Mitochondrial genetic diversity, selection and recombination in a canine transmissible cancer

Andrea Strakova, Máire Ní Leathlobhair, Guo Dong Wang, Ting Ting Yin, Ilona Airikkala-Otter, Janice L. Allen, Karen M. Allum, Leontine Bansse-Issa, Jocelyn L. Bisson, Artemio Castillo Domracheva, Karina F. De Castro, Anne M. Corrigan, Hugh R. Cran, Jane T. Crawford, Stephen M. Cutter, Laura Delgadillo Keenan, Edward M. Donelan, Ibikunle A. Faramade, Erika Flores Reynoso, Eleni FotopoulouSkye N. Fruean, Fanny Gallardo-Arrieta, Olga Glebova, Rodrigo F. Häfelin Manrique, Joaquim J.G.P. Henriques, Natalia Ignatenko, Debbie Koenig, Marta Lanza-Perea, Remo Lobetti, Adriana M. Lopezquintana, Thibault Losfelt, Gabriele Marino, Inigo Martincorena, Simón Martínez Castañeda, Mayra F. Martínez-López, Michael Meyer, Berna Nakanwagi, Andrigo B. De Nardi, Winifred Neunzig, Sally J. Nixon, Marsden M. Onsare, Antonio Ortega-Pacheco, Maria C. Peleteiro, Ruth J. Pye, John F. Reece, Jose Rojas Gutierrez, Haleema Sadia, Sheila K. Schmeling, Olga Shamanova, Richard K. Ssuna, Audrey E.Alla Steenland-Smitsvitich, Ismail Thoya Ngoka, Bogdan A. Vitǎlaru, Anna P. De Vos, Johan P. De Vos, Oliver Walkinton, David C. Wedge, Alvaro S. Wehrle-Martinez, Mirjam G. Van Der Wel, Sophie Ae Widdowson, Elizabeth P. Murchison

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

Canine transmissible venereal tumour (CTVT) is a clonally transmissible cancer that originated approximately 11,000 years ago and affects dogs worldwide. Despite the clonal origin of the CTVT nuclear genome, CTVT mitochondrial genomes (mtDNAs) have been acquired by periodic capture from transient hosts. We sequenced 449 complete mtDNAs from a global population of CTVTs, and show that mtDNA horizontal transfer has occurred at least five times, delineating five tumour clades whose distributions track two millennia of dog global migration. Negative selection has operated to prevent accumulation of deleterious mutations in captured mtDNA, and recombination has caused occasional mtDNA re-assortment. These findings implicate functional mtDNA as a driver of CTVT global metastatic spread, further highlighting the important role of mtDNA in cancer evolution.

Original languageEnglish (US)
Article numbere14552
JournaleLife
Volume5
Issue numberMAY2016
DOIs
StatePublished - May 17 2016
Externally publishedYes

Fingerprint

Veterinary Venereal Tumors
Mitochondrial DNA
Genetic Recombination
Canidae
Tumors
Neoplasms
Genes
Dogs
Mitochondrial Genome
Genome
Population

ASJC Scopus subject areas

  • Neuroscience(all)
  • Medicine(all)
  • Immunology and Microbiology(all)
  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Strakova, A., Leathlobhair, M. N., Wang, G. D., Yin, T. T., Airikkala-Otter, I., Allen, J. L., ... Murchison, E. P. (2016). Mitochondrial genetic diversity, selection and recombination in a canine transmissible cancer. eLife, 5(MAY2016), [e14552]. https://doi.org/10.7554/eLife.14552

Mitochondrial genetic diversity, selection and recombination in a canine transmissible cancer. / Strakova, Andrea; Leathlobhair, Máire Ní; Wang, Guo Dong; Yin, Ting Ting; Airikkala-Otter, Ilona; Allen, Janice L.; Allum, Karen M.; Bansse-Issa, Leontine; Bisson, Jocelyn L.; Domracheva, Artemio Castillo; De Castro, Karina F.; Corrigan, Anne M.; Cran, Hugh R.; Crawford, Jane T.; Cutter, Stephen M.; Keenan, Laura Delgadillo; Donelan, Edward M.; Faramade, Ibikunle A.; Reynoso, Erika Flores; Fotopoulou, Eleni; Fruean, Skye N.; Gallardo-Arrieta, Fanny; Glebova, Olga; Häfelin Manrique, Rodrigo F.; Henriques, Joaquim J.G.P.; Ignatenko, Natalia; Koenig, Debbie; Lanza-Perea, Marta; Lobetti, Remo; Lopezquintana, Adriana M.; Losfelt, Thibault; Marino, Gabriele; Martincorena, Inigo; Castañeda, Simón Martínez; Martínez-López, Mayra F.; Meyer, Michael; Nakanwagi, Berna; De Nardi, Andrigo B.; Neunzig, Winifred; Nixon, Sally J.; Onsare, Marsden M.; Ortega-Pacheco, Antonio; Peleteiro, Maria C.; Pye, Ruth J.; Reece, John F.; Gutierrez, Jose Rojas; Sadia, Haleema; Schmeling, Sheila K.; Shamanova, Olga; Ssuna, Richard K.; Steenland-Smitsvitich, Audrey E.Alla; Ngoka, Ismail Thoya; Vitǎlaru, Bogdan A.; De Vos, Anna P.; De Vos, Johan P.; Walkinton, Oliver; Wedge, David C.; Wehrle-Martinez, Alvaro S.; Van Der Wel, Mirjam G.; Widdowson, Sophie Ae; Murchison, Elizabeth P.

