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The TGF-β/HDAC7 axis suppresses TCA cycle metabolism in renal cancer

Mounting evidence points to alterations in mitochondrial metabolism in renal cell carcinoma (RCC). However, the mechanisms that regulate the TCA cycle in RCC remain uncharacterized. Here, we demonstrate that loss of TCA cycle enzyme expression is retained in RCC metastatic tissues. Moreover, proteom...

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Autores principales: Nam, Hyeyoung, Kundu, Anirban, Karki, Suman, Brinkley, Garrett J., Chandrashekar, Darshan S., Kirkman, Richard L., Liu, Juan, Liberti, Maria V., Locasale, Jason W., Mitchell, Tanecia, Varambally, Sooryanarayana, Sudarshan, Sunil
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Clinical Investigation 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8663777/
https://www.ncbi.nlm.nih.gov/pubmed/34609963
http://dx.doi.org/10.1172/jci.insight.148438
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author Nam, Hyeyoung
Kundu, Anirban
Karki, Suman
Brinkley, Garrett J.
Chandrashekar, Darshan S.
Kirkman, Richard L.
Liu, Juan
Liberti, Maria V.
Locasale, Jason W.
Mitchell, Tanecia
Varambally, Sooryanarayana
Sudarshan, Sunil
author_facet Nam, Hyeyoung
Kundu, Anirban
Karki, Suman
Brinkley, Garrett J.
Chandrashekar, Darshan S.
Kirkman, Richard L.
Liu, Juan
Liberti, Maria V.
Locasale, Jason W.
Mitchell, Tanecia
Varambally, Sooryanarayana
Sudarshan, Sunil
author_sort Nam, Hyeyoung
collection PubMed
description Mounting evidence points to alterations in mitochondrial metabolism in renal cell carcinoma (RCC). However, the mechanisms that regulate the TCA cycle in RCC remain uncharacterized. Here, we demonstrate that loss of TCA cycle enzyme expression is retained in RCC metastatic tissues. Moreover, proteomic analysis demonstrates that reduced TCA cycle enzyme expression is far more pronounced in RCC relative to other tumor types. Loss of TCA cycle enzyme expression is correlated with reduced expression of the transcription factor PGC-1α, which is also lost in RCC tissues. PGC-1α reexpression in RCC cells restores the expression of TCA cycle enzymes in vitro and in vivo and leads to enhanced glucose carbon incorporation into TCA cycle intermediates. Mechanistically, TGF-β signaling, in concert with histone deacetylase 7 (HDAC7), suppresses TCA cycle enzyme expression. Our studies show that pharmacologic inhibition of TGF-β restores the expression of TCA cycle enzymes and suppresses tumor growth in an orthotopic model of RCC. Taken together, this investigation reveals a potentially novel role for the TGF-β/HDAC7 axis in global suppression of TCA cycle enzymes in RCC and provides insight into the molecular basis of altered mitochondrial metabolism in this malignancy.
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spelling pubmed-86637772021-12-15 The TGF-β/HDAC7 axis suppresses TCA cycle metabolism in renal cancer Nam, Hyeyoung Kundu, Anirban Karki, Suman Brinkley, Garrett J. Chandrashekar, Darshan S. Kirkman, Richard L. Liu, Juan Liberti, Maria V. Locasale, Jason W. Mitchell, Tanecia Varambally, Sooryanarayana Sudarshan, Sunil JCI Insight Research Article Mounting evidence points to alterations in mitochondrial metabolism in renal cell carcinoma (RCC). However, the mechanisms that regulate the TCA cycle in RCC remain uncharacterized. Here, we demonstrate that loss of TCA cycle enzyme expression is retained in RCC metastatic tissues. Moreover, proteomic analysis demonstrates that reduced TCA cycle enzyme expression is far more pronounced in RCC relative to other tumor types. Loss of TCA cycle enzyme expression is correlated with reduced expression of the transcription factor PGC-1α, which is also lost in RCC tissues. PGC-1α reexpression in RCC cells restores the expression of TCA cycle enzymes in vitro and in vivo and leads to enhanced glucose carbon incorporation into TCA cycle intermediates. Mechanistically, TGF-β signaling, in concert with histone deacetylase 7 (HDAC7), suppresses TCA cycle enzyme expression. Our studies show that pharmacologic inhibition of TGF-β restores the expression of TCA cycle enzymes and suppresses tumor growth in an orthotopic model of RCC. Taken together, this investigation reveals a potentially novel role for the TGF-β/HDAC7 axis in global suppression of TCA cycle enzymes in RCC and provides insight into the molecular basis of altered mitochondrial metabolism in this malignancy. American Society for Clinical Investigation 2021-11-22 /pmc/articles/PMC8663777/ /pubmed/34609963 http://dx.doi.org/10.1172/jci.insight.148438 Text en © 2021 Nam et al. https://creativecommons.org/licenses/by/4.0/This work is licensed under the Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Nam, Hyeyoung
Kundu, Anirban
Karki, Suman
Brinkley, Garrett J.
Chandrashekar, Darshan S.
Kirkman, Richard L.
Liu, Juan
Liberti, Maria V.
Locasale, Jason W.
Mitchell, Tanecia
Varambally, Sooryanarayana
Sudarshan, Sunil
The TGF-β/HDAC7 axis suppresses TCA cycle metabolism in renal cancer
title The TGF-β/HDAC7 axis suppresses TCA cycle metabolism in renal cancer
title_full The TGF-β/HDAC7 axis suppresses TCA cycle metabolism in renal cancer
title_fullStr The TGF-β/HDAC7 axis suppresses TCA cycle metabolism in renal cancer
title_full_unstemmed The TGF-β/HDAC7 axis suppresses TCA cycle metabolism in renal cancer
title_short The TGF-β/HDAC7 axis suppresses TCA cycle metabolism in renal cancer
title_sort tgf-β/hdac7 axis suppresses tca cycle metabolism in renal cancer
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8663777/
https://www.ncbi.nlm.nih.gov/pubmed/34609963
http://dx.doi.org/10.1172/jci.insight.148438
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