Metabolic reprogramming of acute lymphoblastic leukemia cells in response to glucocorticoid treatment

Glucocorticoids (GCs) are metabolic hormones with immunosuppressive effects that have proven effective drugs against childhood acute lymphoblastic leukemia (ALL). Yet, the role of metabolic reprogramming in GC-induced ALL cell death is poorly understood. GCs efficiently block glucose uptake and meta...

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Vydané v:Cell death & disease Ročník 9; číslo 9; s. 846 - 13
Hlavní autori: Dyczynski, Matheus, Vesterlund, Mattias, Björklund, Ann-Charlotte, Zachariadis, Vasilios, Janssen, Jerry, Gallart-Ayala, Hector, Daskalaki, Evangelia, Wheelock, Craig E., Lehtiö, Janne, Grandér, Dan, Tamm, Katja Pokrovskaja, Nilsson, Roland
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: London Nature Publishing Group UK 28.08.2018
Springer Nature B.V
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13/2
38/1
82/58
Acute lymphoblastic leukemia
Ammonia
Antibodies
Apoptosis
Autophagy
Bases (nucleic acids)
Biochemistry
Biomedical and Life Sciences
Cell Biology
Cell Culture
Cell death
Children
Glucocorticoids
Glucose metabolism
Glutamine
Glycolysis
Immunology
Immunosuppressive agents
Ketoglutaric acid
Lecithin
Leukemia
Life Sciences
Lymphatic leukemia
Metabolism
Metabolomics
Phagocytosis
Phosphatidylcholine
Proteomics
Tricarboxylic acid cycle
ISSN:2041-4889, 2041-4889
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Abstract Glucocorticoids (GCs) are metabolic hormones with immunosuppressive effects that have proven effective drugs against childhood acute lymphoblastic leukemia (ALL). Yet, the role of metabolic reprogramming in GC-induced ALL cell death is poorly understood. GCs efficiently block glucose uptake and metabolism in ALL cells, but this does not fully explain the observed induction of autophagy and cell death. Here, we have performed parallel time-course proteomics, metabolomics, and isotope-tracing studies to examine in detail the metabolic effects of GCs on ALL cells. We observed metabolic events associated with growth arrest, autophagy, and catabolism prior to onset of apoptosis: nucleotide de novo synthesis was reduced, while certain nucleobases accumulated; polyamine synthesis was inhibited; and phosphatidylcholine synthesis was induced. GCs suppressed not only glycolysis but also entry of both glucose and glutamine into the TCA cycle. In contrast, expression of glutamine-ammonia ligase (GLUL) and cellular glutamine content was robustly increased by GC treatment, suggesting induction of glutamine synthesis, similar to nutrient-starved muscle. Modulating medium glutamine and dimethyl-α-ketoglutarate (dm-αkg) to favor glutamine synthesis reduced autophagosome content of ALL cells, and dm-αkg also rescued cell viability. These data suggest that glutamine synthesis affects autophagy and possibly onset of cell death in response to GCs, which should be further explored to understand mechanism of action and possible sources of resistance.
AbstractList Glucocorticoids (GCs) are metabolic hormones with immunosuppressive effects that have proven effective drugs against childhood acute lymphoblastic leukemia (ALL). Yet, the role of metabolic reprogramming in GC-induced ALL cell death is poorly understood. GCs efficiently block glucose uptake and metabolism in ALL cells, but this does not fully explain the observed induction of autophagy and cell death. Here, we have performed parallel time-course proteomics, metabolomics, and isotope-tracing studies to examine in detail the metabolic effects of GCs on ALL cells. We observed metabolic events associated with growth arrest, autophagy, and catabolism prior to onset of apoptosis: nucleotide de novo synthesis was reduced, while certain nucleobases accumulated; polyamine synthesis was inhibited; and phosphatidylcholine synthesis was induced. GCs suppressed not only glycolysis but also entry of both glucose and glutamine into the TCA cycle. In contrast, expression of glutamine-ammonia ligase (GLUL) and cellular glutamine content was robustly increased by GC treatment, suggesting induction of glutamine synthesis, similar to nutrient-starved muscle. Modulating medium glutamine and dimethyl-α-ketoglutarate (dm-αkg) to favor glutamine synthesis reduced autophagosome content of ALL cells, and dm-αkg also rescued cell viability. These data suggest that glutamine synthesis affects autophagy and possibly onset of cell death in response to GCs, which should be further explored to understand mechanism of action and possible sources of resistance.
