Oligodendroglioma: pathology, molecular mechanisms and markers

Acta Neuropathologica

Volumn 129, Issue 6, 2015, Pages 809-827

  Wesseling, Pieter ^a,b   van den Bent, Martin ^c   Perry, Arie ^d  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ERASMUS MC CANCER INSTITUTE   (Netherlands)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

1p 19q loss; Glioblastoma; Histopathology; Mixed glioma; Molecular marker; Oligodendroglioma

Indexed keywords

ISOCITRATE DEHYDROGENASE 1; ISOCITRATE DEHYDROGENASE 2; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; VASCULOTROPIN RECEPTOR; TUMOR MARKER;

AGGRESSION; ASTROCYTE; ASTROCYTOMA; CHROMOSOME 19Q; CHROMOSOME 1P; CHROMOSOME 7; FOLLOW UP; GENE MUTATION; GENETIC HETEROGENEITY; GLIA CELL; HISTOPATHOLOGY; HUMAN; NEURAL STEM CELL; OLIGODENDROGLIA; OLIGODENDROGLIOMA; PATHOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; TUMOR CLASSIFICATION; TUMOR DIAGNOSIS; WORLD HEALTH ORGANIZATION; BRAIN NEOPLASMS; GENETICS; METABOLISM; PATHOLOGY;

BIOMARKERS, TUMOR; BRAIN NEOPLASMS; HUMANS; OLIGODENDROGLIOMA;

EID: 84929707126     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-015-1424-1     Document Type: Review

References (136)

1. Agnihotri S, Aldape KD, Zadeh G (2014) Isocitrate dehydrogenase status and molecular subclasses of glioma and glioblastoma. Neurosurg Focus 37:E13. doi:10.3171/2014.9.FOCUS14505
2. Aldape K, Burger PC, Perry A (2007) Clinicopathologic aspects of 1p/19q loss and the diagnosis of oligodendroglioma. Arch Pathol Lab Med 131:242–251. doi:10.1043/1543-2165(2007)131[242:CAOQLA]2.0.CO;2
3. Appin CL, Brat DJ (2015) Molecular pathways in gliomagenesis and their relevance to neuropathologic diagnosis. Adv Anat Pathol 22:50–58. doi:10.1097/PAP.0000000000000048
4. Appin CL, Gao J, Chisolm C, Torian M, Alexis D, Vincentelli C, Schniederjan MJ, Hadjipanayis C, Olson JJ, Hunter S et al (2013) Glioblastoma with oligodendroglioma component (GBM-O): molecular genetic and clinical characteristics. Brain Pathol 23:454–461. doi:10.1111/bpa.12018
5. Arita H, Narita Y, Fukushima S, Tateishi K, Matsushita Y, Yoshida A, Miyakita Y, Ohno M, Collins VP, Kawahara N et al (2013) Upregulating mutations in the TERT promoter commonly occur in adult malignant gliomas and are strongly associated with total 1p19q loss. Acta Neuropathol 126:267–276. doi:10.1007/s00401-013-1141-6
6. Bady P, Sciuscio D, Diserens AC, Bloch J, van den Bent MJ, Marosi C, Dietrich PY, Weller M, Mariani L, Heppner FL et al (2012) MGMT methylation analysis of glioblastoma on the infinium methylation BeadChip identifies two distinct CpG regions associated with gene silencing and outcome, yielding a prediction model for comparisons across datasets, tumor grades, and CIMP-status. Acta Neuropathol 124:547–560. doi:10.1007/s00401-012-1016-2
7. Baily P, Bucy PC (1929) Oligodendrogliomas of the brain. J Pathol Bacteriol 32:735–751
8. Barresi V, Mondello S, Branca G, Rajan TS, Vitarelli E, Tuccari G (2014) p-CREB expression in human gliomas: potential use in the differential diagnosis between astrocytoma and oligodendroglioma. Hum Pathol. doi:10.1016/j.humpath.2014.10.011
9. Best MG, Sol N, Zijl S, Reijneveld JC, Wesseling P, Wurdinger T (2015) Liquid biopsies in patients with diffuse glioma. Acta Neuropathol. doi:10.1007/s00401-015-1399-y
10. Bettegowda C, Agrawal N, Jiao Y, Sausen M, Wood LD, Hruban RH, Rodriguez FJ, Cahill DP, McLendon R, Riggins G et al (2011) Mutations in CIC and FUBP1 contribute to human oligodendroglioma. Science 333:1453–1455. doi:10.1126/science.1210557
11. Bigner SH, Matthews MR, Rasheed BK, Wiltshire RN, Friedman HS, Friedman AH, Stenzel TT, Dawes DM, McLendon RE, Bigner DD (1999) Molecular genetic aspects of oligodendrogliomas including analysis by comparative genomic hybridization. Am J Pathol 155:375–386. doi:10.1016/S0002-9440(10)65134-6
12. Brat DJ, Verhaak, R.G.W., Aldape, K.D. et al. (2015) Comprehensive, integrative genomic analysis of diffuse lower grade gliomas. N Engl J Med (in press)
13. Broderick DK, Di C, Parrett TJ, Samuels YR, Cummins JM, McLendon RE, Fults DW, Velculescu VE, Bigner DD, Yan H (2004) Mutations of PIK3CA in anaplastic oligodendrogliomas, high-grade astrocytomas, and medulloblastomas. Cancer Res 64:5048–5050. doi:10.1158/0008-5472.CAN-04-1170
