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Forkhead Box M1 positively regulates UBE2C and protects glioma cells from autophagic death

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Pages 1705-1718 | Received 01 Mar 2017, Accepted 01 Jul 2017, Published online: 30 Aug 2017

References

  • Tanaka S, Louis DN, Curry WT, Batchelor TT, Dietrich J. Diagnostic and therapeutic avenues for glioblastoma: no longer a dead end? Nat Rev Clin Oncol. 2013;10(1):14-26. doi:10.1038/nrclinonc.2012.204. PMID:23183634
  • Eyüpoglu IY, Buchfelder M, Savaskan NE. Surgical resection of malignant gliomas-role in optimizing patient outcome. Nat Rev Neurol. 2013;9(3):141-51. doi:10.1038/nrneurol.2012.279. PMID:23358480
  • Wang Y, Jiang T. Understanding high grade glioma: molecular mechanism, therapy and comprehensive management. Cancer Lett. 2013;331(2):139-46. doi:10.1016/j.canlet.2012.12.024. PMID:23340179
  • Seliger C, Meier CR, Becker C, Jick SS, Bogdahn U, Hau P, Leitzmann MF. Statin use and risk of glioma: population-based case-control analysis. Eur J Epidemiol. 2016;31(9):947-52. doi:10.1007/s10654-016-0145-7. PMID:27041698
  • Gentles AJ, Newman AM, Liu CL, Bratman SV, Feng W, Kim D, Nair VS, Xu Y, Khuong A, Hoang CD, et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med. 2015;21(8):938-45. doi:10.1038/nm.3909. PMID:26193342
  • Kopanja D, Pandey A, Kiefer M, Wang Z, Chandan N, Carr JR, Franks R, Yu DY, Guzman G, Maker A, et al. Essential roles of FoxM1 in Ras-induced liver cancer progression and in cancer cells with stem cell features. J Hepatol. 2015;63(2):429-36. doi:10.1016/j.jhep.2015.03.023. PMID:25828473
  • Aytes A, Mitrofanova A, Lefebvre C, Alvarez MJ, Castillo-Martin M, Zheng T, Eastham JA, Gopalan A, Pienta KJ, Shen MM, et al. Cross-species regulatory network analysis identifies a synergistic interaction between FOXM1 and CENPF that drives prostate cancer malignancy. Cancer Cell. 2014;25(5):638-51. doi:10.1016/j.ccr.2014.03.017. PMID:24823640
  • Sanders DA, Ross-Innes CS, Beraldi D, Carroll JS, Balasubramanian S. Genome-wide mapping of FOXM1 binding reveals co-binding with estrogen receptor alpha in breast cancer cells. Genome Biol. 2013;14(1):R6. doi:10.1186/gb-2013-14-1-r6. PMID:23347430
  • Kong X, Li L, Li Z, Le X, Huang C, Jia Z, Cui J, Huang S, Wang L, Xie K. Dysregulated expression of FOXM1 isoforms drives progression of pancreatic cancer. Cancer Res. 2013;73(13):3987-96. doi:10.1158/0008-5472.CAN-12-3859. PMID:23598278
  • Eisinger-Mathason TS, Mucaj V, Biju KM, Nakazawa MS, Gohil M, Cash TP, Yoon SS, Skuli N, Park KM, Gerecht S, et al. Deregulation of the Hippo pathway in soft-tissue sarcoma promotes FOXM1 expression and tumorigenesis. Proc Natl Acad Sci U S A. 2015;112(26):E3402-11. doi:10.1073/pnas.1420005112. PMID:26080399
  • Gong AH, Wei P, Zhang S, Yao J, Yuan Y, Zhou AD, Lang FF, Heimberger AB, Rao G, Huang S. FoxM1 drives a feed-forward STAT3-activation signaling loop that promotes the self-renewal and tumorigenicity of glioblastoma stem-like cells. Cancer Res. 2015;75(11):2337-48. doi:10.1158/0008-5472.CAN-14-2800. PMID:25832656
  • Park HJ, Wang Z, Costa RH, Tyner A, Lau LF, Raychaudhuri P. An N-terminal inhibitory domain modulates activity of FoxM1 during cell cycle. Oncogene. 2008;27(12):1696-704. doi:10.1038/sj.onc.1210814. PMID:17891172
