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

Roenick P Olmo^#^{1

2}, Yaovi M H Todjro^#¹, Eric R G R Aguiar^#^{1

3}, João Paulo P de Almeida¹, Flávia V Ferreira¹, Juliana N Armache¹, Isaque J S de Faria¹, Alvaro G A Ferreira⁴, Siad C G Amadou¹, Ana Teresa S Silva¹, Kátia P R de Souza¹, Ana Paula P Vilela¹, Antinea Babarit², Cheong H Tan⁵, Mawlouth Diallo⁶, Alioune Gaye⁶, Christophe Paupy⁷, Judicaël Obame-Nkoghe^{8

9}, Tessa M Visser¹⁰, Constantianus J M Koenraadt¹⁰, Merril A Wongsokarijo¹¹, Ana Luiza C Cruz¹², Mariliza T Prieto¹³, Maisa C P Parra¹⁴, Maurício L Nogueira^{14

15}, Vivian Avelino-Silva¹⁶, Renato N Mota¹⁷, Magno A Z Borges¹⁸, Betânia P Drumond¹², Erna G Kroon¹², Mario Recker^{19

20}, Luigi Sedda²¹, Eric Marois², Jean-Luc Imler², João T Marques^{22

23}

Affiliations

¹ Department of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil.
² Université de Strasbourg, CNRS UPR9022, INSERM U1257, Strasbourg, France.
³ Department of Biological Sciences (DCB), Center of Biotechnology and Genetics (CBG), State University of Santa Cruz (UESC), Ilhéus, Brazil.
⁴ Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte, Minas Gerais, Brazil.
⁵ Environmental Health Institute, Vector Biology and Control Division, National Environment Agency, Singapore, Singapore.
⁶ Pôle de Zoologie Médicale, Institut Pasteur de Dakar, Dakar, Senegal.
⁷ Maladies Infectieuses et Vecteurs: Écologie, Génétique, Évolution et Contrôle (MIVEGEC); Université de Montpellier, Institut de Recherche pour le Développement, CNRS, Montpellier, France.
⁸ Laboratoire de Biologie Moléculaire et Cellulaire, Département de Biologie, Université des Sciences et Techniques de Masuku, Franceville, Gabon.
⁹ Écologie des Systèmes Vectoriels, Centre Interdisciplinaire de Recherches Médicales de Franceville, Franceville, Gabon.
¹⁰ Laboratory of Entomology, Wageningen University and Research, Wageningen, the Netherlands.
¹¹ Central Laboratory of the Bureau of Public Health, Paramaribo, Suriname.
¹² Department of Microbiology, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Brazil.
¹³ Secretaria Municipal de Saúde, Seção de Controle de Vetores, Santos City Hall, Santos, Brazil.
¹⁴ Laboratory of Research in Virology, Faculdade de Medicina de São José do Rio Preto (FAMERP), São José do Rio Preto, Brazil.
¹⁵ Departament of Pathology, University of Texas Medical Branch, Galveston, TX, USA.
¹⁶ Department of Infectious and Parasitic Diseases, Faculdade de Medicina da Universidade de São Paulo (FMUSP), Cerqueira Cesar, Brazil.
¹⁷ Health Surveillance (Zoonosis Control), Brumadinho City Hall, Brumadinho, Brazil.
¹⁸ Center for Biological and Health Sciences, Universidade Estadual de Montes Claros, Montes Claros, Brazil.
¹⁹ Centre for Ecology and Conservation, University of Exeter, Penryn Campus, Penryn, UK.
²⁰ Institute of Tropical Medicine, Universitätsklinikum Tübingen, Tübingen, Germany.
²¹ Lancaster Medical School, Lancaster University, Lancaster, UK.
²² Department of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil. jtm@ufmg.br.
²³ Université de Strasbourg, CNRS UPR9022, INSERM U1257, Strasbourg, France. jtm@ufmg.br.

^# Contributed equally.

PMID: 36604511
DOI: 10.1038/s41564-022-01289-4

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

Roenick P Olmo et al. Nat Microbiol. 2023 Jan.

