Variation in the susceptibility of urban Aedes mosquitoes infected with a densovirus

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).

Article  CAS  Google Scholar 

Kilpatrick, A. M. & Randolph, S. E. Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet 380, 1946–1955 (2012).

PubMed Central  Article  PubMed  Google Scholar 

Koureas, M., Tsakalof, A., Tsatsakis, A. & Hadjichristodoulou, C. Systematic review of biomonitoring studies to determine the association between exposure to organophosphorus and pyrethroid insecticides and human health outcomes. Toxicol. Lett. 210, 155–168 (2012).

Article  CAS  Google Scholar 

Peterson Robert, K. D., Macedo Paula, A. & Davis Ryan, S. A human-health risk assessment for West Nile Virus and insecticides used in mosquito management. Environ. Health Perspect. 114, 366–372 (2006).

Article  CAS  Google Scholar 

Han, W., Tian, Y. & Shen, X. Human exposure to neonicotinoid insecticides and the evaluation of their potential toxicity: an overview. Chemosphere 192, 59–65 (2018).

ADS  Article  CAS  Google Scholar 

Hernández, A. F. et al. Toxic effects of pesticide mixtures at a molecular level: their relevance to human health. Toxicology 307, 136–145 (2013).

Article  CAS  Google Scholar 

Sanchez-Bayo, F. P. Insecticides mode of action in relation to their toxicity to non-target organisms. J. Environ. Anal. Toxicol. s4, 002 (2012).

Google Scholar 

Rivero, A., Vézilier, J., Weill, M., Read, A. F. & Gandon, S. Insecticide control of vector-borne diseases: when is insecticide resistance a problem?. PLoS Pathog. 6, e1001000 (2010).

PubMed Central  Article  CAS  PubMed  Google Scholar 

Hemingway, J., Hawkes, N. J., McCarroll, L. & Ranson, H. The molecular basis of insecticide resistance in mosquitoes. Insect Biochem. Mol. Biol. 34, 653–665 (2004).

Article  CAS  Google Scholar 

Liu, N., Xu, Q., Zhu, F. & Zhang, L. Pyrethroid resistance in mosquitoes. Insect Sci. 13, 159–166 (2006).

Article  CAS  Google Scholar 

Dusfour, I. et al. Management of insecticide resistance in the major Aedes vectors of arboviruses: advances and challenges. PLoS Negl. Trop. Dis. 13, e0007615 (2019).

PubMed Central  Article  CAS  PubMed  Google Scholar 

Faraji, A. & Unlu, I. The eye of the tiger, the thrill of the fight: effective larval and adult control measures against the Asian tiger mosquito, Aedesalbopictus (Diptera: Culicidae), in North America. J. Med. Entomol. 53, 1029–1047 (2016).

Article  Google Scholar 

Chan, K. L., Ho, B. C. & Chan, Y. C. Aedesaegypti (L.) and Aedesalbopictus (Skuse) in Singapore City. Bull. World Health Organ. 44, 629–633 (1971).

PubMed Central  CAS  PubMed  Google Scholar 

Sansinenea, E. Bacillusthuringiensis Biotechnology (Springer, New York, 2012).

Google Scholar 

Mulla, M. S., Darwazeh, H. A. & Zgomba, M. Effect of some environmental factors on the efficacy of Bacillussphaericus 2362 and Bacillusthuringiensis (H-14) against mosquitoes. Bull. Soc. Vector Ecol. 15, 166–175 (1990).

Google Scholar 

Marina, C. F., Arredondo-Jiménez, J. I., Castillo, A. & Williams, T. Sublethal effects of iridovirus disease in a mosquito. Oecologia 119, 383–388 (1999).

ADS  Article  Google Scholar 

Delhon, G. et al. Genome of invertebrate iridescent virus type 3 (mosquito iridescent virus). J. Virol. 80, 8439–8449 (2006).

PubMed Central  Article  CAS  PubMed  Google Scholar 

Linley, J. R. & Nielsen, H. T. Transmission of a mosquito iridescent virus in Aedestaeniorhynchus: I. Laboratory experiments. J. Invertebr. Pathol. 12, 7–16 (1968).

Article  CAS  Google Scholar 

Carlson, J., Suchman, E. & Buchatsky, L. Densoviruses for control and genetic manipulation of mosquitoes. In Advances in Virus Research, Vol. 68 361–392 (Academic Press, 2006).

Johnson, R. M. & Rasgon, J. L. Densonucleosis viruses (‘densoviruses’) for mosquito and pathogen control. Curr. Opin. Insect Sci. 28, 90–97 (2018).

