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Polymorphism of two very similar MHC class Ib loci in rainbow trout (Oncorhynchus mykiss)

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Abstract

As part of an ongoing elucidation of rainbow trout major histocompatibility complex (MHC) class I, the polymorphism of two MHC class Ib loci was analyzed. These loci, Onmy-UCA and Onmy-UDA, are situated head-to-tail and share more than 89% nucleotide identity in their open reading frames. They share 80% identity with some trout Ia alleles. The deduced amino acid sequences suggest that the UCA and UDA molecules are transported to endosomal compartments and may bind peptides in their binding groove. Our survey revealed seven UCA and eight UDA alleles. Similarity indices overlap when comparing within and between UCA and UDA alleles and some cross-locus motif variation is observed. In most trout both UCA and UDA transcripts were found. However, there probably is functional redundancy, because some trout lacked transcription of one of the two loci. Furthermore, for some UCA and UDA alleles, splicing deficiencies, early stop codons, and upstream start codons were found, which may interfere with efficient protein expression. The present study is the first extensive report on MHC class Ib polymorphism assigned to locus in ectotherm species.

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References

  • Afanassieff M, Goto RM, Ha J, Sherman MA, Zhong L, Auffray C, Coudert F, Zoorob R, Miller MM (2001) At least one class I gene in restriction fragment pattern-Y (Rfp-Y), the second MHC gene cluster in the chicken, is transcribed, polymorphic, and shows divergent specialization in antigen binding region. J Immunol 166:3324–3333

    PubMed  Google Scholar 

  • Allendorf FW, Thorgaard GH (1984) Tetraploidy and the evolution of salmonid fishes. In: Turner BJ (ed) Evolutionary genetics of fishes. Plenum, pp 1–53

  • 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

    PubMed  Google Scholar 

  • Barouch D, Friede T, Stevanovic S, Tussey L, Smith K, Rowland-Jones S, Braud V, McMichael A, Rammensee HG (1995) HLA-A2 subtypes are functionally distinct in peptide binding and presentation. J Exp Med 182:1847–1856

    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  PubMed  Google Scholar 

  • Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC (1987) Structure of the human class I histocompatibility antigen, HLA-A2. Nature 329:506–512

    Article  PubMed  Google Scholar 

  • Braud VM, Allan DS, McMichael AJ (1999) Functions of nonclassical MHC and non-MHC-encoded class I molecules. Curr Opin Immunol 11:100–108

    Article  PubMed  Google Scholar 

  • Flajnik MF, Kasahara M (2001) Comparative genomics of the MHC: glimpses into the evolution of the adaptive immune system. Immunity 15:351–362

    Article  PubMed  Google Scholar 

  • Flajnik MF, Kasahara M, Shum BP, Salter-Cid L, Taylor E, Du Pasquier L (1993) A novel type of class I gene organization in vertebrates: a large family of non-MHC-linked class I genes is expressed at the RNA level in the amphibian Xenopus. EMBO J 12:4385–4396

    Google Scholar 

  • Furuhashi Y, Iwata T, Sikorski P, Atkins E, Doi Y (2000) Structure and morphology of the aliphatic polyester poly-β-propiolactone in solution-grown chain-folded lamellar crystals. Macromolecules 33:9423–9431

    Article  Google Scholar 

  • Germain RN (1994) MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell 76:287–299

    Article  PubMed  Google Scholar 

  • Hansen JD, Strassburger P (2000) Description of an ectothermic TCR coreceptor, CD8 alpha, in rainbow trout. J Immunol 164:3132–3139

    PubMed  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  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

    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

    Google Scholar 

  • Hashimoto K, Okamura K, Yamaguchi H, Ototake M, Nakanishi T, Kurosawa Y (1999) Conservation and diversification of MHC class I and its related molecules in vertebrates. Immunol Rev 167:81–100

    PubMed  Google Scholar 

  • Hughes AL, Nei M (1989) Evolution of the major histocompatibility complex: independent origin of nonclassical class I genes in different groups of mammals. Mol Biol Evol 6:559–579

    PubMed  Google Scholar 

  • Jayawardena-Wolf J, Benlagha K, Chiu YH, Mehr R, Bendelac A (2001) CD1d endosomal trafficking is independently regulated by an intrinsic CD1d-encoded tyrosine motif and by the invariant chain. Immunity 15:897–908

    Article  PubMed  Google Scholar 

  • Khakoo SI, Rajalingam R, Shum BP, Weidenbach K, Flodin L, Muir DG, Canavez F, Cooper SL, Valiante NM, Lanier LL, Parham P (2000) Rapid evolution of NK cell receptor systems demonstrated by comparison of chimpanzees and humans. Immunity 12:687–698

    Article  PubMed  Google Scholar 

  • Kelley LA, MacCallum RM, Sternberg MJ (2000) Enhanced genome annotation using structural profiles in the program 3D-PSSM. J Mol Biol 299:499–520

    Article  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

    PubMed  Google Scholar 

  • Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER, Jones PP, Parham P, Wakeland EK, Watkins DI (1990) Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics 31:217–219

