Inactivation of the ATMIN/ATM pathway protects against glioblastoma formation

被引:20
作者
Blake, Sophia M. [1 ,2 ,11 ]
Stricker, Stefan H. [3 ,4 ,12 ]
Halavach, Hanna [1 ,2 ]
Poetsch, Anna R. [2 ,5 ,6 ,7 ]
Cresswell, George [2 ,5 ]
Kelly, Gavin [2 ,8 ]
Kanu, Nnennaya [1 ,2 ,13 ]
Marino, Silvia [9 ]
Luscombe, Nicholas M. [2 ,5 ,6 ,7 ]
Pollard, Steven M. [3 ,4 ,14 ]
Behrens, Axel [1 ,2 ,10 ]
机构
[1] Francis Crick Inst, Adult Stem Cell Lab, London, England
[2] Francis Crick Inst, Lincolns Inn Fields Lab, London, England
[3] UCL, Samantha Dickson Brain Canc Unit, London, England
[4] UCL, Dept Canc Biol, UCL Cacn Inst, London, England
[5] Francis Crick Inst, Bioinformat & Computat Biol Lab, London, England
[6] UCL, Dept Genet Evolut & Environm, UCL Genet Inst, London, England
[7] Okinawa Inst Sci & Technol, Onna, Okinawa, Japan
[8] Francis Crick Inst, Bioinformat & Biostat, London, England
[9] Barts & London Queen Marys Sch Med & Dent, Blizard Inst, London, England
[10] Kings Coll London, Fac Life Sci & Med, London WC2R 2LS, England
[11] Boehringer Ingelheim RCV Gmbh & Co KG, Dept Pharmacol & Translat Res, Vienna, Austria
[12] German Res Ctr Environm Hlth, Inst Stem Cell Res, Helmholtz Zentrum Munchn, Neuherberg, Germany
[13] UCL, UCL Canc Iinst, Translat Canc Therapeut Lab, London, England
[14] Univ Edinburgh, MRC Ctr Regenerat Med, Edinburgh, Midlothian, Scotland
基金
英国生物技术与生命科学研究理事会; 欧洲研究理事会; 英国医学研究理事会;
关键词
DNA-DAMAGE-RESPONSE; NEURAL STEM-CELLS; MALIGNANT ASTROCYTIC GLIOMA; ATAXIA-TELANGIECTASIA; IONIZING-RADIATION; HUMAN CANCER; KINASE ATM; P53; GROWTH; INHIBITION;
D O I
10.7554/eLife.08711
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Glioblastoma multiforme (GBM) is the most aggressive human primary brain cancer. Using a Trp53-deficient mouse model of GBM, we show that genetic inactivation of the Atm cofactor Atmin, which is dispensable for embryonic and adult neural development, strongly suppresses GBM formation. Mechanistically, expression of several GBM-associated genes, including Pdgfra, was normalized by Atmin deletion in the Trp53-null background. Pharmacological ATM inhibition also reduced Pdgfra expression, and reduced the proliferation of Trp53-deficient primary glioma cells from murine and human tumors, while normal neural stem cells were unaffected. Analysis of GBM datasets showed that PDGFRA expression is also significantly increased in human TP53-mutant compared with TP53-wild-type tumors. Moreover, combined treatment with ATM and PDGFRA inhibitors efficiently killed TP53-mutant primary human GBM cells, but not untransformed neural stem cells. These results reveal a new requirement for ATMIN-dependent ATM signaling in TP53-deficient GBM, indicating a pro-tumorigenic role for ATM in the context of these tumors.
引用
收藏
页数:24
相关论文
共 61 条
[21]   Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours [J].
Graeber, TG ;
Osmanian, C ;
Jacks, T ;
Housman, DE ;
Koch, CJ ;
Lowe, SW ;
Giaccia, AJ .
NATURE, 1996, 379 (6560) :88-91
[22]  
Hermanson M, 1996, CANCER RES, V56, P164
[23]   Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM [J].
Hickson, I ;
Yan, Z ;
Richardson, CJ ;
Green, SJ ;
Martin, NMB ;
Orr, AI ;
Reaper, PM ;
Jackson, SP ;
Curtin, NJ ;
Smith, GCM .
CANCER RESEARCH, 2004, 64 (24) :9152-9159
[24]  
Homsi Jade, 2007, Cancer Control, V14, P285
[25]   PDGFRα-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling [J].
Jackson, Erica L. ;
Garcia-Verdugo, Jose Manuel ;
Gil-Perotin, Sara ;
Roy, Monica ;
Quinones-Hinojosa, Alfredo ;
VandenBerg, Scott ;
Alvarez-Buylla, Arturo .
NEURON, 2006, 51 (02) :187-199
[26]   Mutational Analysis Reveals the Origin and Therapy-Driven Evolution of Recurrent Glioma [J].
Johnson, Brett E. ;
Mazor, Tali ;
Hong, Chibo ;
Barnes, Michael ;
Aihara, Koki ;
McLean, Cory Y. ;
Fouse, Shaun D. ;
Yamamoto, Shogo ;
Ueda, Hiroki ;
Tatsuno, Kenji ;
Asthana, Saurabh ;
Jalbert, Llewellyn E. ;
Nelson, Sarah J. ;
Bollen, Andrew W. ;
Gustafson, W. Clay ;
Charron, Elise ;
Weiss, William A. ;
Smirnov, Ivan V. ;
Song, Jun S. ;
Olshen, Adam B. ;
Cha, Soonmee ;
Zhao, Yongjun ;
Moore, Richard A. ;
Mungall, Andrew J. ;
Jones, Steven J. M. ;
Hirst, Martin ;
Marra, Marco A. ;
Saito, Nobuhito ;
Aburatani, Hiroyuki ;
Mukasa, Akitake ;
Berger, Mitchel S. ;
Chang, Susan M. ;
Taylor, Barry S. ;
Costello, Joseph F. .
SCIENCE, 2014, 343 (6167) :189-193
[27]   Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer [J].
Jonkers, J ;
Meuwissen, R ;
van der Gulden, H ;
Peterse, H ;
van der Valk, M ;
Berns, A .
NATURE GENETICS, 2001, 29 (04) :418-425
[28]   The Zinc-finger protein ASCIZ regulates B cell development via DYNLL1 and Bim [J].
Jurado, Sabine ;
Gleeson, Kimberly ;
O'Donnell, Kristy ;
Izon, David J. ;
Walkley, Carl R. ;
Strasser, Andreas ;
Tarlinton, David M. ;
Heierhorst, Joerg .
JOURNAL OF EXPERIMENTAL MEDICINE, 2012, 209 (09) :1629-1639
[29]   ATM Substrate Chk2-interacting Zn2+ Finger (ASCIZ) Is a Bi-functional Transcriptional Activator and Feedback Sensor in the Regulation of Dynein Light Chain (DYNLL1) Expression [J].
Jurado, Sabine ;
Conlan, Lindus A. ;
Baker, Emma K. ;
Ng, Jane-Lee ;
Tenis, Nora ;
Hoch, Nicolas C. ;
Gleeson, Kimberly ;
Smeets, Monique ;
Izon, David ;
Heierhorst, Joerg .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2012, 287 (05) :3156-3164
[30]   ATMIN defines an NBS1-independent pathway of ATM signalling [J].
Kanu, Nnennaya ;
Behrens, Axel .
EMBO JOURNAL, 2007, 26 (12) :2933-2941