Plasmodium P36 determines host cell receptor usage during sporozoite invasion

Plasmodium sporozoites, the mosquito-transmitted forms of the malaria parasite, first infect the liver for an initial round of replication before the emergence of pathogenic blood stages. Sporozoites represent attractive targets for antimalarial preventive strategies, yet the mechanisms of parasite...

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Main Authors: Giulia Manzoni, Carine Marinach, Selma Topçu, Sylvie Briquet, Morgane Grand, Matthieu Tolle, Marion Gransagne, Julien Lescar, Chiara Andolina, Jean-François Franetich, Mirjam B Zeisel, Thierry Huby, Eric Rubinstein, Georges Snounou, Dominique Mazier, François Nosten, Thomas F Baumert, Olivier Silvie
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/25903
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language English
format Article
sources DOAJ
author Giulia Manzoni
Carine Marinach
Selma Topçu
Sylvie Briquet
Morgane Grand
Matthieu Tolle
Marion Gransagne
Julien Lescar
Chiara Andolina
Jean-François Franetich
Mirjam B Zeisel
Thierry Huby
Eric Rubinstein
Georges Snounou
Dominique Mazier
François Nosten
Thomas F Baumert
Olivier Silvie
spellingShingle Giulia Manzoni
Carine Marinach
Selma Topçu
Sylvie Briquet
Morgane Grand
Matthieu Tolle
Marion Gransagne
Julien Lescar
Chiara Andolina
Jean-François Franetich
Mirjam B Zeisel
Thierry Huby
Eric Rubinstein
Georges Snounou
Dominique Mazier
François Nosten
Thomas F Baumert
Olivier Silvie
Plasmodium P36 determines host cell receptor usage during sporozoite invasion
eLife
malaria
hepatocyte
sporozoite
P. vivax
P. berghei
P. yoelii
author_facet Giulia Manzoni
Carine Marinach
Selma Topçu
Sylvie Briquet
Morgane Grand
Matthieu Tolle
Marion Gransagne
Julien Lescar
Chiara Andolina
Jean-François Franetich
Mirjam B Zeisel
Thierry Huby
Eric Rubinstein
Georges Snounou
Dominique Mazier
François Nosten
Thomas F Baumert
Olivier Silvie
author_sort Giulia Manzoni
title Plasmodium P36 determines host cell receptor usage during sporozoite invasion
title_short Plasmodium P36 determines host cell receptor usage during sporozoite invasion
title_full Plasmodium P36 determines host cell receptor usage during sporozoite invasion
title_fullStr Plasmodium P36 determines host cell receptor usage during sporozoite invasion
title_full_unstemmed Plasmodium P36 determines host cell receptor usage during sporozoite invasion
title_sort plasmodium p36 determines host cell receptor usage during sporozoite invasion
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2017-05-01
description Plasmodium sporozoites, the mosquito-transmitted forms of the malaria parasite, first infect the liver for an initial round of replication before the emergence of pathogenic blood stages. Sporozoites represent attractive targets for antimalarial preventive strategies, yet the mechanisms of parasite entry into hepatocytes remain poorly understood. Here we show that the two main species causing malaria in humans, Plasmodium falciparum and Plasmodium vivax, rely on two distinct host cell surface proteins, CD81 and the Scavenger Receptor BI (SR-BI), respectively, to infect hepatocytes. By contrast, CD81 and SR-BI fulfil redundant functions during infection by the rodent parasite P. berghei. Genetic analysis of sporozoite factors reveals the 6-cysteine domain protein P36 as a major parasite determinant of host cell receptor usage. Our data provide molecular insights into the invasion pathways used by different malaria parasites to infect hepatocytes, and establish a functional link between a sporozoite putative ligand and host cell receptors.
