Oncogenes induce the cancer-associated fibroblast phenotype: Metabolic symbiosis and "fibroblast addiction" are new therapeutic targets for drug discovery

Metabolic coupling, between mitochondria in cancer cells and catabolism in stromal fibroblasts, promotes tumor growth, recurrence, metastasis, and predicts anticancer drug resistance. Catabolic fibroblasts donate the necessary fuels (such as L-lactate, ketones, glutamine, other amino acids, and fatt...

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Veröffentlicht in:Cell cycle (Georgetown, Tex.) Jg. 12; H. 17; S. 2723 - 2732
Hauptverfasser: Lisanti, Michael P., Martinez-Outschoorn, Ubaldo E., Sotgia, Federica
Format: Journal Article
Sprache:Englisch
Veröffentlicht: United States Taylor & Francis 01.09.2013
Landes Bioscience
Schlagworte:
BRCA1
cancer-associated fibroblast
Drug Discovery
Fibroblasts - drug effects
Fibroblasts - metabolism
Fibroblasts - pathology
glycolysis
Humans
metabolic symbiosis
Molecular Targeted Therapy
Neoplasms - drug therapy
Neoplasms - metabolism
Neoplasms - pathology
NFkB
oncogene
Oncogenes - genetics
oxidative stress
Phenotype
RAS
stromal biomarkers
TGF-beta
tumor microenvironment
tumor suppressor
cancer-associated fibroblast
TGF-beta
RAS
glycolysis
tumor suppressor
BRCA1
NFkB
stromal biomarkers
tumor microenvironment
oncogene
metabolic symbiosis
oxidative stress
ISSN:1538-4101, 1551-4005, 1551-4005
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Abstract Metabolic coupling, between mitochondria in cancer cells and catabolism in stromal fibroblasts, promotes tumor growth, recurrence, metastasis, and predicts anticancer drug resistance. Catabolic fibroblasts donate the necessary fuels (such as L-lactate, ketones, glutamine, other amino acids, and fatty acids) to anabolic cancer cells, to metabolize via their TCA cycle and oxidative phosphorylation (OXPHOS). This provides a simple mechanism by which metabolic energy and biomass are transferred from the host microenvironment to cancer cells. Recently, we showed that catabolic metabolism and "glycolytic reprogramming" in the tumor microenvironment are orchestrated by oncogene activation and inflammation, which originates in epithelial cancer cells. Oncogenes drive the onset of the cancer-associated fibroblast phenotype in adjacent normal fibroblasts via paracrine oxidative stress. This oncogene-induced transition to malignancy is "mirrored" by a loss of caveolin-1 (Cav-1) and an increase in MCT4 in adjacent stromal fibroblasts, functionally reflecting catabolic metabolism in the tumor microenvironment. Virtually identical findings were obtained using BRCA1-deficient breast and ovarian cancer cells. Thus, oncogene activation (RAS, NFkB, TGF-β) and/or tumor suppressor loss (BRCA1) have similar functional effects on adjacent stromal fibroblasts, initiating "metabolic symbiosis" and the cancer-associated fibroblast phenotype. New therapeutic strategies that metabolically uncouple oxidative cancer cells from their glycolytic stroma or modulate oxidative stress could be used to target this lethal subtype of cancers. Targeting "fibroblast addiction" in primary and metastatic tumor cells may expose a critical Achilles' heel, leading to disease regression in both sporadic and familial cancers.
AbstractList Metabolic coupling, between mitochondria in cancer cells and catabolism in stromal fibroblasts, promotes tumor growth, recurrence, metastasis, and predicts anticancer drug resistance. Catabolic fibroblasts donate the necessary fuels (such as L-lactate, ketones, glutamine, other amino acids, and fatty acids) to anabolic cancer cells, to metabolize via their TCA cycle and oxidative phosphorylation (OXPHOS). This provides a simple mechanism by which metabolic energy and biomass are transferred from the host microenvironment to cancer cells. Recently, we showed that catabolic metabolism and "glycolytic reprogramming" in the tumor microenvironment are orchestrated by oncogene activation and inflammation, which originates in epithelial cancer cells. Oncogenes drive the onset of the cancer-associated fibroblast phenotype in adjacent normal fibroblasts via paracrine oxidative stress. This oncogene-induced transition to malignancy is "mirrored" by a loss of caveolin-1 (Cav-1) and an increase in MCT4 in adjacent stromal fibroblasts, functionally reflecting catabolic metabolism in the tumor microenvironment. Virtually identical findings were obtained using BRCA1-deficient breast and ovarian cancer cells. Thus, oncogene activation (RAS, NFkB, TGF-β) and/or tumor suppressor loss (BRCA1) have similar functional effects on adjacent stromal fibroblasts, initiating "metabolic symbiosis" and the cancer-associated fibroblast phenotype. New therapeutic strategies that metabolically uncouple oxidative cancer cells from their glycolytic stroma or modulate oxidative stress could be used to target this lethal subtype of cancers. Targeting "fibroblast addiction" in primary and metastatic tumor cells may expose a critical Achilles' heel, leading to disease regression in both sporadic and familial cancers.
