The role of the peritrophic matrix and red blood cell concentration in Plasmodium vivax infection of Anopheles aquasalis

Abstract

BackgroundPlasmodium vivax is predominant in the Amazon region, and enhanced knowledge of its development inside a natural vector, Anopheles aquasalis, is critical for future strategies aimed at blocking parasite development. The peritrophic matrix (PM), a chitinous layer produced by the mosquito midgut in response to blood ingestion, is a protective barrier against pathogens. Plasmodium can only complete its life-cycle, and consequently be transmitted to a new host, after successfully passing this barrier. Interestingly, fully engorged mosquitoes that had a complete blood meal form a thicker, well-developed PM than ones that feed in small amounts. The amount of red blood cells (RBC) in the blood meal directly influences the production of digestive enzymes and can protect parasites from being killed during the meal digestion. A specific study interrupting the development of the PM associated with the proteolytic activity inhibition, and distinct RBC concentrations, during the P. vivax infection of the New World malaria vector An. aquasalis is expected to clarify whether these factors affect the parasite development.ResultsAbsence of PM in the vector caused a significant reduction in P. vivax infection. However, the association of chitinase with trypsin inhibitor restored infection rates to those of mosquitoes with a structured PM. Also, only the ingestion of trypsin inhibitor by non-chitinase treated mosquitoes increased the infection intensity. Moreover, the RBC concentration in the infected P. vivax blood meal directly influenced the infection rate and its intensity. A straight correlation was observed between RBC concentrations and infection intensity.ConclusionsThis study established that there is a balance between the PM role, RBC concentration and digestive enzyme activity influencing the establishment and development of P. vivax infection inside An. aquasalis. Our results indicate that the absence of PM in the midgut facilitates digestive enzyme dispersion throughout the blood meal, causing direct damage to P. vivax. On the other hand, high RBC concentrations support a better and thick, well-developed PM and protect P. vivax from being killed. Further studies of this complex system may provide insights into other details of the malaria vector response to P. vivax infection.

Prospects, challenges and current status of RNAi through insect feeding

“…Those pores can be temporary and can change depending on the ingested meal, potentially affecting dsRNA transport across the PM. In mosquitoes, the porosity of the PM increases after a blood meal to allow migration of digestive enzymes secreted by exocytosis from epithelial cells . However, our review of the current literature suggests that there is no experimental evidence on how the PM pore size could affect dsRNA transport.…”

“…In mosquitoes, the porosity of the PM increases after a blood meal to allow migration of digestive enzymes secreted by exocytosis from epithelial cells. 20,21 However, our review of the current literature suggests that there is no experimental evidence on how the PM pore size could affect dsRNA transport. Overall, the exact role of the PM after arrival of dsRNA in the gut is still poorly understood.…”

Gut microbiota is essential in PGRP-LA regulated immune protection against Plasmodium berghei infection

“…During this process, two physical barriers are encountered by Plasmodium. The first barrier, peritrophic matrix (PM), composed of chitin, proteoglycans and proteins, is produced by intestinal epithelial cells in response to blood-feeding [5,6]. PM poses an indispensable role in the defense of Plasmodium because its maturation time coincides with the ookinete invasion time [7].…”

Sexual forms obtained in a continuous in vitro cultured Colombian strain of Plasmodium falciparum (FCB2)

“…A standard 0.5% mercurochrome midgut stain was used for parasite form count. Each individual's infection rate (percentage of mosquitoes infected in the midgut) and infection intensity (the median of oocysts in mosquito midgut) was recorded and compared to experimental groups (FCB2) [5]. In vivo gametocyte infectivity was determined by analysing oocysts' phenotypical characteristics in mosquito midgut [17].…”

“…Sexual form fusion (macrogamete and microgamete) occurs inside the mosquito midgut; gametes then mate to form zygotes, which transform into ookinetes and embed themselves within insect midgut epithelial cells [3,4]. Physiological conditions occur simultaneously during the ookinete stage thereby facilitating parasite mobility and oocyst formation and maturation; ookinetes differentiate into oocysts and release large amounts of sporozoites into the haemocoel upon maturation which are responsible for mosquito vector-human transmission [3,5].…”