Crosstalk between AML and stromal cells triggers acetate secretion through the metabolic rewiring of stromal cells

Acute myeloid leukaemia (AML) cells interact and modulate components of their surrounding microenvironment into their own benefit. Stromal cells have been shown to support AML survival and progression through various mechanisms. Nonetheless, whether AML cells could establish beneficial metabolic int...

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Veröffentlicht in:	eLife Jg. 11
Hauptverfasser:	Vilaplana-Lopera, Nuria, Cuminetti, Vincent, Almaghrabi, Ruba, Papatzikas, Grigorios, Rout, Ashok Kumar, Jeeves, Mark, González, Elena, Alyahyawi, Yara, Cunningham, Alan, Erdem, Ayşegül, Schnütgen, Frank, Raghavan, Manoj, Potluri, Sandeep, Cazier, Jean-Baptiste, Schuringa, Jan Jacob, Reed, Michelle AC, Arranz, Lorena, Günther, Ulrich L, Garcia, Paloma
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	England eLife Sciences Publications Ltd 02.09.2022 eLife Sciences Publications, Ltd
Schlagworte:	Acetates Acetic acid acute myeloid leukaemia Acute myeloid leukemia Animals Biochemistry and Chemical Biology Bone marrow Cancer Biology Cell interactions Cell lines Experiments Gap junctions Glucose Glycolysis human Humans Leukemia, Myeloid, Acute - metabolism Lipids Metabolism Metabolites Mice microenvironment Microenvironments mouse NMR Nuclear magnetic resonance Pyruvates Pyruvic acid Reactive oxygen species Reactive Oxygen Species - metabolism Signal Transduction Standard deviation Stromal cells Stromal Cells - metabolism Transcriptomes Tricarboxylic acid cycle Tumor Microenvironment microenvironment mouse chemical biology acute myeloid leukaemia biochemistry cancer biology metabolism human nuclear magnetic resonance
ISSN:	2050-084X, 2050-084X
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Abstract	Acute myeloid leukaemia (AML) cells interact and modulate components of their surrounding microenvironment into their own benefit. Stromal cells have been shown to support AML survival and progression through various mechanisms. Nonetheless, whether AML cells could establish beneficial metabolic interactions with stromal cells is underexplored. By using a combination of human AML cell lines and AML patient samples together with mouse stromal cells and a MLL-AF9 mouse model, here we identify a novel metabolic crosstalk between AML and stromal cells where AML cells prompt stromal cells to secrete acetate for their own consumption to feed the tricarboxylic acid cycle (TCA) and lipid biosynthesis. By performing transcriptome analysis and tracer-based metabolic NMR analysis, we observe that stromal cells present a higher rate of glycolysis when co-cultured with AML cells. We also find that acetate in stromal cells is derived from pyruvate via chemical conversion under the influence of reactive oxygen species (ROS) following ROS transfer from AML to stromal cells via gap junctions. Overall, we present a unique metabolic communication between AML and stromal cells and propose two different molecular targets, ACSS2 and gap junctions, that could potentially be exploited for adjuvant therapy.
