Follicular helper T cell signature of replicative exhaustion, apoptosis, and senescence in common variable immunodeficiency.


Journal

European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201

Informations de publication

Date de publication:
07 2022
Historique:
revised: 08 02 2022
received: 29 06 2021
accepted: 09 05 2022
pubmed: 15 5 2022
medline: 14 7 2022
entrez: 14 5 2022
Statut: ppublish

Résumé

Common variable immunodeficiency (CVID) is the most frequent primary antibody deficiency whereby follicular helper T (Tfh) cells fail to establish productive responses with B cells in germinal centers. Here, we analyzed the frequency, phenotype, transcriptome, and function of circulating Tfh (cTfh) cells in CVID patients displaying autoimmunity as an additional phenotype. A group of patients showed a high frequency of cTfh1 cells and a prominent expression of PD-1 and ICOS as well as a cTfh mRNA signature consistent with highly activated, but exhausted, senescent, and apoptotic cells. Plasmatic CXCL13 levels were elevated in this group and positively correlated with cTfh1 cell frequency and PD-1 levels. Monoallelic variants in RTEL1, a telomere length- and DNA repair-related gene, were identified in four patients belonging to this group. Their blood lymphocytes showed shortened telomeres, while their cTfh were more prone to apoptosis. These data point toward a novel pathogenetic mechanism in CVID, whereby alterations in DNA repair and telomere elongation might predispose to antibody deficiency. A Th1, highly activated but exhausted and apoptotic cTfh phenotype was associated with this form of CVID.

Identifiants

pubmed: 35562849
doi: 10.1002/eji.202149480
pmc: PMC9542315
doi:

Substances chimiques

Programmed Cell Death 1 Receptor 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1171-1189

Commentaires et corrections

Type : ErratumIn

Informations de copyright

© 2022 The Authors. European Journal of Immunology published by Wiley-VCH GmbH.

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Auteurs

Giulia Milardi (G)

Division of Immunology, Transplantation, and Infectious Diseases, Diabetes Research Institute, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Biagio Di Lorenzo (B)

Division of Immunology, Transplantation, and Infectious Diseases, Diabetes Research Institute, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Jolanda Gerosa (J)

Division of Immunology, Transplantation, and Infectious Diseases, Diabetes Research Institute, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Federica Barzaghi (F)

Pediatric Immunohematology and Bone Marrow Transplantation Unit, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.
Pathogenesis and therapy of primary immunodeficiencies Unit, San Raffaele Telethon Institute for Gene Therapy, Sr-TIGET, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Gigliola Di Matteo (G)

Department of Systems Medicine, University of Rome Tor Vergata, Via Cracovia 50, Rome, 00133, Italy.
Immune and Infectious Diseases Division, Research Unit of Primary Immunodeficiencies, Academic Department of Pediatrics, Bambino Gesù Children's Hospital, IRCCS, Piazza di Sant'Onofrio 4, Rome, 00165, Italy.

Maryam Omrani (M)

Pathogenesis and therapy of primary immunodeficiencies Unit, San Raffaele Telethon Institute for Gene Therapy, Sr-TIGET, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.
Department of Computer Science, Systems and Communication, University of Milano-Bicocca, Piazza dell'Ateneo Nuovo 1, Milan, 20126, Italy.

Tatiana Jofra (T)

Division of Immunology, Transplantation, and Infectious Diseases, Diabetes Research Institute, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Ivan Merelli (I)

Pathogenesis and therapy of primary immunodeficiencies Unit, San Raffaele Telethon Institute for Gene Therapy, Sr-TIGET, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.
Department of Bioinformatics, Institute for Biomedical Technologies, National Research Council, Via Fratelli Cervi 93, Segrate, 20090, Italy.

