TY - JOUR
T1 - Species-specific escape of Plasmodium sporozoites from oocysts of avian, rodent, and human malarial parasites
AU - Orfano, Alessandra S.
AU - Nacif-Pimenta, Rafael
AU - Duarte, Ana P.M.
AU - Villegas, Luis M.
AU - Rodrigues, Nilton B.
AU - Pinto, Luciana C.
AU - Campos, Keillen M.M.
AU - Pinilla, Yudi T.
AU - Chaves, Bárbara
AU - Barbosa Guerra, Maria G.V.
AU - Monteiro, Wuelton M.
AU - Smith, Ryan C.
AU - Molina-Cruz, Alvaro
AU - Lacerda, Marcus V.G.
AU - Secundino, Nágila F.C.
AU - Jacobs-Lorena, Marcelo
AU - Barillas-Mury, Carolina
AU - Pimenta, Paulo F.P.
N1 - Funding Information:
ASO and RNP are Ph.D. students of the Graduate Program in Health Sciences of the FIOCRUZ‑Minas Gerais. KMMC, YTP and BC are Ph.D. students of the Graduate Program in Tropical Medicine of the UEA/FMT‑HVD. APMD, LMV, NBR and LCP are pos‑doctoral fellows. PFPP is a senior visiting fellow at the FMT‑ HVD supported by Amazonas State Research Support Foundation (FAPEAM). PFPP, NFCS, MGVB and MVGL are senior fellows from the Brazilian Council for Scientific and Technological Development (CNPq).
Funding Information:
This study was partially funded by Bill and Melinda Gates Foundation (TransEpi Study), by grant from the National Institutes of Health R01AI031478 and by the following Brazilian agencies: Foundation of the Institute Oswaldo Cruz (FIOCRUZ), Strategic Programme for Supporting Health Research (PAPES V), Bra‑ zilian Council for Scientific and Technological Development (CNPq), Minas Gerais State Research Support Foundation (FAPEMIG) and Amazonas State Research Support Foundation (FAPEAM). ASO, RNP, KMMC, YTP and BC received Ph.D. scholarships from one of the following Brazilian agencies: FAPEAM, FIOCRUZ, CNPq and CAPES. APMD, LMV, NBR and LCP received pos‑doctoral scholarships from CNPq or CAPES. PFPP, NFCS, MGVB and MVGL are senior fellows from CNPq.
Publisher Copyright:
© 2016 The Author(s).
PY - 2016/8/2
Y1 - 2016/8/2
N2 - Background: Malaria 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. Results: Here, 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. Conclusions: This 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.
AB - Background: Malaria 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. Results: Here, 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. Conclusions: This 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.
KW - Avian
KW - Human
KW - Mosquito vector
KW - Murine
KW - Oocyst
KW - Plasmodium
KW - Sporozoite escape
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U2 - 10.1186/s12936-016-1451-y
DO - 10.1186/s12936-016-1451-y
M3 - Article
C2 - 27480269
AN - SCOPUS:84980016050
VL - 15
JO - Malaria Journal
JF - Malaria Journal
SN - 1475-2875
IS - 1
M1 - 394
ER -