Skip to main content
Top
Published in: Brain Tumor Pathology 1/2020

Open Access 01-01-2020 | Glioblastoma | Original Article

Giant cell glioblastoma is a distinctive subtype of glioma characterized by vulnerability to DNA damage

Authors: Kaoru Ogawa, Akira Kurose, Akihisa Kamataki, Kenichiro Asano, Kosuke Katayama, Hidekachi Kurotaki

Published in: Brain Tumor Pathology | Issue 1/2020

Login to get access

Abstract

Giant cell glioblastoma (GC-GBM) consists of large cells with pleomorphic nuclei. As a contrast to GC-GBM, we defined monotonous small GBM (MS-GBM) as GBM that consists of small cells with monotonous small nuclei, and compared the DNA damage as well as other pathological features. GC-GBM showed minimal invasion (< 2 mm) and focal sarcomatous areas. TERTp was wild type in GC-GBM but mutant in MS-GBM. OLIG2 expression was significantly higher in MS-GBM (P < 0.01) (77% in MS-GBM and 7% in GC-GBM). GC-GBM showed significantly higher DNA double-strand breaks (DSBs) compared with MS-GBM (P < 0.01) (76% in GC-GBM and 15% in MS-GBM). Nearly, all large cells in GC-GBM underwent DSBs. Thus, significant DSBs in GC-GBM might be induced by an innate lesser stemness characteristic and be followed by mitotic slippage, resulting in polyploidization and the large pleomorphic nuclei. We conclude that GC-GBM is a distinctive subtype of glioma characterized by its vulnerability to DNA damage and that wild-type TERTp and lower OLIG2 function might induce this feature. Notably, even large pleomorphic nuclei with severe DSBs demonstrated Ki67 positivity, which alerts pathologists to the interpretation of Ki67 positivity, because cells with large nuclei undergoing severe DSBs cannot be recognized as proliferating cells that contribute to tumor aggressiveness.
Literature
1.
go back to reference Louis DN, Ohgaki K, Wiestler OD, Cavenee WK, Ellison DW, Figarella-Branger D, Perry A, Reifenberger G, von Deimling A (2016) WHO classification of tumours of the central nervous system. Revised 4th Edition. IARC, Lyon Louis DN, Ohgaki K, Wiestler OD, Cavenee WK, Ellison DW, Figarella-Branger D, Perry A, Reifenberger G, von Deimling A (2016) WHO classification of tumours of the central nervous system. Revised 4th Edition. IARC, Lyon
2.
go back to reference Oh JE, Ohta T, Nonoguchi N, Satomi K, Capper D, Pierscianek D, Sure U, Vital A, Paulus W, Mittelbronn M, Antonelli M, Kleihues P, Giangaspero F, Ohgaki H (2016) Genetic alterations in gliosarcoma and giant cell glioblastoma. Brain Pathol 26(4):517–522CrossRef Oh JE, Ohta T, Nonoguchi N, Satomi K, Capper D, Pierscianek D, Sure U, Vital A, Paulus W, Mittelbronn M, Antonelli M, Kleihues P, Giangaspero F, Ohgaki H (2016) Genetic alterations in gliosarcoma and giant cell glioblastoma. Brain Pathol 26(4):517–522CrossRef
3.
go back to reference Temme A, Geiger KD, Wiedemuth R, Conseur K, Pietsch T, Felsberg J, Reifenberger G, Tatsuka M, Hagel C, Westphal M, Berger H, Simon M, Weller M, Schackert G (2010) Giant cell glioblastoma is associated with altered aurora b expression and concomitant p53 mutation. J Neuropathol Exp Neurol 69(6):632–642CrossRef Temme A, Geiger KD, Wiedemuth R, Conseur K, Pietsch T, Felsberg J, Reifenberger G, Tatsuka M, Hagel C, Westphal M, Berger H, Simon M, Weller M, Schackert G (2010) Giant cell glioblastoma is associated with altered aurora b expression and concomitant p53 mutation. J Neuropathol Exp Neurol 69(6):632–642CrossRef
