ALKBH5 modulates hematopoietic stem and progenitor cell energy metabolism through m6A modification-mediated RNA stability control

N6-methyladenosine (m6A) RNA modification controls numerous cellular processes. To what extent these post-transcriptional regulatory mechanisms play a role in hematopoiesis has not been fully elucidated. We here show that the m6A demethylase alkB homolog 5 (ALKBH5) controls mitochondrial ATP product...

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Published inCell reports (Cambridge) Vol. 42; no. 10; p. 113163
Main Authors Gao, Yimeng, Zimmer, Joshua T., Vasic, Radovan, Liu, Chengyang, Gbyli, Rana, Zheng, Shu-Jian, Patel, Amisha, Liu, Wei, Qi, Zhihong, Li, Yaping, Nelakanti, Raman, Song, Yuanbin, Biancon, Giulia, Xiao, Andrew Z., Slavoff, Sarah, Kibbey, Richard G., Flavell, Richard A., Simon, Matthew D., Tebaldi, Toma, Li, Hua-Bing, Halene, Stephanie
Format Journal Article
LanguageEnglish
Published Elsevier Inc 31.10.2023
Cell Press
Elsevier
Subjects
ALKBH5
ATP production
CP: Molecular biology
CP: Stem cell research
energy metabolism
hematopoietic stem and progenitor cells
leukemia
m6A modification
oxidative phosphorylation
OXPHOS
RNA stability
stress hematopoiesis
RNA stability
leukemia
m6A modification
ALKBH5
stress hematopoiesis
CP: Stem cell research
hematopoietic stem and progenitor cells
CP: Molecular biology
ATP production
OXPHOS
energy metabolism
oxidative phosphorylation
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Abstract N6-methyladenosine (m6A) RNA modification controls numerous cellular processes. To what extent these post-transcriptional regulatory mechanisms play a role in hematopoiesis has not been fully elucidated. We here show that the m6A demethylase alkB homolog 5 (ALKBH5) controls mitochondrial ATP production and modulates hematopoietic stem and progenitor cell (HSPC) fitness in an m6A-dependent manner. Loss of ALKBH5 results in increased RNA methylation and instability of oxoglutarate-dehydrogenase (Ogdh) messenger RNA and reduction of OGDH protein levels. Limited OGDH availability slows the tricarboxylic acid (TCA) cycle with accumulation of α-ketoglutarate (α-KG) and conversion of α-KG into L-2-hydroxyglutarate (L-2-HG). L-2-HG inhibits energy production in both murine and human hematopoietic cells in vitro. Impaired mitochondrial energy production confers competitive disadvantage to HSPCs and limits clonogenicity of Mll-AF9-induced leukemia. Our study uncovers a mechanism whereby the RNA m6A demethylase ALKBH5 regulates the stability of metabolic enzyme transcripts, thereby controlling energy metabolism in hematopoiesis and leukemia. [Display omitted] •Loss of ALKBH5 attenuates hematopoietic fitness in response to stress•ALKBH5 regulates the stability of Ogdh mRNA and of other metabolic enzymes•L-2-HG accumulates in response to OGDH downregulation and attenuates the energy metabolism•L-2-HG inhibits proliferation of both normal and malignant hematopoietic cells Gao et al. find that ALKBH5 regulates hematopoietic stem and progenitor cell fitness in response to stress. ALKBH5 modulates energy metabolism by controlling stability of Ogdh and other metabolic enzyme transcripts. Accumulation of L-2-HG further inhibits the energy metabolism of hematopoietic cells. These findings provide insights on ALKBH5 in hematopoiesis.
