Analysis of isocitrate dehydrogenase-1/2 gene mutations in gliomas

Chinese Medical Journal

Volumn 123, Issue 24, 2010, Pages 3697-3705

  Yu, Lei ^a   Qi, Song Tao ^a   Li, Zhi Yong ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

ketoglutarate; 2 hydroxyglutarate; Glioma; Hypoxia inducible factor; Isocitrate dehydrogenase 1 mutation

Indexed keywords

2 HYDROXYGLUTARIC ACID; 2 OXOGLUTARIC ACID; HYPOXIA INDUCIBLE FACTOR; ISOCITRATE DEHYDROGENASE; ISOCITRATE DEHYDROGENASE 1; ISOCITRATE DEHYDROGENASE ISOENZYME; NITROSOUREA DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TEMOZOLOMIDE; UNCLASSIFIED DRUG;

AGE; AMINO ACID SUBSTITUTION; DIAGNOSTIC VALUE; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GLIOBLASTOMA; GLIOMA; HUMAN; MUTATIONAL ANALYSIS; NEUROPATHOLOGY; PROGNOSIS; REVIEW; SOMATIC MUTATION;

ADULT; AGE FACTORS; BRAIN NEOPLASMS; GENES, P53; GLIOMA; GLUTARATES; HUMANS; ISOCITRATE DEHYDROGENASE; KETOGLUTARIC ACIDS; MIDDLE AGED; MUTATION; NADP; NEOPLASM GRADING; PROGNOSIS;

EID: 78650606956     PISSN: 03666999     EISSN: None     Source Type: Journal    
DOI: 10.3760/cma.j.issn.0366-6999.2010.24.033     Document Type: Review

References (89)

