SpringerLink
Log in

The Marsupial Major Histocompatibility Complex

  • Chapter
  • First Online:
Marsupial Genetics and Genomics

Abstract

The major histocompatibility complex (MHC) contains genes that play essential roles in the innate and adaptive immune responses, and has been one of the most studied genomic regions among vertebrates. The marsupial MHC has been intensively investigated in several species, with the genomic organization having been characterized in the gray short-tailed opossum and tammar wallaby, and gene sequences and genetic diversity examined in a number of representative marsupials. These studies have significantly contributed to our understanding of the marsupial immune system, evolution of MHC, and wildlife health and conservation. This review will provide a comprehensive summary of current knowledge on the marsupial MHC.

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

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
EUR 29.95
Price includes VAT (Germany)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
EUR 160.49
Price includes VAT (Germany)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
EUR 213.99
Price includes VAT (Germany)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
EUR 213.99
Price includes VAT (Germany)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, Wayne RK (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA 101:3490–3494.

    Article  PubMed  CAS  Google Scholar 

  • Baker ML, Miller RD (2007) Evolution of mammalian CD1: marsupial CD1 is not orthologous to the eutherian isoforms and is a pseudogene in the opossum Monodelphis domestica. Immunology 121:113–121.

    Article  PubMed  CAS  Google Scholar 

  • Baker ML, Melman SD, Huntley J, Miller RD (2009) Evolution of the opossum major histocompatibility complex: evidence for diverse alternative splice patterns and low polymorphism among class I genes. Immunology 128:e418–e431.

    Article  PubMed  Google Scholar 

  • Belov K, Lam MKP, 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, et al. (2006) Reconstructing an ancestral mammalian immune supercomplex from a marsupial Major Histocompatibility Complex. PLoS Biology 4:e46.

    Article  PubMed  Google Scholar 

  • Brown AS, Girjes AA, Lavin MF, Timms P, Woolcock JB (1987) Chlamydial disease in koalas. Aust Vet J 64:346–350.

    Article  PubMed  CAS  Google Scholar 

  • Browning TL, Belov K, Miller RD, Eldridge MDB (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 

  • Canfield PJ, Hemsley S, Connolly J (1996) Histological and immunohistological study of the develo** and involuting superficial cervical thymus in the koala (Phascolarctos cinereus). J Anat 189:159–169.

    PubMed  Google Scholar 

  • Cheng Y, Siddle HV, Beck S, Eldridge MDB, Belov K (2009a) High levels of genetic variation at MHC class II DBB loci in the tammar wallaby (Macropus eugenii). Immunogenetics 61:111–118.

    Article  PubMed  CAS  Google Scholar 

  • Cheng Y, Wakefield M, Siddle HV, et al. (2009b) Isolation and characterization of 10 MHC Class I-associated microsatellite loci in tammar wallaby (Macropus eugenii). Mol Ecol Resour 9:346–349.

    Article  PubMed  CAS  Google Scholar 

  • Cisternas PA, Armati PJ (2000) Immune system cell markers in the northern brown bandicoot, Isoodon macrourus. Dev Comp Immunol 24:771–782.

    Article  PubMed  CAS  Google Scholar 

  • Coleman J, Caley P (2000) Possums as a reservoir of bovine TB. In: Montague TL (ed) The Brushtail Possum: Biology, Impact and Management of an Introduced Marsupial. Manaaki Whenua, Lincoln.

    Google Scholar 

  • Cooper DW, Larsen E (2006) Immunocontraception of mammalian wildlife: ecological and immunogenic issues. Reproduction 132:821–828.

    Article  PubMed  CAS  Google Scholar 

  • Cooper DW, McKenzie LM (1997) Genetics of tammar wallabies. In: Saunders N, Hinds L (eds) Marsupial Biology: Recent Research, New Perspectives. UNSW Press, Sydney.

    Google Scholar 

  • Coutinho HB, King G, Sewell HF, et al. (1993) Immunocytochemical study of Peyer’s patches follicular-associated epithelium in the marsupial, Didelphis albiventris. Dev Comp Immunol 17:537–548.

