BRCA1-associated protein inhibits glioma cell proliferation and migration and glioma stem cell self-renewal via the TGF-β/PI3K/AKT/mTOR signalling pathway

go back to reference K.A. McNeill, Epidemiology of brain tumors. Neurol Clin 34, 981–998 (2016)CrossRef K.A. McNeill, Epidemiology of brain tumors. Neurol Clin 34, 981–998 (2016)CrossRef

go back to reference Q.T. Ostrom, H. Gittleman, L. Stetson, S. Virk, J.S. Barnholtz-Sloan, Epidemiology of intracranial Gliomas. Prog Neurol 30, 1–11 (2018) Q.T. Ostrom, H. Gittleman, L. Stetson, S. Virk, J.S. Barnholtz-Sloan, Epidemiology of intracranial Gliomas. Prog Neurol 30, 1–11 (2018)

go back to reference R. Stupp, M. Brada, M.J. van den Bent, J.C. Tonn, G. Pentheroudakis, High-grade glioma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 25(Suppl 3), iii93–ii101 (2014) R. Stupp, M. Brada, M.J. van den Bent, J.C. Tonn, G. Pentheroudakis, High-grade glioma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 25(Suppl 3), iii93–ii101 (2014)

go back to reference D. Matias, J. Balca-Silva, L.G. Dubois, B. Pontes, V.P. Ferrer, L. Rosario, A. do Carmo, J. Echevarria-Lima, A.B. Sarmento-Ribeiro, M.C. Lopes, V. Moura-Neto, Dual treatment with shikonin and temozolomide reduces glioblastoma tumor growth, migration and glial-to-mesenchymal transition. Cell Oncol 40, 247–261 (2017) D. Matias, J. Balca-Silva, L.G. Dubois, B. Pontes, V.P. Ferrer, L. Rosario, A. do Carmo, J. Echevarria-Lima, A.B. Sarmento-Ribeiro, M.C. Lopes, V. Moura-Neto, Dual treatment with shikonin and temozolomide reduces glioblastoma tumor growth, migration and glial-to-mesenchymal transition. Cell Oncol 40, 247–261 (2017)

go back to reference J.I. Bastien, K.A. McNeill, H.A. Fine, Molecular characterizations of glioblastoma, targeted therapy, and clinical results to date. Cancer 121, 502–516 (2015)CrossRef J.I. Bastien, K.A. McNeill, H.A. Fine, Molecular characterizations of glioblastoma, targeted therapy, and clinical results to date. Cancer 121, 502–516 (2015)CrossRef

go back to reference S. Li, C.Y. Ku, A.A. Farmer, Y.S. Cong, C.F. Chen, W.H. Lee, Identification of a novel cytoplasmic protein that specifically binds to nuclear localization signal motifs. J Biol Chem 273, 6183–6189 (1998)CrossRef S. Li, C.Y. Ku, A.A. Farmer, Y.S. Cong, C.F. Chen, W.H. Lee, Identification of a novel cytoplasmic protein that specifically binds to nuclear localization signal motifs. J Biol Chem 273, 6183–6189 (1998)CrossRef

go back to reference C. Chen, R.E. Lewis, M.A. White, IMP modulates KSR1-dependent multivalent complex formation to specify ERK1/2 pathway activation and response thresholds. J Biol Chem 283, 12789–12796 (2008)CrossRef C. Chen, R.E. Lewis, M.A. White, IMP modulates KSR1-dependent multivalent complex formation to specify ERK1/2 pathway activation and response thresholds. J Biol Chem 283, 12789–12796 (2008)CrossRef

