TERT promoter mutation status is necessary and sufficient to diagnose IDH-wildtype diffuse astrocytic glioma with molecular features of glioblastoma

被引：76

作者：

Fujimoto, Kenji ^{[1
,2
]}

Arita, Hideyuki ^{[1
,3
]}

Satomi, Kaishi ^{[1
,4
]}

Yamasaki, Kai ^{[1
,5
]}

Matsushita, Yuko ^{[1
,6
]}

Nakamura, Taishi ^{[1
,7
]}

Miyakita, Yasuji ^{[6
]}

Umehara, Toru ^{[3
]}

Kobayashi, Keiichi ^{[8
]}

Tamura, Kaoru ^{[9
]}

Tanaka, Shota ^{[10
]}

Higuchi, Fumi ^{[11
]}

Okita, Yoshiko ^{[12
]}

Kanemura, Yonehiro ^{[13
]}

Fukai, Junya ^{[14
]}

Sakamoto, Daisuke ^{[15
]}

Uda, Takehiro ^{[16
]}

Machida, Ryunosuke ^{[17
]}

Kuchiba, Aya ^{[18
]}

Maehara, Taketoshi ^{[9
]}

Nagane, Motoo ^{[8
]}

Nishikawa, Ryo ^{[18
]}

Suzuki, Hiroyoshi ^{[19
]}

Shibuya, Makoto ^{[20
]}

Komori, Takashi ^{[21
]}

Narita, Yoshitaka ^{[6
]}

Ichimura, Koichi ^{[1
,22
]}

机构：

[1] Natl Canc Ctr, Div Brain Tumor Translat Res, Chuo Ku, 5-1-1 Tsukiji, Tokyo 1040045, Japan

[2] Kumamoto Univ, Grad Sch Life Sci, Dept Neurosurg, Kumamoto, Japan

[3] Osaka Univ, Dept Neurosurg, Grad Sch Med, Osaka, Japan

[4] Natl Canc Ctr, Dept Diagnost Pathol, Tokyo, Japan

[5] Osaka City Gen Hosp, Dept Pediat Hematol & Oncol, Osaka, Japan

[6] Natl Canc Ctr, Dept Neurosurg & Neurooncol, Tokyo, Japan

[7] Yokohama City Univ, Grad Sch Med, Dept Neurosurg, Yokohama, Kanagawa, Japan

[8] Kyorin Univ, Fac Med, Dept Neurosurg, Tokyo, Japan

[9] Tokyo Med & Dent Univ, Dept Neurosurg, Tokyo, Japan

[10] Univ Tokyo, Dept Neurosurg, Tokyo, Japan

[11] Dokkyo Med Univ, Dept Neurosurg, Mibu, Tochigi, Japan

[12] Osaka Int Canc Inst, Dept Neurosurg, Osaka, Japan

[13] Natl Hosp Org, Inst Clin Res, Dept Biomed Res & Innovat, Osaka Natl Hosp, Osaka, Japan

[14] Wakayama Med Univ, Dept Neurol Surg, Wakayama, Japan

[15] Hyogo Coll Med, Dept Neurosurg, Nishinomiya, Hyogo, Japan

[16] Osaka City Univ, Dept Neurosurg, Grad Sch Med, Osaka, Japan

[17] Natl Canc Ctr, Ctr Res Adm & Support, Biostat Div, Tokyo, Japan

[18] Saitama Med Univ, Dept Neurooncol Neurosurg, Int Med Ctr, Saitama, Japan

[19] Natl Hosp Org, Sendai Med Ctr, Dept Pathol & Lab Med, Sendai, Miyagi, Japan

[20] Tokyo Med Univ, Hachi Med Ctr, Cent Clin Lab, Tokyo, Japan

[21] Tokyo Metropolitan Neurol Hosp, Dept Lab Med & Pathol Neuropathol, Tokyo, Japan

[22] Juntendo Univ, Dept Brain Dis Translat Res, Fac Med, Bunkyo Ku, 2-1-1 Hongo, Tokyo 1138421, Japan

来源：

ACTA NEUROPATHOLOGICA | 2021年 / 142卷 / 02期

关键词：

Lower grade glioma; IDH-wildtype; TERT promoter mutation; Copy-number alteration; CENTRAL-NERVOUS-SYSTEM; METHYLATION; CLASSIFICATION; AMPLIFICATION; PROGRESSION; TUMORS; TOOL;

