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1. Cytotoxic anti-circumsporozoite antibodies target malaria sporozoites in the host skin

Author

Silvia Beatriz Boscardin, Tomoko Ishino, Marcio Massao Yamamoto, Olivier Silvie, Rogerio Amino, Sylvie Dartevelle, François Traincard, Masao Yuda, Raquel Hoffmann Panatieri, Joana Tavares, Eduardo Aliprandini, Sabine Thiberge, Infection et Immunité paludéennes - Malaria Infection and Immunity, Institut Pasteur [Paris] (IP), Instituto de Investigação e Inovação em Saúde (I3S), Universidade do Porto = University of Porto, Instituto de Biologia Molecular e Celular - institute for molecular and cell biology [Porto, Portugal] (IBMC), Department of Parasitology [São Paulo] (IBS), Institute of Biomedical Sciences (ICB/USP), Universidade de São Paulo = University of São Paulo (USP)-Universidade de São Paulo = University of São Paulo (USP), Centre de Production et Infection des Anophèles (plateforme) - Center for the Production and Infection of Anopheles (platform) (CEPIA), Centre d'Immunologie et des Maladies Infectieuses (CIMI), Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Ehime University [Matsuyama, Japon], Mie University Graduate School / Faculty of Medicine [Japan], Mie University, Ingénierie des Anticorps (plate-forme) - Antibody Engineering (Platform), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), This work was supported by funds from Institut Pasteur, Paris, the French National Research Agency (grant no. ANR-14-CE16-Im3alaria), the French Government’s ‘Investissement d’Avenir’ program, Laboratoire d’Excellence ‘Integrative Biology of Emerging Infectious Diseases’ (grant no. ANR-10-LABX-62-IBEID) and ‘ParaFrap’ (grant no. ANR-11-LABX-0024), the São Paulo Research Foundation (FAPESP, grant no. 2014/50631-0), the National Council for Scientific and Technological Development (CNPq), the BNP Paribas CIB, the Portuguese Science and Technology Foundation (FCT, grant no. IF/00881/2012/CP0158) and the European Social Fund (Human Potential Operational Programme)., We thank the team of the Centre of Production and Infection of Anopheles, Institut Pasteur, in particular M. Szatanik, C. Thouvenot, S. Golba, J. Pham and A. Lorthiois for providing mosquitoes and P. falciparum SPZs, the team of the Platform of Dynamic Imaging, Institut Pasteur, in particular Dr S. Shorte and M.-A. Nicola for the access to the confocal microscopes and IVIS system, Dr K. Kim from the Albert Einstein College of Medicine for providing the P. yoelii YM GFP-luciferase, Dr V. Nussenzweig from New York University for providing the P. berghei and falciparumnized P. berghei parasites, Dr M. Soares from the Instituto Gulbenkian for providing the JHT−/− mice, Dr P.-M. Lledo and Dr P. Bruhns from the Institut Pasteur for providing, respectively, the C3−/− and the FcRγ−/− mice, the team of the Clinical Investigation and Access to BioResources, in particular M.-N. Ungeheuer for providing the erythrocytes for the P. falciparum culture, Dr P. Baldacci and Dr P. Formaglio for their critical reading of the manuscript., ANR-14-CE16-0030,IM3alaria,Imagerie et amélioration de la protection immunitaire contre le parasite responsable du paludisme.(2014), ANR-10-LABX-0062,IBEID,Integrative Biology of Emerging Infectious Diseases(2010), ANR-11-LABX-0024,ParaFrap,Alliance française contre les maladies parasitaires(2011), Amino, Rogerio, Appel à projets générique - Imagerie et amélioration de la protection immunitaire contre le parasite responsable du paludisme. - - IM3alaria2014 - ANR-14-CE16-0030 - Appel à projets générique - VALID, Integrative Biology of Emerging Infectious Diseases - - IBEID2010 - ANR-10-LABX-0062 - LABX - VALID, Laboratoires d'excellence - Alliance française contre les maladies parasitaires - - ParaFrap2011 - ANR-11-LABX-0024 - LABX - VALID, Institut Pasteur [Paris], Universidade do Porto, Universidade de São Paulo (USP)-Universidade de São Paulo (USP), Centre d'Immunologie et de Maladies Infectieuses (CIMI), Ehime University [Matsuyama], and Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS)

