YAP/TAZ drives cell proliferation and tumour growth via a polyamine–eIF5A hypusination–LSD1 axis

Metabolic reprogramming is central to oncogene-induced tumorigenesis by providing the necessary building blocks and energy sources, but how oncogenic signalling controls metabolites that play regulatory roles in driving cell proliferation and tumour growth is less understood. Here we show that oncog...

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Published inNature cell biology Vol. 24; no. 3; pp. 373 - 383
Main Authors Li, Hongde, Wu, Bo-Kuan, Kanchwala, Mohammed, Cai, Jing, Wang, Li, Xing, Chao, Zheng, Yonggang, Pan, Duojia
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.03.2022
Nature Publishing Group
Subjects
13/106
13/109
13/51
14/63
38/1
38/77
38/91
42
631/67/68/2486
631/80/86
692/699/67
692/699/67/2327
Adaptor Proteins, Signal Transducing - genetics
Adaptor Proteins, Signal Transducing - metabolism
Biomedical and Life Sciences
Biosynthesis
Cancer Research
Carcinogenesis - genetics
Cell Biology
Cell growth
Cell proliferation
Cell Proliferation - genetics
Developmental Biology
Energy sources
Epigenetics
Gene expression
Genes
Histone Demethylases - genetics
Histone Demethylases - metabolism
Histones
Humans
Life Sciences
Metabolism
Metabolites
Neoplasms - genetics
Neoplasms - pathology
Ornithine decarboxylase
Phosphoproteins - genetics
Phosphoproteins - metabolism
Polyamines
Stem Cells
Suppressors
Trans-Activators - metabolism
Transcription
Translation
Tumorigenesis
Tumors
YAP-Signaling Proteins
Yes-associated protein
Online AccessGet full text

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Abstract Metabolic reprogramming is central to oncogene-induced tumorigenesis by providing the necessary building blocks and energy sources, but how oncogenic signalling controls metabolites that play regulatory roles in driving cell proliferation and tumour growth is less understood. Here we show that oncogene YAP/TAZ promotes polyamine biosynthesis by activating the transcription of the rate-limiting enzyme ornithine decarboxylase 1. The increased polyamine levels, in turn, promote the hypusination of eukaryotic translation factor 5A (eIF5A) to support efficient translation of histone demethylase LSD1, a transcriptional repressor that mediates a bulk of YAP/TAZ-downregulated genes including tumour suppressors in YAP/TAZ-activated cells. Accentuating the importance of the YAP/TAZ–polyamine–eIF5A hypusination–LSD1 axis, inhibiting polyamine biosynthesis or LSD1 suppressed YAP/TAZ-induced cell proliferation and tumour growth. Given the frequent upregulation of YAP/TAZ activity and polyamine levels in diverse cancers, our identification of YAP/TAZ as an upstream regulator and LSD1 as a downstream effector of the oncometabolite polyamine offers a molecular framework in which oncogene-induced metabolic and epigenetic reprogramming coordinately drives tumorigenesis, and suggests potential therapeutic strategies in YAP/TAZ- or polyamine-dependent human malignancies. Li et al. show that YAP/TAZ directly promotes polyamine biosynthesis and activates eIF5A activity to upregulate LSD1 expression, thereby suppressing various genes including tumour suppressors to enhance tumour growth.
