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Distribution of ancient α1 and α2 domain lineages between two classical MHC class I genes and their alleles in grass carp

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Abstract

Major histocompatibility complex (MHC) class I molecules play a crucial role in the immune response by binding and presenting pathogen-derived peptides to specific CD8+ T cells. From cDNA of 20 individuals of wild grass carp (Ctenopharyngodon idellus), we could amplify one or two alleles each of classical MHC class I genes Ctid-UAA and Ctid-UBA. In total, 27 and 22 unique alleles of Ctid-UAA and Ctid-UBA were found. The leader, α1, transmembrane and cytoplasmic regions distinguish between Ctid-UAA and Ctid-UBA, and their encoded α1 domain sequences belong to the ancient lineages α1-V and α1-II, respectively, which separated several hundred million years ago. However, Ctid-UAA and Ctid-UBA share allelic lineage variation in their α2 and α3 sequences, in a pattern suggestive of past interlocus recombination events that transferred α2+α3 fragments. The allelic Ctid-UAA and Ctid-UBA variation involves ancient variation between domain lineages α2-I and α2-II, which in the present study was dated back to before the ancestral separation of teleost fish and spotted gar (> 300 million years ago). This is the first report with compelling evidence that recombination events combining different ancient α1 and α2 domain lineages had a major impact on the allelic variation of two different classical MHC class I genes within the same species.

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References

  • Aoyagi K, Dijkstra JM, Xia C, Denda I, Ototake M, Hashimoto K, Nakanishi T (2002) Classical MHC class I genes composed of highly divergent sequence lineages share a single locus in rainbow trout (Oncorhynchus mykiss). J Immunol 168:260–273

    Article  CAS  PubMed  Google Scholar 

  • Bingulac-Popovic J, Figueroa F, Sato A, Talbot WS, Johnson SL, Gates M, Postlethwait JH, Klein J (1997) Mapping of mhc class I and class II regions to different linkage groups in the zebrafish, Danio rerio. Immunogenetics 46:129–134

    Article  CAS  PubMed  Google Scholar 

  • Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC (1987) The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329:512–518

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Jia Z, Zhang T, Zhang N, Lin C, Gao F, Wang L, Li X, Jiang Y, Li X, Gao GF, Xia C (2010) MHC class I presentation and regulation by IFN in bony fish determined by molecular analysis of the class I locus in grass carp. J Immunol 185:2209–2221

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Zhang N, Qi J, Chen R, Dijkstra JM, Li X, Wang Z, Wang J, Wu Y, Xia C (2017) The structure of the MHC class I molecule of bony fishes provides insights into the conserved nature of the antigen-presenting system. J Immunol 199:3668–3678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dijkstra JM, Kiryu I, Yoshiura Y, Kumánovics A, Kohara M, Hayashi N, Ototake M (2006) Polymorphism of two very similar MHC class Ib loci in rainbow trout (Oncorhynchus mykiss). Immunogenetics 58:152–167

    Article  CAS  PubMed  Google Scholar 

  • Dijkstra JM, Katagiri T, Hosomichi K, Yanagiya K, Inoko H, Ototake M, Aoki T, Hashimoto K, Shiina T (2007) A third broad lineage of major histocompatibility complex (MHC) class I in teleost fish; MHC class II linkage and processed genes. Immunogenetics 59:305–321

    Article  CAS  PubMed  Google Scholar 

  • Dijkstra JM, Grimholt U, Leong J, Koop BF, Hashimoto K (2013) Comprehensive analysis of MHC class II genes in teleost fish genomes reveals dispensability of the peptide-loading DM system in a large part of vertebrates. BMC Evol Biol 13:260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dirscherl H, McConnell SC, Yoder JA, de Jong JL (2014) The MHC class I genes of zebrafish. Dev Comp Immunol 46:11–23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan S, Wang Y, Wang S, Wang X, Wu Y, Li Z, Zhang N, Xia C (2018) Polymorphism and peptide-binding specificities of porcine major histocompatibility complex (MHC) class I molecules. Mol Immunol 93:236–245

    Article  CAS  PubMed  Google Scholar 

  • Figueroa F, Günther E, Klein J (1988 Sep 15) MHC polymorphism pre-dating speciation. Nature. 335(6187):265–267

    Article  CAS  PubMed  Google Scholar 

  • Grimholt U, Hordvik I, Fosse VM, Olsaker I, Endresen C, Lie O (1993) Molecular cloning of major histocompatibility complex class I cDNAs from Atlantic salmon (Salmo salar). Immunogenetics 37:469–473

    Article  CAS  PubMed  Google Scholar 

  • Grimholt U, Tsukamoto K, Azuma T, Leong J, Koop BF, Dijkstra JM (2015) A comprehensive analysis of teleost MHC class I sequences. BMC Evol Biol 15:32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hansen JD, Strassburger P, Du Pasquier L (1996) Conservation of an alpha 2 domain within the teleostean world, MHC class I from the rainbow trout Oncorhynchus mykiss. Dev Comp Immunol 20:417–425