Glucocorticoids (GCs) are metabolic hormones with immunosuppressive effects that have proven effective drugs against childhood acute lymphoblastic leukemia (ALL). Yet, the role of metabolic reprogramming in GC-induced ALL cell death is poorly understood. GCs efficiently block glucose uptake and metabolism in ALL cells, but this does not fully explain the observed induction of autophagy and cell death. Here, we have performed parallel time-course proteomics, metabolomics, and isotope-tracing studies to examine in detail the metabolic effects of GCs on ALL cells. We observed metabolic events associated with growth arrest, autophagy, and catabolism prior to onset of apoptosis: nucleotide de novo synthesis was reduced, while certain nucleobases accumulated; polyamine synthesis was inhibited; and phosphatidylcholine synthesis was induced. GCs suppressed not only glycolysis but also entry of both glucose and glutamine into the TCA cycle. In contrast, expression of glutamine-ammonia ligase (GLUL) and cellular glutamine content was robustly increased by GC treatment, suggesting induction of glutamine synthesis, similar to nutrient-starved muscle. Modulating medium glutamine and dimethyl-α-ketoglutarate (dm-αkg) to favor glutamine synthesis reduced autophagosome content of ALL cells, and dm-αkg also rescued cell viability. These data suggest that glutamine synthesis affects autophagy and possibly onset of cell death in response to GCs, which should be further explored to understand mechanism of action and possible sources of resistance.Glucocorticoids (GCs) are metabolic hormones with immunosuppressive effects that have proven effective drugs against childhood acute lymphoblastic leukemia (ALL). Yet, the role of metabolic reprogramming in GC-induced ALL cell death is poorly understood. GCs efficiently block glucose uptake and metabolism in ALL cells, but this does not fully explain the observed induction of autophagy and cell death. Here, we have performed parallel time-course proteomics, metabolomics, and isotope-tracing studies to examine in detail the metabolic effects of GCs on ALL cells. We observed metabolic events associated with growth arrest, autophagy, and catabolism prior to onset of apoptosis: nucleotide de novo synthesis was reduced, while certain nucleobases accumulated; polyamine synthesis was inhibited; and phosphatidylcholine synthesis was induced. GCs suppressed not only glycolysis but also entry of both glucose and glutamine into the TCA cycle. In contrast, expression of glutamine-ammonia ligase (GLUL) and cellular glutamine content was robustly increased by GC treatment, suggesting induction of glutamine synthesis, similar to nutrient-starved muscle. Modulating medium glutamine and dimethyl-α-ketoglutarate (dm-αkg) to favor glutamine synthesis reduced autophagosome content of ALL cells, and dm-αkg also rescued cell viability. These data suggest that glutamine synthesis affects autophagy and possibly onset of cell death in response to GCs, which should be further explored to understand mechanism of action and possible sources of resistance.
ArticleNumber 846
Author Wheelock, Craig E.
Lehtiö, Janne
Grandér, Dan
Nilsson, Roland
Zachariadis, Vasilios
Gallart-Ayala, Hector
Björklund, Ann-Charlotte
Janssen, Jerry
Tamm, Katja Pokrovskaja
Vesterlund, Mattias
Dyczynski, Matheus
Daskalaki, Evangelia
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  fullname: Dyczynski, Matheus
  organization: Department of Oncology-Pathology, Cancer Centre Karolinska, Karolinska Institutet, Karolinska University Hospital
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  givenname: Mattias
  surname: Vesterlund
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  givenname: Ann-Charlotte
  surname: Björklund
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  givenname: Jerry
  surname: Janssen
  fullname: Janssen, Jerry
  organization: Department of Oncology-Pathology, Cancer Centre Karolinska, Karolinska Institutet, Karolinska University Hospital
– sequence: 6
  givenname: Hector
  surname: Gallart-Ayala
  fullname: Gallart-Ayala, Hector
  organization: Division of Physiological Chemistry 2, Department of Medical Biochemistry and Biophysics, Karolinska Institutet
– sequence: 7
  givenname: Evangelia
  surname: Daskalaki
  fullname: Daskalaki, Evangelia
  organization: Division of Physiological Chemistry 2, Department of Medical Biochemistry and Biophysics, Karolinska Institutet
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  givenname: Craig E.
  surname: Wheelock
  fullname: Wheelock, Craig E.
  organization: Division of Physiological Chemistry 2, Department of Medical Biochemistry and Biophysics, Karolinska Institutet
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  orcidid: 0000-0002-8100-9562
  surname: Lehtiö
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  organization: Department of Oncology-Pathology, Science for Life Laboratory, Karolinska Institutet
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  givenname: Dan
  surname: Grandér
  fullname: Grandér, Dan
  organization: Department of Oncology-Pathology, Cancer Centre Karolinska, Karolinska Institutet, Karolinska University Hospital
– sequence: 11
  givenname: Katja Pokrovskaja
  orcidid: 0000-0001-6359-1256
  surname: Tamm
  fullname: Tamm, Katja Pokrovskaja
  email: katja.pokrovskaja@ki.se
  organization: Department of Oncology-Pathology, Cancer Centre Karolinska, Karolinska Institutet, Karolinska University Hospital
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  givenname: Roland
  orcidid: 0000-0002-6020-7498
  surname: Nilsson
  fullname: Nilsson, Roland
  email: roland.nilsson@ki.se
  organization: Cardiovascular Medicine Unit, Department of Medicine, Karolinska Institutet, Division of Cardiovascular Medicine, Karolinska University Hospital, Center for Molecular Medicine, Karolinska Institutet
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Snippet Glucocorticoids (GCs) are metabolic hormones with immunosuppressive effects that have proven effective drugs against childhood acute lymphoblastic leukemia...
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SubjectTerms 13/2
38/1
82/58
Acute lymphoblastic leukemia
Ammonia
Antibodies
Apoptosis
Autophagy
Bases (nucleic acids)
Biochemistry
Biomedical and Life Sciences
Cell Biology
Cell Culture
Cell death
Children
Glucocorticoids
Glucose metabolism
Glutamine
Glycolysis
Immunology
Immunosuppressive agents
Ketoglutaric acid
Lecithin
Leukemia
Life Sciences
Lymphatic leukemia
Metabolism
Metabolomics
Phagocytosis
Phosphatidylcholine
Proteomics
Tricarboxylic acid cycle
Title Metabolic reprogramming of acute lymphoblastic leukemia cells in response to glucocorticoid treatment
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