Tristetraprolin activation by resveratrol inhibits the proliferation and metastasis of colorectal cancer cells

  • Authors:
    • Se-Ra Lee
    • Hua Jin
    • Won-Tae Kim
    • Won-Jung Kim
    • Sung Zoo Kim
    • Sun-Hee Leem
    • Soo Mi Kim
  • View Affiliations

  • Published online on: June 25, 2018     https://doi.org/10.3892/ijo.2018.4453
  • Pages: 1269-1278
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )


Abstract

Resveratrol (RSV) is a polyphenolic compound that naturally occurs in grapes, peanuts and berries. Considerable research has been conducted to determine the benefits of RSV against various human cancer types. Tristetraprolin (TTP) is an AU-rich element-binding protein that regulates mRNA stability and has decreased expression in human cancer. The present study investigated the biological effect of RSV on TTP gene regulation in colon cancer cells. RSV inhibited the proliferation and invasion/metastasis of HCT116 and SNU81 colon cancer cells. Furthermore, RSV induced a dose-dependent increase in TTP expression in HCT116 and SNU81 cells. The microarray experiment revealed that RSV significantly increased TTP expression by downregulating E2F transcription factor 1 (E2F1), a downstream target gene of TTP and regulated genes associated with inflammation, cell proliferation, cell death, angiogenesis and metastasis. Although TTP silencing inhibited TTP mRNA expression, the expression was subsequently restored by RSV. Small interfering RNA-induced TTP inhibition attenuated the effects of RSV on cell growth. In addition, RSV induced the mRNA-decaying activity of TTP and inhibited the relative luciferase activity of baculoviral IAP repeat containing 3 (cIAP2), large tumor suppressor kinase 2 (LATS2), E2F1, and lin‑28 homolog A (Lin28) in HCT116 and SNU81 cells. Therefore, RSV enhanced the inhibitory activity of TTP in HCT116 and SNU81 cells by negatively regulating cIAP2, E2F1, LATS2, and Lin28 expression. In conclusion, RSV suppressed the proliferation and invasion/metastasis of colon cancer cells by activating TTP.

References

1 

Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A and Bray F: Global patterns and trends in colorectal cancer incidence and mortality. Gut. 66:683–691. 2017. View Article : Google Scholar

2 

Pan R, Zhu M, Yu C, Lv J, Guo Y, Bian Z, Yang L, Chen Y, Hu Z, Chen Z, et al China Kadoorie Biobank Collaborative Group: Cancer incidence and mortality: A cohort study in China, 2008-2013. Int J Cancer. 141:1315–1323. 2017. View Article : Google Scholar : PubMed/NCBI

3 

Chen W, Zheng R, Zhang S, Zeng H, Xia C, Zuo T, Yang Z, Zou X and He J: Cancer incidence and mortality in China, 2013. Cancer Lett. 401:63–71. 2017. View Article : Google Scholar : PubMed/NCBI

4 

Shin A, Jung KW and Won YJ: Colorectal cancer mortality in Hong Kong of China, Japan, South Korea, and Singapore. World J Gastroenterol. 19:979–983. 2013. View Article : Google Scholar : PubMed/NCBI

5 

Fitzgerald TL, Biswas T, O'Brien K, Zervos EE and Wong JH: Neoadjuvant radiotherapy for rectal cancer: Adherence to evidence-based guidelines in clinical practice. World J Surg. 37:639–645. 2013. View Article : Google Scholar

6 

Murray DM, Katz ML, Post DM, Pennell ML, Young GS, Tatum CM and Paskett ED: Enhancing cancer screening in primary care: Rationale, design, analysis plan, and recruitment results. Contemp Clin Trials. 34:356–363. 2013. View Article : Google Scholar : PubMed/NCBI

7 

Halabi WJ, Kang CY, Jafari MD, Nguyen VQ, Carmichael JC, Mills S, Stamos MJ and Pigazzi A: Robotic-assisted colorectal surgery in the United States: A nationwide analysis of trends and outcomes. World J Surg. 37:2782–2790. 2013. View Article : Google Scholar : PubMed/NCBI

8 

Lu YW and Wang KH: Research progress on genetic heterogeneity between primary and paired metastatic colorectal cancer. Yi Chuan. 39:482–490. 2017.PubMed/NCBI

9 

Kopetz S, Chang GJ, Overman MJ, Eng C, Sargent DJ, Larson DW, Grothey A, Vauthey JN, Nagorney DM and McWilliams RR: Improved survival in metastatic colorectal cancer is associated with adoption of hepatic resection and improved chemotherapy. J Clin Oncol. 27:3677–3683. 2009. View Article : Google Scholar : PubMed/NCBI

10 

Loree JM and Kopetz S: Recent developments in the treatment of metastatic colorectal cancer. Ther Adv Med Oncol. 9:551–564. 2017. View Article : Google Scholar : PubMed/NCBI