    Article  PubMed  CAS  Google Scholar 

  • Coutinho HB, Nogueira JC, King G, et al. (1994) Immunocytochemical study of the ontogeny of Peyer’s patches in the Brazilian marsupial Didelphis albiventris. J Anat 185:347–354.

    PubMed  Google Scholar 

  • Cowan E (2000) Biological control of possums. In: Montague TL (ed) The Brushtail Possum: Biology, Impact and Management of an Introduced Marsupial. Manaaki Whenua, Lincoln.

    Google Scholar 

  • Cresswell P, Ackerman AL, Giodini A, Peaper DR, Wearsch PA (2005) Mechanisms of MHC class I-restricted antigen processing and cross-presentation. Immunol Rev 207:145–157.

    Article  PubMed  CAS  Google Scholar 

  • Cross JGR, Harrison GA, Coggill P, et al. (2005) Analysis of the genomic region containing the tammar wallaby (Macropus eugenii) orthologues of MHC class III genes. Cytogenet Genome Res 111:110–117.

    Article  PubMed  CAS  Google Scholar 

  • Daly K, Church WB, Nicholas K, Williamson P (2007) Comparative modeling of marsupial MHC class I molecules identifies structural polymorphisms affecting functional motifs. J Exp Zool 307A:611–624.

    Article  CAS  Google Scholar 

  • de Groot N, Doxiadis GGM, de Vos-Rouweler AJM, de Groot NG, Verschoor EJ, Bontrop RE (2008) Comparative genetics of a highly divergent DRB microsatellite in different macaque species. Immunogenetics 60:737–748.

    Article  PubMed  CAS  Google Scholar 

  • Deakin JE, Papenfuss AT, Belov K, et al. (2006) Evolution and comparative analysis of the MHC Class III inflammatory region. BMC Genomics 7:281.

    Article  PubMed  Google Scholar 

  • Deakin JE, Siddle HV, Cross JGR, Belov K, Graves JAM (2007) Class I genes have split from the MHC in the tammar wallaby. Cytogenet Genome Res 116:205–211.

    Article  PubMed  CAS  Google Scholar 

  • Doxiadis GGM, de Groot N, Claas FHJ, Doxiadis IIN, van Rood JJ, Bontrop RE (2007) A highly divergent microsatellite facilitating fast and accurate DRB haploty** in humans and rhesus macaques. Proc Natl Acad Sci USA 104:8907–8912.

    Article  PubMed  CAS  Google Scholar 

  • Edwards SV, Potts WK (1996) Polymorphism of genes in the major histocompatibility complex: implications for conservation genetics of vertebrates. In: Smith TB, Wayne RK (eds) Molecular Genetic Approaches in Conservation. Oxford University Press, Oxford.

    Google Scholar 

  • Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327.

    Article  PubMed  Google Scholar 

  • Gouin N, Deakin JE, Miska KB, et al. (2006a) Linkage map** and physical localization of the major histocompatibility complex region of the marsupial Monodelphis domestica. Cytogenet Genome Res 112:277–285.

    Article  PubMed  CAS  Google Scholar 

  • Gouin N, Wright AM, Miska KB, et al. (2006b) Modo-UG, a marsupial nonclassical MHC class I locus. Immunogenetics 58:396–406.

    Article  PubMed  CAS  Google Scholar 

  • Hemsley S, Canfield PJ (1997) Histopathological and immunohistochemical investigation of naturally occurring chlamydial conjunctivitis and urogenital inflammation in koalas (Phascolarctos cinereus). J Comp Pathol 116:273–290.

    Article  PubMed  CAS  Google Scholar 

  • Holland OJ, Cowan PE, Gleeson DM, Chamley LW (2008a) High variability in the MHC class II DA beta chain of the brushtail possum (Trichosurus vulpecula). Immunogenetics 60: 775–781.

    Article  PubMed  CAS  Google Scholar 

  • Holland OJ, Cowan PE, Gleeson DM, Chamley LW (2008b) Identification of novel major histocompatibility complex class I sequences in a marsupial, the brushtail possum (Trichosurus vulpecula). Immunogenetics 60:609–619.

