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The salivary transcriptome of Anopheles gambiae (Diptera: Culicidae) larvae: A microarrray-based study

ABSTRACT: In spite of the many recent developments in the field of vector sialomics, the salivary glands of larvalmosquitoes have been largely unexplored. We used whole-transcriptome microarray analysis to create a gene-expression profile of the salivary gland tissue of fourth-instar Anopheles gambiae larvae, and compare it to the gene-expression profile of a matching group of whole larvae. We identified a total of 221 probes with expression values that were (a) significantly enriched in the salivary glands, and (b)sufficiently annotated as to allow the prediction of the presence/absence of signal peptides in their corresponding gene products. Based on available annotation of the protein sequences associated with these probes, we propose that the main roles of larval salivary secretions include: (a) immune response, (b) mouthpart lubrication, (c) nutrient metabolism, and (d) xenobiotic detoxification. Other highlights of the study include the cloning of a transcript encoding a previously unknown salivary defensin (AgDef5), the confirmation of mucus secretion by the larval salivary glands, and the first report of salivary lipocalins in the Culicidae. Keywords: Anopheles gambiae, salivary gland, Diptera, gene expression, salivary defensin, transcriptome, salivary lipocalin

ORGANISM(S): Anopheles gambiae Plasmodium falciparum

PROVIDER: GSE9642 | GEO | 2008/05/01

SECONDARY ACCESSION(S): PRJNA103503

REPOSITORIES: GEO

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Project description:Although the salivary transcriptome of adult mosquitoes has been thoroughly described in several recent papers, very little information exists regarding the biological role of larval salivary glands in the Culicidae. We used whole-transcriptome AffymetrixÂ® chips to compare the transcriptional profiles of Anopheles gambiae larval (L4) salivary glands and whole larvae. We identified a total of 277 transcripts as being significantly enriched in the salivary glands. Based on available annotation for the known or predicted protein sequences encoded by these transcripts, 41 were identified as corresponding to secreted proteins, 233 as corresponding to non-secreted (housekeeping) proteins, and 3 as encoding proteins of unknown function. Based on functional annotation of the putatively secreted gene products, we propose that larval salivary secretions have roles in nutrient digestion, detoxification, immunity, and mouthpart lubrication. Interestingly, several components of the larval saliva (e.g. apyrase and serine proteases) have also been reported to exist in adult female saliva, where they are though to help regulate a vertebrate hostâs immune response to bloodfeeding. In conclusion, our results suggest that the salivary glands are important components of both the digestive and immune systems of larval mosquitoes, and that their study might provide clues about the evolution of adaptations to bloodfeeding observed in adults. Experiment Overall Design: We attempted to identify transcripts that are both present and significantly enriched in the salivary glands (SG) of the 4th instar Anopheles gambiae larva. Transcripts were considered as present in the SG if the built-in Affymetrix detection call scored them as such in all three biological replicates of the experiment. Expression values (i.e. signal intensities) of transcripts from the salivary glands were compared to those of a matching group of whole 4th instar larvae using a t-test. Transcripts showing an expression value two-fold or higher (p < 0.01; false discovery rate=1%) in the SG as compared to whole larvae were considered to be significantly enriched.

Project description:Simultaneous analysis of Plasmodium falciparum and Anopheles gambiae gene expression: an assessment of parasite maturation and of the mosquito response to infection. Malaria is probably the most lethal and most prevalent parasitic disease in the world, causing more than one million deaths per year. In spite of intensive research, no vaccine exists and good vaccine candidates are still a necessity. Plasmodium sporozoites from mosquito midguts are not as infective as those from salivary glands, presenting a different type of motility which is presumably associated with their invasive capacity. It is assumed that these differences are due to maturation of sporozoites, which happens either in the salivary glands or somewhere along the way from the midgut to the glands. Indeed, the invasion of the salivary gland is considered to be an essential step for malaria transmission to the host and it is known to causes expression of multiple genes in the parasite and activation of some immune-response genes in the insect. Here we compared the gene expression profile of P. falciparum parasites from midgut and salivary glands in order to search for genes involved in parasite maturation; on the assumption that any differentially expressed genes found under this condition could be potentially related to the higher infectivity of the salivary gland derived sporozoites and therefore would be potentially good vaccine candidates. Also, because very little is known about mosquito genes involved in the response to Plasmodium, we compared the gene expression profile of infected and uninfected midguts and salivary glands. Our results demonstrate that, upon infection, at least 13 genes are differentially expressed in the mosquito midgut and 43 in the salivary gland. Gene ontology enrichment analysis showed that among other things, in mosquito salivary glands, infection causes multiple genes related to chitin metabolism to be differentially expressed. Also and more importantly, at least 54 genes were differentially expressed in P. falciparum from salivary glands in comparison to midgut (19 down-regulated and 35 up-regulated). Last, we show for the first time that P. falciparum causes multiple genes in the salivary gland to be regulated and that some of those genes could be potentially beneficial to the parasite.

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The salivary transcriptome of Anopheles gambiae (Diptera: Culicidae) larvae: A microarrray-based study

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