Metabolomic profile of glycolysis and the pentose phosphate pathway identifies the central role of glucose-6-phosphate dehydrogenase in clear cell-renal cell carcinoma

The analysis of cancer metabolome has shown that proliferating tumor cells require a large quantities of different nutrients in order to support their high rate of proliferation. In this study we analyzed the metabolic profile of glycolysis and the pentose phosphate pathway (PPP) in human clear cell...

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Published in	Oncotarget Vol. 6; no. 15; pp. 13371 - 13386
Main Authors	Lucarelli, Giuseppe, Galleggiante, Vanessa, Rutigliano, Monica, Sanguedolce, Francesca, Cagiano, Simona, Bufo, Pantaleo, Lastilla, Gaetano, Maiorano, Eugenio, Ribatti, Domenico, Giglio, Andrea, Serino, Grazia, Vavallo, Antonio, Bettocchi, Carlo, Selvaggi, Francesco Paolo, Battaglia, Michele, Ditonno, Pasquale
Format	Journal Article
Language	English
Published	United States Impact Journals LLC 30.05.2015
Subjects	Adult Aged Aged, 80 and over Carcinoma, Renal Cell - enzymology Carcinoma, Renal Cell - pathology Cell Proliferation - physiology Chromatography, Liquid Female Gas Chromatography-Mass Spectrometry Glucosephosphate Dehydrogenase - metabolism Glycolysis - physiology Humans Kidney Neoplasms - enzymology Kidney Neoplasms - pathology Male Metabolomics Middle Aged NADP - metabolism Pentose Phosphate Pathway - physiology Reactive Oxygen Species - metabolism Real-Time Polymerase Chain Reaction Research Paper Tumor Cells, Cultured renal cell carcinoma metabolomics pentose phosphate pathway G6PDH glycolysis
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ISSN	1949-2553 1949-2553
DOI	10.18632/oncotarget.3823

