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Cancer-associated cells release citrate to support tumour metastatic progression

by Federlin, Marianne , Mycielska, Maria E , Riegel, Dania , Proescholdt, Martin , Heinke, Stefanie , Haerteis, Silke , Parkinson, Eric K , Jordan, Katrin , Aung, Thiha , Berneburg, Mark , Wagner, Christine , Adamski, Jerzy , Gaumann, Andreas , Schwertner, Barbara , Geissler, Edward K , Stanton, Evan H , Liebisch, Gerhard , Ziegler, Christine , Klein, Christoph A , Buchalla, Wolfgang , Milenkovic, Vladimir M , Schmidl, Christian , Tokarz, Janina , Drexler, Konstantin , Madej, Gregor , Schmidt, Katharina M , Artati, Anna , Wetzel, Christian H , Kolodziejczyk, Maria , Jagla, Wolfgang , Haferkamp, Sebastian , Brabletz, Thomas , Cecil, Alexander , Schlitt, Hans J

in Amino acids / Angiogenesis / Cancer / Cancer-Associated Fibroblasts - metabolism / Cancer-Associated Fibroblasts - physiology / Cell interactions / Cell Line, Tumor / Citric acid / Citric Acid - metabolism / Epigenesis, Genetic / Epigenetics / Fatty acids / Fibroblasts / Humans / Invasiveness / Metabolism / Metabolites / Metastases / Metastasis / Neoplasm Metastasis - genetics / Neoplasm Metastasis - pathology / Pancreatic cancer / Pancreatic Neoplasms / Pancreatic Neoplasms - metabolism / Pancreatic Neoplasms - pathology / Prostate / Stroma / Stromal Cells - metabolism / Tumor Microenvironment - physiology / Tumors

2021

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2021

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2021

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Journal Article

Cancer-associated cells release citrate to support tumour metastatic progression

Federlin, Marianne,

Mycielska, Maria E,

Riegel, Dania,

Proescholdt, Martin,

Heinke, Stefanie,

Haerteis, Silke,

Parkinson, Eric K,

Jordan, Katrin,

Aung, Thiha,

Berneburg, Mark,

Wagner, Christine,

Adamski, Jerzy,

Gaumann, Andreas,

Schwertner, Barbara,

Geissler, Edward K,

Stanton, Evan H,

Liebisch, Gerhard,

Ziegler, Christine,

Klein, Christoph A,

Buchalla, Wolfgang,

Milenkovic, Vladimir M,

Schmidl, Christian,

Tokarz, Janina,

Drexler, Konstantin,

Madej, Gregor,

Schmidt, Katharina M,

Artati, Anna,

Wetzel, Christian H,

Kolodziejczyk, Maria,

Jagla, Wolfgang,

Haferkamp, Sebastian,

Brabletz, Thomas,

Cecil, Alexander,

Schlitt, Hans J

2021

Overview

Citrate is important for lipid synthesis and epigenetic regulation in addition to ATP production. We have previously reported that cancer cells import extracellular citrate via the pmCiC transporter to support their metabolism. Here, we show for the first time that citrate is supplied to cancer by cancer-associated stroma (CAS) and also that citrate synthesis and release is one of the latter’s major metabolic tasks. Citrate release from CAS is controlled by cancer cells through cross-cellular communication. The availability of citrate from CAS regulated the cytokine profile, metabolism and features of cellular invasion. Moreover, citrate released by CAS is involved in inducing cancer progression especially enhancing invasiveness and organ colonisation. In line with the in vitro observations, we show that depriving cancer cells of citrate using gluconate, a specific inhibitor of pmCiC, significantly reduced the growth and metastatic spread of human pancreatic cancer cells in vivo and muted stromal activation and angiogenesis. We conclude that citrate is supplied to tumour cells by CAS and citrate uptake plays a significant role in cancer metastatic progression.

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Publisher

Life Science Alliance,Life Science Alliance LLC

Subject

Amino acids

/ Angiogenesis

/ Cancer

/ Cancer-Associated Fibroblasts - metabolism

/ Cancer-Associated Fibroblasts - physiology

/ Cell interactions

/ Cell Line, Tumor