Partial RAG deficiency in humans induces dysregulated peripheral lymphocyte development and humoral tolerance defect with accumulation of T-bet


Journal

Nature immunology
ISSN: 1529-2916
Titre abrégé: Nat Immunol
Pays: United States
ID NLM: 100941354

Informations de publication

Date de publication:
08 2022
Historique:
received: 10 06 2021
accepted: 16 06 2022
pubmed: 29 7 2022
medline: 10 8 2022
entrez: 28 7 2022
Statut: ppublish

Résumé

The recombination-activating genes (RAG) 1 and 2 are indispensable for diversifying the primary B cell receptor repertoire and pruning self-reactive clones via receptor editing in the bone marrow; however, the impact of RAG1/RAG2 on peripheral tolerance is unknown. Partial RAG deficiency (pRD) manifesting with late-onset immune dysregulation represents an 'experiment of nature' to explore this conundrum. By studying B cell development and subset-specific repertoires in pRD, we demonstrate that reduced RAG activity impinges on peripheral tolerance through the generation of a restricted primary B cell repertoire, persistent antigenic stimulation and an inflammatory milieu with elevated B cell-activating factor. This unique environment gradually provokes profound B cell dysregulation with widespread activation, remarkable extrafollicular maturation and persistence, expansion and somatic diversification of self-reactive clones. Through the model of pRD, we reveal a RAG-dependent 'domino effect' that impacts stringency of tolerance and B cell fate in the periphery.

Identifiants

pubmed: 35902638
doi: 10.1038/s41590-022-01271-6
pii: 10.1038/s41590-022-01271-6
pmc: PMC9355881
doi:

Substances chimiques

DNA-Binding Proteins 0
Homeodomain Proteins 0
Nuclear Proteins 0
RAG2 protein, human 0
RAG-1 protein 128559-51-3

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1256-1272

Subventions

Organisme : NIAID NIH HHS
ID : R01 AI153830
Pays : United States
Organisme : NIAID NIH HHS
ID : K08 AI103035
Pays : United States
Organisme : Intramural NIH HHS
ID : ZIA AI001222
Pays : United States
Organisme : NIAID NIH HHS
ID : P01 AI061093
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI100887
Pays : United States

Informations de copyright

© 2022. The Author(s).

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Auteurs

Krisztian Csomos (K)

Division of Pediatric Allergy/Immunology, University of South Florida at Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA. kcsomos@usf.edu.

Boglarka Ujhazi (B)

Division of Pediatric Allergy/Immunology, University of South Florida at Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.

Peter Blazso (P)

Division of Pediatric Allergy/Immunology, University of South Florida at Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.
Department of Pediatrics, University of Szeged, Szeged, Hungary.

Jose L Herrera (JL)

Cancer and Blood Disorders Institute and Department of Surgery, Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.
Department of Orthopaedic Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, USA.

Christopher M Tipton (CM)

Department of Medicine, Division of Rheumatology, Emory University, Atlanta, GA, USA.

Tomoki Kawai (T)

Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD, USA.

Sumai Gordon (S)

Division of Pediatric Allergy/Immunology, University of South Florida at Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.

Maryssa Ellison (M)

Division of Pediatric Allergy/Immunology, University of South Florida at Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.

Kevin Wu (K)

Division of Pediatric Allergy/Immunology, University of South Florida at Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.

Matthew Stowell (M)

Division of Pediatric Allergy/Immunology, University of South Florida at Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.

Lauren Haynes (L)

Division of Pediatric Allergy/Immunology, University of South Florida at Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.

Rachel Cruz (R)

Division of Pediatric Allergy/Immunology, University of South Florida at Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.

Bence Zakota (B)

Division of Pediatric Allergy/Immunology, University of South Florida at Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.

Johnny Nguyen (J)

Department of Pathology & Laboratory Medicine, Johns Hopkins All Children's Hospital, St Petersburg, FL, USA.

Michelle Altrich (M)

Eurofins Viracor Laboratories, Lee Summit's, MO, USA.

Christoph B Geier (CB)

Immunology Outpatient Clinic, Vienna, Austria.

Svetlana Sharapova (S)

Belarusian Research Center for Pediatric Oncology, Minsk, Belarus.

Joseph F Dasso (JF)

Division of Pediatric Allergy/Immunology, University of South Florida at Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.

Jennifer W Leiding (JW)

Division of Pediatric Allergy/Immunology, University of South Florida at Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.

Grace Smith (G)

Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Waleed Al-Herz (W)

Department of Pediatrics, Faculty of Medicine, Kuwait University, Kuwait City, Kuwait.

Mayra de Barros Dorna (M)

Department of Pediatrics, Faculdade de Medicina da Universidade de São Paulo, São Paulo, Brasil.

