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Infection intensity-dependent responses of Anopheles gambiae to the African malaria parasite Plasmodium falciparum.

ABSTRACT: Malaria remains a devastating disease despite efforts at control and prevention. Extensive studies using mostly rodent infection models reveal that successful Plasmodium parasite transmission by the African mosquito vector Anopheles gambiae depends on finely tuned vector-parasite interactions. Here we investigate the transcriptional response of A. gambiae to geographically related Plasmodium falciparum populations at various infection intensities and different infection stages. These responses are compared with those of mosquitoes infected with the rodent parasite Plasmodium berghei. We demonstrate that mosquito responses are largely dependent on the intensity of infection. A major transcriptional suppression of genes involved in the regulation of midgut homeostasis is detected in low-intensity P. falciparum infections, the most common type of infection in Africa. Importantly, genes transcriptionally induced during these infections tend to be phylogenetically unique to A. gambiae. These data suggest that coadaptation between vectors and parasites may act to minimize the impact of infection on mosquito fitness by selectively suppressing specific functional classes of genes. RNA interference (RNAi)-mediated gene silencing provides initial evidence for important roles of the mosquito G protein-coupled receptors (GPCRs) in controlling infection intensity-dependent antiparasitic responses.

SUBMITTER: Mendes AM

PROVIDER: S-EPMC3257935 | biostudies-literature | 2011 Nov

REPOSITORIES: biostudies-literature

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Infection intensity-dependent responses of Anopheles gambiae to the African malaria parasite Plasmodium falciparum.

Mendes Antonio M AM Awono-Ambene Parfait H PH Nsango Sandrine E SE Cohuet Anna A Fontenille Didier D Kafatos Fotis C FC Christophides George K GK Morlais Isabelle I Vlachou Dina D

Infection and immunity 20110815 11

Malaria remains a devastating disease despite efforts at control and prevention. Extensive studies using mostly rodent infection models reveal that successful Plasmodium parasite transmission by the African mosquito vector Anopheles gambiae depends on finely tuned vector-parasite interactions. Here we investigate the transcriptional response of A. gambiae to geographically related Plasmodium falciparum populations at various infection intensities and different infection stages. These responses a ...[more]

PMID: 21844236

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Project description:Transmission of malaria is dependent on the successful completion of the Plasmodium lifecycle in the Anopheles vector. Major obstacles are encountered in the midgut tissue, where most parasites are killed by the mosquito's immune system. In the present study, DNA microarray analyses have been used to compare Anopheles gambiae responses to invasion of the midgut epithelium by the ookinete stage of the human pathogen Plasmodium falciparum and the rodent experimental model pathogen P. berghei. Invasion by P. berghei had a more profound impact on the mosquito transcriptome, including a variety of functional gene classes, while P. falciparum elicited a broader immune response at the gene transcript level. Ingestion of human malaria-infected blood lacking invasive ookinetes also induced a variety of immune genes, including several anti-Plasmodium factors. Twelve selected genes were assessed for effect on infection with both parasite species and bacteria using RNAi gene silencing assays, and seven of these genes were found to influence mosquito resistance to both parasite species. An MD2-like receptor, AgMDL1, and an immunolectin, FBN39, showed specificity in regulating only resistance to P. falciparum, while the antimicrobial peptide gambicin and a novel putative short secreted peptide, IRSP5, were more specific for defense against the rodent parasite P. berghei. While all the genes that affected Plasmodium development also influenced mosquito resistance to bacterial infection, four of the antimicrobial genes had no effect on Plasmodium development. Our study shows that the impact of P. falciparum and P. berghei infection on A. gambiae biology at the gene transcript level is quite diverse, and the defense against the two Plasmodium species is mediated by antimicrobial factors with both universal and Plasmodium-species specific activities. Furthermore, our data indicate that the mosquito is capable of sensing infected blood constituents in the absence of invading ookinetes, thereby inducing anti-Plasmodium immune responses.

Project description:In the fight against malaria, transmission blocking interventions (TBIs) such as transmission blocking vaccines or drugs, are promising approaches to complement conventional tools. They aim to prevent the infection of vectors and thereby reduce the subsequent exposure of a human population to infectious mosquitoes. The effectiveness of these approaches has been shown to depend on the initial intensity of infection in mosquitoes, often measured as the mean number of oocysts resulting from an infectious blood meal in absence of intervention. In mosquitoes exposed to a high intensity of infection, current TBI candidates are expected to be ineffective at completely blocking infection but will decrease parasite load and therefore, potentially also affect key parameters of vector transmission. The present study investigated the consequences of changes in oocyst intensity on subsequent parasite development and mosquito survival. To address this, we experimentally produced different intensities of infection for Anopheles gambiae females from Burkina Faso by diluting gametocytes from three natural Plasmodium falciparum local isolates and used a newly developed non-destructive method based on the exploitation of mosquito sugar feeding to track parasite and mosquito life history traits throughout sporogonic development. Our results indicate the extrinsic incubation period (EIP) of P. falciparum and mosquito survival did not vary with parasite density but differed significantly between parasite isolates with estimated EIP50 of 16 (95% CI: 15-18), 14 (95% CI: 12-16) and 12 (95% CI: 12-13) days and median longevity of 25 (95% CI: 22-29), 15 (95% CI: 13-15) and 18 (95% CI: 17-19) days for the three isolates respectively. Our results here do not identify unintended consequences of the decrease of parasite loads in mosquitoes on the parasite incubation period or on mosquito survival, two key parameters of vectorial capacity, and hence support the use of transmission blocking strategies to control malaria.

Dataset Information

Infection intensity-dependent responses of Anopheles gambiae to the African malaria parasite Plasmodium falciparum.

Publications

Infection intensity-dependent responses of Anopheles gambiae to the African malaria parasite Plasmodium falciparum.

Similar Datasets

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