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      Infection by chikungunya virus modulates the expression of several proteins in Aedes aegypti salivary glands

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          Abstract

          Background

          Arthropod-borne viral infections cause several emerging and resurging infectious diseases. Among the diseases caused by arboviruses, chikungunya is responsible for a high level of severe human disease worldwide. The salivary glands of mosquitoes are the last barrier before pathogen transmission.

          Methods

          We undertook a proteomic approach to characterize the key virus/vector interactions and host protein modifications that occur in the salivary glands that could be responsible for viral transmission by using quantitative two-dimensional electrophoresis.

          Results

          We defined the protein modulations in the salivary glands of Aedes aegypti that were triggered 3 and 5 days after an oral infection (3 and 5 DPI) with chikungunya virus (CHIKV). Gel profile comparisons showed that CHIKV at 3 DPI modulated the level of 13 proteins, and at 5 DPI 20 proteins. The amount of 10 putatively secreted proteins was regulated at both time points. These proteins were implicated in blood-feeding or in immunity, but many have no known function. CHIKV also modulated the quantity of proteins involved in several metabolic pathways and in cell signalling.

          Conclusion

          Our study constitutes the first analysis of the protein response of Aedes aegypti salivary glands infected with CHIKV. We found that the differentially regulated proteins in response to viral infection include structural proteins and enzymes for several metabolic pathways. Some may favour virus survival, replication and transmission, suggesting a subversion of the insect cell metabolism by arboviruses. For example, proteins involved in blood-feeding such as the short D7, an adenosine deaminase and inosine-uridine preferring nucleoside hydrolase, may favour virus transmission by exerting an increased anti-inflammatory effect. This would allow the vector to bite without the bite being detected. Other proteins, like the anti-freeze protein, may support vector protection.

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          Two Chikungunya Isolates from the Outbreak of La Reunion (Indian Ocean) Exhibit Different Patterns of Infection in the Mosquito, Aedes albopictus

          Marie Vazeille, Sara Moutailler, Daniel Coudrier … (2007)
          Background A Chikungunya (CHIK) outbreak hit La Réunion Island in 2005–2006. The implicated vector was Aedes albopictus. Here, we present the first study on the susceptibility of Ae. albopictus populations to sympatric CHIKV isolates from La Réunion Island and compare it to other virus/vector combinations. Methodology and Findings We orally infected 8 Ae. albopictus collections from La Réunion and 3 from Mayotte collected in March 2006 with two Chikungunya virus (CHIKV) from La Réunion: (i) strain 05.115 collected in June 2005 with an Alanine at the position 226 of the glycoprotein E1 and (ii) strain 06.21 collected in November 2005 with a substitution A226V. Two other CHIKV isolates and four additional mosquito strains/species were also tested. The viral titer of the infectious blood-meal was 107 plaque forming units (pfu)/mL. Dissemination rates were assessed by immunofluorescent staining on head squashes of surviving females 14 days after infection. Rates were at least two times higher with CHIKV 06.21 compared to CHIKV 05.115. In addition, 10 individuals were analyzed every day by quantitative RT-PCR. Viral RNA was quantified on (i) whole females and (ii) midguts and salivary glands of infected females. When comparing profiles, CHIKV 06.21 produced nearly 2 log more viral RNA copies than CHIKV 05.115. Furthermore, females infected with CHIKV 05.115 could be divided in two categories: weakly susceptible or strongly susceptible, comparable to those infected by CHIKV 06.21. Histological analysis detected the presence of CHIKV in salivary glands two days after infection. In addition, Ae. albopictus from La Réunion was as efficient vector as Ae. aegypti and Ae. albopictus from Vietnam when infected with the CHIKV 06.21. Conclusions Our findings support the hypothesis that the CHIK outbreak in La Réunion Island was due to a highly competent vector Ae. albopictus which allowed an efficient replication and dissemination of CHIKV 06.21.
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            Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives.

            Jose Ribeiro, Ivo Francischetti (2003)
            This review addresses the problems insects and ticks face to feed on blood and the solutions these invertebrates engender to overcome these obstacles, including a sophisticated salivary cocktail of potent pharmacologic compounds. Recent advances in transcriptome and proteome research allow an unprecedented insight into the complexity of these compounds, indicating that their molecular diversity as well as the diversity of their targets is still larger than previously thought.
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              Chikungunya Virus and Aedes Mosquitoes: Saliva Is Infectious as soon as Two Days after Oral Infection

              Mathieu Dubrulle, Laurence Mousson, Sara Moutailler … (2009)
              Background Aedes aegypti and Aedes albopictus are potential vectors of chikungunya virus (CHIKV). The recent CHIKV outbreaks were caused by a new variant characterized by a mutation in the E1 glycoprotein gene (E1-226V) which has favored a better transmissibility by Ae. albopictus. As Ae. albopictus tends to replace Ae. aegypti in many regions, one question remained: is Ae. albopictus as efficient as Ae. aegypti to transmit the variant E1-226V of CHIKV? Methodology and Findings We infected orally both species with the variant E1-226V and estimated the infection, the viral dissemination, and the transmission rate by real time RT-PCR. Additionally, we used an in vitro assay to determine the amount of virus delivered by mosquitoes in their saliva. We found that Ae. aegypti as well as Ae. albopictus ensured a high replication of the virus which underwent an efficient dissemination as detectable in the salivary glands at day 2 post-infection (pi). Infectious CHIKV particles were delivered by salivary glands from day 2 with a maximum at day 6 pi for Ae. albopictus (103.3 PFU) and day 7 pi for Ae. aegypti (102.5 PFU). Conclusions Ae. albopictus is slightly more efficient than Ae. aegypti to transmit the variant E1-226V of CHIKV. These results will help to design an efficient vector control to limit transmission as soon as the first human cases are diagnosed.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Parasit Vectors
                Journal ID (iso-abbrev): Parasit Vectors
                Title: Parasites & Vectors
                Publisher: BioMed Central
                ISSN (Electronic): 1756-3305
                Publication date Collection: 2012
                Publication date (Electronic): 15 November 2012
                Volume: 5
                Page: 264
                Affiliations
                [1 ]Unité de Génétique Moléculaire des Bunyavirus, 25 rue du Dr Roux, 75724, Paris cedex 15
                [2 ]Unité de Biochimie et de Biologie Moléculaire des Insectes, Institut Pasteur, 28 rue du Dr Roux, 75724 cedex 15, Paris, France
                [3 ]Plate-forme protéomique PF5, Institut Pasteur, 28 rue du Dr Roux, 75724 cedex 15, Paris, France
                [4 ]present address: Unité Interactions Moléculaires Flavivirus-Hôtes, Institut Pasteur, 25, rue du Dr Roux, 75724 cedex 15, Paris, France
                Article
                Publisher ID: 1756-3305-5-264
                DOI: 10.1186/1756-3305-5-264
                PMC ID: 3549772
                PubMed ID: 23153178
                SO-VID: ac44c856-d3ab-462a-bc0b-bb19d33919b9
                Copyright © Copyright ©2012 Tchankouo-Nguetcheu et al.; licensee BioMed Central Ltd.
                License:

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Date received : 29 August 2012
                Date accepted : 12 November 2012
                Categories
                Subject: Research

                ScienceOpen disciplines: Parasitology
                Keywords: mosquito salivary gland,aedes aegypti,two-dimensional gel electrophoresis,mass spectrometry,chikungunya virus,proteomics
                Data availability:
                ScienceOpen disciplines: Parasitology
                Keywords: mosquito salivary gland, aedes aegypti, two-dimensional gel electrophoresis, mass spectrometry, chikungunya virus, proteomics

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