukocyte antigen proteins. J. Immunol. 200:2957–64
    [Google Scholar]
  148. 148. 
    Ladowski JM, Reyes LM, Martens GR, Butler JR, Wang ZY et al. 2018. Swine leukocyte antigen class II is a xenoantigen. Transplantation 102:249–54
    [Google Scholar]
  149. 149. 
    Endale Ahanda M-L, Fritz ER, Estellé J, Hu Z-L, Madsen O et al. 2012. Prediction of altered 3′-UTR miRNA-binding sites from RNA-seq data: the swine leukocyte antigen complex (SLA) as a model region. PLOS ONE 7:e48607 https://doi.org/10.1371/journal.pone.0048607
    [Crossref] [Google Scholar]
  150. 150. 
    Herrera-Uribe J, Zaldívar-López S, Aguilar C, Luque C, Bautista R et al. 2018. Regulatory role of microRNA in mesenteric lymph nodes after Salmonella Typhimurium infection. Vet. Res. 49:9 https://doi.org/10.1186/s13567-018-0506-1
    [Crossref] [Google Scholar]
  151. 151. 
    Zhang K, Ge L, Dong S, Liu Y, Wang D et al. 2019. Global miRNA, lncRNA, and mRNA transcriptome profiling of endometrial epithelial cells reveals genes related to porcine reproductive failure caused by porcine reproductive and respiratory syndrome virus. Front. Immunol. 10:1221 https://doi.org/10.3389/fimmu.2019.01221 Genomic regulation of SLA genes including noncoding RNAs and regulatory variants.
    [Crossref] [Google Scholar]
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