Molecular and Genomic Alterations in Glioblastoma Multiforme

American Journal of Pathology

Volumn 185, Issue 7, 2015, Pages 1820-1833

  Crespo, Ines ^a   Vital, Ana Louisa ^a   Gonzalez Tablas, María ^b   Patino, María Del Carmen ^b   Otero, Alvaro ^c,d   Lopes, María Celeste ^a   De Oliveira, Catarina ^a   Domingues, Patricia ^a,b,d   Orfao, Alberto ^b,d   Tabernero, Maria Dolores ^b,c,d  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF SALAMANCA   (Spain)

^c HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

^d INSTITUTO DE INVESTIGACIÓN BIOMÉDICA DE SALAMANCA IBSAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; ISOCITRATE DEHYDROGENASE 1; ISOCITRATE DEHYDROGENASE 2; MESSENGER RNA; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; PHOSPHATASE AND TENSIN HOMOLOG; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR; PROTEIN KINASE B; PROTEIN MDM2; PROTEIN MDMX; PROTEIN P16; PROTEIN P53; RAS PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; DNA METHYLATION; EPIGENETICS; GENE AMPLIFICATION; GENE EXPRESSION; GENE INTERACTION; GENE MUTATION; GENETIC VARIABILITY; GLIOBLASTOMA; HUMAN; INTRACELLULAR SIGNALING; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; ANIMAL; BRAIN TUMOR; GENETICS; GENOMICS; METABOLISM; MOUSE; MUTATION; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN NEOPLASMS; EPIGENOMICS; GENOMICS; GLIOBLASTOMA; HUMANS; MICE; MUTATION; SIGNAL TRANSDUCTION;

EID: 84931449647     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2015.02.023     Document Type: Review

References (100)

1. H. Ohgaki, P. Dessen, B. Jourde, S. Horstmann, T. Nishikawa, P.L. Di Patre, C. Burkhard, D. Schuler, N.M. Probst-Hensch, P.C. Maiorka, N. Baeza, P. Pisani, Y. Yonekawa, M.G. Yasargil, U.M. Lutolf, and P. Kleihues Genetic pathways to glioblastoma: a population-based study Cancer Res 64 2004 6892 6899
2. C.W. Brennan, R.G. Verhaak, A. McKenna, B. Campos, H. Noushmehr, S.R. Salama TCGA Research Network The somatic genomic landscape of glioblastoma Cell 155 2013 462 477
3. M. Nakamura, T. Watanabe, Y. Yonekawa, P. Kleihues, and H. Ohgaki Promoter methylation of the DNA repair gene MGMT in astrocytomas is frequently associated with G: C - > A: t mutations of the TP53 tumor suppressor gene Carcinogenesis 22 2001 1715 1719
4. M. Nakamura, E. Ishida, K. Shimada, M. Kishi, H. Nakase, T. Sakaki, and N. Konishi Frequent LOH on 22q12.3 and TIMP-3 inactivation occur in the progression to secondary glioblastomas Lab Invest 85 2005 165 175
5. M. Nakamura, Y. Yonekawa, P. Kleihues, and H. Ohgaki Promoter hypermethylation of the RB1 gene in glioblastomas Lab Invest 81 2001 77 82
6. M. Nakamura, T. Watanabe, U. Klangby, C. Asker, K. Wiman, Y. Yonekawa, P. Kleihues, and H. Ohgaki p14ARF deletion and methylation in genetic pathways to glioblastomas Brain Pathol 11 2001 159 168
7. Y. Jiao, P.J. Killela, Z.J. Reitman, A.B. Rasheed, C.M. Heaphy, R.F. de Wilde, F.J. Rodriguez, S. Rosemberg, S.M. Oba-Shinjo, S.K. Nagahashi Marie, C. Bettegowda, N. Agrawal, E. Lipp, C. Pirozzi, G. Lopez, Y. He, H. Friedman, A.H. Friedman, G.J. Riggins, M. Holdhoff, P. Burger, R. McLendon, D.D. Bigner, B. Vogelstein, A.K. Meeker, K.W. Kinzler, N. Papadopoulos, L.A. Diaz, and H. Yan Frequent ATRX, CIC, FUBP1 and IDH1 mutations refine the classification of malignant gliomas Oncotarget 3 2012 709 722
