BCAT1 promotes cell proliferation through amino acid catabolism in gliomas carrying wild-type IDH1 - Nature Medicine
- ️Radlwimmer, Bernhard
- ️Sun Jun 23 2013
Lieth, E. et al. Nitrogen shuttling between neurons and glial cells during glutamate synthesis. J. Neurochem. 76, 1712–1723 (2001).
Hutson, S.M. The case for regulating indispensable amino acid metabolism: the branched-chain α-keto acid dehydrogenase kinase-knockout mouse. Biochem. J. 400, e1–e3 (2006).
Ichihara, A. & Koyama, E. Transaminase of branched chain amino acids. I. Branched chain amino acids–α-ketoglutarate transaminase. J. Biochem. 59, 160–169 (1966).
Taylor, R.T. & Jenkins, W.T. Leucine aminotransferase. II. Purification and characterization. J. Biol. Chem. 241, 4396–4405 (1966).
García-Espinosa, M.A., Wallin, R., Hutson, S.M. & Sweatt, A.J. Widespread neuronal expression of branched-chain aminotransferase in the CNS: implications for leucine/glutamate metabolism and for signaling by amino acids. J. Neurochem. 100, 1458–1468 (2007).
Hall, T.R., Wallin, R., Reinhart, G.D. & Hutson, S.M. Branched chain aminotransferase isoenzymes. Purification and characterization of the rat brain isoenzyme. J. Biol. Chem. 268, 3092–3098 (1993).
Sweatt, A.J. et al. Branched-chain amino acid catabolism: unique segregation of pathway enzymes in organ systems and peripheral nerves. Am. J. Physiol. Endocrinol. Metab. 286, E64–E76 (2004).
Hutson, S.M., Sweatt, A.J. & Lanoue, K.F. Branched-chain [corrected] amino acid metabolism: implications for establishing safe intakes. J. Nutr. 135 (suppl. 6), 1557S–1564S (2005).
Eagle, H. Nutrition needs of mammalian cells in tissue culture. Science 122, 501–514 (1955).
DeBerardinis, R.J. & Cheng, T. Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene 29, 313–324 (2010).
DeBerardinis, R.J. et al. Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc. Natl. Acad. Sci. USA 104, 19345–19350 (2007).
Seltzer, M.J. et al. Inhibition of glutaminase preferentially slows growth of glioma cells with mutant IDH1. Cancer Res. 70, 8981–8987 (2010).
Wise, D.R. et al. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc. Natl. Acad. Sci. USA 105, 18782–18787 (2008).
Yang, C. et al. Glioblastoma cells require glutamate dehydrogenase to survive impairments of glucose metabolism or Akt signaling. Cancer Res. 69, 7986–7993 (2009).
Metallo, C.M. et al. Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature 481, 380–384 (2012).
Mullen, A.R. et al. Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature 481, 385–388 (2012).
Wise, D.R. et al. Hypoxia promotes isocitrate dehydrogenase–dependent carboxylation of α-ketoglutarate to citrate to support cell growth and viability. Proc. Natl. Acad. Sci. USA 108, 19611–19616 (2011).
Balss, J. et al. Analysis of the IDH1 codon 132 mutation in brain tumors. Acta Neuropathol. 116, 597–602 (2008).
Ichimura, K. et al. IDH1 mutations are present in the majority of common adult gliomas but rare in primary glioblastomas. Neuro-oncol. 11, 341–347 (2009).
Parsons, D.W. et al. An integrated genomic analysis of human glioblastoma multiforme. Science 321, 1807–1812 (2008).
Yan, H. et al. IDH1 and IDH2 mutations in gliomas. N. Engl. J. Med. 360, 765–773 (2009).
Brennan, C. et al. Glioblastoma subclasses can be defined by activity among signal transduction pathways and associated genomic alterations. PLoS ONE 4, e7752 (2009).
Colman, H. et al. A multigene predictor of outcome in glioblastoma. Neuro-oncol. 12, 49–57 (2010).
