Mosquito vector competence for dengue is modulated by insect-specific viruses.
Journal
Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869
Informations de publication
Date de publication:
01 2023
01 2023
Historique:
received:
10
08
2022
accepted:
16
11
2022
entrez:
5
1
2023
pubmed:
6
1
2023
medline:
10
1
2023
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 36604511
doi: 10.1038/s41564-022-01289-4
pii: 10.1038/s41564-022-01289-4
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
135-149Subventions
Organisme : NIAID NIH HHS
ID : U01 AI151807
Pays : United States
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
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: 10.1146/annurev-med-050715-105122
Bhatt, S. et al. The global distribution and burden of dengue. Nature 496, 504–507 (2013).
doi: 10.1038/nature12060
Messina, J. P. et al. Global spread of dengue virus types: mapping the 70 year history. Trends Microbiol. 22, 138–146 (2014).
doi: 10.1016/j.tim.2013.12.011
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: 10.1016/S1473-3099(19)30161-6
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: 10.1038/s41564-019-0376-y
Cromwell, E. A. et al. The relationship between entomological indicators of Aedes aegypti abundance and dengue virus infection. PLoS Negl. Trop. Dis. 11, e0005429 (2017).
doi: 10.1371/journal.pntd.0005429
de Almeida, J. P., Aguiar, E. R., Armache, J. N., Olmo, R. P. & Marques, J. T. The virome of vector mosquitoes. Curr. Opin. Virol. 49, 7–12 (2021).
doi: 10.1016/j.coviro.2021.04.002
Aguiar, E. R. G. R. et al. Sequence-independent characterization of viruses based on the pattern of viral small RNAs produced by the host. Nucleic Acids Res. 43, 6191–6206 (2015).
doi: 10.1093/nar/gkv587
Boyles, S. M. et al. Under-the-radar dengue virus infections in natural populations of Aedes aegypti mosquitoes. mSphere 5, e00316–20 (2020).
doi: 10.1128/mSphere.00316-20
Ramos-Nino, M. E. et al. High prevalence of Phasi Charoen-like virus from wild-caught Aedes aegypti in Grenada, W.I. as revealed by metagenomic analysis. PLoS ONE 15, e0227998 (2020).
doi: 10.1371/journal.pone.0227998
Shi, C. et al. Stable distinct core eukaryotic viromes in different mosquito species from Guadeloupe, using single mosquito viral metagenomics. Microbiome 7, 121 (2019).
doi: 10.1186/s40168-019-0734-2
Zakrzewski, M. et al. Mapping the virome in wild-caught Aedes aegypti from Cairns and Bangkok. Sci. Rep. 8, 4690 (2018).
doi: 10.1038/s41598-018-22945-y
Patterson, E. I., Villinger, J., Muthoni, J. N., Dobel-Ober, L. & Hughes, G. L. Exploiting insect-specific viruses as a novel strategy to control vector-borne disease. Curr. Opin. Insect Sci. 39, 50–56 (2020).
doi: 10.1016/j.cois.2020.02.005
Vasilakis, N. & Tesh, R. B. Insect-specific viruses and their potential impact on arbovirus transmission. Curr. Opin. Virol. 15, 69–74 (2015).
doi: 10.1016/j.coviro.2015.08.007
Aguiar, E. R. G. R., Olmo, R. P. & Marques, J. T. Virus-derived small RNAs: molecular footprints of host-pathogen interactions. Wiley Interdiscip. Rev. RNA 7, 824–837 (2016).
doi: 10.1002/wrna.1361
Morazzani, E. M., Wiley, M. R., Murreddu, M. G., Adelman, Z. N. & Myles, K. M. Production of virus-derived ping-pong-dependent piRNA-like small RNAs in the mosquito soma. PLoS Pathog. 8, e1002470 (2012).
doi: 10.1371/journal.ppat.1002470
Myles, K. M., Wiley, M. R., Morazzani, E. M. & Adelman, Z. N. Alphavirus-derived small RNAs modulate pathogenesis in disease vector mosquitoes. Proc. Natl Acad. Sci. USA 105, 19938–19943 (2008).
doi: 10.1073/pnas.0803408105
Frangeul, L., Blanc, H., Saleh, M.-C. & Suzuki, Y. Differential small RNA responses against co-infecting insect-specific viruses in Aedes albopictus mosquitoes. Viruses 12, 468 (2020).
