Somatic evolution and global expansion of an ancient transmissible cancer lineage

Adrian Baez-Ortega; Kevin Gori; Andrea Strakova; Janice L Allen; Karen M Allum; Leontine Bansse-Issa; Thinlay N Bhutia; Jocelyn L Bisson; Cristóbal Briceño; Artemio Castillo Domracheva; Anne M Corrigan; Hugh R Cran; Jane T Crawford; Eric Davis; Karina F de Castro; Andrigo B de Nardi; Anna P de Vos; Laura Delgadillo Keenan; Edward M Donelan; Adela R Espinoza Huerta; Ibikunle A Faramade; Mohammed Fazil; Eleni Fotopoulou; Skye N Fruean; Fanny Gallardo-Arrieta; Olga Glebova; Pagona G Gouletsou; Rodrigo F Häfelin Manrique; Joaquim J G P Henriques; Rodrigo S Horta; Natalia Ignatenko; Yaghouba Kane; Cathy King; Debbie Koenig; Ada Krupa; Steven J Kruzeniski; Young-Mi Kwon; Marta Lanza-Perea; Mihran Lazyan; Adriana M Lopez Quintana; Thibault Losfelt; Gabriele Marino; Simón Martínez Castañeda; Mayra F Martínez-López; Michael Meyer; Edward J Migneco; Berna Nakanwagi; Karter B Neal; Winifred Neunzig; Máire Ní Leathlobhair; Sally J Nixon; Antonio Ortega-Pacheco; Francisco Pedraza-Ordoñez; Maria C Peleteiro; Katherine Polak; Ruth J Pye; John F Reece; Jose Rojas Gutierrez; Haleema Sadia; Sheila K Schmeling; Olga Shamanova; Alan G Sherlock; Maximilian Stammnitz; Audrey E Steenland-Smit; Alla Svitich; Lester J Tapia Martínez; Ismail Thoya Ngoka; Cristian G Torres; Elizabeth M Tudor; Mirjam G van der Wel; Bogdan A Viţălaru; Sevil A Vural; Oliver Walkinton; Jinhong Wang; Alvaro S Wehrle-Martinez; Sophie A E Widdowson; Michael R Stratton; Ludmil B Alexandrov; Iñigo Martincorena; Elizabeth P Murchison

doi:10.1126/science.aau9923

Somatic evolution and global expansion of an ancient transmissible cancer lineage

Adrian Baez-Ortega, Kevin Gori, Andrea Strakova, Janice L Allen, Karen M Allum, Leontine Bansse-Issa, Thinlay N Bhutia, Jocelyn L Bisson, Cristóbal Briceño, Artemio Castillo Domracheva, Anne M Corrigan, Hugh R Cran, Jane T Crawford, Eric Davis, Karina F de Castro, Andrigo B de Nardi, Anna P de Vos, Laura Delgadillo Keenan, Edward M Donelan, Adela R Espinoza HuertaIbikunle A Faramade, Mohammed Fazil, Eleni Fotopoulou, Skye N Fruean, Fanny Gallardo-Arrieta, Olga Glebova, Pagona G Gouletsou, Rodrigo F Häfelin Manrique, Joaquim J G P Henriques, Rodrigo S Horta, Natalia Ignatenko, Yaghouba Kane, Cathy King, Debbie Koenig, Ada Krupa, Steven J Kruzeniski, Young-Mi Kwon, Marta Lanza-Perea, Mihran Lazyan, Adriana M Lopez Quintana, Thibault Losfelt, Gabriele Marino, Simón Martínez Castañeda, Mayra F Martínez-López, Michael Meyer, Edward J Migneco, Berna Nakanwagi, Karter B Neal, Winifred Neunzig, Máire Ní Leathlobhair, Sally J Nixon, Antonio Ortega-Pacheco, Francisco Pedraza-Ordoñez, Maria C Peleteiro, Katherine Polak, Ruth J Pye, John F Reece, Jose Rojas Gutierrez, Haleema Sadia, Sheila K Schmeling, Olga Shamanova, Alan G Sherlock, Maximilian Stammnitz, Audrey E Steenland-Smit, Alla Svitich, Lester J Tapia Martínez, Ismail Thoya Ngoka, Cristian G Torres, Elizabeth M Tudor, Mirjam G van der Wel, Bogdan A Viţălaru, Sevil A Vural, Oliver Walkinton, Jinhong Wang, Alvaro S Wehrle-Martinez, Sophie A E Widdowson, Michael R Stratton, Ludmil B Alexandrov, Iñigo Martincorena, Elizabeth P Murchison

