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Citations to this article

Metabolic stress regulates cytoskeletal dynamics and metastasis of cancer cells
M. Cecilia Caino, … , Silvano Bosari, Dario C. Altieri
M. Cecilia Caino, … , Silvano Bosari, Dario C. Altieri
Published June 10, 2013
Citation Information: J Clin Invest. 2013;123(7):2907-2920. https://doi.org/10.1172/JCI67841.
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Metabolic stress regulates cytoskeletal dynamics and metastasis of cancer cells

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Abstract

Metabolic reprogramming is an important driver of tumor progression; however, the metabolic regulators of tumor cell motility and metastasis are not understood. Here, we show that tumors maintain energy production under nutrient deprivation through the function of HSP90 chaperones compartmentalized in mitochondria. Using cancer cell lines, we found that mitochondrial HSP90 proteins, including tumor necrosis factor receptor–associated protein-1 (TRAP-1), dampen the activation of the nutrient-sensing AMPK and its substrate UNC-51–like kinase (ULK1), preserve cytoskeletal dynamics, and release the cell motility effector focal adhesion kinase (FAK) from inhibition by the autophagy initiator FIP200. In turn, this results in enhanced tumor cell invasion in low nutrients and metastatic dissemination to bone or liver in disease models in mice. Moreover, we found that phosphorylated ULK1 levels were correlated with shortened overall survival in patients with non–small cell lung cancer. These results demonstrate that mitochondrial HSP90 chaperones, including TRAP-1, overcome metabolic stress and promote tumor cell metastasis by limiting the activation of the nutrient sensor AMPK and preventing autophagy.

Authors

M. Cecilia Caino, Young Chan Chae, Valentina Vaira, Stefano Ferrero, Mario Nosotti, Nina M. Martin, Ashani Weeraratna, Michael O’Connell, Danielle Jernigan, Alessandro Fatatis, Lucia R. Languino, Silvano Bosari, Dario C. Altieri

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Trends in Cell Biology 2014
TRAP1 Regulates Proliferation, Mitochondrial Function and has Prognostic Significance in NSCLC
J Agorreta, J Hu, D Liu, D Delia, H Turley, DJ Ferguson, F Iborra, MJ Pajares, M Larrayoz, I Zudaire, R Pio, LM Montuenga, AL Harris, K Gatter, F Pezzella
Molecular cancer research : MCR 2014
In vitro models of tumor vessels and matrix: Engineering approaches to investigate transport limitations and drug delivery in cancer
BR Seo, P DelNero, C Fischbach
Advanced Drug Delivery Reviews 2014
The CT20 peptide causes detachment and death of metastatic breast cancer cells by promoting mitochondrial aggregation and cytoskeletal disruption
MW Lee, R Bassiouni, NA Sparrow, A Iketani, RJ Boohaker, C Moskowitz, P Vishnubhotla, AS Khaled, J Oyer, A Copik, C Fernandez-Valle, JM Perez, AR Khaled
Cell Death and Disease 2014
Deletion of the Mitochondrial Chaperone TRAP-1 Uncovers Global Reprogramming of Metabolic Networks
S Lisanti, M Tavecchio, YC Chae, Q Liu, AK Brice, ML Thakur, LR Languino, DC Altieri
Cell Reports 2014
Down-regulation of malignant potential by alpha linolenic acid in human and mouse colon cancer cells
JP Chamberland, HS Moon
Familial Cancer 2014
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 2009

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