Species-specific escape of Plasmodium sporozoites from oocysts of avian, rodent, and human malarial parasites.

Alessandra S Orfano,Bárbara Chaves,Nágila F C Secundino,Rafael Nacif-Pimenta,Luis M Villegas,Wuelton M Monteiro,Marcelo Jacobs-Lorena,Marcus V G Lacerda,Paulo F P Pimenta,Ryan C Smith,Maria G V Barbosa Guerra,Keillen M M Campos,Nilton B Rodrigues,Yudi T Pinilla,Luciana C Pinto,Alvaro Molina-Cruz,Carolina Barillas-Mury,Ana P M Duarte

doi:10.1186/s12936-016-1451-y

Abstract

BackgroundMalaria is transmitted when an infected mosquito delivers Plasmodium sporozoites into a vertebrate host. There are many species of Plasmodium and, in general, the infection is host-specific. For example, Plasmodium gallinaceum is an avian parasite, while Plasmodium berghei infects mice. These two parasites have been extensively used as experimental models of malaria transmission. Plasmodium falciparum and Plasmodium vivax are the most important agents of human malaria, a life-threatening disease of global importance. To complete their life cycle, Plasmodium parasites must traverse the mosquito midgut and form an oocyst that will divide continuously. Mature oocysts release thousands of sporozoites into the mosquito haemolymph that must reach the salivary gland to infect a new vertebrate host. The current understanding of the biology of oocyst formation and sporozoite release is mostly based on experimental infections with P.berghei, and the conclusions are generalized to other Plasmodium species that infect humans without further morphological analyses.ResultsHere, it is described the microanatomy of sporozoite escape from oocysts of four Plasmodium species: the two laboratory models, P. gallinaceum and P. berghei, and the two main species that cause malaria in humans, P.vivax and P. falciparum. It was found that sporozoites have species-specific mechanisms of escape from the oocyst. The two model species of Plasmodium had a common mechanism, in which the oocyst wall breaks down before sporozoites emerge. In contrast, P. vivax and P. falciparum sporozoites show a dynamic escape mechanism from the oocyst via polarized propulsion.ConclusionsThis study demonstrated that Plasmodium species do not share a common mechanism of sporozoite escape, as previously thought, but show complex and species-specific mechanisms. In addition, the knowledge of this phenomenon in human Plasmodium can facilitate transmission-blocking studies and not those ones only based on the murine and avian models.

Highlights

Malaria is transmitted when an infected mosquito delivers Plasmodium sporozoites into a vertebrate host
Careful comparative scanning electron microscope (SEM) analyses of infected midguts dissected from susceptible mosquito vectors, containing distinct Plasmodium species, revealed several new details of the oocyst surface and the sporozoite escape process that are unique to each Plasmodium species
Escape of Plasmodium gallinaceum sporozoites from oocysts Magnification of dissected midguts showed hundreds of rounded avian P. gallinaceum oocysts on the midgut surface of the infected Ae. aegypti

Summary

Introduction

Malaria is transmitted when an infected mosquito delivers Plasmodium sporozoites into a vertebrate host. Plasmodium falciparum and Plasmodium vivax are the most important agents of human malaria, a life-threatening disease of global importance To complete their life cycle, Plasmodium parasites must traverse the mosquito midgut and form an oocyst that will divide continuously. The oocysts progress to the asexual phase of multiplication known as sporogony, which is completed in approximately 1–2 weeks, the longest phase of the Plasmodium life cycle in the mosquito vector. This biological process produces thousands of sporozoites, the final form of Plasmodium in the vector. Once inside the salivary gland, the sporozoites are ready to be injected into a new vertebrate host via a mosquito bite, completing the Plasmodium life cycle in the invertebrate vector [16,17,18]

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