11 

Midgley RS, Yanagisawa Y and Kerr DJ: Evolution of nonsurgical therapy for colorectal cancer. Nat Clin Pract Gastroenterol Hepatol. 6:108–120. 2009. View Article : Google Scholar : PubMed/NCBI

12 

McCubrey JA, Lertpiriyapong K, Steelman LS, Abrams SL, Yang LV, Murata RM, Rosalen PL, Scalisi A, Neri LM, Cocco L, et al: Effects of resveratrol, curcumin, berberine and other nutra-ceuticals on aging, cancer development, cancer stem cells and microRNAs. Aging (Albany NY). 9:1477–1536. 2017.

13 

de Lima E Silva TC, da Silveira LTR, Fragoso MF, da Silva FRM, Martinez MF, Zapaterini JR, Diniz OHG, Scarano WR and Barbisan LF: Maternal resveratrol treatment reduces the risk of mammary carcinogenesis in female offspring prenatally exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Horm Cancer. 8:286–297. 2017. View Article : Google Scholar : PubMed/NCBI

14 

Perez-Vizcaino F and Fraga CG: Research trends in flavonoids and health. Arch Biochem Biophys. 646:107–112. 2018. View Article : Google Scholar : PubMed/NCBI

15 

Darwish MA, Abo-Youssef AM, Khalaf MM, Abo-Saif AA, Saleh IG and Abdelghany TM: Resveratrol influences platinum pharmacokinetics: A novel mechanism in protection against cisplatin-induced nephrotoxicity. Toxicol Lett. 290:73–82. 2018. View Article : Google Scholar : PubMed/NCBI

16 

Kiskova T, Demeckova V, Jendzelovska Z, Kiktava M, Venglovska K, Bohmdorfer M, Jager W and Thalhammer T: Nocturnal resveratrol administration inhibits chemically induced breast cancer formation in rats. J Physiol Pharmacol. 68:867–875. 2017.

17 

Guthrie AR, Chow HS and Martinez JA: Effects of resveratrol on drug- and carcinogen-metabolizing enzymes, implications for cancer prevention. Pharmacol Res Perspect. 5:e002942017. View Article : Google Scholar : PubMed/NCBI

18 

Bartolacci C, Andreani C, Amici A and Marchini C: Walking a tightrope: A perspective of resveratrol effects on breast cancer. Curr Protein Pept Sci. 19:311–322. 2018. View Article : Google Scholar

19 

Rauf A, Imran M, Butt MS, Nadeem M, Peters DG and Mubarak MS: Resveratrol as an anti-cancer agent: A review. Crit Rev Food Sci Nutr. 58:1428–1447. 2018. View Article : Google Scholar

20 

Feng Y, Zhou J and Jiang Y: Resveratrol in lung cancer- a systematic review. J BUON. 21:950–953. 2016.PubMed/NCBI

21 

Yin TF, Wang M, Qing Y, Lin YM and Wu D: Research progress on chemopreventive effects of phytochemicals on colorectal cancer and their mechanisms. World J Gastroenterol. 22:7058–7068. 2016. View Article : Google Scholar : PubMed/NCBI

22 

Li C, Xu X, Tao Z, Sun C and Pan Y: Resveratrol derivatives: An updated patent review (2012–2015). Expert Opin Ther Pat. 1–12. 2016.

23 

Li YH, Niu YB, Sun Y, Zhang F, Liu CX, Fan L and Mei QB: Role of phytochemicals in colorectal cancer prevention. World J Gastroenterol. 21:9262–9272. 2015. View Article : Google Scholar : PubMed/NCBI

24 

Fajardo AM and Piazza GA: Chemoprevention in gastrointestinal physiology and disease. Anti-inflammatory approaches for colorectal cancer chemoprevention. Am J Physiol Gastrointest Liver Physiol. 309:G59–G70. 2015. View Article : Google Scholar : PubMed/NCBI

25 

Carter LG, D'Orazio JA and Pearson KJ: Resveratrol and cancer: Focus on in vivo evidence. Endocr Relat Cancer. 21:R209–R225. 2014. View Article : Google Scholar : PubMed/NCBI

26 

Juan ME, Alfaras I and Planas JM: Colorectal cancer chemoprevention by trans-resveratrol. Pharmacol Res. 65:584–591. 2012. View Article : Google Scholar : PubMed/NCBI

27 

Gong WH, Zhao N, Zhang ZM, Zhang YX, Yan L and Li JB: The inhibitory effect of resveratrol on COX-2 expression in human colorectal cancer: A promising therapeutic strategy. Eur Rev Med Pharmacol Sci. 21:1136–1143. 2017.PubMed/NCBI