14. Buckley PG, Alcock L, Heffernan J, Woods J, Brett F, Stallings RL, Farrell MA (2011) Loss of chromosome 1p/19q in oligodendroglial tumors: refinement of chromosomal critical regions and evaluation of internexin immunostaining as a surrogate marker. J Neuropathol Exp Neurol 70:177–182. doi:10.1097/NEN.0b013e31820c765b
15. Bunse L, Schumacher T, Sahm F, Pusch S, Oezen I, Rauschenbach K, Gonzalez M, Solecki G, Osswald M, Capper D et al (2015) Proximity ligation assay evaluates IDH1R132H presentation in gliomas. J Clin Investig 125:1–14. doi:10.1172/JCI77780
16. Burger PC (2002) What is an oligodendroglioma? Brain Pathol 12:257–259
17. Burnet NG, Jefferies SJ, Benson RJ, Hunt DP, Treasure FP (2005) Years of life lost (YLL) from cancer is an important measure of population burden—and should be considered when allocating research funds. Br J Cancer 92:241–245. doi:10.1038/sj.bjc.6602321
18. Cairncross G, Wang M, Shaw E, Jenkins R, Brachman D, Buckner J, Fink K, Souhami L, Laperriere N, Curran W et al (2013) Phase III trial of chemoradiotherapy for anaplastic oligodendroglioma: long-term results of RTOG 9402. J Clin Oncol Off J Am Soc Clin Oncol 31:337–343. doi:10.1200/JCO.2012.43.2674
19. Cairncross JG, Ueki K, Zlatescu MC, Lisle DK, Finkelstein DM, Hammond RR, Silver JS, Stark PC, Macdonald DR, Ino Y et al (1998) Specific genetic predictors of chemotherapeutic response and survival in patients with anaplastic oligodendrogliomas. J Natl Cancer Inst 90:1473–1479
20. Cairncross JG, Wang M, Jenkins RB, Shaw EG, Giannini C, Brachman DG, Buckner JC, Fink KL, Souhami L, Laperriere NJ et al (2014) Benefit from procarbazine, lomustine, and vincristine in oligodendroglial tumors is associated with mutation of IDH. J Clin Oncol Off J Am Soc Clin Oncol 32:783–790. doi:10.1200/JCO.2013.49.3726
21. Capper D, Reuss D, Schittenhelm J, Hartmann C, Bremer J, Sahm F, Harter PN, Jeibmann A, von Deimling A (2011) Mutation-specific IDH1 antibody differentiates oligodendrogliomas and oligoastrocytomas from other brain tumors with oligodendroglioma-like morphology. Acta Neuropathol 121:241–252. doi:10.1007/s00401-010-0770-2
22. Ciriello G, Miller ML, Aksoy BA, Senbabaoglu Y, Schultz N, Sander C (2013) Emerging landscape of oncogenic signatures across human cancers. Nat Genet 45:1127–1133. doi:10.1038/ng.2762
23. Claes A, Idema AJ, Wesseling P (2007) Diffuse glioma growth: a guerilla war. Acta Neuropathol 114:443–458. doi:10.1007/s00401-007-0293-7
24. Donahue B, Scott CB, Nelson JS, Rotman M, Murray KJ, Nelson DF, Banker FL, Earle JD, Fischbach JA, Asbell SO et al (1997) Influence of an oligodendroglial component on the survival of patients with anaplastic astrocytomas: a report of Radiation Therapy Oncology Group 83-02. Int J Radiat Oncol Biol Phys 38:911–914
25. Ducray F, Idbaih A, de Reynies A, Bieche I, Thillet J, Mokhtari K, Lair S, Marie Y, Paris S, Vidaud M et al (2008) Anaplastic oligodendrogliomas with 1p19q codeletion have a proneural gene expression profile. Mol cancer 7:41. doi:10.1186/1476-4598-7-41
26. Ducray F, Mokhtari K, Criniere E, Idbaih A, Marie Y, Dehais C, Paris S, Carpentier C, Dieme MJ, Adam C et al (2011) Diagnostic and prognostic value of alpha internexin expression in a series of 409 gliomas. Eur J Cancer 47:802–808. doi:10.1016/j.ejca.2010.11.031
27. Eigenbrod S, Roeber S, Thon N, Giese A, Krieger A, Grasbon-Frodl E, Egensperger R, Tonn JC, Kreth FW, Kretzschmar HA (2011) alpha-Internexin in the diagnosis of oligodendroglial tumors and association with 1p/19q status. J Neuropathol Exp Neurol 70:970–978. doi:10.1097/NEN.0b013e3182333ef5
28. Ellingson BM, Lai A, Harris RJ, Selfridge JM, Yong WH, Das K, Pope WB, Nghiemphu PL, Vinters HV, Liau LM et al (2013) Probabilistic radiographic atlas of glioblastoma phenotypes. Am J Neuroradiol 34:533–540. doi:10.3174/ajnr.A3253
29. Elmahdi A, Frary AJ, Scotton WJ, O’Donovan DG, Price SJ (2013) Glioblastomas with oligodendroglial component have the same clinical phenotype as classical glioblastomas. Br J Neurosurg 27:419–424. doi:10.3109/02688697.2013.767315
30. Esmaeili M, Hamans BC, Navis AC, van Horssen R, Bathen TF, Gribbestad IS, Leenders WP, Heerschap A (2014) IDH1 R132H mutation generates a distinct phospholipid metabolite profile in glioma. Cancer Res 74:4898–4907. doi:10.1158/0008-5472.CAN-14-0008
