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


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.


Vyšlo v časopise: Genomic Restructuring in the Tasmanian Devil Facial Tumour: Chromosome Painting and Gene Mapping Provide Clues to Evolution of a Transmissible Tumour. PLoS Genet 8(2): e32767. doi:10.1371/journal.pgen.1002483
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002483

Souhrn

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.


Zdroje

1. HawkinsCEBaarsCHestermanHHockingGJJonesME 2006 Emerging disease and population decline of an island endemic, the Tasmanian devil Sarcophilus harrisii. Biological Conservation 131 307 324

2. LachishSJonesMMccallumH 2007 The impact of disease on the survival and population growth rate of the Tasmanian devil. Journal of Animal Ecology 76 926 936

3. JonesMECockburnAHamedeRHawkinsCHestermanH 2008 Life-history change in disease-ravaged Tasmanian devil populations. Proceedings of the National Academy of Sciences of the United States of America 105 10023 10027

4. McCallumHTompkinsDMJonesMLachishSMarvanekS 2007 Distribution and impacts of Tasmanian devil facial tumor disease. Ecohealth 4 318 325

5. PyecroftSBPearseAMLohRSwiftKBelovK 2007 Towards a case definition for devil facial tumour disease: What is it? Ecohealth 4 346 351

6. JonesMMcCallumH 2007 Managing an emerging disease in a threatened species: Tasmanian devil facial tumour disease. Australian & New Zealand Journal of Obstetrics & Gynaecology 47 A16 A16

7. MurchisonEPTovarCHsuABenderHSKheradpourP 2010 The Tasmanian Devil Transcriptome Reveals Schwann Cell Origins of a Clonally Transmissible Cancer. Science 327 84 87

8. PearseAMSwiftK 2006 Allograft theory: Transmission of devil facial-tumour disease. Nature 439 549 549

9. SiddleHVKreissAEldridgeMDNoonanEClarkeCJ 2007 Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proc Natl Acad Sci U S A 104 16221 16226

10. DasUDasAK 2000 Review of canine transmissible venereal sarcoma. Vet Res Commun 24 545 556

11. HaymanDLMartinPG 1974 Mammalia I: Monotremata and Marsupialia. JohnB Animal Cytogenetics Berlin and Stuttgart Gebriider Borntraeger

12. RofeRHaymanD 1985 G-banding evidence for a conserved complement in the Marsupialia. Cytogenet Cell Genet 39 40 50

13. YoungGJGravesJAMBarbieriIWoolleyPACooperDW 1982 The chromosomes of dasyurids (Marsupialia). ArcherM Carnivorous Marsupials Sydney Royal Zoological Society of New South Wales 783 795

14. De LeoAAGuedelhaNToderRVoullaireLFerguson-SmithMA 1999 Comparative chromosome painting between marsupial orders: relationships with a 2n = 14 ancestral marsupial karyotype. Chromosome Res 7 509 517

15. RensWO'BrienPCFaircloughHHarmanLGravesJA 2003 Reversal and convergence in marsupial chromosome evolution. Cytogenetic and Genome Research 102 282 290

16. MikkelsenTSWakefieldMJAkenBAmemiyaCTChangJL 2007 Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature 447 167 177

17. RenfreeMBPapenfussATDeakinJELindsayJHeiderT 2011 Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development. Genome Biol 12 R81

18. RensWO'BrienPCYangFGravesJAFerguson-SmithMA 1999 Karyotype relationships between four distantly related marsupials revealed by reciprocal chromosome painting. Chromosome Res 7 461 474

19. CRES 2006 Sarcophilus harrisii (Tasmanian Devil). O'Brien SJMenningerJCNashWG Atlas of Mammalian Chromosomes New York Wiley 30

20. MartinPGHaymanDL 1967 Quantitative comparisons between karyotypes of Australian marsupials from 3 different superfamilies. Chromosoma 20 290 &

21. MorozovaOMarraMA 2008 From cytogenetics to next-generation sequencing technologies: advances in the detection of genome rearrangements in tumors. Biochem Cell Biol 86 81 91

22. CampbellPJStephensPJPleasanceEDO'MearaSLiH 2008 Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing. Nat Genet 40 722 729

