ISSN: 2008-2258
Vol 14, No 4 (2021): Autumn
Effects of trichostatin A on the intrinsic and extrinsic apoptotic pathway, cell viability, and apoptosis induction in hepatocellular carcinoma cell lines
Gastroenterology and Hepatology from Bed to Bench,
,
https://doi.org/10.22037/ghfbb.v14i4.2179
Abstract
Background: Modulation of the acetylation status of histones, histones modification, plays an important role in regulating gene transcription and expression. Histone deacetylation controlled by histone deacetylases (HDACs) leads to gene downregulation. Histone deacetylase inhibitors (HDACIs) are an emerging class of therapeutics with potential anticancer effects. They can induce apoptosis through the activation of both extrinsic and intrinsic apoptotic pathways. The current study was assigned to investigate the effect of trichostatin A (TSA) on mitochondrial/intrinsic [pro- (Bax, Bak, and Bim) and anti- (Bcl-2, Bcl-xL, and Mcl-1) apoptotic genes] and cytoplasmic/extrinsic (DR4, DR5, FAS, FAS-L, and TRAIL genes) pathways, histone deacetylase 1, 2, and 3, p53, p73, cell viability, and apoptosis in hepatocellular carcinoma (HCC) HCCLM3, MHCC97H, and MHCC97L cell lines. Methods: The HCCLM3, MHCC97H, and MHCC97L cells were cultured and treated with TSA. To determine viability, apoptosis, and the relative expression level of the mentioned genes, MTT assay, cell apoptosis assay, and qRT-PCR were done respectively. Results: TSA up-regulated the Bax, Bak, Bim, DR4, DR5, FAS, FAS-L, TRAIL, p53, and p73 and down-regulated Bcl-2, Bcl-xL, Mcl-1, histone deacetylases 1, 2, and 3 significantly resulting in apoptosis induction. Maximal and minimal apoptosis was seen in MHCC97H and HCCLM3 cell line (93.94 and 39.68 %) respectively after 24 and 48 h. Therefore, the MHCC97H cell line was more sensitive to TSA. Conclusion: Our findings demonstrated that HDAC inhibitor TSA can induce apoptosis and inhibit cell growth through both mitochondrial/intrinsic and cytoplasmic/extrinsic apoptotic pathways in hepatocellular carcinoma HCCLM3, MHCC97H, and MHCC97L cell lines.
Keywords:
- Trichostatin A, Extrinsic, Intrinsic, Pathway, Apoptosis
How to Cite
Sanaei , M., & Kavoosi, F. (2021). Effects of trichostatin A on the intrinsic and extrinsic apoptotic pathway, cell viability, and apoptosis induction in hepatocellular carcinoma cell lines . Gastroenterology and Hepatology from Bed to Bench, 14(4). https://doi.org/10.22037/ghfbb.v14i4.2179
References
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11. Ashkenazi A. Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nature Reviews Cancer 2002; 2:420-430.
12. Nakata S, Yoshida T, Horinaka M, Shiraishi T, Wakada M, Sakai T. Histone deacetylase inhibitors upregulate death receptor 5/TRAIL-R2 and sensitize apoptosis induced by TRAIL/APO2-L in human malignant tumor cells. Oncogene 2004; 23:6261-6271.
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17.Muscolini M, Cianfrocca R, Sajeva A, Mozzetti S, Ferrandina G, Costanzo A, et al. Trichostatin A up-regulates p73 and induces Bax-dependent apoptosis in cisplatin-resistant ovarian cancer cells. Mol Cancer Ther 2008; 7:1410-1419.
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19. Sanaei M, Kavoosi F, Arabloo M. Effect of Curcumin in Comparison With Trichostatin A on the Reactivation of Estrogen Receptor Alpha Gene Expression, Cell Growth Inhibition and Apoptosis Induction in Hepatocellular Carcinoma Hepa 1-6 Cell lLine. Asian Pacific Journal of Cancer Prevention. 2020;21: 1045-1050.
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21. Sanaei M, Kavoosi F, Roustazadeh A, Shahsavani H. In vitro effect of the histone deacetylase inhibitor valproic acid on viability and apoptosis of the PLC/PRF5 human hepatocellular carcinoma cell line. Asian Pacific journal of cancer prevention: APJCP 2018; 19:2507.
