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Research Article

A second transmissible cancer in Tasmanian devils

Ruth J. Pye, David Pemberton, Cesar Tovar, Jose M. C. Tubio, Karen A. Dun, Samantha Fox, Jocelyn Darby, Dane Hayes, Graeme W. Knowles, Alexandre Kreiss, Hannah V. T. Siddle, Kate Swift, A. Bruce Lyons, Elizabeth P. Murchison, and Gregory M. Woods
  1. aMenzies Institute for Medical Research, University of Tasmania, Hobart, TAS 7000, Australia;
  2. bSave the Tasmanian Devil Program, Tasmanian Department of Primary Industries, Parks, Water and the Environment, Hobart, TAS 7000, Australia;
  3. cDepartment of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES, United Kingdom;
  4. dDepartment of Cytogenetics, Royal Hobart Hospital, Hobart, TAS 7000, Australia;
  5. eMount Pleasant Laboratories, Tasmanian Department of Primary Industries, Parks, Water and the Environment, Prospect, TAS 7250, Australia;
  6. fCentre for Biological Science, University of Southampton, Highfield Campus, Southampton SO17 1BJ, United Kingdom;
  7. gSchool of Medicine, University of Tasmania, Hobart, TAS 7000, Australia

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PNAS January 12, 2016 113 (2) 374-379; first published December 28, 2015; https://doi.org/10.1073/pnas.1519691113
Ruth J. Pye
aMenzies Institute for Medical Research, University of Tasmania, Hobart, TAS 7000, Australia;
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David Pemberton
bSave the Tasmanian Devil Program, Tasmanian Department of Primary Industries, Parks, Water and the Environment, Hobart, TAS 7000, Australia;
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Cesar Tovar
aMenzies Institute for Medical Research, University of Tasmania, Hobart, TAS 7000, Australia;
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Jose M. C. Tubio
cDepartment of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES, United Kingdom;
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Karen A. Dun
dDepartment of Cytogenetics, Royal Hobart Hospital, Hobart, TAS 7000, Australia;
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Samantha Fox
bSave the Tasmanian Devil Program, Tasmanian Department of Primary Industries, Parks, Water and the Environment, Hobart, TAS 7000, Australia;
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Jocelyn Darby
aMenzies Institute for Medical Research, University of Tasmania, Hobart, TAS 7000, Australia;
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Dane Hayes
eMount Pleasant Laboratories, Tasmanian Department of Primary Industries, Parks, Water and the Environment, Prospect, TAS 7250, Australia;
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Graeme W. Knowles
eMount Pleasant Laboratories, Tasmanian Department of Primary Industries, Parks, Water and the Environment, Prospect, TAS 7250, Australia;
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Alexandre Kreiss
aMenzies Institute for Medical Research, University of Tasmania, Hobart, TAS 7000, Australia;
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Hannah V. T. Siddle
fCentre for Biological Science, University of Southampton, Highfield Campus, Southampton SO17 1BJ, United Kingdom;
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Kate Swift
eMount Pleasant Laboratories, Tasmanian Department of Primary Industries, Parks, Water and the Environment, Prospect, TAS 7250, Australia;
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A. Bruce Lyons
gSchool of Medicine, University of Tasmania, Hobart, TAS 7000, Australia
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Elizabeth P. Murchison
cDepartment of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES, United Kingdom;
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  • For correspondence: epm27@cam.ac.uk G.M.Woods@utas.edu.au
Gregory M. Woods
aMenzies Institute for Medical Research, University of Tasmania, Hobart, TAS 7000, Australia;
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  • For correspondence: epm27@cam.ac.uk G.M.Woods@utas.edu.au
  1. Edited by Stephen P. Goff, Columbia University College of Physicians and Surgeons, New York, NY, and approved November 30, 2015 (received for review October 9, 2015)

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Significance

Transmissible cancers are somatic cell lineages that are spread between individuals via the transfer of living cancer cells. Only three transmissible cancers have been reported in nature, suggesting that such diseases emerge rarely. One of the known transmissible cancers affects Tasmanian devils, and is threatening this species with extinction. Here we report the discovery of a second transmissible cancer in Tasmanian devils. This cancer causes facial tumors that are grossly indistinguishable from those caused by the first-described transmissible cancer in this species; however, tumors derived from this second clone are genetically distinct. These findings indicate that Tasmanian devils have spawned at least two different transmissible cancers, and suggest that transmissible cancers may arise more frequently in nature than previously considered.

