Genomic Restructuring in the Tasmanian Devil Facial Tumour: Chromosome Painting and Gene Mapping Provide Clues to Evolution of a Transmissible Tumour

Janine Deakin, Hannah Bender, Anne-Maree Pearse, Willem Rens, Patricia O'Brien, Malcolm Ferguson-Smith, Yuanyuan Cheng, Katrina Morris, Robyn Taylor, Andrew Stuart, Katherine Belov, Chris Amemiya, Elizabeth Murchison, Anthony Papenfuss, Jennifer Marshall Graves

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    Abstract

    Devil facial tumour disease (DFTD) is a fatal, transmissible malignancy that threatens the world’s largest marsupial carnivore, the Tasmanian devil, with extinction. First recognised in 1996, DFTD has had a catastrophic effect on wild devil numbers, and intense research efforts to understand and contain the disease have since demonstrated that the tumour is a clonal cell line transmitted by allograft. We used chromosome painting and gene mapping to deconstruct the DFTD karyotype and determine the chromosome and gene rearrangements involved in carcinogenesis. Chromosome painting on three different DFTD tumour strains determined the origins of marker chromosomes and provided a general overview of the rearrangement in DFTD karyotypes. Mapping of 105 BAC clones by fluorescence in situ hybridisation provided a finer level of resolution of genome rearrangements in DFTD strains. Our findings demonstrate that only limited regions of the genome, mainly chromosomes 1 and X, are rearranged in DFTD. Regions rearranged in DFTD are also highly rearranged between different marsupials. Differences between strains are limited, reflecting the unusually stable nature of DFTD. Finally, our detailed maps of both the devil and tumour karyotypes provide a physical framework for future genomic investigations into DFTD.
    Original languageEnglish
    Pages (from-to)1-16
    Number of pages16
    JournalPLoS Genetics
    Volume8
    DOIs
    Publication statusPublished - 2012

    Fingerprint

    Chromosome Painting
    Chromosome Mapping
    tumor
    chromosome mapping
    chromosome
    genomics
    neoplasms
    gene
    Neoplasms
    karyotype
    karyotyping
    Karyotype
    Marsupialia
    marsupial
    Metatheria
    chromosomes
    chromosome painting
    genome
    Genome
    allografting

    Cite this

    Deakin, Janine ; Bender, Hannah ; Pearse, Anne-Maree ; Rens, Willem ; O'Brien, Patricia ; Ferguson-Smith, Malcolm ; Cheng, Yuanyuan ; Morris, Katrina ; Taylor, Robyn ; Stuart, Andrew ; Belov, Katherine ; Amemiya, Chris ; Murchison, Elizabeth ; Papenfuss, Anthony ; Marshall Graves, Jennifer. / Genomic Restructuring in the Tasmanian Devil Facial Tumour: Chromosome Painting and Gene Mapping Provide Clues to Evolution of a Transmissible Tumour. In: PLoS Genetics. 2012 ; Vol. 8. pp. 1-16.
    @article{438adcd8b8944ae1a6f66a594fff379e,
    title = "Genomic Restructuring in the Tasmanian Devil Facial Tumour: Chromosome Painting and Gene Mapping Provide Clues to Evolution of a Transmissible Tumour",
    abstract = "Devil facial tumour disease (DFTD) is a fatal, transmissible malignancy that threatens the world’s largest marsupial carnivore, the Tasmanian devil, with extinction. First recognised in 1996, DFTD has had a catastrophic effect on wild devil numbers, and intense research efforts to understand and contain the disease have since demonstrated that the tumour is a clonal cell line transmitted by allograft. We used chromosome painting and gene mapping to deconstruct the DFTD karyotype and determine the chromosome and gene rearrangements involved in carcinogenesis. Chromosome painting on three different DFTD tumour strains determined the origins of marker chromosomes and provided a general overview of the rearrangement in DFTD karyotypes. Mapping of 105 BAC clones by fluorescence in situ hybridisation provided a finer level of resolution of genome rearrangements in DFTD strains. Our findings demonstrate that only limited regions of the genome, mainly chromosomes 1 and X, are rearranged in DFTD. Regions rearranged in DFTD are also highly rearranged between different marsupials. Differences between strains are limited, reflecting the unusually stable nature of DFTD. Finally, our detailed maps of both the devil and tumour karyotypes provide a physical framework for future genomic investigations into DFTD.",
    author = "Janine Deakin and Hannah Bender and Anne-Maree Pearse and Willem Rens and Patricia O'Brien and Malcolm Ferguson-Smith and Yuanyuan Cheng and Katrina Morris and Robyn Taylor and Andrew Stuart and Katherine Belov and Chris Amemiya and Elizabeth Murchison and Anthony Papenfuss and {Marshall Graves}, Jennifer",
    year = "2012",
    doi = "10.1371/journal.pgen.1002483",
    language = "English",
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    Deakin, J, Bender, H, Pearse, A-M, Rens, W, O'Brien, P, Ferguson-Smith, M, Cheng, Y, Morris, K, Taylor, R, Stuart, A, Belov, K, Amemiya, C, Murchison, E, Papenfuss, A & Marshall Graves, J 2012, 'Genomic Restructuring in the Tasmanian Devil Facial Tumour: Chromosome Painting and Gene Mapping Provide Clues to Evolution of a Transmissible Tumour', PLoS Genetics, vol. 8, pp. 1-16. https://doi.org/10.1371/journal.pgen.1002483

