Diagnostic and prognostic molecular markers in common adult gliomas

Expert Review of Molecular Diagnostics

Volumn 10, Issue 5, 2010, Pages 637-649

  Rivera, Andreana L ^a   Pelloski, Christopher E ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

astrocytoma; biomarkers; EGFR; gene expression; glioblastoma; glioma; MGMT; oligodendroglioma; TCGA; temozolomide

Indexed keywords

CEDIRANIB; CHITINASE 3 LIKE 1 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; ISOCITRATE DEHYDROGENASE; LOMUSTINE; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROCARBAZINE; PROTEIN; PROTEIN KINASE B; RAS PROTEIN; TEMOZOLOMIDE; UNCLASSIFIED DRUG; VINCRISTINE; TUMOR MARKER;

ADULT; ASTROCYTOMA; CANCER RESISTANCE; CANCER SURVIVAL; CANCER SURVIVOR; CHROMOSOME 10; CHROMOSOME 19Q; CHROMOSOME 1P; CLINICAL FEATURE; CLINICAL TRIAL; DNA METHYLATION; EPENDYMOMA; GENE EXPRESSION PROFILING; GENE MUTATION; GLIOBLASTOMA; GLIOMA; HETEROZYGOSITY LOSS; HUMAN; OLIGODENDROGLIOMA; OVERALL SURVIVAL; PROGNOSIS; PROMOTER REGION; RADIATION DOSE; REVIEW; TUMOR CLASSIFICATION; CENTRAL NERVOUS SYSTEM NEOPLASMS; CLINICAL TRIAL (TOPIC); GENETICS; METABOLISM; PATHOLOGY; TREATMENT OUTCOME;

ADULT; CENTRAL NERVOUS SYSTEM NEOPLASMS; CLINICAL TRIALS AS TOPIC; GENE EXPRESSION PROFILING; GLIOMA; HUMANS; PROGNOSIS; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL;

EID: 77954730530     PISSN: 14737159     EISSN: 17448352     Source Type: Journal    
DOI: 10.1586/erm.10.44     Document Type: Review

References (111)

