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Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer

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...

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Autores principales: Strakova, Andrea, Nicholls, Thomas J., Baez-Ortega, Adrian, Ní Leathlobhair, Máire, Sampson, Alexander T., Hughes, Katherine, Bolton, Isobelle A. G., Gori, Kevin, Wang, Jinhong, Airikkala-Otter, Ilona, Allen, Janice L., Allum, Karen M., Arnold, Clara L., Bansse-Issa, Leontine, Bhutia, Thinlay N., Bisson, Jocelyn L., Blank, Kelli, Briceño, Cristóbal, Castillo Domracheva, Artemio, Corrigan, Anne M., Cran, Hugh R., Crawford, Jane T., Cutter, Stephen M., Davis, Eric, de Castro, Karina F., De Nardi, Andrigo B., de Vos, Anna P., Delgadillo Keenan, Laura, Donelan, Edward M., Espinoza Huerta, Adela R., Faramade, Ibikunle A., Fazil, Mohammed, Fotopoulou, Eleni, Fruean, Skye N., Gallardo-Arrieta, Fanny, Glebova, Olga, Gouletsou, Pagona G., Häfelin Manrique, Rodrigo F., Henriques, Joaquim J. G. P., Horta, Rodrigo S., Ignatenko, Natalia, Kane, Yaghouba, King, Cathy, Koenig, Debbie, Krupa, Ada, Kruzeniski, Steven J., Lanza-Perea, Marta, Lazyan, Mihran, Lopez Quintana, Adriana M., Losfelt, Thibault, Marino, Gabriele, Martínez Castañeda, Simón, Martínez-López, Mayra F., Masuruli, Bedan M., Meyer, Michael, Migneco, Edward J., Nakanwagi, Berna, Neal, Karter B., Neunzig, Winifred, Nixon, Sally J., Ortega-Pacheco, Antonio, Pedraza-Ordoñez, Francisco, Peleteiro, Maria C., Polak, Katherine, Pye, Ruth J., Ramirez-Ante, Juan C., Reece, John F., Rojas Gutierrez, Jose, Sadia, Haleema, Schmeling, Sheila K., Shamanova, Olga, Sherlock, Alan G., Steenland-Smit, Audrey E., Svitich, Alla, Tapia Martínez, Lester J., Thoya Ngoka, Ismail, Torres, Cristian G., Tudor, Elizabeth M., van der Wel, Mirjam G., Vițălaru, Bogdan A., Vural, Sevil A., Walkinton, Oliver, Wehrle-Martinez, Alvaro S., Widdowson, Sophie A. E., Zvarich, Irina, Chinnery, Patrick F., Falkenberg, Maria, Gustafsson, Claes M., Murchison, Elizabeth P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7297733/
https://www.ncbi.nlm.nih.gov/pubmed/32546718
http://dx.doi.org/10.1038/s41467-020-16765-w
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author Strakova, Andrea
Nicholls, Thomas J.
Baez-Ortega, Adrian
Ní Leathlobhair, Máire
Sampson, Alexander T.
Hughes, Katherine
Bolton, Isobelle A. G.
Gori, Kevin
Wang, Jinhong
Airikkala-Otter, Ilona
Allen, Janice L.
Allum, Karen M.
Arnold, Clara L.
Bansse-Issa, Leontine
Bhutia, Thinlay N.
Bisson, Jocelyn L.
Blank, Kelli
Briceño, Cristóbal
Castillo Domracheva, Artemio
Corrigan, Anne M.
Cran, Hugh R.
Crawford, Jane T.
Cutter, Stephen M.
Davis, Eric
de Castro, Karina F.
De Nardi, Andrigo B.
de Vos, Anna P.
Delgadillo Keenan, Laura
Donelan, Edward M.
Espinoza Huerta, Adela R.
Faramade, Ibikunle A.
Fazil, Mohammed
Fotopoulou, Eleni
Fruean, Skye N.
Gallardo-Arrieta, Fanny
Glebova, Olga
Gouletsou, Pagona G.
Häfelin Manrique, Rodrigo F.
Henriques, Joaquim J. G. P.
Horta, Rodrigo S.
Ignatenko, Natalia
Kane, Yaghouba
King, Cathy
Koenig, Debbie
Krupa, Ada
Kruzeniski, Steven J.
Lanza-Perea, Marta
Lazyan, Mihran
Lopez Quintana, Adriana M.
Losfelt, Thibault
Marino, Gabriele
Martínez Castañeda, Simón
Martínez-López, Mayra F.
Masuruli, Bedan M.
Meyer, Michael
Migneco, Edward J.
Nakanwagi, Berna
Neal, Karter B.
Neunzig, Winifred
Nixon, Sally J.
Ortega-Pacheco, Antonio
Pedraza-Ordoñez, Francisco
Peleteiro, Maria C.
