Comprehensive proteome profiling in Aedes albopictus to decipher Wolbachia-arbovirus interference phenomenon

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Abstract

Background

Aedes albopictus is a vector of arboviruses that cause severe diseases in humans such as Chikungunya, Dengue and Zika fevers. The vector competence of Ae. albopictus varies depending on the mosquito population involved and the virus transmitted. Wolbachia infection status in believed to be among key elements that determine viral transmission efficiency. Little is known about the cellular functions mobilized in Ae. albopictus during co-infection by Wolbachia and a given arbovirus. To decipher this tripartite interaction at the molecular level, we performed a proteome analysis in Ae. albopictus C6/36 cells mono-infected by Wolbachia wAlbB strain or Chikungunya virus (CHIKV), and bi-infected.

Results

We first confirmed significant inhibition of CHIKV by Wolbachia. Using two-dimensional gel electrophoresis followed by nano liquid chromatography coupled with tandem mass spectrometry, we identified 600 unique differentially expressed proteins mostly related to glycolysis, translation and protein metabolism. Wolbachia infection had greater impact on cellular functions than CHIKV infection, inducing either up or down-regulation of proteins associated with metabolic processes such as glycolysis and ATP metabolism, or structural glycoproteins and capsid proteins in the case of bi-infection with CHIKV. CHIKV infection inhibited expression of proteins linked with the processes of transcription, translation, lipid storage and miRNA pathways.

Conclusions

The results of our proteome profiling have provided new insights into the molecular pathways involved in tripartite Ae. albopictus- Wolbachia-CHIKV interaction and may help defining targets for the better implementation of Wolbachia-based strategies for disease transmission control.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-017-3985-y) contains supplementary material, which is available to authorized users.

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Most cited references 29

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The Proteomics Identifications (PRIDE) database and associated tools: status in 2013

Juan Antonio Vizcaíno, Richard Côté, Attila Csordas … (2012)

The PRoteomics IDEntifications (PRIDE, http://www.ebi.ac.uk/pride) database at the European Bioinformatics Institute is one of the most prominent data repositories of mass spectrometry (MS)-based proteomics data. Here, we summarize recent developments in the PRIDE database and related tools. First, we provide up-to-date statistics in data content, splitting the figures by groups of organisms and species, including peptide and protein identifications, and post-translational modifications. We then describe the tools that are part of the PRIDE submission pipeline, especially the recently developed PRIDE Converter 2 (new submission tool) and PRIDE Inspector (visualization and analysis tool). We also give an update about the integration of PRIDE with other MS proteomics resources in the context of the ProteomeXchange consortium. Finally, we briefly review the quality control efforts that are ongoing at present and outline our future plans.

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Critical review of the vector status of Aedes albopictus.

N G Gratz (2004)

The mosquito Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae), originally indigenous to South-east Asia, islands of the Western Pacific and Indian Ocean, has spread during recent decades to Africa, the mid-east, Europe and the Americas (north and south) after extending its range eastwards across Pacific islands during the early 20th century. The majority of introductions are apparently due to transportation of dormant eggs in tyres. Among public health authorities in the newly infested countries and those threatened with the introduction, there has been much concern that Ae. albopictus would lead to serious outbreaks of arbovirus diseases (Ae. albopictus is a competent vector for at least 22 arboviruses), notably dengue (all four serotypes) more commonly transmitted by Aedes (Stegomyia) aegypti (L.). Results of many laboratory studies have shown that many arboviruses are readily transmitted by Ae. albopictus to laboratory animals and birds, and have frequently been isolated from wild-caught mosquitoes of this species, particularly in the Americas. As Ae. albopictus continues to spread, displacing Ae. aegypti in some areas, and is anthropophilic throughout its range, it is important to review the literature and attempt to predict whether the medical risks are as great as have been expressed in scientific journals and the popular press. Examination of the extensive literature indicates that Ae. albopictus probably serves as a maintenance vector of dengue in rural areas of dengue-endemic countries of South-east Asia and Pacific islands. Also Ae. albopictus transmits dog heartworm Dirofilaria immitis (Leidy) (Spirurida: Onchocercidae) in South-east Asia, south-eastern U.S.A. and both D. immitis and Dirofilaria repens (Raillet & Henry) in Italy. Despite the frequent isolation of dengue viruses from wild-caught mosquitoes, there is no evidence that Ae. albopictus is an important urban vector of dengue, except in a limited number of countries where Ae. aegypti is absent, i.e. parts of China, the Seychelles, historically in Japan and most recently in Hawaii. Further research is needed on the dynamics of the interaction between Ae. albopictus and other Stegomyia species. Surveillance must also be maintained on the vectorial role of Ae. albopictus in countries endemic for dengue and other arboviruses (e.g. Chikungunya, EEE, Ross River, WNV, LaCrosse and other California group viruses), for which it would be competent and ecologically suited to serve as a bridge vector.

