FOXM1 and STAT3 interaction confers radioresistance in glioblastoma cells

Oncotarget

Volumn 7, Issue 47, 2016, Pages 77365-77377

  Maachani, Uday B ^a   Shankavaram, Uma ^a   Kramp, Tamalee ^a   Tofilon, Philip J ^a   Camphausen, Kevin ^a   Tandle, Anita T ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

FOXM1; Glioblastoma multiforme; Glioma stem cells; Radio resistance; STAT3

Indexed keywords

MRE11 PROTEIN; POLO LIKE KINASE 1; RAD51 PROTEIN; STAT3 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXM1; UNCLASSIFIED DRUG; FORKHEAD BOX PROTEIN M1; FOXM1 PROTEIN, HUMAN; PEPTIDE; PROTEIN BINDING; PROTEOME; SIOMYCIN A; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CELL CYCLE PROGRESSION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; GENE CONTROL; GENE EXPRESSION REGULATION; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MOUSE; MRE11 GENE; NONHUMAN; PLK1 GENE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; RAD51 GENE; RADIOSENSITIVITY; RECOMBINATION REPAIR; UPREGULATION; BRAIN TUMOR; CELL CYCLE; DRUG EFFECTS; GENETICS; GLIOBLASTOMA; HOMOLOGOUS RECOMBINATION; KAPLAN MEIER METHOD; METABOLISM; MITOSIS; MORTALITY; PROCEDURES; PROGNOSIS; PROTEIN TRANSPORT; RADIATION TOLERANCE; RNA INTERFERENCE; TUMOR CELL LINE;

BRAIN NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; FORKHEAD BOX PROTEIN M1; GLIOBLASTOMA; HOMOLOGOUS RECOMBINATION; HUMANS; KAPLAN-MEIER ESTIMATE; MITOSIS; PEPTIDES; PROGNOSIS; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEOME; PROTEOMICS; RADIATION TOLERANCE; RNA INTERFERENCE; RNA, SMALL INTERFERING; STAT3 TRANSCRIPTION FACTOR;

EID: 84998772503     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.12670     Document Type: Article

References (47)

1. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTCNCIC trial. Lancet Oncol. 2009; 10:459-466.
2. Giese A, Bjerkvig R, Berens ME and Westphal M. Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol. 2003; 21:1624-1636.
3. Hittelman WN, Liao Y, Wang L and Milas L. Are cancer stem cells radioresistant? Future Oncol. 2010; 6:1563-1576.
4. Raychaudhuri P and Park HJ. FoxM1: a master regulator of tumor metastasis. Cancer Res. 2011; 71:4329-4333.
5. Monteiro LJ, Khongkow P, Kongsema M, Morris JR, Man C, Weekes D, Koo CY, Gomes AR, Pinto PH, Varghese V, Kenny LM, Charles Coombes R, Freire R, Medema RH and Lam EW. The Forkhead Box M1 protein regulates BRIP1 expression and DNA damage repair in epirubicin treatment. Oncogene. 2013; 32:4634-4645.
6. Koo CY, Muir KW and Lam EW. FOXM1: From cancer initiation to progression and treatment. Biochim Biophys Acta. 2012; 1819:28-37.
7. Alvarez-Fernandez M and Medema RH. Novel functions of FoxM1: from molecular mechanisms to cancer therapy. Front Oncol. 2013; 3:30.
8. Rickman DS, Bobek MP, Misek DE, Kuick R, Blaivas M, Kurnit DM, Taylor J and Hanash SM. Distinctive molecular profiles of high-grade and low-grade gliomas based on oligonucleotide microarray analysis. Cancer Res. 2001; 61:6885-6891.
9. Liu MG, Dai BB, Kang SH, Ban KC, Huang FJ, Lang FF, Aldape KD, Xie TX, Pelloski CE, Xie KP, Sawaya R and Huang SY. FoxM1B is overexpressed in human glioblastomas and critically regulates the tumorigenicity of glioma cells. Cancer Research. 2006; 66:3593-3602.
10. Radhakrishnan SK, Rhat UG, Hughes DE, Wang IC, Costa RH and Gartel AL. Identification of a chemical inhibitor of the oncogenic transcription factor forkhead box M1. Cancer Research. 2006; 66:9731-9735.
11. Wang IC, Chen YJ, Hughes D, Petrovic V, Major ML, Park HJ, Tan YJ, Ackerson T and Costa RH. Forkhead box m1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol Cell Biol. 2005; 25:10875-10894.
12. Laoukili J, Kooistra MRH, Bras A, Kauw J, Kerkhoven RM, Morrison A, Clevers H and Medema RH. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol. 2005; 7:126-U134.
13. Warde-Farley D, Donaldson SL, Comes O, Zuberi K, Badrawi R, Chao P, Franz M, Grouios C, Kazi F, Lopes CT, Maitland A, Mostafavi S, Montojo J, et al. The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res. 2010; 38:W214-W220.
14. Zhang N, Wu XJ, Yang LX, Xiao FZ, Zhang H, Zhou AD, Huang ZS and Huang SY. FoxM1 Inhibition Sensitizes Resistant Glioblastoma Cells to Temozolomide by Downregulating the Expression of DNA-Repair Gene Rad51. Clinical Cancer Research. 2012; 18:5961-5971.
15. Khongkow P, Karunarathna U, Khongkow M, Gong C, Gomes AR, Yague E, Monteiro LJ, Kongsema M, Zona S, Man EPS, Tsang JWH, Coombes RC, Wu KJ, et al. FOXM1 targets NBS1 to regulate DNA damage-induced senescence and epirubicin resistance. Oncogene. 2014; 33:4144-4155.
16. Yu H and Jove R. The stats of cancer-New molecular targets come of age. Nat Rev Cancer. 2004; 4:97-105.
17. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao YX, Pestell RG, Albanese C and Darnell JE. Stat3 as an oncogene. Cell. 1999; 98:295-303.
18. Yang YP, Chang YL, Huang PI, Chiou GY, Tseng LM, Chiou SH, Chen MH, Chen MT, Shih YH, Chang CH, Hsu CC, Ma HI, Wang CT, Tsai LL, Yu CC and Chang CJ. Resveratrol suppresses tumorigenicity and enhances radiosensitivity in primary glioblastoma tumor initiating cells by inhibiting the STAT3 axis. J Cell Physiol. 2012; 227:976-993.
19. Mencalha AL, Binato R, Ferreira GM, Du Rocher B and Abdelhay E. Forkhead Box M1 (FoxM1) Gene Is a New STAT3 Transcriptional Factor Target and Is Essential for Proliferation, Survival and DNA Repair of K562 Cell Line. Plos One. 2012; 7.
20. McDowall MD, Scott MS and Barton GJ. PIPs: human protein-protein interaction prediction database. Nucleic Acids Res. 2009; 37:D651-D656.
21. Gyorffy B, Surowiak P, Budczies J and Lanczky A. Online Survival Analysis Software to Assess the Prognostic Value of Biomarkers Using Transcriptomic Data in Non-Small-Cell Lung Cancer. Plos One. 2013; 8.
22. Gyorffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li QY and Szallasi Z. An online survival analysis tool to rapidly assess the effect of 22, 277 genes on breast cancer prognosis using microarray data of 1, 809 patients. Breast Cancer Res Tr. 2010; 123:725-731.
23. Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, Oh EY, Gaber MW, Finklestein D, Allen M, Frank A, Bayazitov IT, Zakharenko SS, Gajjar A, Davidoff A and Gilbertson RJ. A perivascular niche for brain tumor stem cells. Cancer Cell. 2007; 11:69-82.
24. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD and Dirks PB. Identification of human brain tumour initiating cells. Nature. 2004; 432:396-401.