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25. Xu Y, Liu L, Qiu X, Liu Z, Li H, Li Z, et al. CCL21/CCR7 prevents apoptosis via the ERK pathway in human non-small cell lung cancer cells. PLoS One 2012; 7:33262-33271
26. Zhang Y-L, Pang L-Q, Wu Y, Wang X-Y, Wang C-Q, Fan Y. Significance of Bcl-xL in human colon carcinoma. World journal of gastroenterology: WJG 2008;14: 3069-3075.
27. Wang B, Ni Z, Dai X, Qin L, Li X, Xu L, et al. The Bcl-2/xL inhibitor ABT-263 increases the stability of Mcl-1 mRNA and protein in hepatocellular carcinoma cells. Mol Cancer 2014;13: 98-104.
28. Nakamoto N, Higuchi H, Kanamori H, Kurita S, Tada S, Takaishi H, et al. Cyclooxygenase-2 inhibitor and interferon-β synergistically induce apoptosis in human hepatoma cells in vitro and in vivo. Int J Oncol 2006; 29:625-635.
29. Werner J-M, Kuhl S, Stavrinou P, Roehn G, Krischek B, Blau T, et al. Expression of FAS-L differs from primary to relapsed low-grade gliomas and predicts progression-free survival. Anticancer Research. 2017;37: 6639-6648.
30. Zuo C, Qiu X, Liu N, Yang D, Xia M, Liu J, et al. Interferon-α and cyclooxygenase-2 inhibitor cooperatively mediates TRAIL-induced apoptosis in hepatocellular carcinoma. Experimental cell research. 2015;333(2):316-26.
31. Jin KL, Pak JH, Park J-Y, Choi WH, Lee J-Y, Kim J-H, et al. Expression profile of histone deacetylases 1, 2 and 3 in ovarian cancer tissues. J Gynecol Oncol 2008; 19:185-190.
32. Fang JY, Chen YX, Juan L, Rong L, Li Y, Zhu HY, et al. Epigenetic modification regulates both expression of tumor-associated genes and cell cycle progressing in human colon cancer cell lines: Colo-320 and SW1116. Cell Res 2004; 14:217-226.
33. Johnson MR, Wang K, Smith JB, Heslin MJ, Diasio RB. Quantitation of dihydropyrimidine dehydrogenase expression by real-time reverse transcription polymerase chain reaction. Analytical biochemistry. 2000;278:175-184.
34. Rosato RR, Almenara JA, Dai Y, Grant S. Simultaneous activation of the intrinsic and extrinsic pathways by histone deacetylase (HDAC) inhibitors and tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) synergistically induces mitochondrial damage and apoptosis in human leukemia cells. Molecular Cancer Therapeutics. 2003;2: 1273-1284.
35. Matthews GM, Newbold A, Johnstone RW. Intrinsic and extrinsic apoptotic pathway signaling as determinants of histone deacetylase inhibitor antitumor activity. Advances in cancer research.2012; 116: 165-197.
36. Kim H-R, Kim E-J, Yang S-H, Jeong E-T, Park C, Lee J-H, et al. Trichostatin A induces apoptosis in lung cancer cells via simultaneous activation of the death receptor-mediated and mitochondrial pathway. Experimental & molecular medicine. 2006; 38:616-624.
37. Sanaei M, Kavoosi F. Effect of Trichostatin A on Histone Deacetylases 1, 2 and 3, p21Cip1/Waf1/Sdi1, p27Kip1, and p57Kip2 Gene Expression in Breast Cancer SK-BR-3 Cell Line. Asian Pacific Journal of Cancer Biology. 2020; 5:57-62.
38. Shankar S, Singh TR, Fandy TE, Luetrakul T, Ross DD, Srivastava RK. Interactive effects of histone deacetylase inhibitors and TRAIL on apoptosis in human leukemia cells: involvement of both death receptor and mitochondrial pathways. International journal of molecular medicine. 2005; 16:1125-1138.
39. Inoue S, Riley J, Gant TW, Dyer MJ, Cohen GM. Apoptosis induced by histone deacetylase inhibitors in leukemic cells is mediated by Bim and Noxa. Leukemia. 2007;21: 1773-1782.
40. Montani MSG, Granato M, Santoni C, Del Porto P, Merendino N, D’Orazi G, et al. Histone deacetylase inhibitors VPA and TSA induce apoptosis and autophagy in pancreatic cancer cells. Cellular Oncology. 2017; 40:167-180.
