Dengue Virus Infection of Aedes aegypti Alters Extracellular Vesicle Protein Cargo to Enhance Virus Transmission

Gold, Alexander S.; Feitosa-Suntheimer, Fabiana; Araujo, Ricardo Vieira; Hekman, Ryan; Asad, Sultan; Londoño-Rentería, Berlin; Emili, Andrew; Colpitts, Tonya M.

doi:10.3390/ijms21186609

Cited by 11 publications

(7 citation statements)

References 57 publications

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“…The calmodulin gene AAEL012326 is overexpressed in a strain susceptible to dengue compared to one refractory to dengue ( Chauhan et al 2012 ) and produces a protein product that is found in extracellular vesicles produced by Ae. aegypti cells infected by dengue, but not uninfected control cells ( Gold et al 2020 ). The putative 60S ribosomal protein gene AAEL011587 is upregulated in response to chikungunya infection and to chikungunya and dengue coinfection ( Shrinet et al 2017 ).…”

Section: Resultsmentioning

confidence: 99%

Strong Positive Selection inAedes aegyptiand the Rapid Evolution of Insecticide Resistance

Love

Sikder

Vivero

et al. 2023

Molecular Biology and Evolution

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Aedes aegypti vectors the pathogens that cause dengue, yellow fever, Zika virus, and chikungunya, and is a serious threat to public health in tropical regions. Decades of work has illuminated many aspects of Ae. aegypti’s biology and global population structure, and has identified insecticide resistance genes; however, the size and repetitive nature of the Ae. aegypti genome have limited our ability to detect positive selection in this mosquito. Combining new whole genome sequences from Colombia with publicly available data from Africa and the Americas, we identify multiple strong candidate selective sweeps in Ae. aegypti, many of which overlap genes linked to or implicated in insecticide resistance. We examine the voltage-gated sodium channel gene in three American cohorts, and find evidence for successive selective sweeps in Colombia. The most recent sweep encompasses an intermediate-frequency haplotype containing four candidate insecticide resistance mutations that are in near-perfect linkage disequilibrium with one another in the Colombian sample. We hypothesize that this haplotype may continue to rapidly increase in frequency and perhaps spread geographically in the coming years. These results extend our knowledge of how insecticide resistance has evolved in this species, and add to a growing body of evidence suggesting Ae. aegypti has an extensive genomic capacity to rapidly adapt to insecticide-based vector control.

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Section: Resultsmentioning

confidence: 99%

Strong Positive Selection inAedes aegyptiand the Rapid Evolution of Insecticide Resistance

Love

Sikder

Vivero

et al. 2023

Molecular Biology and Evolution

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“…aegypti are AAEL001951-PA and actin (Q6QNY2_AEDAE and Q4JQ54_CULPP), with 4.9-and 9.5-fold changes, respectively. All phagocytic activities in mosquitoes involve restructuring the actin cytoskeleton [26,51]. Meanwhile, mosquito cytoplasmic actin has many biological functions, including cell signalling and immunity [52].…”

Section: Discussionmentioning

confidence: 99%

Evaluation of Total Female and Male Aedes aegypti Proteomes Reveals Significant Predictive Protein–Protein Interactions, Functional Ontologies, and Differentially Abundant Proteins

Shettima

Joseph

Ishak

et al. 2021

Insects

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Aedes aegypti is a significant vector for many tropical and subtropical flavivirus diseases. Only the female mosquito transmits pathogens, while the male plays a vital role in mating and species continuity. This study explored the total proteomes of females and males based on the physiological and genetic differences of female and male mosquitoes. Protein extracts from mosquitoes were analysed using LC–ESI–MS/MS for protein identification, protein interaction network analysis, functional ontology enrichment, and differential protein abundance analyses. Protein identification revealed 422 and 682 proteins exclusive to males and females, respectively, with 608 common proteins found in both sexes. The most significant PPIs (<1.0 × 10−16) were for common proteins, followed by proteins exclusive to females (<1.0 × 10−16) and males (1.58 × 10−12). Significant functional enrichments were observed in the biological process, molecular function, and cellular component for the male and female proteins. The abundance of the proteins differed, with one protein showing an increase (elongation factor 1 α, EF1α) and two showing reductions (actin family) in females versus males. Overall, the study verified the total proteomes differences between male and female Ae. aegypti based on protein identification and interactions, functional ontologies, and differentially abundant proteins. Some of the identified proteins merit further investigation to elucidate their roles in blocking viral transmission.

