The creatine kinase pathway is a metabolic vulnerability in EVI1-positive acute myeloid leukemia

Transcriptomic and metabolic profiling reveals that the creatine kinase pathway is essential for growth of acute myeloid leukemias expressing the transcription factor EVI1. Expression of the MECOM (also known as EVI1 ) proto-oncogene is deregulated by chromosomal translocations in some cases of acut...

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Published inNature medicine Vol. 23; no. 3; pp. 301 - 313
Main Authors Fenouille, Nina, Bassil, Christopher F, Ben-Sahra, Issam, Benajiba, Lina, Alexe, Gabriela, Ramos, Azucena, Pikman, Yana, Conway, Amy S, Burgess, Michael R, Li, Qing, Luciano, Frédéric, Auberger, Patrick, Galinsky, Ilene, DeAngelo, Daniel J, Stone, Richard M, Zhang, Yi, Perkins, Archibald S, Shannon, Kevin, Hemann, Michael T, Puissant, Alexandre, Stegmaier, Kimberly
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.03.2017
Nature Publishing Group
Subjects
13/31
59/5
692/699/67/1990/283/1897
692/699/67/2327
96
96/1
96/34
96/35
Acute myelocytic leukemia
Adult
Aged
Aged, 80 and over
Analysis
ATP
Biomedicine
Blotting, Western
Cancer
Cancer Research
Care and treatment
Cell cycle
Cell metabolism
Computer Simulation
Core Binding Factor Alpha 2 Subunit - genetics
Core Binding Factor Alpha 2 Subunit - metabolism
Creatine Kinase - genetics
Creatine Kinase - metabolism
Dehydrogenases
Development and progression
DNA-Binding Proteins - genetics
Female
Flow Cytometry
Gene expression
Gene Expression Profiling
Gene Expression Regulation, Neoplastic - genetics
Genetic aspects
Genome-Wide Association Study
Health aspects
Humans
Infectious Diseases
Kinases
Leukemia
Leukemia, Myeloid, Acute - genetics
Leukemia, Myeloid, Acute - metabolism
Male
MDS1 and EVI1 Complex Locus Protein
Medicine
Metabolic Diseases
Metabolic Networks and Pathways
Metabolism
Metabolites
Metabolomics
Middle Aged
Mitochondria
Molecular Medicine
Mutation
Neurosciences
Oncogenes
Oncology
Physiological aspects
Proteins
Proto-Oncogenes - genetics
RNA, Small Interfering
Transcription factors
Transcription Factors - genetics
New York
San Francisco California
California
United States > US
Massachusetts
Online AccessGet full text

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Abstract Transcriptomic and metabolic profiling reveals that the creatine kinase pathway is essential for growth of acute myeloid leukemias expressing the transcription factor EVI1. Expression of the MECOM (also known as EVI1 ) proto-oncogene is deregulated by chromosomal translocations in some cases of acute myeloid leukemia (AML) and is associated with poor clinical outcome. Here, through transcriptomic and metabolomic profiling of hematopoietic cells, we reveal that EVI1 overexpression alters cellular metabolism. A screen using pooled short hairpin RNAs (shRNAs) identified the ATP-buffering, mitochondrial creatine kinase CKMT1 as necessary for survival of EVI1-expressing cells in subjects with EVI1-positive AML. EVI1 promotes CKMT1 expression by repressing the myeloid differentiation regulator RUNX1. Suppression of arginine–creatine metabolism by CKMT1 -directed shRNAs or by the small molecule cyclocreatine selectively decreased the viability, promoted the cell cycle arrest and apoptosis of human EVI1-positive cell lines, and prolonged survival in both orthotopic xenograft models and mouse models of primary AML. CKMT1 inhibition altered mitochondrial respiration and ATP production, an effect that was abrogated by phosphocreatine-mediated reactivation of the arginine–creatine pathway. Targeting CKMT1 is thus a promising therapeutic strategy for this EVI1-driven AML subtype that is highly resistant to current treatment regimens.
