CD70 recruitment to the immunological synapse is dependent on CD20 in B cells

A Abbey B. Arp (Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center) A Andrea Abel Gutierrez (Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center) M Martin ter Beest (Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center) G Guus A. Franken (Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center) H Harry Warner (Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center) A Andrea Rodgers Furones (Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center) A Angelique N. Kenyon (Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center) F Franziska Jäger (Department of Chemistry, Structural Biochemistry, Bijvoet Centre for Biomolecular Research, Faculty of Science, Utrecht University) A Alfredo Cabrera-Orefice (Radboud Institute for Medical Innovation, Radboud University Medical Center) K Kathrin Kläsener (Department of Molecular Immunology, Centre for Biological Signalling Studies and Centre for Integrative Biological Signalling Studies, Centre for Biological Signalling Studies, Biology III, Faculty of Biology, University of Freiburg) S Sjoerd van Deventer (Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center) L Lenny Droesen (Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center) V Vera Marie E. Dunlock (Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center) R René Classens (Department of Medical BioSciences, Radboudumc) J Julian Staniek (Department of Rheumatology and Clinical Immunology, University Medical Center Freiburg, Faculty of Medicine, University of Freiburg) J Jannie Borst (Department of Immunology, Leiden University Medical Center) M Michael Reth (Department of Molecular Immunology, Centre for Biological Signalling Studies and Centre for Integrative Biological Signalling Studies, Centre for Biological Signalling Studies, Biology III, Faculty of Biology, University of Freiburg) U Ulrich Brandt (Radboud Institute for Medical Innovation, Radboud University Medical Center) P Piet Gros (Department of Chemistry, Structural Biochemistry, Bijvoet Centre for Biomolecular Research, Faculty of Science, Utrecht University) T Taco W. Kuijpers (Department of Pediatric Immunology, Rheumatology and Infectious Diseases, Emma Children’s Hospital, Amsterdam University Medical Center) M Mirjam H. M. Heemskerk (Department of Hematology, Leiden University Medical Center) M Marta Rizzi (Department of Rheumatology and Clinical Immunology, University Medical Center Freiburg, Faculty of Medicine, University of Freiburg) L Laia Querol Cano (Department of Medical BioSciences, Radboudumc) A Annemiek B. van Spriel (Department of Medical BioSciences, Radboudumc)

Abstract

CD20 is a four-transmembrane protein expressed at the surface of B cells from late pro-B cells to memory B cells, with the exception of plasma cells. Its expression pattern makes it an attractive therapeutic target for different B cell malignancies and autoimmune diseases. Despite the clinical success of CD20-targeting antibodies, the biology of the CD20 protein is still not well understood. We investigated CD20 binding partners in the membrane of human B cells using immunoprecipitation followed by mass spectrometry analysis. We identified a molecular interaction between CD70 and CD20, and confirmed this using proximity ligation assays. CD20–CD70 spatiotemporal colocalization was validated at the plasma membrane of B cells using high-resolution microscopy. Cell surface expression of CD70 was found to be enhanced upon CD20 overexpression, suggesting a role for CD20 in stabilizing CD70 at the B cell membrane. Moreover, we observed impaired B-T cell synapse formation and defective recruitment of CD70 to the immunological synapse in the absence of CD20. Impaired synapse formation was confirmed by deleting CD20 in primary B cells, and analysis of B cells from a CD20-deficient patient. Finally, CD20-deletion resulted in diminished T cell activation and cytokine secretion. Together, this study demonstrates that CD20 interacts with CD70 at the B cell membrane, and that CD20 is required for immune synapse formation between B and T cells and consequent T cell activation.

Article Details

Volume / Issue Vol. 122, Issue 16
Published April 22, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (24)

A

Abbey B. Arp

Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center

A

Andrea Abel Gutierrez

Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center

M

Martin ter Beest

Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center

G

Guus A. Franken

Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center

H

Harry Warner

Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center

A

Andrea Rodgers Furones

Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center

A

Angelique N. Kenyon

Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center

F

Franziska Jäger

Department of Chemistry, Structural Biochemistry, Bijvoet Centre for Biomolecular Research, Faculty of Science, Utrecht University

A

Alfredo Cabrera-Orefice

Radboud Institute for Medical Innovation, Radboud University Medical Center

K

Kathrin Kläsener

Department of Molecular Immunology, Centre for Biological Signalling Studies and Centre for Integrative Biological Signalling Studies, Centre for Biological Signalling Studies, Biology III, Faculty of Biology, University of Freiburg

S

Sjoerd van Deventer

Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center

L

Lenny Droesen

Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center

V

Vera Marie E. Dunlock

Department of Medical BioSciences, Radboud Institute for Medical Innovation, Radboud University Medical Center

R

René Classens

Department of Medical BioSciences, Radboudumc

J

Julian Staniek

Department of Rheumatology and Clinical Immunology, University Medical Center Freiburg, Faculty of Medicine, University of Freiburg

J

Jannie Borst

Department of Immunology, Leiden University Medical Center

M

Michael Reth

Department of Molecular Immunology, Centre for Biological Signalling Studies and Centre for Integrative Biological Signalling Studies, Centre for Biological Signalling Studies, Biology III, Faculty of Biology, University of Freiburg

U

Ulrich Brandt

Radboud Institute for Medical Innovation, Radboud University Medical Center

P

Piet Gros

Department of Chemistry, Structural Biochemistry, Bijvoet Centre for Biomolecular Research, Faculty of Science, Utrecht University

T

Taco W. Kuijpers

Department of Pediatric Immunology, Rheumatology and Infectious Diseases, Emma Children’s Hospital, Amsterdam University Medical Center

M

Mirjam H. M. Heemskerk

Department of Hematology, Leiden University Medical Center

M

Marta Rizzi

Department of Rheumatology and Clinical Immunology, University Medical Center Freiburg, Faculty of Medicine, University of Freiburg

L

Laia Querol Cano

Department of Medical BioSciences, Radboudumc

A

Annemiek B. van Spriel

Department of Medical BioSciences, Radboudumc