8. H. Yan, D.W. Parsons, G. Jin, R. McLendon, B.A. Rasheed, W. Yuan, I. Kos, I. Batinic-Haberle, S. Jones, G.J. Riggins, H. Friedman, A. Friedman, D. Reardon, J. Herndon, K.W. Kinzler, V.E. Velculescu, B. Vogelstein, and D.D. Bigner IDH1 and IDH2 mutations in gliomas N Engl J Med 360 2009 765 773
9. S. Nobusawa, T. Watanabe, P. Kleihues, and H. Ohgaki IDH1 mutations as molecular signature and predictive factor of secondary glioblastomas Clin Cancer Res 15 2009 6002 6007
10. H. Fujisawa, R.M. Reis, M. Nakamura, S. Colella, Y. Yonekawa, P. Kleihues, and H. Ohgaki Loss of heterozygosity on chromosome 10 is more extensive in primary (de novo) than in secondary glioblastomas Lab Invest 80 2000 65 72
11. M. Nakamura, F. Yang, H. Fujisawa, Y. Yonekawa, P. Kleihues, and H. Ohgaki Loss of heterozygosity on chromosome 19 in secondary glioblastomas J Neuropathol Exp Neurol 59 2000 539 543
12. Y. Tohma, C. Gratas, E.G. Van Meir, I. Desbaillets, M. Tenan, O. Tachibana, P. Kleihues, and H. Ohgaki Necrogenesis and Fas/APO-1 (CD95) expression in primary (de novo) and secondary glioblastomas J Neuropathol Exp Neurol 57 1998 239 245
13. D. Xie, Y.X. Zeng, H.J. Wang, J.M. Wen, Y. Tao, J.S. Sham, and X.Y. Guan Expression of cytoplasmic and nuclear Survivin in primary and secondary human glioblastoma Br J Cancer 94 2006 108 114
14. G. Choe, J.K. Park, L. Jouben-Steele, T.J. Kremen, L.M. Liau, H.V. Vinters, T.F. Cloughesy, and P.S. Mischel Active matrix metalloproteinase 9 expression is associated with primary glioblastoma subtype Clin Cancer Res 8 2002 2894 2901
15. K. Watanabe, O. Tachibana, K. Sata, Y. Yonekawa, P. Kleihues, and H. Ohgaki Overexpression of the EGF receptor and p53 mutations are mutually exclusive in the evolution of primary and secondary glioblastomas Brain Pathol 6 1996 217 223
16. M. Furuta, R.J. Weil, A.O. Vortmeyer, S. Huang, J. Lei, T.N. Huang, Y.S. Lee, D.A. Bhowmick, I.A. Lubensky, E.H. Oldfield, and Z. Zhuang Protein patterns and proteins that identify subtypes of glioblastoma multiforme Oncogene 23 2004 6806 6814
17. W. Biernat, P. Kleihues, Y. Yonekawa, and H. Ohgaki Amplification and overexpression of MDM2 in primary (de novo) glioblastomas J Neuropathol Exp Neurol 56 1997 180 185
18. S. Karcher, H.H. Steiner, R. Ahmadi, S. Zoubaa, G. Vasvari, H. Bauer, A. Unterberg, and C. Herold-Mende Different angiogenic phenotypes in primary and secondary glioblastomas Int J Cancer 118 2006 2182 2189
19. S. Godard, G. Getz, M. Delorenzi, P. Farmer, H. Kobayashi, I. Desbaillets, M. Nozaki, A.C. Diserens, M.F. Hamou, P.Y. Dietrich, L. Regli, R.C. Janzer, P. Bucher, R. Stupp, N. de Tribolet, E. Domany, and M.E. Hegi Classification of human astrocytic gliomas on the basis of gene expression: a correlated group of genes with angiogenic activity emerges as a strong predictor of subtypes Cancer Res 63 2003 6613 6625