1. Kleihues P, Louis DN, Scheithauer BW et al. The WHO classification of tumors of the nervous system. J. Neuropathol. Exp. Neurol. 61(3), 215-225 (2002).
2. Scott CB, Scarantino C, Urtasun R et al. Validation and predictive power of Radiation Therapy Oncology Group (RTOG) recursive partitioning analysis classes for malignant glioma patients: a report using RTOG 90-06. Int. J. Radiat. Oncol. Biol. Phys. 40(1), 51-55 (1998).
3. Leighton C, Fisher B, Bauman G et al. Supratentorial low-grade glioma in adults: an analysis of prognostic factors and timing of radiation. J. Clin. Oncol. 15(4), 1294-1301 (1997).
4. Pignatti F, Van Den Bent M, Curran D et al. Prognostic factors for survival in adult patients with cerebral low-grade glioma. J. Clin. Oncol. 20(8), 2076-2084 (2002).
5. Schiff D, Brown PD, Giannini C. Outcome in adult low-grade glioma: the impact of prognostic factors and treatment. Neurology 69(13), 1366-1373 (2007).
6. Okamoto Y, DI Patre PL, Burkhard C et al. Population-based study on incidence, survival rates, and genetic alterations of low-grade diffuse astrocytomas and oligodendrogliomas. Acta Neuropathol. 108(1), 49-56 (2004).
7. Peraud A, Kreth FW, Wiestler OD, Kleihues P, Reulen HJ. Prognostic impact of tp53 mutations and p53 protein overexpression in supratentorial WHO grade II astrocytomas and oligoastrocytomas. Clin. Cancer Res. 8(5), 1117-1124 (2002).
8. Hoshino T, Ahn D, Prados MD, Lamborn K, Wilson CB. Prognostic significance of the proliferative potential of intracranial gliomas measured by bromodeoxyuridine labeling. Int. J. Cancer 53(4), 550-555 (1993).
9. Jaros E, Perry RH, Adam L et al. Prognostic implications of p53 protein, epidermal growth factor receptor, and Ki-67 labelling in brain tumours. Br. J. Cancer 66(2), 373-385 (1992).
10. Johannessen AL, Torp SH. The clinical value of Ki-67/mib-1 labeling index in human astrocytomas. Pathol. Oncol. Res. 12(3), 143-147 (2006).
11. Ohgaki H, Dessen P, Jourde B et al. Genetic pathways to glioblastoma: a population-based study. Cancer Res. 64(19), 6892-6899 (2004).
12. Perry A, Jenkins RB, O'Fallon JR et al. Clinicopathologic study of 85 similarly treated patients with anaplastic astrocytic tumors. An analysis of DNA content (ploidy), cellular proliferation, and p53 expression. Cancer 86(4), 672-683 (1999).
13. Tortosa A, Vinolas N, Villa S et al. Prognostic implication of clinical, radiologic, and pathologic features in patients with anaplastic gliomas. Cancer 97(4), 1063-1071 (2003).
14. Jarvela S, Helin H, Haapasalo J et al. Amplification of the epidermal growth factor receptor in astrocytic tumours by chromogenic in situ hybridization: association with clinicopathological features and patient survival. Neuropathol. Appl. Neurobiol. 32(4), 441-450 (2006).
15. Aldape KD, Ballman K, Furth A et al. Immunohistochemical detection of EGFRVIII in high malignancy grade astrocytomas and evaluation of prognostic significance. J. Neuropathol. Exp. Neurol. 63(7), 700-707 (2004).
16. Liu L, Backlund LM, Nilsson BR et al. Clinical significance of EGFR amplification and the aberrant EGFRVIII transcript in conventionally treated astrocytic gliomas. J. Mol. Med. 83(11), 917-926 (2005).
17. Smith JS, Tachibana I, Passe SM et al. PTEN mutation, EGFR amplification, and outcome in patients with anaplastic astrocytoma and glioblastoma multiforme. J. Natl Cancer Inst. 93(16), 1246-1256 (2001).
18. Stupp R, Hegi ME, Mason WP 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. 10(5), 459-466 (2009).
19. Scherer H. Cerebral astrocytoma and their derivatives. Am. J. Cancer 40, 159-198 (1940).
20. Von Deimling A, Von Ammon K, Schoenfeld D, Wiestler OD, Seizinger BR, Louis DN. Subsets of glioblastoma multiforme defined by molecular genetic analysis. Brain Pathol. 3(1), 19-26 (1993).
21. Filippini G, Falcone C, Boiardi A et al. Prognostic factors for survival in 676 consecutive patients with newly diagnosed primary glioblastoma. Neuro. Oncol. 10(1), 79-87 (2007).
22. Tait MJ, Petrik V, Loosemore A, Bell BA, Papadopoulos MC. Survival of patients with glioblastoma multiforme has not improved between 1993 and 2004: analysis of 625 cases. Br. J. Neurosurg. 21(5), 496-500 (2007).
