IDH1 R132H mutation generates a distinct phospholipid metabolite profile in glioma

Cancer Research

Volumn 74, Issue 17, 2014, Pages 4898-4907

  Esmaeili, Morteza ^a   Hamans, Bob C ^b   Navis, Anna C ^b   Van Horssen, Remco ^c,d   Bathen, Tone F ^a   Gribbestad, Ingrid S ^a   Leenders, William P ^b   Heerschap, Arend ^a,b  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d CPRLab   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ETHANOLAMINE DERIVATIVE; IDH1 PROTEIN, HUMAN; ISOCITRATE DEHYDROGENASE; PHOSPHOETHANOLAMINE; PHOSPHOLIPID; TUMOR MARKER;

ANIMAL; BAGG ALBINO MOUSE; FEMALE; GENETICS; GLIOMA; HUMAN; METABOLISM; MOUSE; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUDE MOUSE; PROCEDURES; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; ETHANOLAMINES; FEMALE; GLIOMA; HUMANS; ISOCITRATE DEHYDROGENASE; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, INBRED BALB C; MICE, NUDE; MUTATION; PHOSPHOLIPIDS; TUMOR MARKERS, BIOLOGICAL;

EID: 84907051444     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0008     Document Type: Article

References (60)

1. Clarke J, Butowski N, Chang S. Recent advances in therapy for glioblastoma. Arch Neurol 2010;67:279-83.
2. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007;114:97-109.
3. Stupp R, Hegi ME, Gilbert MR, Chakravarti A. Chemoradiotherapy in malignant glioma: standard of care and future directions. J Clin Oncol 2007;25:4127-36.
4. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008;321:1807-12.
5. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med 2009;360:765-73.
6. Hartmann C, Meyer J, Balss J, Capper D, Mueller W, Christians A, 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 2009;118:469-74.
7. Houillier C, Wang X, Kaloshi G, Mokhtari K, Guillevin R, Laffaire J, et al. IDH1 or IDH2 mutations predict longer survival and response to temozolomide in low-grade gliomas. Neurology 2010;75:1560-6.
8. Metellus P, Coulibaly B, Colin C, de Paula AM, Vasiljevic A, Taieb D, et al. Absence of IDH mutation identifies a novel radiologic and molecular subtype of WHO grade II gliomas with dismal prognosis. Acta Neuropathol 2010;120:719-29.
9. Metallo CM, Gameiro PA, Bell EL, Mattaini KR, Yang J, Hiller K, et al. Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature 2012;481:380-4.
10. Dang L, White DW, Gross S, Bennett BD, Bittinger MA, Driggers EM, et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 2009;462:739-44.
11. Leonardi R, Subramanian C, Jackowski S, Rock CO. Cancer-associated isocitrate dehydrogenase mutations inactivate NADPH-dependent reductive carboxylation. J Biol Chem 2012;287:14615-20.
12. Dang L, Jin S, Su SM. IDH mutations in glioma and acute myeloid leukemia. Trends Mol Med 2010;16:387-97.
13. Yen KE, Bittinger MA, Su SM, Fantin VR. Cancer-associated IDH mutations: biomarker and therapeutic opportunities. Oncogene 2010; 29:6409-17.
14. Reitman ZJ, Jin G, Karoly ED, Spasojevic I, Yang J, Kinzler KW, et al. Profiling the effects of isocitrate dehydrogenase 1 and 2 mutations on the cellular metabolome. Proc Natl Acad Sci U S A 2011;108:3270-5.
15. Choi C, Ganji SK, DeBerardinis RJ, Hatanpaa KJ, Rakheja D, Kovacs Z, et al. 2-hydroxyglutarate detection by magnetic resonance spectroscopy in IDH-mutated patients with gliomas. Nat Med 2012;18:624-9.
16. Pope WB, Prins RM, Albert Thomas M, Nagarajan R, Yen KE, Bittinger MA, et al. Non-invasive detection of 2-hydroxyglutarate and other metabolites in IDH1 mutant glioma patients using magnetic resonance spectroscopy. J Neurooncol 2012;107:197-205.
17. Andronesi OC, Kim GS, Gerstner E, Batchelor T, Tzika AA, Fantin VR, et al. Detection of 2-hydroxyglutarate in IDH-mutated glioma patients by in vivo spectral-editing and 2D correlation magnetic resonance spectroscopy. Sci Transl Med 2012;4:116ra4.
18. Elkhaled A, Jalbert LE, Phillips JJ, Yoshihara HA, Parvataneni R, Srinivasan R, et al. Magnetic resonance of 2-hydroxyglutarate in IDH1-mutated low-grade gliomas. Sci Transl Med 2012;4:116ra5.