  • Laoukili J, Kooistra MR, Brás A, Kauw J, Kerkhoven RM, Morrison A, Clevers H, Medema RH. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol. 2005;7(2):126-36. doi:10.1038/ncb1217. PMID:15654331
  • Zhang Y, Zhang N, Dai B, Liu M, Sawaya R, Xie K, Huang S. FoxM1B transcriptionally regulates vascular endothelial growth factor expression and promotes the angiogenesis and growth of glioma cells. Cancer Res. 2008;68(21):8733-42. doi:10.1158/0008-5472.CAN-08-1968. PMID:18974115
  • Zhang N, Wei P, Gong A, Chiu WT, Lee HT, Colman H, Huang H, Xue J, Liu M, Wang Y, et al. FoxM1 promotes β-catenin nuclear localization and controls Wnt target-gene expression and glioma tumorigenesis. Cancer Cell. 2011;20(4):427-42. doi:10.1016/j.ccr.2011.08.016. PMID:22014570
  • Li D, Wei P, Peng Z, Huang C, Tang H, Jia Z, Cui J, Le X, Huang S, Xie K. The critical role of dysregulated FOXM1-PLAUR signaling in human colon cancer progression and metastasis. Clin Cancer Res. 2013;19(1):62-72. doi:10.1158/1078-0432.CCR-12-1588. PMID:23136192
  • Chiu WT, Huang YF, Tsai HY, Chen CC, Chang CH, Huang SC, Hsu KF, Chou CY. FOXM1 confers to epithelial-mesenchymal transition, stemness and chemoresistance in epithelial ovarian carcinoma cells. Oncotarget. 2015;6(4):2349-65. doi:10.18632/oncotarget.2957. PMID:25537512
  • Yu G, Zhou A, Xue J, Huang C, Zhang X, Kang SH, Chiu WT, Tan C, Xie K, Wang J, et al. FoxM1 promotes breast tumorigenesis by activating PDGF-A and forming a positive feedback loop with the PDGF/AKT signaling pathway. Oncotarget. 2015;6(13):11281-94. doi:10.18632/oncotarget.3596. PMID:25869208
  • Pallante P, Malapelle U, Berlingieri MT, Bellevicine C, Sepe R, Federico A, Rocco D, Galgani M, Chiariotti L, Sanchez-Cespedes M, et al. UbcH10 overexpression in human lung carcinomas and its correlation with EGFR and p53 mutational status. Eur J Cancer. 2013;49(5):1117-26. doi:10.1016/j.ejca.2012.09.033. PMID:23102841
  • Berlingieri MT, Pallante P, Guida M, Nappi C, Masciullo V, Scambia G, Ferraro A, Leone V, Sboner A, Barbareschi M, et al. UbcH10 expression may be a useful tool in the prognosis of ovarian carcinomas. Oncogene. 2007;26(14):2136-40. doi:10.1038/sj.onc.1210010. PMID:17016443
  • Nath S, Banerjee T, Sen D, Das T, Roychoudhury S. Spindle assembly checkpoint protein Cdc20 transcriptionally activates expression of ubiquitin carrier protein UbcH10. J Biol Chem. 2011;286(18):15666-77. doi:10.1074/jbc.M110.160671. PMID:21454660
  • Li SZ, Song Y, Zhang HH, Jin BX, Liu Y, Liu WB, Zhang XD, Du RL. UbcH10 overexpression increases carcinogenesis and blocks ALLN susceptibility in colorectal cancer. Sci Rep. 2014;4:6910. doi:10.1038/srep06910. PMID:25376843
  • Endesfelder D, Burrell RA, Kanu N, McGranahan N, Howell M, Parker PJ, Downward J, Swanton C, Kschischo M. Chromosomal instability selects gene copy-number variants encoding core regulators of proliferation in ER+ breast cancer. Cancer Res. 2014;74(17):4853-63. doi:10.1158/0008-5472.CAN-13-2664. PMID:24970479
  • Chang L, Zhang Z, Yang J, McLaughlin SH, Barford D. Atomic structure of the APC/C and its mechanism of protein ubiquitination. Nature. 2015;522(7557):450-4. doi:10.1038/nature14471. PMID:26083744
