Monocytes and Macrophages, Targets of Severe Acute Respiratory Syndrome Coronavirus 2: The Clue for Coronavirus Disease 2019 Immunoparalysis.


Journal

The Journal of infectious diseases
ISSN: 1537-6613
Titre abrégé: J Infect Dis
Pays: United States
ID NLM: 0413675

Informations de publication

Date de publication:
02 08 2021
Historique:
received: 13 10 2020
accepted: 22 01 2021
pubmed: 26 1 2021
medline: 10 8 2021
entrez: 25 1 2021
Statut: ppublish

Résumé

Coronavirus disease 2019 (COVID-19) clinical expression is pleiomorphic, severity is related to age and comorbidities such as diabetes and hypertension, and pathophysiology involves aberrant immune activation and lymphopenia. We wondered if the myeloid compartment was affected during COVID-19 and if monocytes and macrophages could be infected by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Monocytes and monocyte-derived macrophages (MDMs) from COVID-19 patients and controls were infected with SARS-CoV-2 and extensively investigated with immunofluorescence, viral RNA extraction and quantification, and total RNA extraction followed by reverse-transcription quantitative polymerase chain reaction using specific primers, supernatant cytokines (interleukins 6, 10, and 1β; interferon-β; transforming growth factor-β1, and tumor necrosis factor-α), and flow cytometry. The effect of M1- vs M2-type or no polarization prior to infection was assessed. SARS-CoV-2 efficiently infected monocytes and MDMs, but their infection is abortive. Infection was associated with immunoregulatory cytokines secretion and the induction of a macrophagic specific transcriptional program characterized by the upregulation of M2-type molecules. In vitro polarization did not account for permissivity to SARS-CoV-2, since M1- and M2-type MDMs were similarly infected. In COVID-19 patients, monocytes exhibited lower counts affecting all subsets, decreased expression of HLA-DR, and increased expression of CD163, irrespective of severity. SARS-CoV-2 drives monocytes and macrophages to induce host immunoparalysis for the benefit of COVID-19 progression.SARS-CoV-2 infection of macrophages induces a specific M2 transcriptional program. In Covid-19 patients, monocyte subsets were decreased associated with up-expression of the immunoregulatory molecule CD163 suggesting that SARS-CoV-2 drives immune system for the benefit of Covid-19 disease progression.

Sections du résumé

BACKGROUND
Coronavirus disease 2019 (COVID-19) clinical expression is pleiomorphic, severity is related to age and comorbidities such as diabetes and hypertension, and pathophysiology involves aberrant immune activation and lymphopenia. We wondered if the myeloid compartment was affected during COVID-19 and if monocytes and macrophages could be infected by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2).
METHODS
Monocytes and monocyte-derived macrophages (MDMs) from COVID-19 patients and controls were infected with SARS-CoV-2 and extensively investigated with immunofluorescence, viral RNA extraction and quantification, and total RNA extraction followed by reverse-transcription quantitative polymerase chain reaction using specific primers, supernatant cytokines (interleukins 6, 10, and 1β; interferon-β; transforming growth factor-β1, and tumor necrosis factor-α), and flow cytometry. The effect of M1- vs M2-type or no polarization prior to infection was assessed.
RESULTS
SARS-CoV-2 efficiently infected monocytes and MDMs, but their infection is abortive. Infection was associated with immunoregulatory cytokines secretion and the induction of a macrophagic specific transcriptional program characterized by the upregulation of M2-type molecules. In vitro polarization did not account for permissivity to SARS-CoV-2, since M1- and M2-type MDMs were similarly infected. In COVID-19 patients, monocytes exhibited lower counts affecting all subsets, decreased expression of HLA-DR, and increased expression of CD163, irrespective of severity.
CONCLUSIONS
SARS-CoV-2 drives monocytes and macrophages to induce host immunoparalysis for the benefit of COVID-19 progression.SARS-CoV-2 infection of macrophages induces a specific M2 transcriptional program. In Covid-19 patients, monocyte subsets were decreased associated with up-expression of the immunoregulatory molecule CD163 suggesting that SARS-CoV-2 drives immune system for the benefit of Covid-19 disease progression.

