Pediatric high-grade glioma: Biologically and clinically in need of new thinking

Neuro-Oncology

Volumn 19, Issue 2, 2017, Pages 153-161

  Jones, Chris ^a   Karajannis, Matthias A ^b   Jones, David T W ^c   Kieran, Mark W ^e   Monje, Michelle ^f   Baker, Suzanne J ^g   Becher, Oren J ^h   Cho, Yoon Jae ^f   Gupta, Nalin ⁱ   Hawkins, Cynthia ^j   Hargrave, Darren ^k   Haas Kogan, Daphne A ^e   Jabado, Nada ^l   Li, Xiao Nan ^m   Mueller, Sabine ⁱ   Nicolaides, Theo ⁱ   Packer, Roger J ⁿ   Persson, Anders I ⁱ   Phillips, Joanna J ⁱ   Simonds, Erin F ⁱ   Stafford, James M ^b   Tang, Yujie ^o   Pfister, Stefan M ^c,d   Weiss, William A ⁱ   more..

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^e DANA FARBER CANCER INSTITUTE   (United States)

^f STANFORD UNIVERSITY   (United States)

^g ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^h DUKE UNIVERSITY MEDICAL CENTER   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

^j HOSPITAL FOR SICK CHILDREN   (Canada)

^k GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^l MCGILL UNIVERSITY   (Canada)

^m BAYLOR COLLEGE OF MEDICINE   (United States)

ⁿ CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^o SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

more..

Author keywords

Clinical trials; Dipg; Genomics; Glioma; Pediatric

Indexed keywords

ANTINEOPLASTIC AGENT;

AGE; ARTICLE; BIOCHEMICAL ANALYSIS; BRAIN; CANCER ADJUVANT THERAPY; CANCER GRADING; CANCER RESEARCH; CANCER THERAPY; CARCINOGENESIS; CHILD; CHILDHOOD CANCER; CHROMATIN; CLINICAL EFFECTIVENESS; CLINICAL OUTCOME; DEVELOPMENTAL SIGNALING; DRUG TARGETING; GLIOBLASTOMA; GLIOMA; HUMAN; MEDICAL EXPERT; MOLECULAR ANALYSIS; PERSONALIZED MEDICINE; TUMOR MICROENVIRONMENT; BRAIN TUMOR; CELL TRANSFORMATION; GENETICS; METABOLISM; PATHOLOGY; PROGNOSIS;

BRAIN NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; CHILD; GLIOMA; HUMANS; NEOPLASM GRADING; PROGNOSIS;

EID: 85019378147     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/now101     Document Type: Article

References (90)