go back to reference S.D. Hayes, H. Liu, E. MacDonald, C.M. Sanderson, J.M. Coulson, M.J. Clague, S. Urbe, Direct and indirect control of mitogen-activated protein kinase pathway-associated components, BRAP/IMP E3 ubiquitin ligase and CRAF/RAF1 kinase, by the deubiquitylating enzyme USP15. J Biol Chem 287, 43007–43018 (2012)CrossRef S.D. Hayes, H. Liu, E. MacDonald, C.M. Sanderson, J.M. Coulson, M.J. Clague, S. Urbe, Direct and indirect control of mitogen-activated protein kinase pathway-associated components, BRAP/IMP E3 ubiquitin ligase and CRAF/RAF1 kinase, by the deubiquitylating enzyme USP15. J Biol Chem 287, 43007–43018 (2012)CrossRef

go back to reference S.A. Matheny, C. Chen, R.L. Kortum, G.L. Razidlo, R.E. Lewis, M.A. White, Ras regulates assembly of mitogenic signalling complexes through the effector protein IMP. Nature 427, 256–260 (2004)CrossRef S.A. Matheny, C. Chen, R.L. Kortum, G.L. Razidlo, R.E. Lewis, M.A. White, Ras regulates assembly of mitogenic signalling complexes through the effector protein IMP. Nature 427, 256–260 (2004)CrossRef

go back to reference S.A. Matheny, M.A. White, Ras-sensitive IMP modulation of the Raf/MEK/ERK cascade through KSR1. Methods Enzymol 407, 237–247 (2006)CrossRef S.A. Matheny, M.A. White, Ras-sensitive IMP modulation of the Raf/MEK/ERK cascade through KSR1. Methods Enzymol 407, 237–247 (2006)CrossRef

go back to reference S.A. Matheny, M.A. White, Signaling threshold regulation by the Ras effector IMP. J Biol Chem 284, 11007–11011 (2009)CrossRef S.A. Matheny, M.A. White, Signaling threshold regulation by the Ras effector IMP. J Biol Chem 284, 11007–11011 (2009)CrossRef

go back to reference S. Shoji, K. Hanada, N. Ohsawa, M. Shirouzu, Central catalytic domain of BRAP (RNF52) recognizes the types of ubiquitin chains and utilizes oligoubiquitin for ubiquitylation. Biochem J 474, 3207–3226 (2017) S. Shoji, K. Hanada, N. Ohsawa, M. Shirouzu, Central catalytic domain of BRAP (RNF52) recognizes the types of ubiquitin chains and utilizes oligoubiquitin for ubiquitylation. Biochem J 474, 3207–3226 (2017)

go back to reference J. Czyzyk, H.C. Chen, K. Bottomly, R.A. Flavell, p21 Ras/impedes mitogenic signal propagation regulates cytokine production and migration in CD4 T cells. J Biol Chem 283, 23004–23015 (2008)CrossRef J. Czyzyk, H.C. Chen, K. Bottomly, R.A. Flavell, p21 Ras/impedes mitogenic signal propagation regulates cytokine production and migration in CD4 T cells. J Biol Chem 283, 23004–23015 (2008)CrossRef

go back to reference R.G. Davies, K.M. Wagstaff, E.A. McLaughlin, K.L. Loveland, D.A. Jans, The BRCA1-binding protein BRAP2 can act as a cytoplasmic retention factor for nuclear and nuclear envelope-localizing testicular proteins. Biochim Biophys Acta 1833, 3436–3444 (2013)CrossRef R.G. Davies, K.M. Wagstaff, E.A. McLaughlin, K.L. Loveland, D.A. Jans, The BRCA1-binding protein BRAP2 can act as a cytoplasmic retention factor for nuclear and nuclear envelope-localizing testicular proteins. Biochim Biophys Acta 1833, 3436–3444 (2013)CrossRef

go back to reference M. Asada, K. Ohmi, D. Delia, S. Enosawa, S. Suzuki, A. Yuo, H. Suzuki, S. Mizutani, Brap2 functions as a cytoplasmic retention protein for p21 during monocyte differentiation. Mol Cell Biol 24, 8236–8243 (2004)CrossRef M. Asada, K. Ohmi, D. Delia, S. Enosawa, S. Suzuki, A. Yuo, H. Suzuki, S. Mizutani, Brap2 functions as a cytoplasmic retention protein for p21 during monocyte differentiation. Mol Cell Biol 24, 8236–8243 (2004)CrossRef

