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Genes identified by an expression screen of the vector mosquito Anopheles gambiae display differential molecular immune response to malaria parasites and bacteria.

ABSTRACT: We performed a gene expression screen of the entire transcriptome of the major African malaria vector Anopheles gambiae for immune response genes in adult female mosquitoes, which is the developmental stage infected by malaria parasites. Mosquitoes were immune-stimulated for subtractive cloning by treatment with bacterial lipopolysaccharide, a potent and general elicitor of the innate immune response, and by injury. The screen yielded a highly enriched cDNA library in which more than half of the clones were immune responsive. In this paper, we describe 23 immune-regulated genes, including putative protease inhibitors, serine proteases, regulatory molecules, and a number of genes without known relatives. A molecule related to the protease inhibitor alpha-2-macroglobulin responded strongly to malaria parasite infection, but displayed little or no response to bacteria, whereas other genes exhibited the inverse pattern. These results indicate that the insect immune system discriminates between molecular signals specific to infection with bacteria and malaria parasites.

SUBMITTER: Oduol F

PROVIDER: S-EPMC17211 | biostudies-literature | 2000 Oct

REPOSITORIES: biostudies-literature

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Genes identified by an expression screen of the vector mosquito Anopheles gambiae display differential molecular immune response to malaria parasites and bacteria.

Oduol F F Xu J J Niare O O Natarajan R R Vernick K D KD

Proceedings of the National Academy of Sciences of the United States of America 20001001 21

We performed a gene expression screen of the entire transcriptome of the major African malaria vector Anopheles gambiae for immune response genes in adult female mosquitoes, which is the developmental stage infected by malaria parasites. Mosquitoes were immune-stimulated for subtractive cloning by treatment with bacterial lipopolysaccharide, a potent and general elicitor of the innate immune response, and by injury. The screen yielded a highly enriched cDNA library in which more than half of the ...[more]

PMID: 11005829

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Project description:Recognition of peptidoglycan (PGN) is paramount for insect antibacterial defenses. In the fruit fly Drosophila melanogaster, the transmembrane PGN Recognition Protein LC (PGRP-LC) is a receptor of the Imd signaling pathway that is activated after infection with bacteria, mainly Gram-negative (Gram-). Here we demonstrate that bacterial infections of the malaria mosquito Anopheles gambiae are sensed by the orthologous PGRPLC protein which then activates a signaling pathway that involves the Rel/NF-kappaB transcription factor REL2. PGRPLC signaling leads to transcriptional induction of antimicrobial peptides at early stages of hemolymph infections with the Gram-positive (Gram+) bacterium Staphylococcus aureus, but a different signaling pathway might be used in infections with the Gram- bacterium Escherichia coli. The size of mosquito symbiotic bacteria populations and their dramatic proliferation after a bloodmeal, as well as intestinal bacterial infections, are also controlled by PGRPLC signaling. We show that this defense response modulates mosquito infection intensities with malaria parasites, both the rodent model parasite, Plasmodium berghei, and field isolates of the human parasite, Plasmodium falciparum. We propose that the tripartite interaction between mosquito microbial communities, PGRPLC-mediated antibacterial defense and infections with Plasmodium can be exploited in future interventions aiming to control malaria transmission. Molecular analysis and structural modeling provided mechanistic insights for the function of PGRPLC. Alternative splicing of PGRPLC transcripts produces three main isoforms, of which PGRPLC3 appears to have a key role in the resistance to bacteria and modulation of Plasmodium infections. Structural modeling indicates that PGRPLC3 is capable of binding monomeric PGN muropeptides but unable to initiate dimerization with other isoforms. A dual role of this isoform is hypothesized: it sequesters monomeric PGN dampening weak signals and locks other PGRPLC isoforms in binary immunostimulatory complexes further enhancing strong signals.

Dataset Information

Genes identified by an expression screen of the vector mosquito Anopheles gambiae display differential molecular immune response to malaria parasites and bacteria.

Publications

Genes identified by an expression screen of the vector mosquito Anopheles gambiae display differential molecular immune response to malaria parasites and bacteria.

Similar Datasets

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