5.
go back to reference Pujadas E, Chen L, Rodriguez FJ (2019) Pathologic and molecular aspects of anaplasia in circumscribed gliomas and glioneuronal tumors. Brain Tumor Pathol 36(2):40–51CrossRef Pujadas E, Chen L, Rodriguez FJ (2019) Pathologic and molecular aspects of anaplasia in circumscribed gliomas and glioneuronal tumors. Brain Tumor Pathol 36(2):40–51CrossRef
6.
go back to reference Murakami C, Yoshida Y, Yamazaki T, Yamazaki A, Nakata S, Hokama Y, Ishiuchi S, Akimoto J, Shishido-Hara Y, Yoshimoto Y, Matsumura N, Nobusawa S, Ikota H, Yokoo H (2019) Clinicopathological characteristics of circumscribed high-grade astrocytomas with an unusual combination of BRAF V600E, ATRX, and CDKN2A/B alternations. Brain Tumor Pathol 36(3):103–111CrossRef Murakami C, Yoshida Y, Yamazaki T, Yamazaki A, Nakata S, Hokama Y, Ishiuchi S, Akimoto J, Shishido-Hara Y, Yoshimoto Y, Matsumura N, Nobusawa S, Ikota H, Yokoo H (2019) Clinicopathological characteristics of circumscribed high-grade astrocytomas with an unusual combination of BRAF V600E, ATRX, and CDKN2A/B alternations. Brain Tumor Pathol 36(3):103–111CrossRef
7.
go back to reference Kozak KR, Moody JS (2009) Giant cell glioblastoma: a glioblastoma subtype with distinct epidemiology and superior prognosis. Neuro Oncol 11(6):833–841CrossRef Kozak KR, Moody JS (2009) Giant cell glioblastoma: a glioblastoma subtype with distinct epidemiology and superior prognosis. Neuro Oncol 11(6):833–841CrossRef
8.
go back to reference Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273:5858–5868CrossRef Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273:5858–5868CrossRef
9.
go back to reference Sedelnikova OA, Rogakou EP, Panyutin IG, Bonner WM (2002) Quantitative detection of (125) IdU-induced DNA double-strand breaks with gamma-H2AX antibody. Radiat Res 158:486–492CrossRef Sedelnikova OA, Rogakou EP, Panyutin IG, Bonner WM (2002) Quantitative detection of (125) IdU-induced DNA double-strand breaks with gamma-H2AX antibody. Radiat Res 158:486–492CrossRef
10.
go back to reference Rogakou EP, Boon C, Redon C, Bonner WM (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146:905–916CrossRef Rogakou EP, Boon C, Redon C, Bonner WM (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146:905–916CrossRef
12.
go back to reference Sato Y, Kurose A, Ogawa A, Ogasawara K, Traganos F, Darzynkiewicz Z, Sawai T (2009) Diversity of DNA damage response of astrocytes and glioblastoma cell lines with various p53 status to treatment with etoposide and temozolomide. Cancer Biol Ther 8(5):452–457CrossRef Sato Y, Kurose A, Ogawa A, Ogasawara K, Traganos F, Darzynkiewicz Z, Sawai T (2009) Diversity of DNA damage response of astrocytes and glioblastoma cell lines with various p53 status to treatment with etoposide and temozolomide. Cancer Biol Ther 8(5):452–457CrossRef
13.