Abstract

Clonally transmissible cancers are somatic cell lineages that are spread between individuals via the transfer of living cancer cells. There are only three known naturally occurring transmissible cancers, and these affect dogs, soft-shell clams, and Tasmanian devils, respectively. The Tasmanian devil transmissible facial cancer was first observed in 1996, and is threatening its host species with extinction. Until now, this disease has been consistently associated with a single aneuploid cancer cell lineage that we refer to as DFT1. Here we describe a second transmissible cancer, DFT2, in five devils located in southern Tasmania in 2014 and 2015. DFT2 causes facial tumors that are grossly indistinguishable but histologically distinct from those caused by DFT1. DFT2 bears no detectable cytogenetic similarity to DFT1 and carries a Y chromosome, which contrasts with the female origin of DFT1. DFT2 shows different alleles to both its hosts and DFT1 at microsatellite, structural variant, and major histocompatibility complex (MHC) loci, confirming that it is a second cancer that can be transmitted between devils as an allogeneic, MHC-discordant graft. These findings indicate that Tasmanian devils have spawned at least two distinct transmissible cancer lineages and suggest that transmissible cancers may arise more frequently in nature than previously considered. The discovery of DFT2 presents important challenges for the conservation of Tasmanian devils and raises the possibility that this species is particularly prone to the emergence of transmissible cancers. More generally, our findings highlight the potential for cancer cells to depart from their hosts and become dangerous transmissible pathogens.

  • transmissible cancer
  • contagious cancer
  • Tasmanian devil facial tumor disease
  • Tasmanian devil

Footnotes

  • ↵1E.P.M. and G.M.W. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: epm27{at}cam.ac.uk or G.M.Woods{at}utas.edu.au.
  • Author contributions: R.J.P., D.P., E.P.M., and G.M.W. designed research; R.J.P., C.T., J.M.C.T., K.A.D., S.F., J.D., D.H., G.W.K., A.K., K.S., and E.P.M. performed research; R.J.P., D.P., C.T., J.M.C.T., K.A.D., S.F., G.W.K., A.K., H.V.T.S., K.S., A.B.L., E.P.M., and G.M.W. analyzed data; and E.P.M. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. KT188437 and KT188438).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1519691113/-/DCSupplemental.

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A second transmissible cancer in Tasmanian devils
Ruth J. Pye, David Pemberton, Cesar Tovar, Jose M. C. Tubio, Karen A. Dun, Samantha Fox, Jocelyn Darby, Dane Hayes, Graeme W. Knowles, Alexandre Kreiss, Hannah V. T. Siddle, Kate Swift, A. Bruce Lyons, Elizabeth P. Murchison, Gregory M. Woods
Proceedings of the National Academy of Sciences Jan 2016, 113 (2) 374-379; DOI: 10.1073/pnas.1519691113

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A second transmissible cancer in Tasmanian devils
Ruth J. Pye, David Pemberton, Cesar Tovar, Jose M. C. Tubio, Karen A. Dun, Samantha Fox, Jocelyn Darby, Dane Hayes, Graeme W. Knowles, Alexandre Kreiss, Hannah V. T. Siddle, Kate Swift, A. Bruce Lyons, Elizabeth P. Murchison, Gregory M. Woods
Proceedings of the National Academy of Sciences Jan 2016, 113 (2) 374-379; DOI: 10.1073/pnas.1519691113
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