19. Esmaeili M, Vettukattil R, Bathen TF. 2-hydroxyglutarate as a magnetic resonance biomarker for glioma subtyping. Transl Oncol 2013;6:92-8.
20. Gillies RJ, Morse DL. In vivo magnetic resonance spectroscopy in cancer. Annu Rev Biomed Eng 2005;7:287-326.
21. Nelson SJ. Assessment of therapeutic response and treatment planning for brain tumors using metabolic and physiological MRI. NMR Biomed 2011;24:734-49.
22. Aboagye EO, Bhujwalla ZM. Malignant transformation alters membrane choline phospholipid metabolism of human mammary epithelial cells. Cancer Res 1999;59:80-4.
23. Gillies RJ, Raghunand N, Karczmar GS, Bhujwalla ZM. MRI of the tumor microenvironment. J Magn Reson Imaging 2002;16: 430-50.
24. Glunde K, Bhujwalla ZM, Ronen SM. Choline metabolism in malignant transformation. Nat Rev Cancer 2011;11:835-48.
25. Bruhn H, Frahm J, Gyngell ML, Merboldt KD, Hanicke W, Sauter R, et al.Noninvasive differentiation of tumors with use of localizedH-1MR spectroscopy in vivo: initial experience in patients with cerebral tumors. Radiology 1989;172:541-8.
26. Herminghaus S, Pilatus U, Moller-Hartmann W, Raab P, Lanfermann H, Schlote W, et al. Increased choline levels coincide with enhanced proliferative activity of human neuroepithelial brain tumors. NMR Biomed 2002;15:385-92.
27. Stadlbauer A, Gruber S, Nimsky C, Fahlbusch R, Hammen T, Buslei R, et al. Preoperative grading of gliomas by using metabolite quantification with high-spatial-resolution proton MR spectroscopic imaging. Radiology 2006;238:958-69.
28. Saraswathy S, Crawford FW, Lamborn KR, Pirzkall A, Chang S, Cha S, et al. Evaluation of MR markers that predict survival in patients with newly diagnosed GBM prior to adjuvant therapy. J Neurooncol 2009; 91:69-81.
29. Gupta RK, Cloughesy TF, Sinha U, Garakian J, Lazareff J, Rubino G, et al. Relationships between choline magnetic resonance spectroscopy, apparent diffusion coefficient and quantitative histopathology in human glioma. J Neurooncol 2000;50:215-26.
30. Srinivasan R, Phillips JJ, Vandenberg SR, Polley MY, Bourne G, Au A, et al. Ex vivo MR spectroscopic measure differentiates tumor from treatment effects in GBM. Neuro Oncol 2010;12:1152-61.
31. Sabatier J, Gilard V, Malet-Martino M, Ranjeva JP, Terral C, Breil S, et al. Characterization of choline compounds with in vitro 1H magnetic resonance spectroscopy for the discrimination of primary brain tumors. Invest Radiol 1999;34:230-5.
32. Righi V, Roda JM, Paz J, Mucci A, Tugnoli V, Rodriguez-Tarduchy G, et al. 1H HR-MAS and genomic analysis of human tumor biopsies discriminate between high and low grade astrocytomas. NMR Biomed 2009;22:629-37.
33. McKnight TR, Smith KJ, Chu PW, Chiu KS, Cloyd CP, Chang SM, et al. Choline metabolism, proliferation, and angiogenesis in nonenhancing grades 2 and 3 astrocytoma. J Magn Reson Imaging 2011;33:808-16.
34. Vettukattil R, Gulati M, Sjobakk TE, Jakola AS, Kvernmo NA, Torp SH, et al. Differentiating diffuse World Health Organization Grade II and IV astrocytomas with ex vivo magnetic resonance spectroscopy. Neurosurgery 2013;72:186-95.
35. Luyten PR, Bruntink G, Sloff FM, Vermeulen JW, van der Heijden JI, den Hollander JA, et al. Broadband proton decoupling in human 31P NMR spectroscopy. NMR Biomed 1989;1:177-83.
36. Albers MJ, Krieger MD, Gonzalez-Gomez I, Gilles FH, McComb JG, NelsonMDJr, et al. Proton-decoupled 31P MRS in untreated pediatric brain tumors. Magn Reson Med 2005;53:22-9.
37. Hattingen E, Bahr O, Rieger J, Blasel S, Steinbach J, Pilatus U. Phospholipid metabolites in recurrent glioblastoma: in vivo markers detect different tumor phenotypes before and under antiangiogenic therapy. PLoS ONE 2013;8:e56439.
38. Shechter I, Dai P, Huo L, Guan G. IDH1 gene transcription is sterol regulated and activated by SREBP-1a and SREBP-2 in human hepatoma HepG2 cells: evidence that IDH1 may regulate lipogenesis in hepatic cells. J Lipid Res 2003;44:2169-80.
39. Yang H, Ye D, Guan KL, Xiong Y. IDH1 and IDH2 mutations in tumorigenesis: mechanistic insights and clinical perspectives. Clin Cancer Res 2012;18:5562-71.
