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Potential role of vector-mediated natural selection in dengue virus genotype/lineage replacements in two epidemiologically contrasted settings

Dengue virus (DENV) evolutionary dynamics are characterized by frequent DENV genotype/lineage replacements, potentially associated with changes in disease severity and human immunity. New Caledonia (NC) and Cambodia, two contrasted epidemiological settings, respectively experienced a DENV-1 genotype...

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Autores principales: O’Connor, Olivia, Ou, Tey Putita, Aubry, Fabien, Dabo, Stéphanie, Russet, Sylvie, Girault, Dominique, In, Saraden, Minier, Marine, Lequime, Sebastian, Hoem, Thavry, Boyer, Sébastien, Dussart, Philippe, Pocquet, Nicolas, Burtet-Sarramegna, Valérie, Lambrechts, Louis, Duong, Veasna, Dupont-Rouzeyrol, Myrielle
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Taylor & Francis 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8259877/
https://www.ncbi.nlm.nih.gov/pubmed/34139961
http://dx.doi.org/10.1080/22221751.2021.1944789
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author O’Connor, Olivia
Ou, Tey Putita
Aubry, Fabien
Dabo, Stéphanie
Russet, Sylvie
Girault, Dominique
In, Saraden
Minier, Marine
Lequime, Sebastian
Hoem, Thavry
Boyer, Sébastien
Dussart, Philippe
Pocquet, Nicolas
Burtet-Sarramegna, Valérie
Lambrechts, Louis
Duong, Veasna
Dupont-Rouzeyrol, Myrielle
author_facet O’Connor, Olivia
Ou, Tey Putita
Aubry, Fabien
Dabo, Stéphanie
Russet, Sylvie
Girault, Dominique
In, Saraden
Minier, Marine
Lequime, Sebastian
Hoem, Thavry
Boyer, Sébastien
Dussart, Philippe
Pocquet, Nicolas
Burtet-Sarramegna, Valérie
Lambrechts, Louis
Duong, Veasna
Dupont-Rouzeyrol, Myrielle
author_sort O’Connor, Olivia
collection PubMed
description Dengue virus (DENV) evolutionary dynamics are characterized by frequent DENV genotype/lineage replacements, potentially associated with changes in disease severity and human immunity. New Caledonia (NC) and Cambodia, two contrasted epidemiological settings, respectively experienced a DENV-1 genotype IV to I replacement in 2012 and a DENV-1 genotype I lineage 3–4 replacement in 2005–2007, both followed by a massive dengue outbreak. However, their underlying evolutionary drivers have not been elucidated. Here, we tested the hypothesis that these genotype/lineage switches reflected a higher transmission fitness of the replacing DENV genotype/lineage in the mosquito vector using in vivo competition experiments. For this purpose, field-derived Aedes aegypti from NC and Cambodia were orally challenged with epidemiologically relevant pairs of four DENV-1 genotype I and IV strains from NC or four DENV-1 genotype I lineage 3 and 4 strains from Cambodia, respectively. The relative transmission fitness of each DENV-1 genotype/lineage was measured by quantitative RT–PCR for infection, dissemination, and transmission rates. Results showed a clear transmission fitness advantage of the replacing DENV-1 genotype I from NC within the vector. A similar but more subtle pattern was observed for the DENV-1 lineage 4 replacement in Cambodia. Our results support the hypothesis that vector-driven selection contributed to the DENV-1 genotype/lineage replacements in these two contrasted epidemiological settings, and reinforce the idea that natural selection taking place within the mosquito vector plays an important role in DENV short-term evolutionary dynamics.
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spelling pubmed-82598772021-07-13 Potential role of vector-mediated natural selection in dengue virus genotype/lineage replacements in two epidemiologically contrasted settings O’Connor, Olivia Ou, Tey Putita Aubry, Fabien Dabo, Stéphanie Russet, Sylvie Girault, Dominique In, Saraden Minier, Marine Lequime, Sebastian Hoem, Thavry Boyer, Sébastien Dussart, Philippe Pocquet, Nicolas Burtet-Sarramegna, Valérie Lambrechts, Louis Duong, Veasna Dupont-Rouzeyrol, Myrielle Emerg Microbes Infect Research Article Dengue virus (DENV) evolutionary dynamics are characterized by frequent DENV genotype/lineage replacements, potentially associated with changes in disease severity and human immunity. New Caledonia (NC) and Cambodia, two contrasted epidemiological settings, respectively experienced a DENV-1 genotype IV to I replacement in 2012 and a DENV-1 genotype I lineage 3–4 replacement in 2005–2007, both followed by a massive dengue outbreak. However, their underlying evolutionary drivers have not been elucidated. Here, we tested the hypothesis that these genotype/lineage switches reflected a higher transmission fitness of the replacing DENV genotype/lineage in the mosquito vector using in vivo competition experiments. For this purpose, field-derived Aedes aegypti from NC and Cambodia were orally challenged with epidemiologically relevant pairs of four DENV-1 genotype I and IV strains from NC or four DENV-1 genotype I lineage 3 and 4 strains from Cambodia, respectively. The relative transmission fitness of each DENV-1 genotype/lineage was measured by quantitative RT–PCR for infection, dissemination, and transmission rates. Results showed a clear transmission fitness advantage of the replacing DENV-1 genotype I from NC within the vector. A similar but more subtle pattern was observed for the DENV-1 lineage 4 replacement in Cambodia. Our results support the hypothesis that vector-driven selection contributed to the DENV-1 genotype/lineage replacements in these two contrasted epidemiological settings, and reinforce the idea that natural selection taking place within the mosquito vector plays an important role in DENV short-term evolutionary dynamics. Taylor & Francis 2021-07-05 /pmc/articles/PMC8259877/ /pubmed/34139961 http://dx.doi.org/10.1080/22221751.2021.1944789 Text en © 2021 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group, on behalf of Shanghai Shangyixun Cultural Communication Co., Ltd https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) ), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
O’Connor, Olivia
Ou, Tey Putita
Aubry, Fabien
Dabo, Stéphanie
Russet, Sylvie
Girault, Dominique
In, Saraden
Minier, Marine
Lequime, Sebastian
Hoem, Thavry
Boyer, Sébastien
Dussart, Philippe
Pocquet, Nicolas
Burtet-Sarramegna, Valérie
Lambrechts, Louis
Duong, Veasna
Dupont-Rouzeyrol, Myrielle
Potential role of vector-mediated natural selection in dengue virus genotype/lineage replacements in two epidemiologically contrasted settings
title Potential role of vector-mediated natural selection in dengue virus genotype/lineage replacements in two epidemiologically contrasted settings
title_full Potential role of vector-mediated natural selection in dengue virus genotype/lineage replacements in two epidemiologically contrasted settings
title_fullStr Potential role of vector-mediated natural selection in dengue virus genotype/lineage replacements in two epidemiologically contrasted settings
title_full_unstemmed Potential role of vector-mediated natural selection in dengue virus genotype/lineage replacements in two epidemiologically contrasted settings
title_short Potential role of vector-mediated natural selection in dengue virus genotype/lineage replacements in two epidemiologically contrasted settings
title_sort potential role of vector-mediated natural selection in dengue virus genotype/lineage replacements in two epidemiologically contrasted settings
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8259877/
https://www.ncbi.nlm.nih.gov/pubmed/34139961
http://dx.doi.org/10.1080/22221751.2021.1944789
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