1. Northcott PA, Pfister SM, Jones DT. Next-generation (epi) genetic drivers of childhood brain tumours and the outlook for targeted therapies. Lancet Oncol. 2015;16(6):e293-e302.
2. Jones C, Baker SJ. Unique genetic and epigenetic mechanisms driving paediatric diffuse high-grade glioma. Nat Rev Cancer. 2014;14(10):651-661.
3. Northcott PA, Jones DT, Kool M et al. Medulloblastomics: the end of the beginning. Nat Rev Cancer. 2012;12(12):818-834.
4. Pajtler KW, Witt H, Sill M et al. Molecular classification of ependymal tumors across all CNS compartments, histopathological grades, and age groups. Cancer Cell. 2015;27(5):728-743.
5. Sturm D, Bender S, Jones DT et al. Paediatric and adult glioblastoma: multiform (epi) genomic culprits emerge. Nat Rev Cancer. 2014;14(2):92-107.
6. Taylor MD, Northcott PA, Korshunov A et al. Molecular subgroups of medulloblastoma: the current consensus. Acta Neuropathol. 2012;123(4):465-472.
7. Gajjar A, Pfister SM, Taylor MD et al. Molecular insights into pediatric brain tumors have the potential to transform therapy. Clin Cancer Res. 2014;20(22):5630-5640.
8. Schwartzentruber J, Korshunov A, Liu XY et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature. 2012;482(7384):226-231.
9. Bax DA, Mackay A, Little SE et al. A distinct spectrum of copy number aberrations in pediatric high-grade gliomas. Clin Cancer Res. 2010;16(13):3368-3377.
10. Faury D, Nantel A, Dunn SE et al. Molecular profiling identifies prognostic subgroups of pediatric glioblastoma and shows increased YB-1 expression in tumors. J Clin Oncol. 2007;25(10):1196-1208.
11. Paugh BS, Broniscer A, Qu C et al. Genome-wide analyses identify recurrent amplifications of receptor tyrosine kinases and cell-cycle regulatory genes in diffuse intrinsic pontine glioma. J Clin Oncol. 2011;29(30):3999-4006.
12. Paugh BS, Qu C, Jones C et al. Integrated molecular genetic profiling of pediatric high-grade gliomas reveals key differences with the adult disease. J Clin Oncol. 2010;28(18):3061-3068.
13. Puget S, Philippe C, Bax DA et al. Mesenchymal transition and PDGFRA amplification/mutation are key distinct oncogenic events in pediatric diffuse intrinsic pontine gliomas. PloS one. 2012;7(2):e30313.
14. Zarghooni M, Bartels U, Lee E et al. Whole-genome profiling of pediatric diffuse intrinsic pontine gliomas highlights platelet-derived growth factor receptor alpha and poly (ADP-ribose) polymerase as potential therapeutic targets. J Clin Oncol. 2010;28(8):1337-1344.
15. Wu G, Broniscer A, McEachron TA et al. Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat Genet. 2012;44(3):251-253.
16. Behjati S, Tarpey PS, Presneau N et al. Distinct H3F3A and H3F3B driver mutations define chondroblastoma and giant cell tumor of bone. Nat Genet. 2013;45(12):1479-1482.
17. Bender S, Tang Y, Lindroth AM et al. Reduced H3K27me3 and DNA hypomethylation are major drivers of gene expression in K27 M mutant pediatric high-grade gliomas. Cancer Cell. 2013;24(5):660-672.
18. Bjerke L, Mackay A, Nandhabalan M et al. Histone H3.3. mutations drive pediatric glioblastoma through upregulation of MYCN. Cancer Discov. 2013;3(5):512-519.
19. Chan KM, Fang D, Gan H et al. The histone H3.3K27 M mutation in pediatric glioma reprograms H3K27 methylation and gene expression. Genes Dev. 2013;27(9):985-990.
20. Lewis PW, Muller MM, Koletsky MS et al. Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science. 2013;340(6134):857-861.
21. Sturm D, Witt H, Hovestadt V et al. Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell. 2012;22(4):425-437.
22. Wu G, Diaz AK, Paugh BS et al. The genomic landscape of diffuse intrinsic pontine glioma and pediatric non-brainstem high-grade glioma. Nat Genet. 2014;46(5):444-450.
23. Taylor KR, Mackay A, Truffaux N et al. Recurrent activating ACVR1 mutations in diffuse intrinsic pontine glioma. Nat Genet. 2014;46(5):457-461.
24. Fontebasso AM, Papillon-Cavanagh S, Schwartzentruber J et al. Recurrent somatic mutations in ACVR1 in pediatric midline high-grade astrocytoma. Nat Genet. 2014:462-466.
