Butyrate induces ROS-mediated apoptosis by modulating miR-22/SIRT-1 pathway in hepatic cancer cells

Redox Biology

Volumn 12, Issue , 2017, Pages 340-349

  Pant, Kishor ^a   Yadav, Ajay K ^a   Gupta, Parul ^a   Islam, Rakibul ^a   Saraya, Anoop ^b   Venugopal, Senthil K ^a  

^a SOUTH ASIAN UNIVERSITY   (India)

^b ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

Apoptosis; Cell proliferation; Hepatocellular carcinoma; Non alcoholic fatty liver disease; Short chain fatty acid

Indexed keywords

ACETYLCYSTEINE; BETA CATENIN; BUTYRIC ACID; CASPASE 3; CYTOCHROME C; GLYCOGEN SYNTHASE KINASE 3; MICRORNA 22; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; SIRTUIN 1; SUPEROXIDE DISMUTASE; ANTINEOPLASTIC AGENT; MICRORNA; MIRN22 MICRORNA, HUMAN; SIRT1 PROTEIN, HUMAN;

ABTS RADICAL SCAVENGING ASSAY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME RELEASE; GENE OVEREXPRESSION; GROWTH INHIBITION; HUMAN; HUMAN CELL; INCUBATION TIME; INHIBITION KINETICS; LIVER CANCER; LIVER CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; PROTEIN EXPRESSION; TUNEL ASSAY; CELL SURVIVAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; LIVER TUMOR; METABOLISM; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; BUTYRIC ACID; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIVER NEOPLASMS; MICRORNAS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SIRTUIN 1;

EID: 85014869477     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2017.03.006     Document Type: Article

References (51)

