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Immunogenetics

, Volume 59, Issue 9, pp 753–760 | Cite as

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

  • Hannah V. Siddle
  • Claire Sanderson
  • Katherine Belov
Brief Communication

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.

Keywords

Tasmanian devil Marsupial MHC Transmissible Tumour Conservation 

Notes

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.

Supplementary material

References

  1. Archer M, Baynes A (1972) Prehistoric mammal faunas from two small caves in the extreme southwest of Western Australia. J R Soc West Aust 55:80–89Google Scholar
  2. 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 15:381–390PubMedCrossRefGoogle Scholar
  3. 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 55:402–411PubMedCrossRefGoogle Scholar
  4. Belov K, Lam MK, Colgan DJ (2004) Marsupial MHC class II beta genes are not orthologous to the eutherian beta gene families. J Hered 95:338–345PubMedCrossRefGoogle Scholar
  5. 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:e46PubMedCrossRefGoogle Scholar
  6. Bjorkman PJ, Parham P (1990) Structure, function, and diversity of class I major histocompatibility complex molecules. Annu Rev Biochem 59:253–288PubMedCrossRefGoogle Scholar
  7. 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 329:512–518PubMedCrossRefGoogle Scholar
  8. Bradshaw C, Brook B (2005) Disease and the devil: density-dependent epidemiological processes explain historical population fluctuations in the Tasmanian devil. Ecography 28:181–190CrossRefGoogle Scholar
  9. 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 364:33–39PubMedCrossRefGoogle Scholar
  10. 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 55:791–795PubMedCrossRefGoogle Scholar
  11. Doherty PC, Zinkernagel RM (1975) A biological role for the major histocompatibility antigens. Lancet 1:1406–1409PubMedCrossRefGoogle Scholar
  12. 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): 396–406PubMedCrossRefGoogle Scholar
  13. Hall T (1999) Bioedit: a user friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  14. Hedrick PW, Thomson G (1983) Evidence for balancing selection at HLA. Genetics 104:449–456PubMedGoogle Scholar
  15. 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 13:1119–1127PubMedGoogle Scholar
  16. Hughes A, Nei M (1988) Pattern of nucleotide substitution at the major histocompatibility complex class I loci reveals overdominant selection. Nature 335:1670170Google Scholar
  17. 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, AustraliaGoogle Scholar
  18. Jones ME, Paetkau D, Geffen E, Moritz C (2004) Genetic diversity and population structure of Tasmanian devils, the largest marsupial carnivore. Mol Ecol 13:2197–2209PubMedCrossRefGoogle Scholar
  19. Kirsch J, Lapointe F, Springer M (1997) DNA-hybridization studies of marsupials and their implications for metatherian classification. Aust J Zool 45:211–280CrossRefGoogle Scholar
  20. 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 76:31–36PubMedCrossRefGoogle Scholar
  21. Lam MK, Belov K, Harrison GA, Cooper DW (2001b) An Mhc class I gene in the Australian brushtail possum (Trichosurus vulpecula). Immunogenetics 53:430–433PubMedCrossRefGoogle Scholar
  22. McKenzie LM, Cooper DW (1994) Low MHC class II variability in a marsupial. Reprod Fertil Dev 6:721–726PubMedCrossRefGoogle Scholar
  23. Miska KB, Miller RD (1999) Marsupial MHC class I: classical sequences from the opossum, Monodelphis domestica. Immunogenetics 50:89–93PubMedCrossRefGoogle Scholar
  24. 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 54:381–393PubMedCrossRefGoogle Scholar
  25. 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 15:851–864PubMedCrossRefGoogle Scholar
  26. Murgia C, Pritchard JK, Kim SY, Fassati A, Weiss RA (2006) Clonal origin and evolution of a transmissible cancer. Cell 126:477–487PubMedCrossRefGoogle Scholar
  27. 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 47:578–585PubMedCrossRefGoogle Scholar
  28. Pearse AM, Swift K (2006) Allograft theory: transmission of devil facial-tumour disease. Nature 439:549PubMedCrossRefGoogle Scholar
  29. 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 8:753–766PubMedGoogle Scholar
  30. 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 58:487–493PubMedCrossRefGoogle Scholar
  31. Springer M (1997) Molecular clocks and the timing of the placental and marsupial radiations in relation to the Cretaceous-tertiary boundary. J Mamm Evol 4:285–302CrossRefGoogle Scholar
  32. Stone WH, Bruun DA, Manis GS, Holste SB, Hoffman ES, Spong KD, Malunas TL (1996) The immunobiology of the marsupial Monodelphis domestica. SOS, Fairhaven, NJGoogle Scholar
  33. 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 49:461–463PubMedCrossRefGoogle Scholar
  34. Stroynowski I, Lindahl KF (1994) Antigen presentation by non-classical class I molecules. Curr Opin Immunol 6:38–44PubMedCrossRefGoogle Scholar
  35. 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 22:4673–4680PubMedCrossRefGoogle Scholar
  36. van Oosterhout C, Joyce DA, Cummings SM (2006) Evolution of MHC class IIB in the genome of wild and ornamental guppies, Poecilia reticulata. Heredity 97:111–118PubMedCrossRefGoogle Scholar
  37. Villadangos JA (2001) Presentation of antigens by MHC class II molecules: getting the most out of them. Mol Immunol 38:329–346PubMedCrossRefGoogle Scholar
  38. Wilkinson R, Kotlarski I, Barton M (1992) Koala lymphoid cells: analysis of antigen-specific responses. Vet Immunol Immunopathol 33:237–247PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Hannah V. Siddle
    • 1
  • Claire Sanderson
    • 1
  • Katherine Belov
    • 1
  1. 1.Centre for Advanced Technologies in Animal Genetics and Reproduction, Faculty of Veterinary ScienceUniversity of SydneySydneyAustralia

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