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

Djane Clarys Baia-Da-Silva,Maria Das Graças Vale Barbosa Guerra,Fabio Trindade Maranhão Costa,Marcus Vinicius Guimarães Lacerda,Omaira Vera Lizcano,Nagila Francinete Costa Secundino,Luis Carlos Salazar Alvarez,Wuelton Marcelo Monteiro,Rafael Nacif-Pimenta,Paulo Filemon Paolucci Pimenta,Stefanie Costa Pinto Lopes,Alessandra Silva Orfanó,Denner Oliveira Pascoal,Iria Cabral Rodriguez

doi:10.1186/s13071-018-2752-5

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.

Highlights

Plasmodium 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
This study established that there is a balance between the peritrophic matrix (PM) role, red blood cells (RBC) concentration and digestive enzyme activity influencing the establishment and development of P. vivax modulating the infection inside the New World malaria vector An. aquasalis
An enhanced knowledge of P. vivax development inside the New World malaria vector An. aquasalis is critical for future strategies aimed at blocking parasite development

Summary

Introduction

Plasmodium 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. 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. 70 Anopheles species are considered malaria vectors in the American continent [2]. Anopheles aquasalis is an important malaria vector that breeds in brackish marsh [3] and is distributed predominantly along the South and Central American areas where it is considered the primary coastal malaria vector of P. vivax [4,5,6]. An. aquasalis is a species that has been colonized for several years [7] and in the last decade, it has been used as a good experimental model for interaction studies with P. vivax [8,9,10,11,12,13]

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