Interplay between liver and blood stages of Plasmodium infection dictates malaria severity via γδ T cells and IL-17-promoted stress erythropoiesis
| Autor(a) principal: | |
|---|---|
| Data de Publicação: | 2023 |
| Outros Autores: | , , , , , , , , , , , , , |
| Tipo de documento: | Artigo |
| Idioma: | eng |
| Título da fonte: | Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
| Texto Completo: | http://hdl.handle.net/10451/56786 |
Resumo: | © 2023 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). |
| id |
RCAP_b93c15a7c371138d45ba582cee9c344a |
|---|---|
| oai_identifier_str |
oai:repositorio.ul.pt:10451/56786 |
| network_acronym_str |
RCAP |
| network_name_str |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
| repository_id_str |
7160 |
| spelling |
Interplay between liver and blood stages of Plasmodium infection dictates malaria severity via γδ T cells and IL-17-promoted stress erythropoiesisIL-17Plasmodium infectionAcquired immunityCerebral malariaGamma-delta T cellsMalariaReticulocytesSplenic erythropoiesis© 2023 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).Plasmodium replicates within the liver prior to reaching the bloodstream and infecting red blood cells. Because clinical manifestations of malaria only arise during the blood stage of infection, a perception exists that liver infection does not impact disease pathology. By developing a murine model where the liver and blood stages of infection are uncoupled, we showed that the integration of signals from both stages dictated mortality outcomes. This dichotomy relied on liver stage-dependent activation of Vγ4+ γδ T cells. Subsequent blood stage parasite loads dictated their cytokine profiles, where low parasite loads preferentially expanded IL-17-producing γδ T cells. IL-17 drove extra-medullary erythropoiesis and concomitant reticulocytosis, which protected mice from lethal experimental cerebral malaria (ECM). Adoptive transfer of erythroid precursors could rescue mice from ECM. Modeling of γδ T cell dynamics suggests that this protective mechanism may be key for the establishment of naturally acquired malaria immunity among frequently exposed individuals.We would like to acknowledge Freddy Frischknecht (Integrative Parasitology Center for Infectious Diseases, Heidelberg) for providing the Plasmodium berghei lisp2− parasite line, Immo Prinz (Hannover Medical School, Hannover) for providing genetically modified mouse lines, Ana Parreira (iMM-JLA, Portugal) and Geoff McFadden’s lab (School of BioSciences, University of Melbourne, Australia) for mosquito rearing and infection with Plasmodium parasites, Helena Pinheiro (iMM-JLA, Portugal) for assistance with graphical design, Inês Bento and Miguel Prudêncio for critically reviewing this manuscript, and the Flow Cytometry and Rodent Facilities teams (iMM-JLA, Portugal) for their assistance. Work at iMM-JLA was supported by Fundação para a Ciência e a Tecnologia. Portugal (PTDC/MED-IMU/28664/2017) and the “La caixa” Banking Foundation, Spain (HR17-00264-PoEMM) grants attributed to Â.F.C. and M.M.M., respectively. Work at the Department of Microbiology and Immunology, The University of Melbourne, Australia, was funded by the National Health and Medical Research Council, Australia (1113293, 1154457) and the Australian Research Council, Australia (CE140100011). Â.F.C., S.M., J.L.G., M.I.M., R.M.R., and K.S. were supported by Fundação para a Ciência e a Tecnologia, Portugal (DL57/2016/CP1451/CT0004, DL57/2016/CP1451/CT0010, PD/BD/139053/2018, PD/BD/135454/2017, PTDC/MAT-APL/31602/2017, and CEECIND/00697/2018, respectively), P.L. was supported by Conselho Nacional de Desenvolvimento Científico e Tenológico, Brazil (SN/CGEFO/CNPQ 201801/2015-9), and A.T.T. was supported in part by Alfred P. Sloan Foundation Fellowship (FG-2020-12949).ElsevierRepositório da Universidade de LisboaChora, Ângelo FerreiraMarques, SofiaLisboa Gonçalves, JoanaLima, PriscilaGomes Da Costa, DanielFernandez-Ruiz, DanielMarreiros, Maria InêsRuivo, PedroCarvalho, TâniaRibeiro, Ruy M.Serre, KarineHeath, William R.Silva-Santos, BrunoTate, Ann T.Mota, Maria M.2023-03-23T14:51:11Z20232023-01-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10451/56786engImmunity. 2023 Mar 14;56(3):592-605.e81074-761310.1016/j.immuni.2023.01.0311097-4180info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2024-11-20T18:20:23Zoai:repositorio.ul.pt:10451/56786Portal AgregadorONGhttps://www.rcaap.pt/oai/openairemluisa.alvim@gmail.comopendoar:71602024-11-20T18:20:23Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse |
