Home LiteratureArticle Details
PMID: 22341448 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Genome sequencing and analysis of the Tasmanian devil and its transmissible cancer.

Cell ·Vol. 148 ·No. 4 ·2012-02-17 ·Pages 780-91

Murchison EP, Schulz-Trieglaff OB, Ning Z, Alexandrov LB, Bauer MJ, Fu B, Hims M, Ding Z, Ivakhno S, Stewart C, Ng BL, Wong W, Aken B, White S, Alsop A, Becq J, Bignell GR, Cheetham RK, Cheng W, Connor TR, Cox AJ, Feng ZP, Gu Y, Grocock RJ, Harris SR, Khrebtukova I, Kingsbury Z, Kowarsky M, Kreiss A, Luo S, Marshall J, McBride DJ, Murray L, Pearse AM, Raine K, Rasolonjatovo I, Shaw R, Tedder P, Tregidgo C, Vilella AJ, Wedge DC, Woods GM, Gormley N, Humphray S, Schroth G, Smith G, Hall K, Searle SM, Carter NP, Papenfuss AT, Futreal PA, Campbell PJ, Yang F, Bentley DR, Evers DJ, Stratton MR

Abstract

The Tasmanian devil (Sarcophilus harrisii), the largest marsupial carnivore, is endangered due to a transmissible facial cancer spread by direct transfer of living cancer cells through biting. Here we describe the sequencing, assembly, and annotation of the Tasmanian devil genome and whole-genome sequences for two geographically distant subclones of the cancer. Genomic analysis suggests that the cancer first arose from a female Tasmanian devil and that the clone has subsequently genetically diverged during its spread across Tasmania. The devil cancer genome contains more than 17,000 somatic base substitution mutations and bears the imprint of a distinct mutational process. Genotyping of somatic mutations in 104 geographically and temporally distributed Tasmanian devil tumors reveals the pattern of evolution and spread of this parasitic clonal lineage, with evidence of a selective sweep in one geographical area and persistence of parallel lineages in other populations.

