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Immunogenetics

, Volume 71, Issue 1, pp 49–59 | Cite as

Polymorphism of duck MHC class molecules

  • Lin ZhangEmail author
  • Dongmei Lin
  • Sen Yu
  • Junping Bai
  • Wanchun Jiang
  • Wenzheng Su
  • Yanyan Huang
  • Shaohua Yang
  • Jiaqiang WuEmail author
Original Article
  • 115 Downloads

Abstract

Major histocompatibility complex class I (MHC I) molecules are critically involved in defense against pathogens, and their high polymorphism is advantageous to a range of immune responses, especially in duck displaying biased expression of one MHC I gene. Here, we examined MHC I polymorphism in two duck (Anas platyrhynchos) breeds from China: Shaoxing (SX) and Jinding (JD). Twenty-seven unique UAA alleles identified from the MHC I genes of these breeds were analyzed concerning amino acid composition, homology, and phylogenetic relationships. Based on amino acid sequence homology, allelic groups of Anas platyrhynchos MHC I (Anpl-MHC I) were established and their distribution was analyzed. Then, highly variable sites (HVSs) in peptide-binding domains (PBD) were estimated and located in the three-dimensional structure of Anpl-MHC I. The UAA alleles identified showed high polymorphism, based on full-length sequence homology. By adding the alleles found here to known Anpl-MHC I genes from domestic ducks, they could be divided into 17 groups and four novel groups were revealed for SX and JD ducks. The UAA alleles of the two breeds were not divergent from the MHC I of other duck breeds, and HVSs were mostly located in the peptide-binding groove (PBG), suggesting that they might determine peptide-binding characteristics and subsequently influence peptide presentation and recognition. The results from the present study enrich Anpl-MHC I polymorphism data and clarify the distribution of alleles with different peptide-binding specificities, which might also accelerate effective vaccine development and help control various infections in ducks.

Keywords

Duck Major histocompatibility class I Polymorphism Allelic group Peptide 

Notes

Acknowledgements

This study was carried out with financial support from the 13th 5-Year National Key Research Project of China (2016YFD0500106), the National Science and Technology Pillar Program during the 12th 5-Year Plan Period of China (2015BAD12B03), the Taishan Scholar Project Funds, Shandong Province (ts201511069), and the Agricultural Science and Technology Innovation Project Funds of Shandong Academy of Agricultural Science (CXGC2018E10 and CXGC2016B14).

Author’s contributions

Conceived and designed the experiments: L Zhang, D Lin, and J Wu. Suggested methodologies: L Zhang, D Lin, S Yu, W Jiang, and J Wu. Gene clone and analysis: S Yu, J Bai, and W Jiang. Allelic group division and HVS location: L Zhang and Y Huang. Provided the resources: D Lin, W Su, and S Yang. Wrote the paper: L Zhang and D Lin. Reviewed the paper: W Jiang and J Wu. All authors approved the final version of the paper.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All animal experiments were performed in strict accordance with the guidelines of the Institutional Animal Care and Use Committee of Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences (IACC20060101, January 1, 2006).

