Inhibition of FoxM1-Mediated DNA repair by imipramine blue suppresses breast cancer growth and metastasis

Clinical Cancer Research

Volumn 22, Issue 14, 2016, Pages 3524-3536

  Rajamanickam, Subapriya ^a,b   Panneerdoss, Subbarayalu ^a,b   Gorthi, Aparna ^a,b   Timilsina, Santosh ^a,b   Onyeagucha, Benjamin ^a,b   Kovalskyy, Dmytro ^a   Ivanov, Dmitri ^a   Hanes, Martha A ^b   Vadlamudi, Ratna K ^a   Chen, Yidong ^b   Bishop, Alexander J ^a,b   Arbiser, Jack L ^c,d   Rao, Manjeet K ^a,b  

^a University of Texas Health Science Center   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; IMIPRAMINE BLUE; LIPOSOME; NANOPARTICLE; UNCLASSIFIED DRUG; FORKHEAD BOX PROTEIN M1; FOXM1 PROTEIN, HUMAN; IMIPRAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER INHIBITION; CONTROLLED STUDY; DNA REPAIR; DRUG EFFICACY; DRUG PROTEIN BINDING; DRUG SAFETY; EX VIVO STUDY; GENE EXPRESSION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LUNG METASTASIS; METASTASIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTO ONCOGENE; PROTO ONCOGENE FOXM1; ANIMAL; BREAST TUMOR; CELL CYCLE; CELL PROLIFERATION; DNA DAMAGE; DRUG EFFECTS; EPITHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; MCF-7 CELL LINE; METABOLISM; METASTASIS; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; BREAST NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; DNA DAMAGE; DNA REPAIR; EPITHELIAL CELLS; FEMALE; FORKHEAD BOX PROTEIN M1; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMIPRAMINE; MCF-7 CELLS; MICE; MICE, NUDE; NEOPLASM METASTASIS;

EID: 84976297644     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-2535     Document Type: Article

References (46)

