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The Anopheles gambiae adult midgut peritrophic matrix proteome.

ABSTRACT: Malaria is a devastating disease. For transmission to occur, Plasmodium, the causative agent of malaria, must complete a complex developmental cycle in its mosquito vector. Thus, the mosquito is a potential target for disease control. Plasmodium ookinetes, which develop within the mosquito midgut, must first cross the midgut's peritrophic matrix (PM), a thick extracellular sheath that completely surrounds the blood meal. The PM poses a partial, natural barrier against parasite invasion of the midgut and it is speculated that modifications to the PM may lead to a complete barrier to infection. However, such strategies require thorough characterization of the structure of the PM. Here, we describe for the first time, the complete PM proteome of the main malaria vector, Anopheles gambiae. Altogether, 209 proteins were identified by mass spectrometry. Among them were nine new chitin-binding peritrophic matrix proteins, expanding the list from three to twelve peritrophins. Lastly, we provide a model for the putative interactions among the proteins identified in this study.

SUBMITTER: Dinglasan RR

PROVIDER: S-EPMC2684889 | biostudies-literature | 2009 Feb

REPOSITORIES: biostudies-literature

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The Anopheles gambiae adult midgut peritrophic matrix proteome.

Dinglasan R R RR Dinglasan R R RR Devenport M M Florens L L Johnson J R JR McHugh C A CA Donnelly-Doman M M Carucci D J DJ Yates J R JR Jacobs-Lorena M M

Insect biochemistry and molecular biology 20081111 2

Malaria is a devastating disease. For transmission to occur, Plasmodium, the causative agent of malaria, must complete a complex developmental cycle in its mosquito vector. Thus, the mosquito is a potential target for disease control. Plasmodium ookinetes, which develop within the mosquito midgut, must first cross the midgut's peritrophic matrix (PM), a thick extracellular sheath that completely surrounds the blood meal. The PM poses a partial, natural barrier against parasite invasion of the mi ...[more]

PMID: 19038338

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Project description:BackgroundGenome sequencing of Anopheles gambiae was completed more than ten years ago and has accelerated research on malaria transmission. However, annotation needs to be refined and verified experimentally, as most predicted transcripts have been identified by comparative analysis with genomes from other species. The mosquito midgut-the first organ to interact with Plasmodium parasites-mounts effective antiplasmodial responses that limit parasite survival and disease transmission. High-throughput Illumina sequencing of the midgut transcriptome was used to identify new genes and transcripts, contributing to the refinement of An. gambiae genome annotation.ResultsWe sequenced ~223 million reads from An. gambiae midgut cDNA libraries generated from susceptible (G3) and refractory (L35) mosquito strains. Mosquitoes were infected with either Plasmodium berghei or Plasmodium falciparum, and midguts were collected after the first or second Plasmodium infection. In total, 22,889 unique midgut transcript models were generated from both An. gambiae strain sequences combined, and 76% are potentially novel. Of these novel transcripts, 49.5% aligned with annotated genes and appear to be isoforms or pre-mRNAs of reference transcripts, while 50.5% mapped to regions between annotated genes and represent novel intergenic transcripts (NITs). Predicted models were validated for midgut expression using qRT-PCR and microarray analysis, and novel isoforms were confirmed by sequencing predicted intron-exon boundaries. Coding potential analysis revealed that 43% of total midgut transcripts appear to be long non-coding RNA (lncRNA), and functional annotation of NITs showed that 68% had no homology to current databases from other species. Reads were also analyzed using de novo assembly and predicted transcripts compared with genome mapping-based models. Finally, variant analysis of G3 and L35 midgut transcripts detected 160,742 variants with respect to the An. gambiae PEST genome, and 74% were new variants. Intergenic transcripts had a higher frequency of variation compared with non-intergenic transcripts.ConclusionThis in-depth Illumina sequencing and assembly of the An. gambiae midgut transcriptome doubled the number of known transcripts and tripled the number of variants known in this mosquito species. It also revealed existence of a large number of lncRNA and opens new possibilities for investigating the biological function of many newly discovered transcripts.

Project description:BackgroundThe midgut of hematophagous insects, such as disease transmitting mosquitoes, carries out a variety of essential functions that mostly relate to blood feeding. The midgut of the female malaria vector mosquito Anopheles gambiae is a major site of interactions between the parasite and the vector. Distinct compartments and cell types of the midgut tissue carry out specific functions and vector borne pathogens interact and infect different parts of the midgut.ResultsA microarray based global gene expression approach was used to compare transcript abundance in the four major female midgut compartments (cardia, anterior, anterior part of posterior and posterior part of posterior midgut) and between the male and female Anopheles gambiae midgut. Major differences between the female and male midgut gene expression relate to digestive processes and immunity. Each compartment has a distinct gene function profile with the posterior midgut expressing digestive enzyme genes and the cardia and anterior midgut expressing high levels of antimicrobial peptide and other immune gene transcripts. Interestingly, the cardia expressed several known anti-Plasmodium factors. A parallel peptidomic analysis of the cardia identified known mosquito antimicrobial peptides as well as several putative short secreted peptides that are likely to represent novel antimicrobial factors.ConclusionThe A. gambiae sex specific midgut and female midgut compartment specific transcriptomes correlates with their known functions. The significantly greater functional diversity of the female midgut relate to hematophagy that is associated with digestion and nutrition uptake as well as exposes it to a variety of pathogens, and promotes growth of its endogenous microbial flora. The strikingly high proportion of immunity related factors in the cardia tissue most likely serves the function to increase sterility of ingested sugar and blood. A detailed characterization of the functional specificities of the female mosquito midgut and its various compartments can greatly contribute to our understanding of its role in disease transmission and generate the necessary tools for the development of malaria control strategies.

Dataset Information

The Anopheles gambiae adult midgut peritrophic matrix proteome.

Publications

The Anopheles gambiae adult midgut peritrophic matrix proteome.

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