Characteristics of H3K27M-mutant diffuse gliomas with a non-midline location.
Diffuse intrinsic pontine glioma
Diffuse midline glioma H3 K27-altered
H3K27M
H3K28M
Methylation
Non-midline
Pediatric glioma
Journal
Journal of neuro-oncology
ISSN: 1573-7373
Titre abrégé: J Neurooncol
Pays: United States
ID NLM: 8309335
Informations de publication
Date de publication:
27 Jun 2024
27 Jun 2024
Historique:
received:
02
05
2024
accepted:
31
05
2024
medline:
28
6
2024
pubmed:
28
6
2024
entrez:
27
6
2024
Statut:
aheadofprint
Résumé
Diffuse midline gliomas (DMG) with H3K27 alterations (H3K27M-DMG) are a highly aggressive form of brain cancer. In rare cases, H3K27 mutations have been observed in diffuse non-midline gliomas (DNMG). It is currently unclear how these tumors should be classified. Herein, we analyze the characteristics of DNMG with H3K27M mutations. We reviewed the clinical, radiological and histological characteristics of all patients with an H3K27M mutated diffuse glioma diagnosed in our institution, between 2016 and 2023, to identify cases with a non-midline location. We then performed a molecular characterization (DNA methylation profiling, whole genome and transcriptome sequencing or targeted sequencing) of patients with an H3K27M-mutant DNMG and reviewed previously reported cases. Among 51 patients (18 children and 33 adults) diagnosed with an H3K27M diffuse glioma, we identified two patients (4%) who had a non-midline location. Including our two patients, 39 patients were reported in the literature with an H3K27M-mutant DNMG. Tumors were most frequently located in the temporal lobe (48%), affected adolescents and adults, and were associated with a poor outcome (median overall survival was 10.3 months (0.1-84)). Median age at diagnosis was 19.1 years. Tumors frequently harbored TP53 mutations (74%), ATRX mutations (71%) and PDGFRA mutations or amplifications (44%). In DNA methylation analysis, H3K27M-mutant DNMG clustered within or close to the reference group of H3K27M-mutant DMG. Compared to their midline counterpart, non-midline gliomas with H3K27M mutations seemed more frequently associated with PDGFRA alterations. DNMG with H3K27M mutations share many similarities with their midline counterpart, suggesting that they correspond to a rare anatomical presentation of these tumors. This is of paramount importance, as they may benefit from new therapeutic approaches such as ONC201.
Identifiants
pubmed: 38937309
doi: 10.1007/s11060-024-04733-z
pii: 10.1007/s11060-024-04733-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Louis DN, Perry A, Wesseling P et al (2021) The 2021 WHO classification of tumors of the Central Nervous System: a summary. Neuro-Oncol 23:1231–1251. https://doi.org/10.1093/neuonc/noab106
doi: 10.1093/neuonc/noab106
pubmed: 34185076
pmcid: 8328013
den Dunnen JT, Dalgleish R, Maglott DR et al (2016) HGVS recommendations for the description of sequence variants: 2016 update. Hum Mutat 37:564–569. https://doi.org/10.1002/humu.22981
doi: 10.1002/humu.22981
Tauziède-Espariat A, Debily M, Castel D et al (2022) Deciphering the genetic and epigenetic landscape of pediatric bithalamic tumors. Brain Pathol 32. https://doi.org/10.1111/bpa.13039