1. 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.
2. Ohgaki H. Epidemiology of brain tumors. Methods Mol Biol 2009; 472: 323-342.
3. Zhu YJ, Zhu XD, Wang SH, Shen F, Shen H, Liu WG. A multivariate analysis of the prognostic factors of grade III gliomas. Chin Med J 2008; 121: 1072-1075.
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: 1807-1812.
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: 765-773.
6. Xu X, Zhao J, Xu Z, Peng B, Huang Q, Arnold E, et al. Structures of human cytosolic NADP-dependent isocitrate dehydrogenase reveal a novel self-regulatory mechanism of activity. J Biol Chem 2004; 279: 33946-33957.
7. Zhao S, Lin Y, Xu W, Jiang W, Zha Z, Wang P, et al. Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1alpha. Science 2009; 324: 261-265.
8. Minard KI, McAlister-Henn L. Dependence of peroxisomal beta-oxidation on cytosolic sources of NADPH. J Biol Chem 1999; 274: 3402-3406.
9. 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: 2169-2180.
10. Ronnebaum SM, Ilkayeva O, Burgess SC, Joseph JW, Lu D, Stevens RD, et al. A pyruvate cycling pathway involving cytosolic NADP-dependent isocitrate dehydrogenase regulates glucose-stimulated insulin secretion. J Biol Chem 2006; 281: 30593-30602.
11. Mailloux RJ, Beriault R, Lemire J, Singh R, Chenier DR, Hamel RD, et al. The tricarboxylic acid cycle, an ancient metabolic network with a novel twist. PLoS One 2007; 2: e690.
12. Nakamura H. Thioredoxin and its related molecules: update 2005. Antioxid Redox Signal 2005; 7: 823-828.
13. Lee SM, Koh HJ, Park DC, Song BJ, Huh TL, Park JW. Cytosolic NADP(+)-dependent isocitrate dehydrogenase status modulates oxidative damage to cells. Free Radic Biol Med 2002; 32: 1185-1196.
14. Balss J, Meyer J, Mueller W, Korshunov A, Hartmann C, von Deimling A. Analysis of the IDH1 codon 132 mutation in brain tumors. Acta Neuropathol 2008; 116: 597-602.
15. Horbinski C, Kofler J, Kelly LM, Murdoch GH, Nikiforova MN. Diagnostic use of IDH1/2 mutation analysis in routine clinical testing of formalin-fixed, paraffin-embedded glioma tissues. J Neuropathol Exp Neurol 2009; 68: 1319-1325.
16. Sanson M, Marie Y, Paris S, Idbaih A, Laffaire J, Ducray F, et al. Isocitrate dehydrogenase 1 codon 132 mutation is an important prognostic biomarker in gliomas. J Clin Oncol 2009; 27: 4150-4154.
17. 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 1010 diffuse gliomas. Acta Neuropathol 2009; 118: 469-474.
18. Ichimura K, Pearson DM, Kocialkowski S, Backlund LM, Chan R, Jones DT, et al. IDH1 mutations are present in the majority of common adult gliomas but rare in primary glioblastomas. Neuro Oncol 2009; 11: 341-347.
19. Watanabe T, Nobusawa S, Kleihues P, Ohgaki H. IDH1 mutations are early events in the development of astrocytomas and oligodendrogliomas. Am J Pathol 2009; 174: 1149-1153.
20. Bleeker FE, Lamba S, Leenstra S, Troost D, Hulsebos T, Vandertop WP, et al. IDH1 mutations at residue p.R132 (IDH1(R132)) occur frequently in high-grade gliomas but not in other solid tumors. Hum Mutat 2009; 30: 7-11.
21. Hayden JT, Fruhwald MC, Hasselblatt M, Ellison DW, Bailey S, Clifford SC. Frequent IDH1 mutations in supratentorial primitive neuroectodermal tumors (sPNET) of adults but not children. Cell Cycle 2009; 8: 1806-1807.
22. Seiz M, Tuettenberg J, Meyer J, Essig M, Schmieder K, Mawrin C, et al. Detection of IDH1 mutations in gliomatosis cerebri, but only in tumors with additional solid component: evidence for molecular subtypes. Acta Neuropathol 2010; 120: 261-267.
23. Mardis ER, Ding L, Dooling DJ, Larson DE, McLellan MD, Chen K, et al. Recurring mutations found by sequencing an acute myeloid leukemia genome. N Engl J Med 2009; 361: 1058-1066.
24. Ward PS, Patel J, Wise DR, Abdel-Wahab O, Bennett BD, Coller HA, et al. The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Cancer Cell 2010; 17: 225-234.
