Single cell profiling of circulating autoreactive CD4 T cells from patients with autoimmune liver diseases suggests tissue imprinting

A Anaïs Cardon T Thomas Guinebretière C Chuang Dong L Laurine Gil S Sakina Ado P Pierre-jean Gavlovsky M Martin Braud R Richard Danger (Nantes Université, CHU Nantes, INSERM, Center for Research in Transplantation and Translational Immunology, Unité Mixte de Recherche 1064, Institute of Urology–Nephrology Transplantation of the University Hospital of Nantes, Nantes, France) C Christoph Schultheiß A Aurélie Doméné P Perrine Paul-Gilloteaux C Caroline Chevalier L Laura Bernier J Jean-Paul Judor C Cynthia Fourgeux A Astrid Imbert M Marion Khaldi E Edouard Bardou-Jacquet L Laure Elkrief A Adrien Lannes C Christine Silvain M Matthieu Schnee F Florence Tanne F Fabienne Vavasseur L Lucas Brusselle S Sophie Brouard (Nantes Université, CHU Nantes, INSERM, Center for Research in Transplantation and Translational Immunology, Unité Mixte de Recherche 1064, Institute of Urology–Nephrology Transplantation of the University Hospital of Nantes, Nantes, France) W William W. Kwok J Jean-François Mosnier A Ansgar W. Lohse J Jeremie Poschmann M Mascha Binder J Jérôme Gournay S Sophie Conchon P Pierre Milpied A Amédée Renand

Abstract

Abstract Autoimmune liver diseases (AILD) involve dysregulated CD4 T cell responses against liver self-antigens, but how these autoreactive T cells relate to liver tissue pathology remains unclear. Here we perform single-cell transcriptomic and T cell receptor analyses of circulating, self-antigen-specific CD4 T cells from patients with AILD and identify a subset of liver-autoreactive CD4 T cells with a distinct B-helper transcriptional profile characterized by PD-1, TIGIT and HLA-DR expression. These cells share clonal relationships with expanded intrahepatic T cells and exhibit transcriptional signatures overlapping with tissue-resident T cells in chronically inflamed environments. Using a mouse model, we demonstrate that, following antigen recognition in the liver, CD4 T cells acquire an exhausted phenotype, play a crucial role in liver damage, and are controlled by immune checkpoint pathways. Our findings thus suggest that circulating autoreactive CD4 T cells in AILD are imprinted by chronic antigen exposure to promote liver inflammation, thereby serving as a potential target for developing biomarkers and therapies for AILD.

Article Details

Volume / Issue Vol. 16, Issue 1
Published January 29, 2025
ISSN 2041-1723
Publisher Nature Portfolio

Journal Info

Nature Communications

Nature Portfolio

ISSN: 2041-1723 Open Access Life Sciences

Authors (35)

A

Anaïs Cardon

T

Thomas Guinebretière

C

Chuang Dong

L

Laurine Gil

S

Sakina Ado

P

Pierre-jean Gavlovsky

M

Martin Braud

R

Richard Danger

Nantes Université, CHU Nantes, INSERM, Center for Research in Transplantation and Translational Immunology, Unité Mixte de Recherche 1064, Institute of Urology–Nephrology Transplantation of the University Hospital of Nantes, Nantes, France

C

Christoph Schultheiß

A

Aurélie Doméné

P

Perrine Paul-Gilloteaux

C

Caroline Chevalier

L

Laura Bernier

J

Jean-Paul Judor

C

Cynthia Fourgeux

A

Astrid Imbert

M

Marion Khaldi

E

Edouard Bardou-Jacquet

L

Laure Elkrief

A

Adrien Lannes

C

Christine Silvain

M

Matthieu Schnee

F

Florence Tanne

F

Fabienne Vavasseur

L

Lucas Brusselle

S

Sophie Brouard

Nantes Université, CHU Nantes, INSERM, Center for Research in Transplantation and Translational Immunology, Unité Mixte de Recherche 1064, Institute of Urology–Nephrology Transplantation of the University Hospital of Nantes, Nantes, France

W

William W. Kwok

J

Jean-François Mosnier

A

Ansgar W. Lohse

J

Jeremie Poschmann

M

Mascha Binder

J

Jérôme Gournay

S

Sophie Conchon

P

Pierre Milpied

A

Amédée Renand