Matteo Barcella (M)

Pathogenesis and therapy of primary immunodeficiencies Unit, San Raffaele Telethon Institute for Gene Therapy, Sr-TIGET, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Matteo Filippini (M)

Division of Immunology, Transplantation, and Infectious Diseases, Diabetes Research Institute, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Anastasia Conti (A)

Pathogenesis and therapy of primary immunodeficiencies Unit, San Raffaele Telethon Institute for Gene Therapy, Sr-TIGET, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Francesca Ferrua (F)

Pediatric Immunohematology and Bone Marrow Transplantation Unit, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.
Pathogenesis and therapy of primary immunodeficiencies Unit, San Raffaele Telethon Institute for Gene Therapy, Sr-TIGET, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Francesco Pozzo Giuffrida (F)

Pediatric Immunohematology and Bone Marrow Transplantation Unit, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.
Pathogenesis and therapy of primary immunodeficiencies Unit, San Raffaele Telethon Institute for Gene Therapy, Sr-TIGET, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Francesca Dionisio (F)

Pathogenesis and therapy of primary immunodeficiencies Unit, San Raffaele Telethon Institute for Gene Therapy, Sr-TIGET, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Patrizia Rovere-Querini (P)

Department of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Sarah Marktel (S)

Hematology and Bone Marrow Transplantation Unit, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Andrea Assanelli (A)

Hematology and Bone Marrow Transplantation Unit, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Simona Piemontese (S)

Hematology and Bone Marrow Transplantation Unit, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Immacolata Brigida (I)

Pathogenesis and therapy of primary immunodeficiencies Unit, San Raffaele Telethon Institute for Gene Therapy, Sr-TIGET, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Matteo Zoccolillo (M)

Pathogenesis and therapy of primary immunodeficiencies Unit, San Raffaele Telethon Institute for Gene Therapy, Sr-TIGET, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Emilia Cirillo (E)

Department of Translational Medical Sciences, Section of Pediatrics, Federico II University of Naples, Corso Umberto I, 40, 80138, Italy.

Giuliana Giardino (G)

Department of Translational Medical Sciences, Section of Pediatrics, Federico II University of Naples, Corso Umberto I, 40, 80138, Italy.

Maria Giovanna Danieli (MG)

Department of Clinical and Molecular Sciences, Marche Polytechnic University of Ancona, Clinica Medica, Via Tronto 10/a, Ancona, 60126, Italy.

Fernando Specchia (F)

Department of Pediatrics, S. Orsola-Malpighi Hospital, University of Bologna, Via Giuseppe Massarenti 9, Bologna, 40138, Italy.

Lucia Pacillo (L)

Department of Systems Medicine, University of Rome Tor Vergata, Via Cracovia 50, Rome, 00133, Italy.
Immune and Infectious Diseases Division, Research Unit of Primary Immunodeficiencies, Academic Department of Pediatrics, Bambino Gesù Children's Hospital, IRCCS, Piazza di Sant'Onofrio 4, Rome, 00165, Italy.

Silvia Di Cesare (S)

Department of Systems Medicine, University of Rome Tor Vergata, Via Cracovia 50, Rome, 00133, Italy.
Immune and Infectious Diseases Division, Research Unit of Primary Immunodeficiencies, Academic Department of Pediatrics, Bambino Gesù Children's Hospital, IRCCS, Piazza di Sant'Onofrio 4, Rome, 00165, Italy.

Carmela Giancotta (C)

Department of Systems Medicine, University of Rome Tor Vergata, Via Cracovia 50, Rome, 00133, Italy.
Immune and Infectious Diseases Division, Research Unit of Primary Immunodeficiencies, Academic Department of Pediatrics, Bambino Gesù Children's Hospital, IRCCS, Piazza di Sant'Onofrio 4, Rome, 00165, Italy.

Francesca Romano (F)

Pediatric Immunology Division, Department of Pediatrics, Anna Meyer Children's University Hospital, Viale Gaetano Pieraccini 24, Florence, 50139, Italy.

Alessandro Matarese (A)

Department of Respiratory Medicine, Santi Antonio, Biagio and Cesare Arrigo Hospital, Via Venezia 16, Alessandria, 15121, Italy.

Alfredo Antonio Chetta (AA)

Department of Medicine and Surgery, Respiratory Disease and Lung Function Unit, University of Parma, Str. dell'Università 12, Parma, 43121, Italy.

Matteo Trimarchi (M)

Otorhinolaryngology Unit, Head and Neck Department, IRCCS San Raffaele Scientific Institute, Via Olgettina 60, Milan, 20132, Italy.
Pathology Unit, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Andrea Laurenzi (A)

Division of Immunology, Transplantation, and Infectious Diseases, Diabetes Research Institute, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Maurizio De Pellegrin (M)

Unit of Orthopaedics, IRCCS San Raffaele Scientific Institute, Via Olgettina 60, Milan, 20132, Italy.

