Suberoylanilide hydroxamic acid (SAHA) reverses chemoresistance in head and neck cancer cells by targeting cancer stem cells via the downregulation of nanog

Genes and Cancer

Volumn 6, Issue 3-4, 2015, Pages 169-181

  Kumar, Bhavna ^a,b   Yadav, Arti ^b   Lang, James C ^a,b   Teknos, Theodoros N ^a,b   Kumar, Pawan ^a,b  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Cancer Stem Cells; Chemoresistance; HDAC; Human papillomavirus (HPV); Nanog; SAHA; Tumorsphere

Indexed keywords

HISTONE DEACETYLASE 1; TRANSCRIPTION FACTOR NANOG; VORINOSTAT;

ARTICLE; CANCER PATIENT; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; HEAD AND NECK CANCER; HUMAN; HUMAN CELL; IC50; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION;

EID: 84947020651     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: None     Document Type: Article

References (55)

1. Leemans CR, Braakhuis BJM and Brakenhoff RH. The molecular biology of head and neck cancer. Nat Rev Cancer. 2011; 11(1):9-22.
2. Mehanna H, Paleri V, West CML and Nutting C. Head and neck cancer-Part 1: Epidemiology, presentation, and prevention. BMJ. 2010; 341:c4684.
3. Siegel R, Ma J, Zou Z and Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014; 64(1):9-29.
4. Kalavrezos N and Bhandari R. Current trends and future perspectives in the surgical management of oral cancer. Oral Oncol. 2010; 46(6):429-432.
5. Siegel R, Naishadham D and Jemal A. Cancer statistics, 2012. CA Cancer J Clin. 2012; 62(1):10-29.
6. Marur S and Forastiere AA. Head and neck cancer: changing epidemiology, diagnosis, and treatment. Mayo Clin Proc. 2008; 83(4):489-501.
7. Worden FP, Kumar B, Lee JS, Wolf GT, Cordell KG, Taylor JM, Urba SG, Eisbruch A, Teknos TN, Chepeha DB, Prince ME, Tsien CI, D’Silva NJ, Yang K, Kurnit DM, Mason HL, et al. Chemoselection as a strategy for organ preservation in advanced oropharynx cancer: response and survival positively associated with HPV16 copy number. J Clin Oncol. 2008; 26(19):3138-3146.
8. Hrzenjak A, Moinfar F, Kremser ML, Strohmeier B, Staber PB, Zatloukal K and Denk H. Valproate inhibition of histone deacetylase 2 affects differentiation and decreases proliferation of endometrial stromal sarcoma cells. Mol Cancer Ther. 2006; 5(9):2203-2210.
9. Huang BH, Laban M, Leung CH, Lee L, Lee CK, Salto-Tellez M, Raju GC and Hooi SC. Inhibition of histone deacetylase 2 increases apoptosis and p21Cip1/WAF1 expression, independent of histone deacetylase 1. Cell Death Differ. 2005; 12(4):395-404.
10. Zhu P, Martin E, Mengwasser J, Schlag P, Janssen KP and Gottlicher M. Induction of HDAC2 expression upon loss of APC in colorectal tumorigenesis. Cancer Cell. 2004; 5(5):455-463.
11. Myzak MC, Dashwood WM, Orner GA, Ho E and Dashwood RH. Sulforaphane inhibits histone deacetylase in vivo and suppresses tumorigenesis in Apc-minus mice. Faseb J. 2006; 20(3):506-508.
12. Westendorf JJ, Zaidi SK, Cascino JE, Kahler R, van Wijnen AJ, Lian JB, Yoshida M, Stein GS and Li X. Runx2 (Cbfa1, AML-3) interacts with histone deacetylase 6 and represses the p21(CIP1/WAF1) promoter. Mol Cell Biol. 2002; 22(22):7982-7992.
13. Fraga MF, Ballestar E, Villar-Garea A, Boix-Chornet M, Espada J, Schotta G, Bonaldi T, Haydon C, Ropero S, Petrie K, Iyer NG, Perez-Rosado A, Calvo E, Lopez JA, Cano A, Calasanz MJ, et al. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet. 2005; 37(4):391-400.
14. Oehme I, Deubzer HE, Wegener D, Pickert D, Linke JP, Hero B, Kopp-Schneider A, Westermann F, Ulrich SM, von Deimling A, Fischer M and Witt O. Histone deacetylase 8 in neuroblastoma tumorigenesis. Clin Cancer Res. 2009; 15(1):91-99.
15. Park SY, Jun JA, Jeong KJ, Heo HJ, Sohn JS, Lee HY, Park CG and Kang J. Histone deacetylases 1, 6 and 8 are critical for invasion in breast cancer. Oncol Rep. 25(6):1677-1681.
16. Senese S, Zaragoza K, Minardi S, Muradore I, Ronzoni S, Passafaro A, Bernard L, Draetta GF, Alcalay M, Seiser C and Chiocca S. Role for histone deacetylase 1 in human tumor cell proliferation. Mol Cell Biol. 2007; 27(13):4784-4795.
17. Haberland M, Montgomery RL and Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet. 2009; 10(1):32-42.
