Obesity-associated changes in molecular biology of primary breast cancer

Ha-Linh Nguyen, Tatjana Geukens, Marion Maetens, Samuel Aparicio, Ayse Bassez, Ake Borg, Jane Brock, Annegien Broeks, Carlos Caldas, Fatima Cardoso, Maxim Schepper, Mauro Delorenzi, Caroline A. Drukker, Annuska M. Glas, Andrew R. Green, Edoardo Isnaldi, Jórunn Eyfjörð, Hazem Khout, Stian Knappskog, Savitri Krishnamurthy, Sunil R. Lakhani, Anita Langerod, John W. M. Martens, Amy E. McCart Reed, Leigh Murphy, Stefan Naulaerts, Serena Nik-Zainal, Ines Nevelsteen, Patrick Neven, Martine Piccart, Coralie Poncet, Kevin Punie, Colin Purdie, Emad A. Rakha, Andrea Richardson, Emiel Rutgers, Anne Vincent-Salomon, Peter T. Simpson, Marjanka K. Schmidt, Christos Sotiriou, Paul N. Span, Kiat Tee Benita Tan, Alastair Thompson, Stefania Tommasi, Karen Baelen, Marc Vijver, Steven Laere, Laura van’t Veer, Giuseppe Viale, Alain Viari, Hanne Vos, Anke T. Witteveen, Hans Wildiers, Giuseppe Floris, Abhishek D. Garg, Ann Smeets, Diether Lambrechts, Elia Biganzoli, François Richard and Christine Desmedt ()
Additional contact information
Ha-Linh Nguyen: Laboratory for Translational Breast Cancer Research, Department of Oncology
Tatjana Geukens: Laboratory for Translational Breast Cancer Research, Department of Oncology
Marion Maetens: Laboratory for Translational Breast Cancer Research, Department of Oncology
Samuel Aparicio: BC Cancer Research Centre
Ayse Bassez: Department of Human Genetics
Ake Borg: Lund University
Jane Brock: Brigham and Women’s Hospital
Annegien Broeks: Antoni van Leeuwenhoek, the Netherlands Cancer Institute
Carlos Caldas: Cancer Research UK Cambridge Institute and Department of Oncology, Li Ka Shing Centre, University of Cambridge
Fatima Cardoso: Breast Unit, Champalimaud Clinical Center/Champalimaud Foundation
Maxim Schepper: Laboratory for Translational Breast Cancer Research, Department of Oncology
Mauro Delorenzi: University of Lausanne
Caroline A. Drukker: Department of Surgical Oncology, Antoni van Leeuwenhoek Hospital
Annuska M. Glas: Agendia
Andrew R. Green: University of Nottingham
Edoardo Isnaldi: Laboratory for Translational Breast Cancer Research, Department of Oncology
Jórunn Eyfjörð: University of Iceland
Hazem Khout: University Hospitals of Leicester NHS Trust
Stian Knappskog: University of Bergen
Savitri Krishnamurthy: The University of Texas MD Anderson Cancer Center
Sunil R. Lakhani: The University of Queensland
Anita Langerod: Oslo University Hospital
John W. M. Martens: Erasmus University Medical Center
Amy E. McCart Reed: The University of Queensland
Leigh Murphy: University of Manitoba and Cancer Care Manitoba Research Institute
Stefan Naulaerts: Laboratory of Cell Stress & Immunity, Department of Cellular & Molecular Medicine
Serena Nik-Zainal: University of Cambridge
Ines Nevelsteen: University Hospitals Leuven
Patrick Neven: University Hospitals Leuven
Martine Piccart: Institut Jules Bordet and Université Libre de Bruxelles
Coralie Poncet: European Organisation for Research and Treatment of Cancer (EORTC) Headquarters
Kevin Punie: Leuven Cancer Institute and University Hospitals Leuven
Colin Purdie: University of Dundee, NHS Tayside
Emad A. Rakha: University of Nottingham
Andrea Richardson: Johns Hopkins University School of Medicine
Emiel Rutgers: Netherlands Cancer Institute
Anne Vincent-Salomon: PSL Research University
Peter T. Simpson: The University of Queensland
Marjanka K. Schmidt: Netherlands Cancer Institute—Antoni van Leeuwenhoek Hospital
Christos Sotiriou: Institut Jules Bordet, Universite Libre de Bruxelles
Paul N. Span: Radboud University Medical Center
Kiat Tee Benita Tan: Sengkang General Hospital
Alastair Thompson: Dan L Duncan Comprehensive Cancer Center, Baylor College of Medicine
Stefania Tommasi: Molecular Diagnostics and Pharmacogenetics Unit, IRCCS Istituto Tumouri “Giovanni Paolo II”
Karen Baelen: Laboratory for Translational Breast Cancer Research, Department of Oncology
Marc Vijver: Amsterdam University Medical Centers, Cancer Center Amsterdam, University of Amsterdam
Steven Laere: Center for Oncological Research (CORE), Integrated Personalized and Precision Oncology Network (IPPON), University of Antwerp
Laura van’t Veer: UCSF Helen Diller Family Comprehensive Cancer Center
Giuseppe Viale: IEO, European Institute of Oncology IRCCS
Alain Viari: Synergie Lyon Cancer, Plateforme de Bio-informatique ‘Gilles Thomas’
Hanne Vos: University Hospitals Leuven
Anke T. Witteveen: Agendia
Hans Wildiers: Leuven Cancer Institute and University Hospitals Leuven
Giuseppe Floris: University Hospitals Leuven
Abhishek D. Garg: Laboratory of Cell Stress & Immunity, Department of Cellular & Molecular Medicine
Ann Smeets: University Hospitals Leuven
Diether Lambrechts: Department of Human Genetics
Elia Biganzoli: Università degli Studi di Milano
François Richard: Laboratory for Translational Breast Cancer Research, Department of Oncology
Christine Desmedt: Laboratory for Translational Breast Cancer Research, Department of Oncology

Nature Communications, 2023, vol. 14, issue 1, 1-17

Abstract: Abstract Obesity is associated with an increased risk of developing breast cancer (BC) and worse prognosis in BC patients, yet its impact on BC biology remains understudied in humans. This study investigates how the biology of untreated primary BC differs according to patients’ body mass index (BMI) using data from >2,000 patients. We identify several genomic alterations that are differentially prevalent in overweight or obese patients compared to lean patients. We report evidence supporting an ageing accelerating effect of obesity at the genetic level. We show that BMI-associated differences in bulk transcriptomic profile are subtle, while single cell profiling allows detection of more pronounced changes in different cell compartments. These analyses further reveal an elevated and unresolved inflammation of the BC tumor microenvironment associated with obesity, with distinct characteristics contingent on the estrogen receptor status. Collectively, our analyses imply that obesity is associated with an inflammaging-like phenotype. We conclude that patient adiposity may play a significant role in the heterogeneity of BC and should be considered for BC treatment tailoring.

Date: 2023
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DOI: 10.1038/s41467-023-39996-z

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