    Article  PubMed  CAS  Google Scholar 

  • Holland OJ, Cowan PE, Gleeson DM, Chamley LW (2008c) Novel alleles in classical major histocompatibility complex class II loci of the brushtail possum (Trichosurus vulpecula). Immunogenetics 60:449–460.

    Article  PubMed  CAS  Google Scholar 

  • Houlden B, Greville W, Sherwin W (1996) Evolution of MHC class I loci in marsupials: characterization of sequences from Koala (Phascolarctos cinerus). Mol Biol Evol 13:1119–1127.

    Article  PubMed  CAS  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  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Infante AJ, Samples NK, Croix DA, Redding TS, VandeBerg JL, Stone WH (1991) Cellular immune response of a marsupial, Monodelphis domestica. Dev Comp Immunol 15:189–199.

    Article  PubMed  CAS  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 

  • Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexs. Immunogenetics 56:683–695.

    Article  PubMed  CAS  Google Scholar 

  • Klein J (1986) Natural History of the Major Histocompatibility Complex. Wiley, New York.

    Google Scholar 

  • Kumanovics A, Takada T, Lindahl KF (2003) Genomic organization of the mammalian MHC. Annu Rev Immunol 21:629–657.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lam MKP, 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 

  • LaPlante ES, Burrell R, Watre AL, Taylor DL, Zimmermann B (1969) Skin allograft studies in the pouch of the young opossum. Transplantation 7:67–72.

    Article  PubMed  CAS  Google Scholar 

  • Mayer WE, Williams NS, O’hUigin C, Vincek V, Zaleska-Rutczynska Z, Klein J (1993) Class I major histocompatibility complex genes of the red-necked wallaby, Macropus rufogriseus. Mol Phylogenet Evol 2:23–30.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Meyer-Lucht Y, Otten C, Puttker T, Sommer S (2008) Selection, diversity and evolutionary patterns of the MHC class II DAB in free-ranging Neotropical marsupials. BMC Genetics 9:39.

    Article  PubMed  Google Scholar 

  • Miller HC, Lambert DM (2004) Genetic drift outweighs balancing selection in sha** post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Mol Ecol 13:3709–3721.

    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, Wright AM, Lundgren R, et al. (2004) Analysis of a marsupial MHC region containing two recently duplicated class I loci. Mamm Genome 15:851–864.

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Gu X, Sitnikova T (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci USA 94:7799–7806.

    Article  PubMed  CAS  Google Scholar 

  • Nilsson MA, Gullberg A, Spotorno AE, Arnason U, Janke A (2003) Radiation of extant marsupials after the K/T boundary: evidence from complete mitochondrial genomes. J Mol Evol 57:S3–S12.

    Article  PubMed  CAS  Google Scholar 

  • O’Brien S, Evermann J (1988) Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol 3:254–259.

    Article  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.

    Article  PubMed  Google Scholar 

  • Old JM, Carman RL, Fry G, Deane EM (2006) The immune tissues of the endangered red-tailed phascogale (Phascogale calura). J Anat 208:381–387.

    Article  PubMed  CAS  Google Scholar 

  • Parham P, Strominger JL (eds) (1982) Histocompatibility Antigens Structure and Function. Receptors and Recognition Series B, Vol 14. Chapman and Hall, New York.

    Google Scholar 

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

    Google Scholar 

  • Pieters J (2000) MHC class II-restricted antigen processing and presentation. Adv Immunol 75:159–208.

    Article  PubMed  CAS  Google Scholar 

  • Potts WK, Slev PR (1995) Pathogen-based models favoring MHC genetic diversity. Immunol Rev 143:181–197.

    Article  PubMed  CAS  Google Scholar 

  • Rowlands DT (1976) Immunity in prototherian and metatherian mammals. In: Marchalonis JJ (ed) Comparative Immunology. Blackwell Scientific, London, pp. 367–389.

    Google Scholar 

  • Santucci F, Ibrahim KM, Bruzzone A, Hewit GM (2007) Selection on MHC-linked microsatellite loci in sheep populations. Heredity 99:340–348.

    Article  PubMed  CAS  Google Scholar 

  • Sato A, Figueroa F, Murray BW, et al. (2000) Nonlinkage of major histocompatibility complex classI and classII loci in bony fishes. Immunogenetics 51:108–116.

