Extrafollicular IgD−CD27−CXCR5−CD11c− DN3 B cells infiltrate inflamed tissues in autoimmune fibrosis and in severe COVID-19

Summary: Although therapeutic B cell depletion dramatically resolves inflammation in many diseases in which antibodies appear not to play a central role, distinct extrafollicular pathogenic B cell subsets that accumulate in disease lesions have hitherto not been identified. The circulating immunoglo...

Full description

Bibliographic Details
Main Authors: Hugues Allard-Chamard, Naoki Kaneko, Alice Bertocchi, Na Sun, Julie Boucau, Hsiao-Hsuan Kuo, Jocelyn R. Farmer, Cory Perugino, Vinay S. Mahajan, Samuel J.H. Murphy, Katherine Premo, Thomas Diefenbach, Musie Ghebremichael, Grace Yuen, Alekhya Kotta, Zafer Akman, Mathias Lichterfeld, Bruce D. Walker, Xu G. Yu, Masafumi Moriyama, Takashi Maehara, Seiji Nakamura, John H. Stone, Robert F. Padera, Shiv Pillai
Format: Article
Language:English
Published: Elsevier 2023-06-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723006411
_version_ 1797807281398611968
author Hugues Allard-Chamard
Naoki Kaneko
Alice Bertocchi
Na Sun
Julie Boucau
Hsiao-Hsuan Kuo
Jocelyn R. Farmer
Cory Perugino
Vinay S. Mahajan
Samuel J.H. Murphy
Katherine Premo
Thomas Diefenbach
Musie Ghebremichael
Grace Yuen
Alekhya Kotta
Zafer Akman
Mathias Lichterfeld
Bruce D. Walker
Xu G. Yu
Masafumi Moriyama
Takashi Maehara
Seiji Nakamura
John H. Stone
Robert F. Padera
Shiv Pillai
author_facet Hugues Allard-Chamard
Naoki Kaneko
Alice Bertocchi
Na Sun
Julie Boucau
Hsiao-Hsuan Kuo
Jocelyn R. Farmer
Cory Perugino
Vinay S. Mahajan
Samuel J.H. Murphy
Katherine Premo
Thomas Diefenbach
Musie Ghebremichael
Grace Yuen
Alekhya Kotta
Zafer Akman
Mathias Lichterfeld
Bruce D. Walker
Xu G. Yu
Masafumi Moriyama
Takashi Maehara
Seiji Nakamura
John H. Stone
Robert F. Padera
Shiv Pillai
author_sort Hugues Allard-Chamard
collection DOAJ
description Summary: Although therapeutic B cell depletion dramatically resolves inflammation in many diseases in which antibodies appear not to play a central role, distinct extrafollicular pathogenic B cell subsets that accumulate in disease lesions have hitherto not been identified. The circulating immunoglobulin D (IgD)−CD27−CXCR5−CD11c+ DN2 B cell subset has been previously studied in some autoimmune diseases. A distinct IgD−CD27−CXCR5−CD11c− DN3 B cell subset accumulates in the blood both in IgG4-related disease, an autoimmune disease in which inflammation and fibrosis can be reversed by B cell depletion, and in severe COVID-19. These DN3 B cells prominently accumulate in the end organs of IgG4-related disease and in lung lesions in COVID-19, and double-negative B cells prominently cluster with CD4+ T cells in these lesions. Extrafollicular DN3 B cells may participate in tissue inflammation and fibrosis in autoimmune fibrotic diseases, as well as in COVID-19.
first_indexed 2024-03-13T06:20:13Z
format Article
id doaj.art-f6449a71ead94ed7a5350e782a784b4a
institution Directory Open Access Journal
issn 2211-1247
language English
last_indexed 2024-03-13T06:20:13Z
publishDate 2023-06-01
publisher Elsevier
record_format Article
series Cell Reports
spelling doaj.art-f6449a71ead94ed7a5350e782a784b4a2023-06-10T04:27:22ZengElsevierCell Reports2211-12472023-06-01426112630Extrafollicular IgD−CD27−CXCR5−CD11c− DN3 B cells infiltrate inflamed tissues in autoimmune fibrosis and in severe COVID-19Hugues Allard-Chamard0Naoki Kaneko1Alice Bertocchi2Na Sun3Julie Boucau4Hsiao-Hsuan Kuo5Jocelyn R. Farmer6Cory Perugino7Vinay S. Mahajan8Samuel J.H. Murphy9Katherine Premo10Thomas Diefenbach11Musie Ghebremichael12Grace Yuen13Alekhya Kotta14Zafer Akman15Mathias Lichterfeld16Bruce D. Walker17Xu G. Yu18Masafumi Moriyama19Takashi Maehara20Seiji Nakamura21John H. Stone22Robert F. Padera23Shiv Pillai24Ragon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USA; Division of Rheumatology, Faculté de médecine et des sciences de la santé de l'Université de Sherbrooke et Centre de Recherche Clinique Étienne-Le Bel, Sherbrooke, QC J1K 2R1, CanadaRagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USA; Section of Oral and Maxillofacial Oncology, Division of Maxillofacial Diagnostic and Surgical Sciences, Faculty of Dental Science, Kyushu University, Fukuoka, JapanRagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USA; Division of Rheumatology Allergy and Immunology, Massachusetts General Hospital, Boston, MA 02114, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USA; Department of Pathology, Brigham and Women’s Hospital, Boston, MA 02115, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USA; Department of Medicine, Brigham and Women’s Hospital, Boston, MA 02115, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USA; Howard Hughes Medical Institute, Chevy Chase, MD 20815, USA; Department of Biology and Institute of Medical Engineering and Science, Massachusetts Institute of Technology, Cambridge, MA 02139, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USASection of Oral and Maxillofacial Oncology, Division of Maxillofacial Diagnostic and Surgical