41. Mühlethaler-Mottet A, Flahaut M, Bourloud KB, Auderset K, Meier R, Joseph J-M, et al. Histone deacetylase inhibitors strongly sensitise neuroblastoma cells to TRAIL-induced apoptosis by a caspases-dependent increase of the pro-to anti-apoptotic proteins ratio. BMC cancer. 2006; 6:1-13.
42. Meng J, Zhang H-H, Zhou C-X, Li C, Zhang F, Mei Q-B. The histone deacetylase inhibitor trichostatin A induces cell cycle arrest and apoptosis in colorectal cancer cells via p53-dependent and-independent pathways. Oncology reports. 2012; 28:384-388.
43. Eckschlager T, Plch J, Stiborova M, Hrabeta J. Histone deacetylase inhibitors as anticancer drugs. International journal of molecular sciences. 2017;18: 1414-1421.
44. Wu L-F, Li G-P, Su J-D, Pu Z-J, Feng J-L, Ye Y-Q, et al. Involvement of NF-κB activation in the apoptosis induced by extracellular adenosine in human hepatocellular carcinoma HepG2 cells. Biochemistry and Cell Biology. 2010; 88:705-714.
45. Muscolini M, Cianfrocca R, Sajeva A, Mozzetti S, Ferrandina G, Costanzo A, et al. Trichostatin A up-regulates p73 and induces Bax-dependent apoptosis in cisplatin-resistant ovarian cancer cells. Molecular Cancer Therapeutics. 2008;7: 1410-1419.
46. Decrion-Barthod A-Z, Bosset M, Plissonnier M-L, Marchini A, Nicolier M, Launay S, et al. Sodium butyrate with UCN-01 has marked antitumour activity against cervical cancer cells. Anticancer research. 2010; 30:4049-4061.
2. Ververis K, Hiong A, Karagiannis TC, Licciardi PV. Histone deacetylase inhibitors (HDACIs): multitargeted anticancer agents. Biologics: targets & therapy 2013; 7:47-53.
3. Dokmanovic M, Marks PA. Prospects: histone deacetylase inhibitors. J Cell Biochem 2005; 96:293-304.
4. Kim T-Y, Bang Y-J, Robertson KD. Histone deacetylase inhibitors for cancer therapy. Epigenetics 2006; 1:15-24.
5. Mottamal M, Zheng S, Huang TL, Wang G. Histone deacetylase inhibitors in clinical studies as templates for new anticancer agents. Molecules 2015;20: 3898-3941.
6. Doi S, Soda H, Oka M, Tsurutani J, Kitazaki T, Nakamura Y, Fukuda M, Yamada Y, Kamihira S, Kohno S. The histone deacetylase inhibitor FR901228 induces caspase-dependent apoptosis via the mitochondrial pathway in small cell lung cancer cells. Mol Cancer Ther 2004; 3:1397-1402.
7. Opferman JT, Kothari A. Anti-apoptotic BCL-2 family members in development. Cell Death Differ 2018; 25:37-45.
8. Sayers TJ. Targeting the extrinsic apoptosis signaling pathway for cancer therapy. Cancer Immunol, Immunother 2011;60:1173-1180.
9. Yagita H, Takeda K, Hayakawa Y, Smyth MJ, Okumura K. TRAIL and its receptors as targets for cancer therapy. Cancer Sci 2004; 95:777-783.
10. Xu W, Parmigiani R, Marks P. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 2007;26: 5541-5552.
11. Ashkenazi A. Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nature Reviews Cancer 2002; 2:420-430.
12. Nakata S, Yoshida T, Horinaka M, Shiraishi T, Wakada M, Sakai T. Histone deacetylase inhibitors upregulate death receptor 5/TRAIL-R2 and sensitize apoptosis induced by TRAIL/APO2-L in human malignant tumor cells. Oncogene 2004; 23:6261-6271.
13. Insinga A, Monestiroli S, Ronzoni S, Gelmetti V, Marchesi F, Viale A, et al. Inhibitors of histone deacetylases induce tumor-selective apoptosis through activation of the death receptor pathway. Nat Med 2005; 11:71-76.
14. Hrabeta J, Stiborova M, Adam V, Kizek R, Eckschlager T. Histone deacetylase inhibitors in cancer therapy. A review. Biomedical Papers 2014; 158:161-169.
15. Meng J, Zhang H-H, Zhou C-X, Li C, Zhang F, Mei Q-B. The histone deacetylase inhibitor trichostatin A induces cell cycle arrest and apoptosis in colorectal cancer cells via p53-dependent and-independent pathways. Oncol Rep 2012; 28:384-388.