25. Taylor MD, Poppleton H, Fuller C, Su XP, Liu YX, Jensen P, Magdaleno S, Dalton J, Calabrese C, Board J, MacDonald T, Rutka J, Guha A, Gajjar A, Curran T and Gilbertson RJ. Radial glia cells are candidate stem cells of ependymoma. Cancer Cell. 2005; 8:323-335.
26. Wu A, Oh S, Wiesner SM, Ericson K, Chen L, Hall WA, Champoux PE, Low WC and Ohlfest JR. Persistence of CD133(+) cells in human and mouse glioma cell lines: detailed characterization of GL261 glioma cells with cancer stem cell-like properties. Stem Cells Dev. 2008; 17:173-184.
27. Tibes R, Qiu YH, Hennessy B, Andreeff M, Miiis GB and Kornblau SM. Reverse phase protein array: validation of a novel proteomic technology and utility for analysis of primary leukemia specimens and hematopoietic stem cells. Mol Cancer Ther. 2006; 5:2512-2521.
28. Nakano I, Joshi K, Visnyei K, Hu B, Watanabe M, Lam D, Wexler E, Saigusa K, Nakamura Y, Laks DR, Mischel PS, Viapiano M and Kornblum HI. Siomycin A targets brain tumor stem cells partially through a MELK-mediated pathway. Neuro-Oncology. 2011; 13:622-634.
29. Zhang N, Wu XJ, Yang LX, Xiao FZ, Zhang H, Zhou AD, Huang ZS and Huang SY. FoxM1 Inhibition Sensitizes Resistant Glioblastoma Cells to Temozolomide by Downregulating the Expression of DNA-Repair Gene Rad51. Clinical Cancer Research. 2012; 18:5961-5971.
30. Wierstra I. FOXM1 (Forkhead box M1) in Tumorigenesis: Overexpression in Human Cancer, Implication in Tumorigenesis, Oncogenic Functions, Tumor-Suppressive Properties, and Target of Anticancer Therapy. Adv Cancer Res. 2013; 119:191-419.
31. Liu MG, Dai BB, Kang SH, Ban KC, Huang FJ, Lang FF, Aldape KD, Xie TX, Pelloski CE, Xie KP, Sawaya R and Huang SY. FoxM1B is overexpressed in human glioblastomas and critically regulates the tumorigenicity of glioma cells. Cancer Research. 2006; 66:3593-3602.
32. Gartel AL. A new target for proteasome inhibitors: FoxM1. Expert Opin Inv Drug. 2010; 19:235-242.
33. Gartel AL. The oncogenic transcription factor FOXM1 and anticancer therapy. Cell Cycle. 2012; 11:3341-3342.
34. Korver W, Roose J and Clevers H. The winged-helix transcription factor Trident is expressed in cycling cells. Nucleic Acids Res. 1997; 25:1715-1719.
35. Tan YJ, Raychaudhuri P and Costa RH. Chk2 mediates stabilization of the FoxM1 transcription factor to stimulate expression of DNA repair genes. Mol Cell Biol. 2007; 27:1007-1016.
36. Janssen A, van der Burg M, Szuhai K, Kops GJPL and Medema RH. Chromosome Segregation Errors as a Cause of DNA Damage and Structural Chromosome Aberrations. Science. 2011; 333:1895-1898.
37. Bao SD, Wu QL, McLendon RE, Hao YL, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD and Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006; 444:756-760.
38. Singh-Gupta V, Zhang H, Banerjee S, Kong D, Raffoul JJ, Sarkar FH and Hillman GG. Radiation-induced HIF-1 alpha cell survival pathway is inhibited by soy isoflavones in prostate cancer cells. Int J Cancer. 2009; 124:1675-1684.
39. Yu H, Kortylewski M and Pardoll D. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat Rev Immunol. 2007; 7:41-51.
40. Gong AH, Wei P, Zhang SC, Yao J, Yuan Y, Zhou AD, Lang FF, Heimberger AB, Rao G and Huang SY. FoxM1 Drives a Feed-Forward STAT3-Activation Signaling Loop That Promotes the Self-Renewal and Tumorigenicity of Glioblastoma Stem-like Cells. Cancer Research. 2015; 75:2337-2348.
41. Halasi M and Gartel AL. A novel mode of FoxM1 regulation Positive auto-regulatory loop. Cell Cycle. 2009; 8:1966-1967.
42. McCord AM, Jamal M, Shankavaram UT, Lang FF, Camphausen K and Tofilon PJ. Physiologic oxygen concentration enhances the stem-like properties of CD133+ human glioblastoma cells in vitro (vol 7, pg 489, 2009). Mol Cancer Res. 2009; 7:987-987.
43. McCord AM, Jamal M, Williams ES, Camphausen K and Tofilon PJ. CD133(+) Glioblastoma Stem-like Cells are Radiosensitive with a Defective DNA Damage Response Compared with Established Cell Lines. Clinical Cancer Research. 2009; 15:5145-5153.
44. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F and Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Research. 2004; 64:7011-7021.
45. Camphausen K, Burgan W, Cerra M, Oswald KA, Trepel JB, Lee MJ and Tofilon PJ. Enhanced radiation-induced cell killing and prolongation of gammaH2AX foci expression by the histone deacetylase inhibitor MS-275. Cancer Res. 2004; 64:316-321.
46. Maachani UB, Kramp T, Hanson R, Zhao S, Celiku O, Shankavaram U, Colombo R, Caplen NJ, Camphausen K and Tandle A. Targeting MPS1 Enhances Radiosensitization of Human Glioblastoma by Modulating DNA Repair Proteins. Mol Cancer Res. 2015; 13:852-862.
47. Pierce AJ, Johnson RD, Thompson LH and Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 1999; 13:2633-2638.