Disruption of constitutive CXCR4 oligomers impairs oncogenic properties in lymphoid neoplasms

S Simon Mobach (Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam) N Nick D. Bergkamp (Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam) Z Ziliang Ma (Department of Biomolecular Mass Spectrometry and Proteomics, Biomolecular Mass Spectrometry and Proteomics, Bijvoet Center for Biomolecular Research, Utrecht University) M Marco V. Haselager (Amsterdam University Medical Center location University of Amsterdam, Department of Hematology) S Stephanie M. Anbuhl (Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam) D Daphne Jurriens (Cell Biology, Neurobiology and Biophysics, Department of Biology, Faculty of Science, Utrecht University) J Jelle van den Bor (Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam) Z Ziming Wang C Caitrin Crudden (Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam) J Jamie L. Roos (Amsterdam University Medical Center location University of Amsterdam, Department of Hematology) C Claudia V. Perez Almeria (Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam) R Rick A. Boergonje (Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam) M Martin J. Lohse R Reggie Bosma (Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam) E Eric Eldering (Lymphoma and Myeloma Center Amsterdam) M Marco Siderius (Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam) W Wei Wu M Marcel Spaargaren (Lymphoma and Myeloma Center Amsterdam) S Sanne H. Tonino (Amsterdam University Medical Center location University of Amsterdam, Department of Hematology) A Arnon P. Kater (Amsterdam University Medical Center location University of Amsterdam, Department of Hematology) M Martine J. Smit R Raimond Heukers (Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam)

Abstract

The chemokine receptor CXCR4 is overexpressed in many cancers and contributes to pathogenesis, disease progression, and resistance to therapies. CXCR4 is known to form oligomers, but the potential functional relevance in malignancies remains elusive. Using a nanobody-based BRET method, we demonstrate that oligomerization of endogenous CXCR4 on lymphoid cancer cell lines correlates with enhanced expression levels. Specific disruption of CXCR4 oligomers reduced basal cell migration and prosurvival signaling via changes in the phosphoproteome, indicating the existence of constitutive CXCR4 oligomer-mediated signaling. Oligomer disruption also inhibited growth of primary CLL 3D spheroids and sensitized primary malignant cells to clinically used Bcl-2 inhibitor venetoclax. Given its limited efficacy in some patients and the ability to develop resistance, sensitizing malignant B cells to venetoclax is of clinical relevance. Taken together, we established a noncanonical and critical role for CXCR4 oligomers in lymphoid neoplasms and demonstrated that their selective targeting has clinical potential.

Article Details

Volume / Issue Vol. 122, Issue 24
Published June 17, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (22)

S

Simon Mobach

Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam

N

Nick D. Bergkamp

Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam

Z

Ziliang Ma

Department of Biomolecular Mass Spectrometry and Proteomics, Biomolecular Mass Spectrometry and Proteomics, Bijvoet Center for Biomolecular Research, Utrecht University

M

Marco V. Haselager

Amsterdam University Medical Center location University of Amsterdam, Department of Hematology

S

Stephanie M. Anbuhl

Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam

D

Daphne Jurriens

Cell Biology, Neurobiology and Biophysics, Department of Biology, Faculty of Science, Utrecht University

J

Jelle van den Bor

Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam

Z

Ziming Wang

C

Caitrin Crudden

Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam

J

Jamie L. Roos

Amsterdam University Medical Center location University of Amsterdam, Department of Hematology

C

Claudia V. Perez Almeria

Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam

R

Rick A. Boergonje

Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam

M

Martin J. Lohse

R

Reggie Bosma

Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam

E

Eric Eldering

Lymphoma and Myeloma Center Amsterdam

M

Marco Siderius

Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam

W

Wei Wu

M

Marcel Spaargaren

Lymphoma and Myeloma Center Amsterdam

S

Sanne H. Tonino

Amsterdam University Medical Center location University of Amsterdam, Department of Hematology

A

Arnon P. Kater

Amsterdam University Medical Center location University of Amsterdam, Department of Hematology

M

Martine J. Smit

R

Raimond Heukers

Department of Chemistry and Pharmaceutical Sciences, Division of Medicinal Chemistry, Amsterdam Institute for Molecular and Life Sciences, Vrije Universiteit Amsterdam