Experimental adaptation of dengue virus 1 to Aedes albopictus mosquitoes by in vivo selection

Bellone, Rachel; Lequime, Sébastian; Jupille, Henri; Göertz, Giel P.; Aubry, Fabien; Mousson, Laurence; Piorkowski, Géraldine; Yen, Pei‐Shi; Gabiane, Gaëlle; Vazeille, Marie; Sakuntabhai, Anavaj; Pijlman, Gorben P.; Lamballerie, Xavier de; Lambrechts, Louis; Failloux, Anna‐Bella

doi:10.1038/s41598-020-75042-4

Cited by 13 publications

(11 citation statements)

References 63 publications

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“…Recently, a study reporting passage of DENV1 in Ae. albopictus mosquitoes found identical mutations altering SLII stability ( Bellone et al, 2020 ). These examples illustrate our ability to recapitulate and identify subtle shifts in the DMFE to uncover molecular mechanisms of selection and adaptation operating on DENV populations in cells and in host populations.…”

Section: Resultsmentioning

confidence: 99%

Principles of dengue virus evolvability derived from genotype-fitness maps in human and mosquito cells

Dolan

Taguwa

Rangel

et al. 2021

eLife

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Dengue virus (DENV) cycles between mosquito and mammalian hosts. To examine how DENV populations adapt to these different host environments we used serial passage in human and mosquito cell lines and estimated fitness effects for all single-nucleotide variants in these populations using ultra-deep sequencing. This allowed us to determine the contributions of beneficial and deleterious mutations to the collective fitness of the population. Our analysis revealed that the continuous influx of a large burden of deleterious mutations counterbalances the effect of rare, host-specific beneficial mutations to shape the path of adaptation. Beneficial mutations preferentially map to intrinsically disordered domains in the viral proteome and cluster to defined regions in the genome. These phenotypically redundant adaptive alleles may facilitate host-specific DENV adaptation. Importantly, the evolutionary constraints described in our simple system mirror trends observed across DENV and Zika strains, indicating it recapitulates key biophysical and biological constraints shaping long-term viral evolution.

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Section: Resultsmentioning

confidence: 99%

Principles of dengue virus evolvability derived from genotype-fitness maps in human and mosquito cells

Dolan

Taguwa

Rangel

et al. 2021

eLife

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“…Regarding the latter, it is also worthwhile to investigate whether the combined effect of repNS-iSNVs detected here amid the SD cases could elicit severe phenotypes. Epistatic relationships were recently documented for DENV [ 57 , 58 ].…”

Section: Discussionmentioning

confidence: 99%

Dengue Virus Serotype 2 Intrahost Diversity in Patients with Different Clinical Outcomes

Torres

Mendonça

Rodrigues

et al. 2021

Viruses

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Intrahost genetic diversity is thought to facilitate arbovirus adaptation to changing environments and hosts, and it might also be linked to viral pathogenesis. Dengue virus serotype 2 (DENV-2) has circulated in Brazil since 1990 and is associated with severe disease and explosive outbreaks. Intending to shed light on the viral determinants for severe dengue pathogenesis, we sought to analyze the DENV-2 intrahost genetic diversity in 68 patient cases clinically classified as dengue fever (n = 31), dengue with warning signs (n = 19), and severe dengue (n = 18). Unlike previous DENV intrahost diversity studies whose approaches employed PCR, here we performed viral whole-genome deep sequencing from clinical samples with an amplicon-free approach, representing the real intrahost diversity scenario. Striking differences were detected in the viral population structure between the three clinical categories, which appear to be driven mainly by different infection times and selection pressures, rather than being linked with the clinical outcome itself. Diversity in the NS2B gene, however, showed to be constrained, irrespective of clinical outcome and infection time. Finally, 385 non-synonymous intrahost single-nucleotide variants located along the viral polyprotein, plus variants located in the untranslated regions, were consistently identified among the samples. Of them, 124 were exclusively or highly detected among cases with warning signs and among severe cases. However, there was no variant that by itself appeared to characterize the cases of greater severity, either due to its low intrahost frequency or the conservative effect on amino acid substitution. Although further studies are necessary to determine their real effect on viral proteins, this heightens the possibility of epistatic interactions. The present analysis represents an initial effort to correlate DENV-2 genetic diversity to its pathogenic potential and thus contribute to understanding the virus’s dynamics within its human host.

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“…There are various methods for transferring blood-borne microbes between hosts in the laboratory including vector-mediated, subcutaneous (SC), intramuscular, intraperitoneal, intradermal (ID), intravenous, and intraocular inoculations. These methods range from ones that require little or no human intervention, such as transmission by arthropod vectors (e.g., Bellone et al, 2020), to others that require increasing levels of training and dexterity while providing greater control, from basic subcutaneous (e.g., Michelitsch et al, 2021) and intramuscular (e.g., Bastos et al, 2020) inoculations to more advanced methods including intraperitoneal (e.g., Kosoy et al, 1999),…”

Section: Transmission Methodsmentioning

confidence: 99%

A road map for in vivo evolution experiments with blood‐borne parasitic microbes

Rodríguez‐Pastor

Shafran

Knossow

et al. 2022

Molecular Ecology Resources

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Laboratory experiments in which blood‐borne parasitic microbes evolve in their animal hosts offer an opportunity to study parasite evolution and adaptation in real time and under natural settings. The main challenge of these experiments is to establish a protocol that is both practical over multiple passages and accurately reflects natural transmission scenarios and mechanisms. We provide a guide to the steps that should be considered when designing such a protocol, and we demonstrate its use via a case study. We highlight the importance of choosing suitable ancestral genotypes, treatments, number of replicates per treatment, types of negative controls, dependent variables, covariates, and the timing of checkpoints for the experimental design. We also recommend specific preliminary experiments to determine effective methods for parasite quantification, transmission, and preservation. Although these methodological considerations are technical, they also often have conceptual implications. To this end, we encourage other researchers to design and conduct in vivo evolution experiments with blood‐borne parasitic microbes, despite the challenges that the work entails.

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Experimental adaptation of dengue virus 1 to Aedes albopictus mosquitoes by in vivo selection

Cited by 13 publications

References 63 publications

Principles of dengue virus evolvability derived from genotype-fitness maps in human and mosquito cells

Principles of dengue virus evolvability derived from genotype-fitness maps in human and mosquito cells

Dengue Virus Serotype 2 Intrahost Diversity in Patients with Different Clinical Outcomes

A road map for in vivo evolution experiments with blood‐borne parasitic microbes

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