31. Fallon KB, Palmer CA, Roth KA, Nabors LB, Wang W, Carpenter M, Banerjee R, Forsyth P, Rich K, Perry A (2004) Prognostic value of 1p, 19q, 9p, 10q, and EGFR–FISH analyses in recurrent oligodendrogliomas. J Neuropathol Exp Neurol 63:314–322
32. Figarella-Branger D, Mokhtari K, Colin C, Uro-Coste E, Jouvet A, Dehais C, Carpentier C, Villa C, Maurage C, Eimer S et al (2014) Prognostic relevance of histomolecular classification of diffuse adult high-grade gliomas with necrosis. Brain Pathol. doi:10.1111/bpa.12227
33. Figarella-Branger D, Mokhtari K, Dehais C, Jouvet A, Uro-Coste E, Colin C, Carpentier C, Forest F, Maurage CA, Vignaud JM et al (2014) Mitotic index, microvascular proliferation, and necrosis define 3 groups of 1p/19q codeleted anaplastic oligodendrogliomas associated with different genomic alterations. Neuro oncol 16:1244–1254. doi:10.1093/neuonc/nou047
34. Gajjar A, Pfister SM, Taylor MD, Gilbertson RJ (2014) Molecular insights into pediatric brain tumors have the potential to transform therapy. Clin Cancer Res Off J Am Assoc Cancer Res 20:5630–5640. doi:10.1158/1078-0432.CCR-14-0833
35. Giannini C, Burger PC, Berkey BA, Cairncross JG, Jenkins RB, Mehta M, Curran WJ, Aldape K (2008) Anaplastic oligodendroglial tumors: refining the correlation among histopathology, 1p 19q deletion and clinical outcome in Intergroup Radiation Therapy Oncology Group Trial 9402. Brain Pathol 18:360–369. doi:10.1111/j.1750-3639.2008.00129.x
36. Giannini C, Scheithauer BW, Weaver AL, Burger PC, Kros JM, Mork S, Graeber MB, Bauserman S, Buckner JC, Burton J et al (2001) Oligodendrogliomas: reproducibility and prognostic value of histologic diagnosis and grading. J Neuropathol Exp Neurol 60:248–262
37. Goodenberger ML, Jenkins RB (2012) Genetics of adult glioma. Cancer Genet 205:613–621. doi:10.1016/j.cancergen.2012.10.009
38. Griffin CA, Burger P, Morsberger L, Yonescu R, Swierczynski S, Weingart JD, Murphy KM (2006) Identification of der(1;19)(q10;p10) in five oligodendrogliomas suggests mechanism of concurrent 1p and 19q loss. J Neuropathol Exp Neurol 65:988–994. doi:10.1097/01.jnen.0000235122.98052.8f
39. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70
40. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674. doi:10.1016/j.cell.2011.02.013
41. Hartmann C, Hentschel B, Wick W, Capper D, Felsberg J, Simon M, Westphal M, Schackert G, Meyermann R, Pietsch T et al (2010) 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 120:707–718. doi:10.1007/s00401-010-0781-z
42. Heath JA, Ng J, Beshay V, Coleman L, Lo P, Amor DJ (2013) Anaplastic oligodendroglioma in an adolescent with Lynch syndrome. Pediatr Blood Cancer 60:E13–E15. doi:10.1002/pbc.24424
43. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L et al (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003. doi:10.1056/NEJMoa043331
44. Hegi ME, Janzer RC, Lambiv WL, Gorlia T, Kouwenhoven MC, Hartmann C, von Deimling A, Martinet D, Besuchet Schmutz N, Diserens AC et al (2012) Presence of an oligodendroglioma-like component in newly diagnosed glioblastoma identifies a pathogenetically heterogeneous subgroup and lacks prognostic value: central pathology review of the EORTC_26981/NCIC_CE.3 trial. Acta Neuropathol 123:841–852. doi:10.1007/s00401-011-0938-4
45. Horbinski C (2013) What do we know about IDH1/2 mutations so far, and how do we use it? Acta Neuropathol 125:621–636. doi:10.1007/s00401-013-1106-9
46. Huse JT, Diamond EL, Wang L, Rosenblum MK (2015) Mixed glioma with molecular features of composite oligodendroglioma and astrocytoma: a true “oligoastrocytoma”? Acta Neuropathol 129:151–153. doi:10.1007/s00401-014-1359-y
47. Idbaih A, Marie Y, Pierron G, Brennetot C, Hoang-Xuan K, Kujas M, Mokhtari K, Sanson M, Lejeune J, Aurias A et al (2005) Two types of chromosome 1p losses with opposite significance in gliomas. Ann Neurol 58:483–487. doi:10.1002/ana.20607
48. Jenkins RB, Blair H, Ballman KV, Giannini C, Arusell RM, Law M, Flynn H, Passe S, Felten S, Brown PD et al (2006) 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 66:9852–9861. doi:10.1158/0008-5472.CAN-06-1796
49. Jeuken J, Cornelissen S, Boots-Sprenger S, Gijsen S, Wesseling P (2006) Multiplex ligation-dependent probe amplification: a diagnostic tool for simultaneous identification of different genetic markers in glial tumors. J Mol Diagn 8:433–443. doi:10.2353/jmoldx.2006.060012