Sciences, Faculty of Dental Science, Kyushu University, Fukuoka, JapanRagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USA; Section of Oral and Maxillofacial Oncology, Division of Maxillofacial Diagnostic and Surgical Sciences, Faculty of Dental Science, Kyushu University, Fukuoka, JapanSection of Oral and Maxillofacial Oncology, Division of Maxillofacial Diagnostic and Surgical Sciences, Faculty of Dental Science, Kyushu University, Fukuoka, JapanDivision of Rheumatology Allergy and Immunology, Massachusetts General Hospital, Boston, MA 02114, USADepartment of Pathology, Brigham and Women’s Hospital, Boston, MA 02115, USARagon Institute of MGH, MIT and Harvard, Cambridge, MA 02139, USA; Corresponding authorSummary: Although therapeutic B cell depletion dramatically resolves inflammation in many diseases in which antibodies appear not to play a central role, distinct extrafollicular pathogenic B cell subsets that accumulate in disease lesions have hitherto not been identified. The circulating immunoglobulin D (IgD)−CD27−CXCR5−CD11c+ DN2 B cell subset has been previously studied in some autoimmune diseases. A distinct IgD−CD27−CXCR5−CD11c− DN3 B cell subset accumulates in the blood both in IgG4-related disease, an autoimmune disease in which inflammation and fibrosis can be reversed by B cell depletion, and in severe COVID-19. These DN3 B cells prominently accumulate in the end organs of IgG4-related disease and in lung lesions in COVID-19, and double-negative B cells prominently cluster with CD4+ T cells in these lesions. Extrafollicular DN3 B cells may participate in tissue inflammation and fibrosis in autoimmune fibrotic diseases, as well as in COVID-19.http://www.sciencedirect.com/science/article/pii/S2211124723006411CP: Immunology
spellingShingle Hugues Allard-Chamard
Naoki Kaneko
Alice Bertocchi
Na Sun
Julie Boucau
Hsiao-Hsuan Kuo
Jocelyn R. Farmer
Cory Perugino
Vinay S. Mahajan
Samuel J.H. Murphy
Katherine Premo
Thomas Diefenbach
Musie Ghebremichael
Grace Yuen
Alekhya Kotta
Zafer Akman
Mathias Lichterfeld
Bruce D. Walker
Xu G. Yu
Masafumi Moriyama
Takashi Maehara
Seiji Nakamura
John H. Stone
Robert F. Padera
Shiv Pillai
Extrafollicular IgD−CD27−CXCR5−CD11c− DN3 B cells infiltrate inflamed tissues in autoimmune fibrosis and in severe COVID-19
Cell Reports
CP: Immunology
title Extrafollicular IgD−CD27−CXCR5−CD11c− DN3 B cells infiltrate inflamed tissues in autoimmune fibrosis and in severe COVID-19
title_full Extrafollicular IgD−CD27−CXCR5−CD11c− DN3 B cells infiltrate inflamed tissues in autoimmune fibrosis and in severe COVID-19
title_fullStr Extrafollicular IgD−CD27−CXCR5−CD11c− DN3 B cells infiltrate inflamed tissues in autoimmune fibrosis and in severe COVID-19
title_full_unstemmed Extrafollicular IgD−CD27−CXCR5−CD11c− DN3 B cells infiltrate inflamed tissues in autoimmune fibrosis and in severe COVID-19
title_short Extrafollicular IgD−CD27−CXCR5−CD11c− DN3 B cells infiltrate inflamed tissues in autoimmune fibrosis and in severe COVID-19
title_sort extrafollicular igd cd27 cxcr5 cd11c dn3 b cells infiltrate inflamed tissues in autoimmune fibrosis and in severe covid 19
topic CP: Immunology
url http://www.sciencedirect.com/science/article/pii/S2211124723006411
work_keys_str_mv AT huguesallardchamard extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT naokikaneko extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT alicebertocchi extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT nasun extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT julieboucau extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT hsiaohsuankuo extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT jocelynrfarmer extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT coryperugino extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT vinaysmahajan extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT samueljhmurphy extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT katherinepremo extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT thomasdiefenbach extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT musieghebremichael extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT graceyuen extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT alekhyakotta extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT zaferakman extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT mathiaslichterfeld extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT brucedwalker extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT xugyu extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT masafumimoriyama extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT takashimaehara extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT seijinakamura extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT johnhstone extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT robertfpadera extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19
AT shivpillai extrafollicularigdcd27cxcr5cd11cdn3bcellsinfiltrateinflamedtissuesinautoimmunefibrosisandinseverecovid19