AbstractList N 6 -methyladenosine (m 6 A) RNA modification controls numerous cellular processes. To what extent these post-transcriptional regulatory mechanisms play a role in hematopoiesis has not been fully elucidated. We here show that the m 6 A demethylase alkB homolog 5 (ALKBH5) controls mitochondrial ATP production and modulates hematopoietic stem and progenitor cell (HSPC) fitness in an m 6 A-dependent manner. Loss of ALKBH5 results in increased RNA methylation and instability of oxoglutarate-dehydrogenase ( Ogdh ) messenger RNA and reduction of OGDH protein levels. Limited OGDH availability slows the tricarboxylic acid (TCA) cycle with accumulation of α-ketoglutarate (α-KG) and conversion of α-KG into L-2-hydroxyglutarate (L-2-HG). L-2-HG inhibits energy production in both murine and human hematopoietic cells in vitro . Impaired mitochondrial energy production confers competitive disadvantage to HSPCs and limits clonogenicity of Mll-AF9 -induced leukemia. Our study uncovers a mechanism whereby the RNA m 6 A demethylase ALKBH5 regulates the stability of metabolic enzyme transcripts, thereby controlling energy metabolism in hematopoiesis and leukemia. • Loss of ALKBH5 attenuates hematopoietic fitness in response to stress • ALKBH5 regulates the stability of Ogdh mRNA and of other metabolic enzymes • L-2-HG accumulates in response to OGDH downregulation and attenuates the energy metabolism • L-2-HG inhibits proliferation of both normal and malignant hematopoietic cells Gao et al. find that ALKBH5 regulates hematopoietic stem and progenitor cell fitness in response to stress. ALKBH5 modulates energy metabolism by controlling stability of Ogdh and other metabolic enzyme transcripts. Accumulation of L-2-HG further inhibits the energy metabolism of hematopoietic cells. These findings provide insights on ALKBH5 in hematopoiesis.
N6-methyladenosine (m6A) RNA modification controls numerous cellular processes. To what extent these post-transcriptional regulatory mechanisms play a role in hematopoiesis has not been fully elucidated. We here show that the m6A demethylase alkB homolog 5 (ALKBH5) controls mitochondrial ATP production and modulates hematopoietic stem and progenitor cell (HSPC) fitness in an m6A-dependent manner. Loss of ALKBH5 results in increased RNA methylation and instability of oxoglutarate-dehydrogenase (Ogdh) messenger RNA and reduction of OGDH protein levels. Limited OGDH availability slows the tricarboxylic acid (TCA) cycle with accumulation of α-ketoglutarate (α-KG) and conversion of α-KG into L-2-hydroxyglutarate (L-2-HG). L-2-HG inhibits energy production in both murine and human hematopoietic cells in vitro. Impaired mitochondrial energy production confers competitive disadvantage to HSPCs and limits clonogenicity of Mll-AF9-induced leukemia. Our study uncovers a mechanism whereby the RNA m6A demethylase ALKBH5 regulates the stability of metabolic enzyme transcripts, thereby controlling energy metabolism in hematopoiesis and leukemia.
N6-methyladenosine (m6A) RNA modification controls numerous cellular processes. To what extent these post-transcriptional regulatory mechanisms play a role in hematopoiesis has not been fully elucidated. We here show that the m6A demethylase alkB homolog 5 (ALKBH5) controls mitochondrial ATP production and modulates hematopoietic stem and progenitor cell (HSPC) fitness in an m6A-dependent manner. Loss of ALKBH5 results in increased RNA methylation and instability of oxoglutarate-dehydrogenase (Ogdh) messenger RNA and reduction of OGDH protein levels. Limited OGDH availability slows the tricarboxylic acid (TCA) cycle with accumulation of α-ketoglutarate (α-KG) and conversion of α-KG into L-2-hydroxyglutarate (L-2-HG). L-2-HG inhibits energy production in both murine and human hematopoietic cells in vitro. Impaired mitochondrial energy production confers competitive disadvantage to HSPCs and limits clonogenicity of Mll-AF9-induced leukemia. Our study uncovers a mechanism whereby the RNA m6A demethylase ALKBH5 regulates the stability of metabolic enzyme transcripts, thereby controlling energy metabolism in hematopoiesis and leukemia. [Display omitted] •Loss of ALKBH5 attenuates hematopoietic fitness in response to stress•ALKBH5 regulates the stability of Ogdh mRNA and of other metabolic enzymes•L-2-HG accumulates in response to OGDH downregulation and attenuates the energy metabolism•L-2-HG inhibits proliferation of both normal and malignant hematopoietic cells Gao et al. find that ALKBH5 regulates hematopoietic stem and progenitor cell fitness in response to stress. ALKBH5 modulates energy metabolism by controlling stability of Ogdh and other metabolic enzyme transcripts. Accumulation of L-2-HG further inhibits the energy metabolism of hematopoietic cells. These findings provide insights on ALKBH5 in hematopoiesis.
