Resveratrol epigenetically regulates the expression of zinc finger protein 36 in non‑small cell lung cancer cell lines
- Authors:
- Ahmad Fudhaili
- Nal Ae Yoon
- Seokmin Kang
- Jinhyun Ryu
- Joo Yeon Jeong
- Dong Hoon Lee
- Sang Soo Kang
-
Affiliations: Department of Anatomy and Convergence Medical Science, Institute of Health Sciences, College of Medicine, Gyeongsang National University, Jinju, Gyeongnam 52727, Republic of Korea - Published online on: November 30, 2018 https://doi.org/10.3892/or.2018.6898
- Pages: 1377-1386
This article is mentioned in:
Abstract
Sanduja S, Blanco FF, Young LE, Kaza V and Dixon DA: The role of tristetraprolin in cancer and inflammation. Front Biosci. 17:174–88. 2012. View Article : Google Scholar : | |
Sanduja S, Blanco FF and Dixon DA: The roles of TTP and BRF proteins in regulated mRNA decay. Wiley Interdiscip Rev RNA. 2:42–57. 2011. View Article : Google Scholar : PubMed/NCBI | |
Xu L, Ning H, Gu L, Wang Q, Lu W, Peng H, Cui W, Ying B, Ross CR, Wilson GM, et al: Tristetraprolin induces cell cylces arrest in breast tumor cell through targeting AP-1/c-Jun and NF-κB pathway. Oncotarget. 6:41679–41691. 2015. View Article : Google Scholar : PubMed/NCBI | |
Yoon NA, Jo HG, Lee UH, Park JH, Yoon JE, Ryu JY, Kang SS, Min YJ, Ju SA, Seo EH, et al: Tristetraprolin suppresses the EMT through the down-regulation of Twist1 and Snail1 in cancer cells. Oncotarget. 7:8931–8943. 2016. View Article : Google Scholar : PubMed/NCBI | |
Sohn BH, Park IY, Lee JJ, Yang SJ, Jang YJ, Park KC, Kim DJ, Lee DC, Sohn HA, Kim TW, et al: Functional switching of TGF-beta1 signaling in liver cancer via epigenetic modulation of a single CpG Site in TTP promoter. Gastroenterology. 138:1898–1908. 2010. View Article : Google Scholar : PubMed/NCBI | |
Sobolewski C, Sanduja S, Blanco FF, Hu L and Dixon DA: Histone deacetylase inhibitors activate tristetraprolin expression through induction of early growth response protein 1 (EGR1) in Colorectal Cancer Cells. Biomolecules. 5:2035–2055. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zheng XT, Xiao XQ and Dai JJ: Sodium butyrate down-regulates tristetraprolin-mediated cyclin B1 expression independent of the formation of processing bodies. Int J Biochem Cell Biol. 69:241–248. 2015. View Article : Google Scholar : PubMed/NCBI | |
Tran DD, Koch A, Allister A, Saran S, Ewald F, Kock M, Nashan B and Tamura T: Treatment with MAPKAP2 (MK2) inhibitor and DNA methylation inhibitor, 5-aza dC, synergistically triggers apoptosis in hepatocellular carcinoma (HCC) via tristetraprolin (TTP). Cell Signal. 28:1872–1880. 2016. View Article : Google Scholar : PubMed/NCBI | |
Laird PW: Cancer epigenetics. Hum Mol Genet. 14:R65–R76. 2005. View Article : Google Scholar : PubMed/NCBI | |
Su LJ, Mahabir S, Ellison GL, McGuinn LA and Reid BC: Epigenetic contributions to the relationship between cancer and dietary intake of nutrients, bioactive food components, and environmental toxicants. Front Genet. 2:912012. View Article : Google Scholar : PubMed/NCBI | |
Ferguson-Smith AC and Greally JM: Epigenetics: Perceptive enzymes. Nature. 449:148–149. 2007. View Article : Google Scholar : PubMed/NCBI | |
Meeran SM, Ahmed A and Tollefsbol TO: Epigenetic targets of bioactive dietary components for cancer prevention and therapy. Clin Epigenetics. 1:101–116. 2010. View Article : Google Scholar : PubMed/NCBI | |
Suzuki H, Itoh F, Toyota M, Kikuchi T, Kakiuchi H, Hinoda Y and Imai K: Distinct methylation pattern and microsatellite instability in sporadic gastric cancer. Int J Cancer. 83:309–313. 1999. View Article : Google Scholar : PubMed/NCBI | |
Herman JG, Latif F, Weng Y, Lerman MI, Zbar B, Liu S, Samid D, Duan DS, Gnarra JR, Linehan WM, et al: Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc Natl Acad Sci USA. 91:9700–9704. 1994. View Article : Google Scholar : PubMed/NCBI | |