go back to reference A.J. Fulcher, D.M. Roth, S. Fatima, G. Alvisi, D.A. Jans, The BRCA-1 binding protein BRAP2 is a novel, negative regulator of nuclear import of viral proteins, dependent on phosphorylation flanking the nuclear localization signal. FASEB J 24, 1454–1466 (2010) A.J. Fulcher, D.M. Roth, S. Fatima, G. Alvisi, D.A. Jans, The BRCA-1 binding protein BRAP2 is a novel, negative regulator of nuclear import of viral proteins, dependent on phosphorylation flanking the nuclear localization signal. FASEB J 24, 1454–1466 (2010)

go back to reference K. Ozaki, H. Sato, K. Inoue, T. Tsunoda, Y. Sakata, H. Mizuno, T.H. Lin, Y. Miyamoto, A. Aoki, Y. Onouchi, S.H. Sheu, S. Ikegawa, K. Odashiro, M. Nobuyoshi, S.H. Juo, M. Hori, Y. Nakamura, T. Tanaka, SNPs in BRAP associated with risk of myocardial infarction in Asian populations. Nat Genet 41, 329–333 (2009)CrossRef K. Ozaki, H. Sato, K. Inoue, T. Tsunoda, Y. Sakata, H. Mizuno, T.H. Lin, Y. Miyamoto, A. Aoki, Y. Onouchi, S.H. Sheu, S. Ikegawa, K. Odashiro, M. Nobuyoshi, S.H. Juo, M. Hori, Y. Nakamura, T. Tanaka, SNPs in BRAP associated with risk of myocardial infarction in Asian populations. Nat Genet 41, 329–333 (2009)CrossRef

go back to reference L. Wu, B. Xi, D. Hou, X. Zhao, J. Liu, H. Cheng, Y. Shen, X. Wang, J. Mi, The single nucleotide polymorphisms in BRAP decrease the risk of metabolic syndrome in a Chinese young adult population. Diab Vasc Dis Res 10, 202–207 (2013)CrossRef L. Wu, B. Xi, D. Hou, X. Zhao, J. Liu, H. Cheng, Y. Shen, X. Wang, J. Mi, The single nucleotide polymorphisms in BRAP decrease the risk of metabolic syndrome in a Chinese young adult population. Diab Vasc Dis Res 10, 202–207 (2013)CrossRef

go back to reference Y.C. Liao, Y.S. Wang, Y.C. Guo, K. Ozaki, T. Tanaka, H.F. Lin, M.H. Chang, K.C. Chen, M.L. Yu, S.H. Sheu, S.H. Juo, BRAP activates inflammatory cascades and increases the risk for carotid atherosclerosis. Mol Med 17, 1065–1074 (2011)CrossRef Y.C. Liao, Y.S. Wang, Y.C. Guo, K. Ozaki, T. Tanaka, H.F. Lin, M.H. Chang, K.C. Chen, M.L. Yu, S.H. Sheu, S.H. Juo, BRAP activates inflammatory cascades and increases the risk for carotid atherosclerosis. Mol Med 17, 1065–1074 (2011)CrossRef

go back to reference F. Zhang, C. Liu, Y. Xu, G. Qi, G. Yuan, Z. Cheng, J. Wang, G. Wang, Z. Wang, W. Zhu, Z. Zhou, X. Zhao, L. Tian, C. Jin, J. Yuan, G. Zhang, Y. Chen, L. Wang, T. Lu, H. Yan, Y. Ruan, W. Yue, D. Zhang, A two-stage association study suggests BRAP as a susceptibility gene for schizophrenia. PLoS One 9, e86037 (2014)CrossRef F. Zhang, C. Liu, Y. Xu, G. Qi, G. Yuan, Z. Cheng, J. Wang, G. Wang, Z. Wang, W. Zhu, Z. Zhou, X. Zhao, L. Tian, C. Jin, J. Yuan, G. Zhang, Y. Chen, L. Wang, T. Lu, H. Yan, Y. Ruan, W. Yue, D. Zhang, A two-stage association study suggests BRAP as a susceptibility gene for schizophrenia. PLoS One 9, e86037 (2014)CrossRef