1. Helleday T, Petermann E, Lundin C, Hodgson B, Sharma RA. DNA repair pathways as targets for cancer therapy. Nat Rev Cancer 2008;8:193-204.
2. Costantino L, Sotiriou SK, Rantala JK, Magin S, Mladenov E, Helleday T, et al. Break-induced replication repair of damaged forks induces genomic duplications in human cells. Science 2014;343:88-91.
3. Frosina G. Overexpression of enzymes that repair endogenous damage to DNA. Eur J Biochem 2000;267:2135-49.
4. Sarasin A, Kauffmann A. Overexpression of DNA repair genes is associated with metastasis: a new hypothesis. Mutat Res 2008;659:49-55.
5. Munson JM, Fried L, Rowson SA, Bonner MY, Karumbaiah L, Diaz B, et al. Anti-invasive adjuvant therapy with imipramine blue enhances chemotherapeutic efficacy against glioma. Sci Transl Med 2012;4:127ra36.
6. Yang WH, Su YH, Hsu WH, Wang CC, Arbiser JL, Yang MH. Imipramine blue halts head and neck cancer invasion through promoting F-box and leucine-rich repeat protein 14-mediated Twist1 degradation. Oncogene. 2015 Aug 10. [Epub ahead of print].
7. Khongkow P, Karunarathna U, Khongkow M, Gong C, Gomes AR, Yague E, et al. FOXM1 targets NBS1 to regulate DNA damage-induced senescence and epirubicin resistance. Oncogene 2014;33:4144-55.
8. Gstaiger M, Jordan R, Lim M, Catzavelos C, Mestan J, Slingerland J, et al. Skp2 is oncogenic and overexpressed in human cancers. Proc Natl Acad Sci U S A 2001;98:5043-8.
9. Wu J, Zhang X, Zhang L, Wu CY, Rezaeian AH, Chan CH, et al. Skp2 E3 ligase integrates ATM activation and homologous recombination repair by ubiquitinating NBS1. Mol Cell 2012;46:351-61.
10. Branzei D, Foiani M. Regulation of DNA repair throughout the cell cycle. Nat Rev Mol Cell Biol 2008;9:297-308.
11. Li Y, Zhang S, Huang S. FoxM1: a potential drug target for glioma. Future Oncol 2012;8:223-6.
12. Fan C, Oh DS, Wessels L, Weigelt B, Nuyten DS, Nobel AB, et al. Concordance among gene-expression-based predictors for breast cancer. N Engl J Med 2006;355:560-9.
13. Imam JS, Plyler JR, Bansal H, Prajapati S, Bansal S, Rebeles J, et al. Genomic loss of tumor suppressor miRNA-204 promotes cancer cell migration and invasion by activating AKT/mTOR/Rac1 signaling and actin reorganization. PLoS ONE 2012;7:e52397.
14. Arjonen A, Kaukonen R, Mattila E, Rouhi P, Hognas G, Sihto H, et al. Mutant p53-associated myosin-X upregulation promotes breast cancer invasion and metastasis. J Clin Invest 2014;124:1069-82.
15. Bagheri-Yarmand R, Mandal M, Taludker AH, Wang RA, Vadlamudi RK, Kung HJ, et al. Etk/Bmx tyrosine kinase activates Pak1 and regulates tumorigenicity of breast cancer cells. J Biol Chem 2001;276: 29403-9.
16. Kocaturk B, Versteeg HH. Orthotopic injection of breast cancer cells into the mammary fat pad of mice to study tumor growth. J Vis Exp 2015;8.
17. Zhu H, Yan H, Jin W, Dai C, Chen Z, Zheng F, et al. The staining patterns of 53BP1 nuclear foci and 53BP1 mRNA level are associated with cervical cancer progression and metastasis. Int J Gynecol Pathol 2014; 33:241-7.
18. Gunn A, Bennardo N, Cheng A, Stark JM. Correct end use during end joining of multiple chromosomal double strand breaks is influenced by repair protein RAD50, DNA-dependent protein kinase DNA-PKcs, and transcription context. J Biol Chem 2011;286:42470-82.
19. Pierce AJ, Johnson RD, Thompson LH, Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev 1999;13:2633-8.
20. Stark JM, Pierce AJ, Oh J, Pastink A, Jasin M. Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol Cell Biol 2004;24:9305-16.
21. Imam JS, Buddavarapu K, Lee-Chang JS, Ganapathy S, Camosy C, Chen Y, et al. MicroRNA-185 suppresses tumor growth and progression by targeting the Six1 oncogene in human cancers. Oncogene 2010;29:4971-9.
22. Mohammed H, Russell IA, Stark R, Rueda OM, Hickey TE, Tarulli GA, et al. Progesterone receptor modulates ERalpha action in breast cancer. Nature 2015;523:313-7.
23. Brenneman MA, Weiss AE, Nickoloff JA, Chen DJ. XRCC3 is required for efficient repair of chromosome breaks by homologous recombination. Mutat Res 2000;459:89-97.