1. [1] den Besten, G., van Eunen, K., Groen, A.K., Venema, K., Reijngoud, D.-J., Bakker, B.M., The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54 (2013), 2325–2340, 10.1194/jlr.R036012.
2. [2] Louis, M., Rosato, R.R., Brault, L., Osbild, S., Battaglia, E., Yang, X.-H., Grant, S., Bagrel, D., The histone deacetylase inhibitor sodium butyrate induces breast cancer cell apoptosis through diverse cytotoxic actions including glutathione depletion and oxidative stress. Int. J. Oncol. 25 (2004), 1701–1711.
3. [3] Louis, P., Hold, G.L., Flint, H.J., The gut microbiota, bacterial metabolites and colorectal cancer. Nat. Rev. Microbiol. 12 (2014), 661–672, 10.1038/nrmicro3344.
4. [4] Lane, A.A., Chabner, B.A., Histone deacetylase inhibitors in cancer therapy. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 27 (2009), 5459–5468, 10.1200/JCO.2009.22.1291.
5. [5] Berni Canani, R., Di Costanzo, M., Leone, L., The epigenetic effects of butyrate: potential therapeutic implications for clinical practice. Clin. Epigenetics, 4, 2012, 4, 10.1186/1868-7083-4-4.
6. [6] Barshishat, M., Levi, I., Benharroch, D., Schwartz, B., Butyrate down-regulates CD44 transcription and liver colonisation in a highly metastatic human colon carcinoma cell line. Br. J. Cancer 87 (2002), 1314–1320, 10.1038/sj.bjc.6600574.
7. [7] Zeng, H., Briske-Anderson, M., Prolonged butyrate treatment inhibits the migration and invasion potential of HT1080 tumor cells. J. Nutr. 135 (2005), 291–295.
8. [8] Chen, H.-C., Jeng, Y.-M., Yuan, R.-H., Hsu, H.-C., Chen, Y.-L., SIRT1 promotes tumorigenesis and resistance to chemotherapy in hepatocellular carcinoma and its expression predicts poor prognosis. Ann. Surg. Oncol. 19 (2011), 2011–2019, 10.1245/s10434-011-2159-4.
9. [9] Zhang, T., Rong, N., Chen, J., Zou, C., Jing, H., Zhu, X., Zhang, W., SIRT1 expression is associated with the chemotherapy response and prognosis of patients with advanced NSCLC. PLoS One, 8, 2013, e79162, 10.1371/journal.pone.0079162.
10. [10] Osama, A., Sabry, D., Hassany, S.M., Abdelmoneim, S.S., Sabry, A., SIRT-1expression is associated with expression of NANOG in patients with colorectal adenocarcinoma. Cancer Biomark. Sect. Dis. Markers 17 (2016), 155–163, 10.3233/CBM-160626.
11. [11] Cao, B., He, X., Wang, W., Shi, M., SIRT1 Influences the sensitivity of A549 non-small cell lung cancer cell line to cisplatin via modulating the Noxa expression. Zhongguo Fei Ai Za Zhi Chin. J. Lung Cancer 19 (2016), 57–63, 10.3779/j.issn.1009-3419.2016.02.01.
12. [12] Ha, M., Kim, V.N., Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 15 (2014), 509–524, 10.1038/nrm3838.
13. [13] Jansson, M.D., Lund, A.H., MicroRNA and cancer. Mol. Oncol. 6 (2012), 590–610, 10.1016/j.molonc.2012.09.006.
14. [14] Jiang, G., Wen, L., Zheng, H., Jian, Z., Deng, W., miR-204-5p targeting SIRT1 regulates hepatocellular carcinoma progression. Cell Biochem. Funct. 34 (2016), 505–510, 10.1002/cbf.3223.
15. [15] Duan, K., Ge, Y.-C., Zhang, X.-P., Wu, S.-Y., Feng, J.-S., Chen, S.-L., Zhang, L.I., Yuan, Z.-H., Fu, C.-H., miR-34a inhibits cell proliferation in prostate cancer by downregulation of SIRT1 expression. Oncol. Lett. 10 (2015), 3223–3227, 10.3892/ol.2015.3645.
16. [16] Chen, H., Lu, Q., Fei, X., Shen, L., Jiang, D., Dai, D., miR-22 inhibits the proliferation, motility, and invasion of human glioblastoma cells by directly targeting SIRT1. Tumour Biol. J. Int. Soc. Oncodev. Biol. Med. 37 (2016), 6761–6768, 10.1007/s13277-015-4575-8.
17. [17] Kumar, S., Gupta, P., Khanal, S., Shahi, A., Kumar, P., Sarin, S.K., Venugopal, S.K., Overexpression of microRNA-30a inhibits hepatitis B virus X protein-induced autophagosome formation in hepatic cells. FEBS J. 282 (2015), 1152–1163, 10.1111/febs.13209.
18. [18] Rao, X., Huang, X., Zhou, Z., Lin, X., An improvement of the 2ˆ(–delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. Biostat. Bioinform. Biomath. 3 (2013), 71–85.
19. [19] Kataoka, M., Fukura, Y., Shinohara, Y., Baba, Y., Analysis of mitochondrial membrane potential in the cells by microchip flow cytometry. Electrophoresis 26 (2005), 3025–3031, 10.1002/elps.200410402.
