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Significance of molecular classification of ependymomas: C11orf95-RELA fusion-negative supratentorial ependymomas are a heterogeneous group of tumors

Extensive molecular analyses of ependymal tumors have revealed that supratentorial and posterior fossa ependymomas have distinct molecular profiles and are likely to be different diseases. The presence of C11orf95-RELA fusion genes in a subset of supratentorial ependymomas (ST-EPN) indicated the exi...

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Autores principales: Fukuoka, Kohei, Kanemura, Yonehiro, Shofuda, Tomoko, Fukushima, Shintaro, Yamashita, Satoshi, Narushima, Daichi, Kato, Mamoru, Honda-Kitahara, Mai, Ichikawa, Hitoshi, Kohno, Takashi, Sasaki, Atsushi, Hirato, Junko, Hirose, Takanori, Komori, Takashi, Satomi, Kaishi, Yoshida, Akihiko, Yamasaki, Kai, Nakano, Yoshiko, Takada, Ai, Nakamura, Taishi, Takami, Hirokazu, Matsushita, Yuko, Suzuki, Tomonari, Nakamura, Hideo, Makino, Keishi, Sonoda, Yukihiko, Saito, Ryuta, Tominaga, Teiji, Matsusaka, Yasuhiro, Kobayashi, Keiichi, Nagane, Motoo, Furuta, Takuya, Nakada, Mitsutoshi, Narita, Yoshitaka, Hirose, Yuichi, Ohba, Shigeo, Wada, Akira, Shimizu, Katsuyoshi, Kurozumi, Kazuhiko, Date, Isao, Fukai, Junya, Miyairi, Yousuke, Kagawa, Naoki, Kawamura, Atsufumi, Yoshida, Makiko, Nishida, Namiko, Wataya, Takafumi, Yamaoka, Masayoshi, Tsuyuguchi, Naohiro, Uda, Takehiro, Takahashi, Mayu, Nakano, Yoshiteru, Akai, Takuya, Izumoto, Shuichi, Nonaka, Masahiro, Yoshifuji, Kazuhisa, Kodama, Yoshinori, Mano, Masayuki, Ozawa, Tatsuya, Ramaswamy, Vijay, Taylor, Michael D., Ushijima, Toshikazu, Shibui, Soichiro, Yamasaki, Mami, Arai, Hajime, Sakamoto, Hiroaki, Nishikawa, Ryo, Ichimura, Koichi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6278135/
https://www.ncbi.nlm.nih.gov/pubmed/30514397
http://dx.doi.org/10.1186/s40478-018-0630-1
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author Fukuoka, Kohei
Kanemura, Yonehiro
Shofuda, Tomoko
Fukushima, Shintaro
Yamashita, Satoshi
Narushima, Daichi
Kato, Mamoru
Honda-Kitahara, Mai
Ichikawa, Hitoshi
Kohno, Takashi
Sasaki, Atsushi
Hirato, Junko
Hirose, Takanori
Komori, Takashi
Satomi, Kaishi
Yoshida, Akihiko
Yamasaki, Kai
Nakano, Yoshiko
Takada, Ai
Nakamura, Taishi
Takami, Hirokazu
Matsushita, Yuko
Suzuki, Tomonari
Nakamura, Hideo
Makino, Keishi
Sonoda, Yukihiko
Saito, Ryuta
Tominaga, Teiji
Matsusaka, Yasuhiro
Kobayashi, Keiichi
Nagane, Motoo
Furuta, Takuya
Nakada, Mitsutoshi
Narita, Yoshitaka
Hirose, Yuichi
Ohba, Shigeo
Wada, Akira
Shimizu, Katsuyoshi
Kurozumi, Kazuhiko
Date, Isao
Fukai, Junya
Miyairi, Yousuke
Kagawa, Naoki
Kawamura, Atsufumi
Yoshida, Makiko
Nishida, Namiko
Wataya, Takafumi
Yamaoka, Masayoshi
Tsuyuguchi, Naohiro
Uda, Takehiro
Takahashi, Mayu
Nakano, Yoshiteru
Akai, Takuya
Izumoto, Shuichi
Nonaka, Masahiro
Yoshifuji, Kazuhisa
Kodama, Yoshinori
Mano, Masayuki
Ozawa, Tatsuya
Ramaswamy, Vijay
Taylor, Michael D.