18. Peng L and Seto E. Deacetylation of nonhistone proteins by HDACs and the implications in cancer. Handb Exp Pharmacol. 2011; 206:39-56.
19. Baltus GA, Kowalski MP, Tutter AV and Kadam S. A Positive Regulatory Role for the mSin3A-HDAC Complex in Pluripotency through Nanog and Sox2. Journal of Biological Chemistry. 2009; 284(11):6998-7006.
20. You JS, Kang JK, Seo D-W, Park JH, Park JW, Lee JC, Jeon YJ, Cho EJ and Han J-W. Depletion of Embryonic Stem Cell Signature by Histone Deacetylase Inhibitor in NCCIT Cells: Involvement of Nanog Suppression. Cancer Research. 2009; 69(14):5716-5725.
21. Lehrmann H, Pritchard LL and Harel-Bellan A. Histone acetyltransferases and deacetylases in the control of cell proliferation and differentiation. Adv Cancer Res. 2002; 86:41-65.
22. Gregoretti IV, Lee YM and Goodson HV. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J Mol Biol. 2004; 338(1):17-31.
23. Khan O and La Thangue NB. HDAC inhibitors in cancer biology: emerging mechanisms and clinical applications. Immunol Cell Biol. 2012; 90(1):85-94.
24. Kim HJ and Bae SC. Histone deacetylase inhibitors: molecular mechanisms of action and clinical trials as anticancer drugs. Am J Transl Res. 2011; 3(2):166-179.
25. West AC and Johnstone RW. New and emerging HDAC inhibitors for cancer treatment. The Journal of Clinical Investigation. 2014; 124(1):30-39.
26. Marks PA. Discovery and development of SAHA as an anticancer agent. Oncogene. 2007; 26(9):1351-1356.
27. Breslow R, Jursic B, Yan ZF, Friedman E, Leng L, Ngo L, Rifkind RA and Marks PA. Potent cytodifferentiating agents related to hexamethylenebisacetamide. Proc Natl Acad Sci U S A. 1991; 88(13):5542-5546.
28. Johnstone RW and Licht JD. Histone deacetylase inhibitors in cancer therapy: is transcription the primary target? Cancer Cell. 2003; 4(1):13-18.
29. Butler LM, Zhou X, Xu WS, Scher HI, Rifkind RA, Marks PA and Richon VM. The histone deacetylase inhibitor SAHA arrests cancer cell growth, up-regulates thioredoxinbinding protein-2, and down-regulates thioredoxin. Proc Natl Acad Sci U S A. 2002; 99(18):11700-11705.
30. Jeter CR, Liu B, Liu X, Chen X, Liu C, Calhoun-Davis T, Repass J, Zaehres H, Shen JJ and Tang DG. NANOG promotes cancer stem cell characteristics and prostate cancer resistance to androgen deprivation. Oncogene. 2011; 30(36):3833-3845.
31. Xie X, Piao L, Cavey GS, Old M, Teknos TN, Mapp AK and Pan Q. Phosphorylation of Nanog is essential to regulate Bmi1 and promote tumorigenesis. Oncogene. 2013; 33(16):2040-2052.
32. Kumar B, Yadav A, Lang JC, Cipolla MJ, Schmitt AC, Arradaza N, Teknos TN and Kumar P. YM155 reverses cisplatin resistance in head and neck cancer by decreasing cytoplasmic survivin levels. Mol Cancer Ther. 2012; 11(9):1988-1998.
33. Chou TC and Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul. 1984; 22:27-55.
34. Hauswald H, Simon C, Hecht S, Debus J and Lindel K. Long-term outcome and patterns of failure in patients with advanced head and neck cancer. Radiation Oncology. 2011; 6(1):70.
35. Leemans CR, Braakhuis BJ and Brakenhoff RH. The molecular biology of head and neck cancer. Nat Rev Cancer. 2011; 11(1):9-22.
36. Chang HH, Chiang CP, Hung HC, Lin CY, Deng YT and Kuo MY. Histone deacetylase 2 expression predicts poorer prognosis in oral cancer patients. Oral Oncol. 2009; 45(7):610-614.
37. Theocharis S, Klijanienko J, Giaginis C, Rodriguez J, Jouffroy T, Girod A, Alexandrou P and Sastre-Garau X. Histone deacetylase-1 and -2 expression in mobile tongue squamous cell carcinoma: associations with clinicopathological parameters and patients survival. Journal of Oral Pathology & Medicine. 2011; 40(9):706-714.
38. Rahmani M, Reese E, Dai Y, Bauer C, Payne SG, Dent P, Spiegel S and Grant S. Coadministration of histone deacetylase inhibitors and perifosine synergistically induces apoptosis in human leukemia cells through Akt and ERK1/2 inactivation and the generation of ceramide and reactive oxygen species. Cancer Res. 2005; 65(6):2422-2432.
39. Khan O and La Thangue NB. Drug Insight: histone deacetylase inhibitor-based therapies for cutaneous T-cell lymphomas. Nat Clin Pract Oncol. 2008; 5(12):714-726.