25. Kang MR, Kim MS, Oh JE, Kim YR, Song SY, Seo SI, et al. Mutational analysis of IDH1 codon 132 in glioblastomas and other common cancers. Int J Cancer 2009; 125: 353-355.
26. Sjoblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, et al. The consensus coding sequences of human breast and colorectal cancers. Science 2006; 314: 268-274.
27. Park SW, Chung NG, Han JY, Eom HS, Lee JY, Yoo NJ, et al. Absence of IDH2 codon 172 mutation in common human cancers. Int J Cancer 2009; 125: 2485-2486.
28. Green A, Beer P. Somatic mutations of IDH1 and IDH2 in the leukemic transformation of myeloproliferative neoplasms. N Engl J Med 2010; 362: 369-370.
29. Murugan AK, Bojdani E, Xing M. Identification and functional characterization of isocitrate dehydrogenase 1 (IDH1) mutations in thyroid cancer. Biochem Biophys Res Commun 2010; 393: 555-559.
30. Holdhoff M, Parsons DW, Jr Diaz LA. Mutations of IDH1 and IDH2 are not detected in brain metastases of colorectal cancer. J Neurooncol 2009; 94: 297.
31. Lopez GY, Reitman ZJ, Solomon D, Waldman T, Bigner DD, McLendon RE, et al. IDH1(R132) mutation identified in one human melanoma metastasis, but not correlated with metastases to the brain. Biochem Biophys Res Commun 2010; 398: 585-587.
32. Nobusawa S, Watanabe T, Kleihues P, Ohgaki H. IDH1 mutations as molecular signature and predictive factor of secondary glioblastomas. Clin Cancer Res 2009; 15: 6002-6007.
33. Labussiere M, Idbaih A, Wang XW, Marie Y, Boisselier B, Falet C, et al. All the 1p19q codeleted gliomas are mutated on IDH1 or IDH2. Neurology 2010; 74: 1886-1890.
34. Levine AJ. P53, the cellular gatekeeper for growth and division. Cell 1997; 88: 323-331.
35. Ohgaki H, Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am J Pathol 2007; 170: 1445-1453.
36. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 2007; 21: 2683-2710.
37. Weber R G, Sabel M, Reifenberger J, Sommer C, Oberstrass J, Reifenberger G, et al. Characterization of genomic alterations associated with glioma progression by comparative genomic hybridization. Oncogene 1996; 13: 983-994.
38. Korshunov A, Meyer J, Capper D, Christians A, Remke M, Witt H, et al. Combined molecular analysis of BRAF and IDH1 distinguishes pilocytic astrocytoma from diffuse astrocytoma. Acta Neuropathol 2009; 118: 401-405.
39. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005; 352: 997-1003.
40. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009; 10: 459-466.
41. Ducray F, El HS, Idbaih A. Diagnostic and prognostic markers in gliomas. Curr Opin Oncol 2009; 21: 537-542.
42. McDonald KL, McDonnell J, Muntoni A, Henson JD, Hegi ME, von Deimling A, et al. Presence of alternative lengthening of telomeres mechanism in patients with glioblastoma identifies a less aggressive tumor type with longer survival. J Neuropathol Exp Neurol 2010; 69: 729-736.
43. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 2010; 17: 510-522.
44. Watanabe T, Vital A, Nobusawa S, Kleihues P, Ohgaki H. Selective acquisition of IDH1 R132C mutations in astrocytomas associated with Li-Fraumeni syndrome. Acta Neuropathol 2009; 117: 653-656.
45. De Carli E, Wang X, Puget S. IDH1 and IDH2 mutations in gliomas. N Engl J Med 2009; 360: 2248-2249.
46. Pollack IF, Hamilton RL, Sobol RW, Nikiforova MN, Lyons-Weiler MA, Laframboise WA, et al. IDH1 mutations are common in malignant gliomas arising in adolescents: a report from the Children's Oncology Group. Childs Nerv Syst 2010; Epub ahead of print.
47. Cairncross G, Berkey B, Shaw E, Jenkins R, Scheithauer B, Brachman D, et al. Phase III trial of chemotherapy plus radiotherapy compared with radiotherapy alone for pure and mixed anaplastic oligodendroglioma: Intergroup Radiation Therapy Oncology Group Trial 9402. J Clin Oncol 2006; 24: 2707-2714.
48. van den Bent MJ, Carpentier AF, Brandes AA, Sanson M, Taphoorn MJ, Bernsen HJ, et al. Adjuvant procarbazine, lomustine, and vincristine improves progression-free survival but not overall survival in newly diagnosed anaplastic oligodendrogliomas and oligoastrocytomas: a randomized European Organisation for Research and Treatment of Cancer phase III trial. J Clin Oncol 2006; 24: 2715-2722.
