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PMID: 22238333 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Magnetic resonance of 2-hydroxyglutarate in IDH1-mutated low-grade gliomas.

Science translational medicine ·Vol. 4 ·No. 116 ·2012-01-11 ·Pages 116ra5

Elkhaled A, Jalbert LE, Phillips JJ, Yoshihara HAI, Parvataneni R, Srinivasan R, Bourne G, Berger MS, Chang SM, Cha S, Nelson SJ

Abstract

Recent studies have indicated that a significant survival advantage is conferred to patients with gliomas whose lesions harbor mutations in the genes isocitrate dehydrogenase 1 and 2 (IDH1/2). IDH1/2 mutations result in aberrant enzymatic production of the potential oncometabolite D-2-hydroxyglutarate (2HG). Here, we report on the ex vivo detection of 2HG in IDH1-mutated tissue samples from patients with recurrent low-grade gliomas using the nuclear magnetic resonance technique of proton high-resolution magic angle spinning spectroscopy. Relative 2HG levels from pathologically confirmed mutant IDH1 tissues correlated with levels of other ex vivo metabolites and histopathology parameters associated with increases in mitotic activity, relative tumor content, and cellularity. Ex vivo spectroscopic measurements of choline-containing species and in vivo magnetic resonance measurements of diffusion parameters were also correlated with 2HG levels. These data provide extensive characterization of mutant IDH1 lesions while confirming the potential diagnostic value of 2HG as a surrogate marker of patient survival. Such information may augment the ability of clinicians to monitor therapeutic response and provide criteria for stratifying patients to specific treatment regimens.

