Steroid Hormone Signaling Is Essential to Regulate Innate Immune Cells and Fight Bacterial Infection in Drosophila

Detalhes bibliográficos
Autor(a) principal: Regan, Jennifer C.
Data de Publicação: 2013
Outros Autores: Brandão, Ana S., Leitão, Alexandre B., Mantas Dias, Ângela Raquel, Sucena, Élio, Jacinto, António, Zaidman-Rémy, Anna
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: https://doi.org/10.1371/journal.ppat.1003720
Resumo: This work was supported by PTDC/BIA-BCM/65872/2006 (www.fct.pt) and ERC-AJ208631 (erc.europa.eu) grants (AJ), ARC (www.arc-cancer.net) and FCT SFRH/BPD/44613/2008 (AZR), EMBO ALTF 178-2009 (www.embo.org) (JCR), and the Gulbenkian Institute PhD Program (www.igc.gulbenkian.pt) and FCT SFRH/BD/51175/2010 (ABL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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spelling Steroid Hormone Signaling Is Essential to Regulate Innate Immune Cells and Fight Bacterial Infection in DrosophilaPEPTIDE GENE-EXPRESSIONAPOPTOTIC CELLSPSEUDOMONAS-AERUGINOSAHEMOCYTE MIGRATIONCELLULAR-IMMUNITYMUTANTS REVEALHOST-DEFENSEBLOOD-CELLSPHAGOCYTOSISRECEPTORParasitologyMicrobiologyImmunologyMolecular BiologyGeneticsVirologyThis work was supported by PTDC/BIA-BCM/65872/2006 (www.fct.pt) and ERC-AJ208631 (erc.europa.eu) grants (AJ), ARC (www.arc-cancer.net) and FCT SFRH/BPD/44613/2008 (AZR), EMBO ALTF 178-2009 (www.embo.org) (JCR), and the Gulbenkian Institute PhD Program (www.igc.gulbenkian.pt) and FCT SFRH/BD/51175/2010 (ABL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Coupling immunity and development is essential to ensure survival despite changing internal conditions in the organism. Drosophila metamorphosis represents a striking example of drastic and systemic physiological changes that need to be integrated with the innate immune system. However, nothing is known about the mechanisms that coordinate development and immune cell activity in the transition from larva to adult. Here, we reveal that regulation of macrophage-like cells (hemocytes) by the steroid hormone ecdysone is essential for an effective innate immune response over metamorphosis. Although it is generally accepted that steroid hormones impact immunity in mammals, their action on monocytes (e.g. macrophages and neutrophils) is still not well understood. Here in a simpler model system, we used an approach that allows in vivo, cell autonomous analysis of hormonal regulation of innate immune cells, by combining genetic manipulation with flow cytometry, high-resolution time-lapse imaging and tissue-specific transcriptomic analysis. We show that in response to ecdysone, hemocytes rapidly upregulate actin dynamics, motility and phagocytosis of apoptotic corpses, and acquire the ability to chemotax to damaged epithelia. Most importantly, individuals lacking ecdysone-activated hemocytes are defective in bacterial phagocytosis and are fatally susceptible to infection by bacteria ingested at larval stages, despite the normal systemic and local production of antimicrobial peptides. This decrease in survival is comparable to the one observed in pupae lacking immune cells altogether, indicating that ecdysone-regulation is essential for hemocyte immune functions and survival after infection. Microarray analysis of hemocytes revealed a large set of genes regulated at metamorphosis by EcR signaling, among which many are known to function in cell motility, cell shape or phagocytosis. This study demonstrates an important role for steroid hormone regulation of immunity in vivo in Drosophila, and paves the way for genetic dissection of the mechanisms at work behind steroid regulation of innate immune cells.Centro de Estudos de Doenças Crónicas (CEDOC)NOVA Medical School|Faculdade de Ciências Médicas (NMS|FCM)RUNRegan, Jennifer C.Brandão, Ana S.Leitão, Alexandre B.Mantas Dias, Ângela RaquelSucena, ÉlioJacinto, AntónioZaidman-Rémy, Anna2017-09-14T22:03:00Z2013-102013-10-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/article15application/pdfhttps://doi.org/10.1371/journal.ppat.1003720eng1553-7366PURE: 3129368http://www.scopus.com/inward/record.url?scp=84887276025&partnerID=8YFLogxKhttps://doi.org/10.1371/journal.ppat.1003720info: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:RCAAP2024-03-11T04:11:29Zoai:run.unl.pt:10362/23259Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-20T03:27:43.617636Repositório 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 Steroid Hormone Signaling Is Essential to Regulate Innate Immune Cells and Fight Bacterial Infection in Drosophila
title Steroid Hormone Signaling Is Essential to Regulate Innate Immune Cells and Fight Bacterial Infection in Drosophila
spellingShingle Steroid Hormone Signaling Is Essential to Regulate Innate Immune Cells and Fight Bacterial Infection in Drosophila
Regan, Jennifer C.