Royal (Dick) School of Veterinary Studies

Research output: Contribution to journal › Article › peer-review

Abstract

The canine transmissible venereal tumor (CTVT) is a cancer lineage that arose several millennia ago and survives by "metastasizing" between hosts through cell transfer. The somatic mutations in this cancer record its phylogeography and evolutionary history. We constructed a time-resolved phylogeny from 546 CTVT exomes and describe the lineage's worldwide expansion. Examining variation in mutational exposure, we identify a highly context-specific mutational process that operated early in the cancer's evolution but subsequently vanished, correlate ultraviolet-light mutagenesis with tumor latitude, and describe tumors with heritable hyperactivity of an endogenous mutational process. CTVT displays little evidence of ongoing positive selection, and negative selection is detectable only in essential genes. We illustrate how long-lived clonal organisms capture changing mutagenic environments, and reveal that neutral genetic drift is the dominant feature of long-term cancer evolution.

Original language	English
Journal	Science
Volume	365
Issue number	6452
DOIs	https://doi.org/10.1126/science.aau9923
Publication status	Published - 2 Aug 2019

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Somatic evolution and global expansion of an ancient transmissibleAccepted author manuscript, 4.27 MB

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Baez-Ortega, A., Gori, K., Strakova, A., Allen, J. L., Allum, K. M., Bansse-Issa, L., Bhutia, T. N., Bisson, J. L., Briceño, C., Castillo Domracheva, A., Corrigan, A. M., Cran, H. R., Crawford, J. T., Davis, E., de Castro, K. F., B de Nardi, A., de Vos, A. P., Delgadillo Keenan, L., Donelan, E. M., ... Murchison, E. P. (2019). Somatic evolution and global expansion of an ancient transmissible cancer lineage. Science, 365(6452). https://doi.org/10.1126/science.aau9923

@article{f34b369d63dd4dc18101e952ba9a35e9,

title = "Somatic evolution and global expansion of an ancient transmissible cancer lineage",

abstract = "The canine transmissible venereal tumor (CTVT) is a cancer lineage that arose several millennia ago and survives by {"}metastasizing{"} between hosts through cell transfer. The somatic mutations in this cancer record its phylogeography and evolutionary history. We constructed a time-resolved phylogeny from 546 CTVT exomes and describe the lineage's worldwide expansion. Examining variation in mutational exposure, we identify a highly context-specific mutational process that operated early in the cancer's evolution but subsequently vanished, correlate ultraviolet-light mutagenesis with tumor latitude, and describe tumors with heritable hyperactivity of an endogenous mutational process. CTVT displays little evidence of ongoing positive selection, and negative selection is detectable only in essential genes. We illustrate how long-lived clonal organisms capture changing mutagenic environments, and reveal that neutral genetic drift is the dominant feature of long-term cancer evolution.",