Noushmehr, H. et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17, 510–522 (2010).
Sturm, D. et al. Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 22, 425–437 (2012).
Toedt, G. et al. Molecular signatures classify astrocytic gliomas by IDH1 mutation status. Int. J. Cancer 128, 1095–1103 (2011).
Verhaak, R.G. et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17, 98–110 (2010).
Hartmann, C. et al. Patients with IDH1 wild type anaplastic astrocytomas exhibit worse prognosis than IDH1-mutated glioblastomas, and IDH1 mutation status accounts for the unfavorable prognostic effect of higher age: implications for classification of gliomas. Acta Neuropathol. 120, 707–718 (2010).
Sasaki, M. et al. D-2-hydroxyglutarate produced by mutant IDH1 perturbs collagen maturation and basement membrane function. Genes Dev. 26, 2038–2049 (2012).
Sasaki, M. et al. IDH1(R132H) mutation increases murine haematopoietic progenitors and alters epigenetics. Nature 488, 656–659 (2012).
Dang, L., Jin, S. & Su, S.M. IDH mutations in glioma and acute myeloid leukemia. Trends Mol. Med. 16, 387–397 (2010).
Dang, L. et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462, 739–744 (2009).
Figueroa, M.E. et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 18, 553–567 (2010).
Lu, C. et al. IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature 483, 474–478 (2012).
Xu, W. et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of α-ketoglutarate–dependent dioxygenases. Cancer Cell 19, 17–30 (2011).
Schramm, G. et al. PathWave: discovering patterns of differentially regulated enzymes in metabolic pathways. Bioinformatics 26, 1225–1231 (2010).
Gravendeel, L.A. et al. Intrinsic gene expression profiles of gliomas are a better predictor of survival than histology. Cancer Res. 69, 9065–9072 (2009).
Turcan, S. et al. IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 483, 479–483 (2012).
Reitman, Z.J. & Yan, H. Isocitrate dehydrogenase 1 and 2 mutations in cancer: alterations at a crossroads of cellular metabolism. J. Natl. Cancer Inst. 102, 932–941 (2010).
She, P. et al. Disruption of BCATm in mice leads to increased energy expenditure associated with the activation of a futile protein turnover cycle. Cell Metab. 6, 181–194 (2007).
Goto, M. et al. Structural determinants for branched-chain aminotransferase isozyme-specific inhibition by the anticonvulsant drug gabapentin. J. Biol. Chem. 280, 37246–37256 (2005).
Sontheimer, H. A role for glutamate in growth and invasion of primary brain tumors. J. Neurochem. 105, 287–295 (2008).
Pasquali, M., Monsen, G., Richardson, L., Alston, M. & Longo, N. Biochemical findings in common inborn errors of metabolism. Am. J. Med. Genet. C. Semin. Med. Genet. 142C, 64–76 (2006).
Koppenol, W.H., Bounds, P.L. & Dang, C.V. Otto Warburg's contributions to current concepts of cancer metabolism. Nat. Rev. Cancer 11, 325–337 (2011).
de Bont, J.M. et al. Differential expression and prognostic significance of SOX genes in pediatric medulloblastoma and ependymoma identified by microarray analysis. Neuro-oncol. 10, 648–660 (2008).
Goto, M., Shinno, H. & Ichihara, A. Isozyme patterns of branched-chain amino acid transaminase in human tissues and tumors. Gann 68, 663–667 (1977).
Weggen, S. et al. Identification of amplified genes from SV40 large T antigen–induced rat PNET cell lines by subtractive cDNA analysis and radiation hybrid mapping. Oncogene 20, 2023–2031 (2001).
Yoshikawa, R. et al. ECA39 is a novel distant metastasis-related biomarker in colorectal cancer. World J. Gastroenterol. 12, 5884–5889 (2006).