40. Claes A, Schuuring J, Boots-Sprenger S, Hendriks-Cornelissen S, Dekkers M, van der Kogel AJ, et al. Phenotypic and genotypic characterization of orthotopic human glioma models and its relevance for the study of anti-glioma therapy. Brain Pathol 2008; 18:423-33.
41. Navis AC, Niclou SP, Fack F, Stieber D, Lith Sv, Verrijp K, et al. Increased mitochondrial activity in a novel IDH1-R132H mutant human oligodendroglioma xenograft model: in situ detection of 2-HG and a-KG. Acta Neuropathol Commun 2013;1:18.
42. Capper D, Zentgraf H, Balss J, Hartmann C, von Deimling A. Monoclonal antibody specific for IDH1 R132H mutation. Acta Neuropathol 2009;118:599-601.
43. Gruetter R. Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn Reson Med 1993;29:804-11.
44. Staewen RS, Johnson AJ, Ross BD, Parrish T, Merkle H, Garwood M. 3-D FLASH imaging using a single surface coil and a new adiabatic pulse, BIR-4. Invest Radiol 1990;25:559-67.
45. Naressi A, Couturier C, Devos JM, Janssen M, Mangeat C, de Beer R, et al. Java-based graphical user interface for the MRUI quantitation package. MAGMA 2001;12:141-52.
46. Vanhamme L, van den Boogaart A, Van Huffel S. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson 1997;129:35-43.
47. Gribbestad IS, Petersen SB, Fjosne HE, Kvinnsland S, Krane J. 1H NMR spectroscopic characterization of perchloric acid extracts from breast carcinomas and non-involved breast tissue. NMR Biomed 1994;7:181-94.
48. Esteve V, Celda B, Martinez-Bisbal MC. Use of 1H and 31P HRMAS to evaluate the relationship between quantitative alterations in metabolite concentrations and tissue features in human brain tumour biopsies. Anal Bioanal Chem 2012;403:2611-25.
49. Ward CS, Venkatesh HS, Chaumeil MM, Brandes AH, Vancriekinge M, Dafni H, et al. Noninvasive detection of target modulation following phosphatidylinositol 3-kinase inhibition using hyperpolarized 13C magnetic resonance spectroscopy. Cancer Res 2010;70:1296-305.
50. Hubesch B, Sappey-Marinier D, Roth K, Meyerhoff DJ, Matson GB, Weiner MW. P-31 MR spectroscopy of normal human brain and brain tumors. Radiology 1990;174:401-9.
51. Bleeker FE, Atai NA, Lamba S, Jonker A, Rijkeboer D, Bosch KS, et al. The prognostic IDH1(R132) mutation is associated with reduced NADP+-dependent IDH activity in glioblastoma. Acta Neuropathol 2010;119:487-94.
52. Luchman HA, Stechishin OD, Dang NH, Blough MD, Chesnelong C, Kelly JJ, et al. An in vivo patient-derived model of endogenous IDH1- mutant glioma. Neuro Oncol 2012;14:184-91.
53. Klink B, Miletic H, Stieber D, Huszthy PC, Valenzuela JA, Balss J, et al. A novel, diffusely infiltrative xenograft model of human anaplastic oligodendroglioma with mutations in FUBP1, CIC, and IDH1. PLoS ONE 2013;8:e59773.
54. Piaskowski S, Bienkowski M, Stoczynska-Fidelus E, Stawski R, Sieruta M, Szybka M, et al. Glioma cells showing IDH1 mutation cannot be propagated in standard cell culture conditions. Br J Cancer 2011;104: 968-70.
55. Klomp DW, Wijnen JP, Scheenen TW, Heerschap A. Efficient 1H to 31P polarization transfer on a clinical 3T MR system. Magn Reson Med 2008;60:1298-305.
56. Wijnen JP, Scheenen TW, Klomp DW, Heerschap A. 31P magnetic resonance spectroscopic imaging with polarisation transfer of phosphomono- and diesters at 3 T in the human brain: relation with age and spatial differences. NMR Biomed 2010;23:968-76.
57. Rohle D, Popovici-Muller J,Palaskas N, Turcan S, Grommes C,Campos C, et al. An inhibitor of mutant IDH1 delays growth and promotes differentiation of glioma cells. Science 2013;340:626-30.
58. van Lith SA, Navis AC, Verrijp K, Niclou SP, Bjerkvig R, Wesseling P, et al. Glutamate as chemotactic fuel for diffuse glioma cells; are they glutamate suckers? Biochim Biophys Acta 2014;1846: 66-74.
59. Farber SA, Slack BE, Blusztajn JK. Acceleration of phosphatidylcholine synthesis and breakdown by inhibitors of mitochondrial function in neuronal cells: a model of the membrane defect of Alzheimer's disease. FASEB J 2000;14:2198-206.
60. Warburg O. On the origin of cancer cells. Science 1956;123: 309-14.