N6-methyladenosine (m6A) RNA modification controls numerous cellular processes. To what extent these post-transcriptional regulatory mechanisms play a role in hematopoiesis has not been fully elucidated. We here show that the m6A demethylase alkB homolog 5 (ALKBH5) controls mitochondrial ATP production and modulates hematopoietic stem and progenitor cell (HSPC) fitness in an m6A-dependent manner. Loss of ALKBH5 results in increased RNA methylation and instability of oxoglutarate-dehydrogenase (Ogdh) messenger RNA and reduction of OGDH protein levels. Limited OGDH availability slows the tricarboxylic acid (TCA) cycle with accumulation of α-ketoglutarate (α-KG) and conversion of α-KG into L-2-hydroxyglutarate (L-2-HG). L-2-HG inhibits energy production in both murine and human hematopoietic cells in vitro. Impaired mitochondrial energy production confers competitive disadvantage to HSPCs and limits clonogenicity of Mll-AF9-induced leukemia. Our study uncovers a mechanism whereby the RNA m6A demethylase ALKBH5 regulates the stability of metabolic enzyme transcripts, thereby controlling energy metabolism in hematopoiesis and leukemia.N6-methyladenosine (m6A) RNA modification controls numerous cellular processes. To what extent these post-transcriptional regulatory mechanisms play a role in hematopoiesis has not been fully elucidated. We here show that the m6A demethylase alkB homolog 5 (ALKBH5) controls mitochondrial ATP production and modulates hematopoietic stem and progenitor cell (HSPC) fitness in an m6A-dependent manner. Loss of ALKBH5 results in increased RNA methylation and instability of oxoglutarate-dehydrogenase (Ogdh) messenger RNA and reduction of OGDH protein levels. Limited OGDH availability slows the tricarboxylic acid (TCA) cycle with accumulation of α-ketoglutarate (α-KG) and conversion of α-KG into L-2-hydroxyglutarate (L-2-HG). L-2-HG inhibits energy production in both murine and human hematopoietic cells in vitro. Impaired mitochondrial energy production confers competitive disadvantage to HSPCs and limits clonogenicity of Mll-AF9-induced leukemia. Our study uncovers a mechanism whereby the RNA m6A demethylase ALKBH5 regulates the stability of metabolic enzyme transcripts, thereby controlling energy metabolism in hematopoiesis and leukemia.
ArticleNumber 113163
Author Song, Yuanbin
Liu, Wei
Biancon, Giulia
Flavell, Richard A.
Gao, Yimeng
Qi, Zhihong
Simon, Matthew D.
Kibbey, Richard G.
Li, Yaping
Li, Hua-Bing
Tebaldi, Toma
Vasic, Radovan
Xiao, Andrew Z.
Halene, Stephanie
Zimmer, Joshua T.
Liu, Chengyang
Slavoff, Sarah
Nelakanti, Raman
Gbyli, Rana
Zheng, Shu-Jian
Patel, Amisha
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– sequence: 2
  givenname: Joshua T.
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  fullname: Zimmer, Joshua T.
  organization: Department of Molecular Biophysics & Biochemistry, Yale University, New Haven, CT 06511, USA
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  givenname: Radovan
  surname: Vasic
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  organization: Section of Hematology, Department of Internal Medicine, Yale Cancer Center, and Yale Center for RNA Science and Medicine, Yale University School of Medicine, New Haven, CT 06520, USA
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  surname: Liu
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  surname: Patel
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  surname: Song
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  email: stephanie.halene@yale.edu
  organization: Section of Hematology, Department of Internal Medicine, Yale Cancer Center, and Yale Center for RNA Science and Medicine, Yale University School of Medicine, New Haven, CT 06520, USA
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Issue 10
Keywords RNA stability
leukemia
m6A modification
ALKBH5
stress hematopoiesis
CP: Stem cell research
hematopoietic stem and progenitor cells
CP: Molecular biology
ATP production
OXPHOS
energy metabolism
oxidative phosphorylation
Language English
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Present address: Institute for Regenerative Medicine, Shanghai East Hospital, Frontier Science Center for Stem Cell Research, School of Life Sciences and Technology, Tongji University, Shanghai 200092, China
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Snippet N6-methyladenosine (m6A) RNA modification controls numerous cellular processes. To what extent these post-transcriptional regulatory mechanisms play a role in...
N 6 -methyladenosine (m 6 A) RNA modification controls numerous cellular processes. To what extent these post-transcriptional regulatory mechanisms play a role...
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SubjectTerms ALKBH5
ATP production
CP: Molecular biology
CP: Stem cell research
energy metabolism
hematopoietic stem and progenitor cells
leukemia
m6A modification
oxidative phosphorylation
OXPHOS
RNA stability
stress hematopoiesis
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Title ALKBH5 modulates hematopoietic stem and progenitor cell energy metabolism through m6A modification-mediated RNA stability control
URI https://dx.doi.org/10.1016/j.celrep.2023.113163
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Volume 42
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