Upregulation of p53 by tannic acid treatment suppresses the proliferation of human colorectal carcinoma

1. N. A. Alqallaf, H. A. G. Saleh, A. M. Abdu, S. H. Almuntaser, S. A. Bin Rakhis, A. A. Almughamis, A. A. Ghanim, A. S. Alkhathami, N. A. Aldossari and G. M. Ahmad, Colon cancer screening and prevention, Indo. Am. J. Pharm. Sci.5 (2018) 13071–13078; https://doi.org/10.5281/zenodo.1495157Search in Google Scholar

2. R. L. Siegel, K. D. Miller, S. A. Fedewa, D. J. Ahnen, R. G. S. Meester, A. Barzi and A. Jemal, Colorectal cancer statistics, CA: Cancer J. Clin.67 (2017) 177–193; https://doi.org/10.3322/caac.2139510.3322/caac.2139528248415Search in Google Scholar

3. H. S. Wong and W. C. Chang, Correlation of clinical features and genetic profiles of stromal interaction molecule 1 (STIM1) in colorectal cancers, Oncotarget6 (2015) 42169–42182; https://doi.org/10.18632/oncotarget.588810.18632/oncotarget.5888474721726543234Search in Google Scholar

4. B. K. Edwards, E. Ward, B. A. Kohler, C. Eheman, A. G. Zauber, R. N. Anderson, A. Jemal, M. J. Schymura, I. Lansdorp-Vogelaar, L. C. Seeff, M. van Ballegooijen, S. L. Goede and L. A. G. Ries, Annual report to the nation on the status of cancer, 1975-2006, Featuring colorectal cancer trends and impact of interventions (Risk factors, screening, and treatment) to reduce future rates, Cancer116 (2010) 544–573; https://doi.org/10.1002/cncr.2476010.1002/cncr.24760361972619998273Search in Google Scholar

5. M. Wang, Y. R. Li and X. D. Hu, Chebulinic acid derived from triphala is a promising antitumour agent in human colorectal carcinoma cell lines, BMC Complement. Altern. Med.18 (2018) 342; https://doi.org/10.1186/s12906-018-2412-510.1186/s12906-018-2412-5630717430587184Search in Google Scholar

6. H. M. Li, S. Krstin and M. Wink, Modulation of multidrug resistant in cancer cells by EGCG, tannic acid and curcumin, Phytomedicine50 (2018) 213–222; https://doi.org/10.1016/j.phymed.2018.09.16910.1016/j.phymed.2018.09.16930466981Search in Google Scholar

7. Y. M. Zheng, J. Z. Shen, Y. Wang, A. X. Lu and W. S. Ho, Anti-oxidant and anti-cancer activities of Angelica dahurica extract via induction of apoptosis in colon cancer cells, Phytomedicine23 (2016) 1267–1274; https://doi.org/10.1016/j.phymed.2015.11.00810.1016/j.phymed.2015.11.00826776960Search in Google Scholar

8. S. Dasari and P. B. Tchounwou, Cisplatin in cancer therapy: molecular mechanisms of action, Eur. J. Pharmacol.740 (2014) 364–378; https://doi.org/10.1016/j.ejphar.2014.07.02510.1016/j.ejphar.2014.07.025414668425058905Search in Google Scholar

9. P. Apostolou, M. Toloudi, M. Chatziioannou, E. Ioannou, D. R. Knocke, J. Nester, D. Komiotis and I. Papasotiriou, Anvirzel in combination with cisplatin in breast, colon, lung, prostate, melanoma and pancreatic cancer cell lines, BMC Pharmacol. Toxicol.14 (2013) 18; https://doi.org/10.1186/2050-6511-14-1810.1186/2050-6511-14-18363717223521834Search in Google Scholar

10. G. Maisetta, G. Batoni, P. Caboni, S. Esin, A. C. Rinaldi and P. Zucca, Tannin profile, antioxidant properties, and antimicrobial activity of extracts from two Mediterranean species of parasitic plant Cytinus, BMC Complement. Altern. Med.19 (2019) 82; https://doi.org/10.1186/s12906-019-2487-710.1186/s12906-019-2487-7645122530952208Search in Google Scholar