20. K. Somasundaram, S.P. Reddy, K. Vinnakota, R. Britto, M. Subbarayan, S. Nambiar, A. Hebbar, C. Samuel, M. Shetty, H.K. Sreepathi, V. Santosh, A.S. Hegde, S. Hegde, P. Kondaiah, and M.R. Rao Upregulation of ASCL1 and inhibition of Notch signaling pathway characterize progressive astrocytoma Oncogene 24 2005 7073 7083
21. R.G. Verhaak, K.A. Hoadley, E. Purdom, V. Wang, Y. Qi, M.D. Wilkerson, C.R. Miller, L. Ding, T. Golub, J.P. Mesirov, G. Alexe, M. Lawrence, M. O'Kelly, P. Tamayo, B.A. Weir, S. Gabriel, W. Winckler, S. Gupta, L. Jakkula, H.S. Feiler, J.G. Hodgson, C.D. James, J.N. Sarkaria, C. Brennan, A. Kahn, P.T. Spellman, R.K. Wilson, T.P. Speed, J.W. Gray, M. Meyerson, G. Getz, C.M. Perou, and D.N. Hayes Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1 Cancer Cell 17 2010 98 110
22. H. Ohgaki, and P. Kleihues Genetic pathways to primary and secondary glioblastoma Am J Pathol 170 2007 1445 1453
23. H. Mao, D.G. Lebrun, J. Yang, V.F. Zhu, and M. Li Deregulated signaling pathways in glioblastoma multiforme: molecular mechanisms and therapeutic targets Cancer Invest 30 2012 48 56
24. The Cancer Genome Atlas (TCGA) Research Network Comprehensive genomic characterization defines human glioblastoma genes and core pathways Nature 455 2008 1061 1068
25. G.P. Dunn, M.L. Rinne, J. Wykosky, G. Genovese, S.N. Quayle, I.F. Dunn, P.K. Agarwalla, M.G. Chheda, B. Campos, A. Wang, C. Brennan, K.L. Ligon, F. Furnari, W.K. Cavenee, R.A. Depinho, L. Chin, and W.C. Hahn Emerging insights into the molecular and cellular basis of glioblastoma Genes Dev 26 2012 756 784
26. M. Nakada, D. Kita, T. Watanabe, Y. Hayashi, L. Teng, I.V. Pyko, and J. Hamada Aberrant signaling pathways in glioma Cancers (Basel) 3 2011 3242 3278
27. Y. Zheng, B.C. McFarland, D. Drygin, H. Yu, S.L. Bellis, H. Kim, M. Bredel, and E.N. Benveniste Targeting protein kinase CK2 suppresses prosurvival signaling pathways and growth of glioblastoma Clin Cancer Res 19 2013 6484 6494
28. L. Fredriksson, H. Li, and U. Eriksson The PDGF family: four gene products form five dimeric isoforms Cytokine Growth Factor Rev 15 2004 197 204
29. A. Alentorn, Y. Marie, C. Carpentier, B. Boisselier, M. Giry, M. Labussiére, K. Mokhtari, K. Hoang-Xuan, M. Sanson, J.Y. Delattre, and A. Idbaih Prevalence clinico-pathological value, and co-occurrence of PDGFRA abnormalities in diffuse gliomas Neuro Oncol 14 2012 1393 1403
30. E. Rheinbay, M.L. Suva, S.M. Gillespie, H. Wakimoto, A.P. Patel, M. Shahid, O. Oksuz, S.D. Rabkin, R.L. Martuza, M.N. Rivera, D.N. Louis, S. Kasif, A.S. Chi, and B.E. Bernstein An aberrant transcription factor network essential for Wnt signaling and stem cell maintenance in glioblastoma Cell Rep 3 2013 1567 1579
31. M.K. Nicholas, R.V. Lukas, N.F. Jafri, L. Faoro, and R. Salgia Epidermal growth factor receptor-mediated signal transduction in the development and therapy of gliomas Clin Cancer Res 12 2006 7261 7270
32. P.H. Huang, A.M. Xu, and F.M. White Oncogenic EGFR signaling networks in glioma Sci Signal 2 2009 re6
33. K.J. Hatanpaa, S. Burma, D. Zhao, and A.A. Habib Epidermal growth factor receptor in glioma: signal transduction, neuropathology, imaging, and radioresistance Neoplasia 12 2010 675 684
