Abstract
Mutations in the enzyme cytosolic isocitrate dehydrogenase 1 (IDH1) are a common feature of a major subset of primary human brain cancers. These mutations occur at a single amino acid residue of the IDH1 active site, resulting in loss of the enzyme's ability to catalyse conversion of isocitrate to alpha-ketoglutarate. However, only a single copy of the gene is mutated in tumours, raising the possibility that the mutations do not result in a simple loss of function. Here we show that cancer-associated IDH1 mutations result in a new ability of the enzyme to catalyse the NADPH-dependent reduction of alpha-ketoglutarate to R(-)-2-hydroxyglutarate (2HG). Structural studies demonstrate that when arginine 132 is mutated to histidine, residues in the active site are shifted to produce structural changes consistent with reduced oxidative decarboxylation of isocitrate and acquisition of the ability to convert alpha-ketoglutarate to 2HG. Excess accumulation of 2HG has been shown to lead to an elevated risk of malignant brain tumours in patients with inborn errors of 2HG metabolism. Similarly, in human malignant gliomas harbouring IDH1 mutations, we find markedly elevated levels of 2HG. These data demonstrate that the IDH1 mutations result in production of the onco-metabolite 2HG, and indicate that the excess 2HG which accumulates in vivo contributes to the formation and malignant progression of gliomas.
MeSH Terms
Arginine/genetics
Brain Neoplasms/genetics,metabolism,pathology
Catalytic Domain
Cell Line
Crystallography, X-Ray
Disease Progression
Enzyme Assays
Glioma/genetics,metabolism,pathology
Glutarates/metabolism
Histidine/genetics,metabolism
Humans
Isocitrate Dehydrogenase/genetics,metabolism
Ketoglutaric Acids/metabolism
Models, Molecular
Mutant Proteins/genetics,metabolism
Mutation/genetics
Protein Conformation
Chemicals
Glutarates
Ketoglutaric Acids
Mutant Proteins
alpha-hydroxyglutarate
Histidine
Arginine
Isocitrate Dehydrogenase
IDH1 protein, human
Authors & Affiliations
20 authors, click to expand affiliations / ORCID
Dang Lenny
Agios Pharmaceuticals, Cambridge, Massachusetts 02139, USA.
White David W
Gross Stefan
Bennett Bryson D
Bittinger Mark A
Driggers Edward M
Fantin Valeria R
Jang Hyun Gyung
Jin Shengfang
Keenan Marie C
Marks Kevin M
Prins Robert M
Ward Patrick S
Yen Katharine E
Liau Linda M
Rabinowitz Joshua D
Cantley Lewis C
Thompson Craig B
Vander Heiden Matthew G
Su Shinsan M
References (24)
24 references, click to expand
-
A high-performance liquid chromatography-tandem mass spectrometry method for quantitation of nitrogen-containing intracellular metabolites.
J Am Soc Mass Spectrom. 2006 Jan;17(1):37-50
PMID: 16352439
-
The role of oxidative damage in the neuropathology of organic acidurias: insights from animal studies.
J Inherit Metab Dis. 2004;27(4):427-48
PMID: 15303000
-
NMDA receptor activation and respiratory chain complex V inhibition contribute to neurodegeneration in d-2-hydroxyglutaric aciduria.
Eur J Neurosci. 2002 Jul;16(1):21-8
PMID: 12153528
-
Measurement of urinary D- and L-2-hydroxyglutarate enantiomers by stable-isotope-dilution liquid chromatography-tandem mass spectrometry after derivatization with diacetyl-L-tartaric anhydride.
Clin Chem. 2004 Aug;50(8):1391-5
PMID: 15166110
-
An integrated genomic analysis of human glioblastoma multiforme.
Science. 2008 Sep 26;321(5897):1807-12
PMID: 18772396
-
Hydroxyglutaric aciduria and malignant brain tumor: a case report and literature review.
J Neurooncol. 2009 Jan;91(2):233-6
PMID: 18931888
-
A lysine-tyrosine pair carries out acid-base chemistry in the metal ion-dependent pyridine dinucleotide-linked beta-hydroxyacid oxidative decarboxylases.
Biochemistry. 2009 Apr 28;48(16):3565-77
PMID: 19281248
-
IDH1 mutations are early events in the development of astrocytomas and oligodendrogliomas.
Am J Pathol. 2009 Apr;174(4):1149-53
PMID: 19246647
-
Simultaneous determination of multiple intracellular metabolites in glycolysis, pentose phosphate pathway and tricarboxylic acid cycle by liquid chromatography-mass spectrometry.
J Chromatogr A. 2007 Apr 20;1147(2):153-64
PMID: 17376459
-
Metabolic signaling between neurons and glial cells: a short review.
J Physiol Paris. 2002 Apr-Jun;96(3-4):283-8
PMID: 12445907
-
Coot: model-building tools for molecular graphics.
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
PMID: 15572765
-
Recurring mutations found by sequencing an acute myeloid leukemia genome.
N Engl J Med. 2009 Sep 10;361(11):1058-66
PMID: 19657110
-
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. 2009 Oct;118(4):469-74
PMID: 19554337
-
The CCP4 suite: programs for protein crystallography.
Acta Crystallogr D Biol Crystallogr. 1994 Sep 1;50(Pt 5):760-3
PMID: 15299374
-
Processing of X-ray diffraction data collected in oscillation mode.
Methods Enzymol. 1997;276:307-26
PMID: 27754618
-
Analysis of the IDH1 codon 132 mutation in brain tumors.
Acta Neuropathol. 2008 Dec;116(6):597-602
PMID: 18985363
-
Mutations in the D-2-hydroxyglutarate dehydrogenase gene cause D-2-hydroxyglutaric aciduria.
Am J Hum Genet. 2005 Feb;76(2):358-60
PMID: 15609246
-
Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy.
Nat Biotechnol. 2008 Oct;26(10):1179-86
PMID: 18820684
-
Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1alpha.
Science. 2009 Apr 10;324(5924):261-5
PMID: 19359588
-
D-2-hydroxyglutaric acid induces oxidative stress in cerebral cortex of young rats.
Eur J Neurosci. 2003 May;17(10):2017-22
PMID: 12786967
-
Structures of human cytosolic NADP-dependent isocitrate dehydrogenase reveal a novel self-regulatory mechanism of activity.
J Biol Chem. 2004 Aug 6;279(32):33946-57
PMID: 15173171
-
IDH1 mutations at residue p.R132 (IDH1(R132)) occur frequently in high-grade gliomas but not in other solid tumors.
Hum Mutat. 2009 Jan;30(1):7-11
PMID: 19117336
-
White matter disease in cerebral organic acid disorders: clinical implications and suggested pathomechanisms.
Neuropediatrics. 2002 Oct;33(5):225-31
PMID: 12536363
-
IDH1 and IDH2 mutations in gliomas.
N Engl J Med. 2009 Feb 19;360(8):765-73
PMID: 19228619