  • Zhang Z, Liu P, Wang J, Gong T, Zhang F, Ma J, Han N. Ubiquitin-conjugating enzyme E2C regulates apoptosis-dependent tumor progression of non-small cell lung cancer via ERK pathway. Med Oncol. 2015;32(5):149. doi:10.1007/s12032-015-0609-8. PMID:25832867
  • Donato G, Iofrida G, Lavano A, Volpentesta G, Signorelli F, Pallante PL, Berlingieri MT, Pierantoni MG, Palmieri D, Conforti F, et al. Analysis of UbcH10 expression represents a useful tool for the diagnosis and therapy of astrocytic tumors. Clin Neuropathol. 2008;27(4):219-23. doi:10.5414/NPP27219. PMID:18666437
  • Jiang L, Huang CG, Lu YC, Luo C, Hu GH, Liu HM, Chen JX, Han HX. Expression of ubiquitin-conjugating enzyme E2C/UbcH10 in astrocytic tumors. Brain Res. 2008;1201:161-6. doi:10.1016/j.brainres.2008.01.037
  • Jiang L, Bao Y, Luo C, Hu G, Huang C, Ding X, Sun K, Lu Y. Knockdown of ubiquitin-conjugating enzyme E2C/UbcH10 expression by RNA interference inhibits glioma cell proliferation and enhances cell apoptosis in vitro. J Cancer Res Clin Oncol. 2010;136(2):211-7. doi:10.1007/s00432-009-0651-z. PMID:19657671
  • Chiu HW, Ho SY, Guo HR, Wang YJ. Combination treatment with arsenic trioxide and irradiation enhances autophagic effects in U118-MG cells through increased mitotic arrest and regulation of PI3K/Akt and ERK1/2 signaling pathways. Autophagy. 2009;5(4):472-83. doi:10.4161/auto.6.3.11229. PMID:19242099
  • Ma J, Meng F, Li S, Liu L, Zhao L, Liu Y, Hu Y, Li Z, Yao Y, Xi Z, et al. Autophagy induction by endothelial-monocyte activating polypeptide II contributes to the inhibition of malignant biological behaviors by the combination of EMAP II with rapamycin in human glioblastoma. Front Mol Neurosci. 2015;8:74. doi:10.3389/fnmol.2015.00074. PMID:26648842
  • Lei HY, Chang CP. Induction of autophagy by concanavalin A and its application in anti-tumor therapy. Autophagy. 2007;3(4):402-4. doi:10.4161/auto.4280. PMID:17471013
  • Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 3rd ed. 2016;12(1):1-222. doi:10.1080/15548627.2015.1100356. PMID:26799652
  • Mauvezin C, Neufeld TP. Bafilomycin A1 disrupts autophagic flux by inhibiting both V-ATPase-dependent acidification and Ca-P60A/SERCA-dependent autophagosome-lysosome fusion. Autophagy. 2015;11(8):1437-8. doi:10.1080/15548627.2015.1066957. PMID:26156798
  • Shinojima N, Yokoyama T, Kondo Y, Kondo S. Roles of the Akt/mTOR/p70s6k and ERK1/2 signaling pathways in curcumin-induced autophagy. Autophagy. 2007;3(6):635-7. doi:10.4161/auto.4916. PMID:17786026
  • Liu J, Guo S, Li Q, Yang L, Xia Z, Zhang L, Huang Z, Zhang N. Phosphoglycerate dehydrogenase induces glioma cells proliferation and invasion by stabilizing forkhead box M1. J Neurooncol. 2013;111(3):245-55. doi:10.1007/s11060-012-1018-x. PMID:23229761
  • Wang IC, Ustiyan V, Zhang Y, Cai Y, Kalin TV, Kalinichenko VV. Foxm1 transcription factor is required for the initiation of lung tumorigenesis by oncogenic Kras(G12D.). Oncogene. 2014;33(46):5391-6. doi:10.1038/onc.2013.475. PMID:24213573
  • Cui J, Shi M, Xie D, Wei D, Jia Z, Zheng S, Gao Y, Huang S, Xie K. FOXM1 promotes the warburg effect and pancreatic cancer progression via transactivation of LDHA expression. Clin Cancer Res. 2014;20(10):2595-606. doi:10.1158/1078-0432.CCR-13-2407. PMID:24634381