25. Buczkowicz P, Hoeman C, Rakopoulos P et al. Genomic analysis of diffuse intrinsic pontine gliomas identifies three molecular subgroups and recurrent activating ACVR1 mutations. Nat Genet. 2014:451-456.
26. Castel D, Philippe C, Calmon R et al. Histone H3F3A and HIST1H3B K27 M mutations define two subgroups of diffuse intrinsic pontine gliomas with different prognosis and phenotypes. Acta Neuropathol. 2015;130(6):815-827.
27. Venneti S, Santi M, Felicella MM et al. A sensitive and specific histopathologic prognostic marker for H3F3A K27 M mutant pediatric glioblastomas. Acta Neuropathol. 2014;128(5):743-753.
28. Bechet D, Gielen GG, Korshunov A et al. Specific detection of methionine 27 mutation in histone 3 variants (H3K27 M) in fixed tissue from high-grade astrocytomas. Acta Neuropathol. 2014;128(5):733-741.
29. Grasso CS, Tang Y, Truffaux N et al. Functionally defined therapeutic targets in diffuse intrinsic pontine glioma. Nat Med. 2015;21(6):555-559.
30. Hashizume R, Andor N, Ihara Y et al. Pharmacologic inhibition of histone demethylation as a therapy for pediatric brainstem glioma. Nat Med. 2014;20(12):1394-1396.
31. Funato K, Major T, Lewis PW et al. Use of human embryonic stem cells to model pediatric gliomas with H3.3K27 M histone mutation. Science. 2014;346(6216):1529-1533.
32. Nguyen AT, Colin C, Nanni-Metellus I et al. Evidence for BRAF V600E and H3F3A K27M double mutations in paediatric glial and glioneuronal tumours. Neuropathol Appl Neurobiol. 2015;41(3):403-408.
33. Zhang J, Wu G, Miller CP et al. Whole-genome sequencing identifies genetic alterations in pediatric low-grade gliomas. Nat Genet. 2013;45(6):602-612.
34. Hegi ME, Diserens AC, Gorlia T et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352(10):997-1003.
35. Cohen KJ, Pollack IF, Zhou T et al. Temozolomide in the treatment of high-grade gliomas in children: a report from the Children's Oncology Group. Neuro Oncol. 2011;13(3):317-323.
36. Broniscer A, Chintagumpala M, Fouladi M et al. Temozolomide after radiotherapy for newly diagnosed high-grade glioma and unfavorable low-grade glioma in children. J Neurooncol. 2006;76(3):313-319.
37. Lashford LS, Thiesse P, Jouvet A et al. Temozolomide in malignant gliomas of childhood: a United Kingdom Children's Cancer Study Group and French Society for Pediatric Oncology Intergroup Study. J Clin Oncol. 2002;20(24):4684-4691.
38. Ruggiero A, Cefalo G, Garre ML et al. Phase II trial of temozolomide in children with recurrent high-grade glioma. J Neurooncol. 2006;77(1):89-94.
39. Korshunov A, Ryzhova M, Hovestadt V et al. Integrated analysis of pediatric glioblastoma reveals a subset of biologically favorable tumors with associated molecular prognostic markers. Acta Neuropathol. 2015;129(5):669-678.
40. Cohen KJ, Heideman RL, Zhou T et al. Temozolomide in the treatment of children with newly diagnosed diffuse intrinsic pontine gliomas: a report from the Children's Oncology Group. Neuro Oncol. 2011;13(4):410-416.
41. Rizzo D, Scalzone M, Ruggiero A et al. Temozolomide in the treatment of newly diagnosed diffuse brainstem glioma in children: a broken promise? J Chemother. 2015;27(2):106-110.
42. Chassot A, Canale S, Varlet P et al. Radiotherapy with concurrent and adjuvant temozolomide in children with newly diagnosed diffuse intrinsic pontine glioma. J Neurooncol. 2012;106(2):399-407.
43. Hargrave D, Bartels U, Bouffet E. Diffuse brainstem glioma in children: critical review of clinical trials. Lancet Oncol. 2006;7(3):241-248.
44. Taylor KR, Vinci M, Bullock AN et al. ACVR1 mutations in DIPG: lessons learned from FOP. Cancer Res. 2014;74(17):4565-4570.
45. Noushmehr H, Weisenberger DJ, Diefes K et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell. 2010;17(5):510-522.
46. Nicolaides TP, Li H, Solomon DA et al. Targeted therapy for BRAFV600E malignant astrocytoma. Clin Cancer Res. 2011;17(24):7595-7604.
