Acetylation-mediated remodeling of the nucleolus regulates cellular acetyl-CoA responses

The metabolite acetyl-coenzyme A (acetyl-CoA) serves as an essential element for a wide range of cellular functions including adenosine triphosphate (ATP) production, lipid synthesis, and protein acetylation. Intracellular acetyl-CoA concentrations are associated with nutrient availability, but the...

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Published inPLoS biology Vol. 18; no. 11; p. e3000981
Main Authors Houston, Ryan, Sekine, Shiori, Calderon, Michael J, Seifuddin, Fayaz, Wang, Guanghui, Kawagishi, Hiroyuki, Malide, Daniela A, Li, Yuesheng, Gucek, Marjan, Pirooznia, Mehdi, Nelson, Alissa J, Stokes, Matthew P, Stewart-Ornstein, Jacob, Mullett, Steven J, Wendell, Stacy G, Watkins, Simon C, Finkel, Toren, Sekine, Yusuke
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.11.2020
Public Library of Science (PLoS)
Subjects
Acetates - metabolism
Acetic acid
Acetyl Coenzyme A - biosynthesis
Acetylation
Adenosine triphosphate
Amino acids
Animal tissues
ATP Citrate (pro-S)-Lyase - deficiency
ATP Citrate (pro-S)-Lyase - genetics
ATP Citrate (pro-S)-Lyase - metabolism
Autophagy
Biological activity
Biology and Life Sciences
Biosynthesis
Cell Line
Cell Nucleolus - metabolism
Cell Nucleolus - ultrastructure
Cell proliferation
Chromatin remodeling
Cloning
CRISPR
Deacetylation
Deprivation
Embryo fibroblasts
Engineering and Technology
Enzymes
Exports
Fatty acids
Fibroblasts
Fibrosarcoma
Gene Expression
Gene Knockout Techniques
Glioblastoma
Glioblastoma cells
Glucose
HCT116 Cells
Hepatocytes
Histone Deacetylases - metabolism
Histones
Humans
Hypoxia
Lipids
Lymphocytes
Lymphocytes T
Metabolic flux
Metabolism
Metabolites
Models, Biological
Nuclear Proteins - metabolism
Nucleoli
Nutrient availability
Nutrients
Physical Sciences
Protein Processing, Post-Translational
Proteins
Research and Analysis Methods
Ribosomal Proteins - metabolism
Signal processing
Signal transduction
Tumor cells
Tumor Suppressor Protein p53 - metabolism
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Abstract The metabolite acetyl-coenzyme A (acetyl-CoA) serves as an essential element for a wide range of cellular functions including adenosine triphosphate (ATP) production, lipid synthesis, and protein acetylation. Intracellular acetyl-CoA concentrations are associated with nutrient availability, but the mechanisms by which a cell responds to fluctuations in acetyl-CoA levels remain elusive. Here, we generate a cell system to selectively manipulate the nucleo-cytoplasmic levels of acetyl-CoA using clustered regularly interspaced short palindromic repeat (CRISPR)-mediated gene editing and acetate supplementation of the culture media. Using this system and quantitative omics analyses, we demonstrate that acetyl-CoA depletion alters the integrity of the nucleolus, impairing ribosomal RNA synthesis and evoking the ribosomal protein-dependent activation of p53. This nucleolar remodeling appears to be mediated through the class IIa histone deacetylases (HDACs). Our findings highlight acetylation-mediated control of the nucleolus as an important hub linking acetyl-CoA fluctuations to cellular stress responses.
AbstractList [...]in accordance with the nutrient availability and the cellular metabolic state, protein acetylation can reversibly regulate a variety of biological processes including gene expression, signal transduction pathways, and metabolic flux [6,7]. [...]accumulating evidence has indicated that in tumor cells, in cells under metabolic stress such as hypoxia, and in certain types of cells such as neurons, T cells, and hepatocytes, the acetate-ACSS2 pathway can play a critical role in cell proliferation, lipid synthesis, and acetylation of histones and non-histone proteins [11,12,18–26]. [...]it has been demonstrated that ACLY-deficient mouse embryonic fibroblasts (MEFs) and LN229 human glioblastoma cells exhibit up-regulation of ACSS2 and that exogenously added acetate can be utilized for acetyl-CoA production in these cells [27]. Recent findings have indicated that acetyl-CoA locally produced in the nucleus by nuclear targeted ACLY or ACSS2 contributes to site-specific histone acetylation, which specifies gene induction and chromatin remodeling in a context dependent manner [22,23,26,29,31–33]. [...]nutrient deprivation or starvation causes a rapid decline in acetyl-CoA levels in cultured cells and in some mouse tissues, which is accompanied by deacetylation of proteins [29,34]. [...]using the clustered regularly interspaced short palindromic repeat (CRISPR)-Cas9 system, we targeted the ACLY gene in HT1080 human fibrosarcoma cells to make ACLY-deficient cell lines.