24. Silva VC, Cassimeris L. Stathmin and microtubules regulate mitotic entry in HeLa cells by controlling activation of both Aurora kinase A and Plk1. Mol Biol Cell 2013;24:3819-31.
25. Brenneman MA, Wagener BM, Miller CA, Allen C, Nickoloff JA. XRCC3 controls the fidelity of homologous recombination: roles for XRCC3 in late stages of recombination. Mol Cell 2002;10:387-95.
26. Musgrove EA, Caldon CE, Barraclough J, Stone A, Sutherland RL. Cyclin D as a therapeutic target in cancer. Nat Rev Cancer 2011;11:558-72.
27. Mencalha AL, Binato R, Ferreira GM, Du Rocher B, 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:e48160.
28. Hollander MC, Philburn RT, Patterson AD, Wyatt MA, Fornace AJ Jr. Genomic instability in Gadd45a-/- cells is coupled with S-phase checkpoint defects. Cell Cycle 2005;4:704-9.
29. Harkin DP, Bean JM, Miklos D, Song YH, Truong VB, Englert C, et al. Induction of GADD45 and JNK/SAPK-dependent apoptosis following inducible expression of BRCA1. Cell 1999;97:575-86.
30. Panier S, Boulton SJ. Double-strand break repair: 53BP1 comes into focus. Nat Rev Mol Cell Biol 2014;15:7-18.
31. Zona S, Bella L, Burton MJ, de Moraes GN, Lam EWF. FOXM1: an emerging master regulator of DNA damage response and genotoxic agent resistance. Biochim Biophys Acta 2014;1839:1316-22.
32. Baumann P, West SC. Role of the human RAD51 protein in homologous recombination and double-stranded break repair. Trends Biochem Sci 1998;23:247-51.
33. Wang IC, Chen YJ, Hughes D, Petrovic V, Major ML, Park HJ, et al. 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;25:10875-94.
34. Li X, Yao R, Yue L, Qiu W, Qi W, Liu S, et al. FOXM1 mediates resistance to docetaxel in gastric cancer via up-regulating Stathmin. J Cell Mol Med 2014;18:811-23.
35. Anders L, Ke N, Hydbring P, Choi YJ, Widlund HR, Chick JM, et al. A systematic screen for CDK4/6 substrates links FOXM1 phosphorylation to senescence suppression in cancer cells. Cancer Cell 2011;20:620-34.
36. Wierstra I, Alves J. FOXM1, a typical proliferation-associated transcription factor. Biol Chem 2007;388:1257-74.
37. Chen X, Muller GA, Quaas M, Fischer M, Han N, Stutchbury B, et al. The forkhead transcription factor FOXM1 controls cell cycle-dependent gene expression through an atypical chromatin binding mechanism. Mol Cell Biol 2013;33:227-36.
38. Jirawatnotai S, Hu Y, Michowski W, Elias JE, Becks L, Bienvenu F, et al. A function for cyclin D1 in DNA repair uncovered by protein interactome analyses in human cancers. Nature 2011;474:230-4.
39. Wang XC, Tian LL, Tian J, Jiang XY. Overexpression of SKP2 promotes the radiation resistance of esophageal squamous cell carcinoma. Radiat Res 2012;177:52-8.
40. Smolarz B, Makowska M, Samulak D, Michalska MM, Mojs E, Wilczak M, et al. Association between single nucleotide polymorphisms (SNPs) of XRCC2 and XRCC3 homologous recombination repair genes and triplenegative breast cancer in Polish women. Clin Exp Med 2015;15:151-7.
41. Petermann E, Orta ML, Issaeva N, Schultz N, Helleday T. Hydroxyureastalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol Cell 2010;37:492-502.
42. Yang X, Zhang Y, Hosaka K, Andersson P, Wang J, Tholander F, et al. VEGF-B promotes cancer metastasis through a VEGF-A-independent mechanism and serves as a marker of poor prognosis for cancer patients. Proc Natl Acad Sci U S A 2015;112:E2900-9.
43. Zhang Y, Zhang N, Dai B, Liu M, Sawaya R, Xie K, et al. FoxM1B transcriptionally regulates vascular endothelial growth factor expression and promotes the angiogenesis and growth of glioma cells. Cancer Res 2008;68:8733-42.
44. Ji H, Cao R, Yang Y, Zhang Y, Iwamoto H, Lim S, et al. TNFR1 mediates TNFalpha-induced tumour lymphangiogenesis and metastasis by modulating VEGF-C-VEGFR3 signalling. Nat Commun 2014;5:4944.
45. Yang X, Zhang Y, Yang Y, Lim S, Cao Z, Rak J, et al. Vascular endothelial growth factor-dependent spatiotemporal dual roles of placental growth factor in modulation of angiogenesis and tumor growth. Proc Natl Acad Sci U S A 2013;110:13932-7.
46. Cao Y, Arbiser J, D'Amato RJ, D'Amore PA, Ingber DE, Kerbel R, et al. Fortyyear journey of angiogenesis translational research. Sci Transl Med 2011;3:114rv3.