50. Jeuken JW, Cornelissen SJ, Vriezen M, Dekkers MM, Errami A, Sijben A, Boots-Sprenger SH, Wesseling P (2007) MS-MLPA: an attractive alternative laboratory assay for robust, reliable, and semiquantitative detection of MGMT promoter hypermethylation in gliomas. Lab Investig J Tech Methods Pathol 87:1055–1065. doi:10.1038/labinvest.3700664
51. Jeuken JW, Sprenger SH, Boerman RH, von Deimling A, Teepen HL, van Overbeeke JJ, Wesseling P (2001) Subtyping of oligo-astrocytic tumours by comparative genomic hybridization. J Pathol 194:81–87. doi:10.1002/path.837
52. Jeuken JW, Sprenger SH, Wesseling P, Macville MV, von Deimling A, Teepen HL, van Overbeeke JJ, Boerman RH (1999) Identification of subgroups of high-grade oligodendroglial tumors by comparative genomic hybridization. J Neuropathol Exp Neurol 58:606–612
53. Jiang H, Ren X, Cui X, Wang J, Jia W, Zhou Z, Lin S (2013) 1p/19q codeletion and IDH1/2 mutation identified a subtype of anaplastic oligoastrocytomas with prognosis as favorable as anaplastic oligodendrogliomas. Neuro Oncol 15:775–782. doi:10.1093/neuonc/not027
54. Jiao Y, Killela PJ, Reitman ZJ, Rasheed AB, Heaphy CM, de Wilde RF, Rodriguez FJ, Rosemberg S, Oba-Shinjo SM, Nagahashi Marie SK et al (2012) Frequent ATRX, CIC, FUBP1 and IDH1 mutations refine the classification of malignant gliomas. Oncotarget 3:709–722
55. Johnson BE, Mazor T, Hong C, Barnes M, Aihara K, McLean CY, Fouse SD, Yamamoto S, Ueda H, Tatsuno K et al (2014) Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science 343:189–193. doi:10.1126/science.1239947
56. Joseph NM, Phillips J, Dahiya S, Felicella M, Tihan T, Brat DJ, Perry A (2013) Diagnostic implications of IDH1-R132H and OLIG2 expression patterns in rare and challenging glioblastoma variants. Mod Pathol Off J US Can Acad Pathol. doi:10.1038/modpathol.2012.173
57. Kalinina J, Carroll A, Wang L, Yu Q, Mancheno DE, Wu S, Liu F, Ahn J, He M, Mao H et al (2012) Detection of “oncometabolite” 2-hydroxyglutarate by magnetic resonance analysis as a biomarker of IDH1/2 mutations in glioma. J Mol Med (Berl) 90:1161–1171. doi:10.1007/s00109-012-0888-x
58. Kannan K, Inagaki A, Silber J, Gorovets D, Zhang J, Kastenhuber ER, Heguy A, Petrini JH, Chan TA, Huse JT (2012) Whole-exome sequencing identifies ATRX mutation as a key molecular determinant in lower-grade glioma. Oncotarget 3:1194–1203
59. Killela PJ, Reitman ZJ, Jiao Y, Bettegowda C, Agrawal N, Diaz LA Jr, Friedman AH, Friedman H, Gallia GL, Giovanella BC et al (2013) TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. Proc Natl Acad Sci USA 110:6021–6026. doi:10.1073/pnas.1303607110
60. Kleihues P, Cavenee WK (2000) Pathology and genetics of tumours of the nervous system: World Health Organization classification of tumours. IARC Press, Lyon
61. Koeller KK, Rushing EJ (2005) From the archives of the AFIP: oligodendroglioma and its variants: radiologic-pathologic correlation. Radiogr Rev Publ Radiol Soc N Am 25:1669–1688. doi:10.1148/rg.256055137
62. Koelsche C, Sahm F, Capper D, Reuss D, Sturm D, Jones DT, Kool M, Northcott PA, Wiestler B, Bohmer K et al (2013) Distribution of TERT promoter mutations in pediatric and adult tumors of the nervous system. Acta Neuropathol 126:907–915. doi:10.1007/s00401-013-1195-5
63. Kreiger PA, Okada Y, Simon S, Rorke LB, Louis DN, Golden JA (2005) Losses of chromosomes 1p and 19q are rare in pediatric oligodendrogliomas. Acta Neuropathol 109:387–392. doi:10.1007/s00401-004-0976-2
64. Kros JM (2011) Grading of gliomas: the road from eminence to evidence. J Neuropathol Exp Neurol 70:101–109. doi:10.1097/NEN.0b013e31820681aa
65. Kros JM, Gorlia T, Kouwenhoven MC, Zheng PP, Collins VP, Figarella-Branger D, Giangaspero F, Giannini C, Mokhtari K, Mork SJ et al (2007) Panel review of anaplastic oligodendroglioma from European Organization For Research and Treatment of Cancer Trial 26951: assessment of consensus in diagnosis, influence of 1p/19q loss, and correlations with outcome. J Neuropathol Exp Neurol 66:545–551. doi:10.1097/01.jnen.0000263869.84188.72
66. Kros JM, Mustafa DM, Dekker LJ, Sillevis Smitt PA, Luider TM, Zheng PP (2014) Circulating glioma biomarkers. Neuro Oncol. doi:10.1093/neuonc/nou207
67. Kros JM, Troost D, van Eden CG, van der Werf AJ, Uylings HB (1988) Oligodendroglioma. A comparison of two grading systems. Cancer 61:2251–2259