16. Henderson C, Mizzau M, Paroni G, Maestro R, Schneider C, Brancolini C. Role of caspases, Bid, and p53 in the apoptotic response triggered by histone deacetylase inhibitors trichostatin-A (TSA) and suberoylanilide hydroxamic acid (SAHA). J Biol Chem 2003;278: 12579-12589.
17.Muscolini M, Cianfrocca R, Sajeva A, Mozzetti S, Ferrandina G, Costanzo A, et al. Trichostatin A up-regulates p73 and induces Bax-dependent apoptosis in cisplatin-resistant ovarian cancer cells. Mol Cancer Ther 2008; 7:1410-1419.
18. Kim H-R, Kim E-J, Yang S-H, Jeong E-T, Park C, Lee J-H, et al. Trichostatin A induces apoptosis in lung cancer cells via simultaneous activation of the death receptor-mediated and mitochondrial pathway. Exp Mol Med 2006;38: 616-624.
19. Sanaei M, Kavoosi F, Arabloo M. Effect of Curcumin in Comparison With Trichostatin A on the Reactivation of Estrogen Receptor Alpha Gene Expression, Cell Growth Inhibition and Apoptosis Induction in Hepatocellular Carcinoma Hepa 1-6 Cell lLine. Asian Pacific Journal of Cancer Prevention. 2020;21: 1045-1050.
20. Sanaei M, Kavoosi F. Effect of curcumin and trichostatin a on the expression of DNA methyltransfrase 1 in hepatocellular carcinoma cell line hepa 1-6. Iranian Journal of Pediatric Hematology and Oncology 2018; 8:193-201.
21. Sanaei M, Kavoosi F, Roustazadeh A, Shahsavani H. In vitro effect of the histone deacetylase inhibitor valproic acid on viability and apoptosis of the PLC/PRF5 human hepatocellular carcinoma cell line. Asian Pacific journal of cancer prevention: APJCP 2018; 19:2507.
22. 15. Cao XX, Mohuiddin I, Chada S, Mhashilkar AM, Ozvaran MK, McConkey DJ, et al. Adenoviral transfer of mda-7 leads to BAX up-regulation and apoptosis in mesothelioma cells, and is abrogated by over-expression of BCL-XL. Mol Med 2002;8(12):869-76.
23. Morrison DJ, English MA, Licht JD. WT1 induces apoptosis through transcriptional regulation of the proapoptotic Bcl-2 family member Bak. Cancer research. 2005; 65:8174-8182.
24. Zhang X-Q, Dong J-J, Cai T, Shen X, Zhou X-J, Liao L. High glucose induces apoptosis via upregulation of Bim expression in proximal tubule epithelial cells. Oncotarget 2017;8: 24119-24125.
25. Xu Y, Liu L, Qiu X, Liu Z, Li H, Li Z, et al. CCL21/CCR7 prevents apoptosis via the ERK pathway in human non-small cell lung cancer cells. PLoS One 2012; 7:33262-33271
26. Zhang Y-L, Pang L-Q, Wu Y, Wang X-Y, Wang C-Q, Fan Y. Significance of Bcl-xL in human colon carcinoma. World journal of gastroenterology: WJG 2008;14: 3069-3075.
27. Wang B, Ni Z, Dai X, Qin L, Li X, Xu L, et al. The Bcl-2/xL inhibitor ABT-263 increases the stability of Mcl-1 mRNA and protein in hepatocellular carcinoma cells. Mol Cancer 2014;13: 98-104.
28. Nakamoto N, Higuchi H, Kanamori H, Kurita S, Tada S, Takaishi H, et al. Cyclooxygenase-2 inhibitor and interferon-β synergistically induce apoptosis in human hepatoma cells in vitro and in vivo. Int J Oncol 2006; 29:625-635.
29. Werner J-M, Kuhl S, Stavrinou P, Roehn G, Krischek B, Blau T, et al. Expression of FAS-L differs from primary to relapsed low-grade gliomas and predicts progression-free survival. Anticancer Research. 2017;37: 6639-6648.
30. Zuo C, Qiu X, Liu N, Yang D, Xia M, Liu J, et al. Interferon-α and cyclooxygenase-2 inhibitor cooperatively mediates TRAIL-induced apoptosis in hepatocellular carcinoma. Experimental cell research. 2015;333(2):316-26.
31. Jin KL, Pak JH, Park J-Y, Choi WH, Lee J-Y, Kim J-H, et al. Expression profile of histone deacetylases 1, 2 and 3 in ovarian cancer tissues. J Gynecol Oncol 2008; 19:185-190.
