DNA methylation-based reclassification of olfactory neuroblastoma

Olfactory neuroblastoma/esthesioneuroblastoma (ONB) is an uncommon neuroectodermal neoplasm thought to arise from the olfactory epithelium. Little is known about its molecular pathogenesis. For this study, a retrospective cohort of n  = 66 tumor samples with the institutional diagnosis of ONB was an...

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Published inActa neuropathologica Vol. 136; no. 2; pp. 255 - 271
Main Authors Capper, David, Engel, Nils W., Stichel, Damian, Lechner, Matt, Glöss, Stefanie, Schmid, Simone, Koelsche, Christian, Schrimpf, Daniel, Niesen, Judith, Wefers, Annika K., Jones, David T. W., Sill, Martin, Weigert, Oliver, Ligon, Keith L., Olar, Adriana, Koch, Arend, Forster, Martin, Moran, Sebastian, Tirado, Oscar M., Sáinz-Jaspeado, Miguel, Mora, Jaume, Esteller, Manel, Alonso, Javier, del Muro, Xavier Garcia, Paulus, Werner, Felsberg, Jörg, Reifenberger, Guido, Glatzel, Markus, Frank, Stephan, Monoranu, Camelia M., Lund, Valerie J., von Deimling, Andreas, Pfister, Stefan, Buslei, Rolf, Ribbat-Idel, Julika, Perner, Sven, Gudziol, Volker, Meinhardt, Matthias, Schüller, Ulrich
Format Journal Article
LanguageEnglish
Published Berlin/Heidelberg Springer Berlin Heidelberg 01.08.2018
Springer
Springer Nature B.V
Subjects
Adenocarcinoma
Analysis
Chromosome 1
Copy number
CpG islands
Cytokeratin
Deoxyribonucleic acid
Diagnosis
DNA
DNA fingerprinting
DNA methylation
DNA sequencing
Embedding
Gene mutation
Genomes
Genomics
Head & neck cancer
Immunohistochemistry
Keratin
Medical schools
Medicine
Medicine & Public Health
Methylation
Methyltransferases
Mutation
Mutation hot spots
Neuroblastoma
Neurosciences
Olfactory epithelium
Original Paper
p53 Protein
Pathology
Phenotypes
Reclassification
Squamous cell carcinoma
Tumor proteins
Tumors
Sinonasal Tumors
Esthesioneuroblastoma
IDH1 Mutation
Sinonasal Adenocarcinoma
CpG Island Methylator Phenotype (CIMP)
Online AccessGet full text
ISSN0001-6322
1432-0533
1432-0533
DOI10.1007/s00401-018-1854-7

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Abstract Olfactory neuroblastoma/esthesioneuroblastoma (ONB) is an uncommon neuroectodermal neoplasm thought to arise from the olfactory epithelium. Little is known about its molecular pathogenesis. For this study, a retrospective cohort of n  = 66 tumor samples with the institutional diagnosis of ONB was analyzed by immunohistochemistry, genome-wide DNA methylation profiling, copy number analysis, and in a subset, next-generation panel sequencing of 560 tumor-associated genes. DNA methylation profiles were compared to those of relevant differential diagnoses of ONB. Unsupervised hierarchical clustering analysis of DNA methylation data revealed four subgroups among institutionally diagnosed ONB. The largest group ( n  = 42, 64%, Core ONB) presented with classical ONB histology and no overlap with other classes upon methylation profiling-based t-distributed stochastic neighbor embedding (t-SNE) analysis. A second DNA methylation group ( n  = 7, 11%) with CpG island methylator phenotype (CIMP) consisted of cases with strong expression of cytokeratin, no or scarce chromogranin A expression and IDH2 hotspot mutation in all cases. T-SNE analysis clustered these cases together with sinonasal carcinoma with IDH2 mutation. Four cases (6%) formed a small group characterized by an overall high level of DNA methylation, but without CIMP. The fourth group consisted of 13 cases that had heterogeneous DNA methylation profiles and strong cytokeratin expression in most cases. In t-SNE analysis, these cases mostly grouped among sinonasal adenocarcinoma, squamous cell carcinoma, and undifferentiated carcinoma. Copy number analysis indicated highly recurrent chromosomal changes among Core ONB with a high frequency of combined loss of chromosome 1–4, 8–10, and 12. NGS sequencing did not reveal highly recurrent mutations in ONB, with the only recurrently mutated genes being TP53 and DNMT3A . In conclusion, we demonstrate that institutionally diagnosed ONB are a heterogeneous group of tumors. Expression of cytokeratin, chromogranin A, the mutational status of IDH2 as well as DNA methylation patterns may greatly aid in the precise classification of ONB.