Identifiants

pubmed: 33493287
pii: 6119539
doi: 10.1093/infdis/jiab044
pmc: PMC7928817
doi:

Substances chimiques

Cytokines 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

395-406

Subventions

Organisme : Fondation Méditerranée Infection
Organisme : Fondation pour la Recherche Médicale

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press for the Infectious Diseases Society of America. All rights reserved. For permissions, e-mail: journals.permissions@oup.com.

Auteurs

Asma Boumaza (A)

Aix-Marseille Université, Institut de recherche pour le développement, Assitance publique-hopitaux de Marseille, Microbe, Phylogeny and infection, Marseille, France.
Institut hospitalo-universitaire Méditerranée infection, Marseille, France.

Laetitia Gay (L)

Aix-Marseille Université, Institut de recherche pour le développement, Assitance publique-hopitaux de Marseille, Microbe, Phylogeny and infection, Marseille, France.
Institut hospitalo-universitaire Méditerranée infection, Marseille, France.
ImCheck Therapeutics, Marseille, France.

Soraya Mezouar (S)

Aix-Marseille Université, Institut de recherche pour le développement, Assitance publique-hopitaux de Marseille, Microbe, Phylogeny and infection, Marseille, France.
Institut hospitalo-universitaire Méditerranée infection, Marseille, France.

Eloïne Bestion (E)

Aix-Marseille Université, Institut de recherche pour le développement, Assitance publique-hopitaux de Marseille, Microbe, Phylogeny and infection, Marseille, France.
Institut hospitalo-universitaire Méditerranée infection, Marseille, France.
Genoscience Pharma, Marseille, France.

Aïssatou Bailo Diallo (AB)

Aix-Marseille Université, Institut de recherche pour le développement, Assitance publique-hopitaux de Marseille, Microbe, Phylogeny and infection, Marseille, France.
Institut hospitalo-universitaire Méditerranée infection, Marseille, France.

Moise Michel (M)

Aix-Marseille Université, Institut de recherche pour le développement, Assitance publique-hopitaux de Marseille, Microbe, Phylogeny and infection, Marseille, France.
Institut hospitalo-universitaire Méditerranée infection, Marseille, France.

Benoit Desnues (B)

Aix-Marseille Université, Institut de recherche pour le développement, Assitance publique-hopitaux de Marseille, Microbe, Phylogeny and infection, Marseille, France.
Institut hospitalo-universitaire Méditerranée infection, Marseille, France.

Didier Raoult (D)

Aix-Marseille Université, Institut de recherche pour le développement, Assitance publique-hopitaux de Marseille, Microbe, Phylogeny and infection, Marseille, France.
Institut hospitalo-universitaire Méditerranée infection, Marseille, France.

Bernard La Scola (B)

Aix-Marseille Université, Institut de recherche pour le développement, Assitance publique-hopitaux de Marseille, Microbe, Phylogeny and infection, Marseille, France.
Institut hospitalo-universitaire Méditerranée infection, Marseille, France.

Philippe Halfon (P)

Aix-Marseille Université, Institut de recherche pour le développement, Assitance publique-hopitaux de Marseille, Microbe, Phylogeny and infection, Marseille, France.
Institut hospitalo-universitaire Méditerranée infection, Marseille, France.
ImCheck Therapeutics, Marseille, France.

Joana Vitte (J)

Aix-Marseille Université, Institut de recherche pour le développement, Assitance publique-hopitaux de Marseille, Microbe, Phylogeny and infection, Marseille, France.
Institut hospitalo-universitaire Méditerranée infection, Marseille, France.

Daniel Olive (D)

Centre de recherche en cancérologie de Marseille, Inserm Unité mixte de recherche 1068, Centre National de la Recherche Scientifique Unité mixte de recherche 7258, Institut Paoli Calmettes, Marseille, France.

Jean-Louis Mege (JL)

Aix-Marseille Université, Institut de recherche pour le développement, Assitance publique-hopitaux de Marseille, Microbe, Phylogeny and infection, Marseille, France.
Institut hospitalo-universitaire Méditerranée infection, Marseille, France.
Aix-Marseille Université, Assistance publique-hoptiaux de Marseille, Hopital de la Conception, Laboratoire d'Immunologie, Marseille, France.

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