Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer

Andrea Strakova; Thomas J. Nicholls; Adrian Baez-Ortega; Máire Ní Leathlobhair; Alexander T. Sampson; Katherine Hughes; Isobelle A.G. Bolton; Kevin Gori; Jinhong Wang; Ilona Airikkala-Otter; Janice L. Allen; Karen M. Allum; Clara L. Arnold; Leontine Bansse-Issa; Thinlay N. Bhutia; Jocelyn L. Bisson; Kelli Blank; Cristóbal Briceño; Artemio Castillo Domracheva; Anne M. Corrigan; Hugh R. Cran; Jane T. Crawford; Stephen M. Cutter; 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; Marta Lanza-Perea; Mihran Lazyan; Adriana M. Lopez Quintana; Thibault Losfelt; Gabriele Marino; Simón Martínez Castañeda; Mayra F. Martínez-López; Bedan M. Masuruli; Michael Meyer; Edward J. Migneco; Berna Nakanwagi; Karter B. Neal; Winifred Neunzig; Sally J. Nixon; Antonio Ortega-Pacheco; Francisco Pedraza-Ordoñez; Maria C. Peleteiro; Katherine Polak; Ruth J. Pye; Juan C. Ramirez-Ante; John F. Reece; Jose Rojas Gutierrez; Haleema Sadia; Sheila K. Schmeling; Olga Shamanova; Alan G. Sherlock; 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. Vițălaru; Sevil A. Vural; Oliver Walkinton; Alvaro S. Wehrle-Martinez; Sophie A.E. Widdowson; Irina Zvarich; Patrick F. Chinnery; Maria Falkenberg; Claes M. Gustafsson; Elizabeth P. Murchison

doi:10.1038/s41467-020-16765-w

Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer

Andrea Strakova, Thomas J. Nicholls, Adrian Baez-Ortega, Máire Ní Leathlobhair, Alexander T. Sampson, Katherine Hughes, Isobelle A.G. Bolton, Kevin Gori, Jinhong Wang, Ilona Airikkala-Otter, Janice L. Allen, Karen M. Allum, Clara L. Arnold, Leontine Bansse-Issa, Thinlay N. Bhutia, Jocelyn L. Bisson, Kelli Blank, Cristóbal Briceño, Artemio Castillo Domracheva, Anne M. CorriganHugh R. Cran, Jane T. Crawford, Stephen M. Cutter, 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, Marta Lanza-Perea, Mihran Lazyan, Adriana M. Lopez Quintana, Thibault Losfelt, Gabriele Marino, Simón Martínez Castañeda, Mayra F. Martínez-López, Bedan M. Masuruli, Michael Meyer, Edward J. Migneco, Berna Nakanwagi, Karter B. Neal, Winifred Neunzig, Sally J. Nixon, Antonio Ortega-Pacheco, Francisco Pedraza-Ordoñez, Maria C. Peleteiro, Katherine Polak, Ruth J. Pye, Juan C. Ramirez-Ante, John F. Reece, Jose Rojas Gutierrez, Haleema Sadia, Sheila K. Schmeling, Olga Shamanova, Alan G. Sherlock, 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. Vițălaru, Sevil A. Vural, Oliver Walkinton, Alvaro S. Wehrle-Martinez, Sophie A.E. Widdowson, Irina Zvarich, Patrick F. Chinnery, Maria Falkenberg, Claes M. Gustafsson, Elizabeth P. Murchison

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Resumen

Autonomous replication and segregation of mitochondrial DNA (mtDNA) creates the potential for evolutionary conflict driven by emergence of haplotypes under positive selection for ‘selfish’ traits, such as replicative advantage. However, few cases of this phenomenon arising within natural populations have been described. Here, we survey the frequency of mtDNA horizontal transfer within the canine transmissible venereal tumour (CTVT), a contagious cancer clone that occasionally acquires mtDNA from its hosts. Remarkably, one canine mtDNA haplotype, A1d1a, has repeatedly and recently colonised CTVT cells, recurrently replacing incumbent CTVT haplotypes. An A1d1a control region polymorphism predicted to influence transcription is fixed in the products of an A1d1a recombination event and occurs somatically on other CTVT mtDNA backgrounds. We present a model whereby ‘selfish’ positive selection acting on a regulatory variant drives repeated fixation of A1d1a within CTVT cells.