Herman JG, Umar A, Polyak K, Graff JR, Ahuja N, Issa JP, Markowitz S, Willson JK, Hamilton SR, Kinzler KW, et al: Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc Natl Acad Sci USA. 95:6870–6875. 1998. View Article : Google Scholar : PubMed/NCBI | |
Delmas D, Lancon A, Colin D, Jannin B and Latruffe N: Resveratrol as a chemopreventive agent: A promising molecule for fighting cancer. Curr Drug Targets. 7:423–442. 2006. View Article : Google Scholar : PubMed/NCBI | |
Ryu J, Yoon NA, Seong H, Jeong JY, Kang S, Park NM, Choi JI, Lee DH, Roh GS, Kim HJ, et al: Resveratrol induces glioma cell apoptosis through activation of tristetraprolin. Mol Cells. 38:991–997. 2015. View Article : Google Scholar : PubMed/NCBI | |
Lee SR, Jin H, Kim WT, Kim WJ, Kim SZ, Leem SH and Kim SM: Tristetraprolin activation by resveratrol inhibits the proliferation and metastasis of colorectal cancer cells. Int J Oncol. 53:1269–1278. 2018.PubMed/NCBI | |
Kim WT, Jin H, Lee SR, Kim SZ, Leem SH and Kim SM: Mediation of the anticancer effect of resveratrol via the upregulation tristetraprolin in gastric cancer cell. Med Chem. 8:29–37. 2018. | |
Li C, Tang C and He G: Tristetraprolin: A novel mediator of the anticancer properties of resveratrol. Genet Mol Res. 15:2016.doi: 10.4238/gmr.15027213. | |
Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔCT method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI | |
DuBois RN, McLane MW, Ryder K, Lau LF and Nathans D: A growth factor-inducible nuclear protein with a novel cysteine/histidine repetitive sequence. J Biol Chem. 265:19185–19191. 1990.PubMed/NCBI | |
Varnum BC, Ma QF, Chi TH, Fletcher B and Herschman HR: The TIS11 primary response gene is a member of a gene family that encodes proteins with a highly conserved sequence containing an unusual Cys-His repeat. Mol Cell Biol. 11:1754–1758. 1991. View Article : Google Scholar : PubMed/NCBI | |
Cao H, Deterding LJ and Blackshear PJ: Phosphorylation site analysis of the anti-inflammatory and mRNA-destabilizing protein tristetraprolin. Expert Rev Proteomics. 4:711–726. 2007. View Article : Google Scholar : PubMed/NCBI | |
Bakheet T, Frevel M, Williams BR, Greer W and Khabar KS: Ared (Human au-rich element-containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins). Nucleic Acids Res. 29:246–254. 2001. View Article : Google Scholar : PubMed/NCBI | |
Chen CY and Shyu AB: AU-rich elements: Characterization and importance in mRNA degradation. Trends Biochem Sci. 20:465–470. 1995. View Article : Google Scholar : PubMed/NCBI | |
Hau HH, Walsh RJ, Ogilvie RL, Williams DA, Reilly CS and Bohjanen PR: Tristetraprolin recruits functional mRNA decay complexes to ARE sequences. J Cell Biochem. 100:1477–1492. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lee HH, Son YJ, Lee WH, Park YW, Chae SW, Cho WJ, Kim YM, Choi HJ, Choi DH, Jung SW, et al: Tristetraprolin regulates expression of VEGF and tumorigenesis in human colon cancer. Int J Cancer. 126:1817–1827. 2010. View Article : Google Scholar : PubMed/NCBI | |
Marderosian M, Sharma A, Funk AP, Vartanian R, Masri J, Jo OD and Gera JF: Tristetraprolin regulates Cyclin D1 and c-Myc mRNA stability in response to rapamycin in an Akt-dependent manner via p38 MAPK signaling. Oncogene. 25:6277–6290. 2006. View Article : Google Scholar : PubMed/NCBI | |
Essafi-Benkhadir K, Onesto C, Stebe E, Monori C and Pagès G: Tristetraprolin inhibits Ras-dependent tumor vascularization by inducing vascular endothelial growth factor mRNA degradation. Mol Biol Cell. 18:4648–4658. 2007. View Article : Google Scholar : PubMed/NCBI | |
Suswam E, Li Y, Zhang X, Gillespie GY, Li X, Shacka JJ, Lu L, Zheng L and King PH: Tristetraprolin downregulates interleukin 8 and vascular endothelial growth factor in malignant glioma cells. Cancer Res. 68:674–682. 2008. View Article : Google Scholar : PubMed/NCBI | |
