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Malaria parasites differentially sense environmental elasticity during transmission

Transmission of malaria‐causing parasites to and by the mosquito relies on active parasite migration and constitutes bottlenecks in the Plasmodium life cycle. Parasite adaption to the biochemically and physically different environments must hence be a key evolutionary driver for transmission efficie...

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Autores principales: Ripp, Johanna, Kehrer, Jessica, Smyrnakou, Xanthoula, Tisch, Nathalie, Tavares, Joana, Amino, Rogerio, Ruiz de Almodovar, Carmen, Frischknecht, Friedrich
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8033522/
https://www.ncbi.nlm.nih.gov/pubmed/33666362
http://dx.doi.org/10.15252/emmm.202113933
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author Ripp, Johanna
Kehrer, Jessica
Smyrnakou, Xanthoula
Tisch, Nathalie
Tavares, Joana
Amino, Rogerio
Ruiz de Almodovar, Carmen
Frischknecht, Friedrich
author_facet Ripp, Johanna
Kehrer, Jessica
Smyrnakou, Xanthoula
Tisch, Nathalie
Tavares, Joana
Amino, Rogerio
Ruiz de Almodovar, Carmen
Frischknecht, Friedrich
author_sort Ripp, Johanna
collection PubMed
description Transmission of malaria‐causing parasites to and by the mosquito relies on active parasite migration and constitutes bottlenecks in the Plasmodium life cycle. Parasite adaption to the biochemically and physically different environments must hence be a key evolutionary driver for transmission efficiency. To probe how subtle but physiologically relevant changes in environmental elasticity impact parasite migration, we introduce 2D and 3D polyacrylamide gels to study ookinetes, the parasite forms emigrating from the mosquito blood meal and sporozoites, the forms transmitted to the vertebrate host. We show that ookinetes adapt their migratory path but not their speed to environmental elasticity and are motile for over 24 h on soft substrates. In contrast, sporozoites evolved more short‐lived rapid gliding motility for rapidly crossing the skin. Strikingly, sporozoites are highly sensitive to substrate elasticity possibly to avoid adhesion to soft endothelial cells on their long way to the liver. Hence, the two migratory stages of Plasmodium evolved different strategies to overcome the physical challenges posed by the respective environments and barriers they encounter.
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spelling pubmed-80335222021-04-14 Malaria parasites differentially sense environmental elasticity during transmission Ripp, Johanna Kehrer, Jessica Smyrnakou, Xanthoula Tisch, Nathalie Tavares, Joana Amino, Rogerio Ruiz de Almodovar, Carmen Frischknecht, Friedrich EMBO Mol Med Reports Transmission of malaria‐causing parasites to and by the mosquito relies on active parasite migration and constitutes bottlenecks in the Plasmodium life cycle. Parasite adaption to the biochemically and physically different environments must hence be a key evolutionary driver for transmission efficiency. To probe how subtle but physiologically relevant changes in environmental elasticity impact parasite migration, we introduce 2D and 3D polyacrylamide gels to study ookinetes, the parasite forms emigrating from the mosquito blood meal and sporozoites, the forms transmitted to the vertebrate host. We show that ookinetes adapt their migratory path but not their speed to environmental elasticity and are motile for over 24 h on soft substrates. In contrast, sporozoites evolved more short‐lived rapid gliding motility for rapidly crossing the skin. Strikingly, sporozoites are highly sensitive to substrate elasticity possibly to avoid adhesion to soft endothelial cells on their long way to the liver. Hence, the two migratory stages of Plasmodium evolved different strategies to overcome the physical challenges posed by the respective environments and barriers they encounter. John Wiley and Sons Inc. 2021-03-05 2021-04-09 /pmc/articles/PMC8033522/ /pubmed/33666362 http://dx.doi.org/10.15252/emmm.202113933 Text en © 2021 The Authors. Published under the terms of the CC BY 4.0 license https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Reports
Ripp, Johanna
Kehrer, Jessica
Smyrnakou, Xanthoula
Tisch, Nathalie
Tavares, Joana
Amino, Rogerio
Ruiz de Almodovar, Carmen
Frischknecht, Friedrich
Malaria parasites differentially sense environmental elasticity during transmission
title Malaria parasites differentially sense environmental elasticity during transmission
title_full Malaria parasites differentially sense environmental elasticity during transmission
title_fullStr Malaria parasites differentially sense environmental elasticity during transmission
title_full_unstemmed Malaria parasites differentially sense environmental elasticity during transmission
title_short Malaria parasites differentially sense environmental elasticity during transmission
title_sort malaria parasites differentially sense environmental elasticity during transmission
topic Reports
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8033522/
https://www.ncbi.nlm.nih.gov/pubmed/33666362
http://dx.doi.org/10.15252/emmm.202113933
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