author = "Adrian Baez-Ortega and Kevin Gori and Andrea Strakova and Allen, {Janice L} and Allum, {Karen M} and Leontine Bansse-Issa and Bhutia, {Thinlay N} and Bisson, {Jocelyn L} and Crist{\'o}bal Brice{\~n}o and {Castillo Domracheva}, Artemio and Corrigan, {Anne M} and Cran, {Hugh R} and Crawford, {Jane T} and Eric Davis and {de Castro}, {Karina F} and {B de Nardi}, Andrigo and {de Vos}, {Anna P} and {Delgadillo Keenan}, Laura and Donelan, {Edward M} and {Espinoza Huerta}, {Adela R} and Faramade, {Ibikunle A} and Mohammed Fazil and Eleni Fotopoulou and Fruean, {Skye N} and Fanny Gallardo-Arrieta and Olga Glebova and Gouletsou, {Pagona G} and {H{\"a}felin Manrique}, {Rodrigo F} and Henriques, {Joaquim J G P} and Horta, {Rodrigo S} and Natalia Ignatenko and Yaghouba Kane and Cathy King and Debbie Koenig and Ada Krupa and Kruzeniski, {Steven J} and Young-Mi Kwon and Marta Lanza-Perea and Mihran Lazyan and {Lopez Quintana}, {Adriana M} and Thibault Losfelt and Gabriele Marino and {Mart{\'i}nez Casta{\~n}eda}, Sim{\'o}n and Mart{\'i}nez-L{\'o}pez, {Mayra F} and Michael Meyer and Migneco, {Edward J} and Berna Nakanwagi and Neal, {Karter B} and Winifred Neunzig and {N{\'i} Leathlobhair}, M{\'a}ire and Nixon, {Sally J} and Antonio Ortega-Pacheco and Francisco Pedraza-Ordo{\~n}ez and Peleteiro, {Maria C} and Katherine Polak and Pye, {Ruth J} and Reece, {John F} and {Rojas Gutierrez}, Jose and Haleema Sadia and Schmeling, {Sheila K} and Olga Shamanova and Sherlock, {Alan G} and Maximilian Stammnitz and Steenland-Smit, {Audrey E} and Alla Svitich and {Tapia Mart{\'i}nez}, {Lester J} and {Thoya Ngoka}, Ismail and Torres, {Cristian G} and Tudor, {Elizabeth M} and {van der Wel}, {Mirjam G} and Vi{\c t}{\u a}laru, {Bogdan A} and Vural, {Sevil A} and Oliver Walkinton and Jinhong Wang and Wehrle-Martinez, {Alvaro S} and Widdowson, {Sophie A E} and Stratton, {Michael R} and Alexandrov, {Ludmil B} and I{\~n}igo Martincorena and Murchison, {Elizabeth P}",

note = "Copyright {\textcopyright} 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.",

year = "2019",

month = aug,

day = "2",

doi = "10.1126/science.aau9923",

language = "English",

volume = "365",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

number = "6452",

}

Baez-Ortega, A, Gori, K, Strakova, A, Allen, JL, Allum, KM, Bansse-Issa, L, Bhutia, TN, Bisson, JL, Briceño, C, Castillo Domracheva, A, Corrigan, AM, Cran, HR, Crawford, JT, Davis, E, de Castro, KF, B de Nardi, A, de Vos, AP, Delgadillo Keenan, L, Donelan, EM, Espinoza Huerta, AR, Faramade, IA, Fazil, M, Fotopoulou, E, Fruean, SN, Gallardo-Arrieta, F, Glebova, O, Gouletsou, PG, Häfelin Manrique, RF, Henriques, JJGP, Horta, RS, Ignatenko, N, Kane, Y, King, C, Koenig, D, Krupa, A, Kruzeniski, SJ, Kwon, Y-M, Lanza-Perea, M, Lazyan, M, Lopez Quintana, AM, Losfelt, T, Marino, G, Martínez Castañeda, S, Martínez-López, MF, Meyer, M, Migneco, EJ, Nakanwagi, B, Neal, KB, Neunzig, W, Ní Leathlobhair, M, Nixon, SJ, Ortega-Pacheco, A, Pedraza-Ordoñez, F, Peleteiro, MC, Polak, K, Pye, RJ, Reece, JF, Rojas Gutierrez, J, Sadia, H, Schmeling, SK, Shamanova, O, Sherlock, AG, Stammnitz, M, Steenland-Smit, AE, Svitich, A, Tapia Martínez, LJ, Thoya Ngoka, I, Torres, CG, Tudor, EM, van der Wel, MG, Viţălaru, BA, Vural, SA, Walkinton, O, Wang, J, Wehrle-Martinez, AS, Widdowson, SAE, Stratton, MR, Alexandrov, LB, Martincorena, I & Murchison, EP 2019, 'Somatic evolution and global expansion of an ancient transmissible cancer lineage', Science, vol. 365, no. 6452. https://doi.org/10.1126/science.aau9923

TY - JOUR

T1 - Somatic evolution and global expansion of an ancient transmissible cancer lineage