  • Liu X, Sun K, Wang H, Dai Y. Knockdown of retinoblastoma protein may sensitize glioma cells to cisplatin through inhibition of autophagy. Neurosci Lett. 2016;620:137-142. doi:10.1016/j.neulet.2016.04.001. PMID:27048711
  • Cho YJ, Woo JH, Lee JS, Jang DS, Lee KT, Choi JH. Eclalbasaponin II induces autophagic and apoptotic cell death in human ovarian cancer cells. J Pharmacol Sci. 2016;132(1):6-14. doi:10.1016/j.jphs.2016.02.006. PMID:27032907
  • Wang B, Fan X, Ma C, Lei H, Long Q, Chai Y. Downregulation of KDM4A suppresses the survival of glioma cells by promoting autophagy. J Mol Neurosci. 2016;60(2):137-144. doi:10.1007/s12031-016-0796-6. PMID:27514525
  • Bowman CJ, Ayer DE, Dynlacht BD. Foxk proteins repress the initiation of starvation-induced atrophy and autophagy programs. Nat Cell Biol. 2014;16(12):1202-1214. doi:10.1038/ncb3062. PMID:25402684
  • Rautou PE, Cazals-Hatem D, Moreau R, Francoz C, Feldmann G, Lebrec D, Ogier-Denis E, Bedossa P, Valla D, Durand F. Acute liver cell damage in patients with anorexia nervosa: a possible role of starvation-induced hepatocyte autophagy. Gastroenterology. 2008;135:840-848. e3. doi:10.1053/j.gastro.2008.05.055. PMID:18644371
  • Dolma S, Selvadurai HJ, Lan X, Lee L, Kushida M, Voisin V, Whetstone H, So M, Aviv T, Park N, et al. Inhibition of dopamine receptor D4 impedes autophagic flux, proliferation, and survival of glioblastoma stem cells. Cancer Cell. 2016;29(6):859-873. doi:10.1016/j.ccell.2016.05.002. PMID:27300435
  • Hewitt G, Carroll B, Sarallah R, Correia-Melo C, Ogrodnik M, Nelson G, Otten EG, Manni D, Antrobus R, Morgan BA, et al. SQSTM1/p62 mediates crosstalk between autophagy and the UPS in DNA repair. Autophagy. 2016;12(10):1917-1930. doi:10.1080/15548627.2016.1210368. PMID:27391408
  • Torricelli C, Daveri E, Salvadori S, Valacchi G, Ietta F, Muscettola M, Carlucci F, Maioli E. Phosphorylation-independent mTORC1 inhibition by the autophagy inducer rottlerin. Cancer Lett. 2015;360(1):17-27. doi:10.1016/j.canlet.2015.01.040. PMID:25661734
  • Oh JM, Choi EK, Carp RI, Kim YS. Oxidative stress impairs autophagic flux in prion protein-deficient hippocampal cells. Autophagy. 2012;8(10):1448-1461. doi:10.4161/auto.21164. PMID:22889724
  • Gómez-Sánchez R, Yakhine-Diop SM, Rodríguez-Arribas M, Bravo-San Pedro JM, Martínez-Chacón G, Uribe-Carretero E, Pinheiro de Castro DC, Pizarro-Estrella E, Fuentes JM, González-Polo RA. mRNA and protein dataset of autophagy markers (LC3 and p62) in several cell lines. Data Brief. 2016;7:641-647. doi:10.1016/j.dib.2016.02.085. PMID:27054171
  • Shvets E, Abada A, Weidberg H, Elazar Z. Dissecting the involvement of LC3B and GATE-16 in p62 recruitment into autophagosomes. Autophagy. 2011;7(7):683-688. doi:10.4161/auto.7.7.15279. PMID:21460636
  • Cha-Molstad H, Kwon YT, Kim BY. Amino-terminal arginylation as a degradation signal for selective autophagy. BMB Rep. 2015;48(9):487-488. doi:10.5483/BMBRep.2015.48.9.176. PMID:26303972
  • Singh K, Sharma A, Mir MC, Drazba JA, Heston WD, Magi-Galluzzi C, Hansel D, Rubin BP, Klein EA, Almasan A. Autophagic flux determines cell death and survival in response to Apo2L/TRAIL (dulanermin). Mol Cancer. 2014;13:70. doi:10.1186/1476-4598-13-70. PMID:24655592