34. C.G. Patil, M. Nuno, A. Elramsisy, D. Mukherjee, C. Carico, J. Dantis, J. Hu, J.S. Yu, X. Fan, K.L. Black, and S.I. Bannykh High levels of phosphorylated MAP kinase are associated with poor survival among patients with glioblastoma during the temozolomide era Neuro Oncol 15 2013 104 111
35. J. Downward Targeting RAS signalling pathways in cancer therapy Nat Rev Cancer 3 2003 11 22
36. V.K. Rajasekhar, A. Viale, N.D. Socci, M. Wiedmann, X. Hu, and E.C. Holland Oncogenic Ras and Akt signaling contribute to glioblastoma formation by differential recruitment of existing mRNAs to polysomes Mol Cell 12 2003 889 901
37. F.B. Furnari, T. Fenton, R.M. Bachoo, A. Mukasa, J.M. Stommel, A. Stegh, W.C. Hahn, K.L. Ligon, D.N. Louis, C. Brennan, L. Chin, R.A. DePinho, and W.K. Cavenee Malignant astrocytic glioma: genetics, biology, and paths to treatment Genes Dev 21 2007 2683 2710
38. D. Koul PTEN signaling pathways in glioblastoma Cancer Biol Ther 7 2008 1321 1325
39. P.K. Vogt PI 3-kinase, mTOR, protein synthesis and cancer Trends Mol Med 7 2001 482 484
40. X. Fan, Y. Aalto, S.G. Sanko, S. Knuutila, D. Klatzmann, and J.S. Castresana Genetic profile, PTEN mutation and therapeutic role of PTEN in glioblastomas Int J Oncol 21 2002 1141 1150
41. E.S. Knudsen, and J.Y. Wang Targeting the RB-pathway in cancer therapy Clin Cancer Res 16 2010 1094 1099
42. A. Matheu, A. Maraver, and M. Serrano The Arf/p53 pathway in cancer and aging Cancer Res 68 2008 6031 6034
43. S. Shangary, and S. Wang Small-molecule inhibitors of the MDM2-p53 protein-protein interaction to reactivate p53 function: a novel approach for cancer therapy Annu Rev Pharmacol Toxicol 49 2009 223 241
44. M. Grzmil, and B.A. Hemmings Deregulated signalling networks in human brain tumours Biochim Biophys Acta 1804 2010 476 483
45. V.R. Dasari, K. Kaur, K.K. Velpula, M. Gujrati, D. Fassett, J.D. Klopfenstein, D.H. Dinh, and J.S. Rao Upregulation of PTEN in glioma cells by cord blood mesenchymal stem cells inhibits migration via downregulation of the PI3K/Akt pathway PLoS One 5 2010 e10350
46. E.G. Van Meir, C.G. Hadjipanayis, A.D. Norden, H.K. Shu, P.Y. Wen, and J.J. Olson Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma CA Cancer J Clin 60 2010 166 193
47. K. Meletis, V. Wirta, S.M. Hede, M. Nister, J. Lundeberg, and J. Frisen p53 Suppresses the self-renewal of adult neural stem cells Development 133 2006 363 369
48. I. Zawlik, D. Kita, S. Vaccarella, M. Mittelbronn, S. Franceschi, and H. Ohgaki Common polymorphisms in the MDM2 and TP53 genes and the relationship between TP53 mutations and patient outcomes in glioblastomas Brain Pathol 19 2009 188 194
49. L.K. Linares, A. Hengstermann, A. Ciechanover, S. Muller, and M. Scheffner HdmX stimulates Hdm2-mediated ubiquitination and degradation of p53 Proc Natl Acad Sci U S A 100 2003 12009 12014
50. P.A. Jones, and S.B. Baylin The epigenomics of cancer Cell 128 2007 683 692
51. N.K. Kloosterhof, J.J. de Rooi, M. Kros, P.H. Eilers, P.A. Sillevis Smitt, M.J. van den Bent, and P.J. French Molecular subtypes of glioma identified by genome-wide methylation profiling Genes Chromosomes Cancer 52 2013 665 674