PEPTIDE GENE-EXPRESSION
APOPTOTIC CELLS
PSEUDOMONAS-AERUGINOSA
HEMOCYTE MIGRATION
CELLULAR-IMMUNITY
MUTANTS REVEAL
HOST-DEFENSE
BLOOD-CELLS
PHAGOCYTOSIS
RECEPTOR
Parasitology
Microbiology
Immunology
Molecular Biology
Genetics
Virology
title_short Steroid Hormone Signaling Is Essential to Regulate Innate Immune Cells and Fight Bacterial Infection in Drosophila
title_full Steroid Hormone Signaling Is Essential to Regulate Innate Immune Cells and Fight Bacterial Infection in Drosophila
title_fullStr Steroid Hormone Signaling Is Essential to Regulate Innate Immune Cells and Fight Bacterial Infection in Drosophila
title_full_unstemmed Steroid Hormone Signaling Is Essential to Regulate Innate Immune Cells and Fight Bacterial Infection in Drosophila
title_sort Steroid Hormone Signaling Is Essential to Regulate Innate Immune Cells and Fight Bacterial Infection in Drosophila
author Regan, Jennifer C.
author_facet Regan, Jennifer C.
Brandão, Ana S.
Leitão, Alexandre B.
Mantas Dias, Ângela Raquel
Sucena, Élio
Jacinto, António
Zaidman-Rémy, Anna
author_role author
author2 Brandão, Ana S.
Leitão, Alexandre B.
Mantas Dias, Ângela Raquel
Sucena, Élio
Jacinto, António
Zaidman-Rémy, Anna
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Centro de Estudos de Doenças Crónicas (CEDOC)
NOVA Medical School|Faculdade de Ciências Médicas (NMS|FCM)
RUN
dc.contributor.author.fl_str_mv Regan, Jennifer C.
Brandão, Ana S.
Leitão, Alexandre B.
Mantas Dias, Ângela Raquel
Sucena, Élio
Jacinto, António
Zaidman-Rémy, Anna
dc.subject.por.fl_str_mv PEPTIDE GENE-EXPRESSION
APOPTOTIC CELLS
PSEUDOMONAS-AERUGINOSA
HEMOCYTE MIGRATION
CELLULAR-IMMUNITY
MUTANTS REVEAL
HOST-DEFENSE
BLOOD-CELLS
PHAGOCYTOSIS
RECEPTOR
Parasitology
Microbiology
Immunology
Molecular Biology
Genetics
Virology
topic PEPTIDE GENE-EXPRESSION
APOPTOTIC CELLS
PSEUDOMONAS-AERUGINOSA
HEMOCYTE MIGRATION
CELLULAR-IMMUNITY
MUTANTS REVEAL
HOST-DEFENSE
BLOOD-CELLS
PHAGOCYTOSIS
RECEPTOR
Parasitology
Microbiology
Immunology
Molecular Biology
Genetics
Virology
description This work was supported by PTDC/BIA-BCM/65872/2006 (www.fct.pt) and ERC-AJ208631 (erc.europa.eu) grants (AJ), ARC (www.arc-cancer.net) and FCT SFRH/BPD/44613/2008 (AZR), EMBO ALTF 178-2009 (www.embo.org) (JCR), and the Gulbenkian Institute PhD Program (www.igc.gulbenkian.pt) and FCT SFRH/BD/51175/2010 (ABL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
publishDate 2013
dc.date.none.fl_str_mv 2013-10
2013-10-01T00:00:00Z
2017-09-14T22:03:00Z
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 https://doi.org/10.1371/journal.ppat.1003720
url https://doi.org/10.1371/journal.ppat.1003720
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv 1553-7366
PURE: 3129368
http://www.scopus.com/inward/record.url?scp=84887276025&partnerID=8YFLogxK
https://doi.org/10.1371/journal.ppat.1003720
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 15
application/pdf
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
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