Zhou, W. et al. Functional evidence for a nasopharyngeal carcinoma-related gene BCAT1 located at 12p12. Oncol. Res. 16, 405–413 (2007).
Reitman, Z.J. et al. Profiling the effects of isocitrate dehydrogenase 1 and 2 mutations on the cellular metabolome. Proc. Natl. Acad. Sci. USA 108, 3270–3275 (2011).
Zhao, S. et al. Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1α. Science 324, 261–265 (2009).
Davoodi, J. et al. Overexpression and characterization of the human mitochondrial and cytosolic branched-chain aminotransferases. J. Biol. Chem. 273, 4982–4989 (1998).
Locasale, J.W. et al. Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis. Nat. Genet. 43, 869–874 (2011).
Possemato, R. et al. Functional genomics reveal that the serine synthesis pathway is essential in breast cancer. Nature 476, 346–350 (2011).
Jain, M. et al. Metabolite profiling identifies a key role for glycine in rapid cancer cell proliferation. Science 336, 1040–1044 (2012).
Hartmann, C. et al. Type and frequency of IDH1 and IDH2 mutations are related to astrocytic and oligodendroglial differentiation and age: a study of 1,010 diffuse gliomas. Acta Neuropathol. 118, 469–474 (2009).
Capper, D., Zentgraf, H., Balss, J., Hartmann, C. & von Deimling, A. Monoclonal antibody specific for IDH1 R132H mutation. Acta Neuropathol. 118, 599–601 (2009).
Buckingham, S.C. et al. Glutamate release by primary brain tumors induces epileptic activity. Nat. Med. 17, 1269–1274 (2011).
Grzendowski, M. et al. Simultaneous extraction of nucleic acids and proteins from tissue specimens by ultracentrifugation: a protocol using the high-salt protein fraction for quantitative proteome analysis. Proteomics 9, 4985–4990 (2009).
Ehrich, M. et al. Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc. Natl. Acad. Sci. USA 102, 15785–15790 (2005).
Campos, B. et al. Differentiation therapy exerts antitumor effects on stem-like glioma cells. Clin. Cancer Res. 16, 2715–2728 (2010).
Turcan, S. et al. IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 483, 479–483 (2012).
Wiederschain, D. et al. Single-vector inducible lentiviral RNAi system for oncology target validation. Cell Cycle 8, 498–504 (2009).
Bai, A.H. et al. MicroRNA-182 promotes leptomeningeal spread of non-sonic hedgehog-medulloblastoma. Acta Neuropathol. 123, 529–538 (2012).
Rolli, C.G., Seufferlein, T., Kemkemer, R. & Spatz, J.P. Impact of tumor cell cytoskeleton organization on invasiveness and migration: a microchannel-based approach. PLoS ONE 5, e8726 (2010).
Sze, D.Y. & Jardetzky, O. Determination of metabolite and nucleotide concentrations in proliferating lymphocytes by 1H-NMR of acid extracts. Biochim. Biophys. Acta 1054, 181–197 (1990).
Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall, R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275 (1951).
Helenius, A. & Simons, K. The binding of detergents to lipophilic and hydrophilic proteins. J. Biol. Chem. 247, 3656–3661 (1972).
Sauer, S.W. et al. Intracerebral accumulation of glutaric and 3-hydroxyglutaric acids secondary to limited flux across the blood-brain barrier constitute a biochemical risk factor for neurodegeneration in glutaryl-CoA dehydrogenase deficiency. J. Neurochem. 97, 899–910 (2006).
She, P. et al. Disruption of BCATm in mice leads to increased energy expenditure associated with the activation of a futile protein turnover cycle. Cell Metab. 6, 181–194 (2007).
Suryawan, A. et al. A molecular model of human branched-chain amino acid metabolism. Am. J. Clin. Nutr. 68, 72–81 (1998).
Hutson, S.M. et al. Role of branched-chain aminotransferase isoenzymes and gabapentin in neurotransmitter metabolism. J. Neurochem. 71, 863–874 (1998).