AbstractList Olfactory neuroblastoma/esthesioneuroblastoma (ONB) is an uncommon neuroectodermal neoplasm thought to arise from the olfactory epithelium. Little is known about its molecular pathogenesis. For this study, a retrospective cohort of n = 66 tumor samples with the institutional diagnosis of ONB was analyzed by immunohistochemistry, genome-wide DNA methylation profiling, copy number analysis, and in a subset, next-generation panel sequencing of 560 tumor-associated genes. DNA methylation profiles were compared to those of relevant differential diagnoses of ONB. Unsupervised hierarchical clustering analysis of DNA methylation data revealed four subgroups among institutionally diagnosed ONB. The largest group (n = 42, 64%, Core ONB) presented with classical ONB histology and no overlap with other classes upon methylation profiling-based t-distributed stochastic neighbor embedding (t-SNE) analysis. A second DNA methylation group (n = 7, 11%) with CpG island methylator phenotype (CIMP) consisted of cases with strong expression of cytokeratin, no or scarce chromogranin A expression and IDH2 hotspot mutation in all cases. T-SNE analysis clustered these cases together with sinonasal carcinoma with IDH2 mutation. Four cases (6%) formed a small group characterized by an overall high level of DNA methylation, but without CIMP. The fourth group consisted of 13 cases that had heterogeneous DNA methylation profiles and strong cytokeratin expression in most cases. In t-SNE analysis, these cases mostly grouped among sinonasal adenocarcinoma, squamous cell carcinoma, and undifferentiated carcinoma. Copy number analysis indicated highly recurrent chromosomal changes among Core ONB with a high frequency of combined loss of chromosome 1-4, 8-10, and 12. NGS sequencing did not reveal highly recurrent mutations in ONB, with the only recurrently mutated genes being TP53 and DNMT3A. In conclusion, we demonstrate that institutionally diagnosed ONB are a heterogeneous group of tumors. Expression of cytokeratin, chromogranin A, the mutational status of IDH2 as well as DNA methylation patterns may greatly aid in the precise classification of ONB.
Olfactory neuroblastoma/esthesioneuroblastoma (ONB) is an uncommon neuroectodermal neoplasm thought to arise from the olfactory epithelium. Little is known about its molecular pathogenesis. For this study, a retrospective cohort of n  = 66 tumor samples with the institutional diagnosis of ONB was analyzed by immunohistochemistry, genome-wide DNA methylation profiling, copy number analysis, and in a subset, next-generation panel sequencing of 560 tumor-associated genes. DNA methylation profiles were compared to those of relevant differential diagnoses of ONB. Unsupervised hierarchical clustering analysis of DNA methylation data revealed four subgroups among institutionally diagnosed ONB. The largest group ( n  = 42, 64%, Core ONB) presented with classical ONB histology and no overlap with other classes upon methylation profiling-based t-distributed stochastic neighbor embedding (t-SNE) analysis. A second DNA methylation group ( n  = 7, 11%) with CpG island methylator phenotype (CIMP) consisted of cases with strong expression of cytokeratin, no or scarce chromogranin A expression and IDH2 hotspot mutation in all cases. T-SNE analysis clustered these cases together with sinonasal carcinoma with IDH2 mutation. Four cases (6%) formed a small group characterized by an overall high level of DNA methylation, but without CIMP. The fourth group consisted of 13 cases that had heterogeneous DNA methylation profiles and strong cytokeratin expression in most cases. In t-SNE analysis, these cases mostly grouped among sinonasal adenocarcinoma, squamous cell carcinoma, and undifferentiated carcinoma. Copy number analysis indicated highly recurrent chromosomal changes among Core ONB with a high frequency of combined loss of chromosome 1–4, 8–10, and 12. NGS sequencing did not reveal highly recurrent mutations in ONB, with the only recurrently mutated genes being TP53 and DNMT3A . In conclusion, we demonstrate that institutionally diagnosed ONB are a heterogeneous group of tumors. Expression of cytokeratin, chromogranin A, the mutational status of IDH2 as well as DNA methylation patterns may greatly aid in the precise classification of ONB.