11. J. Dai and R. J. Mumper, Plant phenolics: extraction, analysis and their antioxidant and anticancer properties, Molecules15 (2010) 7313–7352; https://doi.org/10.3390/molecules1510731310.3390/molecules15107313625914620966876Search in Google Scholar

12. M. P. Borisova, A. A. Kataev and V. S. Sivozhelezov, Action of tannin on cellular membranes: Novel insights from concerted studies on lipid bilayers and native cells, BBA – Biomembrane1861 (2019) 1103–1111; https://doi.org/10.1016/j.bbamem.2019.03.01710.1016/j.bbamem.2019.03.017Search in Google Scholar

13. S. Karakurt and O. Adali, Effect of tannic acid on glutathione S-transferase and NAD(P)H: Quinone oxidoreductase 1 enzymes in rabbit liver and kidney, Fresen. Environ. Bull.20 (2011) 1804–1811.Search in Google Scholar

14. S. Quideau, D. Deffieux, C. Douat-Casassus and L. Pouysegu, Plant polyphenols: Chemical properties, biological activities, and synthesis, Angew. Chem. Int. Edit.50 (2011) 586–621; https://doi.org/10.1002/anie.20100004410.1002/anie.201000044Search in Google Scholar

15. J. Das, R. Ramani and M. O. Suraju, Polyphenol compounds and PKC signaling, Biochim. Biophys. Acta1860 (2016) 2107–2121; https://doi.org/10.1016/j.bbagen.2016.06.02210.1016/j.bbagen.2016.06.022Search in Google Scholar

16. N. Sahiner, S. Sagbas, N. Aktas and C. Silan, Inherently antioxidant and antimicrobial tannic acid release from poly(tannic acid) nanoparticles with controllable degradability, Colloid Surface B142 (2016) 334–343; https://doi.org/10.1016/j.colsurfb.2016.03.00610.1016/j.colsurfb.2016.03.006Search in Google Scholar

17. J. Zhang, D. Chen, D. M. Han, Y. H. Cheng, C. Dai, X. J. Wu, F. Y. Che and X. Y. Heng, Tannic acid mediated induction of apoptosis in human glioma Hs 683 cells, Oncol. Lett.15 (2018) 6845–6850; https://doi.org/10.3892/ol.2018.819710.3892/ol.2018.8197Search in Google Scholar

18. Y. Ren, X. Li, B. Han, N. Zhao, M. Mu, C. Wang, Y. Du, Y. Wang, A. Tong, Y. Liu, L. Zhou, C. You and G. Guo, Improved anti-colorectal carcinomatosis effect of tannic acid co-loaded with oxaliplatin in nanoparticles encapsulated in thermosensitive hydrogel, Eur. J. Pharm. Sci.128 (2019) 279–289; https://doi.org/10.1016/j.ejps.2018.12.00710.1016/j.ejps.2018.12.007Search in Google Scholar

19. X. Zhang, H. Zhang, N. Zhou, J. Xu, M. Si, Z. Jia, X. Du and H. Zhang, Tannic acid modulates excitability of sensory neurons and nociceptive behavior and the Ionic mechanism, Eur. J. Pharmacol.764 (2015) 633–642; https://doi.org/10.1016/j.ejphar.2015.06.04810.1016/j.ejphar.2015.06.048Search in Google Scholar

20 G. Goel, A. K. Puniya and K. Singh, Tannic acid resistance in ruminal streptococcal isolates, J. Basic Microbiol.45 (2005) 243–245; https://doi.org/10.1002/jobm.20041051710.1002/jobm.200410517Search in Google Scholar