Polak, Katherine
Pye, Ruth J.
Ramirez-Ante, Juan C.
Reece, John F.
Rojas Gutierrez, Jose
Sadia, Haleema
Schmeling, Sheila K.
Shamanova, Olga
Sherlock, Alan G.
Steenland-Smit, Audrey E.
Svitich, Alla
Tapia Martínez, Lester J.
Thoya Ngoka, Ismail
Torres, Cristian G.
Tudor, Elizabeth M.
van der Wel, Mirjam G.
Vițălaru, Bogdan A.
Vural, Sevil A.
Walkinton, Oliver
Wehrle-Martinez, Alvaro S.
Widdowson, Sophie A. E.
Zvarich, Irina
Chinnery, Patrick F.
Falkenberg, Maria
Gustafsson, Claes M.
Murchison, Elizabeth P.
author_facet Strakova, Andrea
Nicholls, Thomas J.
Baez-Ortega, Adrian
Ní Leathlobhair, Máire
Sampson, Alexander T.
Hughes, Katherine
Bolton, Isobelle A. G.
Gori, Kevin
Wang, Jinhong
Airikkala-Otter, Ilona
Allen, Janice L.
Allum, Karen M.
Arnold, Clara L.
Bansse-Issa, Leontine
Bhutia, Thinlay N.
Bisson, Jocelyn L.
Blank, Kelli
Briceño, Cristóbal
Castillo Domracheva, Artemio
Corrigan, Anne M.
Cran, Hugh R.
Crawford, Jane T.
Cutter, Stephen M.
Davis, Eric
de Castro, Karina F.
De Nardi, Andrigo B.
de Vos, Anna P.
Delgadillo Keenan, Laura
Donelan, Edward M.
Espinoza Huerta, Adela R.
Faramade, Ibikunle A.
Fazil, Mohammed
Fotopoulou, Eleni
Fruean, Skye N.
Gallardo-Arrieta, Fanny
Glebova, Olga
Gouletsou, Pagona G.
Häfelin Manrique, Rodrigo F.
Henriques, Joaquim J. G. P.
Horta, Rodrigo S.
Ignatenko, Natalia
Kane, Yaghouba
King, Cathy
Koenig, Debbie
Krupa, Ada
Kruzeniski, Steven J.
Lanza-Perea, Marta
Lazyan, Mihran
Lopez Quintana, Adriana M.
Losfelt, Thibault
Marino, Gabriele
Martínez Castañeda, Simón
Martínez-López, Mayra F.
Masuruli, Bedan M.
Meyer, Michael
Migneco, Edward J.
Nakanwagi, Berna
Neal, Karter B.
Neunzig, Winifred
Nixon, Sally J.
Ortega-Pacheco, Antonio
Pedraza-Ordoñez, Francisco
Peleteiro, Maria C.
Polak, Katherine
Pye, Ruth J.
Ramirez-Ante, Juan C.
Reece, John F.
Rojas Gutierrez, Jose
Sadia, Haleema
Schmeling, Sheila K.
Shamanova, Olga
Sherlock, Alan G.
Steenland-Smit, Audrey E.
Svitich, Alla
Tapia Martínez, Lester J.
Thoya Ngoka, Ismail
Torres, Cristian G.
Tudor, Elizabeth M.
van der Wel, Mirjam G.
Vițălaru, Bogdan A.
Vural, Sevil A.
Walkinton, Oliver
Wehrle-Martinez, Alvaro S.
Widdowson, Sophie A. E.
Zvarich, Irina
Chinnery, Patrick F.
Falkenberg, Maria
Gustafsson, Claes M.
Murchison, Elizabeth P.
author_sort Strakova, Andrea
collection PubMed
description 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.
