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

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.

The Sporozoite's Journey Through the Mosquito: A Critical Examination of Host and Parasite Factors Required for Salivary Gland Invasion

“…This raises the question as to whether the processes of oocyst egress are conserved in human malaria parasites. Orfano et al (2016) showed that the mechanism for sporozoite egress from the oocyst differs among Plasmodium species. P. berghei and the avian malaria parasite Plasmodium gallinaceum appear to egress similarly, breaking the oocyst wall.…”

Effects of malaria infection on mosquito olfaction and behavior: extrapolating data to the field

“…Analysis of rodent or avian model systems can yield interesting results, but human, avian and rodent Plasmodium have been shown to develop differently within the vector [49], raising questions about how reliably this data can be extrapolated to human systems.…”

“…However, it also raises additional questions about the confidence with which inferences drawn from the results can be extended to real-world human populations. For example, it has been shown that Plasmodium oocysts develop differently in human, rodent and avian hosts [49], which may also impact immune responses. Only two host-seeking studies have been carried out with the human malaria parasite, P. falciparum, with one reporting increased short-range hostseeking by An.…”

Species Composition, Phenotypic and Genotypic Resistance Levels in Major Malaria Vectors in Teso North and Teso South Subcounties in Busia County, Western Kenya

“…Regrettably, these strategic measures are pretty less operative due to the swift evolvement and proliferation of resistance against extensively utilized insecticides and drugs [10,11]. Taking advantage of the genomic sequences of the malaria vectors and parasites may eventually result in new generations of insecticides and drugs, the upcoming of an efficient vaccine or genetically altered mosquitoes [12][13][14]. Unfortunately, these novel intervention measures may be inaccessible for the next ten years.…”