47. Huillard E, Hashizume R, Phillips JJ et al. Cooperative interactions of BRAFV600E kinase and CDKN2A locus deficiency in pediatric malignant astrocytoma as a basis for rational therapy. Proc Natl Acad Sci U S A. 2012;109(22):8710-8715.
48. Bautista F, Paci A, Minard-Colin V et al. Vemurafenib in pediatric patients with BRAFV600E mutated high-grade gliomas. Pediatr Blood Cancer. 2014;61(6):1101-1103.
49. Robinson GW, Orr BA, Gajjar A. Complete clinical regression of a BRAF V600E-mutant pediatric glioblastoma multiforme after BRAF inhibitor therapy. BMC Cancer. 2014;14:258.
50. Fontebasso AM, Schwartzentruber J, Khuong-Quang DA et al. Mutations in SETD2 and genes affecting histone H3K36 methylation target hemispheric high-grade gliomas. Acta Neuropathol. 2013;125(5):659-669.
51. Paugh BS, Zhu X, Qu C et al. Novel oncogenic PDGFRA mutations in pediatric high-grade gliomas. Cancer Res. 2013;73(20):6219-6229.
52. Phillips JJ, Aranda D, Ellison DW et al. PDGFRA amplification is common in pediatric and adult high-grade astrocytomas and identifies a poor prognostic group in IDH1 mutant glioblastoma. Brain Pathol. 2013;23(5):565-573.
53. Brennan CW, Verhaak RG, McKenna A et al. The somatic genomic landscape of glioblastoma. Cell. 2013;155(2):462-477.
54. Jacob K, Quang-Khuong DA, Jones DT et al. Genetic aberrations leading to MAPK pathway activation mediate oncogene-induced senescence in sporadic pilocytic astrocytomas. Clin Cancer Res. 2011;17(14):4650-4660.
55. Zong H, Parada LF, Baker SJ. Cell of origin for malignant gliomas and its implication in therapeutic development. Cold Spring Harb Perspect Biol. 2015;7(5):00-00.
56. Monje M, Mitra SS, Freret ME et al. Hedgehog-responsive candidate cell of origin for diffuse intrinsic pontine glioma. Proc Natl Acad Sci U S A. 2011;108(11):4453-4458.
57. Tate MC, Lindquist RA, Nguyen T et al. Postnatal growth of the human pons: a morphometric and immunohistochemical analysis. J Comp Neurol. 2015;523(3):449-462.
58. Lebel C, Gee M, Camicioli R et al. Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage. 2012;60(1):340-352.
59. Gibson EM, Purger D, Mount CW et al. Neuronal activity promotes oligodendrogenesis and adaptive myelination in the mammalian brain. Science. 2014;344(6183):1252304.
60. Venkatesh HS, Johung TB, Caretti V et al. Neuronal activity promotes glioma growth through Neuroligin-3 secretion. Cell. 2015;161(4):803-816.
61. Hambardzumyan D, Gutmann DH, Kettenmann H. The role of microglia and macrophages in glioma maintenance and progression. Nat Neurosci. 2015;19(1):20-27.
62. Daginakatte GC, Gutmann DH. Neurofibromatosis-1 (Nf1) heterozygous brain microglia elaborate paracrine factors that promote Nf1-deficient astrocyte and glioma growth. Hum Mol Genet. 2007;16(9):1098-1112.
63. Pong WW, Higer SB, Gianino SM et al. Reduced microglial CX3CR1 expression delays neurofibromatosis-1 glioma formation. Ann Neurol. 2013;73(2):303-308.
64. Komohara Y, Ohnishi K, Kuratsu J et al. Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas. J Pathol. 2008;216(1):15-24.
65. Pyonteck SM, Akkari L, Schuhmacher AJ et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med. 2013;19(10):1264-1272.
66. Engler JR, Robinson AE, Smirnov I et al. Increased microglia/macrophage gene expression in a subset of adult and pediatric astrocytomas. PLoS One. 2012;7(8):e43339.
67. Dorward IG, Luo J, Perry A et al. Postoperative imaging surveillance in pediatric pilocytic astrocytomas. J Neurosurg Pediatr. 2010;6(4):346-352.
68. Caretti V, Sewing AC, Lagerweij T et al. Human pontine glioma cells can induce murine tumors. Acta Neuropathol. 2014;127(6):897-909.
69. Sposto R, Ertel IJ, Jenkin RD et al. The effectiveness of chemotherapy for treatment of high grade astrocytoma in children: results of a randomized trial. A report from the Childrens Cancer Study Group. J Neurooncol. 1989;7(2):165-177.
70. Pollack IF, Boyett JM, Yates AJ et al. The influence of central review on outcome associations in childhood malignant gliomas: results from the CCG-945 experience. Neuro Oncol. 2003;5(3):197-207.