28 

Karimi Dermani F, Saidijam M, Amini R, Mahdavinezhad A, Heydari K and Najafi R: Resveratrol inhibits proliferation, invasion, and epithelial-mesenchymal transition by increasing miR-200c expression in HCT-116 colorectal cancer cells. J Cell Biochem. 118:1547–1555. 2017. View Article : Google Scholar

29 

Buhrmann C, Shayan P, Popper B, Goel A and Shakibaei M: Sirt1 is required for resveratrol-mediated chemopreventive effects in colorectal cancer cells. Nutrients. 8:1452016. View Article : Google Scholar : PubMed/NCBI

30 

Baou M, Jewell A and Murphy JJ: TIS11 family proteins and their roles in posttranscriptional gene regulation. J Biomed Biotechnol. 2009:6345202009. View Article : Google Scholar : PubMed/NCBI

31 

Li C, Tang C and He G: Tristetraprolin: A novel mediator of the anticancer properties of resveratrol. Genet Mol Res. 15:152016.

32 

Deng K, Wang H, Shan T, Chen Y, Zhou H, Zhao Q and Xia J: Tristetraprolin inhibits gastric cancer progression through suppression of IL-33. Sci Rep. 6:245052016. View Article : Google Scholar : PubMed/NCBI

33 

Pandiri I, Chen Y, Joe Y, Kim HJ, Park J, Chung HT and Park JW: Tristetraprolin mediates the anti-proliferative effects of metformin in breast cancer cells. Breast Cancer Res Treat. 156:57–64. 2016. View Article : Google Scholar : PubMed/NCBI

34 

Wei ZR, Liang C, Feng D, Cheng YJ, Wang WM, Yang DJ, Wang YX and Cai QP: Low tristetraprolin expression promotes cell proliferation and predicts poor patients outcome in pancreatic cancer. Oncotarget. 7:17737–17750. 2016.PubMed/NCBI

35 

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 cycle arrest in breast tumor cells through targeting AP-1/c-Jun and NF-κB pathway. Oncotarget. 6:41679–41691. 2015. View Article : Google Scholar : PubMed/NCBI

36 

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

37 

Kang S, Min A, Im SA, Song SH, Kim SG, Kim HA, Kim HJ, Oh DY, Jong HS, Kim TY, et al: TGF-β suppresses COX-2 expression by tristetraprolin-mediated RNA destabilization in A549 human lung cancer cells. Cancer Res Treat. 47:101–109. 2015. View Article : Google Scholar

38 

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

39 

Ryu J, Yoon NA, Seong H, Jeong JY, Kang S, Park N, Choi J, 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

40 

Lee JY, Kim HJ, Yoon NA, Lee WH, Min YJ, Ko BK, Lee BJ, Lee A, Cha HJ, Cho WJ, et al: Tumor suppressor p53 plays a key role in induction of both tristetraprolin and let-7 in human cancer cells. Nucleic Acids Res. 41:5614–5625. 2013. View Article : Google Scholar : PubMed/NCBI

41 

Kim CW, Kim HK, Vo MT, Lee HH, Kim HJ, Min YJ, Cho WJ and Park JW: Tristetraprolin controls the stability of cIAP2 mRNA through binding to the 3′UTR of cIAP2 mRNA. Biochem Biophys Res Commun. 400:46–52. 2010. View Article : Google Scholar : PubMed/NCBI

42 

Lee HH, Lee SR and Leem SH: Tristetraprolin regulates prostate cancer cell growth through suppression of E2F1. J Microbiol Biotechnol. 24:287–294. 2014. View Article : Google Scholar

43 

Lee HH, Vo MT, Kim HJ, Lee UH, Kim CW, Kim HK, Ko MS, Lee WH, Cha SJ, Min YJ, et al: Stability of the LATS2 tumor suppressor gene is regulated by tristetraprolin. J Biol Chem. 285:17329–17337. 2010. View Article : Google Scholar : PubMed/NCBI

44 

Kim CW, Vo MT, Kim HK, Lee HH, Yoon NA, Lee BJ, Min YJ, Joo WD, Cha HJ, Park JW, et al: Ectopic over-expression of tristet-raprolin in human cancer cells promotes biogenesis of let-7 by down-regulation of Lin28. Nucleic Acids Res. 40:3856–3869. 2012. View Article : Google Scholar : PubMed/NCBI

45 

Li W, Matsuoka M, Kai M, Thapa P, Khadge S, Hagge DA, Brennan PJ and Vissa V: Real-time PCR and high-resolution melt analysis for rapid detection of Mycobacterium leprae drug resistance mutations and strain types. J Clin Microbiol. 50:742–753. 2012. View Article : Google Scholar :