D O I：

10.1007/s00401-021-02337-9

中图分类号：

R74 [神经病学与精神病学];

学科分类号：

摘要：

The Consortium to Inform Molecular and Practical Approaches to CNS Tumor Taxonomy (cIMPACT-NOW) update 3 recommends that histologic grade II and III IDH-wildtype diffuse astrocytic gliomas that harbor EGFR amplification, the combination of whole chromosome 7 gain and whole chromosome 10 loss (7 + /10 -), or TERT promoter (pTERT) mutations should be considered as glioblastomas (GBM), World Health Organization grade IV. In this retrospective study, we examined the utility of molecular classification based on pTERT status and copy-number alterations (CNAs) in IDH-wildtype lower grade gliomas (LGGs, grade II, and III). The impact on survival was evaluated for the pTERT mutation and CNAs, including EGFR gain/amplification, PTEN loss, CDKN2A homozygous deletion, and PDGFRA gain/amplification. We analyzed 46 patients with IDH-wildtype/pTERT-mutant (mut) LGGs and 85 with IDH-wildtype/pTERT-wildtype LGGs. EGFR amplification and a combination of EGFR gain and PTEN loss (EGFR + /PTEN -) were significantly more frequent in pTERT-mut patients (p < 0.0001). Cox regression analysis showed that the pTERT mutation was a significant predictor of poor prognosis (hazard ratio [HR] 2.79, 95% confidence interval [CI] 1.55-4.89, p = 0.0008), but neither EGFR amplification nor EGFR + /PTEN - was an independent prognostic factor in IDH-wildtype LGGs. PDGFRA gain/amplification was a significant poor prognostic factor in IDH-wildtype/pTERT-wildtype LGGs (HR 2.44, 95% CI 1.09-5.27, p = 0.03, Cox regression analysis). The IDH-wildtype LGGs with either pTERT-mut or PDGFRA amplification were mostly clustered with GBM by DNA methylation analysis. Thus, our study suggests that analysis of pTERT mutation status is necessary and sufficient to diagnose IDH-wildtype diffuse astrocytic gliomas with molecular features of glioblastoma. The PDGFRA status may help further delineate IDH-wildtype/pTERT-wildtype LGGs. Methylation profiling showed that IDH-wildtype LGGs without molecular features of GBM were a heterogeneous group of tumors. Some of them did not fall into existing categories and had significantly better prognoses than those clustered with GBM.

引用

页码：323 / 338

页数：16

共 26 条

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← 1 2 3 →

共 26 条

[1] Prognostic relevance of genetic alterations in diffuse lower-grade gliomas [J].

Aoki, Kosuke ;

Nakamura, Hideo ;

Suzuki, Hiromichi ;

Matsuo, Keitaro ;

Kataoka, Keisuke ;

Shimamura, Teppei ;

Motomura, Kazuya ;

Ohka, Fumiharu ;

Shiina, Satoshi ;

Yamamoto, Takashi ;

Nagata, Yasunobu ;

Yoshizato, Tetsuichi ;

Mizoguchi, Masahiro ;

Abe, Tatsuya ;

Momii, Yasutomo ;

Muragaki, Yoshihiro ;

Watanabe, Reiko ;

Ito, Ichiro ;

Sanada, Masashi ;

Yajima, Hironori ;

Morita, Naoya ;

Takeuchi, Ichiro ;

Miyano, Satoru ;

Wakabayashi, Toshihiko ;

Ogawa, Seishi ;

Natsume, Atsushi .

NEURO-ONCOLOGY, 2018, 20 (01) :66-77

[2] A combination of TERT promoter mutation and MGMT methylation status predicts clinically relevant subgroups of newly diagnosed glioblastomas [J].