MeSH Terms
Animals Clonal Evolution Endangered Species Facial Neoplasms/epidemiology,genetics,pathology,veterinary Female Genome-Wide Association Study Genomic Instability Male Marsupialia/genetics Molecular Sequence Data Mutation Tasmania/epidemiology
Authors & Affiliations
56 authors, click to expand affiliations / ORCID
Murchison Elizabeth P
Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK. [email protected]
Schulz-Trieglaff Ole B
Ning Zemin
Alexandrov Ludmil B
Bauer Markus J
Fu Beiyuan
Hims Matthew
Ding Zhihao
Ivakhno Sergii
Stewart Caitlin
Ng Bee Ling
Wong Wendy
Aken Bronwen
White Simon
Alsop Amber
Becq Jennifer
Bignell Graham R
Cheetham R Keira
Cheng William
Connor Thomas R
Cox Anthony J
Feng Zhi-Ping
Gu Yong
Grocock Russell J
Harris Simon R
Khrebtukova Irina
Kingsbury Zoya
Kowarsky Mark
Kreiss Alexandre
Luo Shujun
Marshall John
McBride David J
Murray Lisa
Pearse Anne-Maree
Raine Keiran
Rasolonjatovo Isabelle
Shaw Richard
Tedder Philip
Tregidgo Carolyn
Vilella Albert J
Wedge David C
Woods Gregory M
Gormley Niall
Humphray Sean
Schroth Gary
Smith Geoffrey
Hall Kevin
Searle Stephen M J
Carter Nigel P
Papenfuss Anthony T
Futreal P Andrew
Campbell Peter J
Yang Fengtang
Bentley David R
Evers Dirk J
Stratton Michael R
References (57)
57 references, click to expand
  1. Computational detection and location of transcription start sites in mammalian genomic DNA.
    Genome Res. 2002 Mar;12(3):458-61 PMID: 11875034
  2. A census of human cancer genes.
    Nat Rev Cancer. 2004 Mar;4(3):177-83 PMID: 14993899
  3. The phusion assembler.
    Genome Res. 2003 Jan;13(1):81-90 PMID: 12529309
  4. A comprehensive catalogue of somatic mutations from a human cancer genome.
    Nature. 2010 Jan 14;463(7278):191-6 PMID: 20016485
  5. GeneWise and Genomewise.
    Genome Res. 2004 May;14(5):988-95 PMID: 15123596
  6. Allorecognition in the Tasmanian devil (Sarcophilus harrisii), an endangered marsupial species with limited genetic diversity.
    PLoS One. 2011;6(7):e22402 PMID: 21811598
  7. Computational identification of promoters and first exons in the human genome.
    Nat Genet. 2001 Dec;29(4):412-7 PMID: 11726928
  8. Array painting: a protocol for the rapid analysis of aberrant chromosomes using DNA microarrays.
    Nat Protoc. 2009;4(12):1722-36 PMID: 19893508
  9. Accurate whole human genome sequencing using reversible terminator chemistry.
    Nature. 2008 Nov 6;456(7218):53-9 PMID: 18987734
  10. Prediction of complete gene structures in human genomic DNA.
    J Mol Biol. 1997 Apr 25;268(1):78-94 PMID: 9149143
  11. Transmission dynamics of Tasmanian devil facial tumor disease may lead to disease-induced extinction.
    Ecology. 2009 Dec;90(12):3379-92 PMID: 20120807
  12. 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. 2007 Oct 9;104(41):16221-6 PMID: 17911263
  13. Donor derived malignancy following transplantation: a review.
    Cell Tissue Bank. 2007;8(4):267-86 PMID: 17440834
  14. Fast and accurate short read alignment with Burrows-Wheeler transform.
    Bioinformatics. 2009 Jul 15;25(14):1754-60 PMID: 19451168
  15. Patterns of somatic mutation in human cancer genomes.
    Nature. 2007 Mar 8;446(7132):153-8 PMID: 17344846
  16. Swine chromosomal DNA quantification by bivariate flow karyotyping and karyotype interpretation.
    Cytometry. 1992;13(7):703-10 PMID: 1451601
  17. The impact of disease on the survival and population growth rate of the Tasmanian devil.
    J Anim Ecol. 2007 Sep;76(5):926-36 PMID: 17714271
  18. BTL-II: a polymorphic locus with homology to the butyrophilin gene family, located at the border of the major histocompatibility complex class II and class III regions in human and mouse.
    Immunogenetics. 2000 Apr;51(4-5):373-82 PMID: 10803852
  19. A comparative study of karyotypes of muntjacs by chromosome painting.
    Chromosoma. 1995 May;103(9):642-52 PMID: 7587587
  20. The pathology of devil facial tumor disease (DFTD) in Tasmanian Devils (Sarcophilus harrisii).
    Vet Pathol. 2006 Nov;43(6):890-5 PMID: 17099145
  21. Clonally transmissible cancers in dogs and Tasmanian devils.
    Oncogene. 2008 Dec;27 Suppl 2:S19-30 PMID: 19956175
  22. Quantitative comparisons between the karyotypes of Australian marsupials from three different superfamilies.
    Chromosoma. 1967;20(3):290-310 PMID: 5613986
  23. Mitochondrial capture by a transmissible cancer.
    Science. 2011 Jan 21;331(6015):303 PMID: 21252340
  24. A fast and symmetric DUST implementation to mask low-complexity DNA sequences.
    J Comput Biol. 2006 Jun;13(5):1028-40 PMID: 16796549
  25. A large genome center's improvements to the Illumina sequencing system.
    Nat Methods. 2008 Dec;5(12):1005-10 PMID: 19034268
