Histone deacetylase inhibitors inhibit rhabdomyosarcoma by reactive oxygen species-dependent targeting of specificity protein transcription factors

Molecular Cancer Therapeutics

Volumn 14, Issue 9, 2015, Pages 2143-2153

  Hedrick, Erik ^a   Crose, Lisa ^b   Linardic, Corinne M ^b   Safe, Stephen ^a,c  

^a TEXAS A AND M UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c Centre for Translational Cancer Research IBT Texas A and M HSC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE; MICRORNA; MICRORNA 17; MICRORNA 20A; MICRORNA 27A; PANOBINOSTAT; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR SP; UNCLASSIFIED DRUG; VORINOSTAT; ANTINEOPLASTIC AGENT; HISTONE DEACETYLASE INHIBITOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3; TRANSCRIPTION FACTOR SP4;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER PATIENT; CELL GROWTH; CELL INVASION; CELL SURVIVAL; DOWN REGULATION; DRUG MECHANISM; EPIGENETIC REPRESSION; GENE EXPRESSION; HISTONE ACETYLATION; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN TARGETING; RHABDOMYOSARCOMA; RHABDOMYOSARCOMA CELL; TUMOR GROWTH; UPREGULATION; ANIMAL; CELL PROLIFERATION; DISEASE MODEL; DRUG EFFECTS; DRUG SCREENING; HUMAN; METABOLISM; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DOWN-REGULATION; HISTONE DEACETYLASE INHIBITORS; HUMANS; REACTIVE OXYGEN SPECIES; RHABDOMYOSARCOMA; SP1 TRANSCRIPTION FACTOR; SP3 TRANSCRIPTION FACTOR; SP4 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84942122910     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-15-0148     Document Type: Article

References (50)