52. K. Horiguchi, Y. Tomizawa, M. Tosaka, S. Ishiuchi, H. Kurihara, M. Mori, and N. Saito Epigenetic inactivation of RASSF1A candidate tumor suppressor gene at 3p21.3 in brain tumors Oncogene 22 2003 7862 7865
53. A.R. Stone, W. Bobo, D.J. Brat, N.S. Devi, E.G. Van Meir, and P.M. Vertino Aberrant methylation and down-regulation of TMS1/ASC in human glioblastoma Am J Pathol 165 2004 1151 1161
54. R. Martinez, G. Schackert, and M. Esteller Hypermethylation of the proapoptotic gene TMS1/ASC: prognostic importance in glioblastoma multiforme J Neurooncol 82 2007 133 139
55. M. Mellai, A. Piazzi, V. Caldera, L. Annovazzi, O. Monzeglio, R. Senetta, P. Cassoni, and D. Schiffer Promoter hypermethylation of the EMP3 gene in a series of 229 human gliomas Biomed Res Int 2013 2013 756302
56. I. Crespo, A.L. Vital, A.B. Nieto, O. Rebelo, H. Tao, M.C. Lopes, C.R. Oliveira, P.J. French, A. Orfao, and M.D. Tabernero Detailed characterization of alterations of chromosomes 7, 9, and 10 in glioblastomas as assessed by single-nucleotide polymorphism arrays J Mol Diagn 13 2011 634 647
57. A.L. Vital, M.D. Tabernero, I. Crespo, O. Rebelo, H. Tao, F. Gomes, M.C. Lopes, and A. Orfao Intratumoral patterns of clonal evolution in gliomas Neurogenetics 11 2010 227 239
58. C.L. Appin, and D.J. Brat Molecular genetics of gliomas Cancer J 20 2014 66 72
59. N. Nonoguchi, T. Ohta, J.E. Oh, Y.H. Kim, P. Kleihues, and H. Ohgaki TERT promoter mutations in primary and secondary glioblastomas Acta Neuropathol 126 2013 931 937
60. H. Arita, Y. Narita, S. Fukushima, K. Tateishi, Y. Matsushita, A. Yoshida, Y. Miyakita, M. Ohno, V.P. Collins, N. Kawahara, S. Shibui, and K. Ichimura Upregulating mutations in the TERT promoter commonly occur in adult malignant gliomas and are strongly associated with total 1p19q loss Acta Neuropathol 126 2013 267 276
61. H.K. Gan, A.N. Cvrljevic, and T.G. Johns The epidermal growth factor receptor variant III (EGFRvIII): where wild things are altered FEBS J 280 2013 5350 5370
62. I. Crespo, H. Tao, A.B. Nieto, O. Rebelo, P. Domingues, A.L. Vital, C. Patino Mdel, M. Barbosa, M.C. Lopes, C.R. Oliveira, A. Orfao, and M.D. Tabernero Amplified and homozygously deleted genes in glioblastoma: impact on gene expression levels PLoS One 7 2012 e46088
63. C. Carico, M. Nuno, D. Mukherjee, A. Elramsisy, J. Dantis, J. Hu, J. Rudnick, J.S. Yu, K.L. Black, S.I. Bannykh, and C.G. Patil Loss of PTEN is not associated with poor survival in newly diagnosed glioblastoma patients of the temozolomide era PLoS One 7 2012 e33684
64. D. Kita, Y. Yonekawa, M. Weller, and H. Ohgaki PIK3CA alterations in primary (de novo) and secondary glioblastomas Acta Neuropathol 113 2007 295 302
65. G.J. Kitange, B.L. Carlson, M.A. Schroeder, P.T. Grogan, J.D. Lamont, P.A. Decker, W. Wu, C.D. James, and J.N. Sarkaria Induction of MGMT expression is associated with temozolomide resistance in glioblastoma xenografts Neuro Oncol 11 2009 281 291
66. B.C. Christensen, A.A. Smith, S. Zheng, D.C. Koestler, E.A. Houseman, C.J. Marsit, J.L. Wiemels, H.H. Nelson, M.R. Karagas, M.R. Wrensch, K.T. Kelsey, and J.K. Wiencke DNA methylation, isocitrate dehydrogenase mutation, and survival in glioma J Natl Cancer Inst 103 2011 143 153