  26. Origins and evolution of a transmissible cancer.
    Evolution. 2009 Sep;63(9):2340-9 PMID: 19453727
  27. Automated generation of heuristics for biological sequence comparison.
    BMC Bioinformatics. 2005 Feb 15;6:31 PMID: 15713233
  28. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence.
    Nucleic Acids Res. 1997 Mar 1;25(5):955-64 PMID: 9023104
  29. Chromosome heteromorphism quantified by high-resolution bivariate flow karyotyping.
    Am J Hum Genet. 1989 Nov;45(5):739-52 PMID: 2479266
  30. Rfam: an RNA family database.
    Nucleic Acids Res. 2003 Jan 1;31(1):439-41 PMID: 12520045
  31. Tandem repeats finder: a program to analyze DNA sequences.
    Nucleic Acids Res. 1999 Jan 15;27(2):573-80 PMID: 9862982
  32. Homotransplantation of human cell lines.
    Science. 1957 Jan 25;125(3239):158-60 PMID: 13390981
  33. Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil).
    Proc Natl Acad Sci U S A. 2011 Jul 26;108(30):12348-53 PMID: 21709235
  34. The Ensembl automatic gene annotation system.
    Genome Res. 2004 May;14(5):942-50 PMID: 15123590
  35. Database resources of the National Center for Biotechnology Information.
    Nucleic Acids Res. 2010 Jan;38(Database issue):D5-16 PMID: 19910364
  36. Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences.
    Nature. 2007 May 10;447(7141):167-77 PMID: 17495919
  37. Chromosome specific paints from a high resolution flow karyotype of the mouse.
    Nat Genet. 1995 Apr;9(4):369-75 PMID: 7795642
  38. Transplacental and other routes of cancer transmission between individuals.
    J Pediatr Hematol Oncol. 2003 Jun;25(6):430-4 PMID: 12794519
  39. Allograft theory: transmission of devil facial-tumour disease.
    Nature. 2006 Feb 2;439(7076):549 PMID: 16452970
  40. A small-cell lung cancer genome with complex signatures of tobacco exposure.
    Nature. 2010 Jan 14;463(7278):184-90 PMID: 20016488
  41. novoSNP, a novel computational tool for sequence variation discovery.
    Genome Res. 2005 Mar;15(3):436-42 PMID: 15741513
  42. Extensive conservation of genomic imbalances in canine transmissible venereal tumors (CTVT) detected by microarray-based CGH analysis.
    Chromosome Res. 2009;17(7):927-34 PMID: 19798471
  43. Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development.
    Genome Biol. 2011 Aug 29;12(8):R81 PMID: 21854559
  44. Circular binary segmentation for the analysis of array-based DNA copy number data.
    Biostatistics. 2004 Oct;5(4):557-72 PMID: 15475419
  45. Regulation of costimulation in the era of butyrophilins.
    Cytokine. 2009 Jun;46(3):370-5 PMID: 19380239
  46. The Ensembl analysis pipeline.
    Genome Res. 2004 May;14(5):934-41 PMID: 15123589
  47. Conservation of small RNA pathways in platypus.
    Genome Res. 2008 Jun;18(6):995-1004 PMID: 18463306
  48. Genetic diversity and population structure of Tasmanian devils, the largest marsupial carnivore.
    Mol Ecol. 2004 Aug;13(8):2197-209 PMID: 15245394
  49. Flow analysis and sorting of microchromosomes (<3 Mb).
    Cytometry A. 2007 Jun;71(6):410-3 PMID: 17342775
  50. Clonal origin and evolution of a transmissible cancer.
    Cell. 2006 Aug 11;126(3):477-87 PMID: 16901782
  51. miRBase: microRNA sequences, targets and gene nomenclature.
    Nucleic Acids Res. 2006 Jan 1;34(Database issue):D140-4 PMID: 16381832
  52. A new bioinformatics analysis tools framework at EMBL-EBI.
    Nucleic Acids Res. 2010 Jul;38(Web Server issue):W695-9 PMID: 20439314
  53. The Tasmanian devil transcriptome reveals Schwann cell origins of a clonally transmissible cancer.
    Science. 2010 Jan 1;327(5961):84-7 PMID: 20044575
  54. DNA content measurement for DNA ploidy and cell cycle analysis.
    Curr Protoc Cytom. 2001 May;Chapter 7:Unit 7.5 PMID: 18770732
  55. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  56. Genetic analysis of a sarcoma accidentally transplanted from a patient to a surgeon.
    N Engl J Med. 1996 Nov 14;335(20):1494-6 PMID: 8890100
  57. The immunohistochemical characterization of devil facial tumor disease (DFTD) in the Tasmanian Devil (Sarcophilus harrisii).
    Vet Pathol. 2006 Nov;43(6):896-903 PMID: 17099146
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
DOI
10.1016/j.cell.2011.11.065
Email
[email protected]
Published
2012-02-17
Pages
780-91
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC3281993
Subset
IM
Grants
Wellcome Trust · 088340 · United Kingdom
Wellcome Trust · 095908 · United Kingdom
Wellcome Trust · 077012/Z/05/Z · United Kingdom
Databases
GENBANK
AEFK00000000, JN216828
External Links
PubMed source DOI: 10.1016/j.cell.2011.11.065 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2