Variation in Vector Competence for Dengue Viruses Does Not Depend on Mosquito Midgut Binding Affinity

Jonathan Cox,Rebeca Rico-Hesse,Heidi E Brown,A Desiree Labeaud

doi:10.1371/journal.pntd.0001172

Jonathan Cox, Rebeca Rico-Hesse + Show 2 more

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https://doi.org/10.1371/journal.pntd.0001172

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Abstract

BackgroundDengue virus genotypes of Southeast Asian origin have been associated with higher virulence and transmission compared to other genotypes of serotype 2 (DEN-2). We tested the hypothesis that genetic differences in dengue viruses may result in differential binding to the midgut of the primary vector, Aedes aegypti, resulting in increased transmission or vectorial capacity.Methodology/Principal FindingTwo strains of each of the four DEN-2 genotypes (Southeast Asian, American, Indian, and West African) were tested to determine their binding affinity for mosquito midguts from two distinct populations (Tapachula, Chiapas, Mexico and McAllen, Texas, USA). Our previous studies demonstrated that Southeast Asian viruses disseminated up to 65-fold more rapidly in Ae. aegypti from Texas and were therefore more likely to be transmitted to humans. Results shown here demonstrate that viruses from all four genotypes bind to midguts at the same rate, in a titer-dependent manner. In addition, we show population differences when comparing binding affinity for DEN-2 between the Tapachula and McAllen mosquito colonies.ConclusionsIf midgut binding potential is the same for all DEN-2 viruses, then viral replication differences in these tissues and throughout the mosquito can thus probably explain the significant differences in dissemination and vector competence. These conclusions differ from the established paradigms to explain mosquito barriers to infection, dissemination, and transmission.

Highlights

Dengue viruses, which cause millions of cases of dengue fever (DF) and dengue hemorrhagic fever (DHF) each year in over 100 countries, are transmitted by two species of mosquitoes, Aedes aegypti and Aedes albopictus
If midgut binding potential is the same for all DEN-2 viruses, viral replication differences in these tissues and throughout the mosquito can probably explain the significant differences in dissemination and vector competence
In contrast with most studies of vector competence, we have focused on comparing infection, replication, and transmission rates of dengue viruses in field-collected mosquitoes, with generations from eggs not higher than F4, and by comparing many different, low-passage virus strains of the same serotype (DEN-2)

Summary

Introduction

Dengue viruses, which cause millions of cases of dengue fever (DF) and dengue hemorrhagic fever (DHF) each year in over 100 countries, are transmitted by two species of mosquitoes, Aedes aegypti and Aedes albopictus. These vectors directly determine the rates of transmission of dengue viruses to humans, and they determine the global spread and occurrence of disease. Specific factors, including mosquito and viral genetics and the environment, that govern Ae. aegypti transmission of dengue viruses (members of the Flavivirus family), were reviewed recently [3]; it is important to point out that other flaviviruses, such as yellow fever and West Nile differ in their interactions with this mosquito. We tested the hypothesis that genetic differences in dengue viruses may result in differential binding to the midgut of the primary vector, Aedes aegypti, resulting in increased transmission or vectorial capacity

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