32. Fang JY, Chen YX, Juan L, Rong L, Li Y, Zhu HY, et al. Epigenetic modification regulates both expression of tumor-associated genes and cell cycle progressing in human colon cancer cell lines: Colo-320 and SW1116. Cell Res 2004; 14:217-226.
33. Johnson MR, Wang K, Smith JB, Heslin MJ, Diasio RB. Quantitation of dihydropyrimidine dehydrogenase expression by real-time reverse transcription polymerase chain reaction. Analytical biochemistry. 2000;278:175-184.
34. Rosato RR, Almenara JA, Dai Y, Grant S. Simultaneous activation of the intrinsic and extrinsic pathways by histone deacetylase (HDAC) inhibitors and tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) synergistically induces mitochondrial damage and apoptosis in human leukemia cells. Molecular Cancer Therapeutics. 2003;2: 1273-1284.
35. Matthews GM, Newbold A, Johnstone RW. Intrinsic and extrinsic apoptotic pathway signaling as determinants of histone deacetylase inhibitor antitumor activity. Advances in cancer research.2012; 116: 165-197.
36. Kim H-R, Kim E-J, Yang S-H, Jeong E-T, Park C, Lee J-H, et al. Trichostatin A induces apoptosis in lung cancer cells via simultaneous activation of the death receptor-mediated and mitochondrial pathway. Experimental & molecular medicine. 2006; 38:616-624.
37. Sanaei M, Kavoosi F. Effect of Trichostatin A on Histone Deacetylases 1, 2 and 3, p21Cip1/Waf1/Sdi1, p27Kip1, and p57Kip2 Gene Expression in Breast Cancer SK-BR-3 Cell Line. Asian Pacific Journal of Cancer Biology. 2020; 5:57-62.
38. Shankar S, Singh TR, Fandy TE, Luetrakul T, Ross DD, Srivastava RK. Interactive effects of histone deacetylase inhibitors and TRAIL on apoptosis in human leukemia cells: involvement of both death receptor and mitochondrial pathways. International journal of molecular medicine. 2005; 16:1125-1138.
39. Inoue S, Riley J, Gant TW, Dyer MJ, Cohen GM. Apoptosis induced by histone deacetylase inhibitors in leukemic cells is mediated by Bim and Noxa. Leukemia. 2007;21: 1773-1782.
40. Montani MSG, Granato M, Santoni C, Del Porto P, Merendino N, D’Orazi G, et al. Histone deacetylase inhibitors VPA and TSA induce apoptosis and autophagy in pancreatic cancer cells. Cellular Oncology. 2017; 40:167-180.
41. Mühlethaler-Mottet A, Flahaut M, Bourloud KB, Auderset K, Meier R, Joseph J-M, et al. Histone deacetylase inhibitors strongly sensitise neuroblastoma cells to TRAIL-induced apoptosis by a caspases-dependent increase of the pro-to anti-apoptotic proteins ratio. BMC cancer. 2006; 6:1-13.
42. Meng J, Zhang H-H, Zhou C-X, Li C, Zhang F, Mei Q-B. The histone deacetylase inhibitor trichostatin A induces cell cycle arrest and apoptosis in colorectal cancer cells via p53-dependent and-independent pathways. Oncology reports. 2012; 28:384-388.
43. Eckschlager T, Plch J, Stiborova M, Hrabeta J. Histone deacetylase inhibitors as anticancer drugs. International journal of molecular sciences. 2017;18: 1414-1421.
44. Wu L-F, Li G-P, Su J-D, Pu Z-J, Feng J-L, Ye Y-Q, et al. Involvement of NF-κB activation in the apoptosis induced by extracellular adenosine in human hepatocellular carcinoma HepG2 cells. Biochemistry and Cell Biology. 2010; 88:705-714.
45. Muscolini M, Cianfrocca R, Sajeva A, Mozzetti S, Ferrandina G, Costanzo A, et al. Trichostatin A up-regulates p73 and induces Bax-dependent apoptosis in cisplatin-resistant ovarian cancer cells. Molecular Cancer Therapeutics. 2008;7: 1410-1419.
46. Decrion-Barthod A-Z, Bosset M, Plissonnier M-L, Marchini A, Nicolier M, Launay S, et al. Sodium butyrate with UCN-01 has marked antitumour activity against cervical cancer cells. Anticancer research. 2010; 30:4049-4061.
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