Metabolic reprogramming by Acly inhibition using SB-204990 alters glucoregulation and modulates molecular mechanisms associated with aging

Abstract ATP-citrate lyase is a central integrator of cellular metabolism in the interface of protein, carbohydrate, and lipid metabolism. The physiological consequences as well as the molecular mechanisms orchestrating the response to long-term pharmacologically induced Acly inhibition are unknown....

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Main Authors: Alejandro Sola-García, María Ángeles Cáliz-Molina, Isabel Espadas, Michael Petr, Concepción Panadero-Morón, Daniel González-Morán, María Eugenia Martín-Vázquez, Álvaro Jesús Narbona-Pérez, Livia López-Noriega, Guillermo Martínez-Corrales, Raúl López-Fernández-Sobrino, Alejandro Castillo-Peña, Lina M. Carmona-Marin, Enrique Martínez-Force, Oscar Yanes, Maria Vinaixa, Daniel López-López, José Carlos Reyes, Joaquín Dopazo, Franz Martín, Benoit R. Gauthier, Morten Scheibye-Knudsen, Vivian Capilla-González, Alejandro Martín-Montalvo
Format: Article
Language:English
Published: Nature Portfolio 2023-03-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-023-04625-4
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author Alejandro Sola-García
María Ángeles Cáliz-Molina
Isabel Espadas
Michael Petr
Concepción Panadero-Morón
Daniel González-Morán
María Eugenia Martín-Vázquez
Álvaro Jesús Narbona-Pérez
Livia López-Noriega
Guillermo Martínez-Corrales
Raúl López-Fernández-Sobrino
Alejandro Castillo-Peña
Lina M. Carmona-Marin
Enrique Martínez-Force
Oscar Yanes
Maria Vinaixa
Daniel López-López
José Carlos Reyes
Joaquín Dopazo
Franz Martín
Benoit R. Gauthier
Morten Scheibye-Knudsen
Vivian Capilla-González
Alejandro Martín-Montalvo
author_facet Alejandro Sola-García
María Ángeles Cáliz-Molina
Isabel Espadas
Michael Petr
Concepción Panadero-Morón
Daniel González-Morán
María Eugenia Martín-Vázquez
Álvaro Jesús Narbona-Pérez
Livia López-Noriega
Guillermo Martínez-Corrales
Raúl López-Fernández-Sobrino
Alejandro Castillo-Peña
Lina M. Carmona-Marin
Enrique Martínez-Force
Oscar Yanes
Maria Vinaixa
Daniel López-López
José Carlos Reyes
Joaquín Dopazo
Franz Martín
Benoit R. Gauthier
Morten Scheibye-Knudsen
Vivian Capilla-González
Alejandro Martín-Montalvo
author_sort Alejandro Sola-García
collection DOAJ
description Abstract ATP-citrate lyase is a central integrator of cellular metabolism in the interface of protein, carbohydrate, and lipid metabolism. The physiological consequences as well as the molecular mechanisms orchestrating the response to long-term pharmacologically induced Acly inhibition are unknown. We report here that the Acly inhibitor SB-204990 improves metabolic health and physical strength in wild-type mice when fed with a high-fat diet, while in mice fed with healthy diet results in metabolic imbalance and moderated insulin resistance. By applying a multiomic approach using untargeted metabolomics, transcriptomics, and proteomics, we determined that, in vivo, SB-204990 plays a role in the regulation of molecular mechanisms associated with aging, such as energy metabolism, mitochondrial function, mTOR signaling, and folate cycle, while global alterations on histone acetylation are absent. Our findings indicate a mechanism for regulating molecular pathways of aging that prevents the development of metabolic abnormalities associated with unhealthy dieting. This strategy might be explored for devising therapeutic approaches to prevent metabolic diseases.
