HDAC inhibitors target HDAC5, upregulate MicroRNA-125a-5p, and induce apoptosis in breast cancer cells

Molecular Therapy

Volumn 23, Issue 4, 2015, Pages 656-666

  Hsieh, Tsung Hua ^a   Hsu, Chia Yi ^b   Tsai, Cheng Fang ^b   Long, Cheng Yu ^a   Wu, Chin Hu ^a   Wu, Deng Chyang ^c   Lee, Jau Nan ^a   Chang, Wei Chun ^d   Tsai, Eing Mei ^a,b,c  

^a KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^d CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 9; E1A ASSOCIATED P300 PROTEIN; HISTONE DEACETYLASE 5; HISTONE DEACETYLASE INHIBITOR; MICRORNA; MICRORNA 125A 5P; TRANSCRIPTION FACTOR RUNX3; TRICHOSTATIN A; UNCLASSIFIED DRUG; HDAC5 PROTEIN, HUMAN; HISTONE DEACETYLASE; MIRN125 MICRORNA, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER INHIBITION; CANCER STEM CELL; COMPLEX FORMATION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME INHIBITION; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; POSITIVE FEEDBACK; PROTEIN TARGETING; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BREAST TUMOR; DRUG EFFECTS; ENZYMOLOGY; GENETICS; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; APOPTOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; HETEROGRAFTS; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; MICE; MICRORNAS; UP-REGULATION;

EID: 84927055083     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.247     Document Type: Article

References (46)