68. Kros JM, van den Brink WA, van Loon-van Luyt JJ, Stefanko SZ (1997) Signet-ring cell oligodendroglioma—report of two cases and discussion of the differential diagnosis. Acta Neuropathol 93:638–643
69. Kros JM, Van Eden CG, Stefanko SZ, Waayer-Van Batenburg M, van der Kwast TH (1990) Prognostic implications of glial fibrillary acidic protein containing cell types in oligodendrogliomas. Cancer 66:1204–1212
70. Labussiere M, Di Stefano AL, Gleize V, Boisselier B, Giry M, Mangesius S, Bruno A, Paterra R, Marie Y, Rahimian A et al (2014) TERT promoter mutations in gliomas, genetic associations and clinico-pathological correlations. Br J Cancer 111:2024–2032. doi:10.1038/bjc.2014.538
71. Li G, Zhang Z, Zhang J, Jin T, Liang H, Gong L, Cui G, Yang H, He S, Zhang Y et al (2014) Occipital anaplastic oligodendroglioma with multiple organ metastases after a short clinical course: a case report and literature review. Diagn Pathol 9:17. doi:10.1186/1746-1596-9-17
72. Ligon KL, Alberta JA, Kho AT, Weiss J, Kwaan MR, Nutt CL, Louis DN, Stiles CD, Rowitch DH (2004) The oligodendroglial lineage marker OLIG2 is universally expressed in diffuse gliomas. J Neuropathol Exp Neurol 63:499–509
73. Louis DN, Ohgaki H, Wiestler O, Cavenee WK (2007) WHO classification of tumours of the central nervous system. IARC Press, Lyon
74. Louis DN, Perry A, Burger P, Ellison DW, Reifenberger G, von Deimling A, Aldape K, Brat D, Collins VP, Eberhart C et al (2014) International society of neuropathology-haarlem consensus guidelines for nervous system tumor classification and grading. Brain Pathol 24:429–435. doi:10.1111/bpa.12171
75. Lu C, Ward PS, Kapoor GS, Rohle D, Turcan S, Abdel-Wahab O, Edwards CR, Khanin R, Figueroa ME, Melnick A et al (2012) IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature 483:474–478. doi:10.1038/nature10860
76. Maintz D, Fiedler K, Koopmann J, Rollbrocker B, Nechev S, Lenartz D, Stangl AP, Louis DN, Schramm J, Wiestler OD et al (1997) Molecular genetic evidence for subtypes of oligoastrocytomas. J Neuropathol Exp Neurol 56:1098–1104
77. Malley DS, Hamoudi RA, Kocialkowski S, Pearson DM, Collins VP, Ichimura K (2011) A distinct region of the MGMT CpG island critical for transcriptional regulation is preferentially methylated in glioblastoma cells and xenografts. Acta Neuropathol 121:651–661. doi:10.1007/s00401-011-0803-5
78. Mazza E, Belli C, Terreni M, Doglioni C, Losio C, Cantore M, Mambrini A, Reni M (2013) Breast metastases from oligodendroglioma: an unusual extraneural spread in two young women and a review of the literature. Crit Rev Oncol Hematol 88:564–572. doi:10.1016/j.critrevonc.2013.07.010
79. Michotte A, Chaskis C, Sadones J, Veld PI, Neyns B (2009) Primary leptomeningeal anaplastic oligodendroglioma with a 1p36-19q13 deletion: report of a unique case successfully treated with Temozolomide. J Neurol Sci 287:267–270. doi:10.1016/j.jns.2009.08.047
80. Miller CR, Dunham CP, Scheithauer BW, Perry A (2006) Significance of necrosis in grading of oligodendroglial neoplasms: a clinicopathologic and genetic study of newly diagnosed high-grade gliomas. J Clin Oncol Off J Am Soc Clin Oncol 24:5419–5426. doi:10.1200/JCO.2006.08.1497
81. Miller CR, Perry A (2007) Glioblastoma. Arch Pathol Lab Med 131:397–406. doi:10.1043/1543-2165(2007)131[397:G]2.0.CO;2
82. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, Pan F, Pelloski CE, Sulman EP, Bhat KP et al (2010) Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17:510–522. doi:10.1016/j.ccr.2010.03.017
83. Ohgaki H, Kleihues P (2013) The definition of primary and secondary glioblastoma. Clin Cancer Res Off J Am Assoc Cancer Res 19:764–772. doi:10.1158/1078-0432.CCR-12-3002
84. Olar A, Wani KM, Alfaro-Munoz KD, Heathcock LE, van Thuijl HF, Gilbert MR, Armstrong TS, Sulman EP, Cahill DP, Vera-Bolanos E et al (2015) IDH mutation status and role of WHO grade and mitotic index in overall survival in grade II–III diffuse gliomas. Acta Neuropathol. doi:10.1007/s00401-015-1398-z
85. Ostrom QT, Gittleman H, Liao P, Rouse C, Chen Y, Dowling J, Wolinsky Y, Kruchko C, Barnholtz-Sloan J (2014) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2007-2011. Neuro Oncol 16(Suppl 4):1–63. doi:10.1093/neuonc/nou223
86. Otero JJ, Rowitch D, Vandenberg S (2011) OLIG2 is differentially expressed in pediatric astrocytic and in ependymal neoplasms. J Neurooncol 104:423–438. doi:10.1007/s11060-010-0509-x
87. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL et al (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321:1807–1812. doi:10.1126/science.1164382
88. Patel AP, Tirosh I, Trombetta JJ, Shalek AK, Gillespie SM, Wakimoto H, Cahill DP, Nahed BV, Curry WT, Martuza RL et al (2014) Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 344:1396–1401. doi:10.1126/science.1254257
89. Perry A (2001) Oligodendroglial neoplasms: current concepts, misconceptions, and folklore. Adv Anat Pathol 8:183–199
90. Perry A, Aldape KD, George DH, Burger PC (2004) Small cell astrocytoma: an aggressive variant that is clinicopathologically and genetically distinct from anaplastic oligodendroglioma. Cancer 101:2318–2326. doi:10.1002/cncr.20625
91. Perry A, Burton SS, Fuller GN, Robinson CA, Palmer CA, Resch L, Bigio EH, Gujrati M, Rosenblum MK (2010) Oligodendroglial neoplasms with ganglioglioma-like maturation: a diagnostic pitfall. Acta Neuropathol 120:237–252. doi:10.1007/s00401-010-0695-9
92. Perry A, Scheithauer BW, Macaulay RJ, Raffel C, Roth KA, Kros JM (2002) Oligodendrogliomas with neurocytic differentiation. A report of four cases with diagnostic and histogenetic implications. J Neuropathol Exp Neurol 61:947–955
93. Preusser M, Budka H, Rossler K, Hainfellner JA (2007) OLIG2 is a useful immunohistochemical marker in differential diagnosis of clear cell primary CNS neoplasms. Histopathology 50:365–370. doi:10.1111/j.1365-2559.2007.02614.x
94. Preusser M, Charles Janzer R, Felsberg J, Reifenberger G, Hamou MF, Diserens AC, Stupp R, Gorlia T, Marosi C, Heinzl H et al (2008) Anti-O6-methylguanine-methyltransferase (MGMT) immunohistochemistry in glioblastoma multiforme: observer variability and lack of association with patient survival impede its use as clinical biomarker. Brain Pathol 18:520–532. doi:10.1111/j.1750-3639.2008.00153.x
95. Reifenberger J, Reifenberger G, Liu L, James CD, Wechsler W, Collins VP (1994) Molecular genetic analysis of oligodendroglial tumors shows preferential allelic deletions on 19q and 1p. Am J Pathol 145:1175–1190
96. Reuss DE, Sahm F, Schrimpf D, Wiestler B, Capper D, Koelsche C, Schweizer L, Korshunov A, Jones DT, Hovestadt V et al (2015) ATRX and IDH1-R132H immunohistochemistry with subsequent copy number analysis and IDH sequencing as a basis for an “integrated” diagnostic approach for adult astrocytoma, oligodendroglioma and glioblastoma. Acta Neuropathol 129:133–146. doi:10.1007/s00401-014-1370-3
97. Reynolds RM, Boswell E, Hulette CM, Cummings TJ, Haglund MM, Boswell E, Hulette CM, Cumm Ings TJ, Haglund MM (2011) Sudden death from diffuse leptomeningeal oligodendrogliomatosis. J Neurosurg Spine 15:625–629. doi:10.3171/2011.7.SPINE10728
98. Riemenschneider MJ, Jeuken JW, Wesseling P, Reifenberger G (2010) Molecular diagnostics of gliomas: state of the art. Acta Neuropathol 120:567–584. doi:10.1007/s00401-010-0736-4
99. Riemenschneider MJ, Louis DN, Weller M, Hau P (2013) Refined brain tumor diagnostics and stratified therapies: the requirement for a multidisciplinary approach. Acta Neuropathol 126:21–37. doi:10.1007/s00401-013-1127-4
100. Rodriguez FJ, Perry A, Rosenblum MK, Krawitz S, Cohen KJ, Lin D, Mosier S, Lin MT, Eberhart CG, Burger PC (2012) Disseminated oligodendroglial-like leptomeningeal tumor of childhood: a distinctive clinicopathologic entity. Acta Neuropathol 124:627–641. doi:10.1007/s00401-012-1037-x
101. Rodriguez FJ, Schniederjan MJ, Nicolaides T, Tihan T, Burger PC, Perry A (2015) High rate of concurrent BRAF-KIAA1549 gene fusion and 1p deletion in disseminated oligodendroglioma-like leptomeningeal neoplasms (DOLN). Acta Neuropathol. doi:10.1007/s00401-015-1400-9
102. Rodriguez FJ, Tihan T, Lin D, McDonald W, Nigro J, Feuerstein B, Jackson S, Cohen K, Burger PC (2014) Clinicopathologic features of pediatric oligodendrogliomas: a series of 50 patients. Am J Surg Pathol 38:1058–1070. doi:10.1097/PAS.0000000000000221
103. Sahm F, Koelsche C, Meyer J, Pusch S, Lindenberg K, Mueller W, Herold-Mende C, von Deimling A, Hartmann C (2012) CIC and FUBP1 mutations in oligodendrogliomas, oligoastrocytomas and astrocytomas. Acta Neuropathol 123:853–860. doi:10.1007/s00401-012-0993-5