López G, Oberheim Bush NA, Berger MS et al (2017) Diffuse non-midline glioma with H3F3A K27M mutation: a prognostic and treatment dilemma. Acta Neuropathol Commun 5. https://doi.org/10.1186/s40478-017-0440-x
Arrillaga-Romany I, Gardner SL, Odia Y et al (2024) ONC201 (Dordaviprone) in recurrent H3 K27M–Mutant diffuse midline glioma. J Clin Oncol. https://doi.org/10.1200/JCO.23.01134
doi: 10.1200/JCO.23.01134
pubmed: 38335473
Odia Y, Hall MD, Cloughesy TF et al (2024) Selective DRD2 antagonist and ClpP agonist ONC201 in a recurrent non-midline H3 K27M-mutant glioma cohort. https://doi.org/10.1093/neuonc/noae021 . Neuro-Oncol
Parkinson H, Kapushesky M, Shojatalab M et al (2007) ArrayExpress–a public database of microarray experiments and gene expression profiles. Nucleic Acids Res 35:D747–D750. https://doi.org/10.1093/nar/gkl995
doi: 10.1093/nar/gkl995
pubmed: 17132828
Freeberg MA, Fromont LA, D’Altri T et al (2022) The European Genome-Phenome Archive in 2021. Nucleic Acids Res 50:D980–D987. https://doi.org/10.1093/nar/gkab1059
doi: 10.1093/nar/gkab1059
pubmed: 34791407
Barrett T, Wilhite SE, Ledoux P et al (2012) NCBI GEO: archive for functional genomics data sets—update. Nucleic Acids Res 41:D991–D995. https://doi.org/10.1093/nar/gks1193
doi: 10.1093/nar/gks1193
pubmed: 23193258
pmcid: 3531084
Plan France (2025) Médecine Génomique 2025. In: PFMG https://pfmg2025.aviesan.fr/ . Accessed 29 Mar 2024
Hench J, Hultschig C, Brugger J et al (2024) EpiDiP/NanoDiP: a versatile unsupervised machine learning edge computing platform for epigenomic tumour diagnostics. Acta Neuropathol Commun 12:51. https://doi.org/10.1186/s40478-024-01759-2
doi: 10.1186/s40478-024-01759-2
pubmed: 38576030
pmcid: 10993614
Capper D, Jones DTW, Sill M et al (2018) DNA methylation-based classification of central nervous system tumours. Nature 555:469–474. https://doi.org/10.1038/nature26000
doi: 10.1038/nature26000
pubmed: 29539639
pmcid: 6093218
Valério E, Alves de Castro JV, Carraro DM et al (2022) Beyond midline: diffuse Hemispheric Glioma, H3 K27M-Mutant with aggressive behavior. https://doi.org/10.1093/jnen/nlac016 . J Neuropathol Exp Neurol nlac016
Donev K, Sundararajan V, Johnson D et al (2024) Diffuse hemispheric glioma with H3 p.K28M (K27M) mutation: unusual non-midline presentation of diffuse midline glioma, H3 K27M-altered? J. https://doi.org/10.1093/jnen/nlae018 . Neuropathol Exp Neurol
Sturm D, Witt H, Hovestadt V et al (2012) Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of Glioblastoma. Cancer Cell 22:425–437. https://doi.org/10.1016/j.ccr.2012.08.024
doi: 10.1016/j.ccr.2012.08.024
pubmed: 23079654
Meyronet D, Esteban-Mader M, Bonnet C et al (2017) Characteristics of H3 K27M-mutant gliomas in adults. Neuro-Oncol 19:1127–1134. https://doi.org/10.1093/neuonc/now274
doi: 10.1093/neuonc/now274
pubmed: 28201752
pmcid: 5570304
Schulte JD, Buerki RA, Lapointe S et al (2020) Clinical, radiologic, and genetic characteristics of histone H3 K27M-mutant diffuse midline gliomas in adults. Neuro-Oncol Adv. https://doi.org/10.1093/noajnl/vdaa142 . 2:
doi: 10.1093/noajnl/vdaa142
Liu I, Jiang L, Samuelsson ER et al (2022) The landscape of tumor cell states and spatial organization in H3-K27M mutant diffuse midline glioma across age and location. Nat Genet 54:1881–1894. https://doi.org/10.1038/s41588-022-01236-3
doi: 10.1038/s41588-022-01236-3
pubmed: 36471067
pmcid: 9729116