23. Curran WJ JR, Scott CB, Horton J et al. Recursive partitioning analysis of prognostic factors in three radiation therapy oncology group malignant glioma trials. J. Natl Cancer Inst. 85(9), 704-710 (1993).
24. Shaw EG, Seiferheld W, Scott C et al. Reexamining the Radiation Therapy Oncology Group (RTOG) recursive partitioning analysis (RPA) for glioblastoma multiforme (GBM) patients. Int. J. Radiat. Oncol. Biol. Phys. 57(2 Suppl), S135-S136 (2003).
25. Esteller M, Garcia-Foncillas J, Andion E et al. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N. Engl. J. Med. 343(19), 1350-1354 (2000).
26. Stupp R, Mason WP, Van Den Bent MJ et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352(10), 987-996 (2005).
27. Hegi ME, Diserens AC, Gorlia T et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 352(10), 997-1003 (2005).
28. Rivera AL, Pelloski CE, Gilbert MR et al. MGMT promoter methylation is predictive of response to radiotherapy and prognostic in the absence of adjuvant alkylating chemotherapy for glioblastoma. Neuro. Oncol. 12(2), 116-121
29. Cairns-Smith S, Karran P. Epigenetic silencing of the DNA repair enzyme o6-methylguanine-DNA methyltransferase in mex-human cells. Cancer Res. 52(19), 5257-5263 (1992).
30. Pieper RO, Patel S, Ting SA, Futscher BW, Costello JF. Methylation of CpG island transcription factor binding sites is unnecessary for aberrant silencing of the human MGMT gene. J. Biol. Chem. 271(23), 13916-13924 (1996).
31. Kaina B, Christmann M, Naumann S, Roos WP. MGMT: key node in the battle against genotoxicity, carcinogenicity and apoptosis induced by alkylating agents. DNA Repair (Amst.) 6(8), 1079-1099 (2007).
32. Brandes AA, Franceschi E, Tosoni A et al. MGMT promoter methylation status can predict the incidence and outcome of pseudoprogression after concomitant radiochemotherapy in newly diagnosed glioblastoma patients. J. Clin. Oncol. 26(13), 2192-2197 (2008).
33. Brandes AA, Tosoni A, Franceschi E et al. Recurrence pattern after temozolomide concomitant with and adjuvant to radiotherapy in newly diagnosed patients with glioblastoma: correlation with MGMT promoter methylation status. J. Clin. Oncol. 27(8), 1275-1279 (2009).
34. Sonoda Y, Ozawa T, Hirose Y et al. Formation of intracranial tumors by genetically modified human astrocytes defines four pathways critical in the development of human anaplastic astrocytoma. Cancer Res. 61(13), 4956-4960 (2001).
35. Mischel PS, Shai R, Shi T et al. Identification of molecular subtypes of glioblastoma by gene expression profiling. Oncogene 22(15), 2361-2373 (2003). (Pubitemid 36566791)
36. Huncharek M, Kupelnick B. Epidermal growth factor receptor gene amplification as a prognostic marker in glioblastoma multiforme: results of a meta-analysis. Oncol. Res. 12(2), 107-112 (2000).
37. Kleihues P BP, Collins VP, Newcomb EW, Ohgaki H, Cavenee WK. Glioblastoma. In: Pathology and Genetics of Tumours of the Nervous System. Kleihues P (Eds). International Agency for Research on Cancer (IARC) Press, Lyon, France 29-39 (2000).
38. Shinojima N, Tada K, Shiraishi S et al. Prognostic value of epidermal growth factor receptor in patients with glioblastoma multiforme. Cancer Res. 63(20), 6962-6970 (2003).
39. Moscatello DK, Holgado-Madruga M, Emlet DR, Montgomery RB, Wong AJ. Constitutive activation of phosphatidylinositol 3-kinase by a naturally occurring mutant epidermal growth factor receptor. J. Biol. Chem. 273(1), 200-206 (1998).
40. Antonyak MA, Moscatello DK, Wong AJ. Constitutive activation of c-jun N-terminal kinase by a mutant epidermal growth factor receptor. J. Biol. Chem. 273(5), 2817-2822 (1998).
41. Montgomery RB, Moscatello DK, Wong AJ, Cooper JA, Stahl WL. Differential modulation of mitogen-activated protein (MAP) kinase/extracellular signal-related kinase kinase and MAP kinase activities by a mutant epidermal growth factor receptor. J. Biol. Chem. 270(51), 30562-30566 (1995).
42. Pedersen MW, Thykjaer T, Orntoft TF, Damstrup L, Poulsen HS. Profile of differentially expressed genes mediated by the type III epidermal growth factor receptor mutation expressed in a small-cell lung cancer cell line. Br. J. Cancer 85(8), 1211-1218 (2001).