Olfactory neuroblastoma/esthesioneuroblastoma (ONB) is an uncommon neuroectodermal neoplasm thought to arise from the olfactory epithelium. Little is known about its molecular pathogenesis. For this study, a retrospective cohort of n = 66 tumor samples with the institutional diagnosis of ONB was analyzed by immunohistochemistry, genome-wide DNA methylation profiling, copy number analysis, and in a subset, next-generation panel sequencing of 560 tumor-associated genes. DNA methylation profiles were compared to those of relevant differential diagnoses of ONB. Unsupervised hierarchical clustering analysis of DNA methylation data revealed four subgroups among institutionally diagnosed ONB. The largest group (n = 42, 64%, Core ONB) presented with classical ONB histology and no overlap with other classes upon methylation profiling-based t-distributed stochastic neighbor embedding (t-SNE) analysis. A second DNA methylation group (n = 7, 11%) with CpG island methylator phenotype (CIMP) consisted of cases with strong expression of cytokeratin, no or scarce chromogranin A expression and IDH2 hotspot mutation in all cases. T-SNE analysis clustered these cases together with sinonasal carcinoma with IDH2 mutation. Four cases (6%) formed a small group characterized by an overall high level of DNA methylation, but without CIMP. The fourth group consisted of 13 cases that had heterogeneous DNA methylation profiles and strong cytokeratin expression in most cases. In t-SNE analysis, these cases mostly grouped among sinonasal adenocarcinoma, squamous cell carcinoma, and undifferentiated carcinoma. Copy number analysis indicated highly recurrent chromosomal changes among Core ONB with a high frequency of combined loss of chromosome 1-4, 8-10, and 12. NGS sequencing did not reveal highly recurrent mutations in ONB, with the only recurrently mutated genes being TP53 and DNMT3A. In conclusion, we demonstrate that institutionally diagnosed ONB are a heterogeneous group of tumors. Expression of cytokeratin, chromogranin A, the mutational status of IDH2 as well as DNA methylation patterns may greatly aid in the precise classification of ONB.Olfactory neuroblastoma/esthesioneuroblastoma (ONB) is an uncommon neuroectodermal neoplasm thought to arise from the olfactory epithelium. Little is known about its molecular pathogenesis. For this study, a retrospective cohort of n = 66 tumor samples with the institutional diagnosis of ONB was analyzed by immunohistochemistry, genome-wide DNA methylation profiling, copy number analysis, and in a subset, next-generation panel sequencing of 560 tumor-associated genes. DNA methylation profiles were compared to those of relevant differential diagnoses of ONB. Unsupervised hierarchical clustering analysis of DNA methylation data revealed four subgroups among institutionally diagnosed ONB. The largest group (n = 42, 64%, Core ONB) presented with classical ONB histology and no overlap with other classes upon methylation profiling-based t-distributed stochastic neighbor embedding (t-SNE) analysis. A second DNA methylation group (n = 7, 11%) with CpG island methylator phenotype (CIMP) consisted of cases with strong expression of cytokeratin, no or scarce chromogranin A expression and IDH2 hotspot mutation in all cases. T-SNE analysis clustered these cases together with sinonasal carcinoma with IDH2 mutation. Four cases (6%) formed a small group characterized by an overall high level of DNA methylation, but without CIMP. The fourth group consisted of 13 cases that had heterogeneous DNA methylation profiles and strong cytokeratin expression in most cases. In t-SNE analysis, these cases mostly grouped among sinonasal adenocarcinoma, squamous cell carcinoma, and undifferentiated carcinoma. Copy number analysis indicated highly recurrent chromosomal changes among Core ONB with a high frequency of combined loss of chromosome 1-4, 8-10, and 12. NGS sequencing did not reveal highly recurrent mutations in ONB, with the only recurrently mutated genes being TP53 and DNMT3A. In conclusion, we demonstrate that institutionally diagnosed ONB are a heterogeneous group of tumors. Expression of cytokeratin, chromogranin A, the mutational status of IDH2 as well as DNA methylation patterns may greatly aid in the precise classification of ONB.