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“…EVs have been identified and characterized in many arthropod species, including ticks such as Haemaphysalis longicornis [ 22 ], Ixodes scapularis [ 23 ] and Dermacentor andersoni [ 23 ]. They have also been found in Diptera such as Drosophila [ 24 ] and Aedes aegypti [ 25 ], Ornithoctonus hainana spider [ 26 ], Homarus americanus lobster [ 27 ] and Morpho butterfly [ 28 ]. Tick saliva EVs may facilitate pathogen transmission from arthropods to mammals and participate in tick-host-pathogen relationships [ 22 , 23 ].…”

Section: Introductionmentioning

confidence: 99%

Proteomic analysis of extracellular vesicles from tick hemolymph and uptake of extracellular vesicles by salivary glands and ovary cells

Wang

Sun

et al. 2023

Parasites Vectors

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Background Extracellular vesicles (EVs) are a heterogeneous group of cell-derived membranous structures that are important mediators of intercellular communication. Arthropods transport nutrients, signaling molecules, waste and immune factors to all areas of the body via the hemolymph. Little is known about tick hemolymph EVs. Methods Hemolymph was collected from partially fed Rhipicephalus haemaphysaloides and Hyalomma asiaticum ticks by making an incision with a sterile scalpel in the middle (between the femur and metatarsus) of the first pair of legs, which is known as leg amputation. EVs were isolated from hemolymph by differential centrifugation and characterized by transmission electron microscopy (TEM) and nanoparticle tracking analysis (NTA). Proteins extracted from the hemolymph EVs were analyzed by 4D label-free proteomics. The EVs were also examined by western blot and immuno-electron microscopy analysis. Intracellular incorporation of PHK26-labeled EVs was tested by adding labeled EVs to tick salivary glands and ovaries, followed by fluorescence microscopy. Results In this study, 149 and 273 proteins were identified by 4D label-free proteomics in R. haemaphysaloides and H. asiaticum hemolymph EVs, respectively. TEM and NTA revealed that the sizes of the hemolymph EVs from R. haemaphysaloides and H. asiaticum were 133 and 138 nm, respectively. Kyoto Encyclopedia of Genes and Genomes and Gene Ontology enrichment analyses of identified proteins revealed pathways related to binding, catalytic and transporter activity, translation, transport and catabolism, signal transduction and cellular community. The key EV marker proteins RhCD9, RhTSG101, Rh14-3-3 and RhGAPDH were identified using proteomics and western blot. The presence of RhFerritin-2 in tick hemolymph EVs was confirmed by western blot and immuno-electron microscopy. We demonstrated that PKH26-labeled hemolymph EVs are internalized by tick salivary glands and ovary cells in vitro. Conclusions The results suggest that tick EVs are secreted into, and circulated by, the hemolymph. EVs may play roles in the regulation of tick development, metabolism and reproduction. Graphical Abstract

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Dengue Virus Infection of Aedes aegypti Alters Extracellular Vesicle Protein Cargo to Enhance Virus Transmission

Cited by 11 publications

References 57 publications

Strong Positive Selection inAedes aegyptiand the Rapid Evolution of Insecticide Resistance

Strong Positive Selection inAedes aegyptiand the Rapid Evolution of Insecticide Resistance

Evaluation of Total Female and Male Aedes aegypti Proteomes Reveals Significant Predictive Protein–Protein Interactions, Functional Ontologies, and Differentially Abundant Proteins

Proteomic analysis of extracellular vesicles from tick hemolymph and uptake of extracellular vesicles by salivary glands and ovary cells

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