AbstractList Metabolic reprogramming is central to oncogene-induced tumorigenesis by providing the necessary building blocks and energy sources, but how oncogenic signalling controls metabolites that play regulatory roles in driving cell proliferation and tumour growth is less understood. Here we show that oncogene YAP/TAZ promotes polyamine biosynthesis by activating the transcription of the rate-limiting enzyme ornithine decarboxylase 1. The increased polyamine levels, in turn, promote the hypusination of eukaryotic translation factor 5A (eIF5A) to support efficient translation of histone demethylase LSD1, a transcriptional repressor that mediates a bulk of YAP/TAZ-downregulated genes including tumour suppressors in YAP/TAZ-activated cells. Accentuating the importance of the YAP/TAZ–polyamine–eIF5A hypusination–LSD1 axis, inhibiting polyamine biosynthesis or LSD1 suppressed YAP/TAZ-induced cell proliferation and tumour growth. Given the frequent upregulation of YAP/TAZ activity and polyamine levels in diverse cancers, our identification of YAP/TAZ as an upstream regulator and LSD1 as a downstream effector of the oncometabolite polyamine offers a molecular framework in which oncogene-induced metabolic and epigenetic reprogramming coordinately drives tumorigenesis, and suggests potential therapeutic strategies in YAP/TAZ- or polyamine-dependent human malignancies.Li et al. show that YAP/TAZ directly promotes polyamine biosynthesis and activates eIF5A activity to upregulate LSD1 expression, thereby suppressing various genes including tumour suppressors to enhance tumour growth.
Metabolic reprogramming is central to oncogene-induced tumorigenesis by providing the necessary building blocks and energy sources, but how oncogenic signalling controls metabolites that play regulatory roles in driving cell proliferation and tumour growth is less understood. Here we show that oncogene YAP/TAZ promotes polyamine biosynthesis by activating the transcription of the rate-limiting enzyme ornithine decarboxylase 1. The increased polyamine levels, in turn, promote the hypusination of eukaryotic translation factor 5A (eIF5A) to support efficient translation of histone demethylase LSD1, a transcriptional repressor that mediates a bulk of YAP/TAZ-downregulated genes including tumour suppressors in YAP/TAZ-activated cells. Accentuating the importance of the YAP/TAZ–polyamine–eIF5A hypusination–LSD1 axis, inhibiting polyamine biosynthesis or LSD1 suppressed YAP/TAZ-induced cell proliferation and tumour growth. Given the frequent upregulation of YAP/TAZ activity and polyamine levels in diverse cancers, our identification of YAP/TAZ as an upstream regulator and LSD1 as a downstream effector of the oncometabolite polyamine offers a molecular framework in which oncogene-induced metabolic and epigenetic reprogramming coordinately drives tumorigenesis, and suggests potential therapeutic strategies in YAP/TAZ- or polyamine-dependent human malignancies. Li et al. show that YAP/TAZ directly promotes polyamine biosynthesis and activates eIF5A activity to upregulate LSD1 expression, thereby suppressing various genes including tumour suppressors to enhance tumour growth.
Metabolic reprogramming is central to oncogene-induced tumorigenesis by providing the necessary building blocks and energy sources, but how oncogenic signalling controls metabolites that play regulatory roles in driving cell proliferation and tumour growth is less understood. Here we show that oncogene YAP/TAZ promotes polyamine biosynthesis by activating the transcription of the rate-limiting enzyme ornithine decarboxylase 1. The increased polyamine levels, in turn, promote the hypusination of eukaryotic translation factor 5A (eIF5A) to support efficient translation of histone demethylase LSD1, a transcriptional repressor that mediates a bulk of YAP/TAZ-downregulated genes including tumour suppressors in YAP/TAZ-activated cells. Accentuating the importance of the YAP/TAZ-polyamine-eIF5A hypusination-LSD1 axis, inhibiting polyamine biosynthesis or LSD1 suppressed YAP/TAZ-induced cell proliferation and tumour growth. Given the frequent upregulation of YAP/TAZ activity and polyamine levels in diverse cancers, our identification of YAP/TAZ as an upstream regulator and LSD1 as a downstream effector of the oncometabolite polyamine offers a molecular framework in which oncogene-induced metabolic and epigenetic reprogramming coordinately drives tumorigenesis, and suggests potential therapeutic strategies in YAP/TAZ- or polyamine-dependent human malignancies.