Olmo, R. P. et al. Control of dengue virus in the midgut of Aedes aegypti by ectopic expression of the dsRNA-binding protein Loqs2. Nat. Microbiol. 3, 1385–1393 (2018).
doi: 10.1038/s41564-018-0268-6
Sedda, L. et al. The spatial and temporal scales of local dengue virus transmission in natural settings: a retrospective analysis. Parasit. Vectors 11, 79 (2018).
doi: 10.1186/s13071-018-2662-6
Schultz, M. J., Frydman, H. M. & Connor, J. H. Dual insect specific virus infection limits Arbovirus replication in Aedes mosquito cells. Virology 518, 406–413 (2018).
doi: 10.1016/j.virol.2018.03.022
Fredericks, A. C. et al. Aedes aegypti (Aag2)-derived clonal mosquito cell lines reveal the effects of pre-existing persistent infection with the insect-specific bunyavirus Phasi Charoen-like virus on arbovirus replication. PLoS Negl. Trop. Dis. 13, e0007346 (2019).
doi: 10.1371/journal.pntd.0007346
Sedda, L., Taylor, B. M., Eiras, A. E., Marques, J. T. & Dillon, R. J. Using the intrinsic growth rate of the mosquito population improves spatio-temporal dengue risk estimation. Acta Trop. 208, 105519 (2020).
doi: 10.1016/j.actatropica.2020.105519
Lin, J.-J. et al. Aggressive organ penetration and high vector transmissibility of epidemic dengue virus-2 cosmopolitan genotype in a transmission mouse model. PLoS Pathog. 17, e1009480 (2021).
doi: 10.1371/journal.ppat.1009480
Sun, P. et al. A mosquito salivary protein promotes flavivirus transmission by activation of autophagy. Nat. Commun. 11, 260 (2020).
doi: 10.1038/s41467-019-14115-z
Lourenço, J. & Recker, M. Natural, persistent oscillations in a spatial multi-strain disease system with application to dengue. PLoS Comput. Biol. 9, e1003308 (2013).
doi: 10.1371/journal.pcbi.1003308
Lourenço, J. et al. Epidemiological and ecological determinants of Zika virus transmission in an urban setting. eLife 6, e29820 (2017).
doi: 10.7554/eLife.29820
Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).
doi: 10.1073/pnas.0506580102
Flaus, A., Downs, J. A. & Owen-Hughes, T. Histone isoforms and the oncohistone code. Curr. Opin. Genet. Dev. 67, 61–66 (2021).
doi: 10.1016/j.gde.2020.11.003
Lyons, S. M. et al. A subset of replication-dependent histone mRNAs are expressed as polyadenylated RNAs in terminally differentiated tissues. Nucleic Acids Res. 44, 9190–9205 (2016).
Baidaliuk, A. et al. Cell-fusing agent virus reduces arbovirus dissemination in Aedes aegypti mosquitoes in vivo. J. Virol. 93, e00705–e00719 (2019).
Blitvich, B. J. & Firth, A. E. Insect-specific flaviviruses: a systematic review of their discovery, host range, mode of transmission, superinfection exclusion potential and genomic organization. Viruses 7, 1927–1959 (2015).
doi: 10.3390/v7041927
Colpitts, T. M., Barthel, S., Wang, P. & Fikrig, E. Dengue virus capsid protein binds core histones and inhibits nucleosome formation in human liver cells. PLoS ONE 6, e24365 (2011).
doi: 10.1371/journal.pone.0024365
Mourão, D. et al. A histone-like motif in yellow fever virus contributes to viral replication. Preprint at bioRxiv https://doi.org/10.1101/2020.05.05.078782 (2020).
Girardi, E. et al. Histone-derived piRNA biogenesis depends on the ping-pong partners Piwi5 and Ago3 in Aedes aegypti. Nucleic Acids Res. 45, 4881–4892 (2017).
Varjak, M. et al. Aedes aegypti Piwi4 is a noncanonical PIWI protein involved in antiviral responses. mSphere 2, e00144-17 (2017).
doi: 10.1128/mSphere.00144-17
Parry, R. & Asgari, S. Aedes anphevirus: an insect-specific virus distributed worldwide in Aedes aegypti mosquitoes that has complex interplays with Wolbachia and dengue virus infection in cells. J. Virol. 92, e00224-18 (2018).
doi: 10.1128/JVI.00224-18
Zhang, G., Asad, S., Khromykh, A. A. & Asgari, S. Cell fusing agent virus and dengue virus mutually interact in Aedes aegypti cell lines. Sci. Rep. 7, 6935 (2017).
doi: 10.1038/s41598-017-07279-5
Nasar, F., Erasmus, J. H., Haddow, A. D., Tesh, R. B. & Weaver, S. C. Eilat virus induces both homologous and heterologous interference. Virology 484, 51–58 (2015).
doi: 10.1016/j.virol.2015.05.009
Kenney, J. L., Solberg, O. D., Langevin, S. A. & Brault, A. C. Characterization of a novel insect-specific flavivirus from Brazil: potential for inhibition of infection of arthropod cells with medically important flaviviruses. J. Gen. Virol. 95, 2796–2808 (2014).
doi: 10.1099/vir.0.068031-0
Romo, H., Kenney, J. L., Blitvich, B. J. & Brault, A. C. Restriction of Zika virus infection and transmission in Aedes aegypti mediated by an insect-specific flavivirus. Emerg. Microbes Infect. 7, 1–13 (2018).
