Cited by 550Cancer, Hypoxia, and MetabolismRenal cell carcinoma treatmentMetabolism, Diabetes, and Cancer

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Fructose-1,6-bisphosphatase opposes renal carcinoma progression

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Li, Bo, Qiu, Bo, Lee, David S. M., Walton, Zandra E., Ochocki, Joshua D., Mathew, Lijoy K., Mancuso, Anthony, Gade, Terence P. F., Keith, Brian, Nissim, Itzhak, Simon, M. Celeste·2014·Nature

DOI 10.1038/nature13557PMC PMC4162811

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Abstract

Clear cell renal cell carcinoma (ccRCC), the most common form of kidney cancer, is characterized by elevated glycogen levels and fat deposition. These consistent metabolic alterations are associated with normoxic stabilization of hypoxia-inducible factors (HIFs) secondary to von Hippel-Lindau (VHL) mutations that occur in over 90% of ccRCC tumours. However, kidney-specific VHL deletion in mice fails to elicit ccRCC-specific metabolic phenotypes and tumour formation, suggesting that additional mechanisms are essential. Recent large-scale sequencing analyses revealed the loss of several chromatin remodelling enzymes in a subset of ccRCC (these included polybromo-1, SET domain containing 2 and BRCA1-associated protein-1, among others), indicating that epigenetic perturbations are probably important contributors to the natural history of this disease. Here we used an integrative approach comprising pan-metabolomic profiling and metabolic gene set analysis and determined that the gluconeogenic enzyme fructose-1,6-bisphosphatase 1 (FBP1) is uniformly depleted in over six hundred ccRCC tumours examined. Notably, the human FBP1 locus resides on chromosome 9q22, the loss of which is associated with poor prognosis for ccRCC patients. Our data further indicate that FBP1 inhibits ccRCC progression through two distinct mechanisms. First, FBP1 antagonizes glycolytic flux in renal tubular epithelial cells, the presumptive ccRCC cell of origin, thereby inhibiting a potential Warburg effect. Second, in pVHL (the protein encoded by the VHL gene)-deficient ccRCC cells, FBP1 restrains cell proliferation, glycolysis and the pentose phosphate pathway in a catalytic-activity-independent manner, by inhibiting nuclear HIF function via direct interaction with the HIF inhibitory domain. This unique dual function of the FBP1 protein explains its ubiquitous loss in ccRCC, distinguishing FBP1 from previously identified tumour suppressors that are not consistently mutated in all tumours.