topic malaria
hepatocyte
sporozoite
P. vivax
P. berghei
P. yoelii
url https://elifesciences.org/articles/25903
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spelling doaj-b4f9109adff8452b8f21f8a38e13c3302021-05-05T13:28:56ZengeLife Sciences Publications LtdeLife2050-084X2017-05-01610.7554/eLife.25903Plasmodium P36 determines host cell receptor usage during sporozoite invasionGiulia Manzoni0Carine Marinach1Selma Topçu2Sylvie Briquet3Morgane Grand4Matthieu Tolle5Marion Gransagne6Julien Lescar7Chiara Andolina8Jean-François Franetich9Mirjam B Zeisel10Thierry Huby11https://orcid.org/0000-0001-6634-551XEric Rubinstein12https://orcid.org/0000-0001-7623-9665Georges Snounou13Dominique Mazier14François Nosten15https://orcid.org/0000-0002-7951-0745Thomas F Baumert16Olivier Silvie17https://orcid.org/0000-0002-0525-6940Sorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Centre d’Immunologie et des Maladies Infectieuses, U1135, ERL8255, Paris, FranceSorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Centre d’Immunologie et des Maladies Infectieuses, U1135, ERL8255, Paris, FranceSorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Centre d’Immunologie et des Maladies Infectieuses, U1135, ERL8255, Paris, FranceSorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Centre d’Immunologie et des Maladies Infectieuses, U1135, ERL8255, Paris, FranceSorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Centre d’Immunologie et des Maladies Infectieuses, U1135, ERL8255, Paris, FranceSorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Centre d’Immunologie et des Maladies Infectieuses, U1135, ERL8255, Paris, FranceSorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Centre d’Immunologie et des Maladies Infectieuses, U1135, ERL8255, Paris, FranceSorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Centre d’Immunologie et des Maladies Infectieuses, U1135, ERL8255, Paris, FranceShoklo Malaria Research Unit, Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Mae Sot, Thailand; Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, United KingdomSorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Centre d’Immunologie et des Maladies Infectieuses, U1135, ERL8255, Paris, FranceINSERM, U1110, Institut de Recherche sur les Maladies Virales et Hépatiques, Strasbourg, France; Université de Strasbourg, Strasbourg, FranceSorbonne Universités, UPMC Univ Paris 06, INSERM, Institute of Cardiometabolism and Nutrition, UMR_S 1166, Paris, FranceINSERM, U935, Villejuif, France; Université Paris Sud, Institut André Lwoff, Villejuif, FranceSorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Centre d’Immunologie et des Maladies Infectieuses, U1135, ERL8255, Paris, FranceSorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Centre d’Immunologie et des Maladies Infectieuses, U1135, ERL8255, Paris, France; Assistance Publique Hôpitaux de Paris, Centre Hospitalo-Universitaire Pitié-Salpêtrière, Paris, FranceShoklo Malaria Research Unit, Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Mae Sot, Thailand; Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, United KingdomINSERM, U1110, Institut de Recherche sur les Maladies Virales et Hépatiques, Strasbourg, France; Université de Strasbourg, Strasbourg, France; Institut Hospitalo-Universitaire, Pôle Hépato-digestif, Hopitaux Universitaires de Strasbourg, Strasbourg, FranceSorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Centre d’Immunologie et des Maladies Infectieuses, U1135, ERL8255, Paris, FrancePlasmodium sporozoites, the mosquito-transmitted forms of the malaria parasite, first infect the liver for an initial round of replication before the emergence of pathogenic blood stages. Sporozoites represent attractive targets for antimalarial preventive strategies, yet the mechanisms of parasite entry into hepatocytes remain poorly understood. Here we show that the two main species causing malaria in humans, Plasmodium falciparum and Plasmodium vivax, rely on two distinct host cell surface proteins, CD81 and the Scavenger Receptor BI (SR-BI), respectively, to infect hepatocytes. By contrast, CD81 and SR-BI fulfil redundant functions during infection by the rodent parasite P. berghei. Genetic analysis of sporozoite factors reveals the 6-cysteine domain protein P36 as a major parasite determinant of host cell receptor usage. Our data provide molecular insights into the invasion pathways used by different malaria parasites to infect hepatocytes, and establish a functional link between a sporozoite putative ligand and host cell receptors.https://elifesciences.org/articles/25903malariahepatocytesporozoiteP. vivaxP. bergheiP. yoelii