Mosquito vector competence for dengue is modulated by insect-specific viruses

Roenick P. Olmo; Yaovi M.H. Todjro; Eric R.G.R. Aguiar; João Paulo P. de Almeida; Flávia V. Ferreira; Juliana N. Armache; Isaque J.S. de Faria; Alvaro G.A. Ferreira; Siad C.G. Amadou; Ana Teresa S. Silva; Kátia P.R. de Souza; Ana Paula P. Vilela; Antinea Babarit; Cheong H. Tan; Mawlouth Diallo; Alioune Gaye; Christophe Paupy; Judicaël Obame-Nkoghe; Tessa M. Visser; Constantianus J.M. Koenraadt; Merril A. Wongsokarijo; Ana Luiza C. Cruz; Mariliza T. Prieto; Maisa C.P. Parra; Maurício L. Nogueira; Vivian Avelino-Silva; Renato N. Mota; Magno A.Z. Borges; Betânia P. Drumond; Erna G. Kroon; Mario Recker; Luigi Sedda; Eric Marois; Jean Luc Imler; João T. Marques

doi:10.1038/s41564-022-01289-4

Mosquito vector competence for dengue is modulated by insect-specific viruses

Roenick P. Olmo, Yaovi M.H. Todjro, Eric R.G.R. Aguiar, João Paulo P. de Almeida, Flávia V. Ferreira, Juliana N. Armache, Isaque J.S. de Faria, Alvaro G.A. Ferreira, Siad C.G. Amadou, Ana Teresa S. Silva, Kátia P.R. de Souza, Ana Paula P. Vilela, Antinea Babarit, Cheong H. Tan, Mawlouth Diallo, Alioune Gaye, Christophe Paupy, Judicaël Obame-Nkoghe, Tessa M. Visser, Constantianus J.M. KoenraadtMerril A. Wongsokarijo, Ana Luiza C. Cruz, Mariliza T. Prieto, Maisa C.P. Parra, Maurício L. Nogueira, Vivian Avelino-Silva, Renato N. Mota, Magno A.Z. Borges, Betânia P. Drumond, Erna G. Kroon, Mario Recker, Luigi Sedda, Eric Marois, Jean Luc Imler, João T. Marques^*

^*Corresponding author for this work

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

72 Citations (Scopus)

Abstract

Aedes aegypti and A. albopictus mosquitoes are the main vectors for dengue virus (DENV) and other arboviruses, including Zika virus (ZIKV). Understanding the factors that affect transmission of arboviruses from mosquitoes to humans is a priority because it could inform public health and targeted interventions. Reasoning that interactions among viruses in the vector insect might affect transmission, we analysed the viromes of 815 urban Aedes mosquitoes collected from 12 countries worldwide. Two mosquito-specific viruses, Phasi Charoen-like virus (PCLV) and Humaita Tubiacanga virus (HTV), were the most abundant in A. aegypti worldwide. Spatiotemporal analyses of virus circulation in an endemic urban area revealed a 200% increase in chances of having DENV in wild A. aegypti mosquitoes when both HTV and PCLV were present. Using a mouse model in the laboratory, we showed that the presence of HTV and PCLV increased the ability of mosquitoes to transmit DENV and ZIKV to a vertebrate host. By transcriptomic analysis, we found that in DENV-infected mosquitoes, HTV and PCLV block the downregulation of histone H4, which we identify as an important proviral host factor in vivo.

Original language	English
Pages (from-to)	135-149
Journal	Nature Microbiology
Volume	8
Issue number	1
DOIs	https://doi.org/10.1038/s41564-022-01289-4
Publication status	Published - 5 Jan 2023