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Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus.

Mark Q Benedict, Rebecca Levine, William A. Hawley … (2007)

Aedes albopictus, commonly known as the Asian tiger mosquito, is currently the most invasive mosquito in the world. It is of medical importance due to its aggressive daytime human-biting behavior and ability to vector many viruses, including dengue, LaCrosse, and West Nile. Invasions into new areas of its potential range are often initiated through the transportation of eggs via the international trade in used tires. We use a genetic algorithm, Genetic Algorithm for Rule Set Production (GARP), to determine the ecological niche of Ae. albopictus and predict a global ecological risk map for the continued spread of the species. We combine this analysis with risk due to importation of tires from infested countries and their proximity to countries that have already been invaded to develop a list of countries most at risk for future introductions and establishments. Methods used here have potential for predicting risks of future invasions of vectors or pathogens.

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Author and article information

Contributors

Patrick Mavingui: patrick.mavingui@cnrs.fr

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 18 August 2017

Publication date PMC-release: 18 August 2017

Publication date Collection: 2017

Volume: 18

Electronic Location Identifier: 635

Affiliations

[1 ]ISNI 0000 0001 2172 4233, GRID grid.25697.3f, , Université de Lyon, ; Lyon, France

[2 ]ISNI 0000 0001 2150 7757, GRID grid.7849.2, , Université Lyon 1, ; Villeurbanne, France

[3 ]ISNI 0000 0001 2112 9282, GRID grid.4444.0, , CNRS, UMR5557, Ecologie Microbienne, ; Villeurbanne, France

[4 ]INRA, UMR1418, Villeurbanne, France

[5 ]ISNI 0000 0001 2112 9282, GRID grid.4444.0, , Laboratoire Mixte UMR 5240, Plateforme de Protéomique, CNRS, ; Lyon, France

[6 ]ISNI 0000 0001 2106 639X, GRID grid.412041.2, Centre de Génomique Fonctionnelle, Plateforme Protéome, , Université Bordeaux, ; F-33000 Bordeaux, France

[7 ]CNRS 9192, INSERM U1187, IRD 249, Unité Mixte Processus Infectieux en Milieu Insulaire Tropical (PIMIT). Plateforme Technologique CYROI, Université de La Réunion, 2 rue Maxime Rivière, 97490 Sainte Clotilde, île de La Réunion France

Article

Publisher ID: 3985

DOI: 10.1186/s12864-017-3985-y

PMC ID: 5563009

PubMed ID: 28821226

SO-VID: 0eca664d-218e-4d28-8ef5-128a125da898

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 5 April 2017

Date accepted : 1 August 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;

Funded by: ERA-NET BiodivERsA

Award ID: ANR-13-EBID-0007-01, FWF I-1437, DFG KL 2087/6-1

Award Recipient : Patrick Mavingui

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: aedes albopictus,wolbachia,viral inhibition,proteome,glycolysis,metabolism,mirna

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ScienceOpen disciplines: Genetics

Keywords: aedes albopictus, wolbachia, viral inhibition, proteome, glycolysis, metabolism, mirna

Comprehensive proteome profiling in Aedes albopictus to decipher Wolbachia-arbovirus interference phenomenon

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Zika Virus

Most cited references 29

The Proteomics Identifications (PRIDE) database and associated tools: status in 2013

Critical review of the vector status of Aedes albopictus.

Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus.

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