Subjects
0301 basic medicine, MESH: Antibodies, Protozoan/pharmacology, Plasmodium berghei, [SDV]Life Sciences [q-bio], Fc receptor, Protozoan Proteins, MESH: Antibodies, Monoclonal/pharmacology, Antibodies, Protozoan, Applied Microbiology and Biotechnology, MESH: Cell Movement/drug effects, Mice, MESH: Protozoan Proteins/immunology, Cell Movement, MESH: Animals, MESH: Plasmodium falciparum/immunology, Skin, MESH: Pore Forming Cytotoxic Proteins/metabolism, MESH: Sporozoites/cytology, biology, Antibodies, Monoclonal, 3. Good health, Circumsporozoite protein, MESH: Sporozoites/immunology, [SDV] Life Sciences [q-bio], [SDV.IMM.IA]Life Sciences [q-bio]/Immunology/Adaptive immunology, Sporozoites, MESH: Skin/parasitology, MESH: Plasmodium berghei/immunology, [SDV.IMM.IA] Life Sciences [q-bio]/Immunology/Adaptive immunology, MESH: Plasmodium yoelii/cytology, MESH: Malaria/immunology, [SDV.IMM]Life Sciences [q-bio]/Immunology, Female, Antibody, Plasmodium yoelii, Microbiology (medical), Pore Forming Cytotoxic Proteins, [SDV.IMM] Life Sciences [q-bio]/Immunology, medicine.drug_class, Immunology, Plasmodium falciparum, MESH: Plasmodium yoelii/immunology, Monoclonal antibody, complex mixtures, Microbiology, 03 medical and health sciences, parasitic diseases, Genetics, medicine, Animals, MESH: Mice, fungi, Cell Biology, biology.organism_classification, Malaria, 030104 developmental biology, Culicidae, Humoral immunity, biology.protein, MESH: Culicidae, MESH: Female
Abstract

The circumsporozoite protein (CSP) is the major surface protein of malaria sporozoites (SPZs), the motile and invasive parasite stage inoculated in the host skin by infected mosquitoes. Antibodies against the central CSP repeats of different plasmodial species are known to block SPZ infectivity1–5, but the precise mechanism by which these effectors operate is not completely understood. Here, using a rodent Plasmodium yoelii malaria model, we show that sterile protection mediated by anti-P. yoelii CSP humoral immunity depends on the parasite inoculation into the host skin, where antibodies inhibit motility and kill P. yoelii SPZs via a characteristic ‘dotty death’ phenotype. Passive transfer of an anti-repeat monoclonal antibody (mAb) recapitulates the skin inoculation-dependent protection, in a complement- and Fc receptor γ-independent manner. This purified mAb also decreases motility and, notably, induces the dotty death of P. yoelii SPZs in vitro. Cytotoxicity is species-transcendent since cognate anti-CSP repeat mAbs also kill Plasmodium berghei and Plasmodium falciparum SPZs. mAb cytotoxicity requires the actomyosin motor-dependent translocation and stripping of the protective CSP surface coat, rendering the parasite membrane susceptible to the SPZ pore-forming-like protein secreted to wound and traverse the host cell membrane6. The loss of SPZ fitness caused by anti-P. yoelii CSP repeat antibodies is thus a dynamic process initiated in the host skin where SPZs either stop moving7, or migrate and traverse cells to progress through the host tissues7–9 at the eventual expense of their own life. In a rodent malaria model, antibodies against the CSP protein that coats sporozoites lead to Plasmodium yoelii killing in the skin in a process that involves stripping off the CSP coat, rendering parasites susceptible to pore-forming-like proteins.