43. Zhan Y, O'rourke DM. Shp-2-dependent mitogen-activated protein kinase activation regulates EGFRVIII but not wild-type epidermal growth factor receptor phosphorylation and glioblastoma cell survival. Cancer Res. 64(22), 8292-8298 (2004).
44. Mellinghoff IK, Wang MY, Vivanco I et al. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N. Engl. J. Med. 353(19), 2012-2024 (2005).
45. Simmons ML, Lamborn KR, Takahashi M et al. Analysis of complex relationships between age, p53, epidermal growth factor receptor, and survival in glioblastoma patients. Cancer Res. 61(3), 1122-1128 (2001).
46. Heimberger AB, Hlatky R, Suki D et al. Prognostic effect of epidermal growth factor receptor and EGFRVIII in glioblastoma multiforme patients. Clin. Cancer Res. 11(4), 1462-1466 (2005).
47. Pelloski CE, Ballman KV, Furth AF et al. Epidermal growth factor receptor variant III status defines clinically distinct subtypes of glioblastoma. J. Clin. Oncol. 25(16), 2288-2294 (2007).
48. Tuzi NL, Venter DJ, Kumar S, Staddon SL, Lemoine NR, Gullick WJ. Expression of growth factor receptors in human brain tumours. Br. J. Cancer 63(2), 227-233 (1991).
49. Sonoda Y, Ozawa T, Aldape KD, Deen DF, Berger MS, Pieper RO. Akt pathway activation converts anaplastic astrocytoma to glioblastoma multiforme in a human astrocyte model of glioma. Cancer Res. 61(18), 6674-6678 (2001).
50. Schlegel J, Piontek G, Budde B, Neff F, Kraus A. The akt/protein kinase B-dependent anti-apoptotic pathway and the mitogen-activated protein kinase cascade are alternatively activated in human glioblastoma multiforme. Cancer Lett. 158(1), 103-108 (2000).
51. Bouterfa HL, Sattelmeyer V, Czub S, Vordermark D, Roosen K, Tonn JC. Inhibition of ras farnesylation by lovastatin leads to downregulation of proliferation and migration in primary cultured human glioblastoma cells. Anticancer Res. 20(4), 2761-2771 (2000).
52. Chakravarti A, Zhai G, Suzuki Y et al. The prognostic significance of phosphatidylinositol 3-kinase pathway activation in human gliomas. J. Clin. Oncol. 22(10), 1926-1933 (2004).
53. Choe G, Horvath S, Cloughesy TF et al. Analysis of the phosphatidylinositol 3́-kinase signaling pathway in glioblastoma patients in vivo. Cancer Res. 63(11), 2742-2746 (2003).
54. Mawrin C, Diete S, Treuheit T et al. Prognostic relevance of MAPK expression in glioblastoma multiforme. Int. J. Oncol. 23(3), 641-648 (2003).
55. Cho HN, Lee YJ, Cho CK, Lee SJ, Lee YS. Downregulation of ERK2 is essential for the inhibition of radiation-induced cell death in HSP25 overexpressed L929 cells. Cell Death Differ. 9(4), 448-456 (2002).
56. Belka C, Knippers P, Rudner J, Faltin H, Bamberg M, Budach W. MEK1 and ERK1/2 kinases as targets for the modulation of radiation responses. Anticancer Res. 20(5A), 3243-3249 (2000).
57. Gupta AK, Bakanauskas VJ, Cerniglia GJ et al. The ras radiation resistance pathway. Cancer Res. 61(10), 4278-4282 (2001).
58. Jalal Hosseinimehr S, Inanami O, Hamasu T et al. Activation of c-kit by stem cell factor induces radioresistance to apoptosis through ERK-dependent expression of survivin in hl60 cells. J. Radiat. Res. (Tokyo) 45(4), 557-561 (2004).
59. Mori K, Tani M, Kamata K et al. Mitogen-activated protein kinase, ERK1/2, is essential for the induction of vascular endothelial growth factor by ionizing radiation mediated by activator protein-1 in human glioblastoma cells. Free Radic. Res. 33(2), 157-166 (2000).
60. Brown CK, Khodarev NN, YU J et al. Glioblastoma cells block radiation-induced programmed cell death of endothelial cells. FEBS Lett. 565(1-3), 167-170 (2004).
61. Pelloski CE, Lin E, Zhang L et al. Prognostic associations of activated mitogen-activated protein kinase and akt pathways in glioblastoma. Clin. Cancer Res. 12(13), 3935-3941 (2006).
62. Haas-Kogan DA, Prados MD, Tihan T et al. Epidermal growth factor receptor, protein kinase B/akt, and glioma response to erlotinib. J. Natl Cancer Inst. 97(12), 880-887 (2005).