    Article  CAS  PubMed  Google Scholar 

  • Hansen JD, Strassburger P, Thorgaard GH, Young WP, Du Pasquier L (1999) Expression, linkage, and polymorphism of MHC-related genes in rainbow trout, Oncorhynchus mykiss. J Immunol 163:774–786

    CAS  PubMed  Google Scholar 

  • Hashimoto K, Nakanishi T, Kurosawa Y (1990) Isolation of carp genes encoding major histocompatibility complex antigens. Proc Natl Acad Sci U S A 87:6863–6867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill AV (2001) The genomics and genetics of human infectious disease susceptibility. Annu Rev Genomics Hum Genet 2:373–400

    Article  CAS  PubMed  Google Scholar 

  • Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, McLaren S, Sealy I, Caccamo M, Churcher C, Scott C, Barrett JC, Koch R, Rauch GJ, White S, Chow W, Kilian B, Quintais LT, Guerra-Assuncao JA, Zhou Y, Gu Y, Yen J, Vogel JH, Eyre T, Redmond S, Banerjee R, Chi J, Fu B, Langley E, Maguire SF, Laird GK, Lloyd D, Kenyon E, Donaldson S, Sehra H, Almeida-King J, Loveland J, Trevanion S, Jones M, Quail M, Willey D, Hunt A, Burton J, Sims S, McLay K, Plumb B, Davis J, Clee C, Oliver K, Clark R, Riddle C, Elliot D, Threadgold G, Harden G, Ware D, Begum S, Mortimore B, Kerry G, Heath P, Phillimore B, Tracey A, Corby N, Dunn M, Johnson C, Wood J, Clark S, Pelan S, Griffiths G, Smith M, Glithero R, Howden P, Barker N, Lloyd C, Stevens C, Harley J, Holt K, Panagiotidis G, Lovell J, Beasley H, Henderson C, Gordon D, Auger K, Wright D, Collins J, Raisen C, Dyer L, Leung K, Robertson L, Ambridge K, Leongamornlert D, McGuire S, Gilderthorp R, Griffiths C, Manthravadi D, Nichol S, Barker G et al (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kiryu I, Dijkstra JM, Sarder RI, Fujiwara A, Yoshiura Y, Ototake M (2005) New MHC class Ia domain lineages in rainbow trout (Oncorhynchus mykiss) which are shared with other fish species. Fish Shellfish Immunol 18:243–254

    Article  CAS  PubMed  Google Scholar 

  • Kruiswijk CP, Hermsen TT, Westphal AH, Savelkoul HF, Stet RJ (2002) A novel functional class I lineage in zebrafish (Danio rerio), carp (Cyprinus carpio), and large barbus (Barbus intermedius) showing an unusual conservation of the peptide binding domains. J Immunol 169:1936–1947

    Article  CAS  PubMed  Google Scholar 

  • Lukacs MF, Harstad H, Bakke HG, Beetz-Sargent M, McKinnel L, Lubieniecki KP, Koop BF, Grimholt U (2010) Comprehensive analysis of MHC class I genes from the U-, S-, and Z-lineages in Atlantic salmon. BMC Genomics 11:154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumura M, Fremont DH, Peterson PA, Wilson IA (1992 Aug 14) Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science. 257(5072):927–934

    Article  CAS  PubMed  Google Scholar 

  • McConnell SC, Restaino AC, de Jong JL (2014) Multiple divergent haplotypes express completely distinct sets of class I MHC genes in zebrafish. Immunogenetics 66:199–213

    Article  CAS  PubMed  Google Scholar 

  • McConnell SC, Hernandez KM, Wcisel DJ, Kettleborough RN, Stemple DL, Yoder JA, Andrade J, de Jong JL (2016) Alternative haplotypes of antigen processing genes in zebrafish diverged early in vertebrate evolution. Proc Natl Acad Sci U S A 113:E5014–E5023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michalova V, Murray BW, Sultmann H, Klein J (2000) A contig map of the Mhc class I genomic region in the zebrafish reveals ancient synteny. J Immunol 164:5296–5305

    Article  CAS  PubMed  Google Scholar 

  • Nonaka MI, Nonaka M (2010) Evolutionary analysis of two classical MHC class I loci of the medaka fish, Oryzias latipes: haplotype-specific genomic diversity, locus-specific polymorphisms, and interlocus homogenization. Immunogenetics 62:319–332

    Article  CAS  PubMed  Google Scholar 

  • Ono H, Klein D, Vincek V, Figueroa F, O’HUigin C, Tichy H, Klein J (1992) Major histocompatibility complex class II genes of zebrafish. Proc Natl Acad Sci U S A 89:11886–11890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson J, Halliwell JA, Hayhurst JD, Flicek P, Parham P, Marsh SG (2015) The IPD and IMGT/HLA database: allele variant databases. Nucleic Acids Res 43:D423–D431