1. Strahl, BD and Allis, CD (2000). The language of covalent histone modifications. Nature 403: 41-45.
2. Glozak, MA, Sengupta, N, Zhang, X and Seto, E (2005). Acetylation and deacetylation of non-histone proteins. Gene 363: 15-23.
3. Johnstone, RW (2002). Histone-deacetylase inhibitors: novel drugs for the treatment of cancer. Nat Rev Drug Discov 1: 287-299.
4. Dokmanovic, M, Clarke, C and Marks, PA (2007). Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res 5: 981-989.
5. El-Zawahry, A, Lu, P, White, SJ and Voelkel-Johnson, C (2006). In vitro efficacy of AdTRAIL gene therapy of bladder cancer is enhanced by trichostatin A-mediated restoration of CAR expression and downregulation of cFLIP and Bcl-XL. Cancer Gene Ther 13: 281-289.
6. Medina, V, Edmonds, B, Young, GP, James, R, Appleton, S and Zalewski, PD (1997). Induction of caspase-3 protease activity and apoptosis by butyrate and trichostatin A (inhibitors of histone deacetylase): dependence on protein synthesis and synergy with a mitochondrial/cytochrome c-dependent pathway. Cancer Res 57: 3697-3707.
7. Jones, PA and Baylin, SB (2007). The epigenomics of cancer. Cell 128: 683-692.
8. Hsieh, TH, Tsai, CF, Hsu, CY, Kuo, PL, Hsi, E, Suen, JL et al. (2012). n-Butyl benzyl phthalate promotes breast cancer progression by inducing expression of lymphoid enhancer factor 1. PLoS One 7: e42750.
9. Hsieh, TH, Tsai, CF, Hsu, CY, Kuo, PL, Lee, JN, Chai, CY et al. (2012). Phthalates stimulate the epithelial to mesenchymal transition through an HDAC6-dependent mechanism in human breast epithelial stem cells. Toxicol Sci 128: 365-376.
10. Wang, KH, Kao, AP, Chang, CC, Lee, JN, Hou, MF, Long, CY et al. (2010). Increasing CD44+/CD24(-) tumor stem cells, and upregulation of COX-2 and HDAC6, as major functions of HER2 in breast tumorigenesis. Mol Cancer 9: 288.
11. Scott, GK, Mattie, MD, Berger, CE, Benz, SC and Benz, CC (2006). Rapid alteration of microRNA levels by histone deacetylase inhibition. Cancer Res 66: 1277-1281.
12. Brest, P, Lassalle, S, Hofman, V, Bordone, O, Gavric Tanga, V, Bonnetaud, C et al. (2011). MiR-129-5p is required for histone deacetylase inhibitor-induced cell death in thyroid cancer cells. Endocr Relat Cancer 18: 711-719.
13. Jin, H, Liang, L, Liu, L, Deng, W and Liu, J (2013). HDAC inhibitor DWP0016 activates p53 transcription and acetylation to inhibit cell growth in U251 glioblastoma cells. J Cell Biochem 114: 1498-1509.
14. Bartel, DP (2009). MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
15. Chang, TC and Mendell, JT (2007). microRNAs in vertebrate physiology and human disease. Annu Rev Genomics Hum Genet 8: 215-239.
16. Gandellini, P, Profumo, V, Folini, M and Zaffaroni, N (2011). MicroRNAs as new therapeutic targets and tools in cancer. Expert Opin Ther Targets 15: 265-279.
17. Darzynkiewicz, Z, Juan, G, Li, X, Gorczyca, W, Murakami, T and Traganos, F (1997). Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis). Cytometry 27: 1-20.
18. Elefant, N, Berger, A, Shein, H, Hofree, M, Margalit, H and Altuvia, Y (2011). RepTar: a database of predicted cellular targets of host and viral miRNAs. Nucleic Acids Res 39(Database issue): D188-D194.
19. Krüger, J and Rehmsmeier, M (2006). RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res 34(Web Server issue): W451-W454.
20. Jin, YH, Jeon, EJ, Li, QL, Lee, YH, Choi, JK, Kim, WJ et al. (2004). Transforming growth factor-beta stimulates p300-dependent RUNX3 acetylation, which inhibits ubiquitination-mediated degradation. J Biol Chem 279: 29409-29417.
21. Ma, Y, Zhang, P, Wang, F, Zhang, H, Yang, J, Peng, J et al. (2012). miR-150 as a potential biomarker associated with prognosis and therapeutic outcome in colorectal cancer. Gut 61: 1447-1453.
22. Christensen, LL, Tobiasen, H, Holm, A, Schepeler, T, Ostenfeld, MS, Thorsen, K et al.; COLOFOL steering group. (2013). MiRNA-362-3p induces cell cycle arrest through targeting of E2F1, USF2 and PTPN1 and is associated with recurrence of colorectal cancer. Int J Cancer 133: 67-78.
23. Forrest, AR, Kanamori-Katayama, M, Tomaru, Y, Lassmann, T, Ninomiya, N, Takahashi, Y et al. (2010). Induction of microRNAs, mir-155, mir-222, mir-424 and mir-503, promotes monocytic differentiation through combinatorial regulation. Leukemia 24: 460-466.