Young LE, Sanduja S, Bemis-Standoli K, Pena EA, Price RL and Dixon DA: The mRNA binding proteins HuR and tristetraprolin regulate cyclooxygenase 2 expression during colon carcinogenesis. Gastroenterology. 136:1669–1679. 2009. View Article : Google Scholar : PubMed/NCBI | |
Anderson P: Post-transcriptional control of cytokine production. Nat Immunol. 9:353–359. 2008. View Article : Google Scholar : PubMed/NCBI | |
Carrick DM and Balckshear PJ: Comparative expression of tristetraprolin (TTP) family member transcripts in normal human tissues and cancer cell lines. Arch Biochem Biophys. 462:278–285. 2007. View Article : Google Scholar : PubMed/NCBI | |
Gaudet F, Hodgson G, Eden A, Jackson-Grusby L, Dausman J, Gray JW, Leohardt H and Jaenisch R: Induction of tumors in mice by genomic hypomethylation. Science. 300:489–492. 2003. View Article : Google Scholar : PubMed/NCBI | |
Fuso A, Nicolia V, Cavallaro RA and Scarpa S: DNA methylase and demethylase activities are modulated by one-carbon metabolism in Alzheimer's disease models. J Nutr Biochem. 22:242–251. 2011. View Article : Google Scholar : PubMed/NCBI | |
López-Pedrera C, Pérez-Sánchez C, Ramos-Casals M, Santos-Gonzalez M, Rodriguez-Ariza A and Cuadrado MJ: Cardiovascular risk in systemic autoimmune diseases. Epigenetic mechanisms of immune regulatory functions. Clin Dev Immunol. 2012:9746482012. View Article : Google Scholar : PubMed/NCBI | |
Sacconi S, Camaño P, de Greef JC, Lemmers RJ, Salviati L, Boileau P, Lopez de Munain Arregui A, van der Maarel SM and Desnuelle C: Patients with a phenotype consistent with facioscapulohumeral muscular dystrophy display genetic and epigenetic heterogeneity. J Med Genet. 49:41–46. 2012. View Article : Google Scholar : PubMed/NCBI | |
Chik F and Szyf M: Effects of specific DNMT gene depletion on cancer cell transformation and breast cancer cell invasion; Toward selective DNMT inhibitors. Carcinogenesis. 32:224–232. 2011. View Article : Google Scholar : PubMed/NCBI | |
Hardy TM and Tollefsbol TO: Epigenetic diet: Impact on the epigenome and cancer. Epigenomics. 3:503–518. 2011. View Article : Google Scholar : PubMed/NCBI | |
Khan SI, Aumsuwan P, Khan IA, Walker LA and Dasmahapatra AK: Epigenetic events associated with breast cancer and their prevention by dietary components targeting the epigenome. Chem Res Toxicol. 25:61–73. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gerhauser C: Cancer chemoprevention and nutriepigenetics: State of the art and future challenges. Top Curr Chem. 329:73–132. 2013. View Article : Google Scholar : PubMed/NCBI | |
Huang Z, Huang Q, Ji L, Wang Y, Qi X, Liu L, Liu Z and Lu L: Epigenetic regulation of active Chinese herbal components for cancer prevention and treatment. A follow-up review. Pharmacol Res. 114:1–12. 2016. View Article : Google Scholar : PubMed/NCBI | |
Kala R, Shah HN, Martin SL and Tollefsbol TO: Epigenetic-based combinatorial resveratrol and pterostilbene alters DNA damage response by affecting SIRT1 and DNMT enzyme expression, including SIRT1-dependent γ-H2AX and telomerase regulation in triple-negative breast cancer. BMC Cancer. 15:6722015. View Article : Google Scholar : PubMed/NCBI | |
Mirza S, Sharma G, Parshad R, Gupta SD, Pandya P and Ralhan R: Expression of DNA methyltransferases in breast cancer patients and to analyze the effect of natural compounds on DNA methyltransferases and associated proteins. J Breast Cancer. 16:23–31. 2013. View Article : Google Scholar : PubMed/NCBI | |
Garvina S, Ollinger K and Dabrosin C: Resveratrol induces apoptosis and inhibits angiogenesis in human breast cancer xenografts in vivo. Cancer Lett. 231:113–122. 2006. View Article : Google Scholar : PubMed/NCBI | |
Liu YZ, Wu K, Huang J, Liu Y, Wang X, Meng ZJ, Yuan SX, Wang DX, Luo JY, Zuo GW, et al: The PTEN/PI3K/Aktand Wnt/β-catenin signaling pathways are involved in the inhibitory effect of resveratrol on human colon cancer cell proliferation. Int J Oncol. 45:104–112. 2014. View Article : Google Scholar : PubMed/NCBI | |
