PHA-4/FoxA senses nucleolar stress to regulate lipid accumulation in Caenorhabditis elegans

The primary function of the nucleolus is ribosome biogenesis, which is an extremely energetically expensive process. Failures in ribosome biogenesis cause nucleolar stress with an altered energy status. However, little is known about the underlying mechanism linking nucleolar stress to energy metabo...

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Published inNature communications Vol. 9; no. 1; pp. 1195 - 17
Main Authors Wu, Jieyu, Jiang, Xue, Li, Yamei, Zhu, Tingting, Zhang, Jingjing, Zhang, Zhiguo, Zhang, Linqiang, Zhang, Yuru, Wang, Yanli, Zou, Xiaoju, Liang, Bin
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 22.03.2018
Nature Publishing Group
Nature Portfolio
Subjects
38
38/89
631/443/319
631/80/86/2366
64
64/11
82/1
Accumulation
Acetyl-CoA carboxylase
Actinomycin
Biosynthesis
Deactivation
Diacylglycerol O-acyltransferase
Diglycerides
Energy balance
Energy metabolism
Energy storage
Fatty acids
Fatty-acid synthase
Gene expression
Humanities and Social Sciences
Inactivation
Lipids
Lipogenesis
Metabolism
multidisciplinary
Nucleoli
Ribonucleic acid
Ribosomal protein S6
Ribosomal protein S6 kinase
RNA
RNA processing
rRNA
Science
Science (multidisciplinary)
Starvation
Stress
Stresses
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Abstract The primary function of the nucleolus is ribosome biogenesis, which is an extremely energetically expensive process. Failures in ribosome biogenesis cause nucleolar stress with an altered energy status. However, little is known about the underlying mechanism linking nucleolar stress to energy metabolism. Here we show that nucleolar stress is triggered by inactivation of RSKS-1 (ribosomal protein S6 kinase), RRP-8 (ribosomal RNA processing 8), and PRO-2/3 (proximal proliferation), all of which are involved in ribosomal RNA processing or inhibition of rDNA transcription by actinomycin D (AD), leading to excessive lipid accumulation in Caenorhabditis elegans . The transcription factor PHA-4/FoxA acts as a sensor of nucleolar stress to bind to and transactivate the expression of the lipogenic genes pod-2 (acetyl-CoA carboxylase), fasn-1 (fatty acid synthase), and dgat-2 (diacylglycerol O -acyltransferase 2), consequently promoting lipid accumulation. Importantly, inactivation of pha-4 or dgat-2 is sufficient to abolish nucleolar stress-induced lipid accumulation and prolonged starvation survival. The results revealed a distinct PHA-4-mediated lipogenesis pathway that senses nucleolar stress and shifts excessive energy for storage as fat. Nucleolar stress can disrupt ribosome biogenesis and in turn energy metabolism and lipid storage, but how this is regulated is unclear. Here, the authors show in C. elegans that the transcription factor PHA-4/FOXA acts as a sensor for nucleolar stress and can regulate expression of lipogenic genes
AbstractList Abstract The primary function of the nucleolus is ribosome biogenesis, which is an extremely energetically expensive process. Failures in ribosome biogenesis cause nucleolar stress with an altered energy status. However, little is known about the underlying mechanism linking nucleolar stress to energy metabolism. Here we show that nucleolar stress is triggered by inactivation of RSKS-1 (ribosomal protein S6 kinase), RRP-8 (ribosomal RNA processing 8), and PRO-2/3 (proximal proliferation), all of which are involved in ribosomal RNA processing or inhibition of rDNA transcription by actinomycin D (AD), leading to excessive lipid accumulation in Caenorhabditis elegans . The transcription factor PHA-4/FoxA acts as a sensor of nucleolar stress to bind to and transactivate the expression of the lipogenic genes pod-2 (acetyl-CoA carboxylase), fasn-1 (fatty acid synthase), and dgat-2 (diacylglycerol O -acyltransferase 2), consequently promoting lipid accumulation. Importantly, inactivation of pha-4 or dgat-2 is sufficient to abolish nucleolar stress-induced lipid accumulation and prolonged starvation survival. The results revealed a distinct PHA-4-mediated lipogenesis pathway that senses nucleolar stress and shifts excessive energy for storage as fat.
The primary function of the nucleolus is ribosome biogenesis, which is an extremely energetically expensive process. Failures in ribosome biogenesis cause nucleolar stress with an altered energy status. However, little is known about the underlying mechanism linking nucleolar stress to energy metabolism. Here we show that nucleolar stress is triggered by inactivation of RSKS-1 (ribosomal protein S6 kinase), RRP-8 (ribosomal RNA processing 8), and PRO-2/3 (proximal proliferation), all of which are involved in ribosomal RNA processing or inhibition of rDNA transcription by actinomycin D (AD), leading to excessive lipid accumulation in Caenorhabditiselegans. The transcription factor PHA-4/FoxA acts as a sensor of nucleolar stress to bind to and transactivate the expression of the lipogenic genes pod-2 (acetyl-CoA carboxylase), fasn-1 (fatty acid synthase), and dgat-2 (diacylglycerol O-acyltransferase 2), consequently promoting lipid accumulation. Importantly, inactivation of pha-4 or dgat-2 is sufficient to abolish nucleolar stress-induced lipid accumulation and prolonged starvation survival. The results revealed a distinct PHA-4-mediated lipogenesis pathway that senses nucleolar stress and shifts excessive energy for storage as fat.
