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Reciprocal tripartite interactions between the Aedes aegypti midgut microbiota, innate immune system and dengue virus influences vector competence.

Ramirez JL, Souza-Neto J, Torres Cosme R, Rovira J, Ortiz A, Pascale JM, Dimopoulos G - PLoS Negl Trop Dis (2012)

Bottom Line: It is transmitted between humans by the mosquitoes Aedes aegypti and Aedes albopictus, and at least 2.5 billion people are at daily risk of infection.During their lifecycle, mosquitoes are exposed to a variety of microbes, some of which are needed for their successful development into adulthood.However, recent studies have suggested that the adult mosquito's midgut microflora is critical in influencing the transmission of human pathogens.

View Article: PubMed Central - PubMed

Affiliation: W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland, United States of America.

ABSTRACT
Dengue virus is one of the most important arboviral pathogens and the causative agent of dengue fever, dengue hemorrhagic fever, and dengue shock syndrome. It is transmitted between humans by the mosquitoes Aedes aegypti and Aedes albopictus, and at least 2.5 billion people are at daily risk of infection. During their lifecycle, mosquitoes are exposed to a variety of microbes, some of which are needed for their successful development into adulthood. However, recent studies have suggested that the adult mosquito's midgut microflora is critical in influencing the transmission of human pathogens. In this study we assessed the reciprocal interactions between the mosquito's midgut microbiota and dengue virus infection that are, to a large extent, mediated by the mosquito's innate immune system. We observed a marked decrease in susceptibility to dengue virus infection when mosquitoes harbored certain field-derived bacterial isolates in their midgut. Transcript abundance analysis of selected antimicrobial peptide genes suggested that the mosquito's microbiota elicits a basal immune activity that appears to act against dengue virus infection. Conversely, the elicitation of the mosquito immune response by dengue virus infection itself influences the microbial load of the mosquito midgut. In sum, we show that the mosquito's microbiota influences dengue virus infection of the mosquito, which in turn activates its antibacterial responses.

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Related in: MedlinePlus

Dengue virus infection modultaes the mosquito midgut microbiota.(A) Total bacterial 16s RNA levels in the midguts of dengue virus-infected mosquitoes relative to those of uninfected mosquitoes. Bacterial loads were assessed by qPCR from pools of 10 midguts per replicate, and at least 4 independent biological replicates were included. Data were analyzed by one-way ANOVA with Dunnett's post-test; *, p<0.05. (B) Antimicrobial peptide gene transcript abundance in the midgut of dengue virus-infected mosquitoes relative to uninfected mosquitoes at 7 days and 10 days post-infection. Data were analyzed by Mann-Whitney U-test; *, p<0.05.
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pntd-0001561-g005: Dengue virus infection modultaes the mosquito midgut microbiota.(A) Total bacterial 16s RNA levels in the midguts of dengue virus-infected mosquitoes relative to those of uninfected mosquitoes. Bacterial loads were assessed by qPCR from pools of 10 midguts per replicate, and at least 4 independent biological replicates were included. Data were analyzed by one-way ANOVA with Dunnett's post-test; *, p<0.05. (B) Antimicrobial peptide gene transcript abundance in the midgut of dengue virus-infected mosquitoes relative to uninfected mosquitoes at 7 days and 10 days post-infection. Data were analyzed by Mann-Whitney U-test; *, p<0.05.

Mentions: Dengue virus infection of the mosquito's midgut led to significant decrease in the overall bacterial load (as assessed by 16s rRNA transcript levels) at 24 h, 7 days, and 14 days after ingestion of a dengue virus-supplemented blood meal. Interestingly, the difference in the bacterial 16s rRNA transcript levels between dengue virus-infected and uninfected mosquitoes was less prominent at 3 days post-infection (Figure 5A). Analysis of the relative transcript abundance of the antimicrobial peptide genes lysozyme C, and cecropin G revealed that cecropin G transcripts were significantly elevated in dengue-infected mosquitoes at 7 days post-infection but showed no difference from control levels at 10 days post-infection. Lysozyme C also showed a transient changes in transcript abundace, with no difference from control levels at 7 days but significant changes at 10 days post-infection (Figure 5B).