20. [20] Katalinic, V., Modun, D., Music, I., Boban, M., Gender differences in antioxidant capacity of rat tissues determined by 2,2′-azinobis (3-ethylbenzothiazoline 6-sulfonate; ABTS) and ferric reducing antioxidant power (FRAP) assays. Comp. Biochem. Physiol. Toxicol. Pharmacol. CBP 140 (2005), 47–52, 10.1016/j.cca.2005.01.005.
21. [21] Xu, D., Takeshita, F., Hino, Y., Fukunaga, S., Kudo, Y., Tamaki, A., Matsunaga, J., Takahashi, R., Takata, T., Shimamoto, A., Ochiya, T., Tahara, H., miR-22 represses cancer progression by inducing cellular senescence. J. Cell Biol. 193 (2011), 409–424, 10.1083/jcb.201010100.
22. [22] Das, B., Dobrowolski, C., Shahir, A.-M., Feng, Z., Yu, X., Sha, J., Bissada, N.F., Weinberg, A., Karn, J., Ye, F., Short chain fatty acids potently induce latent HIV-1 in T-cells by activating P-TEFb and multiple histone modifications. Virology 474 (2015), 65–81, 10.1016/j.virol.2014.10.033.
23. [23] Cheng, Y., Takeuchi, H., Sonobe, Y., Jin, S., Wang, Y., Horiuchi, H., Parajuli, B., Kawanokuchi, J., Mizuno, T., Suzumura, A., Sirtuin 1 attenuates oxidative stress via upregulation of superoxide dismutase 2 and catalase in astrocytes. J. Neuroimmunol. 269 (2014), 38–43, 10.1016/j.jneuroim.2014.02.001.
24. [24] Bolden, J.E., Peart, M.J., Johnstone, R.W., Anticancer activities of histone deacetylase inhibitors. Nat. Rev. Drug Discov. 5 (2006), 769–784, 10.1038/nrd2133.
25. [25] Ma, X., Ezzeldin, H.H., Diasio, R.B., Histone deacetylase inhibitors: current status and overview of recent clinical trials. Drugs 69 (2009), 1911–1934, 10.2165/11315680-000000000-00000.
26. [26] Tailor, D., Hahm, E.-R., Kale, R.K., Singh, S.V., Singh, R.P., Sodium butyrate induces DRP1-mediated mitochondrial fusion and apoptosis in human colorectal cancer cells. Mitochondrion 16 (2014), 55–64, 10.1016/j.mito.2013.10.004.
27. [27] Medina, V., Edmonds, B., Young, G.P., James, R., Appleton, S., Zalewski, P.D., 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 (1997), 3697–3707.
28. [28] Tang, Y., Chen, Y., Jiang, H., Nie, D., Short-chain fatty acids induced autophagy serves as an adaptive strategy for retarding mitochondria-mediated apoptotic cell death. Cell Death Differ. 18 (2011), 602–618, 10.1038/cdd.2010.117.
29. [29] Rahmani, M., Dai, Y., Grant, S., The histone deacetylase inhibitor sodium butyrate interacts synergistically with phorbol myristate acetate (PMA) to induce mitochondrial damage and apoptosis in human myeloid leukemia cells through a tumor necrosis factor-alpha-mediated process. Exp. Cell Res. 277 (2002), 31–47, 10.1006/excr.2002.5548.
30. [30] Yamakuchi, M., Ferlito, M., Lowenstein, C.J., miR-34a repression of SIRT1 regulates apoptosis. Proc. Natl. Acad. Sci. USA, 2008, 13421–13426, 10.1073/pnas.0801613105.
31. [31] Adlakha, Y.K., Saini, N., MiR-128 exerts pro-apoptotic effect in a p53 transcription-dependent and -independent manner via PUMA-Bak axis. Cell Death Dis., 4, 2013, e542, 10.1038/cddis.2013.46.
32. [32] Zhang, L., Wang, X., Chen, P., MiR-204 down regulates SIRT1 and reverts SIRT1-induced epithelial-mesenchymal transition, anoikis resistance and invasion in gastric cancer cells. BMC Cancer, 13, 2013, 290, 10.1186/1471-2407-13-290.
33. [33] Zhang, J., Yang, Y., Yang, T., Liu, Y., Li, A., Fu, S., Wu, M., Pan, Z., Zhou, W., MicroRNA-22, downregulated in hepatocellular carcinoma and correlated with prognosis, suppresses cell proliferation and tumourigenicity. Br. J. Cancer 103 (2010), 1215–1220, 10.1038/sj.bjc.6605895.
34. [34] Xiong, J., Yu, D., Wei, N., Fu, H., Cai, T., Huang, Y., Wu, C., Zheng, X., Du, Q., Lin, D., Liang, Z., An estrogen receptor α suppressor, microRNA-22, is downregulated in estrogen receptor α-positive human breast cancer cell lines and clinical samples. FEBS J. 277 (2010), 1684–1694, 10.1111/j.1742-4658.2010.07594.x.
35. [35] Li, J., Liang, S., Yu, H., Zhang, J., Ma, D., Lu, X., An inhibitory effect of miR-22 on cell migration and invasion in ovarian cancer. Gynecol. Oncol. 119 (2010), 543–548, 10.1016/j.ygyno.2010.08.034.