    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 

  • Siddle HV, Kreiss A, Eldridge MDB, et al. (2007a) Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proc Natl Acad Sci USA 104:16221–16226.

    Article  PubMed  CAS  Google Scholar 

  • Siddle HV, Marzec J, Cheng Y, Jones M, Belov K (2010) MHC gene copy number variation in Tasmanian devils: implications for the spread of a contagious cancer. Proc Biol Sci. Published online March 10, 2010 doi:10.1098/rspb.2009.2362.

    Google Scholar 

  • Siddle HV, Sanderson C, Belov K (2007b) Characterization of major histocompatibility complex class I and class II genes from the Tasmanian devil (Sarcophilus harrisii). Immunogenetics 59:753–760.

    Article  PubMed  CAS  Google Scholar 

  • Siddle HV, Deakin JE, Coggill P, et al. (2009) MHC-linked and un-linked class I genes in the wallaby. BMC Genomics 10:310.

    Article  PubMed  Google Scholar 

  • Slade RW, Mayer WE (1995) The expressed class II alpha-chain genes of the marsupial major histocompatibility complex belong to eutherian mammal gene families. Mol Biol Evol 12:441–450.

    PubMed  CAS  Google Scholar 

  • Slade RW, Hale PT, Francis DI, Graves JAM, Sturm RA (1994) The marsupial MHC: the tammar wallaby, Macropus eugenii, contains an expressed DNA-like gene on chromosome 1. J Mol Evol 38:496–505.

    Article  PubMed  CAS  Google Scholar 

  • Stone WH, Samples NK, Kraig E, VandeBerg JL (1987) Definition of class I antigens of the MHC of a marsupial (Monodelphis domestica). Arch Zootec 36:219–235.

    Google Scholar 

  • Stone WH, Manis GS, Hoffman ES, Saphire DG, Hubbard GB, VandeBerg JL (1997) Fate of allogeneic skin transplantations in a marsupial (Monodelphis domestica). Lab Anim Sci 47:283–287.

    PubMed  CAS  Google Scholar 

  • Stone WH, Bruun DA, Fuqua C, et al. (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 

  • Trowsdale J, Powis SH (1992) The Mhc: relationship between linkage and function. Curr Opin Genet Dev 2:492–497.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wilson DB, Fox DH, Rowlands DT (1976) Proliferative reactivity of opossum peripheral blood leukocytes to allogeneic cells, mitogens and specific antigens. Transplantation 21:164–167.

    Article  PubMed  Google Scholar 

  • Yadav M, Waring H, Stanley NF (1974) Effect of thymectomy on skin allograft survival in a macropod marsupial Setonix brachyurus. Transplantation 17:30–36.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by the Australian Research Council. We thank our fabulous collaborators Stephan Beck (University College London), Janine Deakin (Australian National University), Rob Miller (University of New Mexico) and Michelle Baker (University of New Mexico) for their contributions to this work.

Author information

Authors and Affiliations

  1. Faculty of Veterinary Science, The University of Sydney, Sydney, NSW, 2006, Australia

    Yuanyuan Cheng, Hannah V. Siddle & Katherine Belov

Authors
  1. Yuanyuan Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hannah V. Siddle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katherine Belov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katherine Belov .

Editor information

Editors and Affiliations

  1. , Ecology, Evolution&Genetics, The Austral, ARC Centre for Excellence for Kangaroo G, Research School of Biology, building 46, Canberra ACT, 0200, Australia

    Janine E. Deakin

  2. , Ecology, Evolution&Genetics, The Austral, ARC Centre for Excellence for Kangaroo G, Research School of Biology, building 46, Canberra ACT, 0200, Australia

    Paul D. Waters

  3. , Ecology, Evolution and Genetics, ARC Centre of Excellence for Kangaroo Ge, Buidling 46, Canberra ACT, 0200, Australia

    Jennifer A. Marshall Graves

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Cheng, Y., Siddle, H.V., Belov, K. (2010). The Marsupial Major Histocompatibility Complex. In: Deakin, J., Waters, P., Marshall Graves, J. (eds) Marsupial Genetics and Genomics. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9023-2_16

Download citation

Publish with us

Policies and ethics

Search

Navigation