    Genomic Restructuring in the Tasmanian Devil Facial Tumour: Chromosome Painting and Gene Mapping Provide Clues to Evolution of a Transmissible Tumour. / Deakin, Janine; Bender, Hannah; Pearse, Anne-Maree; Rens, Willem; O'Brien, Patricia; Ferguson-Smith, Malcolm; Cheng, Yuanyuan; Morris, Katrina; Taylor, Robyn; Stuart, Andrew; Belov, Katherine; Amemiya, Chris; Murchison, Elizabeth; Papenfuss, Anthony; Marshall Graves, Jennifer.

    In: PLoS Genetics, Vol. 8, 2012, p. 1-16.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Genomic Restructuring in the Tasmanian Devil Facial Tumour: Chromosome Painting and Gene Mapping Provide Clues to Evolution of a Transmissible Tumour

    AU - Deakin, Janine

    AU - Bender, Hannah

    AU - Pearse, Anne-Maree

    AU - Rens, Willem

    AU - O'Brien, Patricia

    AU - Ferguson-Smith, Malcolm

    AU - Cheng, Yuanyuan

    AU - Morris, Katrina

    AU - Taylor, Robyn

    AU - Stuart, Andrew

    AU - Belov, Katherine

    AU - Amemiya, Chris

    AU - Murchison, Elizabeth

    AU - Papenfuss, Anthony

    AU - Marshall Graves, Jennifer

    PY - 2012

    Y1 - 2012

    N2 - Devil facial tumour disease (DFTD) is a fatal, transmissible malignancy that threatens the world’s largest marsupial carnivore, the Tasmanian devil, with extinction. First recognised in 1996, DFTD has had a catastrophic effect on wild devil numbers, and intense research efforts to understand and contain the disease have since demonstrated that the tumour is a clonal cell line transmitted by allograft. We used chromosome painting and gene mapping to deconstruct the DFTD karyotype and determine the chromosome and gene rearrangements involved in carcinogenesis. Chromosome painting on three different DFTD tumour strains determined the origins of marker chromosomes and provided a general overview of the rearrangement in DFTD karyotypes. Mapping of 105 BAC clones by fluorescence in situ hybridisation provided a finer level of resolution of genome rearrangements in DFTD strains. Our findings demonstrate that only limited regions of the genome, mainly chromosomes 1 and X, are rearranged in DFTD. Regions rearranged in DFTD are also highly rearranged between different marsupials. Differences between strains are limited, reflecting the unusually stable nature of DFTD. Finally, our detailed maps of both the devil and tumour karyotypes provide a physical framework for future genomic investigations into DFTD.

    AB - Devil facial tumour disease (DFTD) is a fatal, transmissible malignancy that threatens the world’s largest marsupial carnivore, the Tasmanian devil, with extinction. First recognised in 1996, DFTD has had a catastrophic effect on wild devil numbers, and intense research efforts to understand and contain the disease have since demonstrated that the tumour is a clonal cell line transmitted by allograft. We used chromosome painting and gene mapping to deconstruct the DFTD karyotype and determine the chromosome and gene rearrangements involved in carcinogenesis. Chromosome painting on three different DFTD tumour strains determined the origins of marker chromosomes and provided a general overview of the rearrangement in DFTD karyotypes. Mapping of 105 BAC clones by fluorescence in situ hybridisation provided a finer level of resolution of genome rearrangements in DFTD strains. Our findings demonstrate that only limited regions of the genome, mainly chromosomes 1 and X, are rearranged in DFTD. Regions rearranged in DFTD are also highly rearranged between different marsupials. Differences between strains are limited, reflecting the unusually stable nature of DFTD. Finally, our detailed maps of both the devil and tumour karyotypes provide a physical framework for future genomic investigations into DFTD.

    U2 - 10.1371/journal.pgen.1002483

    DO - 10.1371/journal.pgen.1002483

    M3 - Article

    VL - 8

    SP - 1

    EP - 16

    JO - PLoS Genetics

    JF - PLoS Genetics

    SN - 1553-7390

    ER -