Aedes/physiology; Aedes/virology; Africa; Animals; Asia; Female; Humans; Male; Mice; Phylogeny; Virulence; Zika Virus/classification; Zika Virus/genetics; Zika Virus/pathogenicity; Zika Virus/physiology; Zika Virus Infection/mortality; Zika Virus Infection/transmission; Zika Virus Infection/virology; Aedes; Zika Virus; Zika Virus Infection; Chemistry (all); Biochemistry, Genetics and Molecular Biology (all); Physics and Astronomy (all); General Physics and Astronomy; General Biochemistry, Genetics and Molecular Biology; General Chemistry; Multidisciplinary
Abstract :
[en] The global emergence of Zika virus (ZIKV) revealed the unprecedented ability for a mosquito-borne virus to cause congenital birth defects. A puzzling aspect of ZIKV emergence is that all human outbreaks and birth defects to date have been exclusively associated with the Asian ZIKV lineage, despite a growing body of laboratory evidence pointing towards higher transmissibility and pathogenicity of the African ZIKV lineage. Whether this apparent paradox reflects the use of relatively old African ZIKV strains in most laboratory studies is unclear. Here, we experimentally compare seven low-passage ZIKV strains representing the recently circulating viral genetic diversity. We find that recent African ZIKV strains display higher transmissibility in mosquitoes and higher lethality in both adult and fetal mice than their Asian counterparts. We emphasize the high epidemic potential of African ZIKV strains and suggest that they could more easily go unnoticed by public health surveillance systems than Asian strains due to their propensity to cause fetal loss rather than birth defects.
Disciplines :
Life sciences: Multidisciplinary, general & others
Author, co-author :
Aubry, Fabien ✱; Insect-Virus Interactions Unit, Institut Pasteur, UMR2000, CNRS, Paris, France
Jacobs, Sofie ✱; KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute for Medical Research, Laboratory of Virology and Chemotherapy, Leuven, Belgium
Lequime, Sebastian ; KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Clinical and Epidemiological Virology, Leuven, Belgium ; Cluster of Microbial Ecology, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands
Delang, Leen ; KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute for Medical Research, Laboratory of Virology and Chemotherapy, Leuven, Belgium
Fontaine, Albin; Unité Parasitologie et Entomologie, Département Microbiologie et Maladies Infectieuses, Institut de Recherche Biomédicale des Armées (IRBA), Marseille, France ; IRD, SSA, AP-HM, UMR Vecteurs-Infections Tropicales et Méditerranéennes (VITROME), Aix Marseille University, Marseille, France ; IHU Méditerranée Infection, Marseille, France
Jupatanakul, Natapong ; Insect-Virus Interactions Unit, Institut Pasteur, UMR2000, CNRS, Paris, France ; National Center for Genetic Engineering and Biotechnology (BIOTEC), Pathum Thani, Thailand
Miot, Elliott F ; Insect-Virus Interactions Unit, Institut Pasteur, UMR2000, CNRS, Paris, France
Dabo, Stéphanie; Insect-Virus Interactions Unit, Institut Pasteur, UMR2000, CNRS, Paris, France
Manet, Caroline; Mouse Genetics Laboratory, Institut Pasteur, Paris, France
Montagutelli, Xavier ; Mouse Genetics Laboratory, Institut Pasteur, Paris, France
Baidaliuk, Artem ; Insect-Virus Interactions Unit, Institut Pasteur, UMR2000, CNRS, Paris, France ; Evolutionary Genomics of RNA Viruses Group, Institut Pasteur, Paris, France
Gámbaro, Fabiana; Evolutionary Genomics of RNA Viruses Group, Institut Pasteur, Paris, France
Simon-Lorière, Etienne ; Evolutionary Genomics of RNA Viruses Group, Institut Pasteur, Paris, France
Gilsoul, Maxime ; Université de Liège - ULiège > GIGA > GIGA Neurosciences - Molecular Regulation of Neurogenesis
Romero-Vivas, Claudia M; Laboratorio de Enfermedades Tropicales, Departamento de Medicina, Fundación Universidad del Norte, Barranquilla, Colombia
Cao-Lormeau, Van-Mai; Institut Louis Malardé, Papeete, Tahiti, French Polynesia
Jarman, Richard G; Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, USA
Diagne, Cheikh T; Arbovirus and Viral Hemorrhagic Fevers Unit, Institut Pasteur Dakar, Dakar, Senegal
Faye, Oumar; Arbovirus and Viral Hemorrhagic Fevers Unit, Institut Pasteur Dakar, Dakar, Senegal
Faye, Ousmane; Arbovirus and Viral Hemorrhagic Fevers Unit, Institut Pasteur Dakar, Dakar, Senegal
Sall, Amadou A; Arbovirus and Viral Hemorrhagic Fevers Unit, Institut Pasteur Dakar, Dakar, Senegal
Neyts, Johan ; KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute for Medical Research, Laboratory of Virology and Chemotherapy, Leuven, Belgium
Nguyen, Laurent ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Kaptein, Suzanne J F ✱; KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute for Medical Research, Laboratory of Virology and Chemotherapy, Leuven, Belgium. suzanne.kaptein@kuleuven.be
Lambrechts, Louis ✱; Insect-Virus Interactions Unit, Institut Pasteur, UMR2000, CNRS, Paris, France. louis.lambrechts@pasteur.fr
We thank Catherine Lallemand for assistance with mosquito rearing, the Institut Pasteur animal facility staff for the breeding of Ifnar1−/− mice. We thank Diego Ayala, Chris-tophe Paupy, and Davy Jiolle for initially providing the mosquito colony from Gabon and Anubis Vega-Rúa for initially providing the mosquito colony from Guadeloupe. We are grateful to the volunteers and the ICAReB staff for the human blood supply. We thank Elke Maas, Carolien De Keyzer, and Lindsey Bervoets for technical assistance with the AG129 mouse experiments, the KU Leuven Rega animal facility staff for breeding the AG129 mice, and Jelle Matthijnssens and Daan Jansen for resequencing the ZIKV strains at the KU Leuven Rega Institute. We thank Alexandre Hego and the GIGA-Imaging platform for their precious help and advice, and Christian Alfano and Ivan Gladwyn-Ng for their guidance with the vertical transmission experiments. This work was primarily funded by the European Union’s Horizon 2020 research and innovation program under ZikaPLAN grant agreement no. 734584 (to L.L. and J.N.) and under ZIKAlliance grant agreement no. 734548 (to L.N. and J.N.). This work was also supported by Agence Nationale de la Recherche (grants ANR-16-CE35-0004-01, ANR-17-ERC2-0016-01, and ANR-18-CE35-0003-01 to L.L.), the French Government’s Investissement d’Avenir program Laboratoire d’Excellence Integrative Biology of Emerging Infectious Diseases (grant ANR-10-LABX-62-IBEID to L.L. and X.M.), the Inception program (Investisse-ment d’Avenir grant ANR-16-CONV-0005 to L.L.), the Research Foundation Flanders (FWO Ph.D. fellowship 1S21918N to S.J.), and the Fonds de la Recherche Scientifique (FRIA Ph.D. fellowship to M.D.). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
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