Article  Google Scholar 

Grenet, A.-S.G. et al. Les densovirus: une «massive attaque» chez les arthropodes. Virologie 19, 19–31 (2015).

Google Scholar 

Hewson, I. et al. Densovirus associated with sea-star wasting disease and mass mortality. Proc. Natl. Acad. Sci. 111, 17278–17283 (2014).

ADS  Article  CAS  Google Scholar 

Afanasiev, B. N., Galyov, E. E., Buchatsky, L. P. & Kozlov, Y. V. Nucleotide sequence and genornic organization of aedes densonucleosis virus. Virology 185, 323–336 (1991).

Article  CAS  Google Scholar 

Sivaram, A. et al. Isolation and characterization of densonucleosis virus from Aedes aegypti mosquitoes and its distribution in India. Intervirology 52, 1–7 (2009).

Article  CAS  Google Scholar 

Chen, S. et al. Genetic, biochemical, and structural characterization of a new densovirus isolated from a chronically infected Aedesalbopictus C6/36 cell line. Virology 318, 123–133 (2004).

Article  CAS  Google Scholar 

Zhai, Y.-G. et al. Isolation and characterization of the full coding sequence of a novel densovirus from the mosquito Culexpipienspallens. J. Gen. Virol. 89, 195–199 (2008).

Article  CAS  Google Scholar 

Ren, X., Hoiczyk, E. & Rasgon, J. L. Viral Paratransgenesis in the malaria vector Anophelesgambiae. PLoS Pathog. 4, e1000135 (2008).

PubMed Central  Article  CAS  PubMed  Google Scholar 

Jousset, F.-X., Barreau, C., Boublik, Y. & Cornet, M. A Parvo-like virus persistently infecting a C6/36 clone of Aedesalbopictus mosquito cell line and pathogenic for Aedesaegypti larvae. Virus Res. 29, 99–114 (1993).

Article  CAS  Google Scholar 

Afanasiev, B. N. & Carlson, J. O. A new mosquito densovirus from Peru: genomic sequence and in vitro growth characteristics of wild type and hybrid viruses. (2003).

O’Neill, S. L. et al. Insect densoviruses may be widespread in mosquito cell lines. J. Gen. Virol. 76, 2067–2074 (1995).

Article  Google Scholar 

Jousset, F.-X., Baquerizo, E. & Bergoin, M. A new densovirus isolated from the mosquito Culexpipiens (Diptera: Culicidae). Virus Res. 67, 11–16 (2000).

Article  CAS  Google Scholar 

Sangdee, K. & Pattanakitsakul, S. New genetic variation of Aedesalbopictus Densovirus isolated from mosquito C6/36 cell line. Southeast Asian J. Trop. Med. Public Health 43, 12 (2012).

Google Scholar 

Li, J. et al. A novel densovirus isolated from the asian tiger mosquito displays varied pathogenicity depending on its host species. Front. Microbiol. 10, 1549 (2019).

PubMed Central  Article  PubMed  Google Scholar 

Kittayapong, P., Baisley, K. J. & O’Neill, S. L. A mosquito densovirus infecting Aedesaegypti and Aedesalbopictus from Thailand. Am. J. Trop. Med. Hyg. 61, 612–617 (1999).

Article  CAS  Google Scholar 

Barreau, C., Jousset, F. X. & Bergoin, M. Venereal and vertical transmission of the Aedesalbopictus parvovirus in Aedesaegypti mosquitoes. Am. J. Trop. Med. Hyg. 57, 126–131 (1997).

Article  CAS  Google Scholar 

De Valdez, M. R. W., Suchman, E. L., Carlson, J. O. & Black, W. C. A Large Scale Laboratory Cage Trial of Aedes Densonucleosis Virus (AeDNV). J. Med. Entomol. 47, 392–399 (2010).

Article  Google Scholar 

Altinli, M. et al. Sharing cells with Wolbachia: the transovarian vertical transmission of Culexpipiens densovirus. Environ. Microbiol. 21, 3284–3298 (2019).

Article  CAS  Google Scholar 

Wei, W. et al. The pathogenicity of mosquito densovirus (C6/36DNV) and its interaction with dengue virus type II in Aedesalbopictus. Am. J. Trop. Med. Hyg. 75, 1118–1126 (2006).

Article  Google Scholar 

Bouyer, J., Chandre, F., Gilles, J. & Baldet, T. Alternative vector control methods to manage the Zika virus outbreak: more haste, less speed. Lancet Glob. Health 4, e364 (2016).

Article  Google Scholar 

Barreau, C., Jousset, F.-X. & Bergoin, M. Pathogenicity of the Aedesalbopictus parvovirus (AaPV), a denso-like virus, for Aedes aegypti mosquitoes. J. Invertebr. Pathol. 68, 299–309 (1996).