go back to reference J.W. Kim, Y.M. Choe, J.G. Shin, B.L. Park, H.D. Shin, I.G. Choi, B.C. Lee, Associations of BRAP polymorphisms with the risk of alcohol dependence and scores on the alcohol use disorders identification test. Neuropsychiatr Dis Treat 15, 83–94 (2019)CrossRef J.W. Kim, Y.M. Choe, J.G. Shin, B.L. Park, H.D. Shin, I.G. Choi, B.C. Lee, Associations of BRAP polymorphisms with the risk of alcohol dependence and scores on the alcohol use disorders identification test. Neuropsychiatr Dis Treat 15, 83–94 (2019)CrossRef

go back to reference Y. Zhao, L. Wei, M. Shao, X. Huang, J. Chang, J. Zheng, J. Chu, Q. Cui, L. Peng, Y. Luo, W. Tan, W. Tan, D. Lin, C. Wu, BRCA1-Associated Protein Increases Invasiveness of Esophageal Squamous Cell Carcinoma. Gastroenterology 153, 1304–1319 e1305 (2017) Y. Zhao, L. Wei, M. Shao, X. Huang, J. Chang, J. Zheng, J. Chu, Q. Cui, L. Peng, Y. Luo, W. Tan, W. Tan, D. Lin, C. Wu, BRCA1-Associated Protein Increases Invasiveness of Esophageal Squamous Cell Carcinoma. Gastroenterology 153, 1304–1319 e1305 (2017)

go back to reference J. Tang, S. Xi, G. Wang, B. Wang, S. Yan, Y. Wu, Y. Sang, W. Wu, R. Zhang, T. Kang, Prognostic significance of BRCA1-associated protein 1 in colorectal cancer. Med Oncol 30, 541 (2013)CrossRef J. Tang, S. Xi, G. Wang, B. Wang, S. Yan, Y. Wu, Y. Sang, W. Wu, R. Zhang, T. Kang, Prognostic significance of BRCA1-associated protein 1 in colorectal cancer. Med Oncol 30, 541 (2013)CrossRef