The primary function of the nucleolus is ribosome biogenesis, which is an extremely energetically expensive process. Failures in ribosome biogenesis cause nucleolar stress with an altered energy status. However, little is known about the underlying mechanism linking nucleolar stress to energy metabolism. Here we show that nucleolar stress is triggered by inactivation of RSKS-1 (ribosomal protein S6 kinase), RRP-8 (ribosomal RNA processing 8), and PRO-2/3 (proximal proliferation), all of which are involved in ribosomal RNA processing or inhibition of rDNA transcription by actinomycin D (AD), leading to excessive lipid accumulation in Caenorhabditis elegans . The transcription factor PHA-4/FoxA acts as a sensor of nucleolar stress to bind to and transactivate the expression of the lipogenic genes pod-2 (acetyl-CoA carboxylase), fasn-1 (fatty acid synthase), and dgat-2 (diacylglycerol O -acyltransferase 2), consequently promoting lipid accumulation. Importantly, inactivation of pha-4 or dgat-2 is sufficient to abolish nucleolar stress-induced lipid accumulation and prolonged starvation survival. The results revealed a distinct PHA-4-mediated lipogenesis pathway that senses nucleolar stress and shifts excessive energy for storage as fat. Nucleolar stress can disrupt ribosome biogenesis and in turn energy metabolism and lipid storage, but how this is regulated is unclear. Here, the authors show in C. elegans that the transcription factor PHA-4/FOXA acts as a sensor for nucleolar stress and can regulate expression of lipogenic genes
Nucleolar stress can disrupt ribosome biogenesis and in turn energy metabolism and lipid storage, but how this is regulated is unclear. Here, the authors show in C. elegans that the transcription factor PHA-4/FOXA acts as a sensor for nucleolar stress and can regulate expression of lipogenic genes
The primary function of the nucleolus is ribosome biogenesis, which is an extremely energetically expensive process. Failures in ribosome biogenesis cause nucleolar stress with an altered energy status. However, little is known about the underlying mechanism linking nucleolar stress to energy metabolism. Here we show that nucleolar stress is triggered by inactivation of RSKS-1 (ribosomal protein S6 kinase), RRP-8 (ribosomal RNA processing 8), and PRO-2/3 (proximal proliferation), all of which are involved in ribosomal RNA processing or inhibition of rDNA transcription by actinomycin D (AD), leading to excessive lipid accumulation in Caenorhabditis elegans. The transcription factor PHA-4/FoxA acts as a sensor of nucleolar stress to bind to and transactivate the expression of the lipogenic genes pod-2 (acetyl-CoA carboxylase), fasn-1 (fatty acid synthase), and dgat-2 (diacylglycerol O-acyltransferase 2), consequently promoting lipid accumulation. Importantly, inactivation of pha-4 or dgat-2 is sufficient to abolish nucleolar stress-induced lipid accumulation and prolonged starvation survival. The results revealed a distinct PHA-4-mediated lipogenesis pathway that senses nucleolar stress and shifts excessive energy for storage as fat.
ArticleNumber 1195
Author Zhang, Jingjing
Zhu, Tingting
Zhang, Zhiguo
Wang, Yanli
Jiang, Xue
Li, Yamei
Liang, Bin
Wu, Jieyu
Zhang, Linqiang
Zou, Xiaoju
Zhang, Yuru
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  email: xiaojuzou@163.com
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springer_journals_10_1038_s41467_018_03531_2
PublicationCentury 2000
PublicationDate 2018-03-22
PublicationDateYYYYMMDD 2018-03-22
PublicationDate_xml – month: 03
  year: 2018
  text: 2018-03-22
  day: 22
PublicationDecade 2010
PublicationPlace London
PublicationPlace_xml – name: London
– name: England
PublicationTitle Nature communications
PublicationTitleAbbrev Nat Commun
PublicationTitleAlternate Nat Commun
PublicationYear 2018
Publisher Nature Publishing Group UK
Nature Publishing Group
Nature Portfolio
Publisher_xml – name: Nature Publishing Group UK
– name: Nature Publishing Group
– name: Nature Portfolio
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SSID ssj0000391844
Score 2.466275
Snippet The primary function of the nucleolus is ribosome biogenesis, which is an extremely energetically expensive process. Failures in ribosome biogenesis cause...
Abstract The primary function of the nucleolus is ribosome biogenesis, which is an extremely energetically expensive process. Failures in ribosome biogenesis...
Nucleolar stress can disrupt ribosome biogenesis and in turn energy metabolism and lipid storage, but how this is regulated is unclear. Here, the authors show...
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pubmedcentral
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SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Publisher
StartPage 1195
SubjectTerms 38
38/89
631/443/319
631/80/86/2366
64
64/11
82/1
Accumulation
Acetyl-CoA carboxylase
Actinomycin
Biosynthesis
Deactivation
Diacylglycerol O-acyltransferase
Diglycerides
Energy balance
Energy metabolism
Energy storage
Fatty acids
Fatty-acid synthase
Gene expression
Humanities and Social Sciences
Inactivation
Lipids
Lipogenesis
Metabolism
multidisciplinary
Nucleoli
Ribonucleic acid
Ribosomal protein S6
Ribosomal protein S6 kinase
RNA
RNA processing
rRNA
Science
Science (multidisciplinary)
Starvation
Stress
Stresses
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Title PHA-4/FoxA senses nucleolar stress to regulate lipid accumulation in Caenorhabditis elegans
URI https://link.springer.com/article/10.1038/s41467-018-03531-2
https://www.ncbi.nlm.nih.gov/pubmed/29567958
https://www.proquest.com/docview/2017037023
https://search.proquest.com/docview/2018018762
https://pubmed.ncbi.nlm.nih.gov/PMC5864837
https://doaj.org/article/8febfb2911a04f22ae3b3b04afe66b4b
Volume 9
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