21. G. K. Lopes, H. M. Schulman and M. Hermes-Lima, Polyphenol tannic acid inhibits hydroxyl radical formation from Fenton reaction by complexing ferrous ions, Biochim. Biophys. Acta1472 (1999) 142–152; https://doi.org/10.1016/s0304-4165(99)00117-810.1016/S0304-4165(99)00117-8Search in Google Scholar

22. L. Ernster, L. Danielson and M. Ljunggren, Dt diaphorase I. Purification from the soluble fraction of rat-liver cytoplasm, and properties, Biochim. Biophys. Acta58 (1962) 171–188; https://doi.org/10.1016/0006-3002(62)90997-610.1016/0006-3002(62)90997-6Search in Google Scholar

23. Z. Anusevicius, J. Sarlauskas and N. Cenas, Two-electron reduction of quinones by rat liver NAD(P) H:quinone oxidoreductase: quantitative structure-activity relationships, Arch. Biochem. Biophys.404 (2002) 254–262; https://doi.org/10.1016/S0003-9861(02)00273-410.1016/S0003-9861(02)00273-4Search in Google Scholar

24. N. Hamajima, K. Matsuo, H. Iwata, M. Shinoda, Y. Yamamura, T. Kato, S. Hatooka, T. Mitsudomi, M. Suyama, Y. Kagami, M. Ogura, M. Ando, Y. Sugimura and K. Tajima, NAD(P)H: quinone oxidoreductase 1 (NQO1) C609T polymorphism and the risk of eight cancers for Japanese, Int. J. Clin. Oncol.7 (2002) 103–108; https://doi.org/10.1007/s10147020001310.1007/s10147020001312018106Search in Google Scholar

25. H. J. Menzel, J. Sarmanova, P. Soucek, R. Berberich, K. Grunewald, M. Haun and H. G. Kraft, Association of NQO1 polymorphism with spontaneous breast cancer in two independent populations, Br. J. Cancer90 (2004) 1989–1994; https://doi.org/10.1038/sj.bjc.660177910.1038/sj.bjc.6601779241028215138483Search in Google Scholar

26. A. T. Dinkova-Kostova and P. Talalay, NAD(P)H:quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector, Arch. Biochem. Biophys.501 (2010) 116–123; https://doi.org/10.1016/j.abb.2010.03.01910.1016/j.abb.2010.03.019293003820361926Search in Google Scholar

27. G. Asher, P. Tsvetkov, C. Kahana and Y. Shaul, A mechanism of ubiquitin-independent proteasomal degradation of the tumor suppressors p53 and p73, Genes Dev.19 (2005) 316–321; https://doi.org/10.1101/gad.31990510.1101/gad.31990554650915687255Search in Google Scholar

28. G. Asher, Z. Bercovich, P. Tsvetkov, Y. Shaul and C. Kahana, 20S proteasomal degradation of ornithine decarboxylase is regulated by NQO1, Mol. Cell.17 (2005) 645–655; https://doi.org/10.1016/j.molcel.2005.01.02010.1016/j.molcel.2005.01.02015749015Search in Google Scholar

29. K. Mikami, M. Naito, T. Ishiguro, H. Yano, A. Tomida, T. Yamada, N. Tanaka, T. Shirakusa and T. Tsuruo, Immunological quantitation of DT-diaphorase in carcinoma cell lines and clinical colon cancers: advanced tumors express greater levels of DT-diaphorase, Jpn. J. Cancer Res.89 (1998) 910–915; https://doi.org/10.1111/j.1349-7006.1998.tb00648.x10.1111/j.1349-7006.1998.tb00648.x59219499818026Search in Google Scholar

30. O. J. Achadu and N. Revaprasadu, Tannic acid-derivatized graphitic carbon nitride quantum dots as an “on-off-on” fluorescent nanoprobe for ascorbic acid via copper(II) mediation, Mikrochim. Acta186 (2019) 87; https://doi.org/10.1007/s00604-018-3203-x10.1007/s00604-018-3203-x30631929Search in Google Scholar

