Metabolic Adaptation to Nutrients Involves Coregulation of Gene Expression by the RNA Helicase Dbp2 and the Cyc8 Corepressor in Saccharomyces cerevisiae

Cells fine-tune their metabolic programs according to nutrient availability in order to maintain homeostasis. This is achieved largely through integrating signaling pathways and the gene expression program, allowing cells to adapt to nutritional change. Dbp2, a member of the DEAD-box RNA helicase fa...

Full description

Bibliographic Details
Main Authors: Siwen Wang, Zheng Xing, Pete E. Pascuzzi, Elizabeth J. Tran
Format: Article
Language:English
Published: Oxford University Press 2017-07-01
Series:G3: Genes, Genomes, Genetics
Subjects:
Online Access:http://g3journal.org/lookup/doi/10.1534/g3.117.041814
_version_ 1819008908912492544
author Siwen Wang
Zheng Xing
Pete E. Pascuzzi
Elizabeth J. Tran
author_facet Siwen Wang
Zheng Xing
Pete E. Pascuzzi
Elizabeth J. Tran
author_sort Siwen Wang
collection DOAJ
description Cells fine-tune their metabolic programs according to nutrient availability in order to maintain homeostasis. This is achieved largely through integrating signaling pathways and the gene expression program, allowing cells to adapt to nutritional change. Dbp2, a member of the DEAD-box RNA helicase family in Saccharomyces cerevisiae, has been proposed to integrate gene expression with cellular metabolism. Prior work from our laboratory has reported the necessity of DBP2 in proper gene expression, particularly for genes involved in glucose-dependent regulation. Here, by comparing differentially expressed genes in dbp2∆ to those of 700 other deletion strains from other studies, we find that CYC8 and TUP1, which form a complex and inhibit transcription of numerous genes, corepress a common set of genes with DBP2. Gene ontology (GO) annotations reveal that these corepressed genes are related to cellular metabolism, including respiration, gluconeogenesis, and alternative carbon-source utilization genes. Consistent with a direct role in metabolic gene regulation, loss of either DBP2 or CYC8 results in increased cellular respiration rates. Furthermore, we find that corepressed genes have a propensity to be associated with overlapping long noncoding RNAs and that upregulation of these genes in the absence of DBP2 correlates with decreased binding of Cyc8 to these gene promoters. Taken together, this suggests that Dbp2 integrates nutrient availability with energy homeostasis by maintaining repression of glucose-repressed, Cyc8-targeted genes across the genome.
first_indexed 2024-12-21T00:47:57Z
format Article
id doaj.art-d6e55c4e54304ccb9c765ecc03c6c03a
institution Directory Open Access Journal
issn 2160-1836
language English
last_indexed 2024-12-21T00:47:57Z
publishDate 2017-07-01
publisher Oxford University Press
record_format Article
series G3: Genes, Genomes, Genetics
spelling doaj.art-d6e55c4e54304ccb9c765ecc03c6c03a2022-12-21T19:21:28ZengOxford University PressG3: Genes, Genomes, Genetics2160-18362017-07-01772235224710.1534/g3.117.04181421Metabolic Adaptation to Nutrients Involves Coregulation of Gene Expression by the RNA Helicase Dbp2 and the Cyc8 Corepressor in Saccharomyces cerevisiaeSiwen WangZheng XingPete E. PascuzziElizabeth J. TranCells fine-tune their metabolic programs according to nutrient availability in order to maintain homeostasis. This is achieved largely through integrating signaling pathways and the gene expression program, allowing cells to adapt to nutritional change. Dbp2, a member of the DEAD-box RNA helicase family in Saccharomyces cerevisiae, has been proposed to integrate gene expression with cellular metabolism. Prior work from our laboratory has reported the necessity of DBP2 in proper gene expression, particularly for genes involved in glucose-dependent regulation. Here, by comparing differentially expressed genes in dbp2∆ to those of 700 other deletion strains from other studies, we find that CYC8 and TUP1, which form a complex and inhibit transcription of numerous genes, corepress a common set of genes with DBP2. Gene ontology (GO) annotations reveal that these corepressed genes are related to cellular metabolism, including respiration, gluconeogenesis, and alternative carbon-source utilization genes. Consistent with a direct role in metabolic gene regulation, loss of either DBP2 or CYC8 results in increased cellular respiration rates. Furthermore, we find that corepressed genes have a propensity to be associated with overlapping long noncoding RNAs and that upregulation of these genes in the absence of DBP2 correlates with decreased binding of Cyc8 to these gene promoters. Taken together, this suggests that Dbp2 integrates nutrient availability with energy homeostasis by maintaining repression of glucose-repressed, Cyc8-targeted genes across the genome.http://g3journal.org/lookup/doi/10.1534/g3.117.041814helicaseDEAD-boxmetabolismCyc8Dbp2
spellingShingle Siwen Wang
Zheng Xing
Pete E. Pascuzzi
Elizabeth J. Tran
Metabolic Adaptation to Nutrients Involves Coregulation of Gene Expression by the RNA Helicase Dbp2 and the Cyc8 Corepressor in Saccharomyces cerevisiae
G3: Genes, Genomes, Genetics
helicase
DEAD-box
metabolism
Cyc8
Dbp2
title Metabolic Adaptation to Nutrients Involves Coregulation of Gene Expression by the RNA Helicase Dbp2 and the Cyc8 Corepressor in Saccharomyces cerevisiae
title_full Metabolic Adaptation to Nutrients Involves Coregulation of Gene Expression by the RNA Helicase Dbp2 and the Cyc8 Corepressor in Saccharomyces cerevisiae
title_fullStr Metabolic Adaptation to Nutrients Involves Coregulation of Gene Expression by the RNA Helicase Dbp2 and the Cyc8 Corepressor in Saccharomyces cerevisiae
title_full_unstemmed Metabolic Adaptation to Nutrients Involves Coregulation of Gene Expression by the RNA Helicase Dbp2 and the Cyc8 Corepressor in Saccharomyces cerevisiae
title_short Metabolic Adaptation to Nutrients Involves Coregulation of Gene Expression by the RNA Helicase Dbp2 and the Cyc8 Corepressor in Saccharomyces cerevisiae
title_sort metabolic adaptation to nutrients involves coregulation of gene expression by the rna helicase dbp2 and the cyc8 corepressor in saccharomyces cerevisiae
topic helicase
DEAD-box
metabolism
Cyc8
Dbp2
url http://g3journal.org/lookup/doi/10.1534/g3.117.041814
work_keys_str_mv AT siwenwang metabolicadaptationtonutrientsinvolvescoregulationofgeneexpressionbythernahelicasedbp2andthecyc8corepressorinsaccharomycescerevisiae
AT zhengxing metabolicadaptationtonutrientsinvolvescoregulationofgeneexpressionbythernahelicasedbp2andthecyc8corepressorinsaccharomycescerevisiae
AT peteepascuzzi metabolicadaptationtonutrientsinvolvescoregulationofgeneexpressionbythernahelicasedbp2andthecyc8corepressorinsaccharomycescerevisiae
AT elizabethjtran metabolicadaptationtonutrientsinvolvescoregulationofgeneexpressionbythernahelicasedbp2andthecyc8corepressorinsaccharomycescerevisiae