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Plasmodium falciparum parasites exit the infected erythrocyte after haemolysis with saponin and streptolysin O

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Abstract

Malaria is caused by unicellular parasites of the genus Plasmodium, which reside in erythrocytes during the clinically relevant stage of infection. To separate parasite from host cell material, haemolytic agents such as saponin are widely used. Previous electron microscopy studies on saponin-treated parasites reported both, parasites enclosed by the erythrocyte membrane and liberated from the host cell. These ambiguous reports prompted us to investigate haemolysis by live-cell time-lapse microscopy. Using either saponin or streptolysin O to lyse Plasmodium falciparum–infected erythrocytes, we found that ring-stage parasites efficiently exit the erythrocyte upon haemolysis. For late-stage parasites, we found that only approximately half were freed, supporting the previous electron microscopy studies. Immunofluorescence imaging indicated that freed parasites were surrounded by the parasitophorous vacuolar membrane. These results may be of interest for future work using haemolytic agents to enrich for parasite material.

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All data generated or analysed during this study are included in this published article and its supplementary materials.

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Acknowledgements

We thank Elizabeth Egan and Catherine Moreau and past and current members of the Ganter and Guizetti laboratories for discussions. We are grateful to Jude Przyborski for the generous gift of streptolysin O and for the microscopy support from the Infectious Diseases Imaging Platform (IDIP) at the Centre for Integrative Infectious Disease Research, Heidelberg, Germany. We are grateful to the Plasmodium genomics resource PlasmoDB, which facilitated this research. X.S. was as student of the Master Program Molecular Biotechnology at Heidelberg University.

Funding

This work was supported by Zendia GmbH, the German Federal Ministry of Education and Research (KMU-Innovativ Medical technique, 13GW0065A to Zendia GmbH and KMU-Innovative Biochance BIO 326-036 to Zendia GmbH and Heidelberg University). F.F. and M.G. are members of SFB1129. F.F. is a member of the CellNetworks Cluster of Excellence at Heidelberg University and the German Centre for Infection Research, TTU Malaria.

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Contributions

Conceptualisation: K.Q. and M.G.; Methodology: K.Q., M.G and GB; Formal analysis and investigation: K.Q. and X. S.; Writing—original draft preparation: K.Q. and M.G.; Writing—review and editing: K.Q., X.S., F.F., G.B. and M.G; Funding acquisition: F.F. and G.B.; Resources: F.F. and G.B.; Supervision: M.G. and G.B.

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Correspondence to Guido Böse or Markus Ganter.

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Conflict of interest

G.B. is founder and CEO of Zendia GmbH with the goal to develop a commercially available rapid diagnostic test, holding the patents WO2018002327A1 and WO2014096462A3 and country registrations. F.F. served as an advisor for Zendia GmbH and co-directs the BMBF KMU-Innovativ grant BIO-370-036 together with G.B. since 2019. K.Q. is currently employed by Zendia GmbH and X.S. and M.G. were temporarily employed by Zendia GmbH. M.G. is listed as co-inventor on the patent WO2018002327A1.

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Section Editor: Guido Favia

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Electronic supplementary material

Online Resource 1

Live-cell imaging of a late-stage, i.e. hemozoin-containing, parasite during haemolysis with saponin in presence of anti-EXP1 antibody coupled to Alexa Fluor 488. Right, Fluorescent signal of Alexa Fluor 488; left, differential interference contrast (DIC) image. Note, only after lysis, and thus assessable antigen, a specific signal is detectable. (AVI 655 kb)

Online Resource 2a

Ring–stage parasite is freed from erythrocyte membrane after saponin lysis, corresponding movie to Fig. 1a (AVI 156 kb)

Online Resource 2b

Late–stage parasite is still enclosed in erythrocyte membrane after saponin addition, corresponding movie to Fig. 1b (AVI 64 kb)

Online Resource 2c

Late–stage parasite is freed from erythrocyte membrane after saponin addition, corresponding movie to Fig. 1c (AVI 86 kb)

Online Resource 3a

Ring–stage parasite is freed from erythrocyte membrane after SLO lysis, corresponding movie to Fig. 2a (AVI 575 kb)

Online Resource 3b

Late–stage parasite is still enclosed in erythrocyte membrane after SLO addition, corresponding movie to Fig. 2b (AVI 306 kb)

Online Resource 3c

Late–stage parasite is freed from erythrocyte membrane after SLO addition, corresponding movie to Fig. 2c (AVI 263 kb)

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Quadt, K.A., Smyrnakou, X., Frischknecht, F. et al. Plasmodium falciparum parasites exit the infected erythrocyte after haemolysis with saponin and streptolysin O. Parasitol Res 119, 4297–4302 (2020). https://doi.org/10.1007/s00436-020-06932-9

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  • DOI: https://doi.org/10.1007/s00436-020-06932-9

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