In: eLife, Vol. 5, No. MAY2016, e14552, 17.05.2016.

Research output: Contribution to journalArticle

Strakova, A, Leathlobhair, MN, Wang, GD, Yin, TT, Airikkala-Otter, I, Allen, JL, Allum, KM, Bansse-Issa, L, Bisson, JL, Domracheva, AC, De Castro, KF, Corrigan, AM, Cran, HR, Crawford, JT, Cutter, SM, Keenan, LD, Donelan, EM, Faramade, IA, Reynoso, EF, Fotopoulou, E, Fruean, SN, Gallardo-Arrieta, F, Glebova, O, Häfelin Manrique, RF, Henriques, JJGP, Ignatenko, N, Koenig, D, Lanza-Perea, M, Lobetti, R, Lopezquintana, AM, Losfelt, T, Marino, G, Martincorena, I, Castañeda, SM, Martínez-López, MF, Meyer, M, Nakanwagi, B, De Nardi, AB, Neunzig, W, Nixon, SJ, Onsare, MM, Ortega-Pacheco, A, Peleteiro, MC, Pye, RJ, Reece, JF, Gutierrez, JR, Sadia, H, Schmeling, SK, Shamanova, O, Ssuna, RK, Steenland-Smitsvitich, AEA, Ngoka, IT, Vitǎlaru, BA, De Vos, AP, De Vos, JP, Walkinton, O, Wedge, DC, Wehrle-Martinez, AS, Van Der Wel, MG, Widdowson, SA & Murchison, EP 2016, 'Mitochondrial genetic diversity, selection and recombination in a canine transmissible cancer', eLife, vol. 5, no. MAY2016, e14552. https://doi.org/10.7554/eLife.14552
Strakova A, Leathlobhair MN, Wang GD, Yin TT, Airikkala-Otter I, Allen JL et al. Mitochondrial genetic diversity, selection and recombination in a canine transmissible cancer. eLife. 2016 May 17;5(MAY2016). e14552. https://doi.org/10.7554/eLife.14552
Strakova, Andrea ; Leathlobhair, Máire Ní ; Wang, Guo Dong ; Yin, Ting Ting ; Airikkala-Otter, Ilona ; Allen, Janice L. ; Allum, Karen M. ; Bansse-Issa, Leontine ; Bisson, Jocelyn L. ; Domracheva, Artemio Castillo ; De Castro, Karina F. ; Corrigan, Anne M. ; Cran, Hugh R. ; Crawford, Jane T. ; Cutter, Stephen M. ; Keenan, Laura Delgadillo ; Donelan, Edward M. ; Faramade, Ibikunle A. ; Reynoso, Erika Flores ; Fotopoulou, Eleni ; Fruean, Skye N. ; Gallardo-Arrieta, Fanny ; Glebova, Olga ; Häfelin Manrique, Rodrigo F. ; Henriques, Joaquim J.G.P. ; Ignatenko, Natalia ; Koenig, Debbie ; Lanza-Perea, Marta ; Lobetti, Remo ; Lopezquintana, Adriana M. ; Losfelt, Thibault ; Marino, Gabriele ; Martincorena, Inigo ; Castañeda, Simón Martínez ; Martínez-López, Mayra F. ; Meyer, Michael ; Nakanwagi, Berna ; De Nardi, Andrigo B. ; Neunzig, Winifred ; Nixon, Sally J. ; Onsare, Marsden M. ; Ortega-Pacheco, Antonio ; Peleteiro, Maria C. ; Pye, Ruth J. ; Reece, John F. ; Gutierrez, Jose Rojas ; Sadia, Haleema ; Schmeling, Sheila K. ; Shamanova, Olga ; Ssuna, Richard K. ; Steenland-Smitsvitich, Audrey E.Alla ; Ngoka, Ismail Thoya ; Vitǎlaru, Bogdan A. ; De Vos, Anna P. ; De Vos, Johan P. ; Walkinton, Oliver ; Wedge, David C. ; Wehrle-Martinez, Alvaro S. ; Van Der Wel, Mirjam G. ; Widdowson, Sophie Ae ; Murchison, Elizabeth P. / Mitochondrial genetic diversity, selection and recombination in a canine transmissible cancer. In: eLife. 2016 ; Vol. 5, No. MAY2016.
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abstract = "Canine transmissible venereal tumour (CTVT) is a clonally transmissible cancer that originated approximately 11,000 years ago and affects dogs worldwide. Despite the clonal origin of the CTVT nuclear genome, CTVT mitochondrial genomes (mtDNAs) have been acquired by periodic capture from transient hosts. We sequenced 449 complete mtDNAs from a global population of CTVTs, and show that mtDNA horizontal transfer has occurred at least five times, delineating five tumour clades whose distributions track two millennia of dog global migration. Negative selection has operated to prevent accumulation of deleterious mutations in captured mtDNA, and recombination has caused occasional mtDNA re-assortment. These findings implicate functional mtDNA as a driver of CTVT global metastatic spread, further highlighting the important role of mtDNA in cancer evolution.",
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AU - Allen, Janice L.

AU - Allum, Karen M.

AU - Bansse-Issa, Leontine

AU - Bisson, Jocelyn L.

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AU - Lanza-Perea, Marta

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AU - Martincorena, Inigo

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AU - De Nardi, Andrigo B.

AU - Neunzig, Winifred

AU - Nixon, Sally J.

AU - Onsare, Marsden M.

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