MeSH Terms
Amino Acid Sequence Base Sequence Brain Neoplasms/enzymology,genetics,metabolism,surgery DNA Mutational Analysis Glioma/enzymology,genetics,metabolism,surgery Glutarates/metabolism Humans Immunohistochemistry Isocitrate Dehydrogenase/chemistry,genetics Magnetic Resonance Spectroscopy/methods Molecular Sequence Data Mutation/genetics Neoplasm Grading Phantoms, Imaging World Health Organization
Chemicals
Glutarates alpha-hydroxyglutarate Isocitrate Dehydrogenase IDH1 protein, human
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Elkhaled Adam
Department of Radiology and Biomedical Imaging, University of California, San Francisco, San Francisco, CA 94158, USA.
Jalbert Llewellyn E
Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Phillips Joanna J
Department of Pathology, University of California, San Francisco, San Francisco, CA 94158, USA. | Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA 94158, USA.
Yoshihara Hikari A I
Department of Radiology and Biomedical Imaging, University of California, San Francisco, San Francisco, CA 94158, USA.
Parvataneni Rupa
Department of Radiology and Biomedical Imaging, University of California, San Francisco, San Francisco, CA 94158, USA. | Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA 94158, USA.
Srinivasan Radhika
Department of Radiology and Biomedical Imaging, University of California, San Francisco, San Francisco, CA 94158, USA.
Bourne Gabriela
Department of Radiology and Biomedical Imaging, University of California, San Francisco, San Francisco, CA 94158, USA.
Berger Mitchel S
Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA 94158, USA.
Chang Susan M
Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA 94158, USA.
Cha Soonmee
Department of Radiology and Biomedical Imaging, University of California, San Francisco, San Francisco, CA 94158, USA.
Nelson Sarah J
Department of Radiology and Biomedical Imaging, University of California, San Francisco, San Francisco, CA 94158, USA. | Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
References (28)
28 references, click to expand
  1. Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrial NADP+-dependent isocitrate dehydrogenase.
    J Biol Chem. 2001 May 11;276(19):16168-76 PMID: 11278619
  2. Proton NMR chemical shifts and coupling constants for brain metabolites.
    NMR Biomed. 2000 May;13(3):129-53 PMID: 10861994
  3. Molecular neuropathology of low-grade gliomas and its clinical impact.
    Adv Tech Stand Neurosurg. 2010;35:35-64 PMID: 20102110
  4. Detection of 2-hydroxyglutarate in IDH-mutated glioma patients by in vivo spectral-editing and 2D correlation magnetic resonance spectroscopy.
    Sci Transl Med. 2012 Jan 11;4(116):116ra4 PMID: 22238332
  5. An integrated genomic analysis of human glioblastoma multiforme.
    Science. 2008 Sep 26;321(5897):1807-12 PMID: 18772396
  6. Semi-parametric time-domain quantification of HR-MAS data from prostate tissue.
    NMR Biomed. 2010 Dec;23(10):1146-57 PMID: 20842756
  7. IDH1 or IDH2 mutations predict longer survival and response to temozolomide in low-grade gliomas.
    Neurology. 2010 Oct 26;75(17):1560-6 PMID: 20975057
  8. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate.
    Nature. 2009 Dec 10;462(7274):739-44 PMID: 19935646
  9. Cytosolic NADP(+)-dependent isocitrate dehydrogenase status modulates oxidative damage to cells.
    Free Radic Biol Med. 2002 Jun 1;32(11):1185-96 PMID: 12031902
  10. Isocitrate dehydrogenase 1 and 2 mutations in cancer: alterations at a crossroads of cellular metabolism.
    J Natl Cancer Inst. 2010 Jul 7;102(13):932-41 PMID: 20513808
  11. Cytosolic NADP+-dependent isocitrate dehydrogenase plays a key role in lipid metabolism.
    J Biol Chem. 2004 Sep 17;279(38):39968-74 PMID: 15254034
  12. Low-grade gliomas in adults.
    Oncologist. 2006 Jun;11(6):681-93 PMID: 16794247
  13. 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. 2010 Dec;120(6):707-18 PMID: 21088844
  14. Ex vivo MR spectroscopic measure differentiates tumor from treatment effects in GBM.
    Neuro Oncol. 2010 Nov;12(11):1152-61 PMID: 20647244
  15. IDH1 and IDH2 mutations are frequent genetic alterations in acute myeloid leukemia and confer adverse prognosis in cytogenetically normal acute myeloid leukemia with NPM1 mutation without FLT3 internal tandem duplication.
    J Clin Oncol. 2010 Aug 1;28(22):3636-43 PMID: 20567020
  16. Cancer-associated IDH mutations: biomarker and therapeutic opportunities.
    Oncogene. 2010 Dec 9;29(49):6409-17 PMID: 20972461
  17. IDH1 and IDH2 mutations in gliomas.
    N Engl J Med. 2009 Feb 19;360(8):765-73 PMID: 19228619
  18. Quantification of choline- and ethanolamine-containing metabolites in human prostate tissues using 1H HR-MAS total correlation spectroscopy.
    Magn Reson Med. 2008 Jul;60(1):33-40 PMID: 18581409
  19. Implementation of 3 T lactate-edited 3D 1H MR spectroscopic imaging with flyback echo-planar readout for gliomas patients.
    Ann Biomed Eng. 2011 Jan;39(1):193-204 PMID: 20652745
  20. Evaluation of the ERETIC method as an improved quantitative reference for 1H HR-MAS spectroscopy of prostate tissue.
    Magn Reson Med. 2009 Mar;61(3):525-32 PMID: 19235261
  21. The oncometabolite 2-hydroxyglutarate inhibits histone lysine demethylases.
    EMBO Rep. 2011 May;12(5):463-9 PMID: 21460794
  22. Monoclonal antibody specific for IDH1 R132H mutation.
    Acta Neuropathol. 2009 Nov;118(5):599-601 PMID: 19798509
  23. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI.
    J Magn Reson B. 1996 Jun;111(3):209-19 PMID: 8661285
  24. Hydroxyglutaric aciduria and malignant brain tumor: a case report and literature review.
    J Neurooncol. 2009 Jan;91(2):233-6 PMID: 18931888
  25. An automated technique for the quantitative assessment of 3D-MRSI data from patients with glioma.
    J Magn Reson Imaging. 2001 Feb;13(2):167-77 PMID: 11169821
  26. Assessment of therapeutic response and treatment planning for brain tumors using metabolic and physiological MRI.
    NMR Biomed. 2011 Jul;24(6):734-49 PMID: 21538632
  27. Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1alpha.
    Science. 2009 Apr 10;324(5924):261-5 PMID: 19359588
  28. A comparison of statistical methods for clustered data analysis with Gaussian error.
    Stat Med. 1996 Aug 30;15(16):1793-806 PMID: 8870161
Article Info
Journal
Science translational medicine
Abbr.
Sci Transl Med
ISSN
1946-6242
Published
2012-01-11
Pages
116ra5
Language
English
Region
United States
NLM ID
101505086
PMCID
PMC3772177
Subset
IM
Grants
NINDS NIH HHS · K08 NS063456 · United States
NCI NIH HHS · P50 CA097257 · United States
NIGMS NIH HHS · T32 GM008155 · United States
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