go back to reference Takami H, Yoshida A, Fukushima S, Arita H, Matsushita Y, Nakamura T, Ohno M, Miyakita Y, Shibui S, Narita Y, Ichimura K (2015) Revisiting TP53 mutations and immunohistochemistry—a comparative study in 157 diffuse gliomas. Brain Pathol 25(3):256–265CrossRef Takami H, Yoshida A, Fukushima S, Arita H, Matsushita Y, Nakamura T, Ohno M, Miyakita Y, Shibui S, Narita Y, Ichimura K (2015) Revisiting TP53 mutations and immunohistochemistry—a comparative study in 157 diffuse gliomas. Brain Pathol 25(3):256–265CrossRef
14.
go back to reference Killela PJ, Reitman ZJ, Jiao Y, Bettegowda C, Agrawal N, Diaz LA Jr, Friedman AH, Friedman H, Gallia GL, Giovanella BC, Grollman AP, He T-C, He Y, Hruban RH, Jallo GI, Mandahl N, Meeker AK, Mertens F, Netto GJ, Ahmed Rasheed B, Riggins GJ, Rosenquist TA, Schiffman M, Shih I-M, Theodorescu D, Torbenson MS, Velculescu VE, Wang T-L, Wentzensen N, Wood LD, Zhang M, McLendon RE, Bigner DD, Kinzler KW, Vogelstein B, Papadopoulos N, Yan H (2013) TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. PNAS 110(15):6021–6026CrossRef Killela PJ, Reitman ZJ, Jiao Y, Bettegowda C, Agrawal N, Diaz LA Jr, Friedman AH, Friedman H, Gallia GL, Giovanella BC, Grollman AP, He T-C, He Y, Hruban RH, Jallo GI, Mandahl N, Meeker AK, Mertens F, Netto GJ, Ahmed Rasheed B, Riggins GJ, Rosenquist TA, Schiffman M, Shih I-M, Theodorescu D, Torbenson MS, Velculescu VE, Wang T-L, Wentzensen N, Wood LD, Zhang M, McLendon RE, Bigner DD, Kinzler KW, Vogelstein B, Papadopoulos N, Yan H (2013) TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. PNAS 110(15):6021–6026CrossRef
15.
go back to reference van den Bent MJ, Dubbink HJ, Marie Y, Brandes AA, Taphoorn MJ, Wesseling P, Frenay M, Tijssen CC, Lacombe D, Idbaih A, van Marion R, Kros JM, Dinjens WN, Gorlia T, Sanson M (2010) IDH1 and IDH2 mutations are prognostic but not predictive for outcome in anaplastic oligodendroglial tumors: a report of the European Organization for Research and Treatment of Cancer Brain Tumor Group. Clin Cancer Res 16(5):1597–1604CrossRef van den Bent MJ, Dubbink HJ, Marie Y, Brandes AA, Taphoorn MJ, Wesseling P, Frenay M, Tijssen CC, Lacombe D, Idbaih A, van Marion R, Kros JM, Dinjens WN, Gorlia T, Sanson M (2010) IDH1 and IDH2 mutations are prognostic but not predictive for outcome in anaplastic oligodendroglial tumors: a report of the European Organization for Research and Treatment of Cancer Brain Tumor Group. Clin Cancer Res 16(5):1597–1604CrossRef
16.
go back to reference Kurose A, Tanaka T, Huang X, Halicka HD, Traganos F, Dai W, Darzynkiewicz Z (2005) Assessment of ATM phosphorylation on Ser-1981 induced by DNA topoisomerase I and II inhibitors in relation to Ser-139-histone H2AX phosphorylation, cell cycle phase, and apoptosis. Cytometry A 68(1):1–9CrossRef Kurose A, Tanaka T, Huang X, Halicka HD, Traganos F, Dai W, Darzynkiewicz Z (2005) Assessment of ATM phosphorylation on Ser-1981 induced by DNA topoisomerase I and II inhibitors in relation to Ser-139-histone H2AX phosphorylation, cell cycle phase, and apoptosis. Cytometry A 68(1):1–9CrossRef
18.
go back to reference Hide T, Shibahara I, Kumabe T (2019) Novel concept of the border niche: glioblastoma cells use oligodendrocytes progenitor cells (GAOs) and microglia to acquire stem cell-like features. Brain Tumor Pathol 36(2):63–73CrossRef Hide T, Shibahara I, Kumabe T (2019) Novel concept of the border niche: glioblastoma cells use oligodendrocytes progenitor cells (GAOs) and microglia to acquire stem cell-like features. Brain Tumor Pathol 36(2):63–73CrossRef