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spelling pubmed-72977332020-06-22 Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer Strakova, Andrea Nicholls, Thomas J. Baez-Ortega, Adrian Ní Leathlobhair, Máire Sampson, Alexander T. Hughes, Katherine Bolton, Isobelle A. G. Gori, Kevin Wang, Jinhong Airikkala-Otter, Ilona Allen, Janice L. Allum, Karen M. Arnold, Clara L. Bansse-Issa, Leontine Bhutia, Thinlay N. Bisson, Jocelyn L. Blank, Kelli Briceño, Cristóbal Castillo Domracheva, Artemio Corrigan, Anne M. Cran, Hugh R. Crawford, Jane T. Cutter, Stephen M. Davis, Eric de Castro, Karina F. De Nardi, Andrigo B. de Vos, Anna P. Delgadillo Keenan, Laura Donelan, Edward M. Espinoza Huerta, Adela R. Faramade, Ibikunle A. Fazil, Mohammed Fotopoulou, Eleni Fruean, Skye N. Gallardo-Arrieta, Fanny Glebova, Olga Gouletsou, Pagona G. Häfelin Manrique, Rodrigo F. Henriques, Joaquim J. G. P. Horta, Rodrigo S. Ignatenko, Natalia Kane, Yaghouba King, Cathy Koenig, Debbie Krupa, Ada Kruzeniski, Steven J. Lanza-Perea, Marta Lazyan, Mihran Lopez Quintana, Adriana M. Losfelt, Thibault Marino, Gabriele Martínez Castañeda, Simón Martínez-López, Mayra F. Masuruli, Bedan M. Meyer, Michael Migneco, Edward J. Nakanwagi, Berna Neal, Karter B. Neunzig, Winifred Nixon, Sally J. Ortega-Pacheco, Antonio Pedraza-Ordoñez, Francisco Peleteiro, Maria C. Polak, Katherine Pye, Ruth J. Ramirez-Ante, Juan C. Reece, John F. Rojas Gutierrez, Jose Sadia, Haleema Schmeling, Sheila K. Shamanova, Olga Sherlock, Alan G. Steenland-Smit, Audrey E. Svitich, Alla Tapia Martínez, Lester J. Thoya Ngoka, Ismail Torres, Cristian G. Tudor, Elizabeth M. van der Wel, Mirjam G. Vițălaru, Bogdan A. Vural, Sevil A. Walkinton, Oliver Wehrle-Martinez, Alvaro S. Widdowson, Sophie A. E. Zvarich, Irina Chinnery, Patrick F. Falkenberg, Maria Gustafsson, Claes M. Murchison, Elizabeth P. Nat Commun Article 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. Nature Publishing Group UK 2020-06-16 /pmc/articles/PMC7297733/ /pubmed/32546718 http://dx.doi.org/10.1038/s41467-020-16765-w Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Strakova, Andrea
Nicholls, Thomas J.
Baez-Ortega, Adrian
Ní Leathlobhair, Máire
Sampson, Alexander T.
Hughes, Katherine
Bolton, Isobelle A. G.
Gori, Kevin
Wang, Jinhong
Airikkala-Otter, Ilona
Allen, Janice L.
Allum, Karen M.
Arnold, Clara L.
Bansse-Issa, Leontine
Bhutia, Thinlay N.
Bisson, Jocelyn L.
Blank, Kelli
Briceño, Cristóbal
Castillo Domracheva, Artemio
Corrigan, Anne M.
Cran, Hugh R.
Crawford, Jane T.
Cutter, Stephen M.
Davis, Eric
de Castro, Karina F.
De Nardi, Andrigo B.
de Vos, Anna P.
Delgadillo Keenan, Laura
Donelan, Edward M.
Espinoza Huerta, Adela R.
Faramade, Ibikunle A.
Fazil, Mohammed
Fotopoulou, Eleni
Fruean, Skye N.
Gallardo-Arrieta, Fanny
Glebova, Olga
Gouletsou, Pagona G.
Häfelin Manrique, Rodrigo F.
Henriques, Joaquim J. G. P.
Horta, Rodrigo S.
Ignatenko, Natalia
Kane, Yaghouba
King, Cathy
Koenig, Debbie
Krupa, Ada
Kruzeniski, Steven J.
Lanza-Perea, Marta
Lazyan, Mihran
Lopez Quintana, Adriana M.
Losfelt, Thibault
Marino, Gabriele
Martínez Castañeda, Simón
Martínez-López, Mayra F.
Masuruli, Bedan M.
Meyer, Michael
Migneco, Edward J.
Nakanwagi, Berna
Neal, Karter B.
Neunzig, Winifred
Nixon, Sally J.
Ortega-Pacheco, Antonio
Pedraza-Ordoñez, Francisco
Peleteiro, Maria C.
Polak, Katherine
Pye, Ruth J.
Ramirez-Ante, Juan C.
Reece, John F.
Rojas Gutierrez, Jose
Sadia, Haleema
Schmeling, Sheila K.
Shamanova, Olga
Sherlock, Alan G.
Steenland-Smit, Audrey E.
Svitich, Alla
Tapia Martínez, Lester J.
Thoya Ngoka, Ismail
Torres, Cristian G.
Tudor, Elizabeth M.
van der Wel, Mirjam G.
Vițălaru, Bogdan A.
Vural, Sevil A.
Walkinton, Oliver
Wehrle-Martinez, Alvaro S.
Widdowson, Sophie A. E.
Zvarich, Irina
Chinnery, Patrick F.
Falkenberg, Maria
Gustafsson, Claes M.
Murchison, Elizabeth P.
Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer
title Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer
title_full Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer
title_fullStr Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer
title_full_unstemmed Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer
title_short Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer
title_sort recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7297733/
https://www.ncbi.nlm.nih.gov/pubmed/32546718
http://dx.doi.org/10.1038/s41467-020-16765-w
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