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Abstract	The analysis of cancer metabolome has shown that proliferating tumor cells require a large quantities of different nutrients in order to support their high rate of proliferation. In this study we analyzed the metabolic profile of glycolysis and the pentose phosphate pathway (PPP) in human clear cell-renal cell carcinoma (ccRCC) and evaluate the role of these pathways in sustaining cell proliferation, maintenance of NADPH levels, and production of reactive oxygen species (ROS). Metabolomic analysis showed a clear signature of increased glucose uptake and utilization in ccRCC tumor samples. Elevated levels of glucose-6-phosphate dehydrogenase (G6PDH) in association with higher levels of PPP-derived metabolites, suggested a prominent role of this pathway in RCC-associated metabolic alterations. G6PDH inhibition, caused a significant decrease in cancer cell survival, a decrease in NADPH levels, and an increased production of ROS, suggesting that the PPP plays an important role in the regulation of ccRCC redox homeostasis. Patients with high levels of glycolytic enzymes had reduced progression-free and cancer-specific survivals as compared to subjects with low levels. Our data suggest that oncogenic signaling pathways may promote ccRCC through rerouting the sugar metabolism. Blocking the flux through this pathway may serve as a novel therapeutic target.
AbstractList	The analysis of cancer metabolome has shown that proliferating tumor cells require a large quantities of different nutrients in order to support their high rate of proliferation. In this study we analyzed the metabolic profile of glycolysis and the pentose phosphate pathway (PPP) in human clear cell-renal cell carcinoma (ccRCC) and evaluate the role of these pathways in sustaining cell proliferation, maintenance of NADPH levels, and production of reactive oxygen species (ROS). Metabolomic analysis showed a clear signature of increased glucose uptake and utilization in ccRCC tumor samples. Elevated levels of glucose-6-phosphate dehydrogenase (G6PDH) in association with higher levels of PPP-derived metabolites, suggested a prominent role of this pathway in RCC-associated metabolic alterations. G6PDH inhibition, caused a significant decrease in cancer cell survival, a decrease in NADPH levels, and an increased production of ROS, suggesting that the PPP plays an important role in the regulation of ccRCC redox homeostasis. Patients with high levels of glycolytic enzymes had reduced progression-free and cancer-specific survivals as compared to subjects with low levels. Our data suggest that oncogenic signaling pathways may promote ccRCC through rerouting the sugar metabolism. Blocking the flux through this pathway may serve as a novel therapeutic target. The analysis of cancer metabolome has shown that proliferating tumor cells require a large quantities of different nutrients in order to support their high rate of proliferation. In this study we analyzed the metabolic profile of glycolysis and the pentose phosphate pathway (PPP) in human clear cell-renal cell carcinoma (ccRCC) and evaluate the role of these pathways in sustaining cell proliferation, maintenance of NADPH levels, and production of reactive oxygen species (ROS). Metabolomic analysis showed a clear signature of increased glucose uptake and utilization in ccRCC tumor samples. Elevated levels of glucose-6-phosphate dehydrogenase (G6PDH) in association with higher levels of PPP-derived metabolites, suggested a prominent role of this pathway in RCC-associated metabolic alterations. G6PDH inhibition, caused a significant decrease in cancer cell survival, a decrease in NADPH levels, and an increased production of ROS, suggesting that the PPP plays an important role in the regulation of ccRCC redox homeostasis. Patients with high levels of glycolytic enzymes had reduced progression-free and cancer-specific survivals as compared to subjects with low levels. Our data suggest that oncogenic signaling pathways may promote ccRCC through rerouting the sugar metabolism. Blocking the flux through this pathway may serve as a novel therapeutic target.The analysis of cancer metabolome has shown that proliferating tumor cells require a large quantities of different nutrients in order to support their high rate of proliferation. In this study we analyzed the metabolic profile of glycolysis and the pentose phosphate pathway (PPP) in human clear cell-renal cell carcinoma (ccRCC) and evaluate the role of these pathways in sustaining cell proliferation, maintenance of NADPH levels, and production of reactive oxygen species (ROS). Metabolomic analysis showed a clear signature of increased glucose uptake and utilization in ccRCC tumor samples. Elevated levels of glucose-6-phosphate dehydrogenase (G6PDH) in association with higher levels of PPP-derived metabolites, suggested a prominent role of this pathway in RCC-associated metabolic alterations. G6PDH inhibition, caused a significant decrease in cancer cell survival, a decrease in NADPH levels, and an increased production of ROS, suggesting that the PPP plays an important role in the regulation of ccRCC redox homeostasis. Patients with high levels of glycolytic enzymes had reduced progression-free and cancer-specific survivals as compared to subjects with low levels. Our data suggest that oncogenic signaling pathways may promote ccRCC through rerouting the sugar metabolism. Blocking the flux through this pathway may serve as a novel therapeutic target.
Author	Sanguedolce, Francesca Battaglia, Michele Rutigliano, Monica Cagiano, Simona Lastilla, Gaetano Bettocchi, Carlo Maiorano, Eugenio Vavallo, Antonio Lucarelli, Giuseppe Serino, Grazia Bufo, Pantaleo Ribatti, Domenico Selvaggi, Francesco Paolo Galleggiante, Vanessa Giglio, Andrea Ditonno, Pasquale
AuthorAffiliation	5 National Cancer Institute “Giovanni Paolo II”, Bari, Italy 2 Department of Pathology, University of Foggia, Foggia, Italy 3 Department of Pathology, University of Bari, Bari, Italy 1 Department of Emergency and Organ Transplantation-Urology, Andrology and Kidney Transplantation Unit, University of Bari, Bari, Italy 4 Department of Basic Medical Sciences, Neurosciences and Sensory Organs, University of Bari, Bari, Italy
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Snippet	The analysis of cancer metabolome has shown that proliferating tumor cells require a large quantities of different nutrients in order to support their high...
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SubjectTerms	Adult Aged Aged, 80 and over Carcinoma, Renal Cell - enzymology Carcinoma, Renal Cell - pathology Cell Proliferation - physiology Chromatography, Liquid Female Gas Chromatography-Mass Spectrometry Glucosephosphate Dehydrogenase - metabolism Glycolysis - physiology Humans Kidney Neoplasms - enzymology Kidney Neoplasms - pathology Male Metabolomics Middle Aged NADP - metabolism Pentose Phosphate Pathway - physiology Reactive Oxygen Species - metabolism Real-Time Polymerase Chain Reaction Research Paper Tumor Cells, Cultured
Title	Metabolomic profile of glycolysis and the pentose phosphate pathway identifies the central role of glucose-6-phosphate dehydrogenase in clear cell-renal cell carcinoma
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