Monocytes in sarcoidosis are potent tumour necrosis factor producers and predict disease outcome.


Journal

The European respiratory journal
ISSN: 1399-3003
Titre abrégé: Eur Respir J
Pays: England
ID NLM: 8803460

Informations de publication

Date de publication:
07 2021
Historique:
received: 11 09 2020
accepted: 17 12 2020
pubmed: 16 1 2021
medline: 10 8 2021
entrez: 15 1 2021
Statut: epublish

Résumé

Pulmonary sarcoidosis is an inflammatory disease characterised by granuloma formation and heterogeneous clinical outcome. Tumour necrosis factor (TNF) is a pro-inflammatory cytokine contributing to granuloma formation and high levels of TNF have been shown to associate with progressive disease. Mononuclear phagocytes (MNPs) are potent producers of TNF and highly responsive to inflammation. In sarcoidosis, alveolar macrophages have been well studied. However, MNPs also include monocytes/monocyte-derived cells and dendritic cells, which are poorly studied in sarcoidosis, despite their central role in inflammation. To determine the role of pulmonary monocyte-derived cells and dendritic cells during sarcoidosis. We performed in-depth phenotypic, functional and transcriptomic analysis of MNP subsets from blood and bronchoalveolar lavage (BAL) fluid from 108 sarcoidosis patients and 30 healthy controls. We followed the clinical development of patients and assessed how the repertoire and function of MNP subsets at diagnosis correlated with 2-year disease outcome. Monocytes/monocyte-derived cells were increased in blood and BAL of sarcoidosis patients compared to healthy controls. Interestingly, high frequencies of blood intermediate monocytes at time of diagnosis associated with chronic disease development. RNA sequencing analysis showed highly inflammatory MNPs in BAL of sarcoidosis patients. Furthermore, frequencies of BAL monocytes/monocyte-derived cells producing TNF without exogenous stimulation at time of diagnosis increased in patients that were followed longitudinally. In contrast to alveolar macrophages, the frequency of TNF-producing BAL monocytes/monocyte-derived cells at time of diagnosis was highest in sarcoidosis patients that developed progressive disease. Our data show that pulmonary monocytes/monocyte-derived cells are highly inflammatory and can be used as a predictor of disease outcome in sarcoidosis patients.

Sections du résumé

BACKGROUND
Pulmonary sarcoidosis is an inflammatory disease characterised by granuloma formation and heterogeneous clinical outcome. Tumour necrosis factor (TNF) is a pro-inflammatory cytokine contributing to granuloma formation and high levels of TNF have been shown to associate with progressive disease. Mononuclear phagocytes (MNPs) are potent producers of TNF and highly responsive to inflammation. In sarcoidosis, alveolar macrophages have been well studied. However, MNPs also include monocytes/monocyte-derived cells and dendritic cells, which are poorly studied in sarcoidosis, despite their central role in inflammation.
OBJECTIVE
To determine the role of pulmonary monocyte-derived cells and dendritic cells during sarcoidosis.
METHODS
We performed in-depth phenotypic, functional and transcriptomic analysis of MNP subsets from blood and bronchoalveolar lavage (BAL) fluid from 108 sarcoidosis patients and 30 healthy controls. We followed the clinical development of patients and assessed how the repertoire and function of MNP subsets at diagnosis correlated with 2-year disease outcome.
RESULTS
Monocytes/monocyte-derived cells were increased in blood and BAL of sarcoidosis patients compared to healthy controls. Interestingly, high frequencies of blood intermediate monocytes at time of diagnosis associated with chronic disease development. RNA sequencing analysis showed highly inflammatory MNPs in BAL of sarcoidosis patients. Furthermore, frequencies of BAL monocytes/monocyte-derived cells producing TNF without exogenous stimulation at time of diagnosis increased in patients that were followed longitudinally. In contrast to alveolar macrophages, the frequency of TNF-producing BAL monocytes/monocyte-derived cells at time of diagnosis was highest in sarcoidosis patients that developed progressive disease.
CONCLUSION
Our data show that pulmonary monocytes/monocyte-derived cells are highly inflammatory and can be used as a predictor of disease outcome in sarcoidosis patients.

Identifiants

pubmed: 33446605
pii: 13993003.03468-2020
doi: 10.1183/13993003.03468-2020
pmc: PMC8295505
pii:
doi:

Substances chimiques

Tumor Necrosis Factor-alpha 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright ©The authors 2021.

Déclaration de conflit d'intérêts

Conflict of interest: R. Lepzien has nothing to disclose. Conflict of interest: S. Liu has nothing to disclose. Conflict of interest: P. Czarnewski has nothing to disclose. Conflict of interest: M. Nie has nothing to disclose. Conflict of interest: B. Österberg has nothing to disclose. Conflict of interest: F. Baharom has nothing to disclose. Conflict of interest: J. Pourazar has nothing to disclose. Conflict of interest: G. Rankin has nothing to disclose. Conflict of interest: A. Eklund has nothing to disclose. Conflict of interest: M. Bottai has nothing to disclose. Conflict of interest: S. Kullberg has nothing to disclose. Conflict of interest: A. Blomberg has nothing to disclose. Conflict of interest: J. Grunewald has nothing to disclose. Conflict of interest: A. Smed-Sörensen reports grants from Swedish Heart-Lung Foundation, Swedish Research Council and Karolinska Institutet, during the conduct of the study.

Auteurs

Rico Lepzien (R)

Division of Immunology and Allergy, Dept of Medicine Solna, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden.

Sang Liu (S)

Division of Immunology and Allergy, Dept of Medicine Solna, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden.

Paulo Czarnewski (P)

Dept of Biochemistry and Biophysics, National Bioinformatics Infrastructure Sweden, Science for Life Laboratory, Stockholm University, Stockholm, Sweden.

Mu Nie (M)

Division of Immunology and Allergy, Dept of Medicine Solna, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden.

Björn Österberg (B)

Division of Immunology and Allergy, Dept of Medicine Solna, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden.

Faezzah Baharom (F)

Division of Immunology and Allergy, Dept of Medicine Solna, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden.

Jamshid Pourazar (J)

Dept of Public Health and Clinical Medicine, Division of Medicine, Umeå University, Umeå, Sweden.

Gregory Rankin (G)

Dept of Public Health and Clinical Medicine, Division of Medicine, Umeå University, Umeå, Sweden.

Anders Eklund (A)

Division of Respiratory Medicine, Dept of Medicine Solna and Centre for Molecular Medicine, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden.
Dept of Respiratory Medicine, Theme Inflammation and Infection, Karolinska University Hospital, Stockholm, Sweden.

Matteo Bottai (M)

Division of Biostatistics, Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.

Susanna Kullberg (S)

Division of Respiratory Medicine, Dept of Medicine Solna and Centre for Molecular Medicine, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden.
Dept of Respiratory Medicine, Theme Inflammation and Infection, Karolinska University Hospital, Stockholm, Sweden.

Anders Blomberg (A)

Dept of Public Health and Clinical Medicine, Division of Medicine, Umeå University, Umeå, Sweden.

Johan Grunewald (J)

Division of Respiratory Medicine, Dept of Medicine Solna and Centre for Molecular Medicine, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden.
Dept of Respiratory Medicine, Theme Inflammation and Infection, Karolinska University Hospital, Stockholm, Sweden.

Anna Smed-Sörensen (A)

Division of Immunology and Allergy, Dept of Medicine Solna, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden anna.smed.sorensen@ki.se.

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