Published
2018

2. Development of the malaria parasite in the skin of the mammalian host

Author

Blandine Franke-Fayard, Robert Ménard, Chris J. Janse, Pascale Gueirard, Geneviève Milon, Florence Bernex, Sabine Thiberge, Joana Tavares, Tomoko Ishino, Rogerio Amino, Biologie et Génétique du Paludisme, Institut Pasteur [Paris], Génétique fonctionnelle et médicale (GFM - ENVA), École nationale vétérinaire d'Alfort (ENVA)-Institut National de la Recherche Agronomique (INRA), Laboratoire d'Anatomie Pathologique, École nationale vétérinaire d'Alfort (ENVA), Immunophysiologie et Parasitisme Intracellulaire, Center for Infectious Diseases [LUMC, Leiden] (CID), Leiden University Medical Center (LUMC), We acknowledge funding from Fundação para a Ciência e Tecnologia Grant SFRH/BPD/48340/2008 (to J.T.) and Institut Pasteur, Natixis, the BioMalPar European Network of Excellence, the Agence Nationale pour la Recherche, and the Howard Hughes Medical Institute (to R.M.)., We thank Stéphane Vincent (Institut Pasteur) and Mitinori Saitou (Riken Center for Developmental Biology) for the kind gift of Blimp1-GFP mice. We thank Spencer Shorte, Marie Nguyen-de Bernon, and Marie-Anne Nicola and the Imagopole team (Institut Pasteur) for help with microscopy, cytometry, and bioluminescence, Catherine Bourgouin, Isabelle Thiéry and the other members of the CEPIA platform (Institut Pasteur) for rearing mosquitoes, Masao Yuda (Mie University) for the gift of anti-HSP70 antibodies, Stephan Kappe (Seattle Biomedical Research Institute) for the gift of anti-UIS4 antibodies, and Jean-Jacques Panthier and Geneviève Aubin-Houzelstein (Institut Pasteur) for helpful discussions., Institut National de la Recherche Agronomique (INRA)-École nationale vétérinaire d'Alfort (ENVA), Institut Pasteur [Paris] (IP), École nationale vétérinaire - Alfort (ENVA)-Institut National de la Recherche Agronomique (INRA), École nationale vétérinaire - Alfort (ENVA), and Universiteit Leiden-Universiteit Leiden

Subjects
Plasmodium, Plasmodium berghei, MESH: Plasmodium yoelii/pathogenicity, Schizogony, Mice, 0302 clinical medicine, MESH: Anopheles/parasitology, MESH: Hair Follicle/parasitology, MESH: Dermis/parasitology, Parasite hosting, MESH: Animals, Skin, 0303 health sciences, Multidisciplinary, biology, integumentary system, MESH: Malaria/transmission, MESH: Merozoites/growth & development, Anopheles, Dermis, Biological Sciences, 3. Good health, medicine.anatomical_structure, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, Sporozoites, MESH: Skin/parasitology, MESH: Plasmodium berghei/pathogenicity, intravital imaging Plasmodium schizogony plasmodium-berghei vaccine development sporozoites liver hepatocyte falciparum infection mosquito protein blimp1, Hair Follicle, Plasmodium yoelii, MESH: Plasmodium berghei/genetics, Green Fluorescent Proteins, 030231 tropical medicine, MESH: Host-Parasite Interactions, MESH: Mice, Hairless, Host-Parasite Interactions, 03 medical and health sciences, MESH: Mice, Inbred C57BL, parasitic diseases, schizogony, medicine, Animals, MESH: Mice, MESH: Malaria/parasitology, 030304 developmental biology, Mice, Hairless, Merozoites, MESH: Plasmodium berghei/growth & development, MESH: Green Fluorescent Proteins/genetics, MESH: Plasmodium yoelii/growth & development, medicine.disease, biology.organism_classification, MESH: Plasmodium yoelii/genetics, Virology, Malaria, Mice, Inbred C57BL, MESH: Epidermis/parasitology, MESH: Sporozoites/growth & development, intravital imaging, Epidermis
Abstract

The first step of Plasmodium development in vertebrates is the transformation of the sporozoite, the parasite stage injected by the mosquito in the skin, into merozoites, the stage that invades erythrocytes and initiates the disease. The current view is that, in mammals, this stage conversion occurs only inside hepatocytes. Here, we document the transformation of sporozoites of rodent-infecting Plasmodium into merozoites in the skin of mice. After mosquito bite, ∼50% of the parasites remain in the skin, and at 24 h ∼10% are developing in the epidermis and the dermis, as well as in the immunoprivileged hair follicles where they can survive for weeks. The parasite developmental pathway in skin cells, although frequently abortive, leads to the generation of merozoites that are infective to erythrocytes and are released via merosomes, as typically observed in the liver. Therefore, during malaria in rodents, the skin is not just the route to the liver but is also the final destination for many inoculated parasites, where they can differentiate into merozoites and possibly persist.