Reciprocal tripartite interactions between the Aedes aegypti midgut microbiota, innate immune system and dengue virus influences vector competence.

Ramirez JL, Souza-Neto J, Torres Cosme R, Rovira J, Ortiz A, Pascale JM, Dimopoulos G - PLoS Negl Trop Dis (2012)

Dengue virus infection modultaes the mosquito midgut microbiota.(A) Total bacterial 16s RNA levels in the midguts of dengue virus-infected mosquitoes relative to those of uninfected mosquitoes. Bacterial loads were assessed by qPCR from pools of 10 midguts per replicate, and at least 4 independent biological replicates were included. Data were analyzed by one-way ANOVA with Dunnett's post-test; *, p<0.05. (B) Antimicrobial peptide gene transcript abundance in the midgut of dengue virus-infected mosquitoes relative to uninfected mosquitoes at 7 days and 10 days post-infection. Data were analyzed by Mann-Whitney U-test; *, p<0.05.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3295821&req=5

pntd-0001561-g005: Dengue virus infection modultaes the mosquito midgut microbiota.(A) Total bacterial 16s RNA levels in the midguts of dengue virus-infected mosquitoes relative to those of uninfected mosquitoes. Bacterial loads were assessed by qPCR from pools of 10 midguts per replicate, and at least 4 independent biological replicates were included. Data were analyzed by one-way ANOVA with Dunnett's post-test; *, p<0.05. (B) Antimicrobial peptide gene transcript abundance in the midgut of dengue virus-infected mosquitoes relative to uninfected mosquitoes at 7 days and 10 days post-infection. Data were analyzed by Mann-Whitney U-test; *, p<0.05.
Mentions: Dengue virus infection of the mosquito's midgut led to significant decrease in the overall bacterial load (as assessed by 16s rRNA transcript levels) at 24 h, 7 days, and 14 days after ingestion of a dengue virus-supplemented blood meal. Interestingly, the difference in the bacterial 16s rRNA transcript levels between dengue virus-infected and uninfected mosquitoes was less prominent at 3 days post-infection (Figure 5A). Analysis of the relative transcript abundance of the antimicrobial peptide genes lysozyme C, and cecropin G revealed that cecropin G transcripts were significantly elevated in dengue-infected mosquitoes at 7 days post-infection but showed no difference from control levels at 10 days post-infection. Lysozyme C also showed a transient changes in transcript abundace, with no difference from control levels at 7 days but significant changes at 10 days post-infection (Figure 5B).

Bottom Line: It is transmitted between humans by the mosquitoes Aedes aegypti and Aedes albopictus, and at least 2.5 billion people are at daily risk of infection.During their lifecycle, mosquitoes are exposed to a variety of microbes, some of which are needed for their successful development into adulthood.However, recent studies have suggested that the adult mosquito's midgut microflora is critical in influencing the transmission of human pathogens.

View Article: PubMed Central - PubMed

Affiliation: W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland, United States of America.

ABSTRACT
Dengue virus is one of the most important arboviral pathogens and the causative agent of dengue fever, dengue hemorrhagic fever, and dengue shock syndrome. It is transmitted between humans by the mosquitoes Aedes aegypti and Aedes albopictus, and at least 2.5 billion people are at daily risk of infection. During their lifecycle, mosquitoes are exposed to a variety of microbes, some of which are needed for their successful development into adulthood. However, recent studies have suggested that the adult mosquito's midgut microflora is critical in influencing the transmission of human pathogens. In this study we assessed the reciprocal interactions between the mosquito's midgut microbiota and dengue virus infection that are, to a large extent, mediated by the mosquito's innate immune system. We observed a marked decrease in susceptibility to dengue virus infection when mosquitoes harbored certain field-derived bacterial isolates in their midgut. Transcript abundance analysis of selected antimicrobial peptide genes suggested that the mosquito's microbiota elicits a basal immune activity that appears to act against dengue virus infection. Conversely, the elicitation of the mosquito immune response by dengue virus infection itself influences the microbial load of the mosquito midgut. In sum, we show that the mosquito's microbiota influences dengue virus infection of the mosquito, which in turn activates its antibacterial responses.

Show MeSH
Related in: MedlinePlus