AbstractList Expression of the MECOM (also known as EVI1) proto-oncogene is deregulated by chromosomal translocations in some cases of acute myeloid leukemia (AML) and is associated with poor clinical outcome. Here, through transcriptomic and metabolomic profiling of hematopoietic cells, we reveal that EVI1 overexpression alters cellular metabolism. A screen using pooled short hairpin RNAs (shRNAs) identified the ATP-buffering, mitochondrial creatine kinase CKMT1 as necessary for survival of EVI1-expressing cells in subjects with EVI1-positive AML. EVI1 promotes CKMT1 expression by repressing the myeloid differentiation regulator RUNX1. Suppression of arginine-creatine metabolism by CKMT1-directed shRNAs or by the small molecule cyclocreatine selectively decreased the viability, promoted the cell cycle arrest and apoptosis of human EVI1-positive cell lines, and prolonged survival in both orthotopic xenograft models and mouse models of primary AML. CKMT1 inhibition altered mitochondrial respiration and ATP production, an effect that was abrogated by phosphocreatine-mediated reactivation of the arginine-creatine pathway. Targeting CKMT1 is thus a promising therapeutic strategy for this EVI1-driven AML subtype that is highly resistant to current treatment regimens.
Transcriptomic and metabolic profiling reveals that the creatine kinase pathway is essential for growth of acute myeloid leukemias expressing the transcription factor EVI1. Expression of the MECOM (also known as EVI1 ) proto-oncogene is deregulated by chromosomal translocations in some cases of acute myeloid leukemia (AML) and is associated with poor clinical outcome. Here, through transcriptomic and metabolomic profiling of hematopoietic cells, we reveal that EVI1 overexpression alters cellular metabolism. A screen using pooled short hairpin RNAs (shRNAs) identified the ATP-buffering, mitochondrial creatine kinase CKMT1 as necessary for survival of EVI1-expressing cells in subjects with EVI1-positive AML. EVI1 promotes CKMT1 expression by repressing the myeloid differentiation regulator RUNX1. Suppression of arginine–creatine metabolism by CKMT1 -directed shRNAs or by the small molecule cyclocreatine selectively decreased the viability, promoted the cell cycle arrest and apoptosis of human EVI1-positive cell lines, and prolonged survival in both orthotopic xenograft models and mouse models of primary AML. CKMT1 inhibition altered mitochondrial respiration and ATP production, an effect that was abrogated by phosphocreatine-mediated reactivation of the arginine–creatine pathway. Targeting CKMT1 is thus a promising therapeutic strategy for this EVI1-driven AML subtype that is highly resistant to current treatment regimens.
Expression of the EVI1 proto-oncogene is deregulated by chromosomal translocations in some cases of acute myeloid leukemia (AML) and is associated with poor clinical outcome. Here, through transcriptomic and metabolomic profiling of hematopoietic cells, we reveal that EVI1 overexpression alters cellular metabolism. A pooled shRNA screen identified the ATP-buffering, mitochondrial creatine kinase CKMT1 as a metabolic dependency in EVI1-positive AML. EVI1 promotes CKMT1 expression by repressing the myeloid differentiation regulator RUNX1. Suppression of arginine-creatine metabolism by CKMT1 -directed shRNAs or by the small molecule cyclocreatine selectively decreased the viability, promoted cell cycle arrest and apoptosis of human EVI1-positive AML cells, and prolonged survival in human orthotopic and mouse primary AML models. CKMT1 inhibition alters mitochondrial respiration and ATP production, an effect that is abrogated by phospho-creatine-mediated reactivation of the arginine-creatine pathway. Targeting CKMT1 is a promising therapeutic strategy for this EVI1-driven AML subtype that is highly resistant to current treatment regimens.
