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Evolution of the major histocompatibility complex: Isolation of class II β cDNAs from two monotremes, the platypus and the short-beaked echidna

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Abstract

Extant mammals are composed of three lineages: the eutherians, the marsupials and the monotremes. The majority of the mammalian major histocompatibility complex (MHC) data is based on the eutherian mammals, which generally have three classical MHC class II β chain gene clusters — DRB, DQB and DPB, as well as the non-classical DMB and DOB. Marsupial DMB, DAB and DBB have been characterised. Confusion still surrounds the relationship of the marsupial DAB and DBB genes with the classical eutherian class II clusters. Here we present the first monotreme MHC class II β chain sequences. Four MHC class II β chain sequences were isolated from a spleen cDNA library from the short-beaked echidna , and one from a spleen cDNA library from platypus using a brushtail possum DAB probe. Given the non-orthologous relationship of the monotreme sequences with marsupial and eutherian β chain clusters, we recommend that the five new monotreme sequences be assigned the nomenclature 'DZB', signifying the description of a new mammalian β chain cluster. Our analysis suggests that all mammalian β chain sequences (except DMB) evolved from a common ancestor. Maximum likelihood analysis places the monotreme β chain sequences at the base of the mammalian clade, indicating their ancestral status. However, within the mammalian clade, monophyletic clades are not robust, and elucidation of the order of gene duplication that gave rise to the present-day gene clusters is not yet possible.

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References

  • Air GM, Thompson EO, Richardson BJ, Sharman GB (1971) Amino-acid sequences of kangaroo myoglobin and haemoglobin and the date of marsupial-eutherian divergence. Nature 229:391–394

    CAS  PubMed  Google Scholar 

  • Atwell JL, Marchalonis JJ (1977) Immunoglobulin gamma chains of a monotreme mammal, the echidna (Tachyglossus aculeatus): amino acid composition and partial amino acid sequence. J Immunogenet 4:73–80

    CAS  PubMed  Google Scholar 

  • Auffray C, Novotny J (1986) Speculations on sequence homologies between the fibronectin cell-attachment site, major histocompatibility antigens, and a putative AIDS virus polypeptide. Hum Immunol 15:381–390

    CAS  PubMed  Google Scholar 

  • Beck S, Trowsdale J (1999) Sequence organisation of the class II region of the human MHC. Immunol Rev 167:201–210

    CAS  PubMed  Google Scholar 

  • Belov K, Hellman L (2003) Platypus IgM and the divergence of the two extant monotreme lineages. Aust Mamm 25:87–94

    Google Scholar 

  • Belov K, Hellman L, Cooper DW (2002a) Characterisation of echidna IgM provides insights into the time of divergence of extant mammals. Dev Comp Immunol 26:831–839

    CAS  PubMed  Google Scholar 

  • Belov K, Hellman L, Cooper DW (2002b) Characterisation of IgG1 from a monotreme, Tachyglossus aculeatus. Immunogenetics 53:1065–1071

    CAS  PubMed  Google Scholar 

  • Belov K, Zenger KR, Hellman L, Cooper DW (2002c) Echidna IgA supports mammalian unity and traditional Therian relationship. Mamm Genome 13:656–63

    CAS  PubMed  Google Scholar 

  • Brown JH, Jardetzky T, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC (1993) Three dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364:33–39

    CAS  PubMed  Google Scholar 

  • Campbell RD, Trowsdale J (1993) Map of the human MHC. Immunol Today 14:349–352

    CAS  PubMed  Google Scholar 

  • Diener E, Ealey EH (1965) Immune system in a monotreme: studies on the Australian echidna (Tachyglossus aculeatus). Nature 208:950–953

    CAS  PubMed  Google Scholar 

  • Edwards SV, Wakeland EK, Potts WK (1995) Contrasting histories of avian and mammalian Mhc genes revealed by class II B sequences from songbirds. Proc Natl Acad Sci U S A 92:12200–12204

    Google Scholar 

  • Harrison GA, Young LJ, Watson CM, Miska KB, Miller RD, Deane EM (2003) A survey of type I interferons from a marsupial and monotreme: implications for the evolution of the type I interferon gene family in mammals. Cytokine 21:105–119

    CAS  PubMed  Google Scholar 

  • Hughes AL, Nei M (1990) Evolutionary relationships of class II major-histocompatibility-complex genes in mammals. Mol Biol Evol 7:491–514

    CAS  PubMed  Google Scholar 

  • Hughes AL, Hughes MK, Howell CY, Nei M (1994) Natural selection at the class II major histocompatibility complex loci of mammals. Philos Trans R Soc Lond B Biol Sci 346:359–366; discussion 366–367

    CAS  PubMed  Google Scholar 

  • Johansson J, Aveskogh M, Munday B, Hellman L (2002) Heavy chain V region diversity in the duck-billed platypus (Ornithorhynchus anatinus): Long and highly variable complementarity-determining region 3 compensates for limited germline diversity. J Immunol 168:5155–5162

    CAS  PubMed  Google Scholar 

  • Kaufman J, Salomonsen J, Flajnik M (1994) Evolutionary conservation of MHC class I and class II molecules — different yet the same. Semin Immunol 6:411–424

    CAS  PubMed  Google Scholar 

  • Kelly AP, Monaco JJ, Cho SG, Trowsdale J (1991) A new human HLA class II-related locus, DM. Nature 353:571–573

    Google Scholar 

  • Killian JK, Buckley TR, Stewart N, Munday BL, Jirtle RL (2001) Marsupials and Eutherians reunited: genetic evidence for the Theria hypothesis of mammalian evolution. Mamm Genome 12:513–517