    PubMed  Google Scholar 

  • Kozak M (1986) Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44:283–292

    Article  PubMed  Google Scholar 

  • Kumánovics A, Madan A, Qin S, Rowen L, Hood L, Fischer Lindahl K (2002) QUOD ERAT FACIENDUM: sequence analysis of the H2-D and H2-Q regions of 129/SvJ mice. Immunogenetics 54:479–489

    Article  PubMed  Google Scholar 

  • Lindahl KF, Byers DE, Dabhi VM, Hovik R, Jones EP, Smith GP, Wang CR, Xiao H, Yoshino M (1997) H2–M3, a full-service class Ib histocompatibility antigen. Annu Rev Immunol 15:851–879

    Article  PubMed  Google Scholar 

  • Madden DR (1995) The three-dimensional structure of peptide-MHC complexes. Annu Rev Immunol 13:587–622

    Article  PubMed  Google Scholar 

  • Madden DR, Gorga JC, Strominger JL, Wiley DC (1992) The three-dimensional structure of HLA-B27 at 2.1-A resolution suggests a general mechanism for tight peptide binding to MHC. Cell 70:1035–1048

    Article  PubMed  Google Scholar 

  • Magor KE, Shum BP, Parham P (2004) The beta 2-microglobulin locus of rainbow trout (Oncorhynchus mykiss) contains three polymorphic genes. J Immunol 172:3635–3643

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Matsuo MY, Asakawa S, Shimizu N, Kimura H, Nonaka M (2002) Nucleotide sequence of the MHC class I genomic region of a teleost, the medaka (Oryzias latipes). Immunogenetics 53:930–940

    Article  PubMed  Google Scholar 

  • Miller KM, Withler RE (1998) The salmonid class I MHC: limited diversity in a primitive teleost. Immunol Rev 166:279–293

    PubMed  Google Scholar 

  • Mizuki N, Ota M, Kimura M, Ohno S, Ando H, Katsuyama Y, Yamazaki M, Watanabe K, Goto K, Nakamura S, Bahram S, Inoko H (1997) Triplet repeat polymorphism in the transmembrane region of the MICA gene: a strong association of six GCT repetitions with Behcet disease. Proc Natl Acad Sci U S A 94:1298–1303

    Google Scholar 

  • Moore LJ, Somamoto T, Lie KK, Dijkstra JM, Hordvik I (2005) Characterisation of salmon and trout CD8α and CD8β. Mol Immunol 42:1225–1234

    Article  PubMed  Google Scholar 

  • Morris DR, Geballe AP (2000) Upstream open reading frames as regulators of mRNA translation. Mol Cell Biol 20:8635–8642

    Article  PubMed  Google Scholar 

  • Nakanishi T, Fischer U, Dijkstra JM, Hasegawa S, Somamoto T, Okamoto N, Ototake M (2002) Cytotoxic T cell function in fish. Dev Comp Immunol 26:131–139

    Article  PubMed  Google Scholar 

  • Nicholls A, Honig B (1991) A rapid finite-difference algorithm, utilizing successive over-relaxation to solve the Poisson–Boltzmann equation. J Comput Chem 12:435–445

    Google Scholar 

  • Nicholls A, Sharp KA, Honig B (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11:281–296

    Article  PubMed  Google Scholar 

  • Okamura K, Ototake M, Nakanishi T, Kurosawa Y, Hashimoto K (1997) The most primitive vertebrates with jaws possess highly polymorphic MHC class I genes comparable to those of humans. Immunity 7:777–790

    Article  PubMed  Google Scholar 

  • Onozato H (1984) Diploidization of gynogenetically activated salmonid eggs using hydrostatic pressure. Aquaculture 43:91–97

    Article  Google Scholar 

  • Phillips RB, Zimmerman A, Noakes MA, Palti Y, Morasch MR, Eiben L, Ristow SS, Thorgaard GH, Hansen JD (2003) Physical and genetic mapping of the rainbow trout major histocompatibility regions: evidence for duplication of the class I region. Immunogenetics 55:561–569

    Article  PubMed  Google Scholar 

  • Pond L, Kuhn LA, Teyton L, Schutze MP, Tainer JA, Jackson MR, Peterson PA (1995) A role for acidic residues in di-leucine motif-based targeting to the endocytic pathway. J Biol Chem 270:19989–19997

    Article  PubMed  Google Scholar 

  • Potter TA, Rajan TV, Dick RF 2nd, Bluestone JA (1989) Substitution at residue 227 of H-2 class I molecules abrogates recognition by CD8-dependent, but not CD8-independent, cytotoxic T lymphocytes. Nature 337:73–75

    Article  PubMed  Google Scholar 

  • Rammensee HG, Friede T, Stevanoviic S (1995) MHC ligands and peptide motifs: first listing. Immunogenetics 41:178–228

    Article  PubMed  Google Scholar 

  • Roos C, Walter L (2005) Considerable haplotypic diversity in the RT1-CE class I gene region of the rat major histocompatibility complex. Immunogenetics 56:773–777

