Superior infectivity for mosquito vectors contributes to competitive displacement among strains of dengue virus

Hanley, Kathryn A.; Nelson, J. Arly; Schirtzinger, Erin E.; Whitehead, Stephen S.; Hanson, Christopher T.

doi:10.1186/1472-6785-8-1

Cited by 99 publications

(94 citation statements)

References 87 publications

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“…By comparing the ability of three DENV-3 isolates of a native lineage and three DENV-3 isolates of an invasive lineage to be transmitted by A. aegypti, Hanley et al (19) showed that a clade replacement event in Sri Lanka during the 1980s was associated with enhanced mosquito transmission potential for the invasive lineage. Enhanced transmissibility was associated with a higher body titer and an increased proportion of A. aegypti females with a disseminated infection (19).…”

Section: Discussionmentioning

confidence: 99%

“…Analyses of DENV gene sequence data have shown that clade replacement events are sometimes associated with signals of positive natural selection, such as an increase in the rate of nonsynonymous substitutions (7), but not always (26,47). Some phylogenetic studies have concluded that major clade replacements were primarily due to stochastic events (31,47), whereas others found potentially causal differences in viral fitness between lineages, such as a higher viremia level in the human host (43) or enhanced infectivity to mosquito vectors (3,5,19).…”

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confidence: 99%

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Dengue-1 Virus Clade Replacement in Thailand Associated with Enhanced Mosquito Transmission

Lambrechts

Fansiri

Pongsiri

et al. 2012

J Virol

116

109

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Dengue viruses (DENV) are characterized by extensive genetic diversity and can be organized in multiple, genetically distinct lineages that arise and die out on a regular basis in regions where dengue is endemic. A fundamental question for understanding DENV evolution is the relative extent to which stochastic processes (genetic drift) and natural selection acting on fitness differences among lineages contribute to lineage diversity and turnover. Here, we used a set of recently collected and archived lowpassage DENV-1 isolates from Thailand to examine the role of mosquito vector-virus interactions in DENV evolution. By comparing the ability of 23 viruses isolated on different dates between 1985 and 2009 to be transmitted by a present-day Aedes aegypti population from Thailand, we found that a major clade replacement event in the mid-1990s was associated with virus isolates exhibiting increased titers in the vector's hemocoel, which is predicted to result in a higher probability of transmission. This finding is consistent with the hypothesis that selection for enhanced transmission by mosquitoes is a possible mechanism underlying major DENV clade replacement events. There was significant variation in transmission potential among isolates within each clade, indicating that in addition to vector-driven selection, other evolutionary forces act to maintain viral genetic diversity. We conclude that occasional adaptive processes involving the mosquito vector can drive major DENV lineage replacement events. W orldwide, dengue viruses (DENV) are the most important mosquito-borne viral pathogens of humans. The four antigenically distinct DENV serotypes (DENV-1 to -4) cause a broad spectrum of clinical manifestations. An estimated 50 million people experience dengue illness each year, approximately 500,000 of which are associated with severe, life-threatening disease (18). In addition, a significant portion of infections can be inapparent and thus go undetected by surveillance programs (15). Despite the large disease burden imposed by dengue on the human population, there is currently no commercially available DENV vaccine or antiviral therapy (46). In regions where dengue is endemic and multiple serotypes cocirculate, DENV epidemiological dynamics are characterized by complex oscillations in incidence and serotype prevalence (6,32,43). A variety of ecological (10, 24) and immunological factors (1, 36) are thought to govern these complex spatiotemporal dynamics. There is also compelling evidence for the influence of virological factors in disease incidence and severity (reviewed in reference 37). DENV are single-stranded, positive-sense RNA viruses of the genus Flavivirus (family Flaviviridae) with extensive genetic diversity (21). Each serotype can be divided into large, genetically diverse phylogenetic clusters, which, in turn, consist of multiple, distinct lineages (22). Here, we use the terms clade and lineage interchangeably. In the last 2 decades, in-depth phylogenetic analyses have significantly improved understandi...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Dengue-1 Virus Clade Replacement in Thailand Associated with Enhanced Mosquito Transmission

Lambrechts

Fansiri

Pongsiri

et al. 2012

J Virol

116

109

View full text Add to dashboard Cite

show abstract

“…These cases of coinfection might be related to coinfections in the mosquito vector; however, there are also few reports about mosquito coinfections, and only a few studies have demonstrated the simultaneous existence of natural serotype 2 and 3 infections in Aedes populations from Asia and America [23,24]. Additionally, the presence of intra-host competition in the vector, which may favor the replication of some viral variants over others, has been reported for other infection models, either between two serotypes of the same virus [24] or between strains of the same serotype [25], thereby favoring the transmission of one of the variants. Similar behaviors have been reported for DENV and chikungunya virus coinfections, in which the percentages of infection spread were better for the Chikungunya virus [26].…”