46 

Ashrafi R, Bruneaux M, Sundberg LR, Pulkkinen K and Ketola T: Application of high resolution melting assay (HRM) to study temperature-dependent intraspecific competition in a pathogenic bacterium. Sci Rep. 7:9802017. View Article : Google Scholar : PubMed/NCBI

47 

Du Z, Zhou F, Jia Z, Zheng B, Han S, Cheng J, Zhu G and Huang P: The hedgehog/Gli-1 signaling pathways is involved in the inhibitory effect of resveratrol on human colorectal cancer HCT116 cells. Iran J Basic Med Sci. 19:1171–1176. 2016.PubMed/NCBI

48 

Feng M, Zhong LX, Zhan ZY, Huang ZH and Xiong JP: Resveratrol treatment inhibits proliferation of and induces apoptosis in human colon cancer cells. Med Sci Monit. 22:1101–1108. 2016. View Article : Google Scholar : PubMed/NCBI

49 

Ali I and Braun DP: Resveratrol enhances mitomycin C-mediated suppression of human colorectal cancer cell proliferation by up- regulation of p21WAF1/CIP1. Anticancer Res. 34:5439–5446. 2014.PubMed/NCBI

50 

Liu B, Zhou Z, Zhou W, Liu J, Zhang Q, Xia J, Liu J, Chen N, Li M and Zhu R: Resveratrol inhibits proliferation in human colorectal carcinoma cells by inducing G1/S-phase cell cycle arrest and apoptosis through caspase/cyclin-CDK pathways. Mol Med Rep. 10:1697–1702. 2014. View Article : Google Scholar : PubMed/NCBI

51 

Guo J, Qu H, Chen Y and Xia J: The role of RNA-binding protein tristetraprolin in cancer and immunity. Med Oncol. 34:1962017. View Article : Google Scholar : PubMed/NCBI

52 

Guo J, Wang H, Jiang S, Xia J and Jin S: The Cross-talk between tristetraprolin and cytokines in cancer. Anticancer Agents Med Chem. 17:1477–1486. 2017. View Article : Google Scholar : PubMed/NCBI

53 

Wang Q, Ning H, Peng H, Wei L, Hou R, Hoft DF and Liu J: Tristetraprolin inhibits macrophage IL-27-induced activation of antitumour cytotoxic T cell responses. Nat Commun. 8:8672017. View Article : Google Scholar : PubMed/NCBI

54 

Vo MT, Choi SH, Lee JH, Hong CH, Kim JS, Lee UH, Chung HM, Lee BJ, Park JW and Cho WJ: Tristetraprolin inhibits mitochondrial function through suppression of α-Synuclein expression in cancer cells. Oncotarget. 8:41903–41920. 2017. View Article : Google Scholar : PubMed/NCBI

55 

Zeng B, Zhu D, Su Z, Li Z and Yu Z: Tristetraprolin exerts tumor suppressive functions on the tumorigenesis of glioma by targeting IL-13. Int Immunopharmacol. 39:63–70. 2016. View Article : Google Scholar : PubMed/NCBI

56 

Lee HH, Yang SS, Vo MT, Cho WJ, Lee BJ, Leem SH, Lee SH, Cha HJ and Park JW: Tristetraprolin down-regulates IL-23 expression in colon cancer cells. Mol Cells. 36:571–576. 2013. View Article : Google Scholar : PubMed/NCBI

57 

Cha HJ, Lee HH, Chae SW, Cho WJ, Kim YM, Choi HJ, Choi DH, Jung SW, Min YJ, Lee BJ, et al: Tristetraprolin downregulates the expression of both VEGF and COX-2 in human colon cancer. Hepatogastroenterology. 58:790–795. 2011.PubMed/NCBI

Related Articles

Journal Cover

September 2018
Volume 53 Issue 3

Print ISSN: 1019-6439
Online ISSN:1791-2423

Sign up for eToc alerts

Recommend to Library

Copy and paste a formatted citation
APA
Lee, S., Jin, H., Kim, W., Kim, W., Kim, S., Leem, S., & Kim, S. (2018). Tristetraprolin activation by resveratrol inhibits the proliferation and metastasis of colorectal cancer cells. International Journal of Oncology, 53, 1269-1278. https://doi.org/10.3892/ijo.2018.4453
MLA
Lee, S., Jin, H., Kim, W., Kim, W., Kim, S., Leem, S., Kim, S."Tristetraprolin activation by resveratrol inhibits the proliferation and metastasis of colorectal cancer cells". International Journal of Oncology 53.3 (2018): 1269-1278.
Chicago
Lee, S., Jin, H., Kim, W., Kim, W., Kim, S., Leem, S., Kim, S."Tristetraprolin activation by resveratrol inhibits the proliferation and metastasis of colorectal cancer cells". International Journal of Oncology 53, no. 3 (2018): 1269-1278. https://doi.org/10.3892/ijo.2018.4453