Silvia Darin (S)

Pediatric Immunohematology and Bone Marrow Transplantation Unit, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Davide Montin (D)

Department of Pediatrics and Public Health, Regina Margherita Hospital, Piazza Polonia 94, Turin, 10126, Italy.

Maddalena Marinoni (M)

Pediatric Unit, Ospedale "F. Del Ponte", Via Filippo del Ponte 19, Varese, 21100, Italy.

Rosa Maria Dellepiane (RM)

Department of Pediatrics, Fondazione IRCCS Cà Granda Ospedale Maggiore Policlinico, University of Milan, Via Francesco Sforza 35, Milan, 20122, Italy.

Valeria Sordi (V)

Division of Immunology, Transplantation, and Infectious Diseases, Diabetes Research Institute, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Vassilios Lougaris (V)

Department of Clinical and Experimental Sciences, Pediatrics Clinic and Institute for Molecular Medicine A. Nocivelli, University of Brescia, Piazza del Mercato 15, Brescia, 25121, Italy.

Angelo Vacca (A)

Department of Biomedical Sciences and Human Oncology, University of Bari Medical School, Piazza Umberto I, 1, Bari, 70121, Italy.

Raffaella Melzi (R)

Division of Immunology, Transplantation, and Infectious Diseases, Diabetes Research Institute, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Rita Nano (R)

Division of Immunology, Transplantation, and Infectious Diseases, Diabetes Research Institute, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Chiara Azzari (C)

Pediatric Immunology Division, Department of Pediatrics, Anna Meyer Children's University Hospital, Viale Gaetano Pieraccini 24, Florence, 50139, Italy.

Lucia Bongiovanni (L)

Pathology Unit, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Claudio Pignata (C)

Department of Translational Medical Sciences, Section of Pediatrics, Federico II University of Naples, Corso Umberto I, 40, 80138, Italy.

Caterina Cancrini (C)

Department of Systems Medicine, University of Rome Tor Vergata, Via Cracovia 50, Rome, 00133, Italy.
Immune and Infectious Diseases Division, Research Unit of Primary Immunodeficiencies, Academic Department of Pediatrics, Bambino Gesù Children's Hospital, IRCCS, Piazza di Sant'Onofrio 4, Rome, 00165, Italy.

Alessandro Plebani (A)

Department of Clinical and Experimental Sciences, Pediatrics Clinic and Institute for Molecular Medicine A. Nocivelli, University of Brescia, Piazza del Mercato 15, Brescia, 25121, Italy.

Lorenzo Piemonti (L)

Division of Immunology, Transplantation, and Infectious Diseases, Diabetes Research Institute, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.
Faculty of Medicine, University Vita-Salute San Raffaele, Via Olgettina 60, Milan, 20132, Italy.

Constantinos Petrovas (C)

Tissue Analysis Core, Immunology Laboratory, Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 9000 Rockville Pike, Bethesda, MD, 20892, USA.

Raffaella Di Micco (R)

Pathogenesis and therapy of primary immunodeficiencies Unit, San Raffaele Telethon Institute for Gene Therapy, Sr-TIGET, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Maurilio Ponzoni (M)

Pathology Unit, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.
Faculty of Medicine, University Vita-Salute San Raffaele, Via Olgettina 60, Milan, 20132, Italy.

Alessandro Aiuti (A)

Pediatric Immunohematology and Bone Marrow Transplantation Unit, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.
Pathogenesis and therapy of primary immunodeficiencies Unit, San Raffaele Telethon Institute for Gene Therapy, Sr-TIGET, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.
Faculty of Medicine, University Vita-Salute San Raffaele, Via Olgettina 60, Milan, 20132, Italy.

Maria Pia Cicalese (MP)

Pediatric Immunohematology and Bone Marrow Transplantation Unit, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.
Pathogenesis and therapy of primary immunodeficiencies Unit, San Raffaele Telethon Institute for Gene Therapy, Sr-TIGET, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

Georgia Fousteri (G)

Division of Immunology, Transplantation, and Infectious Diseases, Diabetes Research Institute, IRCCS San Raffaele Hospital, Via Olgettina 60, Milan, 20132, Italy.

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