Longitudinal molecular profiling elucidates immunometabolism dynamics in breast cancer

Kang Wang, Ioannis Zerdes, Henrik J. Johansson, Dhifaf Sarhan, Yizhe Sun, Dimitris C. Kanellis, Emmanouil G. Sifakis, Artur Mezheyeuski, Xingrong Liu, Niklas Loman, Ingrid Hedenfalk, Jonas Bergh, Jiri Bartek, Thomas Hatschek, Janne Lehtiö, Alexios Matikas and Theodoros Foukakis ()
Additional contact information
Kang Wang: Karolinska Institutet
Ioannis Zerdes: Karolinska Institutet
Henrik J. Johansson: and Science for Life Laboratory
Dhifaf Sarhan: Karolinska Institutet
Yizhe Sun: Karolinska Institutet
Dimitris C. Kanellis: Karolinska Institutet
Emmanouil G. Sifakis: Karolinska Institutet
Artur Mezheyeuski: Rudbeck Laboratory
Xingrong Liu: Karolinska Institutet
Niklas Loman: Lund University Hospital
Ingrid Hedenfalk: Lund University
Jonas Bergh: Karolinska Institutet
Jiri Bartek: Karolinska Institutet
Thomas Hatschek: Karolinska Institutet
Janne Lehtiö: and Science for Life Laboratory
Alexios Matikas: Karolinska Institutet
Theodoros Foukakis: Karolinska Institutet

Nature Communications, 2024, vol. 15, issue 1, 1-24

Abstract: Abstract Although metabolic reprogramming within tumor cells and tumor microenvironment (TME) is well described in breast cancer, little is known about how the interplay of immune state and cancer metabolism evolves during treatment. Here, we characterize the immunometabolic profiles of tumor tissue samples longitudinally collected from individuals with breast cancer before, during and after neoadjuvant chemotherapy (NAC) using proteomics, genomics and histopathology. We show that the pre-, on-treatment and dynamic changes of the immune state, tumor metabolic proteins and tumor cell gene expression profiling-based metabolic phenotype are associated with treatment response. Single-cell/nucleus RNA sequencing revealed distinct tumor and immune cell states in metabolism between cold and hot tumors. Potential drivers of NAC based on above analyses were validated in vitro. In summary, the study shows that the interaction of tumor-intrinsic metabolic states and TME is associated with treatment outcome, supporting the concept of targeting tumor metabolism for immunoregulation.

Date: 2024
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DOI: 10.1038/s41467-024-47932-y

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