Audience Academic
Author Wefers, Annika K.
Lechner, Matt
Schmid, Simone
Weigert, Oliver
Monoranu, Camelia M.
Gudziol, Volker
Buslei, Rolf
Mora, Jaume
Reifenberger, Guido
Frank, Stephan
Stichel, Damian
Schrimpf, Daniel
Olar, Adriana
Esteller, Manel
Lund, Valerie J.
Glöss, Stefanie
Koelsche, Christian
Forster, Martin
Engel, Nils W.
Pfister, Stefan
Ribbat-Idel, Julika
Meinhardt, Matthias
Sáinz-Jaspeado, Miguel
Jones, David T. W.
Ligon, Keith L.
del Muro, Xavier Garcia
Sill, Martin
Perner, Sven
Moran, Sebastian
Niesen, Judith
Koch, Arend
Alonso, Javier
Tirado, Oscar M.
Felsberg, Jörg
von Deimling, Andreas
Paulus, Werner
Glatzel, Markus
Capper, David
Schüller, Ulrich
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  fullname: Engel, Nils W.
  organization: Center for Neuropathology, Ludwig-Maximilians-University, Department of Oncology and Hematology with Sections Bone Marrow Transplant and Pneumology, Hubertus Wald Tumorzentrum/University Cancer Center Hamburg, University Medical Center Hamburg
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/29730775$$D View this record in MEDLINE/PubMed
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Keywords Sinonasal Tumors
Esthesioneuroblastoma
IDH1 Mutation
Sinonasal Adenocarcinoma
CpG Island Methylator Phenotype (CIMP)
Language English
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PublicationSubtitle Pathology and Mechanisms of Neurological Disease
PublicationTitle Acta neuropathologica
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– reference: 30094618 - Acta Neuropathol. 2018 Sep;136(3):505
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Snippet Olfactory neuroblastoma/esthesioneuroblastoma (ONB) is an uncommon neuroectodermal neoplasm thought to arise from the olfactory epithelium. Little is known...
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SubjectTerms Adenocarcinoma
Analysis
Chromosome 1
Copy number
CpG islands
Cytokeratin
Deoxyribonucleic acid
Diagnosis
DNA
DNA fingerprinting
DNA methylation
DNA sequencing
Embedding
Gene mutation
Genomes
Genomics
Head & neck cancer
Immunohistochemistry
Keratin
Medical schools
Medicine
Medicine & Public Health
Methylation
Methyltransferases
Mutation
Mutation hot spots
Neuroblastoma
Neurosciences
Olfactory epithelium
Original Paper
p53 Protein
Pathology
Phenotypes
Reclassification
Squamous cell carcinoma
Tumor proteins
Tumors
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Title DNA methylation-based reclassification of olfactory neuroblastoma
URI https://link.springer.com/article/10.1007/s00401-018-1854-7
https://www.ncbi.nlm.nih.gov/pubmed/29730775
https://www.proquest.com/docview/2034869807
https://www.proquest.com/docview/2035708185
Volume 136
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