49. Wick W, Hartmann C, Engel C, Stoffels M, Felsberg J, Stockhammer F, et al. NOA-04 randomized phase III trial of sequential radiochemotherapy of anaplastic glioma with procarbazine, lomustine, and vincristine or temozolomide. J Clin Oncol 2009; 27: 5874-5880.
50. Felsberg J, Erkwoh A, Sabel MC, Kirsch L, Fimmers R, Blaschke B, et al. Oligodendroglial tumors: refinement of candidate regions on chromosome arm 1p and correlation of 1p/19q status with survival. Brain Pathol 2004; 14: 121-130.
51. Esteller M, Garcia-Foncillas J, Andion E, Goodman SN, Hidalgo OF, Vanaclocha V, et al. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med 2000; 343: 1350-1354.
52. Herrlinger U, Rieger J, Koch D, Loeser S, Blaschke B, Kortmann RD, et al. Phase II trial of lomustine plus temozolomide chemotherapy in addition to radiotherapy in newly diagnosed glioblastoma: UKT-03. J Clin Oncol 2006; 24: 4412-4417.
53. Glas M, Happold C, Rieger J, Wiewrodt D, Bahr O, Steinbach J P, et al. Long-term survival of patients with glioblastoma treated with radiotherapy and lomustine plus temozolomide. J Clin Oncol 2009; 27: 1257-1261.
54. Bujko M, Kober P, Matyja E, Nauman P, Dyttus-Cebulok K, Czeremszynska B, et al. Prognostic value of IDH1 mutations identified with PCR-RFLP assay in glioblastoma patients. Mol Diagn Ther 2010; 14: 163-169.
55. Weller M, Felsberg J, Hartmann C, Berger H, Steinbach J P, Schramm J, et al. Molecular predictors of progression-free and overall survival in patients with newly diagnosed glioblastoma: a prospective translational study of the German Glioma Network. J Clin Oncol 2009; 27: 5743-5750.
56. Toedt G, Barbus S, Wolter M, Felsberg J, Tews B, Blond F, et al. Molecular signatures classify astrocytic gliomas by IDH1 mutation status. Int J Cancer 2010; Epub ahead of print.
57. Dang L, White DW, Gross S, Bennett BD, Bittinger MA, Driggers EM, et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 2009; 462: 739-744.
58. Gross S, Cairns RA, Minden MD, Driggers EM, Bittinger MA, Jang H G, et al. Cancer-associated metabolite 2-hydroxyglutarate accumulates in acute myelogenous leukemia with isocitrate dehydrogenase 1 and 2 mutations. J Exp Med 2010; 207: 339-344.
59. Garber K. Oncometabolite? IDH1 discoveries raise possibility of new metabolism targets in brain cancers and leukemia. J Natl Cancer Inst 2010; 102: 926-928.
60. Kil IS, Kim S Y, Lee SJ, Park JW. Small interfering RNA-mediated silencing of mitochondrial NADP+-dependent isocitrate dehydrogenase enhances the sensitivity of HeLa cells toward tumor necrosis factor-alpha and anticancer drugs. Free Radic Biol Med 2007; 43: 1197-1207.
61. Lee JK, Edderkaoui M, Truong P, Ohno I, Jang KT, Berti A, et al. NADPH oxidase promotes pancreatic cancer cell survival via inhibiting JAK2 dephosphorylation by tyrosine phosphatases. Gastroenterology 2007; 133: 1637-1648.
62. Kil IS, Huh TL, Lee YS, Lee YM, Park JW. Regulation of replicative senescence by NADP+-dependent isocitrate dehydrogenase. Free Radic Biol Med 2006; 40: 110-119.
63. 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: 487-494.
64. Thompson CB. Metabolic enzymes as oncogenes or tumor suppressors. N Engl J Med 2009; 360: 813-815.
65. Struys EA. D-2-Hydroxyglutaric aciduria: unravelling the biochemical pathway and the genetic defect. J Inherit Metab Dis 2006; 29: 21-29.
66. Brehmer S, Pusch S, Schmieder K, von Deimling A, Hartmann C. Mutational analysis of D2HGDH and L2HGDH in brain tumours without IDH1 or IDH2 mutations. Neuropathol Appl Neurobiol 2010; Epub ahead of print.
67. Aghili M, Zahedi F, Rafiee E. Hydroxyglutaric aciduria and malignant brain tumor: a case report and literature review. J Neurooncol 2009; 91: 233-236.