20.
go back to reference Cheng B, Crasta K (2017) Consequences of mitotic slippage for antimicrotubule drug therapy. Endocr Relat Cancer 24(9):T97–T106CrossRef Cheng B, Crasta K (2017) Consequences of mitotic slippage for antimicrotubule drug therapy. Endocr Relat Cancer 24(9):T97–T106CrossRef
21.
go back to reference Mosrati MA, Malmström A, Lysiak M, Krysztofiak A, Hallbeck M, Milos P, Hallbeck AL, Bratthäll C, Strandéus M, Stenmark-Askmalm M, Söderkvist P (2015) TERT promoter mutations and polymorphisms as prognostic factors in primary glioblastoma. Oncotarget 6(18):16663–16673CrossRef Mosrati MA, Malmström A, Lysiak M, Krysztofiak A, Hallbeck M, Milos P, Hallbeck AL, Bratthäll C, Strandéus M, Stenmark-Askmalm M, Söderkvist P (2015) TERT promoter mutations and polymorphisms as prognostic factors in primary glioblastoma. Oncotarget 6(18):16663–16673CrossRef
22.
go back to reference Ahmad F, Patrick S, Sheikh T, Sharma V, Pathak P, Malgulwar PB, Kumar A, Joshi SD, Sarkar C, Sen E (2017) Telomerase reverse transcriptase (TERT)—enhancer of zeste homolog 2 (EZH2) network regulates lipid metabolism and DNA damage responses in glioblastoma. J Neurochem 143(6):671–683CrossRef Ahmad F, Patrick S, Sheikh T, Sharma V, Pathak P, Malgulwar PB, Kumar A, Joshi SD, Sarkar C, Sen E (2017) Telomerase reverse transcriptase (TERT)—enhancer of zeste homolog 2 (EZH2) network regulates lipid metabolism and DNA damage responses in glioblastoma. J Neurochem 143(6):671–683CrossRef
24.
go back to reference Ligon KL, Alberta JA, Kho AT, Weiss J, Kwaan MR, Nutt CL, Louis DN, Stiles CD, Rowitch DH (2004) The oligodendroglial lineage marker OLIG2 is universally expressed in diffuse gliomas. J Neuropathol Exp Neurol 63(5):499–509CrossRef Ligon KL, Alberta JA, Kho AT, Weiss J, Kwaan MR, Nutt CL, Louis DN, Stiles CD, Rowitch DH (2004) The oligodendroglial lineage marker OLIG2 is universally expressed in diffuse gliomas. J Neuropathol Exp Neurol 63(5):499–509CrossRef
25.
go back to reference Suvà ML, Rheinbay E, Gillespie SM, Patel AP, Wakimoto H, Rabkin SD, Riggi N, Chi AS, Cahill DP, Nahed BV, Curry WT, Martuza RL, Rivera MN, Rossetti N, Kasif S, Beik S, Kadri S, Tirosh I, Wortman I, Shalek AK, Rozenblatt-Rosen O, Regev A, Louis DN, Bernstein BE (2014) Reconstructing and reprogramming the tumor-propagating potential of glioblastoma stem-like cells. Cell 157(3):580–594CrossRef Suvà ML, Rheinbay E, Gillespie SM, Patel AP, Wakimoto H, Rabkin SD, Riggi N, Chi AS, Cahill DP, Nahed BV, Curry WT, Martuza RL, Rivera MN, Rossetti N, Kasif S, Beik S, Kadri S, Tirosh I, Wortman I, Shalek AK, Rozenblatt-Rosen O, Regev A, Louis DN, Bernstein BE (2014) Reconstructing and reprogramming the tumor-propagating potential of glioblastoma stem-like cells. Cell 157(3):580–594CrossRef
Metadata
Title
Giant cell glioblastoma is a distinctive subtype of glioma characterized by vulnerability to DNA damage
Authors
Kaoru Ogawa
Akira Kurose
Akihisa Kamataki
Kenichiro Asano
Kosuke Katayama
Hidekachi Kurotaki
Publication date
01-01-2020
Publisher
Springer Singapore
Published in
Brain Tumor Pathology / Issue 1/2020
Print ISSN: 1433-7398
Electronic ISSN: 1861-387X
DOI
https://doi.org/10.1007/s10014-019-00355-w