1. Paulino AC, Okcu MF. Rhabdomyosarcoma. Curr Probl Cancer 2008;32:7-34.
2. Breitfeld PP, Meyer WH. Rhabdomyosarcoma: new windows of opportunity. Oncologist 2005;10:518-27.
3. Parham DM, Ellison DA. Rhabdomyosarcomas in adults and children: an update. Arch Pathol Lab Med 2006;130:1454-65.
4. Sebire NJ, Malone M. Myogenin and MyoD1 expression in paediatric rhabdomyosarcomas. J Clin Pathol 2003;56:412-6.
5. Kumar S, Perlman E, Harris CA, Raffeld M, Tsokos M. Myogenin is a specific marker for rhabdomyosarcoma: an immunohistochemical study in paraffin-embedded tissues. Mod Pathol 2000;13:988-93.
6. Scrable HJ, Witte DP, Lampkin BC, Cavenee WK. Chromosomal localization of the human rhabdomyosarcoma locus by mitotic recombination mapping. Nature 1987;329:645-7.
7. Breneman JC, Lyden E, Pappo AS, Link MP, Anderson JR, Parham DM, et al. Prognostic factors and clinical outcomes in children and adolescents with metastatic rhabdomyosarcoma-a report from the Intergroup Rhabdomyosarcoma Study IV. J Clin Oncol 2003;21:78-84.
8. Barr FG, Galili N, Holick J, Biegel JA, Rovera G, Emanuel BS. Rearrangement of the PAX3 paired box gene in the paediatric solid tumour alveolar rhabdomyosarcoma. Nat Genet 1993;3:113-7.
9. Davis RJ, D'Cruz CM, Lovell MA, Biegel JA, Barr FG. Fusion of PAX7 to FKHR by the variant t(1;13)(p36;q14) translocation in alveolar rhabdomyosarcoma. Cancer Res 1994;54:2869-72.
10. Maurer HM. The Intergroup Rhabdomyosarcoma Study (NIH): objectives and clinical staging classification. J Pediatr Surg 1975;10:977-8.
11. Hettmer S, Li Z, Billin AN, Barr FG, Cornelison DD, Ehrlich AR, et al. Rhabdomyosarcoma: current challenges and their implications for developing therapies. Cold Spring Harb Perspect Med 2014;4:a025650.
12. Hudson MM, Ness KK, Gurney JG, Mulrooney DA, Chemaitilly W, Krull KR, et al. Clinical ascertainment of health outcomes among adults treated for childhood cancer. JAMA 2013;309:2371-81.
13. Chadalapaka G, Jutooru I, Sreevalsan S, Pathi S, Kim K, Chen C, et al. Inhibition of rhabdomyosarcoma cell and tumor growth by targeting specificity protein (Sp) transcription factors. Int J Cancer 2013;132:795-806.
14. Taniguchi E, Nishijo K, McCleish AT, Michalek JE, Grayson MH, Infante AJ, et al. PDGFR-A is a therapeutic target in alveolar rhabdomyosarcoma. Oncogene 2008;27:6550-60.
15. Libura J, Drukala J, Majka M, Tomescu O, Navenot JM, Kucia M, et al. CXCR4-SDF-1 signaling is active in rhabdomyosarcoma cells and regulates locomotion, chemotaxis, and adhesion. Blood 2002;100:2597-606.
16. Mayeenuddin LH, Yu Y, Kang Z, Helman LJ, Cao L. Insulin-like growth factor 1 receptor antibody induces rhabdomyosarcoma cell death via a process involving AKT and Bcl-x(L). Oncogene 2010;29:6367-77.
17. Miekus K, Lukasiewicz E, Jarocha D, Sekula M, Drabik G, Majka M. The decreased metastatic potential of rhabdomyosarcoma cells obtained through MET receptor downregulation and the induction of differentiation. Cell Death Dis 2013;4:e459.
18. Chen X, Stewart E, Shelat AA, Qu C, Bahrami A, Hatley M, et al. Targeting oxidative stress in embryonal rhabdomyosarcoma. Cancer Cell 2013;24:710-24.
19. Jutooru I, Guthrie AS, Chadalapaka G, Pathi S, Kim K, Burghardt R, et al. Mechanism of action of phenethylisothiocyanate and other reactive oxygen species-inducing anticancer agents. Mol Cell Biol 2014;34:2382-95.
20. O'Hagan HM, Wang W, Sen S, Destefano Shields C, Lee SS, Zhang YW, et al. Oxidative damage targets complexes containing DNA methyltransferases, SIRT1, and polycomb members to promoter CpG Islands. Cancer Cell 2011;20:606-19.
21. Jutooru I, Chadalapaka G, Abdelrahim M, Basha MR, Samudio I, Konopleva M, et al. Methyl 2-cyano-3,12-dioxooleana-1,9-dien-28-oate decreases specificity protein transcription factors and inhibits pancreatic tumor growth: role of microRNA-27a. Mol Pharmacol 2010;78:226-36.
22. Pathi SS, Jutooru I, Chadalapaka G, Sreevalsan S, Anand S, Thatcher GR, et al. GT-094, a NO-NSAID, inhibits colon cancer cell growth by activation of a reactive oxygen species-microRNA-27a: ZBTB10-specificity protein pathway. Mol Cancer Res 2011;9:195-202.
23. Jutooru I, Chadalapaka G, Lei P, Safe S. Inhibition of NFkappaB and pancreatic cancer cell and tumor growth by curcumin is dependent on specificity protein down-regulation. J Biol Chem 2010;285:25332-44.
24. Chintharlapalli S, Papineni S, Lei P, Pathi S, Safe S. Betulinic acid inhibits colon cancer cell and tumor growth and induces proteasome-dependent and -independent downregulation of specificity proteins (Sp) transcription factors. BMC Cancer 2011;11:371.