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Global virome of Aedes mosquitoes
Olmo, R. P. (Creator), Todjro, Y. M. H. (Creator), Aguiar, E. R. G. R. (Creator), de Almeida, J. P. P. (Creator), Ferreira, F. V. (Creator), Armache, J. N. (Creator), de Faria, I. J. S. (Creator), Ferreira, A. G. A. (Creator), Amadou, S. C. G. (Creator), Silva, A. T. S. (Creator), de Souza, K. P. R. (Creator), Vilela, A. P. P. (Creator), Babarit, A. (Creator), Tan, C. H. (Creator), Diallo, M. (Creator), Gaye, A. (Creator), Paupy, C. (Creator), Obame-Nkoghe, J. (Creator), Visser, T. M. (Creator), Koenraadt, C. J. M. (Creator), Wongsokarijo, M. A. (Creator), Cruz, A. L. C. (Creator), Prieto, M. T. (Creator), Parra, M. C. P. (Creator), Nogueira, M. L. (Creator), Avelino-Silva, V. (Creator), Mota, R. N. (Creator), Borges, M. A. Z. (Creator), Drumond, B. P. (Creator), Kroon, E. G. (Creator), Recker, M. (Creator), Sedda, L. (Creator), Marois, E. (Creator), Imler, J. L. (Creator) & Marques, J. T. (Creator), Universidade Federal de Minas Gerais, 17 Apr 2021
https://www.ncbi.nlm.nih.gov/bioproject/722589
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Olmo, R. P., Todjro, Y. M. H., Aguiar, E. R. G. R., de Almeida, J. P. P., Ferreira, F. V., Armache, J. N., de Faria, I. J. S., Ferreira, A. G. A., Amadou, S. C. G., Silva, A. T. S., de Souza, K. P. R., Vilela, A. P. P., Babarit, A., Tan, C. H., Diallo, M., Gaye, A., Paupy, C., Obame-Nkoghe, J., Visser, T. M., ... Marques, J. T. (2023). Mosquito vector competence for dengue is modulated by insect-specific viruses. Nature Microbiology, 8(1), 135-149. https://doi.org/10.1038/s41564-022-01289-4

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abstract = "Aedes aegypti and A. albopictus mosquitoes are the main vectors for dengue virus (DENV) and other arboviruses, including Zika virus (ZIKV). Understanding the factors that affect transmission of arboviruses from mosquitoes to humans is a priority because it could inform public health and targeted interventions. Reasoning that interactions among viruses in the vector insect might affect transmission, we analysed the viromes of 815 urban Aedes mosquitoes collected from 12 countries worldwide. Two mosquito-specific viruses, Phasi Charoen-like virus (PCLV) and Humaita Tubiacanga virus (HTV), were the most abundant in A. aegypti worldwide. Spatiotemporal analyses of virus circulation in an endemic urban area revealed a 200% increase in chances of having DENV in wild A. aegypti mosquitoes when both HTV and PCLV were present. Using a mouse model in the laboratory, we showed that the presence of HTV and PCLV increased the ability of mosquitoes to transmit DENV and ZIKV to a vertebrate host. By transcriptomic analysis, we found that in DENV-infected mosquitoes, HTV and PCLV block the downregulation of histone H4, which we identify as an important proviral host factor in vivo.",

author = "Olmo, {Roenick P.} and Todjro, {Yaovi M.H.} and Aguiar, {Eric R.G.R.} and {de Almeida}, {Jo{\~a}o Paulo P.} and Ferreira, {Fl{\'a}via V.} and Armache, {Juliana N.} and {de Faria}, {Isaque J.S.} and Ferreira, {Alvaro G.A.} and Amadou, {Siad C.G.} and Silva, {Ana Teresa S.} and {de Souza}, {K{\'a}tia P.R.} and Vilela, {Ana Paula P.} and Antinea Babarit and Tan, {Cheong H.} and Mawlouth Diallo and Alioune Gaye and Christophe Paupy and Judica{\"e}l Obame-Nkoghe and Visser, {Tessa M.} and Koenraadt, {Constantianus J.M.} and Wongsokarijo, {Merril A.} and Cruz, {Ana Luiza C.} and Prieto, {Mariliza T.} and Parra, {Maisa C.P.} and Nogueira, {Maur{\'i}cio L.} and Vivian Avelino-Silva and Mota, {Renato N.} and Borges, {Magno A.Z.} and Drumond, {Bet{\^a}nia P.} and Kroon, {Erna G.} and Mario Recker and Luigi Sedda and Eric Marois and Imler, {Jean Luc} and Marques, {Jo{\~a}o T.}",

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doi = "10.1038/s41564-022-01289-4",

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Olmo, RP, Todjro, YMH, Aguiar, ERGR, de Almeida, JPP, Ferreira, FV, Armache, JN, de Faria, IJS, Ferreira, AGA, Amadou, SCG, Silva, ATS, de Souza, KPR, Vilela, APP, Babarit, A, Tan, CH, Diallo, M, Gaye, A, Paupy, C, Obame-Nkoghe, J, Visser, TM , Koenraadt, CJM, Wongsokarijo, MA, Cruz, ALC, Prieto, MT, Parra, MCP, Nogueira, ML, Avelino-Silva, V, Mota, RN, Borges, MAZ, Drumond, BP, Kroon, EG, Recker, M, Sedda, L, Marois, E, Imler, JL & Marques, JT 2023, 'Mosquito vector competence for dengue is modulated by insect-specific viruses', Nature Microbiology, vol. 8, no. 1, pp. 135-149. https://doi.org/10.1038/s41564-022-01289-4

TY - JOUR

T1 - Mosquito vector competence for dengue is modulated by insect-specific viruses

AU - Olmo, Roenick P.

