Comprehensive analysis of early T cell responses to acute Zika Virus infection during the first epidemic in Bahia, Brazil.


Journal

PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081

Informations de publication

Date de publication:
2024
Historique:
received: 27 11 2023
accepted: 05 04 2024
medline: 10 5 2024
pubmed: 10 5 2024
entrez: 9 5 2024
Statut: epublish

Résumé

In most cases, Zika virus (ZIKV) causes a self-limited acute illness in adults, characterized by mild clinical symptoms that resolve within a few days. Immune responses, both innate and adaptive, play a central role in controlling and eliminating virus-infected cells during the early stages of infection. To test the hypothesis that circulating T cells exhibit phenotypic and functional activation characteristics during the viremic phase of ZIKV infection. A comprehensive analysis using mass cytometry was performed on peripheral blood mononuclear cells obtained from patients with acute ZIKV infection (as confirmed by RT-PCR) and compared with that from healthy donors (HD). The frequency of IFN-γ-producing T cells in response to peptide pools covering immunogenic regions of structural and nonstructural ZIKV proteins was quantified using an ELISpot assay. Circulating CD4+ and CD8+ T lymphocytes from ZIKV-infected patients expressed higher levels of IFN-γ and pSTAT-5, as well as cell surface markers associated with proliferation (Ki-67), activation ((HLA-DR, CD38) or exhaustion (PD1 and CTLA-4), compared to those from HD. Activation of CD4+ and CD8+ memory T cell subsets, including Transitional Memory T Cells (TTM), Effector Memory T cells (TEM), and Effector Memory T cells Re-expressing CD45RA (TEMRA), was prominent among CD4+ T cell subset of ZIKV-infected patients and was associated with increased levels of IFN-γ, pSTAT-5, Ki-67, CTLA-4, and PD1, as compared to HD. Additionally, approximately 30% of ZIKV-infected patients exhibited a T cell response primarily directed against the ZIKV NS5 protein. Circulating T lymphocytes spontaneously produce IFN-γ and express elevated levels of pSTAT-5 during the early phase of ZIKV infection whereas recognition of ZIKV antigen results in the generation of virus-specific IFN-γ-producing T cells.

Sections du résumé

BACKGROUND BACKGROUND
In most cases, Zika virus (ZIKV) causes a self-limited acute illness in adults, characterized by mild clinical symptoms that resolve within a few days. Immune responses, both innate and adaptive, play a central role in controlling and eliminating virus-infected cells during the early stages of infection.
AIM OBJECTIVE
To test the hypothesis that circulating T cells exhibit phenotypic and functional activation characteristics during the viremic phase of ZIKV infection.
METHODS METHODS
A comprehensive analysis using mass cytometry was performed on peripheral blood mononuclear cells obtained from patients with acute ZIKV infection (as confirmed by RT-PCR) and compared with that from healthy donors (HD). The frequency of IFN-γ-producing T cells in response to peptide pools covering immunogenic regions of structural and nonstructural ZIKV proteins was quantified using an ELISpot assay.
RESULTS RESULTS
Circulating CD4+ and CD8+ T lymphocytes from ZIKV-infected patients expressed higher levels of IFN-γ and pSTAT-5, as well as cell surface markers associated with proliferation (Ki-67), activation ((HLA-DR, CD38) or exhaustion (PD1 and CTLA-4), compared to those from HD. Activation of CD4+ and CD8+ memory T cell subsets, including Transitional Memory T Cells (TTM), Effector Memory T cells (TEM), and Effector Memory T cells Re-expressing CD45RA (TEMRA), was prominent among CD4+ T cell subset of ZIKV-infected patients and was associated with increased levels of IFN-γ, pSTAT-5, Ki-67, CTLA-4, and PD1, as compared to HD. Additionally, approximately 30% of ZIKV-infected patients exhibited a T cell response primarily directed against the ZIKV NS5 protein.
CONCLUSION CONCLUSIONS
Circulating T lymphocytes spontaneously produce IFN-γ and express elevated levels of pSTAT-5 during the early phase of ZIKV infection whereas recognition of ZIKV antigen results in the generation of virus-specific IFN-γ-producing T cells.

Identifiants

pubmed: 38722858
doi: 10.1371/journal.pone.0302684
pii: PONE-D-23-37988
doi:

Substances chimiques

Interferon-gamma 82115-62-6

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0302684

Informations de copyright

Copyright: © 2024 Samri et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Auteurs

Assia Samri (A)

Sorbonne-Université, Inserm 1135, CNRS ERL8255, Centre d'immunologie et des Maladies Infectieuses, Cimi, Paris, France.

Antonio Carlos Bandeira (AC)

Secretaria de Saúde da Bahia, Salvador, Bahia, Brazil.
Instituto Gonçalo Moniz, Fundação Oswaldo Cruz (FIOCRUZ), Salvador, Brazil.

Luana Leandro Gois (LL)

Instituto Gonçalo Moniz, Fundação Oswaldo Cruz (FIOCRUZ), Salvador, Brazil.
Escola Bahiana de Medicina e Saúde Pública (EBMSP), Salvador, Brazil.
Departamento de Biointeração, Instituto de Ciências da Saúde, Universidade Federal da Bahia, Salvador, Brazil.

Carlos Gustavo Regis Silva (CGR)

Escola Bahiana de Medicina e Saúde Pública (EBMSP), Salvador, Brazil.

Alice Rousseau (A)

Sorbonne-Université, Inserm 1135, CNRS ERL8255, Centre d'immunologie et des Maladies Infectieuses, Cimi, Paris, France.

Aurelien Corneau (A)

Faculté de Médecine Pierre et Marie Curie, Plateforme de Cytométrie (CyPS), UMS30-LUMIC, Paris, France.

Nadine Tarantino (N)

Sorbonne-Université, Inserm 1135, CNRS ERL8255, Centre d'immunologie et des Maladies Infectieuses, Cimi, Paris, France.

Christopher Maucourant (C)

Sorbonne-Université, Inserm 1135, CNRS ERL8255, Centre d'immunologie et des Maladies Infectieuses, Cimi, Paris, France.

Gabriel Andrade Nonato Queiroz (GAN)

Instituto Gonçalo Moniz, Fundação Oswaldo Cruz (FIOCRUZ), Salvador, Brazil.
Escola Bahiana de Medicina e Saúde Pública (EBMSP), Salvador, Brazil.

Vincent Vieillard (V)

Sorbonne-Université, Inserm 1135, CNRS ERL8255, Centre d'immunologie et des Maladies Infectieuses, Cimi, Paris, France.

Hans Yssel (H)

Sorbonne-Université, Inserm 1135, CNRS ERL8255, Centre d'immunologie et des Maladies Infectieuses, Cimi, Paris, France.

Gubio Soares Campos (GS)

Departamento de Biointeração, Instituto de Ciências da Saúde, Universidade Federal da Bahia, Salvador, Brazil.

Silvia Sardi (S)

Departamento de Biointeração, Instituto de Ciências da Saúde, Universidade Federal da Bahia, Salvador, Brazil.

Brigitte Autran (B)

Sorbonne-Université, Inserm 1135, CNRS ERL8255, Centre d'immunologie et des Maladies Infectieuses, Cimi, Paris, France.

Maria Fernanda Rios Grassi (MF)

Instituto Gonçalo Moniz, Fundação Oswaldo Cruz (FIOCRUZ), Salvador, Brazil.
Escola Bahiana de Medicina e Saúde Pública (EBMSP), Salvador, Brazil.

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