[...]in accordance with the nutrient availability and the cellular metabolic state, protein acetylation can reversibly regulate a variety of biological processes including gene expression, signal transduction pathways, and metabolic flux [6,7]. [...]accumulating evidence has indicated that in tumor cells, in cells under metabolic stress such as hypoxia, and in certain types of cells such as neurons, T cells, and hepatocytes, the acetate-ACSS2 pathway can play a critical role in cell proliferation, lipid synthesis, and acetylation of histones and non-histone proteins [11,12,18–26]. [...]it has been demonstrated that ACLY-deficient mouse embryonic fibroblasts (MEFs) and LN229 human glioblastoma cells exhibit up-regulation of ACSS2 and that exogenously added acetate can be utilized for acetyl-CoA production in these cells [27]. Recent findings have indicated that acetyl-CoA locally produced in the nucleus by nuclear targeted ACLY or ACSS2 contributes to site-specific histone acetylation, which specifies gene induction and chromatin remodeling in a context dependent manner [22,23,26,29,31–33]. [...]nutrient deprivation or starvation causes a rapid decline in acetyl-CoA levels in cultured cells and in some mouse tissues, which is accompanied by deacetylation of proteins [29,34]. [...]using the clustered regularly interspaced short palindromic repeat (CRISPR)-Cas9 system, we targeted the ACLY gene in HT1080 human fibrosarcoma cells to make ACLY-deficient cell lines.
The metabolite acetyl-coenzyme A (acetyl-CoA) serves as an essential element for a wide range of cellular functions including adenosine triphosphate (ATP) production, lipid synthesis, and protein acetylation. Intracellular acetyl-CoA concentrations are associated with nutrient availability, but the mechanisms by which a cell responds to fluctuations in acetyl-CoA levels remain elusive. Here, we generate a cell system to selectively manipulate the nucleo-cytoplasmic levels of acetyl-CoA using clustered regularly interspaced short palindromic repeat (CRISPR)-mediated gene editing and acetate supplementation of the culture media. Using this system and quantitative omics analyses, we demonstrate that acetyl-CoA depletion alters the integrity of the nucleolus, impairing ribosomal RNA synthesis and evoking the ribosomal protein-dependent activation of p53. This nucleolar remodeling appears to be mediated through the class IIa histone deacetylases (HDACs). Our findings highlight acetylation-mediated control of the nucleolus as an important hub linking acetyl-CoA fluctuations to cellular stress responses.
The metabolite acetyl-coenzyme A (acetyl-CoA) serves as an essential element for a wide range of cellular functions including adenosine triphosphate (ATP) production, lipid synthesis, and protein acetylation. Intracellular acetyl-CoA concentrations are associated with nutrient availability, but the mechanisms by which a cell responds to fluctuations in acetyl-CoA levels remain elusive. Here, we generate a cell system to selectively manipulate the nucleo-cytoplasmic levels of acetyl-CoA using clustered regularly interspaced short palindromic repeat (CRISPR)-mediated gene editing and acetate supplementation of the culture media. Using this system and quantitative omics analyses, we demonstrate that acetyl-CoA depletion alters the integrity of the nucleolus, impairing ribosomal RNA synthesis and evoking the ribosomal protein-dependent activation of p53. This nucleolar remodeling appears to be mediated through the class IIa histone deacetylases (HDACs). Our findings highlight acetylation-mediated control of the nucleolus as an important hub linking acetyl-CoA fluctuations to cellular stress responses. This study describes a cell system that allows the manipulation of intracellular acetyl-CoA levels by acetate, uncovering an important role for the nucleolus and its regulation by class IIa histone deacetylases in mediating cellular responses to acetyl-CoA fluctuations.