Published
2010

3. Host Cell Traversal Is Important for Progression of the Malaria Parasite through the Dermis to the Liver

Author

Robert Ménard, Tomoko Ishino, Bertrand Boisson, Jean-François Dubremetz, Sabine Thiberge, Marie-Christine Prévost, Rogerio Amino, Masao Yuda, Donatella Giovannini, Pascale Gueirard, Biologie et Génétique du Paludisme, Institut Pasteur [Paris], Federal University of Sao Paulo (Unifesp), Dynamique moléculaire des interactions membranaires (DMIM), Centre National de la Recherche Scientifique (CNRS)-Université Montpellier 2 - Sciences et Techniques (UM2), Microscopie électronique (Plate-forme), Mie University Graduate School / Faculty of Medicine [Japan], Mie University, This work was supported by funds from the Institut Pasteur ('Grand Programme Horizontal Anopheles'), the Howard Hughes Medical Institute, the European Commission (FP6 BioMalPar Network of Excellence), and the Core Research for Evolutional Science and Technology (CREST). R.A. was supported by the Pasteur Institute GPH fellowship, D.G. is a BioMalPar Ph.D. student, T.I. was supported by a fellowship from the Association Pasteur-Japon, M.Y. is a CREST Scholar, and R.M. is a Howard Hughes Medical Institute International Scholar., We thank S. Shorte, P. Roux, and the other members of the 'Platforme d'imagerie dynamique' (Institut Pasteur) for help with confocal microscopy, C. Bourgouin, I. Thiéry, and the other members of the 'Centre de Production et d'Infection des Anophèles' (Institut Pasteur) for mosquito rearing, V. Richard from the Electron Microscopy Facility (University of Montpellier 2), G. Milon, G. Lauvau, and T. Graf for providing the lys-gfp mice, and Patricia Baldacci and Samantha Blazquez for comments on the manuscript., Institut Pasteur [Paris] (IP), and Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Cancer Research, MESH: Sporozoites/chemistry, MICROBIO, Plasmodium berghei, MESH: Mice, Inbred C57BL/parasitology, Cell, Protozoan Proteins, HUMDISEASE, MESH: Sporozoites/pathology, Vacuole, MESH: Virulence, Mice, MESH: Anopheles/parasitology, MESH: Dermis/metabolism, Cell Movement, Parasite hosting, MESH: Animals, MESH: Protozoan Proteins/physiology, MESH: Cell Movement, Cells, Cultured, MESH: Plasmodium berghei/pathogenicity, 0303 health sciences, MESH: Pore Forming Cytotoxic Proteins, biology, Virulence, MESH: Malaria/parasitology, Dermis, 3. Good health, Cell biology, medicine.anatomical_structure, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, Liver, Sporozoites, Hepatocyte, Female, Intracellular, MESH: Sporozoites/metabolism, MESH: Cells, Cultured, Pore Forming Cytotoxic Proteins, MESH: Rats, MESH: Plasmodium berghei/metabolism, Microbiology, 03 medical and health sciences, In vivo, Virology, Immunology and Microbiology(all), Anopheles, medicine, Animals, Point Mutation, Rats, Wistar, Molecular Biology, MESH: Mice, 030304 developmental biology, MESH: Point Mutation, 030306 microbiology, MESH: Plasmodium berghei/chemistry, biology.organism_classification, Malaria, Rats, Mice, Inbred C57BL, Parasitology, CELLBIO, MESH: Liver/parasitology, MESH: Female, MESH: Rats, Wistar/parasitology
Abstract

International audience; The malaria sporozoite, the parasite stage transmitted by the mosquito, is delivered into the dermis and differentiates in the liver. Motile sporozoites can invade host cells by disrupting their plasma membrane and migrating through them (termed cell traversal), or by forming a parasite-cell junction and settling inside an intracellular vacuole (termed cell infection). Traversal of liver cells, observed for sporozoites in vivo, is thought to activate the sporozoite for infection of a final hepatocyte. Here, using Plasmodium berghei, we show that cell traversal is important in the host dermis for preventing sporozoite destruction by phagocytes and arrest by nonphagocytic cells. We also show that cell infection is a pathway that is masked, rather than activated, by cell traversal. We propose that the cell traversal activity of the sporozoite must be turned on for progression to the liver parenchyma, where it must be switched off for infection of a final hepatocyte.

Published
2008

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