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Dynamic partitioning of branched-chain amino acids-derived nitrogen supports renal cancer progression

Metabolic reprogramming is critical for tumor initiation and progression. However, the exact impact of specific metabolic changes on cancer progression is poorly understood. Here, we integrate multimodal analyses of primary and metastatic clonally-related clear cell renal cancer cells (ccRCC) grown...

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Autores principales: Sciacovelli, Marco, Dugourd, Aurelien, Jimenez, Lorea Valcarcel, Yang, Ming, Nikitopoulou, Efterpi, Costa, Ana S. H., Tronci, Laura, Caraffini, Veronica, Rodrigues, Paulo, Schmidt, Christina, Ryan, Dylan Gerard, Young, Timothy, Zecchini, Vincent R., Rossi, Sabrina H., Massie, Charlie, Lohoff, Caroline, Masid, Maria, Hatzimanikatis, Vassily, Kuppe, Christoph, Von Kriegsheim, Alex, Kramann, Rafael, Gnanapragasam, Vincent, Warren, Anne Y., Stewart, Grant D., Erez, Ayelet, Vanharanta, Sakari, Saez-Rodriguez, Julio, Frezza, Christian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9767928/
https://www.ncbi.nlm.nih.gov/pubmed/36539415
http://dx.doi.org/10.1038/s41467-022-35036-4
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author Sciacovelli, Marco
Dugourd, Aurelien
Jimenez, Lorea Valcarcel
Yang, Ming
Nikitopoulou, Efterpi
Costa, Ana S. H.
Tronci, Laura
Caraffini, Veronica
Rodrigues, Paulo
Schmidt, Christina
Ryan, Dylan Gerard
Young, Timothy
Zecchini, Vincent R.
Rossi, Sabrina H.
Massie, Charlie
Lohoff, Caroline
Masid, Maria
Hatzimanikatis, Vassily
Kuppe, Christoph
Von Kriegsheim, Alex
Kramann, Rafael
Gnanapragasam, Vincent
Warren, Anne Y.
Stewart, Grant D.
Erez, Ayelet
Vanharanta, Sakari
Saez-Rodriguez, Julio
Frezza, Christian
author_facet Sciacovelli, Marco
Dugourd, Aurelien
Jimenez, Lorea Valcarcel
Yang, Ming
Nikitopoulou, Efterpi
Costa, Ana S. H.
Tronci, Laura
Caraffini, Veronica
Rodrigues, Paulo
Schmidt, Christina
Ryan, Dylan Gerard
Young, Timothy
Zecchini, Vincent R.
Rossi, Sabrina H.
Massie, Charlie
Lohoff, Caroline
Masid, Maria
Hatzimanikatis, Vassily
Kuppe, Christoph
Von Kriegsheim, Alex
Kramann, Rafael
Gnanapragasam, Vincent
Warren, Anne Y.
Stewart, Grant D.
Erez, Ayelet
Vanharanta, Sakari
Saez-Rodriguez, Julio
Frezza, Christian
author_sort Sciacovelli, Marco
collection PubMed
description Metabolic reprogramming is critical for tumor initiation and progression. However, the exact impact of specific metabolic changes on cancer progression is poorly understood. Here, we integrate multimodal analyses of primary and metastatic clonally-related clear cell renal cancer cells (ccRCC) grown in physiological media to identify key stage-specific metabolic vulnerabilities. We show that a VHL loss-dependent reprogramming of branched-chain amino acid catabolism sustains the de novo biosynthesis of aspartate and arginine enabling tumor cells with the flexibility of partitioning the nitrogen of the amino acids depending on their needs. Importantly, we identify the epigenetic reactivation of argininosuccinate synthase (ASS1), a urea cycle enzyme suppressed in primary ccRCC, as a crucial event for metastatic renal cancer cells to acquire the capability to generate arginine, invade in vitro and metastasize in vivo. Overall, our study uncovers a mechanism of metabolic flexibility occurring during ccRCC progression, paving the way for the development of novel stage-specific therapies.
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spelling pubmed-97679282022-12-22 Dynamic partitioning of branched-chain amino acids-derived nitrogen supports renal cancer progression Sciacovelli, Marco Dugourd, Aurelien Jimenez, Lorea Valcarcel Yang, Ming Nikitopoulou, Efterpi Costa, Ana S. H. Tronci, Laura Caraffini, Veronica Rodrigues, Paulo Schmidt, Christina Ryan, Dylan Gerard Young, Timothy Zecchini, Vincent R. Rossi, Sabrina H. Massie, Charlie Lohoff, Caroline Masid, Maria Hatzimanikatis, Vassily Kuppe, Christoph Von Kriegsheim, Alex Kramann, Rafael Gnanapragasam, Vincent Warren, Anne Y. Stewart, Grant D. Erez, Ayelet Vanharanta, Sakari Saez-Rodriguez, Julio Frezza, Christian Nat Commun Article Metabolic reprogramming is critical for tumor initiation and progression. However, the exact impact of specific metabolic changes on cancer progression is poorly understood. Here, we integrate multimodal analyses of primary and metastatic clonally-related clear cell renal cancer cells (ccRCC) grown in physiological media to identify key stage-specific metabolic vulnerabilities. We show that a VHL loss-dependent reprogramming of branched-chain amino acid catabolism sustains the de novo biosynthesis of aspartate and arginine enabling tumor cells with the flexibility of partitioning the nitrogen of the amino acids depending on their needs. Importantly, we identify the epigenetic reactivation of argininosuccinate synthase (ASS1), a urea cycle enzyme suppressed in primary ccRCC, as a crucial event for metastatic renal cancer cells to acquire the capability to generate arginine, invade in vitro and metastasize in vivo. Overall, our study uncovers a mechanism of metabolic flexibility occurring during ccRCC progression, paving the way for the development of novel stage-specific therapies. Nature Publishing Group UK 2022-12-20 /pmc/articles/PMC9767928/ /pubmed/36539415 http://dx.doi.org/10.1038/s41467-022-35036-4 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Sciacovelli, Marco
Dugourd, Aurelien
Jimenez, Lorea Valcarcel
Yang, Ming
Nikitopoulou, Efterpi
Costa, Ana S. H.
Tronci, Laura
Caraffini, Veronica
Rodrigues, Paulo
Schmidt, Christina
Ryan, Dylan Gerard
Young, Timothy
Zecchini, Vincent R.
Rossi, Sabrina H.
Massie, Charlie
Lohoff, Caroline
Masid, Maria
Hatzimanikatis, Vassily
Kuppe, Christoph
Von Kriegsheim, Alex
Kramann, Rafael
Gnanapragasam, Vincent
Warren, Anne Y.
Stewart, Grant D.
Erez, Ayelet
Vanharanta, Sakari
Saez-Rodriguez, Julio
Frezza, Christian
Dynamic partitioning of branched-chain amino acids-derived nitrogen supports renal cancer progression
title Dynamic partitioning of branched-chain amino acids-derived nitrogen supports renal cancer progression
title_full Dynamic partitioning of branched-chain amino acids-derived nitrogen supports renal cancer progression
title_fullStr Dynamic partitioning of branched-chain amino acids-derived nitrogen supports renal cancer progression
title_full_unstemmed Dynamic partitioning of branched-chain amino acids-derived nitrogen supports renal cancer progression
title_short Dynamic partitioning of branched-chain amino acids-derived nitrogen supports renal cancer progression
title_sort dynamic partitioning of branched-chain amino acids-derived nitrogen supports renal cancer progression
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9767928/
https://www.ncbi.nlm.nih.gov/pubmed/36539415
http://dx.doi.org/10.1038/s41467-022-35036-4
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