Wolbachia infections in Anopheles gambiae cells: transcriptomic characterization of a novel host-symbiont interaction.

The endosymbiotic bacterium Wolbachia is being investigated as a potential control agent in several important vector insect species. Recent studies have shown that Wolbachia can protect the insect host against a wide variety of pathogens, resulting in reduced transmission of parasites and viruses. I...

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Autores principales:	Grant L Hughes, Xiaoxia Ren, Jose L Ramirez, Joyce M Sakamoto, Jason A Bailey, Anne E Jedlicka, Jason L Rasgon
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2011
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/c199b1860f52473c96012ad1e128f152
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spelling	oai:doaj.org-article:c199b1860f52473c96012ad1e128f1522021-11-18T06:03:36ZWolbachia infections in Anopheles gambiae cells: transcriptomic characterization of a novel host-symbiont interaction.1553-73661553-737410.1371/journal.ppat.1001296https://doaj.org/article/c199b1860f52473c96012ad1e128f1522011-02-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21379333/pdf/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374The endosymbiotic bacterium Wolbachia is being investigated as a potential control agent in several important vector insect species. Recent studies have shown that Wolbachia can protect the insect host against a wide variety of pathogens, resulting in reduced transmission of parasites and viruses. It has been proposed that compromised vector competence of Wolbachia-infected insects is due to up-regulation of the host innate immune system or metabolic competition. Anopheles mosquitoes, which transmit human malaria parasites, have never been found to harbor Wolbachia in nature. While transient somatic infections can be established in Anopheles, no stable artificially-transinfected Anopheles line has been developed despite numerous attempts. However, cultured Anopheles cells can be stably infected with multiple Wolbachia strains such as wAlbB from Aedes albopictus, wRi from Drosophila simulans and wMelPop from Drosophila melanogaster. Infected cell lines provide an amenable system to investigate Wolbachia-Anopheles interactions in the absence of an infected mosquito strain. We used Affymetrix GeneChip microarrays to investigate the effect of wAlbB and wRi infection on the transcriptome of cultured Anopheles Sua5B cells, and for a subset of genes used quantitative PCR to validate results in somatically-infected Anopheles mosquitoes. Wolbachia infection had a dramatic strain-specific effect on gene expression in this cell line, with almost 700 genes in total regulated representing a diverse array of functional classes. Very strikingly, infection resulted in a significant down-regulation of many immune, stress and detoxification-related transcripts. This is in stark contrast to the induction of immune genes observed in other insect hosts. We also identified genes that may be potentially involved in Wolbachia-induced reproductive and pathogenic phenotypes. Somatically-infected mosquitoes had similar responses to cultured cells. The data show that Wolbachia has a profound and unique effect on Anopheles gene expression in cultured cells, and has important implications for mechanistic understanding of Wolbachia-induced phenotypes and potential novel strategies to control malaria.Grant L HughesXiaoxia RenJose L RamirezJoyce M SakamotoJason A BaileyAnne E JedlickaJason L RasgonPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 7, Iss 2, p e1001296 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Grant L Hughes Xiaoxia Ren Jose L Ramirez Joyce M Sakamoto Jason A Bailey Anne E Jedlicka Jason L Rasgon Wolbachia infections in Anopheles gambiae cells: transcriptomic characterization of a novel host-symbiont interaction.
description	The endosymbiotic bacterium Wolbachia is being investigated as a potential control agent in several important vector insect species. Recent studies have shown that Wolbachia can protect the insect host against a wide variety of pathogens, resulting in reduced transmission of parasites and viruses. It has been proposed that compromised vector competence of Wolbachia-infected insects is due to up-regulation of the host innate immune system or metabolic competition. Anopheles mosquitoes, which transmit human malaria parasites, have never been found to harbor Wolbachia in nature. While transient somatic infections can be established in Anopheles, no stable artificially-transinfected Anopheles line has been developed despite numerous attempts. However, cultured Anopheles cells can be stably infected with multiple Wolbachia strains such as wAlbB from Aedes albopictus, wRi from Drosophila simulans and wMelPop from Drosophila melanogaster. Infected cell lines provide an amenable system to investigate Wolbachia-Anopheles interactions in the absence of an infected mosquito strain. We used Affymetrix GeneChip microarrays to investigate the effect of wAlbB and wRi infection on the transcriptome of cultured Anopheles Sua5B cells, and for a subset of genes used quantitative PCR to validate results in somatically-infected Anopheles mosquitoes. Wolbachia infection had a dramatic strain-specific effect on gene expression in this cell line, with almost 700 genes in total regulated representing a diverse array of functional classes. Very strikingly, infection resulted in a significant down-regulation of many immune, stress and detoxification-related transcripts. This is in stark contrast to the induction of immune genes observed in other insect hosts. We also identified genes that may be potentially involved in Wolbachia-induced reproductive and pathogenic phenotypes. Somatically-infected mosquitoes had similar responses to cultured cells. The data show that Wolbachia has a profound and unique effect on Anopheles gene expression in cultured cells, and has important implications for mechanistic understanding of Wolbachia-induced phenotypes and potential novel strategies to control malaria.
format	article
author	Grant L Hughes Xiaoxia Ren Jose L Ramirez Joyce M Sakamoto Jason A Bailey Anne E Jedlicka Jason L Rasgon
author_facet	Grant L Hughes Xiaoxia Ren Jose L Ramirez Joyce M Sakamoto Jason A Bailey Anne E Jedlicka Jason L Rasgon
author_sort	Grant L Hughes
title	Wolbachia infections in Anopheles gambiae cells: transcriptomic characterization of a novel host-symbiont interaction.
title_short	Wolbachia infections in Anopheles gambiae cells: transcriptomic characterization of a novel host-symbiont interaction.
title_full	Wolbachia infections in Anopheles gambiae cells: transcriptomic characterization of a novel host-symbiont interaction.
title_fullStr	Wolbachia infections in Anopheles gambiae cells: transcriptomic characterization of a novel host-symbiont interaction.
title_full_unstemmed	Wolbachia infections in Anopheles gambiae cells: transcriptomic characterization of a novel host-symbiont interaction.
title_sort	wolbachia infections in anopheles gambiae cells: transcriptomic characterization of a novel host-symbiont interaction.
publisher	Public Library of Science (PLoS)
publishDate	2011
url	https://doaj.org/article/c199b1860f52473c96012ad1e128f152
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Wolbachia infections in Anopheles gambiae cells: transcriptomic characterization of a novel host-symbiont interaction.

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