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Endothelial cells metabolically regulate breast cancer invasion toward a microvessel

Breast cancer metastasis is initiated by invasion of tumor cells into the collagen type I-rich stroma to reach adjacent blood vessels. Prior work has identified that metabolic plasticity is a key requirement of tumor cell invasion into collagen. However, it remains largely unclear how blood vessels...

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Autores principales: Tan, Matthew L., Jenkins-Johnston, Niaa, Huang, Sarah, Schutrum, Brittany, Vadhin, Sandra, Adhikari, Abhinav, Williams, Rebecca M., Zipfel, Warren R., Lammerding, Jan, Varner, Jeffrey D., Fischbach, Claudia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: AIP Publishing LLC 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10697723/
http://dx.doi.org/10.1063/5.0171109
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author Tan, Matthew L.
Jenkins-Johnston, Niaa
Huang, Sarah
Schutrum, Brittany
Vadhin, Sandra
Adhikari, Abhinav
Williams, Rebecca M.
Zipfel, Warren R.
Lammerding, Jan
Varner, Jeffrey D.
Fischbach, Claudia
author_facet Tan, Matthew L.
Jenkins-Johnston, Niaa
Huang, Sarah
Schutrum, Brittany
Vadhin, Sandra
Adhikari, Abhinav
Williams, Rebecca M.
Zipfel, Warren R.
Lammerding, Jan
Varner, Jeffrey D.
Fischbach, Claudia
author_sort Tan, Matthew L.
collection PubMed
description Breast cancer metastasis is initiated by invasion of tumor cells into the collagen type I-rich stroma to reach adjacent blood vessels. Prior work has identified that metabolic plasticity is a key requirement of tumor cell invasion into collagen. However, it remains largely unclear how blood vessels affect this relationship. Here, we developed a microfluidic platform to analyze how tumor cells invade collagen in the presence and absence of a microvascular channel. We demonstrate that endothelial cells secrete pro-migratory factors that direct tumor cell invasion toward the microvessel. Analysis of tumor cell metabolism using metabolic imaging, metabolomics, and computational flux balance analysis revealed that these changes are accompanied by increased rates of glycolysis and oxygen consumption caused by broad alterations of glucose metabolism. Indeed, restricting glucose availability decreased endothelial cell-induced tumor cell invasion. Our results suggest that endothelial cells promote tumor invasion into the stroma due, in part, to reprogramming tumor cell metabolism.
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spelling pubmed-106977232023-12-06 Endothelial cells metabolically regulate breast cancer invasion toward a microvessel Tan, Matthew L. Jenkins-Johnston, Niaa Huang, Sarah Schutrum, Brittany Vadhin, Sandra Adhikari, Abhinav Williams, Rebecca M. Zipfel, Warren R. Lammerding, Jan Varner, Jeffrey D. Fischbach, Claudia APL Bioeng Articles Breast cancer metastasis is initiated by invasion of tumor cells into the collagen type I-rich stroma to reach adjacent blood vessels. Prior work has identified that metabolic plasticity is a key requirement of tumor cell invasion into collagen. However, it remains largely unclear how blood vessels affect this relationship. Here, we developed a microfluidic platform to analyze how tumor cells invade collagen in the presence and absence of a microvascular channel. We demonstrate that endothelial cells secrete pro-migratory factors that direct tumor cell invasion toward the microvessel. Analysis of tumor cell metabolism using metabolic imaging, metabolomics, and computational flux balance analysis revealed that these changes are accompanied by increased rates of glycolysis and oxygen consumption caused by broad alterations of glucose metabolism. Indeed, restricting glucose availability decreased endothelial cell-induced tumor cell invasion. Our results suggest that endothelial cells promote tumor invasion into the stroma due, in part, to reprogramming tumor cell metabolism. AIP Publishing LLC 2023-12-04 /pmc/articles/PMC10697723/ http://dx.doi.org/10.1063/5.0171109 Text en © 2023 Author(s). https://creativecommons.org/licenses/by/4.0/All article content, except where otherwise noted, is licensed under a Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ).
spellingShingle Articles
Tan, Matthew L.
Jenkins-Johnston, Niaa
Huang, Sarah
Schutrum, Brittany
Vadhin, Sandra
Adhikari, Abhinav
Williams, Rebecca M.
Zipfel, Warren R.
Lammerding, Jan
Varner, Jeffrey D.
Fischbach, Claudia
Endothelial cells metabolically regulate breast cancer invasion toward a microvessel
title Endothelial cells metabolically regulate breast cancer invasion toward a microvessel
title_full Endothelial cells metabolically regulate breast cancer invasion toward a microvessel
title_fullStr Endothelial cells metabolically regulate breast cancer invasion toward a microvessel
title_full_unstemmed Endothelial cells metabolically regulate breast cancer invasion toward a microvessel
title_short Endothelial cells metabolically regulate breast cancer invasion toward a microvessel
title_sort endothelial cells metabolically regulate breast cancer invasion toward a microvessel
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10697723/
http://dx.doi.org/10.1063/5.0171109
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