104. Sahm F, Reuss D, Koelsche C, Capper D, Schittenhelm J, Heim S, Jones DT, Pfister SM, Herold-Mende C, Wick W et al (2014) Farewell to oligoastrocytoma: in situ molecular genetics favor classification as either oligodendroglioma or astrocytoma. Acta Neuropathol 128:551–559. doi:10.1007/s00401-014-1326-7
105. Sahm F, von Deimling A (2015) Farewell to oligoastrocytoma: response to letters. Acta Neuropathol 129:155. doi:10.1007/s00401-014-1366-z
106. Schumacher T, Bunse L, Pusch S, Sahm F, Wiestler B, Quandt J, Menn O, Osswald M, Oezen I, Ott M et al (2014) A vaccine targeting mutant IDH1 induces antitumour immunity. Nature 512:324–327. doi:10.1038/nature13387
107. Smith SF, Simpson JM, Brewer JA, Sekhon LH, Biggs MT, Cook RJ, Little NS (2006) The presence of necrosis and/or microvascular proliferation does not influence survival of patients with anaplastic oligodendroglial tumours: review of 98 patients. J Neurooncol 80:75–82. doi:10.1007/s11060-006-9158-5
108. Snuderl M, Eichler AF, Ligon KL, Vu QU, Silver M, Betensky RA, Ligon AH, Wen PY, Louis DN, Iafrate AJ (2009) Polysomy for chromosomes 1 and 19 predicts earlier recurrence in anaplastic oligodendrogliomas with concurrent 1p/19q loss. Clin Cancer Res Off J Am Assoc Cancer Res 15:6430–6437. doi:10.1158/1078-0432.CCR-09-0867
109. Sottoriva A, Spiteri I, Piccirillo SG, Touloumis A, Collins VP, Marioni JC, Curtis C, Watts C, Tavare S (2013) Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci USA 110:4009–4014. doi:10.1073/pnas.1219747110
110. Sturm D, Witt H, Hovestadt V, Khuong-Quang DA, Jones DT, Konermann C, Pfaff E, Tonjes M, Sill M, Bender S et al (2012) Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 22:425–437. doi:10.1016/j.ccr.2012.08.024
111. Suri V, Jha P, Agarwal S, Pathak P, Sharma MC, Sharma V, Shukla S, Somasundaram K, Mahapatra AK, Kale SS et al (2011) Molecular profile of oligodendrogliomas in young patients. Neuro oncol 13:1099–1106. doi:10.1093/neuonc/nor146
112. Takami H, Yoshida A, Fukushima S, Arita H, Matsushita Y, Nakamura T, Ohno M, Miyakita Y, Shibui S, Narita Y et al (2014) Revisiting TP53 mutations and immunohistochemistry-A comparative study in 157 diffuse gliomas. Brain Pathol. doi:10.1111/bpa.12173
113. Takei H, Yogeswaren ST, Wong KK, Mehta V, Chintagumpala M, Dauser RC, Lau CC, Adesina AM (2008) Expression of oligodendroglial differentiation markers in pilocytic astrocytomas identifies two clinical subsets and shows a significant correlation with proliferation index and progression free survival. J Neurooncol 86:183–190. doi:10.1007/s11060-007-9455-7
114. Takeuchi H, Kubota T, Kitai R, Matsuda K, Hashimoto N, Sato K (2009) Chromosome 1p and 19q deletions in malignant glioneuronal tumors with oligodendroglioma-like component. J Neurooncol 91:33–38. doi:10.1007/s11060-008-9690-6
115. Tanaka Y, Nobusawa S, Yagi S, Ikota H, Yokoo H, Nakazato Y (2012) Anaplastic oligodendroglioma with ganglioglioma-like maturation. Brain Tumor Pathol 29:221–228. doi:10.1007/s10014-011-0078-5
116. Turcan S, Rohle D, Goenka A, Walsh LA, Fang F, Yilmaz E, Campos C, Fabius AW, Lu C, Ward PS et al (2012) IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 483:479–483. doi:10.1038/nature10866
117. van den Bent MJ (2010) Interobserver variation of the histopathological diagnosis in clinical trials on glioma: a clinician’s perspective. Acta Neuropathol 120:297–304. doi:10.1007/s00401-010-0725-7
118. van den Bent MJ, Brandes AA, Taphoorn MJ, Kros JM, Kouwenhoven MC, Delattre JY, Bernsen HJ, Frenay M, Tijssen CC, Grisold W et al (2013) Adjuvant procarbazine, lomustine, and vincristine chemotherapy in newly diagnosed anaplastic oligodendroglioma: long-term follow-up of EORTC brain tumor group study 26951. J Clin Oncol Off J Am Soc Clin Oncol 31:344–350. doi:10.1200/JCO.2012.43.2229
119. van den Bent MJ, Carpentier AF, Brandes AA, Sanson M, Taphoorn MJ, Bernsen HJ, Frenay M, Tijssen CC, Grisold W, Sipos L et al (2006) 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 Off J Am Soc Clin Oncol 24:2715–2722. doi:10.1200/JCO.2005.04.6078
120. van den Bent MJ, Dubbink HJ, Sanson M, van der Lee-Haarloo CR, Hegi M, Jeuken JW, Ibdaih A, Brandes AA, Taphoorn MJ, Frenay M et al (2009) MGMT promoter methylation is prognostic but not predictive for outcome to adjuvant PCV chemotherapy in anaplastic oligodendroglial tumors: a report from EORTC Brain Tumor Group Study 26951. J Clin Oncol Off J Am Soc Clin Oncol 27:5881–5886. doi:10.1200/JCO.2009.24.1034