Castel D, Kergrohen T, Tauziède-Espariat A et al (2020) Histone H3 wild-type DIPG/DMG overexpressing EZHIP extend the spectrum diffuse midline gliomas with PRC2 inhibition beyond H3-K27M mutation. Acta Neuropathol (Berl) 139:1109–1113. https://doi.org/10.1007/s00401-020-02142-w
doi: 10.1007/s00401-020-02142-w
pubmed: 32193787
Sievers P, Sill M, Schrimpf D et al (2021) A subset of pediatric-type thalamic gliomas share a distinct DNA methylation profile, H3K27me3 loss and frequent alteration of EGFR. Neuro-Oncol 23:34–43. https://doi.org/10.1093/neuonc/noaa251
doi: 10.1093/neuonc/noaa251
pubmed: 33130881
Mackay A, Burford A, Carvalho D et al (2017) Integrated Molecular Meta-Analysis of 1,000 Pediatric High-Grade and diffuse intrinsic pontine glioma. Cancer Cell 32:520–537e5. https://doi.org/10.1016/j.ccell.2017.08.017
doi: 10.1016/j.ccell.2017.08.017
pubmed: 28966033
pmcid: 5637314
Williams EA, Brastianos PK, Wakimoto H et al (2023) A comprehensive genomic study of 390 H3F3A-mutant pediatric and adult diffuse high-grade gliomas, CNS WHO grade 4. Acta Neuropathol (Berl) 146:515–525. https://doi.org/10.1007/s00401-023-02609-6
doi: 10.1007/s00401-023-02609-6
pubmed: 37524847
Hoffman LM, Veldhuijzen van Zanten SEM, Colditz N et al (2018) Clinical, radiologic, pathologic, and molecular characteristics of long-term survivors of diffuse intrinsic pontine glioma (DIPG): a collaborative report from the International and European Society for Pediatric Oncology DIPG Registries. J Clin Oncol 36:1963–1972. https://doi.org/10.1200/JCO.2017.75.9308
doi: 10.1200/JCO.2017.75.9308
pubmed: 29746225
pmcid: 6075859
Schüller U, Iglauer P, Dorostkar MM et al (2021) Mutations within FGFR1 are associated with superior outcome in a series of 83 diffuse midline gliomas with H3F3A K27M mutations. Acta Neuropathol (Berl) 141:323–325. https://doi.org/10.1007/s00401-020-02259-y
doi: 10.1007/s00401-020-02259-y
pubmed: 33433639
Auffret L, Ajlil Y, Tauziède-Espariat A et al (2024) A new subtype of diffuse midline glioma, H3 K27 and BRAF/FGFR1 co-altered: a clinico-radiological and histomolecular characterisation. Acta Neuropathol (Berl) 147. https://doi.org/10.1007/s00401-023-02651-4
Qiu T, Chanchotisatien A, Qin Z et al (2020) Imaging characteristics of adult H3 K27M-mutant gliomas. J Neurosurg 133:1662–1670. https://doi.org/10.3171/2019.9.JNS191920
doi: 10.3171/2019.9.JNS191920
La Rocca G, Sabatino G, Altieri R et al (2019) Significance of H3K27M mutation in Nonmidline High-Grade gliomas of cerebral hemispheres. World Neurosurg 131:174–176. https://doi.org/10.1016/j.wneu.2019.08.024
doi: 10.1016/j.wneu.2019.08.024
pubmed: 31415896
Wang L, Li Z, Zhang M et al (2018) H3 K27M–mutant diffuse midline gliomas in different anatomical locations. Hum Pathol 78:89–96. https://doi.org/10.1016/j.humpath.2018.04.015
doi: 10.1016/j.humpath.2018.04.015
pubmed: 29727696
Wang Y, Feng L, Ji P et al (2021) Clinical features and molecular markers on diffuse midline gliomas with H3K27M mutations: a 43 cases retrospective cohort study. https://doi.org/10.3389/fonc.2020.602553 . Front Oncol 10:
Majzner RG, Ramakrishna S, Yeom KW et al (2022) GD2-CAR T cell therapy for H3K27M-mutated diffuse midline gliomas. Nature 603:934–941. https://doi.org/10.1038/s41586-022-04489-4
doi: 10.1038/s41586-022-04489-4
pubmed: 35130560
pmcid: 8967714