Arita, Hideyuki ;

Yamasaki, Kai ;

Matsushita, Yuko ;

Nakamura, Taishi ;

Shimokawa, Asanao ;

Takami, Hirokazu ;

Tanaka, Shota ;

Mukasa, Akitake ;

Shirahata, Mitsuaki ;

Shimizu, Saki ;

Suzuki, Kaori ;

Saito, Kuniaki ;

Kobayashi, Keiichi ;

Higuchi, Fumi ;

Uzuka, Takeo ;

Otani, Ryohei ;

Tamura, Kaoru ;

Sumita, Kazutaka ;

Ohno, Makoto ;

Miyakita, Yasuji ;

Kagawa, Naoki ;

Hashimoto, Naoya ;

Hatae, Ryusuke ;

Yoshimoto, Koji ;

Shinojima, Naoki ;

Nakamura, Hideo ;

Kanemura, Yonehiro ;

Okita, Yoshiko ;

Kinoshita, Manabu ;

Ishibashi, Kenichi ;

Shofuda, Tomoko ;

Kodama, Yoshinori ;

Mori, Kanji ;

Tomogane, Yusuke ;

Fukai, Junya ;

Fujita, Koji ;

Terakawa, Yuzo ;

Tsuyuguchi, Naohiro ;

Moriuchi, Shusuke ;

Nonaka, Masahiro ;

Suzuki, Hiroyoshi ;

Shibuya, Makoto ;

Maehara, Taketoshi ;

Saito, Nobuhito ;

Nagane, Motoo ;

Kawahara, Nobutaka ;

Ueki, Keisuke ;

Yoshimine, Toshiki ;

Miyaoka, Etsuo ;

Nishikawa, Ryo .

ACTA NEUROPATHOLOGICA COMMUNICATIONS, 2016, 4 :79

[3] Upregulating mutations in the TERT promoter commonly occur in adult malignant gliomas and are strongly associated with total 1p19q loss [J].

Arita, Hideyuki ;

Narita, Yoshitaka ;

Fukushima, Shintaro ;

Tateishi, Kensuke ;

Matsushita, Yuko ;

Yoshida, Akihiko ;

Miyakita, Yasuji ;

Ohno, Makoto ;

Collins, V. Peter ;

Kawahara, Nobutaka ;

Shibui, Soichiro ;

Ichimura, Koichi .

ACTA NEUROPATHOLOGICA, 2013, 126 (02) :267-276

[4] cIMPACT-NOW update 5: recommended grading criteria and terminologies for IDH-mutant astrocytomas [J].

Brat, Daniel J. ;

Aldape, Kenneth ;

Colman, Howard ;

Figrarella-Branger, Dominique ;

Fuller, Gregory N. ;

Giannini, Caterina ;

Holland, Eric C. ;

Jenkins, Robert B. ;

Kleinschmidt-DeMasters, Bette ;

Komori, Takashi ;

Kros, Johan M. ;

Louis, David N. ;

McLean, Catriona ;

Perry, Arie ;

Reifenberger, Guido ;

Sarkar, Chitra ;

Stupp, Roger ;

van den Bent, Martin J. ;

von Deimling, Andreas ;

Weller, Michael .

ACTA NEUROPATHOLOGICA, 2020, 139 (03) :603-608

[5] cIMPACT-NOW update 3: recommended diagnostic criteria for "Diffuse astrocytic glioma, IDH-wildtype, with molecular features of glioblastoma, WHO grade IV" [J].

Brat, Daniel J. ;

Aldape, Kenneth ;

Colman, Howard ;

Holland, Eric C. ;

Louis, David N. ;

Jenkins, Robert B. ;

Kleinschmidt-DeMasters, B. K. ;

Perry, Arie ;

Reifenberger, Guido ;

Stupp, Roger ;

von Deimling, Andreas ;

Weller, Michael .

ACTA NEUROPATHOLOGICA, 2018, 136 (05) :805-810

[6] Comprehensive, Integrative Genomic Analysis of Diffuse Lower-Grade Gliomas [J].