Ushijima, Toshikazu
Shibui, Soichiro
Yamasaki, Mami
Arai, Hajime
Sakamoto, Hiroaki
Nishikawa, Ryo
Ichimura, Koichi
author_facet Fukuoka, Kohei
Kanemura, Yonehiro
Shofuda, Tomoko
Fukushima, Shintaro
Yamashita, Satoshi
Narushima, Daichi
Kato, Mamoru
Honda-Kitahara, Mai
Ichikawa, Hitoshi
Kohno, Takashi
Sasaki, Atsushi
Hirato, Junko
Hirose, Takanori
Komori, Takashi
Satomi, Kaishi
Yoshida, Akihiko
Yamasaki, Kai
Nakano, Yoshiko
Takada, Ai
Nakamura, Taishi
Takami, Hirokazu
Matsushita, Yuko
Suzuki, Tomonari
Nakamura, Hideo
Makino, Keishi
Sonoda, Yukihiko
Saito, Ryuta
Tominaga, Teiji
Matsusaka, Yasuhiro
Kobayashi, Keiichi
Nagane, Motoo
Furuta, Takuya
Nakada, Mitsutoshi
Narita, Yoshitaka
Hirose, Yuichi
Ohba, Shigeo
Wada, Akira
Shimizu, Katsuyoshi
Kurozumi, Kazuhiko
Date, Isao
Fukai, Junya
Miyairi, Yousuke
Kagawa, Naoki
Kawamura, Atsufumi
Yoshida, Makiko
Nishida, Namiko
Wataya, Takafumi
Yamaoka, Masayoshi
Tsuyuguchi, Naohiro
Uda, Takehiro
Takahashi, Mayu
Nakano, Yoshiteru
Akai, Takuya
Izumoto, Shuichi
Nonaka, Masahiro
Yoshifuji, Kazuhisa
Kodama, Yoshinori
Mano, Masayuki
Ozawa, Tatsuya
Ramaswamy, Vijay
Taylor, Michael D.
Ushijima, Toshikazu
Shibui, Soichiro
Yamasaki, Mami
Arai, Hajime
Sakamoto, Hiroaki
Nishikawa, Ryo
Ichimura, Koichi
author_sort Fukuoka, Kohei
collection PubMed
description Extensive molecular analyses of ependymal tumors have revealed that supratentorial and posterior fossa ependymomas have distinct molecular profiles and are likely to be different diseases. The presence of C11orf95-RELA fusion genes in a subset of supratentorial ependymomas (ST-EPN) indicated the existence of molecular subgroups. However, the pathogenesis of RELA fusion-negative ependymomas remains elusive. To investigate the molecular pathogenesis of these tumors and validate the molecular classification of ependymal tumors, we conducted thorough molecular analyses of 113 locally diagnosed ependymal tumors from 107 patients in the Japan Pediatric Molecular Neuro-Oncology Group. All tumors were histopathologically reviewed and 12 tumors were re-classified as non-ependymomas. A combination of RT-PCR, FISH, and RNA sequencing identified RELA fusion in 19 of 29 histologically verified ST-EPN cases, whereas another case was diagnosed as ependymoma RELA fusion-positive via the methylation classifier (68.9%). Among the 9 RELA fusion-negative ST-EPN cases, either the YAP1 fusion, BCOR tandem duplication, EP300-BCORL1 fusion, or FOXO1-STK24 fusion was detected in single cases. Methylation classification did not identify a consistent molecular class within this group. Genome-wide methylation profiling successfully sub-classified posterior fossa ependymoma (PF-EPN) into PF-EPN-A (PFA) and PF-EPN-B (PFB). A multivariate analysis using Cox regression confirmed that PFA was the sole molecular marker which was independently associated with patient survival. A clinically applicable pyrosequencing assay was developed to determine the PFB subgroup with 100% specificity using the methylation status of 3 genes, CRIP1, DRD4 and LBX2. Our results emphasized the significance of molecular classification in the diagnosis of ependymomas. RELA fusion-negative ST-EPN appear to be a heterogeneous group of tumors that do not fall into any of the existing molecular subgroups and are unlikely to form a single category. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40478-018-0630-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-62781352018-12-10 Significance of molecular classification of ependymomas: C11orf95-RELA fusion-negative supratentorial ependymomas are a heterogeneous group of tumors Fukuoka, Kohei Kanemura, Yonehiro Shofuda, Tomoko Fukushima, Shintaro Yamashita, Satoshi Narushima, Daichi Kato, Mamoru Honda-Kitahara, Mai Ichikawa, Hitoshi Kohno, Takashi Sasaki, Atsushi Hirato, Junko Hirose, Takanori Komori, Takashi Satomi, Kaishi Yoshida, Akihiko Yamasaki, Kai Nakano, Yoshiko Takada, Ai Nakamura, Taishi Takami, Hirokazu Matsushita, Yuko Suzuki, Tomonari Nakamura, Hideo Makino, Keishi Sonoda, Yukihiko Saito, Ryuta Tominaga, Teiji Matsusaka, Yasuhiro Kobayashi, Keiichi Nagane, Motoo Furuta, Takuya Nakada, Mitsutoshi Narita, Yoshitaka Hirose, Yuichi Ohba, Shigeo Wada, Akira Shimizu, Katsuyoshi Kurozumi, Kazuhiko Date, Isao Fukai, Junya Miyairi, Yousuke Kagawa, Naoki Kawamura, Atsufumi Yoshida, Makiko Nishida, Namiko Wataya, Takafumi Yamaoka, Masayoshi Tsuyuguchi, Naohiro Uda, Takehiro Takahashi, Mayu Nakano, Yoshiteru Akai, Takuya Izumoto, Shuichi Nonaka, Masahiro Yoshifuji, Kazuhisa Kodama, Yoshinori Mano, Masayuki Ozawa, Tatsuya Ramaswamy, Vijay Taylor, Michael D. Ushijima, Toshikazu Shibui, Soichiro Yamasaki, Mami Arai, Hajime Sakamoto, Hiroaki Nishikawa, Ryo Ichimura, Koichi Acta Neuropathol Commun Research Extensive molecular analyses of ependymal tumors have revealed that supratentorial and posterior fossa ependymomas have distinct molecular profiles and are likely to be different diseases. The presence of C11orf95-RELA fusion genes in a subset of supratentorial ependymomas (ST-EPN) indicated the existence of molecular subgroups. However, the pathogenesis of RELA fusion-negative ependymomas remains elusive. To investigate the molecular pathogenesis of these tumors and validate the molecular classification of ependymal tumors, we conducted thorough molecular analyses of 113 locally diagnosed ependymal tumors from 107 patients in the Japan Pediatric Molecular Neuro-Oncology Group. All tumors were histopathologically reviewed and 12 tumors were re-classified as non-ependymomas. A combination of RT-PCR, FISH, and RNA sequencing identified RELA fusion in 19 of 29 histologically verified ST-EPN cases, whereas another case was diagnosed as ependymoma RELA fusion-positive via the methylation classifier (68.9%). Among the 9 RELA fusion-negative ST-EPN cases, either the YAP1 fusion, BCOR tandem duplication, EP300-BCORL1 fusion, or FOXO1-STK24 fusion was detected in single cases. Methylation classification did not identify a consistent molecular class within this group. Genome-wide methylation profiling successfully sub-classified posterior fossa ependymoma (PF-EPN) into PF-EPN-A (PFA) and PF-EPN-B (PFB). A multivariate analysis using Cox regression confirmed that PFA was the sole molecular marker which was independently associated with patient survival. A clinically applicable pyrosequencing assay was developed to determine the PFB subgroup with 100% specificity using the methylation status of 3 genes, CRIP1, DRD4 and LBX2. Our results emphasized the significance of molecular classification in the diagnosis of ependymomas. RELA fusion-negative ST-EPN appear to be a heterogeneous group of tumors that do not fall into any of the existing molecular subgroups and are unlikely to form a single category. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40478-018-0630-1) contains supplementary material, which is available to authorized users. BioMed Central 2018-12-04 /pmc/articles/PMC6278135/ /pubmed/30514397 http://dx.doi.org/10.1186/s40478-018-0630-1 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Fukuoka, Kohei
Kanemura, Yonehiro
Shofuda, Tomoko
Fukushima, Shintaro
Yamashita, Satoshi
Narushima, Daichi
Kato, Mamoru
Honda-Kitahara, Mai
Ichikawa, Hitoshi
Kohno, Takashi
Sasaki, Atsushi
Hirato, Junko
Hirose, Takanori
Komori, Takashi
Satomi, Kaishi
Yoshida, Akihiko
Yamasaki, Kai
Nakano, Yoshiko
Takada, Ai
Nakamura, Taishi
Takami, Hirokazu
Matsushita, Yuko
Suzuki, Tomonari
Nakamura, Hideo
Makino, Keishi
Sonoda, Yukihiko
Saito, Ryuta
Tominaga, Teiji
Matsusaka, Yasuhiro
Kobayashi, Keiichi
Nagane, Motoo
Furuta, Takuya
Nakada, Mitsutoshi
Narita, Yoshitaka
Hirose, Yuichi
Ohba, Shigeo
Wada, Akira
Shimizu, Katsuyoshi
Kurozumi, Kazuhiko
Date, Isao
Fukai, Junya
Miyairi, Yousuke
Kagawa, Naoki
Kawamura, Atsufumi
Yoshida, Makiko
Nishida, Namiko
Wataya, Takafumi
Yamaoka, Masayoshi
Tsuyuguchi, Naohiro
Uda, Takehiro
Takahashi, Mayu
Nakano, Yoshiteru
Akai, Takuya
Izumoto, Shuichi
Nonaka, Masahiro
Yoshifuji, Kazuhisa
Kodama, Yoshinori
Mano, Masayuki
Ozawa, Tatsuya
Ramaswamy, Vijay
Taylor, Michael D.
Ushijima, Toshikazu
Shibui, Soichiro
Yamasaki, Mami
Arai, Hajime
Sakamoto, Hiroaki
Nishikawa, Ryo
Ichimura, Koichi
Significance of molecular classification of ependymomas: C11orf95-RELA fusion-negative supratentorial ependymomas are a heterogeneous group of tumors
title Significance of molecular classification of ependymomas: C11orf95-RELA fusion-negative supratentorial ependymomas are a heterogeneous group of tumors
title_full Significance of molecular classification of ependymomas: C11orf95-RELA fusion-negative supratentorial ependymomas are a heterogeneous group of tumors
title_fullStr Significance of molecular classification of ependymomas: C11orf95-RELA fusion-negative supratentorial ependymomas are a heterogeneous group of tumors
title_full_unstemmed Significance of molecular classification of ependymomas: C11orf95-RELA fusion-negative supratentorial ependymomas are a heterogeneous group of tumors
title_short Significance of molecular classification of ependymomas: C11orf95-RELA fusion-negative supratentorial ependymomas are a heterogeneous group of tumors
title_sort significance of molecular classification of ependymomas: c11orf95-rela fusion-negative supratentorial ependymomas are a heterogeneous group of tumors
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6278135/
https://www.ncbi.nlm.nih.gov/pubmed/30514397
http://dx.doi.org/10.1186/s40478-018-0630-1
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