63. Ichimura K, Schmidt EE, Miyakawa A, Goike HM, Collins VP. Distinct patterns of deletion on 10p and 10q suggest involvement of multiple tumor suppressor genes in the development of astrocytic gliomas of different malignancy grades. Genes Chromosomes Cancer 22(1), 9-15 (1998).
64. Karlbom AE, James CD, Boethius J et al. Loss of heterozygosity in malignant gliomas involves at least three distinct regions on chromosome 10. Hum. Genet. 92(2), 169-174 (1993).
65. Fujisawa H, Reis RM, Nakamura M et al. Loss of heterozygosity on chromosome 10 is more extensive in primary (de novo) than in secondary glioblastomas. Lab. Invest. 80(1), 65-72 (2000).
66. Homma T, Fukushima T, Vaccarella S et al. Correlation among pathology, genotype, and patient outcomes in glioblastoma. J. Neuropathol. Exp. Neurol. 65(9), 846-854 (2006).
67. Tanwar MK, Gilbert MR, Holland EC. Gene expression microarray analysis reveals YKL-40 to be a potential serum marker for malignant character in human glioma. Cancer Res. 62(15), 4364-4368 (2002).
68. Shostak K, Labunskyy V, Dmitrenko V et al. Hc gp-39 gene is upregulated in glioblastomas. Cancer Lett. 198(2), 203-210 (2003).
69. Markert JM, Fuller CM, Gillespie GY et al. Differential gene expression profiling in human brain tumors. Physiol. Genomics 5(1), 21-33 (2001).
70. Lal A, Lash AE, Altschul SF et al. A public database for gene expression in human cancers. Cancer Res. 59(21), 5403-5407 (1999).
71. Nigro JM, Misra A, Zhang L et al. Integrated array-comparative genomic hybridization and expression array profiles identify clinically relevant molecular subtypes of glioblastoma. Cancer Res. 65(5), 1678-1686 (2005).
72. Tso CL, Freije WA, Day A et al. Distinct transcription profiles of primary and secondary glioblastoma subgroups. Cancer Res. 66(1), 159-167 (2006).
73. Colin C, Baeza N, Bartoli C et al. Identification of genes differentially expressed in glioblastoma versus pilocytic astrocytoma using suppression subtractive hybridization. Oncogene 25(19), 2818-2826 (2006).
74. Ling H, Recklies AD. The chitinase 3-like protein human cartilage glycoprotein 39 inhibits cellular responses to the inflammatory cytokines interleukin-1 and tumour necrosis factor-a. Biochem. J. 380(Pt 3), 651-659 (2004).
75. Recklies AD, White C, Ling H. The chitinase 3-like protein human cartilage glycoprotein 39 (hc-gp39) stimulates proliferation of human connective-tissue cells and activates both extracellular signal-regulated kinase-and protein kinase B-mediated signalling pathways. Biochem. J. 365(Pt 1), 119-126 (2002).
76. Pelloski CE, Mahajan A, Maor M et al. YKL-40 expression is associated with poorer response to radiation and shorter overall survival in glioblastoma. Clin. Cancer Res. 11(9), 3326-3334 (2005).
77. Johansen JS, Jensen BV, Roslind A, Nielsen D, Price PA. Serum YKL-40, a new prognostic biomarker in cancer patients? Cancer Epidemiol. Biomarkers Prev. 15(2), 194-202 (2006).
78. Shinojima N, Kochi M, Hamada J et al. The influence of sex and the presence of giant cells on postoperative long-term survival in adult patients with supratentorial glioblastoma multiforme. J. Neurosurg. 101(2), 219-226 (2004).
79. Senger D, Cairncross JG, Forsyth PA. Long-term survivors of glioblastoma: statistical aberration or important unrecognized molecular subtype? Cancer J. 9(3), 214-221 (2003).
80. Krex D, Klink B, Hartmann C et al. Long-term survival with glioblastoma multiforme. Brain 130(Pt 10), 2596-2606 (2007).
81. Burton EC, Lamborn KR, Forsyth P et al. Aberrant p53, mdm2, and proliferation differ in glioblastomas from long-term compared with typical survivors. Clin. Cancer Res. 8(1), 180-187 (2002).
82. Burton EC, Lamborn KR, Feuerstein BG et al. Genetic aberrations defined by comparative genomic hybridization distinguish long-term from typical survivors of glioblastoma. Cancer Res. 62(21), 6205-6210 (2002).
83. Phillips HS, Kharbanda S, Chen R et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9(3), 157-173 (2006).
84. Tso CL, Shintaku P, Chen J et al. Primary glioblastomas express mesenchymal stem-like properties. Mol. Cancer Res. 4(9), 607-619 (2006).