Idioma original	Inglés
Número de artículo	3059
Publicación	Nature Communications
Volumen	11
N.º	1
DOI	https://doi.org/10.1038/s41467-020-16765-w
Estado	Publicada - 1 dic. 2020
Publicado de forma externa	Sí

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Strakova, A., Nicholls, T. J., Baez-Ortega, A., Ní Leathlobhair, M., Sampson, A. T., Hughes, K., Bolton, I. A. G., Gori, K., Wang, J., Airikkala-Otter, I., Allen, J. L., Allum, K. M., Arnold, C. L., Bansse-Issa, L., Bhutia, T. N., Bisson, J. L., Blank, K., Briceño, C., Castillo Domracheva, A., ... Murchison, E. P. (2020). Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer. Nature Communications, 11(1), Artículo 3059. https://doi.org/10.1038/s41467-020-16765-w

@article{30b429aa3be54f9992ed848c00522006,

title = "Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer",

abstract = "Autonomous replication and segregation of mitochondrial DNA (mtDNA) creates the potential for evolutionary conflict driven by emergence of haplotypes under positive selection for {\textquoteleft}selfish{\textquoteright} traits, such as replicative advantage. However, few cases of this phenomenon arising within natural populations have been described. Here, we survey the frequency of mtDNA horizontal transfer within the canine transmissible venereal tumour (CTVT), a contagious cancer clone that occasionally acquires mtDNA from its hosts. Remarkably, one canine mtDNA haplotype, A1d1a, has repeatedly and recently colonised CTVT cells, recurrently replacing incumbent CTVT haplotypes. An A1d1a control region polymorphism predicted to influence transcription is fixed in the products of an A1d1a recombination event and occurs somatically on other CTVT mtDNA backgrounds. We present a model whereby {\textquoteleft}selfish{\textquoteright} positive selection acting on a regulatory variant drives repeated fixation of A1d1a within CTVT cells.",

author = "Andrea Strakova and Nicholls, \{Thomas J.\} and Adrian Baez-Ortega and \{N{\'i} Leathlobhair\}, M{\'a}ire and Sampson, \{Alexander T.\} and Katherine Hughes and Bolton, \{Isobelle A.G.\} and Kevin Gori and Jinhong Wang and Ilona Airikkala-Otter and Allen, \{Janice L.\} and Allum, \{Karen M.\} and Arnold, \{Clara L.\} and Leontine Bansse-Issa and Bhutia, \{Thinlay N.\} and Bisson, \{Jocelyn L.\} and Kelli Blank and Crist{\'o}bal Brice{\~n}o and \{Castillo Domracheva\}, Artemio and Corrigan, \{Anne M.\} and Cran, \{Hugh R.\} and Crawford, \{Jane T.\} and Cutter, \{Stephen M.\} and Eric Davis and \{de Castro\}, \{Karina F.\} and \{De Nardi\}, \{Andrigo B.\} 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 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 Masuruli, \{Bedan M.\} and Michael Meyer and Migneco, \{Edward J.\} and Berna Nakanwagi and Neal, \{Karter B.\} and Winifred Neunzig 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 Ramirez-Ante, \{Juan C.\} and Reece, \{John F.\} and \{Rojas Gutierrez\}, Jose and Haleema Sadia and Schmeling, \{Sheila K.\} and Olga Shamanova and Sherlock, \{Alan G.\} 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 Viț{\u a}laru, \{Bogdan A.\} and Vural, \{Sevil A.\} and Oliver Walkinton and Wehrle-Martinez, \{Alvaro S.\} and Widdowson, \{Sophie A.E.\} and Irina Zvarich and Chinnery, \{Patrick F.\} and Maria Falkenberg and Gustafsson, \{Claes M.\} and Murchison, \{Elizabeth P.\}",

note = "Publisher Copyright: {\textcopyright} 2020, The Author(s).",

year = "2020",

month = dec,

day = "1",

doi = "10.1038/s41467-020-16765-w",

language = "Ingl{\'e}s",

volume = "11",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Research",

number = "1",

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Strakova, A, Nicholls, TJ, Baez-Ortega, A, Ní Leathlobhair, M, Sampson, AT, Hughes, K, Bolton, IAG, Gori, K, Wang, J, Airikkala-Otter, I, Allen, JL, Allum, KM, Arnold, CL, Bansse-Issa, L, Bhutia, TN, Bisson, JL, Blank, K, Briceño, C, Castillo Domracheva, A, Corrigan, AM, Cran, HR, Crawford, JT, Cutter, SM, Davis, E, de Castro, KF, De Nardi, AB, 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, Lanza-Perea, M, Lazyan, M, Lopez Quintana, AM, Losfelt, T, Marino, G, Martínez Castañeda, S, Martínez-López, MF, Masuruli, BM, Meyer, M, Migneco, EJ, Nakanwagi, B, Neal, KB, Neunzig, W, Nixon, SJ, Ortega-Pacheco, A, Pedraza-Ordoñez, F, Peleteiro, MC, Polak, K, Pye, RJ, Ramirez-Ante, JC, Reece, JF, Rojas Gutierrez, J, Sadia, H, Schmeling, SK, Shamanova, O, Sherlock, AG, Steenland-Smit, AE, Svitich, A, Tapia Martínez, LJ, Thoya Ngoka, I, Torres, CG, Tudor, EM, van der Wel, MG, Vițălaru, BA, Vural, SA, Walkinton, O, Wehrle-Martinez, AS, Widdowson, SAE, Zvarich, I, Chinnery, PF, Falkenberg, M, Gustafsson, CM & Murchison, EP 2020, 'Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer', Nature Communications, vol. 11, n.º 1, 3059. https://doi.org/10.1038/s41467-020-16765-w

TY - JOUR

T1 - Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer

AU - Strakova, Andrea

AU - Nicholls, Thomas J.