67. N. Inohara, L. Ding, S. Chen, and G. Nunez Harakiri, a novel regulator of cell death, encodes a protein that activates apoptosis and interacts selectively with survival-promoting proteins Bcl-2 and Bcl-X(L) EMBO J 16 1997 1686 1694
68. J. Jeuken, A. Sijben, C. Alenda, J. Rijntjes, M. Dekkers, S. Boots-Sprenger, R. McLendon, and P. Wesseling Robust detection of EGFR copy number changes and EGFR variant III: technical aspects and relevance for glioma diagnostics Brain Pathol 19 2009 661 671
69. A. Murat, E. Migliavacca, T. Gorlia, W.L. Lambiv, T. Shay, M.F. Hamou, N. de Tribolet, L. Regli, W. Wick, M.C. Kouwenhoven, J.A. Hainfellner, F.L. Heppner, P.Y. Dietrich, Y. Zimmer, J.G. Cairncross, R.C. Janzer, E. Domany, M. Delorenzi, R. Stupp, and M.E. Hegi Stem cell-related "self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma J Clin Oncol 26 2008 3015 3024
70. R. Benito, R. Gil-Benso, V. Quilis, M. Perez, M. Gregori-Romero, P. Roldan, J. Gonzalez-Darder, M. Cerda-Nicolas, and C. Lopez-Gines Primary glioblastomas with and without EGFR amplification: relationship to genetic alterations and clinicopathological features Neuropathology 30 2010 392 400
71. A.B. Heimberger, R. Hlatky, D. Suki, D. Yang, J. Weinberg, M. Gilbert, R. Sawaya, and K. Aldape Prognostic effect of epidermal growth factor receptor and EGFRvIII in glioblastoma multiforme patients Clin Cancer Res 11 2005 1462 1466
72. C.E. Pelloski, K.V. Ballman, A.F. Furth, L. Zhang, E. Lin, E.P. Sulman, K. Bhat, J.M. McDonald, W.K. Yung, H. Colman, S.Y. Woo, A.B. Heimberger, D. Suki, M.D. Prados, S.M. Chang, F.G. Barker 2nd, J.C. Buckner, C.D. James, and K. Aldape Epidermal growth factor receptor variant III status defines clinically distinct subtypes of glioblastoma J Clin Oncol 25 2007 2288 2294
73. N. Montano, T. Cenci, M. Martini, Q.G. D'Alessandris, F. Pelacchi, L. Ricci-Vitiani, G. Maira, R. De Maria, L.M. Larocca, and R. Pallini Expression of EGFRvIII in glioblastoma: prognostic significance revisited Neoplasia 13 2011 1113 1121
74. B.M. Costa, M. Viana-Pereira, R. Fernandes, S. Costa, P. Linhares, R. Vaz, C. Pinheiro, J. Lima, P. Soares, A. Silva, F. Pardal, J. Amorim, R. Nabico, R. Almeida, C. Alegria, M.M. Pires, E. Carvalho, P. Oliveira, J.M. Lopes, and R.M. Reis Impact of EGFR genetic variants on glioma risk and patient outcome Cancer Epidemiol Biomarkers Prev 20 2011 2610 2617
75. M.J. van den Bent, A.A. Brandes, R. Rampling, M.C. Kouwenhoven, J.M. Kros, A.F. Carpentier, P.M. Clement, M. Frenay, M. Campone, J.F. Baurain, J.P. Armand, M.J. Taphoorn, A. Tosoni, H. Kletzl, B. Klughammer, D. Lacombe, and T. Gorlia Randomized phase II trial of erlotinib versus temozolomide or carmustine in recurrent glioblastoma: EORTC brain tumor group study 26034 J Clin Oncol 27 2009 1268 1274
76. I. Paul, S. Bhattacharya, A. Chatterjee, and M.K. Ghosh Current understanding on EGFR and Wnt/beta-catenin signaling in glioma and their possible crosstalk Genes Cancer 4 2013 427 446