31. S. Karakurt and O. Adali, Tannic acid inhibits proliferation, migration, invasion of prostate cancer and modulates drug metabolizing and antioxidant enzymes, Anticancer Agents Med. Chem. 16 (2016) 781–789; https://doi.org/10.2174/187152061666615111111580910.2174/187152061666615111111580926555610Search in Google Scholar

32. S. Karakurt, G. Abuşoğlu and Z. C. Arituluk, Comparison of anticarcinogenic properties of Viburnum opulus and its active compound p-coumaric acid on human colorectal carcinoma, Turk. J. Biol. 44 (2020) 252–263; https://doi.org/10.3906/biy-2002-3010.3906/biy-2002-30758515733110363Search in Google Scholar

33. R. E. Brown, K. L. Jarvis and K. J. Hyland, Protein measurement using bicinchoninic acid – elimination of interfering substances, Anal. Biochem. 180 (1989) 136–139; https://doi.org/10.1016/0003-2697(89)90101-210.1016/0003-2697(89)90101-2Search in Google Scholar

34. P. K. Smith, R. I. Krohn, G. T. Hermanson, A. K. Mallia, F. H. Gartner, M. D. Provenzano, E. K. Fuji-moto, N. M. Goeke, B. J. Olson and D. C. Klenk, Measurement of protein using bicinchoninic acid, Anal. Biochem. 150 (1985) 76–85; https://doi.org/10.1016/0003-2697(85)90442-710.1016/0003-2697(85)90442-7Search in Google Scholar

35. K. J. Livak and T. D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method, Methods25 (2001) 402–408; https://doi.org/10.1006/meth.2001.126210.1006/meth.2001.126211846609Search in Google Scholar

36. H. P. S. Makkar and K. Becker, Effect of pH, temperature, and time on inactivation of tannins and possible implications in detannification studies, J. Agr. Food Chem. 44 (1996) 1291–1295; https://doi.org/10.1021/jf950628710.1021/jf9506287Search in Google Scholar

37. L. C. Katwa, M. Ramakrishna and M. R. R. Rao, Spectrophotometric assay of immobilized tannase, J. Biosci. 3 (1981) 135–142; https://doi.org/10.1007/BF0270265610.1007/BF02702656Search in Google Scholar

38. S. R. Vedula, A. Ravasio, C. T. Lim and B. Ladoux, Collective cell migration: a mechanistic perspective, Physiology (Bethesda)28 (2013) 370–379; https://doi.org/10.1152/physiol.00033.201310.1152/physiol.00033.201324186932Search in Google Scholar

39. O. Ilina and P. Friedl, Mechanisms of collective cell migration at a glance, J. Cell Sci. 122 (2009) 3203–3208; https://doi.org/10.1242/jcs.03652510.1242/jcs.03652519726629Search in Google Scholar

40. P. Vitorino and T. Meyer, Modular control of endothelial sheet migration, Genes Dev. 22 (2008) 3268–3281; https://doi.org/10.1101/gad.172580810.1101/gad.1725808260076719056882Search in Google Scholar

41. D. A. Chapnick and X. Liu, Leader cell positioning drives wound-directed collective migration in TGFbeta-stimulated epithelial sheets, Mol. Biol. Cell25 (2014) 1586–1593; https://doi.org/10.1091/mbc.E14-01-069710.1091/mbc.e14-01-0697Search in Google Scholar

42. X. Liu and X. Wu, Utilizing matrigel transwell invasion assay to detect and enumerate circulating tumor cells, Methods Mol. Biol. 1634 (2017) 277–282; https://doi.org/10.1007/978-1-4939-7144-2_2310.1007/978-1-4939-7144-2_2328819859Search in Google Scholar

43. K. Soejima, N. Mimura, M. Hirashima, H. Maeda, T. Hamamoto, T. Nakagaki and C. Nozaki, A novel human metalloprotease synthesized in the liver and secreted into the blood: possibly, the von Willebrand factor-cleaving protease?, J. Biochem. 130 (2001) 475–480; https://doi.org/10.1093/oxford-journals.jbchem.a003009Search in Google Scholar