40. Fakhry C, Westra WH, Li S, Cmelak A, Ridge JA, Pinto H, Forastiere A and Gillison ML. Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial. J Natl Cancer Inst. 2008; 100(4):261-269.
41. Kumar B, Cordell KG, Lee JS, Worden FP, Prince ME, Tran HH, Wolf GT, Urba SG, Chepeha DB, Teknos TN, Eisbruch A, Tsien CI, Taylor JM, D’Silva NJ, Yang K, Kurnit DM, et al. EGFR, p16, HPV Titer, Bcl-xL and p53, sex, and smoking as indicators of response to therapy and survival in oropharyngeal cancer. J Clin Oncol. 2008; 26(19):3128-3137.
42. Kaka AS, Kumar B, Kumar P, Wakely PE, Jr., Kirsch CM, Old MO, Ozer E, Agrawal A, Carrau RE, Schuller DE, Siddiqui F and Teknos TN. Highly aggressive human papillomavirus-related oropharyngeal cancer: clinical, radiologic, and pathologic characteristics. Oral Surg Oral Med Oral Pathol Oral Radiol. 2013; 116(3):327-335.
43. Quon H and Forastiere AA. Controversies in treatment deintensification of human papillomavirus-associated oropharyngeal carcinomas: should we, how should we, and for whom? J Clin Oncol. 2013; 31(5):520-522.
44. Shangary S, Qin D, McEachern D, Liu M, Miller RS, Qiu S, Nikolovska-Coleska Z, Ding K, Wang G, Chen J, Bernard D, Zhang J, Lu Y, Gu Q, Shah RB, Pienta KJ, et al. Temporal activation of p53 by a specific MDM2 inhibitor is selectively toxic to tumors and leads to complete tumor growth inhibition. Proc Natl Acad Sci U S A. 2008; 105(10):3933-3938.
45. Miyachi M, Kakazu N, Yagyu S, Katsumi Y, Tsubai- Shimizu S, Kikuchi K, Tsuchiya K, Iehara T and Hosoi H. Restoration of p53 pathway by nutlin-3 induces cell cycle arrest and apoptosis in human rhabdomyosarcoma cells. Clin Cancer Res. 2009; 15(12):4077-4084.
46. Bourguignon LY, Earle C, Wong G, Spevak CC and Krueger K. Stem cell marker (Nanog) and Stat-3 signaling promote MicroRNA-21 expression and chemoresistance in hyaluronan/CD44-activated head and neck squamous cell carcinoma cells. Oncogene. 2012; 31(2):149-160.
47. Tsai L-L, Yu C-C, Chang Y-C, Yu C-H and Chou M-Y. Markedly increased Oct4 and Nanog expression correlates with cisplatin resistance in oral squamous cell carcinoma. Journal of Oral Pathology & Medicine. 2011; 40(8):621-628.
48. Lu X, Mazur SJ, Lin T, Appella E and Xu Y. The pluripotency factor nanog promotes breast cancer tumorigenesis and metastasis. Oncogene. 2014; 33(20):2655-2664.
49. Haigentz Jr M, Kim M, Sarta C, Lin J, Keresztes RS, Culliney B, Gaba AG, Smith RV, Shapiro GI, Chirieac LR, Mariadason JM, Belbin TJ, Greally JM, Wright JJ and Haddad RI. Phase II trial of the histone deacetylase inhibitor romidepsin in patients with recurrent/metastatic head and neck cancer. Oral Oncology. 2012; 48(12):1281-1288.
50. Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, Jiang B, Goodman MT, Sibug-Saber M, Cozen W, Liu L, Lynch CF, Wentzensen N, Jordan RC, Altekruse S, Anderson WF, et al. Human Papillomavirus and Rising Oropharyngeal Cancer Incidence in the United States. Journal of Clinical Oncology. 2011; 29(32):4294-4301.
51. Gioanni J, Fischel JL, Lambert JC, Demard F, Mazeau C, Zanghellini E, Ettore F, Formento P, Chauvel P, Lalanne CM and et al. Two new human tumor cell lines derived from squamous cell carcinomas of the tongue: establishment, characterization and response to cytotoxic treatment. European journal of cancer & clinical oncology. 1988; 24(9):1445-1455.
52. Brenner JC, Graham MP, Kumar B, Saunders LM, KupferR, Lyons RH, Bradford CR and Carey TE. Genotyping of 73 UM-SCC head and neck squamous cell carcinoma cell lines. Head & Neck. 2010; 32(4):417-426.
53. Livak KJ and Schmittgen TD. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-[Delta][Delta]CT Method. Methods. 2001; 25(4):402-408.
54. Islam M, Lin G, Brenner JC, Pan Q, Merajver SD, Hou Y, Kumar P and Teknos TN. RhoC Expression and Head and Neck Cancer Metastasis. Molecular Cancer Research. 2009; 7(11):1771-1780.
55. Kumar P, Ning Y and Polverini PJ. Endothelial cells expressing Bcl-2 promotes tumor metastasis by enhancing tumor angiogenesis, blood vessel leakiness and tumor invasion. Lab Invest. 2008; 88(7):740-749.