AU - Baez-Ortega, Adrian

AU - Ní Leathlobhair, Máire

AU - Sampson, Alexander T.

AU - Hughes, Katherine

AU - Bolton, Isobelle A.G.

AU - Gori, Kevin

AU - Wang, Jinhong

AU - Airikkala-Otter, Ilona

AU - Allen, Janice L.

AU - Allum, Karen M.

AU - Arnold, Clara L.

AU - Bansse-Issa, Leontine

AU - Bhutia, Thinlay N.

AU - Bisson, Jocelyn L.

AU - Blank, Kelli

AU - Briceño, Cristóbal

AU - Castillo Domracheva, Artemio

AU - Corrigan, Anne M.

AU - Cran, Hugh R.

AU - Crawford, Jane T.

AU - Cutter, Stephen M.

AU - Davis, Eric

AU - de Castro, Karina F.

AU - De Nardi, Andrigo B.

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 - 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 - Masuruli, Bedan M.

AU - Meyer, Michael

AU - Migneco, Edward J.

AU - Nakanwagi, Berna

AU - Neal, Karter B.

AU - Neunzig, Winifred

AU - Nixon, Sally J.

AU - Ortega-Pacheco, Antonio

AU - Pedraza-Ordoñez, Francisco

AU - Peleteiro, Maria C.

AU - Polak, Katherine

AU - Pye, Ruth J.

AU - Ramirez-Ante, Juan C.

AU - Reece, John F.

AU - Rojas Gutierrez, Jose

AU - Sadia, Haleema

AU - Schmeling, Sheila K.

AU - Shamanova, Olga

AU - Sherlock, Alan G.

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 - Vițălaru, Bogdan A.

AU - Vural, Sevil A.

AU - Walkinton, Oliver

AU - Wehrle-Martinez, Alvaro S.

AU - Widdowson, Sophie A.E.

AU - Zvarich, Irina

AU - Chinnery, Patrick F.

AU - Falkenberg, Maria

AU - Gustafsson, Claes M.

AU - Murchison, Elizabeth P.

PY - 2020/12/1

Y1 - 2020/12/1

N2 - Autonomous replication and segregation of mitochondrial DNA (mtDNA) creates the potential for evolutionary conflict driven by emergence of haplotypes under positive selection for ‘selfish’ traits, such as replicative advantage. However, few cases of this phenomenon arising within natural populations have been described. Here, we survey the frequency of mtDNA horizontal transfer within the canine transmissible venereal tumour (CTVT), a contagious cancer clone that occasionally acquires mtDNA from its hosts. Remarkably, one canine mtDNA haplotype, A1d1a, has repeatedly and recently colonised CTVT cells, recurrently replacing incumbent CTVT haplotypes. An A1d1a control region polymorphism predicted to influence transcription is fixed in the products of an A1d1a recombination event and occurs somatically on other CTVT mtDNA backgrounds. We present a model whereby ‘selfish’ positive selection acting on a regulatory variant drives repeated fixation of A1d1a within CTVT cells.

AB - Autonomous replication and segregation of mitochondrial DNA (mtDNA) creates the potential for evolutionary conflict driven by emergence of haplotypes under positive selection for ‘selfish’ traits, such as replicative advantage. However, few cases of this phenomenon arising within natural populations have been described. Here, we survey the frequency of mtDNA horizontal transfer within the canine transmissible venereal tumour (CTVT), a contagious cancer clone that occasionally acquires mtDNA from its hosts. Remarkably, one canine mtDNA haplotype, A1d1a, has repeatedly and recently colonised CTVT cells, recurrently replacing incumbent CTVT haplotypes. An A1d1a control region polymorphism predicted to influence transcription is fixed in the products of an A1d1a recombination event and occurs somatically on other CTVT mtDNA backgrounds. We present a model whereby ‘selfish’ positive selection acting on a regulatory variant drives repeated fixation of A1d1a within CTVT cells.

UR - https://www.scopus.com/pages/publications/85086571979

U2 - 10.1038/s41467-020-16765-w

DO - 10.1038/s41467-020-16765-w

M3 - Artículo

C2 - 32546718

AN - SCOPUS:85086571979

SN - 2041-1723

VL - 11

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 3059

ER -

Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer

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