Brat, Daniel J. ;

Verhaak, Roel G. W. ;

Al-dape, Kenneth D. ;

Yung, W. K. Alfred ;

Salama, Sofie R. ;

Cooper, Lee A. D. ;

Rheinbay, Esther ;

Miller, C. Ryan ;

Vitucci, Mark ;

Morozova, Olena ;

Robertson, A. Gordon ;

Noushmehr, Houtan ;

Laird, Peter W. ;

Cherniack, Andrew D. ;

Akbani, Rehan ;

Huse, Jason T. ;

Ciriello, Giovanni ;

Poisson, Laila M. ;

Barnholtz-Sloan, Jill S. ;

Berger, Mitchel S. ;

Brennan, Cameron ;

Colen, Rivka R. ;

Colman, Howard ;

Flanders, Adam E. ;

Giannini, Caterina ;

Grifford, Mia ;

Iavarone, Antonio ;

Jain, Rajan ;

Joseph, Isaac ;

Kim, Jaegil ;

Kasaian, Katayoon ;

Mikkelsen, Tom ;

Murray, Bradley A. ;

O'Neill, Brian Patrick ;

Pachter, Lior ;

Parsons, Donald W. ;

Sougnez, Carrie ;

Sulman, Erik P. ;

Vandenberg, Scott R. ;

Van Meir, Erwin G. ;

von Deimling, Andreas ;

Zhang, Hailei ;

Crain, Daniel ;

Lau, Kevin ;

Mallery, David ;

Morris, Scott ;

Paulauskis, Joseph ;

Penny, Robert ;

Shelton, Troy ;

Sherman, Mark .

NEW ENGLAND JOURNAL OF MEDICINE, 2015, 372 (26) :2481-2498

[7] The Somatic Genomic Landscape of Glioblastoma [J].

Brennan, Cameron W. ;

Verhaak, Roel G. W. ;

McKenna, Aaron ;

Campos, Benito ;

Noushmehr, Houtan ;

Salama, Sofie R. ;

Zheng, Siyuan ;

Chakravarty, Debyani ;

Sanborn, J. Zachary ;

Berman, Samuel H. ;

Beroukhim, Rameen ;

Bernard, Brady ;

Wu, Chang-Jiun ;

Genovese, Giannicola ;

Shmulevich, Ilya ;

Barnholtz-Sloan, Jill ;

Zou, Lihua ;

Vegesna, Rahulsimham ;

Shukla, Sachet A. ;

Ciriello, Giovanni ;

Yung, W. K. ;

Zhang, Wei ;

Sougnez, Carrie ;

Mikkelsen, Tom ;

Aldape, Kenneth ;

Bigner, Darell D. ;

Van Meir, Erwin G. ;

Prados, Michael ;

Sloan, Andrew ;

Black, Keith L. ;

Eschbacher, Jennifer ;

Finocchiaro, Gaetano ;

Friedman, William ;

Andrews, David W. ;

Guha, Abhijit ;

Iacocca, Mary ;

O'Neill, Brian P. ;

Foltz, Greg ;

Myers, Jerome ;

Weisenberger, Daniel J. ;

Penny, Robert ;

Kucherlapati, Raju ;

Perou, Charles M. ;

Hayes, D. Neil ;

Gibbs, Richard ;

Marra, Marco ;

Mills, Gordon B. ;

Lander, Eric ;

Spellman, Paul ;

Wilson, Richard .

CELL, 2013, 155 (02) :462-477

[8] DNA methylation-based classification of central nervous system tumours [J].

Capper, David ;

Jones, David T. W. ;

Sill, Martin ;

Hovestadt, Volker ;

Schrimpf, Daniel ;

Sturm, Dominik ;

Koelsche, Christian ;

Sahm, Felix ;

Chavez, Lukas ;

Reuss, David E. ;

Kratz, Annekathrin ;

Wefers, Annika K. ;

Huang, Kristin ;

Pajtler, Kristian W. ;

Schweizer, Leonille ;

Stichel, Damian ;

Olar, Adriana ;

Engel, Nils W. ;

Lindenberg, Kerstin ;

Harter, Patrick N. ;

Braczynski, Anne K. ;

Plate, Karl H. ;

Dohmen, Hildegard ;

Garvalov, Boyan K. ;

Coras, Roland ;

Hoelsken, Annett ;

Hewer, Ekkehard ;

Bewerunge-Hudler, Melanie ;

Schick, Matthias ;

Fischer, Roger ;

Beschorner, Rudi ;

Schittenhelm, Jens ;

Staszewski, Ori ;

Wani, Khalida ;

Varlet, Pascale ;

Pages, Melanie ;

Temming, Petra ;

Lohmann, Dietmar ;

Selt, Florian ;

Witt, Hendrik ;

Milde, Till ;

Witt, Olaf ;

Aronica, Eleonora ;

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