Lee M, Choi B, Kundu JK, Shin YK, Na HK and Surh YJ: Resveratrol suppresses growth of human ovarian cancer cells in culture and in a murine xenograft model: Eukaryotic elongation factor 1A2 as a potential target. Cancer Res. 69:7449–7458. 2009. View Article : Google Scholar : PubMed/NCBI | |
Jiao Y, Li H, Liu Y, Guo A, Xu X, Qu X, Wang S, Zhao J, Li Y and Cao Y: Resveratrol inhibits the invasion of glioblastoma-initiating cells via down-regulation of the PI3K/Akt/NF-κB signaling pathway. Nutrients. 7:4383–4402. 2015. View Article : Google Scholar : PubMed/NCBI | |
Yang T, Zhang J, Zhou J, Zhu M, Wang L and Yan L: Resveratrol inhibits interleukin-6 induced invasion of human gastric cancer cells. Biomed Pharmacother. 99:766–773. 2018. View Article : Google Scholar : PubMed/NCBI | |
Oi N, Jeong CH, Nadas J, Cho YY, Pugliese A, Bode A and Dong Z: Resveratrol, a red Wine polyphenol, suppresses pancreatic cancer by inhibiting leukotriene A4 hydrolase. Cancer Res. 70:9755–9763. 2010. View Article : Google Scholar : PubMed/NCBI | |
Qin W, Zhang K, Clarke K, Weiland T and Sauter ER: Methylation and miRNA effects of resveratrol on mammary tumors vs. normal tissue. Nutr Cancer. 66:270–277. 2014. View Article : Google Scholar : PubMed/NCBI | |
Lee H, Zhang P, Herrmann A, Yang C, Xin H, Wang Z, Hoon DS, Forman SJ, Jove R, Riggs AD, et al: Acetylated STAT3 is crucial for methylation of tumor-suppressor gene promoter and inhibition by resveratrol results in demethylation. Proc Natl Acad Sci USA. 109:7765–7769. 2012. View Article : Google Scholar : PubMed/NCBI | |
Stefanska B, Salamé P, Bednarek A and Fabianowska-Majewska K: Comparative effects of retinoic acid, vitamin D and resveratrol alone and in combination with adenosine analogues on methylation and expression of phosphatase and tensin homologue tumour suppressor gene in breast cancer cells. Br J Nutr. 107:781–790. 2012. View Article : Google Scholar : PubMed/NCBI | |
Papoutsis AJ, Borg JL, Selmin OI and Romagnolo DF: BRCA-1 promoter hypermethylation and silencing induced by the aromatic hydrocarbon receptor-ligand TCDD are prevented by resveratrol in MCF-7 cells. J Nurt Biochem. 23:1324–1332. 2012. View Article : Google Scholar | |
Ohshiro K, Rayala SK, Kondo S, Gaur A, Vadlamudi RK, El-Naggar AK and Kumar R: Identifying the estrogen receptor coactivator PELP1 in autophagosomes. Cancer Res. 67:8164–8171. 2007. View Article : Google Scholar : PubMed/NCBI | |
Whyte L, Huang YY, Torres K and Mehta RG: Molecular mechanisms of resveratrol action in lung cancer cells using dual protein and microarray analyses. Cancer Res. 67:12007–12017. 2007. View Article : Google Scholar : PubMed/NCBI | |
Ebi H, Tomida S, Takeuchi T, Arima C, Sato T, Mitsudomi T, Yatabe Y, Osada H and Takahashi T: Relationship of deregulated signaling converging onto mTOR with prognosis and classification of lung adenocarcinoma shown by two independent in silico analyses. Cancer Res. 69:4027–4035. 2009. View Article : Google Scholar : PubMed/NCBI | |
Wu JY, Tsai KW, Shee JJ, Li YZ, Chen CH, Chuang JJ and Liu YW: 4-Chloro-3,5-dihydroxystilbene, a resveratrol derivative, induces lung cancer cell death. Acta Pharmacol Sin. 31:81–92. 2010. View Article : Google Scholar : PubMed/NCBI | |
Dinkova-Kostova AT, Holtzclaw WD and Wakabayashi N: Keap1, the sensor for electrophiles and oxidants that regulates the phase 2 response, is a zinc metalloprotein. Biochemistry. 44:6889–6899. 2005. View Article : Google Scholar : PubMed/NCBI | |
Kim JH, Park EY, Ha HK, Jo CM, Lee WJ, Lee SS and Kim JW: Resveratrol-loaded nanoparticles induce antioxidant activity against oxidative stress. Asian Australas J Anim Sci. 29:288–298. 2016. View Article : Google Scholar : PubMed/NCBI |