Skip to main content

Advertisement

Log in

Characterization of major histocompatibility complex class I and class II genes from the Tasmanian devil (Sarcophilus harrisii)

  • Brief Communication
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

The Tasmanian devil (Sarcophilus harrisii) is currently threatened by an emerging wildlife disease, devil facial tumour disease. The disease is decreasing devil numbers dramatically and may lead to the extinction of the species. At present, nothing is known about the immune genes or basic immunology of the devil. In this study, we report the construction of the first genetic library for the Tasmanian devil, a spleen cDNA library, and the isolation of full-length MHC Class I and Class II genes. We describe six unique Class II β chain sequences from at least three loci, which belong to the marsupial Class II DA gene family. We have isolated 13 unique devil Class I sequences, representing at least seven Class I loci, two of which are most likely non-classical genes. The MHC Class I sequences from the devil have little heterogeneity, indicating recent divergence. The MHC genes described here are most likely involved in antigen presentation and are an important first step for studying MHC diversity and immune response in the devil.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Archer M, Baynes A (1972) Prehistoric mammal faunas from two small caves in the extreme southwest of Western Australia. J R Soc West Aust 55:80–89

    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

    Article  PubMed  CAS  Google Scholar 

  • Belov K, Lam MK, Hellman L, Colgan DJ (2003) Evolution of the major histocompatibility complex: isolation of class II beta cDNAs from two monotremes, the platypus and the short-beaked echidna. Immunogenetics 55:402–411

    Article  PubMed  CAS  Google Scholar 

  • Belov K, Lam MK, Colgan DJ (2004) Marsupial MHC class II beta genes are not orthologous to the eutherian beta gene families. J Hered 95:338–345

    Article  PubMed  CAS  Google Scholar 

  • Belov K, Deakin JE, Papenfuss AT, Baker ML, Melman SD, Siddle HV, Gouin N, Goode DL, Sargeant TJ, Robinson MD, Wakefield MJ, Mahony S, Cross JG, Benos PV, Samollow PB, Speed TP, Graves JA, Miller RD (2006) Reconstructing an ancestral mammalian immune supercomplex from a marsupial major histocompatibility complex. PLoS Biol 4:e46

    Article  PubMed  CAS  Google Scholar 

  • Bjorkman PJ, Parham P (1990) Structure, function, and diversity of class I major histocompatibility complex molecules. Annu Rev Biochem 59:253–288

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Bradshaw C, Brook B (2005) Disease and the devil: density-dependent epidemiological processes explain historical population fluctuations in the Tasmanian devil. Ecography 28:181–190

    Article  Google Scholar 

  • Brown JH, Jardetzky TS, 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

    Article  PubMed  CAS  Google Scholar 

  • Browning TL, Belov K, Miller RD, Eldridge MD (2004) Molecular cloning and characterization of the polymorphic MHC class II DBB from the tammar wallaby (Macropus eugenii). Immunogenetics 55:791–795

    Article  PubMed  CAS  Google Scholar 

  • Doherty PC, Zinkernagel RM (1975) A biological role for the major histocompatibility antigens. Lancet 1:1406–1409

    Article  PubMed  CAS  Google Scholar 

  • Gouin N, Wright AM, Miska KB, Parra ZE, Samollow PB, Baker ML, Miller RD (2006) Modo-UG, a marsupial nonclassical MHC class I locus. Immunogenetics 58(5–6): 396–406

    Article  PubMed  CAS  Google Scholar 

  • Hall T (1999) Bioedit: a user friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hedrick PW, Thomson G (1983) Evidence for balancing selection at HLA. Genetics 104:449–456

    PubMed  CAS  Google Scholar 

  • Houlden BA, Greville WD, Sherwin WB (1996) Evolution of MHC class I loci in marsupials: characterization of sequences from koala (Phascolarctos cinereus). Mol Biol Evol 13:1119–1127

    PubMed  CAS  Google Scholar 

  • Hughes A, Nei M (1988) Pattern of nucleotide substitution at the major histocompatibility complex class I loci reveals overdominant selection. Nature 335:1670170