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Additional file 6 of Hypoxia-induced P4HA1 overexpression promotes post-ischemic angiogenesis by enhancing endothelial glycolysis through downregulating FBP1
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Additional file 9 of Varied hypoxia adaptation patterns of embryonic brain at different development stages between Tibetan and Dwarf laying chickens
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Additional file 12 of Varied hypoxia adaptation patterns of embryonic brain at different development stages between Tibetan and Dwarf laying chickens
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Additional file 3 of Comprehensive analysis of m6A modification in immune infiltration, metabolism and drug resistance in hepatocellular carcinoma
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Additional file 2 of Hypoxia-induced P4HA1 overexpression promotes post-ischemic angiogenesis by enhancing endothelial glycolysis through downregulating FBP1
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Additional file 6 of Varied hypoxia adaptation patterns of embryonic brain at different development stages between Tibetan and Dwarf laying chickens
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Additional file 4 of Comprehensive analysis of m6A modification in immune infiltration, metabolism and drug resistance in hepatocellular carcinoma
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Additional file 13 of Varied hypoxia adaptation patterns of embryonic brain at different development stages between Tibetan and Dwarf laying chickens
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Additional file 10 of Varied hypoxia adaptation patterns of embryonic brain at different development stages between Tibetan and Dwarf laying chickens
Tang, Q., Yu, R., Wang, Y., Xie, F., Zhang, H., Wu, C., & Fang, M. (2024) · Figshare · doi:10.6084/m9.figshare.26598821
Additional file 11 of Varied hypoxia adaptation patterns of embryonic brain at different development stages between Tibetan and Dwarf laying chickens
Tang, Q., Yu, R., Wang, Y., Xie, F., Zhang, H., Wu, C., & Fang, M. (2024) · Figshare · doi:10.6084/m9.figshare.26598824
Additional file 8 of Hypoxia-induced P4HA1 overexpression promotes post-ischemic angiogenesis by enhancing endothelial glycolysis through downregulating FBP1
Xu, Y., Xia, D., Huang, K., & Liang, M. (2024) · Figshare · doi:10.6084/m9.figshare.26669403
Additional file 4 of Hypoxia-induced P4HA1 overexpression promotes post-ischemic angiogenesis by enhancing endothelial glycolysis through downregulating FBP1
Xu, Y., Xia, D., Huang, K., & Liang, M. (2024) · Figshare · doi:10.6084/m9.figshare.26669391
Additional file 4 of Varied hypoxia adaptation patterns of embryonic brain at different development stages between Tibetan and Dwarf laying chickens
Tang, Q., Yu, R., Wang, Y., Xie, F., Zhang, H., Wu, C., & Fang, M. (2024) · Figshare · doi:10.6084/m9.figshare.26598803
Additional file 3 of A novel 10 glycolysis-related genes signature could predict overall survival for clear cell renal cell carcinoma
Qianwei, X., Zeng, T., Liu, S., Cheng, H., Ma, L., & Wang, Y. (2021) · Figshare · doi:10.6084/m9.figshare.14396794
Additional file 5 of Hypoxia-induced P4HA1 overexpression promotes post-ischemic angiogenesis by enhancing endothelial glycolysis through downregulating FBP1
Xu, Y., Xia, D., Huang, K., & Liang, M. (2024) · Figshare · doi:10.6084/m9.figshare.26669394
Additional file 1 of Hypoxia-induced P4HA1 overexpression promotes post-ischemic angiogenesis by enhancing endothelial glycolysis through downregulating FBP1
Xu, Y., Xia, D., Huang, K., & Liang, M. (2024) · Figshare · doi:10.6084/m9.figshare.26669382
Additional file 1 of Varied hypoxia adaptation patterns of embryonic brain at different development stages between Tibetan and Dwarf laying chickens
Tang, Q., Yu, R., Wang, Y., Xie, F., Zhang, H., Wu, C., & Fang, M. (2024) · Figshare · doi:10.6084/m9.figshare.26598794
Additional file 7 of Varied hypoxia adaptation patterns of embryonic brain at different development stages between Tibetan and Dwarf laying chickens
Tang, Q., Yu, R., Wang, Y., Xie, F., Zhang, H., Wu, C., & Fang, M. (2024) · Figshare · doi:10.6084/m9.figshare.26598812
Additional file 2 of Varied hypoxia adaptation patterns of embryonic brain at different development stages between Tibetan and Dwarf laying chickens
Tang, Q., Yu, R., Wang, Y., Xie, F., Zhang, H., Wu, C., & Fang, M. (2024) · Figshare · doi:10.6084/m9.figshare.26598797
Additional file 7 of Hypoxia-induced P4HA1 overexpression promotes post-ischemic angiogenesis by enhancing endothelial glycolysis through downregulating FBP1
Xu, Y., Xia, D., Huang, K., & Liang, M. (2024) · Figshare · doi:10.6084/m9.figshare.26669400
Additional file 5 of Varied hypoxia adaptation patterns of embryonic brain at different development stages between Tibetan and Dwarf laying chickens
Tang, Q., Yu, R., Wang, Y., Xie, F., Zhang, H., Wu, C., & Fang, M. (2024) · Figshare · doi:10.6084/m9.figshare.26598806
Additional file 3 of Hypoxia-induced P4HA1 overexpression promotes post-ischemic angiogenesis by enhancing endothelial glycolysis through downregulating FBP1
Xu, Y., Xia, D., Huang, K., & Liang, M. (2024) · Figshare · doi:10.6084/m9.figshare.26669388
Additional file 2 of Comprehensive analysis of m6A modification in immune infiltration, metabolism and drug resistance in hepatocellular carcinoma
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BindingDB Entry 50010593: Identification of the New Covalent Allosteric Binding Site of Fructose-1,6-bisphosphatase with Disulfiram Derivatives toward Glucose Reduction.
BindingDB (2021) · UC San Diego · doi:10.7270/q2w099g3
BindingDB Entry 50009047: Small-Molecule Modulators of the Hypoxia-Inducible Factor Pathway: Development and Therapeutic Applications.
BindingDB (2021) · UC San Diego · doi:10.7270/q2qf8x9v
BindingDB Entry 50018336: PFKFB3 inhibitors as potential anticancer agents: Mechanisms of action, current developments, and structure-activity relationships.
BindingDB (2024) · UC San Diego · doi:10.7270/q26h4nnj

Authors: Li, B., Qiu, B., Lee, D. S. M., Walton, Z. E., Ochocki, J. D., Mathew, L. K., Mancuso, A., Gade, T. P. F., Keith, B., Nissim, I., & Simon, M. C.
Affiliations: Abramson Cancer Center (US)
Howard Hughes Medical Institute (US)
University of Pennsylvania (US)
Children's Hospital of Philadelphia (US)
Corresponding author: Simon, M. Celeste
ORCID: Li, Bo
Qiu, Bo
Lee, David S. M.
Walton, Zandra E.
Gade, Terence P. F.
Keith, Brian
Nissim, Itzhak
Simon, M. Celeste
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2014-07-20
Volume: 513
Issue: 7517
Pages: 251-255
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature13557
PMC: PMC4162811
OpenAlex: W2069663698
Cited by: 535
References: 31
Citations by year: 2026: 24 · 2025: 38 · 2024: 44 · 2023: 44 · 2022: 48 · 2021: 64 · 2020: 54 · 2019: 42 · 2018: 54 · 2017: 42 · 2016: 40 · 2015: 33 · 2014: 6
FWCI: 12.92
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Howard Hughes Medical Institute
National Institutes of Health
National Cancer Institute (F30CA177106, P01CA104838, CA104838, F32CA192758, P30CA016520)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK053761, DK-053761, R56DK053761)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Health Sciences › Medicine › Oncology › Renal cell carcinoma treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Keywords: FBP1, clear cell renal cell carcinoma, von Hippel-Lindau protein, hypoxia-inducible factor, glycolysis, pentose phosphate pathway, Warburg effect, renal tubular epithelial cells, tumor progression, chromatin remodeling, cancer metabolism, epigenetic regulation, gluconeogenesis
MeSH terms: Animals, Carcinoma, Renal Cell, Cell Line, Epithelial Cells, Glycolysis, Fructose-Bisphosphatase, Humans, Kidney Neoplasms, Models, Molecular, NADP, Swine, Protein Structure, Tertiary, Disease Progression, Cell Line, Tumor, Cell Proliferation, Basic Helix-Loop-Helix Proteins

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Fructose-1,6-bisphosphatase opposes renal carcinoma progression

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