Audience Academic
Author Bassil, Christopher F
Li, Qing
DeAngelo, Daniel J
Hemann, Michael T
Zhang, Yi
Luciano, Frédéric
Perkins, Archibald S
Galinsky, Ilene
Ben-Sahra, Issam
Auberger, Patrick
Puissant, Alexandre
Burgess, Michael R
Shannon, Kevin
Conway, Amy S
Stegmaier, Kimberly
Benajiba, Lina
Fenouille, Nina
Ramos, Azucena
Alexe, Gabriela
Stone, Richard M
Pikman, Yana
AuthorAffiliation 5 Bioinformatics Graduate Program, Boston University, Boston, MA, USA
11 Department of Pediatrics, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA
12 INSERM UMR 944, Institut Universitaire d’Hématologie, Hôpital St. Louis, 75475 Paris, France
2 Department of Pediatric Oncology, Dana-Farber Cancer Institute and Boston Children’s Hospital, Harvard Medical School, Boston, MA, USA
10 Department of Pathology and Laboratory Medicine, University of Rochester Medical Center, Rochester, New York, NY 14642, USA
3 Department of Genetics and Complex Diseases, Harvard School of Public Health, Boston, MA, USA
1 Koch Institute for Integrative Cancer Research at Massachusetts Institute of Technology, Massachusetts Institute of Technology, Cambridge, MA, USA
4 The Broad Institute of Harvard University and Massachusetts Institute of Technology, Cambridge, MA, USA
9 Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/28191887$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright Springer Nature America, Inc. 2017
COPYRIGHT 2017 Nature Publishing Group
Copyright Nature Publishing Group Mar 2017
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Snippet Transcriptomic and metabolic profiling reveals that the creatine kinase pathway is essential for growth of acute myeloid leukemias expressing the transcription...
Expression of the MECOM (also known as EVI1) proto-oncogene is deregulated by chromosomal translocations in some cases of acute myeloid leukemia (AML) and is...
Expression of the EVI1 proto-oncogene is deregulated by chromosomal translocations in some cases of acute myeloid leukemia (AML) and is associated with poor...
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Enrichment Source
Publisher
StartPage 301
SubjectTerms 13/31
59/5
692/699/67/1990/283/1897
692/699/67/2327
96
96/1
96/34
96/35
Acute myelocytic leukemia
Adult
Aged
Aged, 80 and over
Analysis
ATP
Biomedicine
Blotting, Western
Cancer
Cancer Research
Care and treatment
Cell cycle
Cell metabolism
Computer Simulation
Core Binding Factor Alpha 2 Subunit - genetics
Core Binding Factor Alpha 2 Subunit - metabolism
Creatine Kinase - genetics
Creatine Kinase - metabolism
Dehydrogenases
Development and progression
DNA-Binding Proteins - genetics
Female
Flow Cytometry
Gene expression
Gene Expression Profiling
Gene Expression Regulation, Neoplastic - genetics
Genetic aspects
Genome-Wide Association Study
Health aspects
Humans
Infectious Diseases
Kinases
Leukemia
Leukemia, Myeloid, Acute - genetics
Leukemia, Myeloid, Acute - metabolism
Male
MDS1 and EVI1 Complex Locus Protein
Medicine
Metabolic Diseases
Metabolic Networks and Pathways
Metabolism
Metabolites
Metabolomics
Middle Aged
Mitochondria
Molecular Medicine
Mutation
Neurosciences
Oncogenes
Oncology
Physiological aspects
Proteins
Proto-Oncogenes - genetics
RNA, Small Interfering
Transcription factors
Transcription Factors - genetics
Title The creatine kinase pathway is a metabolic vulnerability in EVI1-positive acute myeloid leukemia
URI https://link.springer.com/article/10.1038/nm.4283
https://www.ncbi.nlm.nih.gov/pubmed/28191887
https://www.proquest.com/docview/1875119890
https://www.proquest.com/docview/1867984417
https://www.proquest.com/docview/1877845273
https://pubmed.ncbi.nlm.nih.gov/PMC5540325
Volume 23
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