Olajumoke Fadugba (O)

Division of Pulmonary, Allergy and Critical Care, Perelman School of Medicine, University of Pennsylvania, Pennsylvania, PA, USA.

Eva Fronkova (E)

Childhood Leukemia Investigation Prague, Department of Pediatric Hematology and Oncology, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic.

Veronika Kanderova (V)

Childhood Leukemia Investigation Prague, Department of Pediatric Hematology and Oncology, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic.

Michael Svaton (M)

Childhood Leukemia Investigation Prague, Department of Pediatric Hematology and Oncology, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic.

Sarah E Henrickson (SE)

Allergy Immunology Division, Department of Pediatrics, The Children's Hospital of Philadelphia, Philadelphia, PA, USA.
Institute for Immunology, the University of Pennsylvania, Philadelphia, PA, USA.

Joseph D Hernandez (JD)

Department of Pediatrics, Division of Allergy, Immunology and Rheumatology, Stanford University, Stanford, CA, USA.

Taco Kuijpers (T)

Deptartment of Pediatric Immunology, Rheumatology and Infectious Diseases, Emma Children's Hospital, Academic Medical Center, Amsterdam, Netherlands.

Snezhina Mihailova Kandilarova (SM)

Department of Clinical Immunology, University Hospital Alexandrovska, Medical University, Sofia, Bulgaria.

Elizaveta Naumova (E)

Department of Clinical Immunology, University Hospital Alexandrovska, Medical University, Sofia, Bulgaria.

Tomas Milota (T)

Department of Immunology, Second Faculty of Medicine Charles University and University Hospital Motol, Prague, Czech Republic.

Anna Sediva (A)

Department of Immunology, Second Faculty of Medicine Charles University and University Hospital Motol, Prague, Czech Republic.

Despina Moshous (D)

Université de Paris, Paris, France.
Pediatric Hematology-Immunology and Rheumatology Unit, Necker-Enfants Malades Université Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France.
Laboratory of Genome Dynamics in the Immune System, INSERM UMR1163, Institut Imagine, Paris, France.

Benedicte Neven (B)

Université de Paris, Paris, France.
Pediatric Hematology-Immunology and Rheumatology Unit, Necker-Enfants Malades Université Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France.
Laboratory of Immunogenetics of Pediatric Autoimmune Diseases, INSERM UMR1163, Institut Imagine, Paris, France.

Tara Saco (T)

Windom Allergy, Asthma and Sinus, Sarasota, FL, USA.

Ravishankar Sargur (R)

Department of Immunology and Allergy, Sheffield Teaching Hospitals, Sheffield, UK.

Sinisa Savic (S)

Department of Clinical Immunology and Allergy, St James's University Hospital, Leeds, UK.
National Institute for Health Research-Leeds Musculoskeletal Biomedical Research Centre and Leeds Institute of Rheumatic and Musculoskeletal Medicine, St James's University Hospital, Leeds, UK.

John Sleasman (J)

Division of Allergy, Immunology and Pulmonary Medicine, Duke University School of Medicine, Durham, NC, USA.

Gauri Sunkersett (G)

Cancer and Blood Disorder Institute, Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.

Brant R Ward (BR)

Division of Allergy and Immunology, Children's Hospital of Richmond, Virginia Commonwealth University, Richmond, VA, USA.

Masanobu Komatsu (M)

Cancer and Blood Disorders Institute and Department of Surgery, Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA.
Department of Orthopaedic Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, USA.

Stefania Pittaluga (S)

Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Attila Kumanovics (A)

Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.

Manish J Butte (MJ)

Division of Immunology, Allergy, and Rheumatology, Department of Pediatrics and Jeffrey Modell Diagnostic and Research Center, University of California, Los Angeles, Los Angeles, CA, USA.

Michael P Cancro (MP)

Department of Pathology, Perelman School of Medicine, University of Pennsylvania, Pennsylvania, PA, USA.

Shiv Pillai (S)

Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of technology and Harvard University, Cambridge, MA, USA.

Eric Meffre (E)

Department of Immunobiology, Yale University, New Haven, CT, USA.
Section of Rheumatology, Allergy and Clinical Immunology, Yale School of Medicine, New Haven, CT, USA.

Luigi D Notarangelo (LD)

Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD, USA.

Jolan E Walter (JE)

Division of Pediatric Allergy/Immunology, University of South Florida at Johns Hopkins All Children's Hospital, St. Petersburg, FL, USA. jolanwalter@usf.edu.
Division of Allergy and Immunology, Massachusetts General Hospital for Children, Boston, MA, USA. jolanwalter@usf.edu.

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