AU - Todjro, Yaovi M.H.

AU - Aguiar, Eric R.G.R.

AU - de Almeida, João Paulo P.

AU - Ferreira, Flávia V.

AU - Armache, Juliana N.

AU - de Faria, Isaque J.S.

AU - Ferreira, Alvaro G.A.

AU - Amadou, Siad C.G.

AU - Silva, Ana Teresa S.

AU - de Souza, Kátia P.R.

AU - Vilela, Ana Paula P.

AU - Babarit, Antinea

AU - Tan, Cheong H.

AU - Diallo, Mawlouth

AU - Gaye, Alioune

AU - Paupy, Christophe

AU - Obame-Nkoghe, Judicaël

AU - Visser, Tessa M.

AU - Koenraadt, Constantianus J.M.

AU - Wongsokarijo, Merril A.

AU - Cruz, Ana Luiza C.

AU - Prieto, Mariliza T.

AU - Parra, Maisa C.P.

AU - Nogueira, Maurício L.

AU - Avelino-Silva, Vivian

AU - Mota, Renato N.

AU - Borges, Magno A.Z.

AU - Drumond, Betânia P.

AU - Kroon, Erna G.

AU - Recker, Mario

AU - Sedda, Luigi

AU - Marois, Eric

AU - Imler, Jean Luc

AU - Marques, João T.

PY - 2023/1/5

Y1 - 2023/1/5

N2 - Aedes aegypti and A. albopictus mosquitoes are the main vectors for dengue virus (DENV) and other arboviruses, including Zika virus (ZIKV). Understanding the factors that affect transmission of arboviruses from mosquitoes to humans is a priority because it could inform public health and targeted interventions. Reasoning that interactions among viruses in the vector insect might affect transmission, we analysed the viromes of 815 urban Aedes mosquitoes collected from 12 countries worldwide. Two mosquito-specific viruses, Phasi Charoen-like virus (PCLV) and Humaita Tubiacanga virus (HTV), were the most abundant in A. aegypti worldwide. Spatiotemporal analyses of virus circulation in an endemic urban area revealed a 200% increase in chances of having DENV in wild A. aegypti mosquitoes when both HTV and PCLV were present. Using a mouse model in the laboratory, we showed that the presence of HTV and PCLV increased the ability of mosquitoes to transmit DENV and ZIKV to a vertebrate host. By transcriptomic analysis, we found that in DENV-infected mosquitoes, HTV and PCLV block the downregulation of histone H4, which we identify as an important proviral host factor in vivo.

AB - Aedes aegypti and A. albopictus mosquitoes are the main vectors for dengue virus (DENV) and other arboviruses, including Zika virus (ZIKV). Understanding the factors that affect transmission of arboviruses from mosquitoes to humans is a priority because it could inform public health and targeted interventions. Reasoning that interactions among viruses in the vector insect might affect transmission, we analysed the viromes of 815 urban Aedes mosquitoes collected from 12 countries worldwide. Two mosquito-specific viruses, Phasi Charoen-like virus (PCLV) and Humaita Tubiacanga virus (HTV), were the most abundant in A. aegypti worldwide. Spatiotemporal analyses of virus circulation in an endemic urban area revealed a 200% increase in chances of having DENV in wild A. aegypti mosquitoes when both HTV and PCLV were present. Using a mouse model in the laboratory, we showed that the presence of HTV and PCLV increased the ability of mosquitoes to transmit DENV and ZIKV to a vertebrate host. By transcriptomic analysis, we found that in DENV-infected mosquitoes, HTV and PCLV block the downregulation of histone H4, which we identify as an important proviral host factor in vivo.

U2 - 10.1038/s41564-022-01289-4

DO - 10.1038/s41564-022-01289-4

M3 - Article

C2 - 36604511

AN - SCOPUS:85145645684

SN - 2058-5276

VL - 8

SP - 135

EP - 149

JO - Nature Microbiology

JF - Nature Microbiology

IS - 1

ER -

Mosquito vector competence for dengue is modulated by insect-specific viruses

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Global virome of Aedes mosquitoes

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