. 2023 Jan;8(1):135-149.

doi: 10.1038/s41564-022-01289-4. Epub 2023 Jan 5.

Authors

Affiliations

¹ Department of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil.
² Université de Strasbourg, CNRS UPR9022, INSERM U1257, Strasbourg, France.
³ Department of Biological Sciences (DCB), Center of Biotechnology and Genetics (CBG), State University of Santa Cruz (UESC), Ilhéus, Brazil.
⁴ Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte, Minas Gerais, Brazil.
⁵ Environmental Health Institute, Vector Biology and Control Division, National Environment Agency, Singapore, Singapore.
⁶ Pôle de Zoologie Médicale, Institut Pasteur de Dakar, Dakar, Senegal.
⁷ Maladies Infectieuses et Vecteurs: Écologie, Génétique, Évolution et Contrôle (MIVEGEC); Université de Montpellier, Institut de Recherche pour le Développement, CNRS, Montpellier, France.
⁸ Laboratoire de Biologie Moléculaire et Cellulaire, Département de Biologie, Université des Sciences et Techniques de Masuku, Franceville, Gabon.
⁹ Écologie des Systèmes Vectoriels, Centre Interdisciplinaire de Recherches Médicales de Franceville, Franceville, Gabon.
¹⁰ Laboratory of Entomology, Wageningen University and Research, Wageningen, the Netherlands.
¹¹ Central Laboratory of the Bureau of Public Health, Paramaribo, Suriname.
¹² Department of Microbiology, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Brazil.
¹³ Secretaria Municipal de Saúde, Seção de Controle de Vetores, Santos City Hall, Santos, Brazil.
¹⁴ Laboratory of Research in Virology, Faculdade de Medicina de São José do Rio Preto (FAMERP), São José do Rio Preto, Brazil.
¹⁵ Departament of Pathology, University of Texas Medical Branch, Galveston, TX, USA.
¹⁶ Department of Infectious and Parasitic Diseases, Faculdade de Medicina da Universidade de São Paulo (FMUSP), Cerqueira Cesar, Brazil.
¹⁷ Health Surveillance (Zoonosis Control), Brumadinho City Hall, Brumadinho, Brazil.
¹⁸ Center for Biological and Health Sciences, Universidade Estadual de Montes Claros, Montes Claros, Brazil.
¹⁹ Centre for Ecology and Conservation, University of Exeter, Penryn Campus, Penryn, UK.
²⁰ Institute of Tropical Medicine, Universitätsklinikum Tübingen, Tübingen, Germany.
²¹ Lancaster Medical School, Lancaster University, Lancaster, UK.
²² Department of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil. jtm@ufmg.br.
²³ Université de Strasbourg, CNRS UPR9022, INSERM U1257, Strasbourg, France. jtm@ufmg.br.

^# Contributed equally.

PMID: 36604511
DOI: 10.1038/s41564-022-01289-4

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.

PubMed Disclaimer

References

1. Weaver, S. C., Charlier, C., Vasilakis, N. & Lecuit, M. Zika, chikungunya, and other emerging vector-borne viral diseases. Annu. Rev. Med 69, 395–408 (2018). - DOI
1. Bhatt, S. et al. The global distribution and burden of dengue. Nature 496, 504–507 (2013). - DOI
1. Messina, J. P. et al. Global spread of dengue virus types: mapping the 70 year history. Trends Microbiol. 22, 138–146 (2014). - DOI
1. Franklinos, L. H. V., Jones, K. E., Redding, D. W. & Abubakar, I. The effect of global change on mosquito-borne disease. Lancet Infect. Dis. 19, e302–e312 (2019). - DOI
1. Kraemer, M. U. G. et al. Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat. Microbiol. 4, 854–863 (2019). - DOI

Publication types

Actions
Actions

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions

Grants and funding

U01 AI151807/AI/NIAID NIH HHS/United States

LinkOut - more resources

Full Text Sources
- Nature Publishing Group
Medical
- MedlinePlus Health Information
Research Materials
- Addgene Non-profit plasmid repository

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

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

Affiliations

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

Authors

Affiliations

Abstract

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Medical

Research Materials