AbstractList	Acute myeloid leukaemia (AML) cells interact and modulate components of their surrounding microenvironment into their own benefit. Stromal cells have been shown to support AML survival and progression through various mechanisms. Nonetheless, whether AML cells could establish beneficial metabolic interactions with stromal cells is underexplored. By using a combination of human AML cell lines and AML patient samples together with mouse stromal cells and a MLL-AF9 mouse model, here we identify a novel metabolic crosstalk between AML and stromal cells where AML cells prompt stromal cells to secrete acetate for their own consumption to feed the tricarboxylic acid cycle (TCA) and lipid biosynthesis. By performing transcriptome analysis and tracer-based metabolic NMR analysis, we observe that stromal cells present a higher rate of glycolysis when co-cultured with AML cells. We also find that acetate in stromal cells is derived from pyruvate via chemical conversion under the influence of reactive oxygen species (ROS) following ROS transfer from AML to stromal cells via gap junctions. Overall, we present a unique metabolic communication between AML and stromal cells and propose two different molecular targets, ACSS2 and gap junctions, that could potentially be exploited for adjuvant therapy. Acute myeloid leukaemia (AML) cells interact and modulate components of their surrounding microenvironment into their own benefit. Stromal cells have been shown to support AML survival and progression through various mechanisms. Nonetheless, whether AML cells could establish beneficial metabolic interactions with stromal cells is underexplored. By using a combination of human AML cell lines and AML patient samples together with mouse stromal cells and a MLL-AF9 mouse model, here we identify a novel metabolic crosstalk between AML and stromal cells where AML cells prompt stromal cells to secrete acetate for their own consumption to feed the tricarboxylic acid cycle (TCA) and lipid biosynthesis. By performing transcriptome analysis and tracer-based metabolic NMR analysis, we observe that stromal cells present a higher rate of glycolysis when co-cultured with AML cells. We also find that acetate in stromal cells is derived from pyruvate via chemical conversion under the influence of reactive oxygen species (ROS) following ROS transfer from AML to stromal cells via gap junctions. Overall, we present a unique metabolic communication between AML and stromal cells and propose two different molecular targets, ACSS2 and gap junctions, that could potentially be exploited for adjuvant therapy.Acute myeloid leukaemia (AML) cells interact and modulate components of their surrounding microenvironment into their own benefit. Stromal cells have been shown to support AML survival and progression through various mechanisms. Nonetheless, whether AML cells could establish beneficial metabolic interactions with stromal cells is underexplored. By using a combination of human AML cell lines and AML patient samples together with mouse stromal cells and a MLL-AF9 mouse model, here we identify a novel metabolic crosstalk between AML and stromal cells where AML cells prompt stromal cells to secrete acetate for their own consumption to feed the tricarboxylic acid cycle (TCA) and lipid biosynthesis. By performing transcriptome analysis and tracer-based metabolic NMR analysis, we observe that stromal cells present a higher rate of glycolysis when co-cultured with AML cells. We also find that acetate in stromal cells is derived from pyruvate via chemical conversion under the influence of reactive oxygen species (ROS) following ROS transfer from AML to stromal cells via gap junctions. Overall, we present a unique metabolic communication between AML and stromal cells and propose two different molecular targets, ACSS2 and gap junctions, that could potentially be exploited for adjuvant therapy.
Author	Jeeves, Mark Papatzikas, Grigorios Rout, Ashok Kumar Reed, Michelle AC Vilaplana-Lopera, Nuria Schuringa, Jan Jacob Cunningham, Alan Cazier, Jean-Baptiste Schnütgen, Frank Raghavan, Manoj Alyahyawi, Yara Potluri, Sandeep Garcia, Paloma Erdem, Ayşegül Cuminetti, Vincent González, Elena Arranz, Lorena Günther, Ulrich L Almaghrabi, Ruba
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Keywords	microenvironment mouse chemical biology acute myeloid leukaemia biochemistry cancer biology metabolism human nuclear magnetic resonance
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Snippet	Acute myeloid leukaemia (AML) cells interact and modulate components of their surrounding microenvironment into their own benefit. Stromal cells have been...
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SubjectTerms	Acetates Acetic acid acute myeloid leukaemia Acute myeloid leukemia Animals Biochemistry and Chemical Biology Bone marrow Cancer Biology Cell interactions Cell lines Experiments Gap junctions Glucose Glycolysis human Humans Leukemia, Myeloid, Acute - metabolism Lipids Metabolism Metabolites Mice microenvironment Microenvironments mouse NMR Nuclear magnetic resonance Pyruvates Pyruvic acid Reactive oxygen species Reactive Oxygen Species - metabolism Signal Transduction Standard deviation Stromal cells Stromal Cells - metabolism Transcriptomes Tricarboxylic acid cycle Tumor Microenvironment
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Title	Crosstalk between AML and stromal cells triggers acetate secretion through the metabolic rewiring of stromal cells
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