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Molecular Cancer Research
Molecular Cancer Research
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Metabolism

Secreted Factors from Adipose Tissue Reprogram Tumor Lipid Metabolism and Induce Motility by Modulating PPARα/ANGPTL4 and FAK

Christina Blücher, Sabine Iberl, Nancy Schwagarus, Silvana Müller, Gerhard Liebisch, Marcus Höring, Maria Soledad Hidrobo, Josef Ecker, Nick Spindler, Arne Dietrich, Ralph Burkhardt and Sonja C. Stadler
Christina Blücher
1Institute of Clinical Chemistry and Laboratory Medicine, University Hospital Regensburg, Regensburg, Germany.
2LIFE Leipzig Research Center for Civilization Diseases, University of Leipzig, Leipzig, Germany.
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  • ORCID record for Christina Blücher
Sabine Iberl
1Institute of Clinical Chemistry and Laboratory Medicine, University Hospital Regensburg, Regensburg, Germany.
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Nancy Schwagarus
3Institute of Laboratory Medicine, Clinical Chemistry and Molecular Diagnostics, University Hospital Leipzig, Leipzig, Germany.
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Silvana Müller
3Institute of Laboratory Medicine, Clinical Chemistry and Molecular Diagnostics, University Hospital Leipzig, Leipzig, Germany.
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Gerhard Liebisch
1Institute of Clinical Chemistry and Laboratory Medicine, University Hospital Regensburg, Regensburg, Germany.
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  • ORCID record for Gerhard Liebisch
Marcus Höring
1Institute of Clinical Chemistry and Laboratory Medicine, University Hospital Regensburg, Regensburg, Germany.
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Maria Soledad Hidrobo
4ZIEL - Institute for Food & Health, Research Group Lipid Metabolism, Technical University of Munich, Munich, Germany.
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Josef Ecker
4ZIEL - Institute for Food & Health, Research Group Lipid Metabolism, Technical University of Munich, Munich, Germany.
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Nick Spindler
5Department of Orthopedics, Trauma and Plastic Surgery, University Hospital Leipzig, Leipzig, Germany.
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Arne Dietrich
6Department of Visceral, Transplantation, Vascular and Thoracic Surgery, University Hospital Leipzig, Leipzig, Germany.
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Ralph Burkhardt
1Institute of Clinical Chemistry and Laboratory Medicine, University Hospital Regensburg, Regensburg, Germany.
2LIFE Leipzig Research Center for Civilization Diseases, University of Leipzig, Leipzig, Germany.
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  • ORCID record for Ralph Burkhardt
Sonja C. Stadler
1Institute of Clinical Chemistry and Laboratory Medicine, University Hospital Regensburg, Regensburg, Germany.
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  • For correspondence: Sonja.Stadler@klinik.uni-regensburg.de
DOI: 10.1158/1541-7786.MCR-19-1223 Published December 2020
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Abstract

Recent studies indicate that adipose tissue in obesity promotes breast cancer progression by secreting protumorigenic chemokines, growth factors, and fatty acids. However, the detailed mechanisms by which hypertrophic adipose tissue influences breast cancer cells are still not well understood. Here we show that co-culture with adipose tissue from high-fat diet induced obese C57BL/6 mice alters transcriptome profiles in triple-negative breast cancer (TNBC) cells, leading to upregulation of genes involved in inflammation and lipid metabolism, such as IL1B, PLIN2, and ANGPTL4. Similar results were obtained by treating TNBC cells with adipose tissue conditioned media (ACM) generated from fat tissue of obese female patients. Many of the upregulated genes were activated by PPAR nuclear receptors, as shown by pathway analyses and gene expression experiments using PPAR agonists and antagonists. Metabolic analysis revealed that TNBC cells cultivated with ACM had significantly higher levels of β-oxidation. Furthermore, ACM-treated TNBC cells displayed a pronounced aggressive cell phenotype, with enhanced wound healing, proliferation, and invasion capabilities. ACM-induced invasion was dependent on the PPAR-target ANGPTL4 and activated FAK signaling, as shown by ANGPTL4 depletion and FAK inhibition. Together, our data suggest that factors released by adipose tissue change PPAR-regulated gene expression and lipid metabolism and induce a more aggressive TNBC cell phenotype. These effects are, at least in parts, mediated by fatty acids provided by the adipose tissue.

Implications: Adipose tissue provides factors for increased progression of TNBC cells, identifying PPAR- and FAK-signaling as potential novel targets for treatment of TNBC, especially in obese women.

Footnotes

  • Note: Supplementary data for this article are available at Molecular Cancer Research Online (http://mcr.aacrjournals.org/).

  • Mol Cancer Res 2020;18:1849–62

  • Received December 19, 2019.
  • Revision received July 16, 2020.
  • Accepted August 24, 2020.
  • Published first August 28, 2020.
  • ©2020 American Association for Cancer Research.
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Molecular Cancer Research: 18 (12)
December 2020
Volume 18, Issue 12
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Secreted Factors from Adipose Tissue Reprogram Tumor Lipid Metabolism and Induce Motility by Modulating PPARα/ANGPTL4 and FAK
Christina Blücher, Sabine Iberl, Nancy Schwagarus, Silvana Müller, Gerhard Liebisch, Marcus Höring, Maria Soledad Hidrobo, Josef Ecker, Nick Spindler, Arne Dietrich, Ralph Burkhardt and Sonja C. Stadler
Mol Cancer Res December 1 2020 (18) (12) 1849-1862; DOI: 10.1158/1541-7786.MCR-19-1223

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Secreted Factors from Adipose Tissue Reprogram Tumor Lipid Metabolism and Induce Motility by Modulating PPARα/ANGPTL4 and FAK
Christina Blücher, Sabine Iberl, Nancy Schwagarus, Silvana Müller, Gerhard Liebisch, Marcus Höring, Maria Soledad Hidrobo, Josef Ecker, Nick Spindler, Arne Dietrich, Ralph Burkhardt and Sonja C. Stadler
Mol Cancer Res December 1 2020 (18) (12) 1849-1862; DOI: 10.1158/1541-7786.MCR-19-1223
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