Section: Introductionmentioning

confidence: 99%

Differential replication of dengue virus serotypes 2 and 3 in coinfections of C6/36 cells and Aedes aegypti mosquitoes

Quintero-Gil

Ospina

Osorio-Benitez

et al. 2014

J Infect Dev Ctries

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Introduction: Different dengue virus (DENV) serotypes have been associated with greater epidemic potential. In turn, the increased frequency in cases of severe forms of dengue has been associated with the cocirculation of several serotypes. Because Colombia is a country with an endemic presence of all four DENV serotypes, the aim of this study was to evaluate the in vivo and in vitro replication of the DENV-2 and DENV-3 strains under individual infection and coinfection conditions. Methodology: C6/36HT cells were infected with the two strains individually or simultaneously (coinfection). Replication capacity was evaluated by RT-qPCR, and the effects on cell viability were assessed with an MTT (3-(4, 5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) assay. Additionally, Aedes aegypti mosquitoes were artificially fed the two strains of each serotype individually or simultaneously. The viral genomes were quantified by RT-qPCR and the survival of the infected mosquitoes was compared to that of uninfected controls. Results: In single infections, three strains significantly affected C6/36HT cell viability, but no significant differences were found in the replication capacities of the strains of the same serotype. In the in vivo infections, mosquito survival was not affected, and no significant differences in replication between strains of the same serotype were found. Finally, in coinfections, serotype 2 replicated with a thousandfold greater efficiency than serotype 3 did both in vitro and in vivo. Conclusions: Due to the cocirculation of serotypes in endemic regions, further studies of coinfections in a natural environment would further an understanding of the transmission dynamics that affect DENV infection epidemiology.

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“…This finding contrasts with other studies of DENV lineage invasions that showed such an advantage. 36,51,58 Notably, although other lineage/genotype replacement events associated with increased disease severity involved a period of lineage/genotype cocirculation, the southeast Asian/American lineage II viruses from our study were introduced into Loreto in the absence of any DENV-2 competitors. 59,60 It is clear that both host and viral factors can play a role in determining dengue disease severity.…”

Section: Denv-2 Lineage II Peru Outbreakmentioning

confidence: 99%

“…aegypti of the National Institutes of Health colony strain were fed for 20 minutes on blood meals composed of 2 mL washed rabbit red blood cells (Hemostat, Dixon, CA) in 10% sucrose combined with 1 mL virus offered in water-jacketed membrane feeders (Lillie Glass, Smyrna, GA) covered with a parafilm seal. 51 Virus titer in the blood meals ranged from 5.48 to 6.48 log 10 FFUs/mL. Engorged mosquitoes were separated, incubated at 28 C and 80% relative humidity on a 12-hour:12-hour light:dark cycle with ad lib access to 10% sucrose solution for 14 days, and then, frozen at −20 C overnight.…”

Section: Denv-2 Lineage II Peru Outbreakmentioning

confidence: 99%

Lineage II of Southeast Asian/American DENV-2 is Associated with a Severe Dengue Outbreak in the Peruvian Amazon

Williams¹,

Mayer²,

Johnson³

et al. 2014

The American Society of Tropical Medicine and Hygiene

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Abstract. During 2010 and 2011, the Loreto region of Peru experienced a dengue outbreak of unprecedented magnitude and severity for the region. This outbreak coincided with the reappearance of dengue virus-2 (DENV-2) in Loreto after almost 8 years. Whole-genome sequence indicated that DENV-2 from the outbreak belonged to lineage II of the southeast Asian/American genotype and was most closely related to viruses circulating in Brazil during 2007 and 2008, whereas DENV-2 previously circulating in Loreto grouped with lineage I (DENV-2 strains circulating in South America since 1990). One amino acid substitution (NS5 A811V) in the 2010 and 2011 isolates resulted from positive selection. However, the 2010 and 2011 DENV-2 did not replicate to higher titers in monocyte-derived dendritic cells and did not infect or disseminate in a higher proportion of Aedes aegypti than DENV-2 isolates previously circulating in Loreto. These results suggest that factors other than enhanced viral replication played a role in the severity of this outbreak.

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Superior infectivity for mosquito vectors contributes to competitive displacement among strains of dengue virus

Cited by 99 publications

References 87 publications

Dengue-1 Virus Clade Replacement in Thailand Associated with Enhanced Mosquito Transmission

Dengue-1 Virus Clade Replacement in Thailand Associated with Enhanced Mosquito Transmission

Differential replication of dengue virus serotypes 2 and 3 in coinfections of C6/36 cells and Aedes aegypti mosquitoes

Lineage II of Southeast Asian/American DENV-2 is Associated with a Severe Dengue Outbreak in the Peruvian Amazon

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