go back to reference F.R. Schumacher, S.L. Schmit, S. Jiao, C.K. Edlund, H. Wang, B. Zhang, L. Hsu, S.C. Huang, C.P. Fischer, J.F. Harju, G.E. Idos, F. Lejbkowicz, F.J. Manion, K. McDonnell, C.E. McNeil, M. Melas, H.S. Rennert, W. Shi, D.C. Thomas, D.J. Van Den Berg, C.M. Hutter, A.K. Aragaki, K. Butterbach, B.J. Caan, C.S. Carlson, S.J. Chanock, K.R. Curtis, C.S. Fuchs, M. Gala, E.L. Giovannucc, S.M. Gogarten, R.B. Hayes, B. Henderson, D.J. Hunter, R.D. Jackson, L.N. Kolonel, C. Kooperberg, S. Kury, A. LaCroix, C.C. Laurie, C.A. Laurie, M. Lemire, D. Levine, J. Ma, K.W. Makar, C. Qu, D. Taverna, C.M. Ulrich, K. Wu, S. Kono, D.W. West, S.I. Berndt, S. Bezieau, H. Brenner, P.T. Campbell, A.T. Chan, J. Chang-Claude, G.A. Coetzee, D.V. Conti, D. Duggan, J.C. Figueiredo, B.K. Fortini, S.J. Gallinger, W.J. Gauderman, G. Giles, R. Green, R. Haile, T.A. Harrison, M. Hoffmeister, J.L. Hopper, T.J. Hudson, E. Jacobs, M. Iwasaki, S.H. Jee, M. Jenkins, W.H. Jia, A. Joshi, L. Li, N.M. Lindor, K. Matsuo, V. Moreno, B. Mukherjee, P.A. Newcomb, J.D. Potter, L. Raskin, G. Rennert, S. Rosse, G. Severi, R.E. Schoen, D. Seminara, X.O. Shu, M.L. Slattery, S. Tsugane, E. White, Y.B. Xiang, B.W. Zanke, W. Zheng, L. Le Marchand, G. Casey, S.B. Gruber, U. Peters, Genome-wide association study of colorectal cancer identifies six new susceptibility loci. Nat Commun 6, 7138 (2015)CrossRef F.R. Schumacher, S.L. Schmit, S. Jiao, C.K. Edlund, H. Wang, B. Zhang, L. Hsu, S.C. Huang, C.P. Fischer, J.F. Harju, G.E. Idos, F. Lejbkowicz, F.J. Manion, K. McDonnell, C.E. McNeil, M. Melas, H.S. Rennert, W. Shi, D.C. Thomas, D.J. Van Den Berg, C.M. Hutter, A.K. Aragaki, K. Butterbach, B.J. Caan, C.S. Carlson, S.J. Chanock, K.R. Curtis, C.S. Fuchs, M. Gala, E.L. Giovannucc, S.M. Gogarten, R.B. Hayes, B. Henderson, D.J. Hunter, R.D. Jackson, L.N. Kolonel, C. Kooperberg, S. Kury, A. LaCroix, C.C. Laurie, C.A. Laurie, M. Lemire, D. Levine, J. Ma, K.W. Makar, C. Qu, D. Taverna, C.M. Ulrich, K. Wu, S. Kono, D.W. West, S.I. Berndt, S. Bezieau, H. Brenner, P.T. Campbell, A.T. Chan, J. Chang-Claude, G.A. Coetzee, D.V. Conti, D. Duggan, J.C. Figueiredo, B.K. Fortini, S.J. Gallinger, W.J. Gauderman, G. Giles, R. Green, R. Haile, T.A. Harrison, M. Hoffmeister, J.L. Hopper, T.J. Hudson, E. Jacobs, M. Iwasaki, S.H. Jee, M. Jenkins, W.H. Jia, A. Joshi, L. Li, N.M. Lindor, K. Matsuo, V. Moreno, B. Mukherjee, P.A. Newcomb, J.D. Potter, L. Raskin, G. Rennert, S. Rosse, G. Severi, R.E. Schoen, D. Seminara, X.O. Shu, M.L. Slattery, S. Tsugane, E. White, Y.B. Xiang, B.W. Zanke, W. Zheng, L. Le Marchand, G. Casey, S.B. Gruber, U. Peters, Genome-wide association study of colorectal cancer identifies six new susceptibility loci. Nat Commun 6, 7138 (2015)CrossRef

go back to reference R.J. Gilbertson, J.N. Rich, Making a tumour's bed: Glioblastoma stem cells and the vascular niche. Nat Rev Cancer 7, 733–736 (2007)CrossRef R.J. Gilbertson, J.N. Rich, Making a tumour's bed: Glioblastoma stem cells and the vascular niche. Nat Rev Cancer 7, 733–736 (2007)CrossRef

go back to reference J. Marjanovic Vicentic, D. Drakulic, I. Garcia, V. Vukovic, P. Aldaz, N. Puskas, I. Nikolic, G. Tasic, S. Raicevic, L. Garros-Regulez, N. Sampron, M.J. Atkinson, N. Anastasov, A. Matheu, M. Stevanovic, SOX3 can promote the malignant behavior of glioblastoma cells. Cell Oncol 42, 41–54 (2019)CrossRef J. Marjanovic Vicentic, D. Drakulic, I. Garcia, V. Vukovic, P. Aldaz, N. Puskas, I. Nikolic, G. Tasic, S. Raicevic, L. Garros-Regulez, N. Sampron, M.J. Atkinson, N. Anastasov, A. Matheu, M. Stevanovic, SOX3 can promote the malignant behavior of glioblastoma cells. Cell Oncol 42, 41–54 (2019)CrossRef