77. X. Xu, J. Zhao, Z. Xu, B. Peng, Q. Huang, E. Arnold, and J. Ding Structures of human cytosolic NADP-dependent isocitrate dehydrogenase reveal a novel self-regulatory mechanism of activity J Biol Chem 279 2004 33946 33957
78. Z.J. Reitman, and H. Yan Isocitrate dehydrogenase 1 and 2 mutations in cancer: alterations at a crossroads of cellular metabolism J Natl Cancer Inst 102 2010 932 941
79. J.W. Joseph, M.V. Jensen, O. Ilkayeva, F. Palmieri, C. Alarcon, C.J. Rhodes, and C.B. Newgard The mitochondrial citrate/isocitrate carrier plays a regulatory role in glucose-stimulated insulin secretion J Biol Chem 281 2006 35624 35632
80. D.W. Parsons, S. Jones, X. Zhang, J.C. Lin, R.J. Leary, P. Angenendt, P. Mankoo, H. Carter, I.M. Siu, G.L. Gallia, A. Olivi, R. McLendon, B.A. Rasheed, S. Keir, T. Nikolskaya, Y. Nikolsky, D.A. Busam, H. Tekleab, L.A. Diaz Jr., J. Hartigan, D.R. Smith, R.L. Strausberg, S.K. Marie, S.M. Shinjo, H. Yan, G.J. Riggins, D.D. Bigner, R. Karchin, N. Papadopoulos, G. Parmigiani, B. Vogelstein, V.E. Velculescu, and K.W. Kinzler An integrated genomic analysis of human glioblastoma multiforme Science 321 2008 1807 1812
81. N.K. Kloosterhof, L.B. Bralten, H.J. Dubbink, P.J. French, and M.J. van den Bent Isocitrate dehydrogenase-1 mutations: a fundamentally new understanding of diffuse glioma? Lancet Oncol 12 2011 83 91
82. T. Watanabe, S. Nobusawa, P. Kleihues, and H. Ohgaki IDH1 mutations are early events in the development of astrocytomas and oligodendrogliomas Am J Pathol 174 2009 1149 1153
83. M. Weller, J. Felsberg, C. Hartmann, H. Berger, J.P. Steinbach, J. Schramm, M. Westphal, G. Schackert, M. Simon, J.C. Tonn, O. Heese, D. Krex, G. Nikkhah, T. Pietsch, O. Wiestler, G. Reifenberger, A. von Deimling, and M. Loeffler 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 27 2009 5743 5750
84. M. Sanson, Y. Marie, S. Paris, A. Idbaih, J. Laffaire, F. Ducray, S. El Hallani, B. Boisselier, K. Mokhtari, K. Hoang-Xuan, and J.Y. Delattre Isocitrate dehydrogenase 1 codon 132 mutation is an important prognostic biomarker in gliomas J Clin Oncol 27 2009 4150 4154
85. S. Zhao, Y. Lin, W. Xu, W. Jiang, Z. Zha, P. Wang, W. Yu, Z. Li, L. Gong, Y. Peng, J. Ding, Q. Lei, K.L. Guan, and Y. Xiong Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1alpha Science 324 2009 261 265
86. L. Dang, D.W. White, S. Gross, B.D. Bennett, M.A. Bittinger, E.M. Driggers, V.R. Fantin, H.G. Jang, S. Jin, M.C. Keenan, K.M. Marks, R.M. Prins, P.S. Ward, K.E. Yen, L.M. Liau, J.D. Rabinowitz, L.C. Cantley, C.B. Thompson, M.G. Vander Heiden, and S.M. Su Cancer-associated IDH1 mutations produce 2-hydroxyglutarate Nature 462 2009 739 744
87. I. Zawlik, S. Vaccarella, D. Kita, M. Mittelbronn, S. Franceschi, and H. Ohgaki Promoter methylation and polymorphisms of the MGMT gene in glioblastomas: a population-based study Neuroepidemiology 32 2009 21 29
88. U. Herrlinger, J. Rieger, D. Koch, S. Loeser, B. Blaschke, R.D. Kortmann, J.P. Steinbach, T. Hundsberger, W. Wick, R. Meyermann, T.C. Tan, C. Sommer, M. Bamberg, G. Reifenberger, and M. Weller Phase II trial of lomustine plus temozolomide chemotherapy in addition to radiotherapy in newly diagnosed glioblastoma: UKT-03 J Clin Oncol 24 2006 4412 4417