References

  1. Bacon LD, Witter RL (1993) Influence of B-haplotype on the relative efficacy of Marek’s disease vaccines of different serotypes. Avian Dis 37(1):53–59Google Scholar
  2. Bacon LD, Witter RL, Crittenden LB, Fadly A, Motta J (1981) B-haplotype influence on Marek’s disease, Rous sarcoma, and lymphoid leucosis virus-induced tumors in chickens. Poult Sci 60(6):1132–1139Google Scholar
  3. Bingham J, Green DJ, Lowther S, Klippel J, Burggraaf S, Anderson DE, Wibawa H, Hoa DM, Long NT, Vu PP, Middleton DJ, Daniels PW (2009) Infection studies with two highly pathogenic avian influenza strains (Vietnamese and Indonesian) in Pekin ducks (Anas platyrhynchos), with particular reference to clinical disease, tissue tropism and viral shedding. Avian Pathol 38(4):267–278Google Scholar
  4. Bjorkman PJ, Parham P (1990) Structure, function, and diversity of class I major histocompatibility complex molecules. Annu Rev Biochem 59(1):253–288Google Scholar
  5. Borbulevych OY, Piepenbrink KH, Baker BM (2011) Conformational melding permits a conserved binding geometry in TCR recognition of foreign and self molecular mimics. J Immunol 186(5):2950–2958Google Scholar
  6. Chan WF, Parks-Dely JA, Magor BG, Magor KE (2016) The minor MHC class I gene UDA of ducks is regulated by let-7 microRNA. J Immunol 197(4):1212–1220Google Scholar
  7. Falk K, Rotzschke O, Stevanovic S, Jung G, Rammensee HG (1991) Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351(6324):290–296Google Scholar
  8. Fan SH, Wang YL, Wang S, Wang X, Wu YN, Li ZB, Zhang NZ, Xia C (2018) Polymorphism and peptide-binding specificities of porcine major histocompatibility complex (MHC) class I molecules. Mol Immunol 93:236–245Google Scholar
  9. Fleming-Canepa X, Jensen SM, Mesa CM, Diaz-Satizabal L, Roth AJ, Parks-Dely JA, Moon DA, Wong JP, Evseev D, Gossen DA, Tetrault DG, Magor KE (2016) Extensive allelic diversity of MHC class I in wild mallard ducks. J Immunol 197(3):783–794Google Scholar
  10. Goto RM, Wang YJ, Taylor RL, Wakenell PS, Hosomichi K, ShiinaT BCS, Briles WE, Miller MM (2009) BG1 has a major role in MHC-linked resistance to malignant lymphoma in the chicken. Proc Natl Acad Sci USA 106(39):16740–16745Google Scholar
  11. Hazes B, Dijkstra BW (1988) Model building of disulfide bonds in proteins with known three-dimensional structure. Protein Eng 2(2):119–125Google Scholar
  12. Hepkema BG, Blankert JJ, Albers GA, Tilanus MG, Egberts E, van der Zijpp AJ, Hensen EJ (1993) Mapping of susceptibility to Marek’s disease within the major histocompatibility (B) complex by refined typing of white leghorn chickens. Anim Genet 24(4):283–287Google Scholar
  13. Jondal M, Schirmbeck R, Reimann J (1996) MHC class I-restricted CTL responses to exogenous antigens. Immunity 5(4):295–302Google Scholar
  14. Kabat EA, Wu TT, Bilofsky H (1997) Unusual distributions of amino acids in complementarity-determining (hypervariable) segments of heavy and light chains of immunoglobulins and their possible roles in specificity of antibody-combining sites. J Biol Chem 252(19):6609–6616Google Scholar
  15. Kane K, Clark WR (1984) The role of class I MHC products in polyclonal activation of CTL function. J Immunol 133(6):2857–2863Google Scholar
  16. Kaufman J (1999) Co-evolving genes in MHC haplotypes: the “rule” for non-mammalian vertebrates? Immunogenetics 50(3–4):228–236Google Scholar
  17. Kaufman J, Andersen R, Avila D, Engberg J, Lambris J, Salomonsen J, Welinder K, Skjødt K (1992) Different features of the MHC class I heterodimer have evolved at different rates: chicken B-F and beta 2-microglobulin sequences reveal invariant surface residues. J Immunol 148(5):1532–1546Google Scholar