The metabolite acetyl-coenzyme A (acetyl-CoA) serves as an essential element for a wide range of cellular functions including adenosine triphosphate (ATP) production, lipid synthesis, and protein acetylation. Intracellular acetyl-CoA concentrations are associated with nutrient availability, but the mechanisms by which a cell responds to fluctuations in acetyl-CoA levels remain elusive. Here, we generate a cell system to selectively manipulate the nucleo-cytoplasmic levels of acetyl-CoA using clustered regularly interspaced short palindromic repeat (CRISPR)-mediated gene editing and acetate supplementation of the culture media. Using this system and quantitative omics analyses, we demonstrate that acetyl-CoA depletion alters the integrity of the nucleolus, impairing ribosomal RNA synthesis and evoking the ribosomal protein-dependent activation of p53. This nucleolar remodeling appears to be mediated through the class IIa histone deacetylases (HDACs). Our findings highlight acetylation-mediated control of the nucleolus as an important hub linking acetyl-CoA fluctuations to cellular stress responses.The metabolite acetyl-coenzyme A (acetyl-CoA) serves as an essential element for a wide range of cellular functions including adenosine triphosphate (ATP) production, lipid synthesis, and protein acetylation. Intracellular acetyl-CoA concentrations are associated with nutrient availability, but the mechanisms by which a cell responds to fluctuations in acetyl-CoA levels remain elusive. Here, we generate a cell system to selectively manipulate the nucleo-cytoplasmic levels of acetyl-CoA using clustered regularly interspaced short palindromic repeat (CRISPR)-mediated gene editing and acetate supplementation of the culture media. Using this system and quantitative omics analyses, we demonstrate that acetyl-CoA depletion alters the integrity of the nucleolus, impairing ribosomal RNA synthesis and evoking the ribosomal protein-dependent activation of p53. This nucleolar remodeling appears to be mediated through the class IIa histone deacetylases (HDACs). Our findings highlight acetylation-mediated control of the nucleolus as an important hub linking acetyl-CoA fluctuations to cellular stress responses.
Author Stewart-Ornstein, Jacob
Finkel, Toren
Houston, Ryan
Stokes, Matthew P
Sekine, Yusuke
Li, Yuesheng
Mullett, Steven J
Calderon, Michael J
Pirooznia, Mehdi
Kawagishi, Hiroyuki
Gucek, Marjan
Nelson, Alissa J
Sekine, Shiori
Wendell, Stacy G
Wang, Guanghui
Seifuddin, Fayaz
Malide, Daniela A
Watkins, Simon C
AuthorAffiliation 3 Department of Cell Biology, Center for Biologic Imaging, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America
4 National Heart, Lung, and Blood Institute, NIH, Bethesda, Maryland, United States of America
7 Department of Pharmacology and Chemical Biology, the Health Sciences Metabolomics and Lipidomics Core, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America
8 Division of Endocrinology and Metabolism, Department of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America
University of Pennsylvania, UNITED STATES
2 Division of Cardiology, Department of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America
5 Cell Signaling Technology, INC., Danvers, Massachusetts, United States of America
1 Aging Institute, Department of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America
6 Department of Computational and Systems Biology, University of Pittsburgh a
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33253182$$D View this record in MEDLINE/PubMed
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SSID ssj0022928
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Snippet The metabolite acetyl-coenzyme A (acetyl-CoA) serves as an essential element for a wide range of cellular functions including adenosine triphosphate (ATP)...
[...]in accordance with the nutrient availability and the cellular metabolic state, protein acetylation can reversibly regulate a variety of biological...
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StartPage e3000981
SubjectTerms Acetates - metabolism
Acetic acid
Acetyl Coenzyme A - biosynthesis
Acetylation
Adenosine triphosphate
Amino acids
Animal tissues
ATP Citrate (pro-S)-Lyase - deficiency
ATP Citrate (pro-S)-Lyase - genetics
ATP Citrate (pro-S)-Lyase - metabolism
Autophagy
Biological activity
Biology and Life Sciences
Biosynthesis
Cell Line
Cell Nucleolus - metabolism
Cell Nucleolus - ultrastructure
Cell proliferation
Chromatin remodeling
Cloning
CRISPR
Deacetylation
Deprivation
Embryo fibroblasts
Engineering and Technology
Enzymes
Exports
Fatty acids
Fibroblasts
Fibrosarcoma
Gene Expression
Gene Knockout Techniques
Glioblastoma
Glioblastoma cells
Glucose
HCT116 Cells
Hepatocytes
Histone Deacetylases - metabolism
Histones
Humans
Hypoxia
Lipids
Lymphocytes
Lymphocytes T
Metabolic flux
Metabolism
Metabolites
Models, Biological
Nuclear Proteins - metabolism
Nucleoli
Nutrient availability
Nutrients
Physical Sciences
Protein Processing, Post-Translational
Proteins
Research and Analysis Methods
Ribosomal Proteins - metabolism
Signal processing
Signal transduction
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Tumor Suppressor Protein p53 - metabolism
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Title Acetylation-mediated remodeling of the nucleolus regulates cellular acetyl-CoA responses
URI https://www.ncbi.nlm.nih.gov/pubmed/33253182
https://www.proquest.com/docview/2479053573
https://www.proquest.com/docview/2466042341
https://pubmed.ncbi.nlm.nih.gov/PMC7728262
https://doaj.org/article/6c3c21ca4aa6456c8fa27412e6208e34
http://dx.doi.org/10.1371/journal.pbio.3000981
Volume 18
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