Antibody-dependent immune responses elicited by blood stage-malaria infection contribute to protective immunity to the pre-erythrocytic stages

Advances in transcriptomics and proteomics have revealed that different life-cycle stages of the malaria parasite, Plasmodium, share antigens, thus allowing for the possibility of eliciting immunity to a parasite life-cycle stage that has not been experienced before. Using the Plasmodium chabaudi (A...

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Main Authors: Irene Tumwine-Downey, Katrien Deroost, Prisca Levy, Sarah McLaughlin, Caroline Hosking, Jean Langhorne
Format: Article
Language:English
Published: Elsevier 2023-01-01
Series:Current Research in Immunology
Online Access:http://www.sciencedirect.com/science/article/pii/S2590255522000257
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author Irene Tumwine-Downey
Katrien Deroost
Prisca Levy
Sarah McLaughlin
Caroline Hosking
Jean Langhorne
author_facet Irene Tumwine-Downey
Katrien Deroost
Prisca Levy
Sarah McLaughlin
Caroline Hosking
Jean Langhorne
author_sort Irene Tumwine-Downey
collection DOAJ
description Advances in transcriptomics and proteomics have revealed that different life-cycle stages of the malaria parasite, Plasmodium, share antigens, thus allowing for the possibility of eliciting immunity to a parasite life-cycle stage that has not been experienced before. Using the Plasmodium chabaudi (AS strain) model of malaria in mice, we investigated how isolated exposure to blood-stage infection, bypassing a liver-stage infection, yields significant protection to sporozoite challenge resulting in lower liver parasite burdens. Antibodies are the main immune driver of this protection. Antibodies induced by blood-stage infection recognise proteins on the surface of sporozoites and can impair sporozoite gliding motility in vitro, suggesting a possible function in vivo. Furthermore, mice lacking B cells and/or secreted antibodies are not protected against a sporozoite challenge in mice that had a previous blood-stage infection. Conversely, effector CD4+ and CD8+ T cells do not seem to play a role in protection from sporozoite challenge of mice previously exposed only to the blood stages of P. chabaudi. The protective response against pre-erythrocytic stages can be induced by infections initiated by serially passaged blood-stage parasites as well as recently mosquito transmitted parasites and is effective against a different strain of P. chabaudi (CB strain), but not against another rodent malaria species, P. yoelii. The possibility to induce protective cross-stage antibodies advocates the need to consider both stage-specific and cross-stage immune responses to malaria, as natural infection elicits exposure to all life-cycle stages. Future investigation into these cross-stage antibodies allows the opportunity for candidate antigens to contribute to malaria vaccine development.
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spelling doaj.art-995bee4633f94ac58122874fca25c04b2023-12-03T05:42:47ZengElsevierCurrent Research in Immunology2590-25552023-01-014100054Antibody-dependent immune responses elicited by blood stage-malaria infection contribute to protective immunity to the pre-erythrocytic stagesIrene Tumwine-Downey0Katrien Deroost1Prisca Levy2Sarah McLaughlin3Caroline Hosking4Jean Langhorne5Malaria Immunology Laboratory, Francis Crick Institute, London, NW1 1AT, UKMalaria Immunology Laboratory, Francis Crick Institute, London, NW1 1AT, UKMalaria Immunology Laboratory, Francis Crick Institute, London, NW1 1AT, UKMalaria Immunology Laboratory, Francis Crick Institute, London, NW1 1AT, UKMalaria Immunology Laboratory, Francis Crick Institute, London, NW1 1AT, UKCorresponding author. Malaria Immunology Laboratory, Francis Crick Institute, 1 Midland Road, London, NW1 1AT, UK.; Malaria Immunology Laboratory, Francis Crick Institute, London, NW1 1AT, UKAdvances in transcriptomics and proteomics have revealed that different life-cycle stages of the malaria parasite, Plasmodium, share antigens, thus allowing for the possibility of eliciting immunity to a parasite life-cycle stage that has not been experienced before. Using the Plasmodium chabaudi (AS strain) model of malaria in mice, we investigated how isolated exposure to blood-stage infection, bypassing a liver-stage infection, yields significant protection to sporozoite challenge resulting in lower liver parasite burdens. Antibodies are the main immune driver of this protection. Antibodies induced by blood-stage infection recognise proteins on the surface of sporozoites and can impair sporozoite gliding motility in vitro, suggesting a possible function in vivo. Furthermore, mice lacking B cells and/or secreted antibodies are not protected against a sporozoite challenge in mice that had a previous blood-stage infection. Conversely, effector CD4+ and CD8+ T cells do not seem to play a role in protection from sporozoite challenge of mice previously exposed only to the blood stages of P. chabaudi. The protective response against pre-erythrocytic stages can be induced by infections initiated by serially passaged blood-stage parasites as well as recently mosquito transmitted parasites and is effective against a different strain of P. chabaudi (CB strain), but not against another rodent malaria species, P. yoelii. The possibility to induce protective cross-stage antibodies advocates the need to consider both stage-specific and cross-stage immune responses to malaria, as natural infection elicits exposure to all life-cycle stages. Future investigation into these cross-stage antibodies allows the opportunity for candidate antigens to contribute to malaria vaccine development.http://www.sciencedirect.com/science/article/pii/S2590255522000257
spellingShingle Irene Tumwine-Downey
Katrien Deroost
Prisca Levy
Sarah McLaughlin
Caroline Hosking
Jean Langhorne
Antibody-dependent immune responses elicited by blood stage-malaria infection contribute to protective immunity to the pre-erythrocytic stages
Current Research in Immunology
title Antibody-dependent immune responses elicited by blood stage-malaria infection contribute to protective immunity to the pre-erythrocytic stages
title_full Antibody-dependent immune responses elicited by blood stage-malaria infection contribute to protective immunity to the pre-erythrocytic stages
title_fullStr Antibody-dependent immune responses elicited by blood stage-malaria infection contribute to protective immunity to the pre-erythrocytic stages
title_full_unstemmed Antibody-dependent immune responses elicited by blood stage-malaria infection contribute to protective immunity to the pre-erythrocytic stages
title_short Antibody-dependent immune responses elicited by blood stage-malaria infection contribute to protective immunity to the pre-erythrocytic stages
title_sort antibody dependent immune responses elicited by blood stage malaria infection contribute to protective immunity to the pre erythrocytic stages
url http://www.sciencedirect.com/science/article/pii/S2590255522000257
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