    CAS  PubMed  Google Scholar 

  • Klein J, Figueroa F (1986) Evolution of the major histocompatibility complex. Crit Rev Immunol 6:295–386

    CAS  Google Scholar 

  • Klein J, O'HUigin C (1995) Class II B Mhc motifs in an evolutionary perspective. Immunol Rev 143:89–111

    CAS  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

    CAS  PubMed  Google Scholar 

  • Konig R, Huang LY, Germain RN (1992) MHC class II interaction with CD4 mediated by a region analogous to the MHC class I binding site for CD8. Nature 356:796–798

    CAS  PubMed  Google Scholar 

  • Lam MK, Belov K, Harrison GA, Cooper DW (2001) Cloning of the MHC class II DRB cDNA from the brushtail possum ( Trichosurus vulpecula). Immunol Lett 76:31–36

    Article  CAS  PubMed  Google Scholar 

  • Marchalonis JJ, Atwell JL, Goding JW (1978) 7S immunoglobulins of a monotremes, the Echidna Tachyglossus aculeatus: two distinct isotypes which bind A protein of Staphylococcus aureus. Immunology 34:97–103

    CAS  PubMed  Google Scholar 

  • Messer M, Weiss A, Shaw D, Westerman M (1998) Evolution of the Monotreme: Phylogenetic relationship to Marsupials and Eutherians, and estimation of divergence dates based on alpha-lactalbumin amino acid sequences. J Mamm Evol 5:95–105

    Article  Google Scholar 

  • Miska KB, Harrison GA, Hellman L, Miller RD (2002) The major histocompatibility complex in monotremes: an analysis of the evolution of Mhc class I genes across all three mammalian subclasses. Immunogenetics 54:381–393

    CAS  PubMed  Google Scholar 

  • O'HUigin C, Sultmann H, Tichy H, Murray BW (1998) Isolation of MHC class II DMA and DMB cDNA sequences in a marsupial: the gray short-tailed opossum ( Monodelphis domestica). J Mol Evol 47:578–585

    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

    Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Retief JD, Winkfein RJ, Dixon GH (1993) Evolution of the monotremes. The sequences of the protamine P1 genes of platypus and echidna. Eur J Biochem 218:457–461

    CAS  PubMed  Google Scholar 

  • Schneider S, Vincek V, Tichy H, Figueroa F, Klein J (1991) MHC class II genes of a marsupial, the red-necked wallaby (Macropus rufogriseus): identification of new gene families. Mol Biol Evol 8:753–766

    CAS  PubMed  Google Scholar 

  • Schopfer R, Figueroa F, Nizetic D, Nevo E, Klein J (1987) Evolutionary diversification of class II P loci in the Mhc of the mole-rat Spalax ehrenbergi. Mol Biol Evol 4:287–299

    CAS  PubMed  Google Scholar 

  • Stone WH, Brunn DA, Foster EB, Manis GS, Hoffman ES, Saphire DG, VandeBerg JL, Infante AJ (1998) Absence of a significant mixed lymphocyte reaction in a marsupial (Monodelphis domestica). Lab Anim Sci 48:184–189

    CAS  PubMed  Google Scholar 

  • Stone WH, Bruun DA, Fuqua C, Glass LC, Reeves A, Holste S, Figueroa F (1999) Identification and sequence analysis of an Mhc class II B gene in a marsupial (Monodelphis domestica). Immunogenetics 49:461–463

    CAS  PubMed  Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4. release 4. 0610 Sutherland, Massachusetts

  • Takahashi K, Rooney AP, Nei M (2000) Origins and divergence times of mammalian class II MHC gene clusters. J Hered 91:198–204

    CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Vernersson M, Aveskogh M, Munday B, Hellman L (2002) Evidence for an early appearance of modern post-switch immunoglobulin isotypes in mammalian evolution (II); cloning of IgE, IgG1 and IgG2 from a monotreme, the duck-billed platypus, Ornithorhynchus anatinus. Eur J Immunol 32:2145–2155

    CAS  PubMed  Google Scholar 

  • Vernersson M, Aveskogh M, Hellman L (2003) Characterization of IgE from a monotreme the Australian Echidna (Tachyglossus aculeatus) and a comparative analysis of the ε chains from all three extant mammalian lineages. Dev Comp Immunol (in press) DOI 10.1016/S0145-305X(03)00084-3

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Acknowledgements

This work was supported by an Australian Research Council Discovery Grant to K.B.

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Authors and Affiliations

  1. Evolutionary Biology Unit, Australian Museum, 6 College St, Sydney, NSW 2010, Australia

    Katherine Belov & Donald J. Colgan

  2. ReproGen, Centre for Advanced Technologies in Animal Genetics and Reproduction, Faculty of Veterinary Science, University of Sydney, PMB 3, Camden , NSW 2570, Australia

    Mary K. P. Lam

  3. Department of Cell and Molecular Biology, Biomedical Centre, Uppsala University, BOX596, Uppsala 75124, Sweden

    Lars Hellman

Authors
  1. Katherine Belov
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  2. Mary K. P. Lam
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  3. Lars Hellman
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  4. Donald J. Colgan
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Corresponding author

Correspondence to Katherine Belov.

Additional information

Nucleotide sequence data reported are available in the GenBank database under the Accession numbers AY288074–AY288078

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Belov, K., Lam, M.K.P., Hellman, L. et al. Evolution of the major histocompatibility complex: Isolation of class II β cDNAs from two monotremes, the platypus and the short-beaked echidna. Immunogenetics 55, 402–411 (2003). https://doi.org/10.1007/s00251-003-0598-1

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  • DOI: https://doi.org/10.1007/s00251-003-0598-1

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