Metabolic coupling, between mitochondria in cancer cells and catabolism in stromal fibroblasts, promotes tumor growth, recurrence, metastasis, and predicts anticancer drug resistance. Catabolic fibroblasts donate the necessary fuels (such as L-lactate, ketones, glutamine, other amino acids, and fatty acids) to anabolic cancer cells, to metabolize via their TCA cycle and oxidative phosphorylation (OXPHOS). This provides a simple mechanism by which metabolic energy and biomass are transferred from the host microenvironment to cancer cells. Recently, we showed that catabolic metabolism and "glycolytic reprogramming" in the tumor microenvironment are orchestrated by oncogene activation and inflammation, which originates in epithelial cancer cells. Oncogenes drive the onset of the cancer-associated fibroblast phenotype in adjacent normal fibroblasts via paracrine oxidative stress. This oncogene-induced transition to malignancy is "mirrored" by a loss of caveolin-1 (Cav-1) and an increase in MCT4 in adjacent stromal fibroblasts, functionally reflecting catabolic metabolism in the tumor microenvironment. Virtually identical findings were obtained using BRCA1-deficient breast and ovarian cancer cells. Thus, oncogene activation (RAS, NFkB, TGF-β) and/or tumor suppressor loss (BRCA1) have similar functional effects on adjacent stromal fibroblasts, initiating "metabolic symbiosis" and the cancer-associated fibroblast phenotype. New therapeutic strategies that metabolically uncouple oxidative cancer cells from their glycolytic stroma or modulate oxidative stress could be used to target this lethal subtype of cancers. Targeting "fibroblast addiction" in primary and metastatic tumor cells may expose a critical Achilles' heel, leading to disease regression in both sporadic and familial cancers.Metabolic coupling, between mitochondria in cancer cells and catabolism in stromal fibroblasts, promotes tumor growth, recurrence, metastasis, and predicts anticancer drug resistance. Catabolic fibroblasts donate the necessary fuels (such as L-lactate, ketones, glutamine, other amino acids, and fatty acids) to anabolic cancer cells, to metabolize via their TCA cycle and oxidative phosphorylation (OXPHOS). This provides a simple mechanism by which metabolic energy and biomass are transferred from the host microenvironment to cancer cells. Recently, we showed that catabolic metabolism and "glycolytic reprogramming" in the tumor microenvironment are orchestrated by oncogene activation and inflammation, which originates in epithelial cancer cells. Oncogenes drive the onset of the cancer-associated fibroblast phenotype in adjacent normal fibroblasts via paracrine oxidative stress. This oncogene-induced transition to malignancy is "mirrored" by a loss of caveolin-1 (Cav-1) and an increase in MCT4 in adjacent stromal fibroblasts, functionally reflecting catabolic metabolism in the tumor microenvironment. Virtually identical findings were obtained using BRCA1-deficient breast and ovarian cancer cells. Thus, oncogene activation (RAS, NFkB, TGF-β) and/or tumor suppressor loss (BRCA1) have similar functional effects on adjacent stromal fibroblasts, initiating "metabolic symbiosis" and the cancer-associated fibroblast phenotype. New therapeutic strategies that metabolically uncouple oxidative cancer cells from their glycolytic stroma or modulate oxidative stress could be used to target this lethal subtype of cancers. Targeting "fibroblast addiction" in primary and metastatic tumor cells may expose a critical Achilles' heel, leading to disease regression in both sporadic and familial cancers.
Author Martinez-Outschoorn, Ubaldo E.
Lisanti, Michael P.
Sotgia, Federica
Author_xml – sequence: 1
  givenname: Michael P.
  surname: Lisanti
  fullname: Lisanti, Michael P.
  email: mlisanti@KimmelCancerCenter.org
– sequence: 2
  givenname: Ubaldo E.
  surname: Martinez-Outschoorn
  fullname: Martinez-Outschoorn, Ubaldo E.
  email: Ubaldo.Martinez-Outschoorn@jeffersonhospital.org
– sequence: 3
  givenname: Federica
  surname: Sotgia
  fullname: Sotgia, Federica
  email: fsotgia@gmail.com
BackLink https://www.ncbi.nlm.nih.gov/pubmed/23860382$$D View this record in MEDLINE/PubMed
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Issue 17
Keywords cancer-associated fibroblast
TGF-beta
RAS
glycolysis
tumor suppressor
BRCA1
NFkB
stromal biomarkers
tumor microenvironment
oncogene
metabolic symbiosis
oxidative stress
Language English
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Snippet Metabolic coupling, between mitochondria in cancer cells and catabolism in stromal fibroblasts, promotes tumor growth, recurrence, metastasis, and predicts...
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SubjectTerms BRCA1
cancer-associated fibroblast
Drug Discovery
Fibroblasts - drug effects
Fibroblasts - metabolism
Fibroblasts - pathology
glycolysis
Humans
metabolic symbiosis
Molecular Targeted Therapy
Neoplasms - drug therapy
Neoplasms - metabolism
Neoplasms - pathology
NFkB
oncogene
Oncogenes - genetics
oxidative stress
Phenotype
RAS
stromal biomarkers
TGF-beta
tumor microenvironment
tumor suppressor
Title Oncogenes induce the cancer-associated fibroblast phenotype: Metabolic symbiosis and "fibroblast addiction" are new therapeutic targets for drug discovery
URI https://www.tandfonline.com/doi/abs/10.4161/cc.25695
https://www.ncbi.nlm.nih.gov/pubmed/23860382
https://www.proquest.com/docview/1431623004
https://pubmed.ncbi.nlm.nih.gov/PMC3899185
Volume 12
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