    Google Scholar 

  • Jones M, Oakwood M, Belcher C, Morris K, Murray A, Woolley P, Firestone K, Johnson B, Burnett S (2003) Carnivore Concerns: problems, issues, and solutions for conserving Australia’s marsupial carnivores. CSIRO, Melbourne, Australia

    Google Scholar 

  • Jones ME, Paetkau D, Geffen E, Moritz C (2004) Genetic diversity and population structure of Tasmanian devils, the largest marsupial carnivore. Mol Ecol 13:2197–2209

    Article  PubMed  CAS  Google Scholar 

  • Kirsch J, Lapointe F, Springer M (1997) DNA-hybridization studies of marsupials and their implications for metatherian classification. Aust J Zool 45:211–280

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lam MK, Belov K, Harrison GA, Cooper DW (2001b) An Mhc class I gene in the Australian brushtail possum (Trichosurus vulpecula). Immunogenetics 53:430–433

    Article  PubMed  CAS  Google Scholar 

  • McKenzie LM, Cooper DW (1994) Low MHC class II variability in a marsupial. Reprod Fertil Dev 6:721–726

    Article  PubMed  CAS  Google Scholar 

  • Miska KB, Miller RD (1999) Marsupial MHC class I: classical sequences from the opossum, Monodelphis domestica. Immunogenetics 50:89–93

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Miska KB, Wright AM, Lundgren R, Sasaki-McClees R, Osterman A, Gale JM, Miller RD (2004) Analysis of a marsupial MHC region containing two recently duplicated class I loci. Mamm Genome 15:851–864

    Article  PubMed  CAS  Google Scholar 

  • Murgia C, Pritchard JK, Kim SY, Fassati A, Weiss RA (2006) Clonal origin and evolution of a transmissible cancer. Cell 126:477–487

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Pearse AM, Swift K (2006) Allograft theory: transmission of devil facial-tumour disease. Nature 439:549

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Siddle HV, Deakin JE, Baker ML, Miller RD, Belov K (2006) Isolation of major histocompatibility complex Class I genes from the tammar wallaby (Macropus eugenii). Immunogenetics 58:487–493

    Article  PubMed  CAS  Google Scholar 

  • Springer M (1997) Molecular clocks and the timing of the placental and marsupial radiations in relation to the Cretaceous-tertiary boundary. J Mamm Evol 4:285–302

    Article  Google Scholar 

  • Stone WH, Bruun DA, Manis GS, Holste SB, Hoffman ES, Spong KD, Malunas TL (1996) The immunobiology of the marsupial Monodelphis domestica. SOS, Fairhaven, NJ

    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

    Article  PubMed  CAS  Google Scholar 

  • Stroynowski I, Lindahl KF (1994) Antigen presentation by non-classical class I molecules. Curr Opin Immunol 6:38–44

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • van Oosterhout C, Joyce DA, Cummings SM (2006) Evolution of MHC class IIB in the genome of wild and ornamental guppies, Poecilia reticulata. Heredity 97:111–118

    Article  PubMed  CAS  Google Scholar 

  • Villadangos JA (2001) Presentation of antigens by MHC class II molecules: getting the most out of them. Mol Immunol 38:329–346

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson R, Kotlarski I, Barton M (1992) Koala lymphoid cells: analysis of antigen-specific responses. Vet Immunol Immunopathol 33:237–247

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Robert Johnson and Larry Vogelnest from Taronga zoo and Stephen Pyecroft from the Department of Primary Industry and Water, Tasmania for providing tissue samples. We would also like to thank Erin Noonan for performing DNA extractions on five individuals for polymorphism data. This work was funded by the Australian Research Council, the Sarah and Anne Payten Canine Cancer Fund and the Department of Primary Industry and Water.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Katherine Belov.

Electronic supplementary material

Below is the link to the electronic supplementary material.

251_2007_238_MOESM1_ESM.pdf

Rights and permissions

Reprints and permissions

About this article

Cite this article

Siddle, H.V., Sanderson, C. & Belov, K. Characterization of major histocompatibility complex class I and class II genes from the Tasmanian devil (Sarcophilus harrisii). Immunogenetics 59, 753–760 (2007). https://doi.org/10.1007/s00251-007-0238-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-007-0238-2

Keywords

Navigation