23. AsthagiriARParryDMButmanJAKimHJTsilouET 2009 Neurofibromatosis type 2. Lancet 373 1974 1986

24. McClatcheyAISaotomeIMercerKCrowleyDGusellaJF 1998 Mice heterozygous for a mutation at the Nf2 tumor suppressor locus develop a range of highly metastatic tumors. Genes Dev 12 1121 1133

25. NowellPC 1976 The clonal evolution of tumor cell populations. Science 194 23 28

26. LengauerCKinzlerKWVogelsteinB 1997 DNA methylation and genetic instability in colorectal cancer cells. Proc Natl Acad Sci U S A 94 2545 2550

27. JonesSChenWDParmigianiGDiehlFBeerenwinkelN 2008 Comparative lesion sequencing provides insights into tumor evolution. Proc Natl Acad Sci U S A 105 4283 4288

28. ShackletonMQuintanaEFearonERMorrisonSJ 2009 Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell 138 822 829

29. McCallumH 2008 Tasmanian devil facial tumour disease: lessons for conservation biology. Trends Ecol Evol 23 631 637

30. LohRBergfeldJHayesDO'HaraAPyecroftS 2006 The pathology of devil facial tumor disease (DFTD) in Tasmanian Devils (Sarcophilus harrisii). Vet Pathol 43 890 895

31. StephensPJGreenmanCDFuBYangFBignellGR 2011 Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144 27 40

32. der-SarkissianHBacchettiSCazesLLondono-VallejoJA 2004 The shortest telomeres drive karyotype evolution in transformed cells. Oncogene 23 1221 1228

33. McGlashanNDObendorfDL 2008 Research priorities in the Tasmanian devil facial tumour debate. European Journal of Oncology 13 229 238

34. MurphyWJLarkinDMEverts-van der WindABourqueGTeslerG 2005 Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309 613 617

35. KemkemerCKohnMCooperDNFroenickeLHogelJ 2009 Gene synteny comparisons between different vertebrates provide new insights into breakage and fusion events during mammalian karyotype evolution. BMC Evol Biol 9 84

36. LachishSMcCallumHMannDPukkCEJonesME 2010 Evaluation of selective culling of infected individuals to control Tasmanian Devil Facial Tumor Disease. Conservation Biology 24 841 851

37. Ferguson-SmithMA 1997 Genetic analysis by chromosome sorting and painting: phylogenetic and diagnostic applications. Eur J Hum Genet 5 253 265

38. SankovicNDelbridgeMLGrütznerFFerguson-SmithMAO'BrienPC 2006 Construction of a highly enriched marsupial Y chromosome-specific BAC sub-library using isolated Y chromosomes. Chromosome Res 14 657 664

39. TeleniusHCarterNPBebbCENordenskjoldMPonderBA 1992 Degenerate oligonucleotide-primed PCR: general amplification of target DNA by a single degenerate primer. Genomics 13 718 725

40. AlsopAEMiethkePRofeRKoinaESankovicN 2005 Characterizing the chromosomes of the Australian model marsupial Macropus eugenii (tammar wallaby). Chromosome Res 13 627 636

41. OsoegawaKWoonPYZhaoBFrengenETatenoM 1998 An improved approach for construction of bacterial artificial chromosome libraries. Genomics 52 1 8

42. AmemiyaCTOtaTLitmanGW 1996 Construction of P1 artificial chromosome (PAC) libraries from lower vertebrates. BirrenBLaiE Nonmammalian Genomic Analyses: A Practical Guide San Diego: Academic Press 223 256

43. DeakinJEKoinaEWatersPDDohertyRPatelVS 2008 Physical map of two tammar wallaby chromosomes: a strategy for mapping in non-model mammals. Chromosome Res 16 1159 1175

44. MohammadiADelbridgeMLWatersPDGravesJA 2009 Conservation of a chromosome arm in two distantly related marsupial species. Cytogenetic and Genome Research 124 147 150

45. RossMTLaBrieSMcPhersonJStantonVPJ 1999 Screening large-insert libraries by hybridization. BoylA Current protocols in human genetics New York Wiley 5.6.1 5.6.52

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