doi: 10.1038/s41426-018-0180-4
Goenaga, S. et al. Potential for co-infection of a mosquito-specific flavivirus, nhumirim virus, to block West Nile virus transmission in mosquitoes. Viruses 7, 5801–5812 (2015).
doi: 10.3390/v7112911
Alefelder, S., Patel, B. K. & Eckstein, F. Incorporation of terminal phosphorothioates into oligonucleotides. Nucleic Acids Res. 26, 4983–4988 (1998).
doi: 10.1093/nar/26.21.4983
Marques, J. T. et al. Loqs and R2D2 act sequentially in the siRNA pathway in Drosophila. Nat. Struct. Mol. Biol. 17, 24–30 (2010).
doi: 10.1038/nsmb.1735
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet j. 17, 10–12 (2011).
doi: 10.14806/ej.17.1.200
Matthews, B. J. et al. Improved reference genome of Aedes aegypti informs arbovirus vector control. Nature 563, 501–507 (2018).
doi: 10.1038/s41586-018-0692-z
Chen, X.-G. et al. Genome sequence of the Asian Tiger mosquito, Aedes albopictus, reveals insights into its biology, genetics, and evolution. Proc. Natl Acad. Sci. USA 112, E5907–E5915 (2015).
doi: 10.1073/pnas.1516410112
Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
doi: 10.1186/gb-2009-10-3-r25
Zerbino, D. R. Using the Velvet de novo assembler for short-read sequencing technologies. Curr. Protoc. Bioinform. https://doi.org/10.1002/0471250953.bi1105s31 (2010).
Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).
doi: 10.1089/cmb.2012.0021
O’Leary, N. A. et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 44, D733–D745 (2016).
doi: 10.1093/nar/gkv1189
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
doi: 10.1016/S0022-2836(05)80360-2
Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152 (2012).
doi: 10.1093/bioinformatics/bts565
Aguiar, E. R. G. R. et al. A single unidirectional piRNA cluster similar to the flamenco locus is the major source of EVE-derived transcription and small RNAs in Aedes aegypti mosquitoes. RNA 26, 581–594 (2020).
doi: 10.1261/rna.073965.119
Whitfield, Z. J. et al. The diversity, structure, and function of heritable adaptive immunity sequences in the Aedes aegypti genome. Curr. Biol. 27, 3511–3519.e7 (2017).
doi: 10.1016/j.cub.2017.09.067
Palatini, U. et al. Comparative genomics shows that viral integrations are abundant and express piRNAs in the arboviral vectors Aedes aegypti and Aedes albopictus. BMC Genomics 18, 512 (2017).
doi: 10.1186/s12864-017-3903-3
Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002).
doi: 10.1093/nar/gkf436
Miller, M. A., Pfeiffer, W. & Schwartz, T. The CIPRES science gateway: a community resource for phylogenetic analyses. In Towns J. Proc. 2011 TeraGrid Conference on Extreme Digital Discovery - TG ’11 41, 1-8 (ACM Press, 2011).
Darriba, D. et al. ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol. Biol. Evol. 37, 291–294 (2020).
doi: 10.1093/molbev/msz189
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).
doi: 10.1093/molbev/msy096
Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47, W256–W259 (2019).
doi: 10.1093/nar/gkz239
Barletta, A. B. F. et al. Microbiota activates IMD pathway and limits Sindbis infection in Aedes aegypti. Parasit. Vectors 10, 103 (2017).
doi: 10.1186/s13071-017-2040-9
Donald, C. L. et al. Full genome sequence and sfRNA interferon antagonist activity of Zika virus from Recife, Brazil. PLoS Negl. Trop. Dis. 10, e0005048 (2016).
doi: 10.1371/journal.pntd.0005048
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
doi: 10.1093/bioinformatics/btu170
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).
doi: 10.1038/nmeth.4197
Robinson, M. D. & Oshlack, A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25 (2010).
doi: 10.1186/gb-2010-11-3-r25
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).
doi: 10.1093/bioinformatics/btp616
Korotkevich, G. et al. Fast gene set enrichment analysis. Preprint at bioRxiv https://doi.org/10.1101/060012 (2016).
Di Tommaso, P. et al. T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res. 39, W13–W17 (2011).
doi: 10.1093/nar/gkr245
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).
doi: 10.1093/sysbio/syq010
Lefort, V., Longueville, J.-E. & Gascuel, O. SMS: Smart Model Selection in PhyML. Mol. Biol. Evol. 34, 2422–2424 (2017).
doi: 10.1093/molbev/msx149
Lambert, D. Zero-inflated Poisson regression, with an application to defects in manufacturing. Technometrics 34, 1–14 (1992).
doi: 10.2307/1269547
Hilbe, J. M. Negative Binomial Regression (2007).
Cameron, A. C. & Trivedi, P. K. Regression Analysis of Count Data (Cambridge Univ. Press, 1998).
Zeileis, A., Kleiber, C. & Jackman, S. Regression models for count data in R. J. Stat. Softw. 27, 8 (2008).
doi: 10.18637/jss.v027.i08