71. Finlay JL, Boyett JM, Yates AJ et al. Randomized phase III trial in childhood high-grade astrocytoma comparing vincristine, lomustine, and prednisone with the eight-drugs-in-1-day regimen. Childrens Cancer Group. J Clin Oncol. 1995;13(1):112-123.
72. Stupp R, van den Bent MJ, Hegi ME. Optimal role of temozolomide in the treatment of malignant gliomas. Curr Neurol Neurosci Rep. 2005;5(3):198-206.
73. Pollack IF, Hamilton RL, Sobol RW et al. IDH1 mutations are common in malignant gliomas arising in adolescents: a report from the Children's Oncology Group. Childs Nerv Syst. 2011;27(1):87-94.
74. Hoffman LM, Geller J, Leach J et al. A feasibility and randomised Phase II study of vorinostat, bevacizumab, or temozolomide during radiation followed by maintenace chemotheraoy in newly-diagnosed pediatric high grade glioma: Childrens Oncology Group Study ACNS0822. Neuro Oncol. 2015;17(Suppl 3):iii39-iii40.
75. Wolff JE, Driever PH, Erdlenbruch B et al. Intensive chemotherapy improves survival in pediatric high-grade glioma after gross total resection: results of the HIT-GBM-C protocol. Cancer. 2010;116(3):705-712.
76. Jenkin RD, Boesel C, Ertel I et al. Brain-stem tumors in childhood: a prospective randomized trial of irradiation with and without adjuvant CCNU, VCR, and prednisone. A report of the Childrens Cancer Study Group. J Neurosurg. 1987;66(2):227-233.
77. Mandell LR, Kadota R, Freeman C et al. There is no role for hyperfractionated radiotherapy in the management of children with newly diagnosed diffuse intrinsic brainstem tumors: results of a Pediatric Oncology Group phase III trial comparing conventional vs. hyperfractionated radiotherapy. Int J Radiat Oncol Biol Phys. 1999;43(5):959-964.
78. Packer RJ, Boyett JM, Zimmerman RA et al. Outcome of children with brain stem gliomas after treatment with 7800 cGy of hyperfractionated radiotherapy. A Childrens Cancer Group phase I/II trial. Cancer. 1994;74(6):1827-1834.
79. Grill J, Puget S, Andreiuolo F et al. Critical oncogenic mutations in newly diagnosed pediatric diffuse intrinsic pontine glioma. Pediatr Blood Cancer. 2012;58(4):489-491.
80. Holdhoff M, Supko JG, Gallia GL et al. Intratumoral concentrations of imatinib after oral administration in patients with glioblastoma multiforme. J Neurooncol. 2010;97(2):241-245.
81. Razis E, Selviaridis P, Labropoulos S et al. Phase II study of neoadjuvant imatinib in glioblastoma: evaluation of clinical and molecular effects of the treatment. Clin Cancer Res. 2009;15(19):6258-6266.
82. Vivanco I, Robins HI, Rohle D et al. Differential sensitivity of gliomaversus lung cancer-specific EGFR mutations to EGFR kinase inhibitors. Cancer Discov. 2012;2(5):458-471.
83. Fouladi M, Stewart CF, Blaney SM et al. A molecular biology and phase II trial of lapatinib in children with refractory CNS malignancies: a pediatric brain tumor consortium study. J Neurooncol. 2013;114(2):173-179.
84. Hashizume R, Smirnov I, Liu S et al. Characterization of a diffuse intrinsic pontine glioma cell line: implications for future investigations and treatment. J Neurooncol. 2012;110(3):305-313.
85. Mistry M, Zhukova N, Merico D et al. BRAF mutation and CDKN2A deletion define a clinically distinct subgroup of childhood secondary highgrade glioma. J Clin Oncol. 2015;33(9):1015-1022.
86. Alexander BM, Galanis E, Yung WK et al. Brain Malignancy Steering Committee clinical trials planning workshop: report from the Targeted Therapies Working Group. Neuro Oncol. 2015;17(2):180-188.
87. Sottoriva A, Spiteri I, Piccirillo SG et al. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci U S A. 2013;110(10):4009-4014.
88. Snuderl M, Fazlollahi L, Le LP et al. Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell. 2011;20(6):810-817.
89. Kim D, Fiske BP, Birsoy K et al. SHMT2 drives glioma cell survival in ischaemia but imposes a dependence on glycine clearance. Nature. 2015;520(7547):363-367.
90. Fecci PE, Heimberger AB, Sampson JH. Immunotherapy for primary brain tumors: no longer a matter of privilege. Clin Cancer Res. 2014;20(22):5620-5629.