89. R. Stupp, M.E. Hegi, W.P. Mason, M.J. van den Bent, M.J. Taphoorn, R.C. Janzer, S.K. Ludwin, A. Allgeier, B. Fisher, K. Belanger, P. Hau, A.A. Brandes, J. Gijtenbeek, C. Marosi, C.J. Vecht, K. Mokhtari, P. Wesseling, S. Villa, E. Eisenhauer, T. Gorlia, M. Weller, D. Lacombe, J.G. Cairncross, and R.O. Mirimanoff 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 10 2009 459 466
90. U. Linz Commentary on 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) Cancer 116 2010 1844 1846
91. A.L. Rivera, C.E. Pelloski, M.R. Gilbert, H. Colman, C. De La Cruz, E.P. Sulman, B.N. Bekele, and K.D. Aldape MGMT promoter methylation is predictive of response to radiotherapy and prognostic in the absence of adjuvant alkylating chemotherapy for glioblastoma Neuro Oncol 12 2010 116 121
92. M. Weller, H. Berger, C. Hartmann, J. Schramm, M. Westphal, M. Simon, R. Goldbrunner, D. Krex, J.P. Steinbach, C.B. Ostertag, M. Loeffler, T. Pietsch, and A. von Deimling Combined 1p/19q loss in oligodendroglial tumors: predictive or prognostic biomarker? Clin Cancer Res 13 2007 6933 6937
93. M. Weller, R. Stupp, G. Reifenberger, A.A. Brandes, M.J. van den Bent, W. Wick, and M.E. Hegi MGMT promoter methylation in malignant gliomas: ready for personalized medicine? Nat Rev Neurol 6 2010 39 51
94. C.H. Fan, W.L. Liu, H. Cao, C. Wen, L. Chen, and G. Jiang O6-methylguanine DNA methyltransferase as a promising target for the treatment of temozolomide-resistant gliomas Cell Death Dis 4 2013 e876
95. A.L. Vital, M.D. Tabernero, A. Castrillo, O. Rebelo, H. Tao, F. Gomes, A.B. Nieto, C. Resende Oliveira, M.C. Lopes, and A. Orfao Gene expression profiles of human glioblastomas are associated with both tumor cytogenetics and histopathology Neuro Oncol 12 2010 991 1003
96. C.L. Tso, W.A. Freije, A. Day, Z. Chen, B. Merriman, A. Perlina, Y. Lee, E.Q. Dia, K. Yoshimoto, P.S. Mischel, L.M. Liau, T.F. Cloughesy, and S.F. Nelson Distinct transcription profiles of primary and secondary glioblastoma subgroups Cancer Res 66 2006 159 167
97. C.L. Nutt, D.R. Mani, R.A. Betensky, P. Tamayo, J.G. Cairncross, C. Ladd, U. Pohl, C. Hartmann, M.E. McLaughlin, T.T. Batchelor, P.M. Black, A. von Deimling, S.L. Pomeroy, T.R. Golub, and D.N. Louis Gene expression-based classification of malignant gliomas correlates better with survival than histological classification Cancer Res 63 2003 1602 1607
98. W.A. Freije, F.E. Castro-Vargas, Z. Fang, S. Horvath, T. Cloughesy, L.M. Liau, P.S. Mischel, and S.F. Nelson Gene expression profiling of gliomas strongly predicts survival Cancer Res 64 2004 6503 6510
99. H.S. Phillips, S. Kharbanda, R. Chen, W.F. Forrest, R.H. Soriano, T.D. Wu, A. Misra, J.M. Nigro, H. Colman, L. Soroceanu, P.M. Williams, Z. Modrusan, B.G. Feuerstein, and K. Aldape Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis Cancer Cell 9 2006 157 173
100. Y. Lee, A.C. Scheck, T.F. Cloughesy, A. Lai, J. Dong, H.K. Farooqi, L.M. Liau, S. Horvath, P.S. Mischel, and S.F. Nelson Gene expression analysis of glioblastomas identifies the major molecular basis for the prognostic benefit of younger age BMC Med Genomics 1 2008 52