121. van den Bent MJ, Erdem-Eraslan L, Idbaih A, de Rooi J, Eilers PH, Spliet WG, den Dunnen WF, Tijssen C, Wesseling P, Sillevis Smitt PA et al (2013) MGMT-STP27 methylation status as predictive marker for response to PCV in anaplastic oligodendrogliomas and oligoastrocytomas. A report from EORTC study 26951. Clin Cancer Res Off J Am Assoc Cancer Res 19:5513–5522. doi:10.1158/1078-0432.CCR-13-1157
122. van Thuijl HF, Scheinin I, Sie D, Alentorn A, van Essen HF, Cordes M, Fleischeuer R, Gijtenbeek AM, Beute G, van den Brink WA et al (2014) Spatial and temporal evolution of distal 10q deletion, a prognostically unfavorable event in diffuse low-grade gliomas. Genome Biol 15:471. doi:10.1186/s13059-014-0471-6
123. Vyberg M, Ulhoi BP, Teglbjaerg PS (2007) Neuronal features of oligodendrogliomas—an ultrastructural and immunohistochemical study. Histopathology 50:887–896. doi:10.1111/j.1365-2559.2007.02686.x
124. Wang XW, Ciccarino P, Rossetto M, Boisselier B, Marie Y, Desestret V, Gleize V, Mokhtari K, Sanson M, Labussiere M (2014) IDH mutations: genotype-phenotype correlation and prognostic impact. BioMed Res Int 2014:540236. doi:10.1155/2014/540236
125. Watanabe T, Nobusawa S, Kleihues P, Ohgaki H (2009) IDH1 mutations are early events in the development of astrocytomas and oligodendrogliomas. Am J Pathol 174:1149–1153. doi:10.2353/ajpath.2009.080958
126. Weller M, Wick W (2014) Neuro-oncology in 2013: improving outcome in newly diagnosed malignant glioma. Nat Rev Neurol 10:68–70. doi:10.1038/nrneurol.2013.268
127. Wick W, Hartmann C, Engel C, Stoffels M, Felsberg J, Stockhammer F, Sabel MC, Koeppen S, Ketter R, Meyermann R et al (2009) NOA-04 randomized phase III trial of sequential radiochemotherapy of anaplastic glioma with procarbazine, lomustine, and vincristine or temozolomide. J Clin Oncol Off J Am Soc Clin Oncol 27:5874–5880. doi:10.1200/JCO.2009.23.6497
128. Wick W, Meisner C, Hentschel B, Platten M, Schilling A, Wiestler B, Sabel MC, Koeppen S, Ketter R, Weiler M et al (2013) Prognostic or predictive value of MGMT promoter methylation in gliomas depends on IDH1 mutation. Neurology 81:1515–1522. doi:10.1212/WNL.0b013e3182a95680
129. Wiens AL, Cheng L, Bertsch EC, Johnson KA, Zhang S, Hattab EM (2012) Polysomy of chromosomes 1 and/or 19 is common and associated with less favorable clinical outcome in oligodendrogliomas: fluorescent in situ hybridization analysis of 84 consecutive cases. J Neuropathol Exp Neurol 71:618–624. doi:10.1097/NEN.0b013e31825b5f7a
130. Wieshmann UC, Milinis K, Paniker J, Das K, Jenkinson MD, Brodbelt A, Crooks D, Keller SS (2015) The role of the corpus callosum in seizure spread: MRI lesion mapping in oligodendrogliomas. Epilepsy Res 109:126–133. doi:10.1016/j.eplepsyres.2014.10.023
131. Wiestler B, Capper D, Holland-Letz T, Korshunov A, von Deimling A, Pfister SM, Platten M, Weller M, Wick W (2013) ATRX loss refines the classification of anaplastic gliomas and identifies a subgroup of IDH mutant astrocytic tumors with better prognosis. Acta Neuropathol 126:443–451. doi:10.1007/s00401-013-1156-z
132. Wiestler B, Capper D, Hovestadt V, Sill M, Jones DT, Hartmann C, Felsberg J, Platten M, Feiden W, Keyvani K et al (2014) Assessing CpG island methylator phenotype, 1p/19q codeletion, and MGMT promoter methylation from epigenome-wide data in the biomarker cohort of the NOA-04 trial. Neuro Oncol 16:1630–1638. doi:10.1093/neuonc/nou138
133. Wiestler B, Capper D, Sill M, Jones DT, Hovestadt V, Sturm D, Koelsche C, Bertoni A, Schweizer L, Korshunov A et al (2014) Integrated DNA methylation and copy-number profiling identify three clinically and biologically relevant groups of anaplastic glioma. Acta Neuropathol 128:561–571. doi:10.1007/s00401-014-1315-x
134. Wilcox P, Li CC, Lee M, Shivalingam B, Brennan J, Suter CM, Kaufman K, Lum T, Buckland ME (2015) Oligoastrocytomas: throwing the baby out with the bathwater? Acta Neuropathol 129:147–149. doi:10.1007/s00401-014-1353-4
135. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, Kos I, Batinic-Haberle I, Jones S, Riggins GJ et al (2009) IDH1 and IDH2 mutations in gliomas. N Engl J Med 360:765–773. doi:10.1056/NEJMoa0808710
136. Zong H, Verhaak RG, Canoll P (2012) The cellular origin for malignant glioma and prospects for clinical advancements. Expert Rev Mol Diagn 12:383–394. doi:10.1586/erm.12.30