  18. Kaufman J, Volk H, Wallny HJ (1995) A “minimal essential Mhc” and an“unrecognized Mhc”: two extremes in selection for polymorphism. Immunol Rev 143(1):63–88Google Scholar
  19. Kaufman J, Milne S, Gobel TW, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401(6756):923–925Google Scholar
  20. Klein J, Rammensee HG, Nagy ZA (1983) The major histocompatibility complex and self and non-self differentiation through the immune system. Die Naturwissenschaften 70(6):265–271Google Scholar
  21. Koch M, Camp S, Collen T, Avila D, Salomonsen J, Wallny HJ, van Hateren A, Hunt L, Jacob JP, Johnston F, Marston DA, Shaw I, Dunbar PR, Cerundolo V, Jones EY, Kaufman J (2007) Structures of an MHC class I molecule from B21 chickens illustrate promiscuous peptide binding. Immunity 27(6):885–899Google Scholar
  22. Li N, Wang Y, Li R, Liu JY, Zhang JZ, Cai YM, Liu SD, Chai TJ, Wei LM (2015) Immune responses of ducks infected with duck Tembusu virus. Front Microbiol 6:425Google Scholar
  23. Liang QL, Luo J, Zhou K, Dong JX, He HX (2011) Immune-related gene expression in response to H5N1 avian influenza virus infection in chicken and duck embryonic fibroblasts. Mol Immunol 48(6–7):924–930Google Scholar
  24. Lie WR, Myers NB, Connolly JM, Gorka J, Lee DR, Hansen TH (1991) The specific binding of peptide ligand to Ld class I major histocompatibility complex molecules determines their antigenic structure. J Exp Med 173(2):449–459Google Scholar
  25. Liu WJ, Kong ZJ, Li HY, Liu ZQ, Yang SH, Huang YY, Zhang XM, Zhang L, Wu JQ (2017) Comparison of host innate immune response of chicken (Gallus gallus) and duck (Anas platyrhynchos) infected with duck-origin Newcastle disease virus. J Agric Biotechnol 25(2):307–315Google Scholar
  26. McKenzie LM, Pecon-Slattery J, Carrington M, O’Brien SJ (1999) Taxonomic hierarchy of HLA class I allele sequences. Genes Immun 1(2):120–129Google Scholar
  27. McMichael AJ, Gotch FM, Noble GR, Beare PA (1983) Cytotoxic T-cell immunity to influenza. N Engl J Med 309(1):13–17Google Scholar
  28. Mesa CM, Thulien KJ, Moon DA, Veniamin SM, Magor KE (2004) The dominant MHC class I gene is adjacent to the polymorphic TAP2 gene in the duck, Anas platyrhynchos. Immunogenetics 56(3):192–203Google Scholar
  29. Moon DA, Veniamin SM, Parks-Dely JA, Magor KE (2005) The MHC of the duck (Anas platyrhynchos) contains five differentially expressed MHC genes. J Immunol 175(10):6702–6712Google Scholar
  30. Nejentsev S, Howson JMM, Walker NM, Szeszko J, Field SF, Stevens HE, Reynolds P, Hardy M, King E, Masters J, HulmeJ MLM, Smyth D, Bailey R, Cooper JD, Ribas G, Campbell RD, Clayton DG, Todd JA, Welcome Trust Case Control Consortium (2007) Localization of type 1 diabetes susceptibility to the MHC class I genes HLA-B and HLA-A. Nature 450(7171):887–892Google Scholar
  31. Petersen J, Wurzbacher SJ, Williamson NA, Ramarathinam SH, Reid HH, Nair AKN, Zhao AY, Nastovska R, Rudge G, Rossjohn J, Purcell AW (2009) Phosphorylated self-peptides alter human leukocyte antigen class I-restricted antigen presentation and generate tumor-specific epitopes. Proc Natl Acad Sci U S A 106(8):2776–2781Google Scholar
  32. Plachy J, Benda V (1981) Location of the gene responsible for Rous sarcoma regression in the B-F region of the B complex (MHC) of the chicken. Folia Biol (Praha) 27(5):363–368Google Scholar
  33. Plachy J, Pink JR, Hala K (1992) Biology of the chicken MHC (B complex). Crit Rev Immunol 12(1–2):47–79Google Scholar
  34. Rawle FC, Knowles BB, Ricciardi RP, Brahmacheri V, Duerksen-Hughes P, Wold WS, Gooding LR (1991) Specificity of the mouse cytotoxic T lymphocyte response to adenovirus 5. E1A is immunodominant in H-2b, but not in H-2d or H-2k mice. J Immunol 146(11):3977–3984Google Scholar