Article  CAS  Google Scholar 

Barreau, C., Jousset, F.-X. & Cornet, M. An efficient and easy method of infection of mosquito larvae from virus-contaminated cell cultures. J. Virol. Methods 49, 153–156 (1994).

Article  CAS  Google Scholar 

Igarashi, A. Isolation of a Singh’s Aedesalbopictus cell clone sensitive to dengue and chikungunya viruses. J. Gen. Virol. 40, 531–544 (1978).

Article  CAS  Google Scholar 

Brackney, D. E. et al. C6/36 Aedesalbopictus cells have a dysfunctional antiviral RNA interference response. PLoS Negl. Trop. Dis. 4, e856 (2010).

PubMed Central  Article  CAS  PubMed  Google Scholar 

Ostfeld, R. S. & Keesing, F. Effects of host diversity on infectious disease. Annu. Rev. Ecol. Evol. Syst. 43, 157–182 (2012).

Article  Google Scholar 

Lambrechts, L., Scott, T. W. & Gubler, D. J. Consequences of the expanding global distribution of aedes albopictus for dengue virus transmission. PLoS Negl. Trop. Dis. 4, e646 (2010).

PubMed Central  Article  PubMed  Google Scholar 

Ledermann, J. P., Suchman, E. L., Black, W. C. & Carlson, J. O. Infection and pathogenicity of the mosquito densoviruses AeDNV, HeDNV, and APeDNV in Aedesaegypti mosquitoes (Diptera: Culicidae). J. Econ. Entomol. 97, 1828–1835 (2004).

Article  Google Scholar 

Hirunkanokpun, S., Carlson, J. O. & Kittayapong, P. Evaluation of mosquito densoviruses for controlling Aedesaegypti (Diptera: Culicidae): variation in efficiency due to virus strain and geographic origin of mosquitoes. Am. J. Trop. Med. Hyg. 78, 784–790 (2008).

Article  CAS  Google Scholar 

Ogoyi, D. O. et al. Linkage and mapping analysis of a non-susceptibility gene to densovirus (nsd-2) in the silkworm, Bombyxmori. Insect Mol. Biol. 12, 117–124 (2003).

Article  CAS  Google Scholar 

Watanabe, H. & Maeda, S. Genetically determined nonsusceptibility of the silkworm, Bombyxmori, to infection with a densonucleosis virus (Densovirus). J. Invertebr. Pathol. 38, 370–373 (1981).

Article  Google Scholar 

Rudolf, V. H. W. & Antonovics, J. Disease transmission by cannibalism: rare event or common occurrence?. Proc. R. Soc. B Biol. Sci. 274, 1205–1210 (2007).

Article  Google Scholar 

Parry, R., Bishop, C., De Hayr, L. & Asgari, S. Density-dependent enhanced replication of a densovirus in Wolbachia-infected Aedes cells is associated with production of piRNAs and higher virus-derived siRNAs. Virology 528, 89–100 (2019).

Article  CAS  Google Scholar 

Rwegoshora, R. T., Baisley, K. J. & Kittayapong, P. Seasonal and spatial variation in natural densovirus infection in Anophelesminimus s.l. in Thailand. Southeast Asian J. Trop. Med. Public Health 31, 7 (2000).

Google Scholar 

Clements, A. N. The biology of mosquitoes: sensory reception and behaviour. Behaviour and aspects of the biology of larvae (1999).

Hajek, A. E. & Shapiro-Ilan, D. I. Ecology of Invertebrate Diseases (Wiley, New York, 2018).

Google Scholar 

Ren, X. & Rasgon, J. L. Potential for the Anophelesgambiae densonucleosis virus to act as an “evolution-proof” biopesticide. J. Virol. 84, 7726–7729 (2010).

PubMed Central  Article  CAS  PubMed  Google Scholar 

Buchatsky, L. P. Densonucleosis of blood sucking mosquitoes. Dis. Aquat. Organ. 6, 145–150 (1989).

Article  Google Scholar 

Brengues, C. et al. Pyrethroid and DDT cross-resistance in Aedesaegypti is correlated with novel mutations in the voltage-gated sodium channel gene. Med. Vet. Entomol. 17, 87–94 (2003).

Article  CAS  Google Scholar 

Boublik, Y., Jousset, F.-X. & Bergoin, M. Complete nucleotide sequence and genomic organization of the Aedesalbopictus parvovirus (AaPV) pathogenic for Aedesaegypti larvae. Virology 200, 752–763 (1994).

Article  CAS  Google Scholar