    Article  PubMed  Google Scholar 

  • Salter RD, Benjamin RJ, Wesley PK, Buxton SE, Garrett TP, Clayberger C, Krensky AM, Norment AM, Littman DR, Parham P (1990) A binding site for the T-cell coreceptor CD8 on the alpha 3 domain of HLA-A2. Nature 345:41–46

    Article  PubMed  Google Scholar 

  • Saper MA, Bjorkman PJ, Wiley DC (1991) Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 A resolution. J Mol Biol 219:277–319

    Article  PubMed  Google Scholar 

  • Sarder MR, Fischer U, Dijkstra JM, Kiryu I, Yoshiura Y, Azuma T, Kollner B, Ototake M (2003) The MHC class I linkage group is a major determinant in the in vivo rejection of allogeneic erythrocytes in rainbow trout (Oncorhynchus mykiss). Immunogenetics 55:315–324

    Article  PubMed  Google Scholar 

  • Sato A, Figueroa F, Murray BW, Malaga-Trillo E, Zaleska-Rutczynska Z, Sultmann H, Toyosawa S, Wedekind C, Steck N, Klein J (2000) Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenetics 51:108–116

    Article  PubMed  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  PubMed  Google Scholar 

  • Shum BP, Azumi K, Zhang S, Kehrer SR, Raison RL, Detrich HW, Parham P (1996) Unexpected beta2-microglobulin sequence diversity in individual rainbow trout. Proc Natl Acad Sci U S A 93:2779–2784

    Google Scholar 

  • Shum BP, Rajalingam R, Magor KE, Azumi K, Carr WH, Dixon B, Stet RJ, Adkison MA, Hedrick RP, Parham P (1999) A divergent non-classical class I gene conserved in salmonids. Immunogenetics 49:479–490

    Article  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

    PubMed  Google Scholar 

  • Shum BP, Mason PM, Magor KE, Flodin LR, Stet RJ, Parham P (2002) Structures of two major histocompatibility complex class I genes of the rainbow trout (Oncorhynchus mykiss). Immunogenetics 54:193–199

    Article  PubMed  Google Scholar 

  • Sun J, Leahy DJ, Kavathas PB (1995) Interaction between CD8 and major histocompatibility complex (MHC) class I mediated by multiple contact surfaces that include the alpha 2 and alpha 3 domains of MHC class I. J Exp Med 182:1275–1280

    Google Scholar 

  • Takasaki N, Park L, Kaeriyama M, Gharrett AJ, Okada N (1996) Characterization of species-specifically amplified SINEs in three salmonid species-chum salmon, pink salmon, and kokanee: the local environment of the genome may be important for the generation of a dominant source gene at a newly retroposed locus. J Mol Evol 42:103–116

    Article  PubMed  Google Scholar 

  • Townsend A, Bodmer H (1989) Antigen recognition by class I-restricted T lymphocytes. Annu Rev Immunol 7:601–624

    PubMed  Google Scholar 

  • Yoshizaki G, Oshiro T, Takashima F (1991) Introduction of carp a-globin gene into rainbow trout. Nippon Suisan Gakkaishi 57:819–824

    Google Scholar 

  • Zeng Z, Castano AR, Segelke BW, Stura EA, Peterson PA, Wilson IA (1997) Crystal structure of mouse CD1: An MHC-like fold with a large hydrophobic binding groove. Science 277:339–345

    Article  PubMed  MathSciNet  Google Scholar 

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Acknowledgement

The study was supported by “the promotion of basic research activities for innovative biosciences” funded by Bio-oriented Technology Research Advancement Institution (BRAIN), Japan.

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  1. Ikunari Kiryu

    Present address: Japan International Research Center for Agricultural Sciences, Ohwashi 1-1, Tsukuba, Ibaraki, 305-8686, Japan

Authors and Affiliations

  1. Inland Station, Fisheries Research Agency, National Research Institute of Aquaculture, Tamaki, Mie, 519-0423, Japan

    Johannes Martinus Dijkstra, Ikunari Kiryu, Yasutoshi Yoshiura & Mitsuru Ototake

  2. Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Aichi, 4701192, Japan

    Johannes Martinus Dijkstra & Nobuhiro Hayashi

  3. Howard Hughes Medical Institute and Center for Immunology, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd, Dallas, TX, 75390-9050, USA

    Attila Kumánovics

  4. Nagano Prefectural Experimental Station of Fisheries, Akashina, Nagano, 399-7102, Japan

    Masakazu Kohara

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  1. Johannes Martinus Dijkstra
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Correspondence to Johannes Martinus Dijkstra.

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Authors J.M. Dijkstra and I. Kiryu contributed equally to this study.

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Dijkstra, J.M., Kiryu, I., Yoshiura, Y. et al. Polymorphism of two very similar MHC class Ib loci in rainbow trout (Oncorhynchus mykiss). Immunogenetics 58, 152–167 (2006). https://doi.org/10.1007/s00251-006-0086-5

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