Metabolic reprogramming is central to oncogene-induced tumorigenesis by providing the necessary building blocks and energy sources, but how oncogenic signaling controls metabolites that play regulatory roles in driving cell proliferation and tumor growth is less understood. Here we show that oncogene YAP/TAZ promotes polyamine biosynthesis by activating the transcription of the rate-limiting enzyme ornithine decarboxylase 1. The increased polyamine levels, in turn, promote the hypusination of eukaryotic translation factor 5A (eIF5A) to support efficient translation of histone demethylase LSD1, a transcriptional repressor that mediates a bulk of YAP/TAZ-downregulated genes including tumor suppressors in YAP/TAZ-activated cells. Accentuating the importance of the YAP/TAZ-polyamine-eIF5A hypusination-LSD1 axis, inhibiting polyamine biosynthesis or LSD1 suppressed YAP/TAZ-induced cell proliferation and tumor growth significantly. Given the frequent upregulation of YAP/TAZ activity and polyamine levels in diverse cancers, our identification of YAP/TAZ as an upstream regulator and LSD1 as a downstream effector of the oncometabolite polyamine offers a molecular framework in which oncogene-induced metabolic and epigenetic reprogramming coordinately drives tumorigenesis, and suggests potential therapeutic strategies in YAP/TAZ- or polyamine-dependent human malignancies.
Author Wu, Bo-Kuan
Cai, Jing
Wang, Li
Li, Hongde
Zheng, Yonggang
Kanchwala, Mohammed
Pan, Duojia
Xing, Chao
AuthorAffiliation 1 Department of Physiology, Howard Hughes Medical Institute, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9040, USA
2 Eugene McDermott Center for Human Growth and Development/Center for Human Genetics, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9040, USA
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/35177822$$D View this record in MEDLINE/PubMed
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H.L. and D.P. conceived the project; H.L. and Y.Z. designed experiments; H.L., J.C., L.W. and B.W. performed the experiments; M.K. and C.X. analyzed RNA-seq and ChIP-seq data. D.P. supervised the study; H.L., Y.Z. and D.P. wrote the manuscript.
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  year: 2022
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  day: 01
PublicationDecade 2020
PublicationPlace London
PublicationPlace_xml – name: London
– name: England
PublicationTitle Nature cell biology
PublicationTitleAbbrev Nat Cell Biol
PublicationTitleAlternate Nat Cell Biol
PublicationYear 2022
Publisher Nature Publishing Group UK
Nature Publishing Group
Publisher_xml – name: Nature Publishing Group UK
– name: Nature Publishing Group
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Snippet Metabolic reprogramming is central to oncogene-induced tumorigenesis by providing the necessary building blocks and energy sources, but how oncogenic...
Metabolic reprogramming is central to oncogene-induced tumorigenesis by providing the necessary building blocks and energy sources, but how oncogenic signaling...
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SubjectTerms 13/106
13/109
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631/67/68/2486
631/80/86
692/699/67
692/699/67/2327
Adaptor Proteins, Signal Transducing - genetics
Adaptor Proteins, Signal Transducing - metabolism
Biomedical and Life Sciences
Biosynthesis
Cancer Research
Carcinogenesis - genetics
Cell Biology
Cell growth
Cell proliferation
Cell Proliferation - genetics
Developmental Biology
Energy sources
Epigenetics
Gene expression
Genes
Histone Demethylases - genetics
Histone Demethylases - metabolism
Histones
Humans
Life Sciences
Metabolism
Metabolites
Neoplasms - genetics
Neoplasms - pathology
Ornithine decarboxylase
Phosphoproteins - genetics
Phosphoproteins - metabolism
Polyamines
Stem Cells
Suppressors
Trans-Activators - metabolism
Transcription
Translation
Tumorigenesis
Tumors
YAP-Signaling Proteins
Yes-associated protein
Title YAP/TAZ drives cell proliferation and tumour growth via a polyamine–eIF5A hypusination–LSD1 axis
URI https://link.springer.com/article/10.1038/s41556-022-00848-5
https://www.ncbi.nlm.nih.gov/pubmed/35177822
https://www.proquest.com/docview/2639130812
https://search.proquest.com/docview/2630919057
https://pubmed.ncbi.nlm.nih.gov/PMC8930503
Volume 24
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