AU - Baez-Ortega, Adrian

AU - Gori, Kevin

AU - Strakova, Andrea

AU - Allen, Janice L

AU - Allum, Karen M

AU - Bansse-Issa, Leontine

AU - Bhutia, Thinlay N

AU - Bisson, Jocelyn L

AU - Briceño, Cristóbal

AU - Castillo Domracheva, Artemio

AU - Corrigan, Anne M

AU - Cran, Hugh R

AU - Crawford, Jane T

AU - Davis, Eric

AU - de Castro, Karina F

AU - B de Nardi, Andrigo

AU - de Vos, Anna P

AU - Delgadillo Keenan, Laura

AU - Donelan, Edward M

AU - Espinoza Huerta, Adela R

AU - Faramade, Ibikunle A

AU - Fazil, Mohammed

AU - Fotopoulou, Eleni

AU - Fruean, Skye N

AU - Gallardo-Arrieta, Fanny

AU - Glebova, Olga

AU - Gouletsou, Pagona G

AU - Häfelin Manrique, Rodrigo F

AU - Henriques, Joaquim J G P

AU - Horta, Rodrigo S

AU - Ignatenko, Natalia

AU - Kane, Yaghouba

AU - King, Cathy

AU - Koenig, Debbie

AU - Krupa, Ada

AU - Kruzeniski, Steven J

AU - Kwon, Young-Mi

AU - Lanza-Perea, Marta

AU - Lazyan, Mihran

AU - Lopez Quintana, Adriana M

AU - Losfelt, Thibault

AU - Marino, Gabriele

AU - Martínez Castañeda, Simón

AU - Martínez-López, Mayra F

AU - Meyer, Michael

AU - Migneco, Edward J

AU - Nakanwagi, Berna

AU - Neal, Karter B

AU - Neunzig, Winifred

AU - Ní Leathlobhair, Máire

AU - Nixon, Sally J

AU - Ortega-Pacheco, Antonio

AU - Pedraza-Ordoñez, Francisco

AU - Peleteiro, Maria C

AU - Polak, Katherine

AU - Pye, Ruth J

AU - Reece, John F

AU - Rojas Gutierrez, Jose

AU - Sadia, Haleema

AU - Schmeling, Sheila K

AU - Shamanova, Olga

AU - Sherlock, Alan G

AU - Stammnitz, Maximilian

AU - Steenland-Smit, Audrey E

AU - Svitich, Alla

AU - Tapia Martínez, Lester J

AU - Thoya Ngoka, Ismail

AU - Torres, Cristian G

AU - Tudor, Elizabeth M

AU - van der Wel, Mirjam G

AU - Viţălaru, Bogdan A

AU - Vural, Sevil A

AU - Walkinton, Oliver

AU - Wang, Jinhong

AU - Wehrle-Martinez, Alvaro S

AU - Widdowson, Sophie A E

AU - Stratton, Michael R

AU - Alexandrov, Ludmil B

AU - Martincorena, Iñigo

AU - Murchison, Elizabeth P

PY - 2019/8/2

Y1 - 2019/8/2

N2 - The canine transmissible venereal tumor (CTVT) is a cancer lineage that arose several millennia ago and survives by "metastasizing" between hosts through cell transfer. The somatic mutations in this cancer record its phylogeography and evolutionary history. We constructed a time-resolved phylogeny from 546 CTVT exomes and describe the lineage's worldwide expansion. Examining variation in mutational exposure, we identify a highly context-specific mutational process that operated early in the cancer's evolution but subsequently vanished, correlate ultraviolet-light mutagenesis with tumor latitude, and describe tumors with heritable hyperactivity of an endogenous mutational process. CTVT displays little evidence of ongoing positive selection, and negative selection is detectable only in essential genes. We illustrate how long-lived clonal organisms capture changing mutagenic environments, and reveal that neutral genetic drift is the dominant feature of long-term cancer evolution.

AB - The canine transmissible venereal tumor (CTVT) is a cancer lineage that arose several millennia ago and survives by "metastasizing" between hosts through cell transfer. The somatic mutations in this cancer record its phylogeography and evolutionary history. We constructed a time-resolved phylogeny from 546 CTVT exomes and describe the lineage's worldwide expansion. Examining variation in mutational exposure, we identify a highly context-specific mutational process that operated early in the cancer's evolution but subsequently vanished, correlate ultraviolet-light mutagenesis with tumor latitude, and describe tumors with heritable hyperactivity of an endogenous mutational process. CTVT displays little evidence of ongoing positive selection, and negative selection is detectable only in essential genes. We illustrate how long-lived clonal organisms capture changing mutagenic environments, and reveal that neutral genetic drift is the dominant feature of long-term cancer evolution.

U2 - 10.1126/science.aau9923

DO - 10.1126/science.aau9923

M3 - Article

C2 - 31371581

SN - 0036-8075

VL - 365

JO - Science

JF - Science

IS - 6452

ER -

Somatic evolution and global expansion of an ancient transmissible cancer lineage

Abstract

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