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sambrook JG, Figueroa F, Beck S (2005) A genome-wide survey of Major Histocompatibility Complex (MHC) genes and their paralogues in zebrafish. BMC Genomics 6:152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shiina T, Dijkstra JM, Shimizu S, Watanabe A, Yanagiya K, Kiryu I, Fujiwara A, Nishida-Umehara C, Kaba Y, Hirono I, Yoshiura Y, Aoki T, Inoko H, Kulski JK, Ototake M (2005) Interchromosomal duplication of major histocompatibility complex class I regions in rainbow trout (Oncorhynchus mykiss), a species with a presumably recent tetraploid ancestry. Immunogenetics 56:878–893

    Article  CAS  PubMed  Google Scholar 

  • Shum BP, Guethlein L, Flodin LR, Adkison MA, Hedrick RP, Nehring RB, Stet RJ, Secombes C, Parham P (2001) Modes of salmonid MHC class I and II evolution differ from the primate paradigm. J Immunol 166:3297–3308

    Article  CAS  PubMed  Google Scholar 

  • Stet RJ, Kruiswijk CP, Saeij JP, Wiegertjes GF (1998) Major histocompatibility genes in cyprinid fishes: theory and practice. Immunol Rev 166:301–316

    Article  CAS  PubMed  Google Scholar 

  • Takeuchi H, Figueroa F, O'hUigin C, Klein J (1995) Cloning and characterization of class I Mhc genes of the zebrafish, Brachydanio rerio. Immunogenetics 42(2):77–84

    Article  CAS  PubMed  Google Scholar 

  • Townsend AR, Gotch FM, Davey J (1985) Cytotoxic T cells recognize fragments of the influenza nucleoprotein. Cell 42:457–467

    Article  CAS  PubMed  Google Scholar 

  • van Erp SH, Dixon B, Figueroa F, Egberts E, Stet RJ (1996) Identification and characterization of a new major histocompatibility complex class I gene in carp (Cyprinus carpio L.). Immunogenetics. 44(1):49–61

    Article  PubMed  Google Scholar 

  • Vandiedonck C, Knight JC (2009) The human major histocompatibility complex as a paradigm in genomics research. Brief Funct Genomic Proteomic 8:379–394

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Lu Y, Zhang Y, Ning Z, Li Y, Zhao Q, Lu H, Huang R, Xia X, Feng Q, Liang X, Liu K, Zhang L, Lu T, Huang T, Fan D, Weng Q, Zhu C, Lu Y, Li W, Wen Z, Zhou C, Tian Q, Kang X, Shi M, Zhang W, Jang S, Du F, He S, Liao L, Li Y, Gui B, He H, Ning Z, Yang C, He L, Luo L, Yang R, Luo Q, Liu X, Li S, Huang W, Xiao L, Lin H, Han B, Zhu Z (2015) The draft genome of the grass carp (Ctenopharyngodon idellus) provides insights into its evolution and vegetarian adaptation. Nat Genet 47:625–631

    Article  CAS  PubMed  Google Scholar 

  • Wu TT, Kabat EA (1970) An analysis of the sequences of the variable regions of Bence Jones proteins and myeloma light chains and their implications for antibody complementarity. J Exp Med 132:211–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia C, Kiryu I, Dijkstra JM, Azuma T, Nakanishi T, Ototake M (2002 Apr) Differences in MHC class I genes between strains of rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 12(4):287–301

    Article  CAS  PubMed  Google Scholar 

  • Yang TY, Hao HF, Jia ZH, Chen WH, Xia C (2006) Characterisation of grass carp (Ctenopharyngodon idellus) MHC class I domain lineages. Fish Shellfish Immunol 21:583–591

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Lin D, Yu S, Bai J, Jiang W, Su W, Huang Y, Yang S, Wu J (2019) Polymorphism of duck MHC class molecules. Immunogenetics 71:49–59

    Article  PubMed  Google Scholar 

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Funding

This work was supported by the 973 Project of the China Ministry of Science and Technology (Grant 2013CB835302), and the National Natural Science Foundation of China (Grant 31572653).

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Conceived and designed the experiments: N Zhang, and C Xia. To assist the sampling: L Ma, Z Qu, X Wei, and M Tang. Gene clone and analysis: Z Li, Y Jiang, N Zhang, and Z Liu. Provided the resources: M Tang and C Xia. Wrote the paper: Z Li. Reviewed the paper: N Zhang and C Xia. All authors approved the final version of the paper.

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Correspondence to Chun Xia.

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Li, Z., Zhang, N., Ma, L. et al. Distribution of ancient α1 and α2 domain lineages between two classical MHC class I genes and their alleles in grass carp. Immunogenetics 71, 395–405 (2019). https://doi.org/10.1007/s00251-019-01111-2

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