  35. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425Google Scholar
  36. Shaw I, Powell TJ, Marston DA, Baker K, van Hateren A, Riegert P, Wiles MV, Milne S, Beck S, Kaufman J (2007) Different evolutionary histories of the two classical class I genes BF1 and BF2 illustrate drift and selection within the stable MHC haplotypes of chickens. J Immunol 178(9):5744–5752Google Scholar
  37. Takeshima SN, Sarai Y, Saitou N, Aida Y (2009) MHC class II DR classification based onantigen-binding groove natural selection. Biochem Biophys Res Commun 385(2):137–142Google Scholar
  38. Walker BA, van Hateren A, Milne S, Beck S, Kaufman J (2005) Chicken TAP genes differ from their human orthologues in locus organisation, size, sequence features and polymorphism. Immunogenetics 57(3–4):232–247Google Scholar
  39. Wallny HJ, Avila D, Hunt LG, Powell TJ, Riegert P, Salomonsen J, Skjodt K, Vainio O, Vilbois F, Wiles MV, Kaufman J (2006) Peptide motifs of the single dominantly expressed class I molecule explain the striking MHC-determined response to Rous sarcoma virus in chickens. Proc Natl Acad Sci U S A 103(5):1434–1439Google Scholar
  40. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25(9):1189–1191Google Scholar
  41. Wu YN, Wang JY, Fan SHH, Chen R, Liu YJ, Zhang JH, Yuan HY, Liang RY, Zhang NZ, Xia C (2017) Structural definition of duck major histocompatibility complex class I molecules that might explain efficient cytotoxic T lymphocyte immunity to influenza a virus. J Virol 91(14):e02511–e02516Google Scholar
  42. Xia C, Lin CY, Xu GX, Hu TJ, Yang TY (2004) cDNA cloning and genomic structure of the duck (Anas platyrhynchos) MHC class I gene. Immunogenetics 56(4):304–309Google Scholar
  43. Xiao GM, Deng YB (2005) Duck cultivation. Hunan science and technology press, HunanGoogle Scholar
  44. Yan RQ, Li XS, Yang TY, Xia C (2005) Characterization of BF2 and β2m in three Chinese chicken lines. Vet Immunol Immunopathol 108(3):417–425Google Scholar
  45. Zhang W, Collins A, Morton NE (2004) Does haplotype diversity predict power for association mapping of disease susceptibility? Hum Genet 115(2):157–164Google Scholar
  46. Zhang JH, Chen Y, Qi JX, Gao F, Liu Y, Liu J, Zhou X, Kaufman J, Xia C, Gao GF (2012) Narrow groove and restricted anchors of MHC class I molecule BF2 *0401 plus peptide transporter restriction can explain disease susceptibility of B4 chickens. J Immunol 189(9):4478–4487Google Scholar
  47. Zhang L, Liu WJ, Wu JQ, Xu ML, Kong ZHJ, Huang YY, Yang SHH (2017) Characterization of duck (Anas platyrhynchos) MHC class I gene in two duck lines. J Genet 96(2):371–375Google Scholar
  48. Zhou M, Xu Y, Lou Z, Cole DK, Li X, Liu Y, Tien P, Rao Z, Gao GF (2004) Complex assembly: crystallization and preliminary X-ray crystallographic studies of MHC H-2Kd complexed with an HBV-core nonapeptide. Acta Crystallogr F Struct Biol Commun 60(Pt8):1473–1475Google Scholar
  49. Zinkernagel RM, Pfau CJ, Hengartner H, Althage A (1985) Susceptibility to murine lymphocytic choriomeningitis maps to class I MHC genes? A model for MHC/disease associations. Nature 316(6031):814–817Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Lin Zhang
    • 1
    Email author
  • Dongmei Lin
    • 2
  • Sen Yu
    • 1
  • Junping Bai
    • 1
    • 2
  • Wanchun Jiang
    • 2
  • Wenzheng Su
    • 1
  • Yanyan Huang
    • 1
  • Shaohua Yang
    • 1
  • Jiaqiang Wu
    • 1
    Email author
  1. 1.Shandong Key Laboratory of Disease Control and Breeding, Institute of Animal Science and Veterinary MedicineShandong Academy of Agricultural ScienceJinanChina
  2. 2.College of Life Sciences and Food EngineeringHebei University of EngineeringHandanChina

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