Wolbachia Infections in Anopheles gambiae Cells: Transcriptomic Characterization of a Novel Host-Symbiont Interaction

PLoS Pathogens

Anne E. Jedlicka¹  Jason A. Bailey²  Xiaoxia Ren³  Grant L. Hughes⁴  Jose L. Ramirez⁴  Joyce M. Sakamoto⁴  Jason L. Rasgon⁴ 

[1] Department of Epidemiology and Preventive Medicine, University of Maryland Baltimore, Baltimore, Maryland, United States of America;The Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, United States of America;The Johns Hopkins Malaria Research Institute, Baltimore, Maryland, United States of America;The W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland, United States of America

关键词: Wolbachia;    Mosquitoes;    Gene regulation;    Anopheles gambiae;    Plasmodium;    Drosophila melanogaster;    Gene expression;    Microarrays;   

DOI  :  10.1371/journal.ppat.1001296

学科分类：生物科学（综合）

来源: Public Library of Science

【 摘 要 】

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.

【 授权许可】

CC BY