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 a 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.

Modulation of Midgut Peritrophins' Expression during <i>Plasmodium Infection</i> in <i>Anopheles stephensi</i> (Diptera:Culicidae)

“…This varying degree of thickness of PM could be due to differential peritrophin expression observed. In the present study, it was observed that most of the peritrophin genes were upregulated by 24 h following blood meal which corroborates with maximum thickness of peritrophic matrix observed at the same time 19 . Earlier, Dana et al 23 demonstrated that the midgut transcripts including peritrophins were present as early as 30 min post-blood meal and further categorized the timedependent differential expression of peritrophins in A. gambiae into early-, mid-and late-phase genes.…”

“…Temporal regulation of secretory vesicular appearance process where PM precursors are accumulated was also demonstrated in the midgut of A. darlingi 25 , A. albimanus 13 and A. stephensi 26 . In contrast, in A. aegypti, the vesicles are formed de novo after blood feeding 19 . The early-, mid-and late-stage peritrophin expression in the A. stephensi midgut observed in our study corroborates with previous studies.…”

“…In A. gambiae, more than 200 proteins have been reported in the proteome of peritrophic matrix, of which twelve are peritrophins 19 . Based on the sequence similarity with A. gambiae peritrophins, presence of secretory signal peptide, chitin-binding domain (s) and glycosylation sites, eight putative peritrophins were identified in A. stephensi.…”

“…However, mosquito midgut membrane-bound proteases such as aminopeptidase and carboxypeptidase are postulated to be ideal candidates for blocking transmission. Therefore, it would be intriguing to elucidate the interaction of peritrophins with these digestive enzymes during normal and infected blood 3,19 . The absence of a PM in adult male mosquitoes implies that the female mosquito PM has a role during blood feeding.…”

VSG overcomes an early barrier to survival of African trypanosomes in tsetse flies

“…Using RNA sequencing, the authors first determined gene expression in midgut cells at 48 and 72 h after feeding mature adults on trypanosome-infected or normal blood. Aksoy et al found that trypanosomes reduced the expression of peritrophins, structural proteins that bind chitin, and digestive enzymes, both associated with PM formation in insects (16)(17)(18). Then Aksoy et al (14) used the entomopathogenic Serratia marcescens in an elegant microbial assay to assess the PM integrity in tsetse flies.…”