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Genomic profiling of sporadic multiple meningiomas
BACKGROUND: Multiple meningiomas (MMs) rarely occur sporadically. It is unclear whether each individual tumor in a single patient behaves similarly. Moreover, the molecular mechanisms underlying the formation of sporadic MMs and clonal formation etiology of these tumors are poorly understood. METHOD...
Autores principales: | , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9107270/ https://www.ncbi.nlm.nih.gov/pubmed/35568945 http://dx.doi.org/10.1186/s12920-022-01258-0 |
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author | Erson-Omay, E. Zeynep Vetsa, Shaurey Vasandani, Sagar Barak, Tanyeri Nadar, Arushii Marianayanam, Neelan Yalcin, Kanat Miyagishima, Danielle Aguilera, Stephanie Marie Robert, Stephanie Mishra-Gorur, Ketu Fulbright, Robert K. McGuone, Declan Günel, Murat Moliterno, Jennifer |
author_facet | Erson-Omay, E. Zeynep Vetsa, Shaurey Vasandani, Sagar Barak, Tanyeri Nadar, Arushii Marianayanam, Neelan Yalcin, Kanat Miyagishima, Danielle Aguilera, Stephanie Marie Robert, Stephanie Mishra-Gorur, Ketu Fulbright, Robert K. McGuone, Declan Günel, Murat Moliterno, Jennifer |
author_sort | Erson-Omay, E. Zeynep |
collection | PubMed |
description | BACKGROUND: Multiple meningiomas (MMs) rarely occur sporadically. It is unclear whether each individual tumor in a single patient behaves similarly. Moreover, the molecular mechanisms underlying the formation of sporadic MMs and clonal formation etiology of these tumors are poorly understood. METHODS: Patients with spatially separated MMs without prior radiation exposure or a family history who underwent surgical resection of at least two meningiomas were included. Unbiased, comprehensive next generation sequencing was performed, and relevant clinical data was analyzed. RESULTS: Fifteen meningiomas and one dural specimen from six patients were included. The majority of tumors (12/15) were WHO Grade I; one patient had bilateral MMs, one of which was Grade II, while the other was Grade I. We found 11/15 of our cohort specimens were of NF2-loss subtype. Meningiomas from 5/6 patients had a monoclonal origin, with the tumor from the remaining patient showing evidence for independent clonal formation. We identified a novel case of non-NF2 mutant MM with monoclonal etiology. MMs due to a monoclonal origin did not always display a homogenous genomic profile, but rather exhibited heterogeneity due to branching evolution. CONCLUSIONS: Both NF2-loss and non-NF2 driven MMs can form due to monoclonal expansion and those tumors can acquire inter-tumoral heterogeneity through branched evolution. Grade I and II meningiomas can occur in the same patient. Thus, the molecular make-up and clinical behavior of one tumor in MMs, cannot reliably lend insight into that of the others and suggests the clinical management strategy for MMs should be tailored individually. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12920-022-01258-0. |
format | Online Article Text |
id | pubmed-9107270 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-91072702022-05-15 Genomic profiling of sporadic multiple meningiomas Erson-Omay, E. Zeynep Vetsa, Shaurey Vasandani, Sagar Barak, Tanyeri Nadar, Arushii Marianayanam, Neelan Yalcin, Kanat Miyagishima, Danielle Aguilera, Stephanie Marie Robert, Stephanie Mishra-Gorur, Ketu Fulbright, Robert K. McGuone, Declan Günel, Murat Moliterno, Jennifer BMC Med Genomics Research Article BACKGROUND: Multiple meningiomas (MMs) rarely occur sporadically. It is unclear whether each individual tumor in a single patient behaves similarly. Moreover, the molecular mechanisms underlying the formation of sporadic MMs and clonal formation etiology of these tumors are poorly understood. METHODS: Patients with spatially separated MMs without prior radiation exposure or a family history who underwent surgical resection of at least two meningiomas were included. Unbiased, comprehensive next generation sequencing was performed, and relevant clinical data was analyzed. RESULTS: Fifteen meningiomas and one dural specimen from six patients were included. The majority of tumors (12/15) were WHO Grade I; one patient had bilateral MMs, one of which was Grade II, while the other was Grade I. We found 11/15 of our cohort specimens were of NF2-loss subtype. Meningiomas from 5/6 patients had a monoclonal origin, with the tumor from the remaining patient showing evidence for independent clonal formation. We identified a novel case of non-NF2 mutant MM with monoclonal etiology. MMs due to a monoclonal origin did not always display a homogenous genomic profile, but rather exhibited heterogeneity due to branching evolution. CONCLUSIONS: Both NF2-loss and non-NF2 driven MMs can form due to monoclonal expansion and those tumors can acquire inter-tumoral heterogeneity through branched evolution. Grade I and II meningiomas can occur in the same patient. Thus, the molecular make-up and clinical behavior of one tumor in MMs, cannot reliably lend insight into that of the others and suggests the clinical management strategy for MMs should be tailored individually. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12920-022-01258-0. BioMed Central 2022-05-14 /pmc/articles/PMC9107270/ /pubmed/35568945 http://dx.doi.org/10.1186/s12920-022-01258-0 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Article Erson-Omay, E. Zeynep Vetsa, Shaurey Vasandani, Sagar Barak, Tanyeri Nadar, Arushii Marianayanam, Neelan Yalcin, Kanat Miyagishima, Danielle Aguilera, Stephanie Marie Robert, Stephanie Mishra-Gorur, Ketu Fulbright, Robert K. McGuone, Declan Günel, Murat Moliterno, Jennifer Genomic profiling of sporadic multiple meningiomas |
title | Genomic profiling of sporadic multiple meningiomas |
title_full | Genomic profiling of sporadic multiple meningiomas |
title_fullStr | Genomic profiling of sporadic multiple meningiomas |
title_full_unstemmed | Genomic profiling of sporadic multiple meningiomas |
title_short | Genomic profiling of sporadic multiple meningiomas |
title_sort | genomic profiling of sporadic multiple meningiomas |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9107270/ https://www.ncbi.nlm.nih.gov/pubmed/35568945 http://dx.doi.org/10.1186/s12920-022-01258-0 |
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