25. Gandhy SU, Kim K, Larsen L, Rosengren RJ, Safe S. Curcumin and synthetic analogs induce reactive oxygen species and decreases specificity protein (Sp) transcription factors by targeting microRNAs. BMC Cancer 2012;12:564.
26. Chadalapaka G, Jutooru I, Safe S. Celastrol decreases specificity proteins (Sp) and fibroblast growth factor receptor-3 (FGFR3) in bladder cancer cells. Carcinogenesis 2012;33:886-94.
27. Jutooru I, Chadalapaka G, Sreevalsan S, Lei P, Barhoumi R, Burghardt R, et al. Arsenic trioxide downregulates specificity protein (Sp) transcription factors and inhibits bladder cancer cell and tumor growth. Exp Cell Res 2010;316:2174-88.
28. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004;23:4051-60.
29. Kumar P, Luo Y, Tudela C, Alexander JM, Mendelson CR. The c-Myc-regulated microRNA-17-92 (miR-17-92) and miR-106a-363 clusters target hCYP19A1 and hGCM1 to inhibit human trophoblast differentiation. Mol Cell Biol 2013;33:1782-96.
30. Li X, Liu X, Xu W, Zhou P, Gao P, Jiang S, et al. c-MYC-regulated miR-23a/24-2/27a cluster promotes mammary carcinoma cell invasion and hepatic metastasis by targeting Sprouty2. J Biol Chem 2013;288:18121-33.
31. Chintharlapalli S, Papineni S, Lee SO, Lei P, Jin UH, Sherman SI, et al. Inhibition of pituitary tumor-transforming gene-1 in thyroid cancer cells by drugs that decrease specificity proteins. Mol Carcinog 2011;50:655-67.
32. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
33. Luo J, Solimini NL, Elledge SJ. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 2009;136:823-37.
34. Oh JE, Han JA, Hwang ES. Downregulation of transcription factor, Sp1, during cellular senescence. Biochem Biophys Res Commun 2007;353:86-91.
35. Ammendola R, Mesuraca M, Russo T, Cimino F. Sp1 DNA binding efficiency is highly reduced in nuclear extracts from aged rat tissues. J Biol Chem 1992;267:17944-8.
36. Adrian GS, Seto E, Fischbach KS, Rivera EV, Adrian EK, Herbert DC, et al. YY1 and Sp1 transcription factors bind the human transferrin gene in an age-related manner. J Gerontol A Biol Sci Med Sci 1996;51:B66-75.
37. Jiang NY, Woda BA, Banner BF, Whalen GF, Dresser KA, Lu D. Sp1, a new biomarker that identifies a subset of aggressive pancreatic ductal adenocarcinoma. Cancer Epidemiol Biomarkers Prev 2008;17:1648-52.
38. Yao JC, Wang L, Wei D, Gong W, Hassan M, Wu TT, et al. Association between expression of transcription factor Sp1 and increased vascular endothelial growth factor expression, advanced stage, and poor survival in patients with resected gastric cancer. Clin Cancer Res 2004;10:4109-17.
39. Zhang J, Zhu ZG, Ji J, Yuan F, Yu YY, Liu BY, et al. Transcription factor Sp1 expression in gastric cancer and its relationship to long-term prognosis. World J Gastroenterol 2005;11:2213-7.
40. Guan H, Cai J, Zhang N, Wu J, Yuan J, Li J, et al. Sp1 is upregulated in human glioma, promotes MMP-2-mediated cell invasion and predicts poor clinical outcome. Int J Cancer 2012;130:593-601.
41. Wang L, Wei D, Huang S, Peng Z, Le X, Wu TT, et al. Transcription factor Sp1 expression is a significant predictor of survival in human gastric cancer. Clin Cancer Res 2003;9:6371-80.
42. Safe S, Imanirad P, Sreevalsan S, Nair V, Jutooru I. Transcription factor Sp1, also known as specificity protein 1 as a therapeutic target. Expert Opin Ther Targets 2014;18:759-69.
43. Linardic CM, Downie DL, Qualman S, Bentley RC, Counter CM. Genetic modeling of human rhabdomyosarcoma. Cancer Res 2005;65:4490-5.
44. Lou Z, O'Reilly S, Liang H, Maher VM, Sleight SD, McCormick JJ. Downregulation of overexpressed sp1 protein in human fibrosarcoma cell lines inhibits tumor formation. Cancer Res 2005;65:1007-17.
45. Xu WS, Parmigiani RB, Marks PA. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 2007;26:5541-52.
46. Pathi SS, Lei P, Sreevalsan S, Chadalapaka G, Jutooru I, Safe S. Pharmacologic doses of ascorbic acid repress specificity protein (Sp) transcription factors and Sp-regulated genes in colon cancer cells. Nutr Cancer 2011;63:1133-42.
47. Perez-Torrado R, Yamada D, Defossez PA. Born to bind: the BTB protein-protein interaction domain. Bioessays 2006;28:1194-202.
48. Abraham J, Nunez-Alvarez Y, Hettmer S, Carrio E, Chen HI, Nishijo K, et al. Lineage of origin in rhabdomyosarcoma informs pharmacological response. Genes Dev 2014;28:1578-91.
49. Schwarzenbach H, Nishida N, Calin GA, Pantel K. Clinical relevance of circulating cell-free microRNAs in cancer. Nat Rev Clin Oncol 2014;11:145-56.
50. Wang J, Zhang KY, Liu SM, Sen S. Tumor-associated circulating microRNAs as biomarkers of cancer. Molecules 2014;19:1912-38.