go back to reference L.M. Nusblat, M.J. Carroll, C.M. Roth, Crosstalk between M2 macrophages and glioma stem cells. Cell Oncol 40, 471–482 (2017)CrossRef L.M. Nusblat, M.J. Carroll, C.M. Roth, Crosstalk between M2 macrophages and glioma stem cells. Cell Oncol 40, 471–482 (2017)CrossRef

go back to reference C.D. Stiles, D.H. Rowitch, Glioma stem cells: a midterm exam. Neuron 58, 832–846 (2008)CrossRef C.D. Stiles, D.H. Rowitch, Glioma stem cells: a midterm exam. Neuron 58, 832–846 (2008)CrossRef

go back to reference I. Pastushenko, C. Blanpain, EMT transition states during tumor progression and metastasis. Trends Cell Biol 29, 212–226 (2019)CrossRef I. Pastushenko, C. Blanpain, EMT transition states during tumor progression and metastasis. Trends Cell Biol 29, 212–226 (2019)CrossRef

go back to reference T. Brabletz, R. Kalluri, M.A. Nieto, R.A. Weinberg, EMT in cancer. Nat Rev Cancer 18, 128–134 (2018)CrossRef T. Brabletz, R. Kalluri, M.A. Nieto, R.A. Weinberg, EMT in cancer. Nat Rev Cancer 18, 128–134 (2018)CrossRef

go back to reference L. Zhang, F. Zhou, P. ten Dijke, Signaling interplay between transforming growth factor-beta receptor and PI3K/AKT pathways in cancer. Trends Biochem Sci 38, 612–620 (2013)CrossRef L. Zhang, F. Zhou, P. ten Dijke, Signaling interplay between transforming growth factor-beta receptor and PI3K/AKT pathways in cancer. Trends Biochem Sci 38, 612–620 (2013)CrossRef

go back to reference D.A. Fruman, C. Rommel, PI3K and cancer: Lessons, challenges and opportunities. Nat Rev Drug Discov 13, 140–156 (2014)CrossRef D.A. Fruman, C. Rommel, PI3K and cancer: Lessons, challenges and opportunities. Nat Rev Drug Discov 13, 140–156 (2014)CrossRef

go back to reference R. Grant, L. Kolb, J. Moliterno, Molecular and genetic pathways in gliomas: The future of personalized therapeutics. CNS Oncology 3, 123–136 (2014)CrossRef R. Grant, L. Kolb, J. Moliterno, Molecular and genetic pathways in gliomas: The future of personalized therapeutics. CNS Oncology 3, 123–136 (2014)CrossRef

go back to reference B. Markman, F. Atzori, J. Perez-Garcia, J. Tabernero, J. Baselga, Status of PI3K inhibition and biomarker development in cancer therapeutics. Ann Oncol 21, 683–691 (2010) B. Markman, F. Atzori, J. Perez-Garcia, J. Tabernero, J. Baselga, Status of PI3K inhibition and biomarker development in cancer therapeutics. Ann Oncol 21, 683–691 (2010)

go back to reference J. Polivka Jr., F. Janku, Molecular targets for cancer therapy in the PI3K/AKT/mTOR pathway. Pharmacol Ther 142, 164–175 (2014)CrossRef J. Polivka Jr., F. Janku, Molecular targets for cancer therapy in the PI3K/AKT/mTOR pathway. Pharmacol Ther 142, 164–175 (2014)CrossRef

go back to reference L.M. Thorpe, H. Yuzugullu, J.J. Zhao, PI3K in cancer: Divergent roles of isoforms, modes of activation and therapeutic targeting. Nat Rev Cancer 15, 7–24 (2015)CrossRef L.M. Thorpe, H. Yuzugullu, J.J. Zhao, PI3K in cancer: Divergent roles of isoforms, modes of activation and therapeutic targeting. Nat Rev Cancer 15, 7–24 (2015)CrossRef