36. [36] Fung, K.Y.C., Brierley, G.V., Henderson, S., Hoffmann, P., McColl, S.R., Lockett, T., Head, R., Cosgrove, L., Butyrate-induced apoptosis in HCT116 colorectal cancer cells includes induction of a cell stress response. J. Proteome Res. 10 (2011), 1860–1869, 10.1021/pr1011125.
37. [37] Rada-Iglesias, A., Enroth, S., Ameur, A., Koch, C.M., Clelland, G.K., Respuela-Alonso, P., Wilcox, S., Dovey, O.M., Ellis, P.D., Langford, C.F., Dunham, I., Komorowski, J., Wadelius, C., Butyrate mediates decrease of histone acetylation centered on transcription start sites and down-regulation of associated genes. Genome Res. 17 (2007), 708–719, 10.1101/gr.5540007.
38. [38] Saunders, L.R., Verdin, E., Sirtuins: critical regulators at the crossroads between cancer and aging. Oncogene 26 (2007), 5489–5504, 10.1038/sj.onc.1210616.
39. [39] Wang, Z., Chen, W., Emerging roles of SIRT1 in cancer drug resistance. Genes Cancer 4 (2013), 82–90, 10.1177/1947601912473826.
40. [40] Pardo, P.S., Mohamed, J.S., Lopez, M.A., Boriek, A.M., Induction of Sirt1 by mechanical stretch of skeletal muscle through the early response factor EGR1 triggers an antioxidative response. J. Biol. Chem. 286 (2011), 2559–2566, 10.1074/jbc.M110.149153.
41. [41] Hori, Y.S., Kuno, A., Hosoda, R., Horio, Y., Regulation of FOXOs and p53 by SIRT1 modulators under oxidative stress. PLoS One, 8, 2013, e73875, 10.1371/journal.pone.0073875.
42. [42] Brunet, A., Sweeney, L.B., Sturgill, J.F., Chua, K.F., Greer, P.L., Lin, Y., Tran, H., Ross, S.E., Mostoslavsky, R., Cohen, H.Y., Hu, L.S., Cheng, H.-L., Jedrychowski, M.P., Gygi, S.P., Sinclair, D.A., Alt, F.W., Greenberg, M.E., Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303 (2004), 2011–2015, 10.1126/science.1094637.
43. [43] Portmann, S., Fahrner, R., Lechleiter, A., Keogh, A., Overney, S., Laemmle, A., Mikami, K., Montani, M., Tschan, M.P., Candinas, D., Stroka, D., Antitumor effect of SIRT1 inhibition in human HCC tumor models in vitro and in vivo. Mol. Cancer Ther. 12 (2013), 499–508, 10.1158/1535-7163.MCT-12-0700.
44. [44] Hwang, K.-E., Kim, Y.-S., Hwang, Y.-R., Kwon, S.-J., Park, D.-S., Cha, B.-K., Kim, B.-R., Yoon, K.-H., Jeong, E.-T., Kim, H.-R., Pemetrexed induces apoptosis in malignant mesothelioma and lung cancer cells through activation of reactive oxygen species and inhibition of sirtuin 1. Oncol. Rep. 33 (2015), 2411–2419, 10.3892/or.2015.3830.
45. [45] Kumari, S., Chaurasia, S.N., Nayak, M.K., Mallick, R.L., Dash, D., Sirtuin inhibition induces apoptosis-like changes in platelets and thrombocytopenia. J. Biol. Chem. 290 (2015), 12290–12299, 10.1074/jbc.M114.615948.
46. [46] Massaoka, M.H., Matsuo, A.L., Figueiredo, C.R., Farias, C.F., Girola, N., Arruda, D.C., Scutti, J.A.B., Romoff, P., Favero, O.A., Ferreira, M.J.P., Lago, J.H.G., Travassos, L.R., Jacaranone induces apoptosis in melanoma cells via ROS-mediated downregulation of Akt and p38 MAPK activation and displays antitumor activity in vivo. PLoS One, 7, 2012, e38698, 10.1371/journal.pone.0038698.
47. [47] Yang, L., Sui, W., Li, Y., Qi, X., Wang, Y., Zhou, Q., Gao, H., Substance P inhibits hyperosmotic stress-induced apoptosis in corneal epithelial cells through the mechanism of Akt activation and reactive oxygen species scavenging via the Neurokinin-1 receptor. PLoS One, 11, 2016, e0149865, 10.1371/journal.pone.0149865.
48. [48] Thakur, R., Mishra, D.P., Pharmacological modulation of beta-catenin and its applications in cancer therapy. J. Cell. Mol. Med. 17 (2013), 449–456, 10.1111/jcmm.12033.
49. [49] Altomare, D.A., Testa, J.R., Perturbations of the AKT signaling pathway in human cancer. Oncogene 24 (2005), 7455–7464, 10.1038/sj.onc.1209085.
50. [50] Crowell, J.A., Steele, V.E., Fay, J.R., Targeting the AKT protein kinase for cancer chemoprevention. Mol. Cancer Ther. 6 (2007), 2139–2148, 10.1158/1535-7163.MCT-07-0120.
51. [51] McCubrey, J.A., Steelman, L.S., Bertrand, F.E., Davis, N.M., Sokolosky, M., Abrams, S.L., Montalto, G., D'Assoro, A.B., Libra, M., Nicoletti, F., Maestro, R., Basecke, J., Rakus, D., Gizak, A., Demidenko, Z., Cocco, L., Martelli, A.M., Cervello, M., GSK-3 as potential target for therapeutic intervention in cancer. Oncotarget 5 (2014), 2881–2911.