| dc.title.none.fl_str_mv |
Interplay between liver and blood stages of Plasmodium infection dictates malaria severity via γδ T cells and IL-17-promoted stress erythropoiesis |
| title |
Interplay between liver and blood stages of Plasmodium infection dictates malaria severity via γδ T cells and IL-17-promoted stress erythropoiesis |
| spellingShingle |
Interplay between liver and blood stages of Plasmodium infection dictates malaria severity via γδ T cells and IL-17-promoted stress erythropoiesis Chora, Ângelo Ferreira IL-17 Plasmodium infection Acquired immunity Cerebral malaria Gamma-delta T cells Malaria Reticulocytes Splenic erythropoiesis |
| title_short |
Interplay between liver and blood stages of Plasmodium infection dictates malaria severity via γδ T cells and IL-17-promoted stress erythropoiesis |
| title_full |
Interplay between liver and blood stages of Plasmodium infection dictates malaria severity via γδ T cells and IL-17-promoted stress erythropoiesis |
| title_fullStr |
Interplay between liver and blood stages of Plasmodium infection dictates malaria severity via γδ T cells and IL-17-promoted stress erythropoiesis |
| title_full_unstemmed |
Interplay between liver and blood stages of Plasmodium infection dictates malaria severity via γδ T cells and IL-17-promoted stress erythropoiesis |
| title_sort |
Interplay between liver and blood stages of Plasmodium infection dictates malaria severity via γδ T cells and IL-17-promoted stress erythropoiesis |
| author |
Chora, Ângelo Ferreira |
| author_facet |
Chora, Ângelo Ferreira Marques, Sofia Lisboa Gonçalves, Joana Lima, Priscila Gomes Da Costa, Daniel Fernandez-Ruiz, Daniel Marreiros, Maria Inês Ruivo, Pedro Carvalho, Tânia Ribeiro, Ruy M. Serre, Karine Heath, William R. Silva-Santos, Bruno Tate, Ann T. Mota, Maria M. |
| author_role |
author |
| author2 |
Marques, Sofia Lisboa Gonçalves, Joana Lima, Priscila Gomes Da Costa, Daniel Fernandez-Ruiz, Daniel Marreiros, Maria Inês Ruivo, Pedro Carvalho, Tânia Ribeiro, Ruy M. Serre, Karine Heath, William R. Silva-Santos, Bruno Tate, Ann T. Mota, Maria M. |
| author2_role |
author author author author author author author author author author author author author author |
| dc.contributor.none.fl_str_mv |
Repositório da Universidade de Lisboa |
| dc.contributor.author.fl_str_mv |
Chora, Ângelo Ferreira Marques, Sofia Lisboa Gonçalves, Joana Lima, Priscila Gomes Da Costa, Daniel Fernandez-Ruiz, Daniel Marreiros, Maria Inês Ruivo, Pedro Carvalho, Tânia Ribeiro, Ruy M. Serre, Karine Heath, William R. Silva-Santos, Bruno Tate, Ann T. Mota, Maria M. |
| dc.subject.por.fl_str_mv |
IL-17 Plasmodium infection Acquired immunity Cerebral malaria Gamma-delta T cells Malaria Reticulocytes Splenic erythropoiesis |
| topic |
IL-17 Plasmodium infection Acquired immunity Cerebral malaria Gamma-delta T cells Malaria Reticulocytes Splenic erythropoiesis |
| description |
© 2023 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). |
| publishDate |
2023 |
| dc.date.none.fl_str_mv |
2023-03-23T14:51:11Z 2023 2023-01-01T00:00:00Z |
| dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
| dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
| format |
article |
| status_str |
publishedVersion |
| dc.identifier.uri.fl_str_mv |
http://hdl.handle.net/10451/56786 |
| url |
http://hdl.handle.net/10451/56786 |
| dc.language.iso.fl_str_mv |
eng |
| language |
eng |
| dc.relation.none.fl_str_mv |
Immunity. 2023 Mar 14;56(3):592-605.e8 1074-7613 10.1016/j.immuni.2023.01.031 1097-4180 |
| dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
| eu_rights_str_mv |
openAccess |
| dc.format.none.fl_str_mv |
application/pdf |
| dc.publisher.none.fl_str_mv |
Elsevier |
| publisher.none.fl_str_mv |
Elsevier |
| dc.source.none.fl_str_mv |
reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação instacron:RCAAP |
| instname_str |
Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
| instacron_str |
RCAAP |
| institution |
RCAAP |
| reponame_str |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
| collection |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
| repository.name.fl_str_mv |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
| repository.mail.fl_str_mv |
mluisa.alvim@gmail.com |
| _version_ |
1817549226511433728 |