85. Freije WA, Castro-Vargas FE, Fang Z et al. Gene expression profiling of gliomas strongly predicts survival. Cancer Res. 64(18), 6503-6510 (2004).
86. Han SJ, Yang I, Otero JJ et al. Secondary gliosarcoma after diagnosis of glioblastoma: clinical experience with 30 consecutive patients. J. Neurosurg. 112(5), 990-996 (2010).
87. Beaumont TL, Kupsky WJ, Barger GR, Sloan AE. Gliosarcoma with multiple extracranial metastases: case report and review of the literature. J. Neurooncol. 83(1), 39-46 (2007).
88. Thiery JP. Epithelial-mesenchymal transitions in development and pathologies. Curr. Opin. Cell Biol. 15(6), 740-746 (2003).
89. Colman H, Zhang L, Sulman EP et al. A multigene predictor of outcome in glioblastoma. Neuro. Oncol. 12(1), 49-57 (2010).
90. Cairncross JG, Macdonald DR. Successful chemotherapy for recurrent malignant oligodendroglioma. Ann. Neurol. 23(4), 360-364 (1988).
91. Cairncross JG, Macdonald DR, Ramsay DA. Aggressive oligodendroglioma: a chemosensitive tumor. Neurosurgery 31(1), 78-82 (1992).
92. Cairncross G, Macdonald D, Ludwin S et al. Chemotherapy for anaplastic oligodendroglioma. National Cancer Institute of Canada Clinical Trials Group. J. Clin. Oncol. 12(10), 2013-2021 (1994).
93. Cairncross JG, Ueki K, Zlatescu MC et al. Specific genetic predictors of chemotherapeutic response and survival in patients with anaplastic oligodendrogliomas. J. Natl Cancer Inst. 90(19), 1473-1479 (1998).
94. Cairncross G, Berkey B, Shaw E 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. 24(18), 2707-2714 (2006).
95. Van Den Bent MJ, Carpentier AF, Brandes AA 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. 24(18), 2715-2722 (2006).
96. Griffin CA, Burger P, Morsberger L et al. Identification of der(1;19)(q10;p10) in five oligodendrogliomas suggests mechanism of concurrent 1p and 19q loss. J. Neuropathol. Exp. Neurol. 65(10), 988-994 (2006).
97. Jenkins RB, Blair H, Ballman KY et al. A t(1;19)(q10;p10) mediates the combined deletions of 1p and 19q and predicts a better prognosis of patients with oligodendroglioma. Cancer Res. 66(20), 9852-9861 (2006).
98. Kuo LT, Kuo KT, Lee MJ et al. Correlation among pathology, genetic and epigenetic profiles, and clinical outcome in oligodendroglial tumors. Int. J. Cancer 124(12), 2872-2879 (2009).
99. Mollemann M, Wolter M, Felsberg J, Collins VP, Reifenberger G. Frequent promoter hypermethylation and low expression of the MGMT gene in oligodendroglial tumors. Int. J. Cancer 113(3), 379-385 (2005).
100. Parsons DW, Jones S, Zhang X et al. An integrated genomic analysis of human glioblastoma multiforme. Science 321(5897), 1807-1812 (2008).
101. 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. 116(6), 597-602 (2008).
102. Yan H, Parsons DW, Jin G et al. IDH1 and IDH2 mutations in gliomas. N. Engl. J. Med. 360(8), 765-773 (2009).
103. Ichimura K, Pearson DM, Kocialkowski S et al. IDH1 mutations are present in the majority of common adult gliomas but rare in primary glioblastomas. Neuro. Oncol. 11(4), 341-347 (2009).
104. Zhao S, Lin Y, Xu W et al. Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1a. Science 324(5924), 261-265 (2009).
105. Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455(7216), 1061-1068 (2008).
106. Bredel M, Scholtens DM, Harsh GR et al. A network model of a cooperative genetic landscape in brain tumors. JAMA 302(3), 261-275 (2009).
107. Li A, Walling J, Ahn S et al. Unsupervised analysis of transcriptomic profiles reveals six glioma subtypes. Cancer Res. 69(5), 2091-2099 (2009).
108. Verhaak RG, Hoadley KA, Purdom E et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17(1), 98-110 (2010).
109. Sorensen AG, Batchelor TT, Zhang WT et al. A "Vascular normalization index" as potential mechanistic biomarker to predict survival after a single dose of cediranib in recurrent glioblastoma patients. Cancer Res. 69(13), 5296-5300 (2009).
110. Ananthnarayan S, Bahng J, Roring J et al. Time course of imaging changes of GBM during extended bevacizumab treatment. J. Neurooncol. 88(3), 339-347 (2008).
111. Romond EH, Perez EA, Bryant J et al. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N. Engl. J. Med. 353(16), 1673-1684 (2005).