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spelling doaj-art-9deabdbc43f647488b325be7381dd75c2025-08-20T02:13:02ZengNature PortfolioCommunications Biology2399-36422023-03-016111910.1038/s42003-023-04625-4Metabolic reprogramming by Acly inhibition using SB-204990 alters glucoregulation and modulates molecular mechanisms associated with agingAlejandro Sola-García0María Ángeles Cáliz-Molina1Isabel Espadas2Michael Petr3Concepción Panadero-Morón4Daniel González-Morán5María Eugenia Martín-Vázquez6Álvaro Jesús Narbona-Pérez7Livia López-Noriega8Guillermo Martínez-Corrales9Raúl López-Fernández-Sobrino10Alejandro Castillo-Peña11Lina M. Carmona-Marin12Enrique Martínez-Force13Oscar Yanes14Maria Vinaixa15Daniel López-López16José Carlos Reyes17Joaquín Dopazo18Franz Martín19Benoit R. Gauthier20Morten Scheibye-Knudsen21Vivian Capilla-González22Alejandro Martín-Montalvo23Andalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideCenter for Healthy Aging, Department of Cellular and Molecular Medicine, University of CopenhagenAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideCenter for Healthy Aging, Department of Cellular and Molecular Medicine, University of CopenhagenInstituto de la Grasa (CSIC), Universidad Pablo de OlavideUniversitat Rovira i Virgili, Department of electronic Engineering & IISPVUniversitat Rovira i Virgili, Department of electronic Engineering & IISPVClinical Bioinformatics Area, Fundación Progreso y Salud (FPS), CDCA, Hospital Virgen del Rocio, c/Manuel Siurot s/nAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideClinical Bioinformatics Area, Fundación Progreso y Salud (FPS), CDCA, Hospital Virgen del Rocio, c/Manuel Siurot s/nAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideCenter for Healthy Aging, Department of Cellular and Molecular Medicine, University of CopenhagenAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideAndalusian Molecular Biology and Regenerative Medicine Centre-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de OlavideAbstract ATP-citrate lyase is a central integrator of cellular metabolism in the interface of protein, carbohydrate, and lipid metabolism. The physiological consequences as well as the molecular mechanisms orchestrating the response to long-term pharmacologically induced Acly inhibition are unknown. We report here that the Acly inhibitor SB-204990 improves metabolic health and physical strength in wild-type mice when fed with a high-fat diet, while in mice fed with healthy diet results in metabolic imbalance and moderated insulin resistance. By applying a multiomic approach using untargeted metabolomics, transcriptomics, and proteomics, we determined that, in vivo, SB-204990 plays a role in the regulation of molecular mechanisms associated with aging, such as energy metabolism, mitochondrial function, mTOR signaling, and folate cycle, while global alterations on histone acetylation are absent. Our findings indicate a mechanism for regulating molecular pathways of aging that prevents the development of metabolic abnormalities associated with unhealthy dieting. This strategy might be explored for devising therapeutic approaches to prevent metabolic diseases.https://doi.org/10.1038/s42003-023-04625-4
spellingShingle Alejandro Sola-García
María Ángeles Cáliz-Molina
Isabel Espadas
Michael Petr
Concepción Panadero-Morón
Daniel González-Morán
María Eugenia Martín-Vázquez
Álvaro Jesús Narbona-Pérez
Livia López-Noriega
Guillermo Martínez-Corrales
Raúl López-Fernández-Sobrino
Alejandro Castillo-Peña
Lina M. Carmona-Marin
Enrique Martínez-Force
Oscar Yanes
Maria Vinaixa
Daniel López-López
José Carlos Reyes
Joaquín Dopazo
Franz Martín
Benoit R. Gauthier
Morten Scheibye-Knudsen
Vivian Capilla-González
Alejandro Martín-Montalvo
Metabolic reprogramming by Acly inhibition using SB-204990 alters glucoregulation and modulates molecular mechanisms associated with aging
Communications Biology
title Metabolic reprogramming by Acly inhibition using SB-204990 alters glucoregulation and modulates molecular mechanisms associated with aging
title_full Metabolic reprogramming by Acly inhibition using SB-204990 alters glucoregulation and modulates molecular mechanisms associated with aging
title_fullStr Metabolic reprogramming by Acly inhibition using SB-204990 alters glucoregulation and modulates molecular mechanisms associated with aging
title_full_unstemmed Metabolic reprogramming by Acly inhibition using SB-204990 alters glucoregulation and modulates molecular mechanisms associated with aging
title_short Metabolic reprogramming by Acly inhibition using SB-204990 alters glucoregulation and modulates molecular mechanisms associated with aging
title_sort metabolic reprogramming by acly inhibition using sb 204990 alters glucoregulation and modulates molecular mechanisms associated with aging
url https://doi.org/10.1038/s42003-023-04625-4
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