68. Kolker S, Pawlak V, Ahlemeyer B, Okun JG, Horster F, Mayatepek E, et al. NMDA receptor activation and respiratory chain complex V inhibition contribute to neurodegeneration in d-2-hydroxyglutaric aciduria. Eur J Neurosci 2002; 16: 21-28.
69. Latini A, Scussiato K, Rosa RB, Llesuy S, Bello-Klein A, Dutra-Filho CS, et al. D-2-hydroxyglutaric acid induces oxidative stress in cerebral cortex of young rats. Eur J Neurosci 2003; 17: 2017-2022.
70. Bayley JP, Devilee P. Warburg tumours and the mechanisms of mitochondrial tumour suppressor genes. Barking up the right tree? Curr Opin Genet Dev 2010; 20: 324-329.
71. Hughes JM, Groot AJ, van der Groep P, Sersansie R, Vooijs M, van Diest PJ, et al. Active HIF-1 in the normal human retina. J Histochem Cytochem 2010; 58: 247-254.
72. MacKenzie ED, Selak MA, Tennant DA, Payne LJ, Crosby S, Frederiksen CM, et al. Cell-permeating alpha-ketoglutarate derivatives alleviate pseudohypoxia in succinate dehydrogenase-deficient cells. Mol Cell Biol 2007; 27: 3282-3289.
73. King A, Selak MA, Gottlieb E. Succinate dehydrogenase and fumarate hydratase: linking mitochondrial dysfunction and cancer. Oncogene 2006; 25: 4675-4682.
74. Pollard PJ, Ratcliffe PJ. Cancer. Puzzling patterns of predisposition. Science 2009; 324: 192-194.
75. Frezza C, Tennant DA, Gottlieb E. IDH1 mutations in gliomas: when an enzyme loses its grip. Cancer Cell 2010; 17: 7-9.
76. Ducray F, Marie Y, Sanson M. IDH1 and IDH2 mutations in gliomas. N Engl J Med 2009; 360: 2248-2249.
77. Meyer J, Pusch S, Balss J, Capper D, Mueller W, Christians A, et al. PCR- and restriction endonuclease-based detection of IDH1 mutations. Brain Pathol 2010; 20: 298-300.
78. Horbinski C, Kelly L, Nikiforov YE, Durso MB, Nikiforova MN. Detection of IDH1 and IDH2 mutations by fluorescence melting curve analysis as a diagnostic tool for brain biopsies. J Mol Diagn 2010; 12: 487-492.
79. Chen G, Wu X, Yao Y, Zhou LF, Mao Y. Direct, real-time PCR (MethyLight) assay for methylation of O6-methylguanine-DNA methyltransferase promoter in glioma. Chin Med J 2009; 122: 1342-1345.
80. Felsberg J, Wolter M, Seul H, Friedensdorf B, Goppert M, Sabel MC, et al. Rapid and sensitive assessment of the IDH1 and IDH2 mutation status in cerebral gliomas based on DNA pyrosequencing. Acta Neuropathol 2010; 119: 501-507.
81. Kato Y, Jin G, Kuan CT, McLendon RE, Yan H, Bigner DD. A monoclonal antibody IMab-1 specifically recognizes IDH1R132H, the most common glioma-derived mutation. Biochem Biophys Res Commun 2009; 390: 547-551.
82. Capper D, Zentgraf H, Balss J, Hartmann C, von Deimling A. Monoclonal antibody specific for IDH1 R132H mutation. Acta Neuropathol 2009; 118: 599-601.
83. Capper D, Sahm F, Hartmann C, Meyermann R, von Deimling A, Schittenhelm J. Application of mutant IDH1 antibody to differentiate diffuse glioma from nonneoplastic central nervous system lesions and therapy-induced changes. Am J Surg Pathol 2010; 34: 1199-1204.
84. Reitman ZJ, Parsons DW, Yan H. IDH1 and IDH2: not your typical oncogenes. Cancer Cell 2010; 17: 215-216.
85. Kimmelman J, Nalbantoglu J. Faithful companions: a proposal for neurooncology trials in pet dogs. Cancer Res 2007; 67: 4541-4544.
86. Reitman ZJ, Olby NJ, Mariani CL, Thomas R, Breen M, Bigner DD, et al. IDH1 and IDH2 hotspot mutations are not found in canine glioma. Int J Cancer 2010; 127: 245-246.
87. Dubbink HJ, Taal W, van Marion R, Kros JM, van Heuvel I, Bromberg JE, et al. IDH1 mutations in low-grade astrocytomas predict survival but not response to temozolomide. Neurology 2009; 73: 1792-1795.
88. van den Bent MJ, Dubbink HJ, Marie Y, Brandes AA, Taphoorn MJ, Wesseling P, et al. IDH1 and IDH2 mutations are prognostic but not predictive for outcome in anaplastic oligodendroglial tumors: a report of the European Organization for Research and Treatment of Cancer Brain Tumor Group. Clin Cancer Res 2010; 16: 1597-1604.
89. Semenza GL. Evaluation of HIF-1 inhibitors as anticancer agents. Drug Discov Today 2007; 12: 853-859.