24. Kano, M, Seki, N, Kikkawa, N, Fujimura, L, Hoshino, I, Akutsu, Y et al. (2010). miR-145, miR-133a and miR-133b: Tumor-suppressive miRNAs target FSCN1 in esophageal squamous cell carcinoma. Int J Cancer 127: 2804-2814.
25. Esquela-Kerscher, A, Trang, P, Wiggins, JF, Patrawala, L, Cheng, A, Ford, L et al. (2008). The let-7 microRNA reduces tumor growth in mouse models of lung cancer. Cell Cycle 7: 759-764.
26. Lin, RJ, Lin, YC and Yu, AL (2010). miR-149∗induces apoptosis by inhibiting Akt1 and E2F1 in human cancer cells. Mol Carcinog 49: 719-727.
27. Pass, HI, Goparaju, C, Ivanov, S, Donington, J, Carbone, M, Hoshen, M et al. (2010). hsa-miR-29c∗ is linked to the prognosis of malignant pleural mesothelioma. Cancer Res 70: 1916-1924.
28. Kim, HJ and Bae, SC (2011). Histone deacetylase inhibitors: molecular mechanisms of action and clinical trials as anti-cancer drugs. Am J Transl Res 3: 166-179.
29. Vigushin, DM, Ali, S, Pace, PE, Mirsaidi, N, Ito, K, Adcock, I et al. (2001). Trichostatin A is a histone deacetylase inhibitor with potent antitumor activity against breast cancer in vivo. Clin Cancer Res 7: 971-976.
30. Alao, JP, Stavropoulou, AV, Lam, EW, Coombes, RC and Vigushin, DM (2006). Histone deacetylase inhibitor, trichostatin A induces ubiquitin-dependent cyclin D1 degradation in MCF-7 breast cancer cells. Mol Cancer 5: 8.
31. Bolden, JE, Peart, MJ and Johnstone, RW (2006). Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 5: 769-784.
32. Wang, S, Huang, J, Lyu, H, Lee, CK, Tan, J, Wang, J et al. (2013). Functional cooperation of miR-125a, miR-125b, and miR-205 in entinostat-induced downregulation of erbB2/erbB3 and apoptosis in breast cancer cells. Cell Death Dis 4: e556.
33. Jiang, L, Huang, Q, Zhang, S, Zhang, Q, Chang, J, Qiu, X et al. (2010). Hsa-miR- 125a-3p and hsa-miR-125a-5p are downregulated in non-small cell lung cancer and have inverse effects on invasion and migration of lung cancer cells. BMC Cancer 10: 318.
34. Potenza, N, Papa, U, Mosca, N, Zerbini, F, Nobile, V and Russo, A (2011). Human microRNA hsa-miR-125a-5p interferes with expression of hepatitis B virus surface antigen. Nucleic Acids Res 39: 5157-5163.
35. Nishida, N, Mimori, K, Fabbri, M, Yokobori, T, Sudo, T, Tanaka, F et al. (2011). MicroRNA-125a-5p is an independent prognostic factor in gastric cancer and inhibits the proliferation of human gastric cancer cells in combination with trastuzumab. Clin Cancer Res 17: 2725-2733.
36. Jiang, L, Huang, Q, Chang, J, Wang, E and Qiu, X (2011). MicroRNA HSA-miR- 125a-5p induces apoptosis by activating p53 in lung cancer cells. Exp Lung Res 37: 387-398.
37. Guo, S, Lu, J, Schlanger, R, Zhang, H, Wang, JY, Fox, MC et al. (2010). MicroRNA miR-125a controls hematopoietic stem cell number. Proc Natl Acad Sci USA 107: 14229-14234.
38. de Ruijter, AJ, van Gennip, AH, Caron, HN, Kemp, S and van Kuilenburg, AB (2003). Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 370(Pt 3): 737-749.
39. Li, H, Xie, H, Liu, W, Hu, R, Huang, B, Tan, YF et al. (2009). A novel microRNA targeting HDAC5 regulates osteoblast differentiation in mice and contributes to primary osteoporosis in humans. J Clin Invest 119: 3666-3677.
40. Milde, T, Oehme, I, Korshunov, A, Kopp-Schneider, A, Remke, M, Northcott, P et al. (2010). HDAC5 and HDAC9 in medulloblastoma: novel markers for risk stratification and role in tumor cell growth. Clin Cancer Res 16: 3240-3252.
41. Bae, SC and Choi, JK (2004). Tumor suppressor activity of RUNX3. Oncogene 23: 4336-4340.
42. Lee, YS, Lee, JW, Jang, JW, Chi, XZ, Kim, JH, Li, YH et al. (2013). Runx3 inactivation is a crucial early event in the development of lung adenocarcinoma. Cancer Cell 24: 603-616.
43. Yano, T, Ito, K, Fukamachi, H, Chi, XZ, Wee, HJ, Inoue, K et al. (2006). The RUNX3 tumor suppressor upregulates Bim in gastric epithelial cells undergoing transforming growth factor beta-induced apoptosis. Mol Cell Biol 26: 4474-4488.
44. Wittmann, J and Jäck, HM (2010). Serum microRNAs as powerful cancer biomarkers. Biochim Biophys Acta 1806: 200-207.
45. Mitchell, PS, Parkin, RK, Kroh, EM, Fritz, BR, Wyman, SK, Pogosova-Agadjanyan, EL et al. (2008). Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 105: 10513-10518.
46. Hsieh, TH, Tsai, CF, Hsu, CY, Kuo, PL, Lee, JN, Chai, CY et al. (2012). Phthalates induce proliferation and invasiveness of estrogen receptor-negative breast cancer through the AhR/HDAC6/c-Myc signaling pathway. FASEB J 26: 778-787.