44. S. Horibata, T. V. Vo, V. Subramanian, P. R. Thompson and S. A. Coonrod, Utilization of the soft agar colony formation assay to identify inhibitors of tumorigenicity in breast cancer cells, J. Vis. Exp. 99 (2015) e52727; https://doi.org/10.3791/5272710.3791/52727Search in Google Scholar

45. S. Borowicz, M. Van Scoyk, S. Avasarala, M. K. Karuppusamy Rathinam, J. Tauler, R. K. Bikkavilli and R. A. Winn, The soft agar colony formation assay, J. Vis. Exp. 92 (2014) e51998; https://doi.org/10.3791/5199810.3791/51998Search in Google Scholar

46. S. Elmore, Apoptosis: a review of programmed cell death, Toxicol Pathol. 35 (2007) 495–516; https://doi.org/10.1080/0192623070132033710.1080/01926230701320337Search in Google Scholar

47. M. M. Metzstein, G. M. Stanfield and H. R. Horvitz, Genetics of programmed cell death in C. elegans: past, present and future, Trends Genet. 14 (1998) 410–416; https://doi.org/10.1016/s0168-9525(98)01573-x10.1016/S0168-9525(98)01573-XSearch in Google Scholar

48. T. Miyashita, S. Krajewski, M. Krajewska, H. G. Wang, H. K. Lin, D. A. Liebermann, B. Hoffman and J. C. Reed, Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo, Oncogene9 (1994) 1799–1805; https://doi.org/10.1016/0092-8674(95)90412-310.1016/0092-8674(95)90412-3Search in Google Scholar

49. A. A. Roman-Rosales, E. Garcia-Villa, L. A. Herrera, P. Gariglio and J. Diaz-Chavez, Mutant p53 gain of function induces HER2 over-expression in cancer cells, BMC Cancer18 (2018) 709; https://doi.org/10.1186/s12885-018-4613-110.1186/s12885-018-4613-1602941129970031Search in Google Scholar

50. H. Solomon, N. Dinowitz, I. S. Pateras, T. Cooks, Y. Shetzer, A. Molchadsky, M. Charni, S. Rabani, G. Koifman, O. Tarcic, Z. Porat, I. Kogan-Sakin, N. Goldfinger, M. Oren, C. C. Harris, V. G. Gorgoulis and V. Rotter, Mutant p53 gain of function underlies high expression levels of colorectal cancer stem cells markers, Oncogene37 (2018) 1669–1684; https://doi.org/10.1038/s41388-017-0060-810.1038/s41388-017-0060-8644859529343849Search in Google Scholar

51. N. C. Synnott, M. R. Bauer, S. Madden, A. Murray, R. Klinger, N. O’Donovan, D. O’Connor, W. M. Gallagher, J. Crown, A. R. Fersht and M. J. Duffy, Mutant p53 as a therapeutic target for the treatment of triple-negative breast cancer: Preclinical investigation with the anti-p53 drug, PK11007, Cancer Lett. 414 (2018) 99–106; https://doi.org/10.1016/j.canlet.2017.09.05310.1016/j.canlet.2017.09.05329069577Search in Google Scholar

52. H. Xiang, Y. Kinoshita, C. M. Knudson, S. J. Korsmeyer, P. A. Schwartzkroin and R. S. Morrison, Bax involvement in p53-mediated neuronal cell death, J. Neurosci. 18 (1998) 1363–1373; https://doi.org/10.1523/JNEUROSCI.18-04-01363.199810.1523/JNEUROSCI.18-04-01363.1998Search in Google Scholar

53. J. H. Sun, Y. J. Wen, Y. Y. Zhou, Y. M. Jiang, Y. X. Chen, H. Z. Zhang, L. H. Guan, X. P. Yao, M. Huang and H. C. Bi, p53 attenuates acetaminophen-induced hepatotoxicity by regulating drug-metabolizing enzymes and transporter expression, Cell Death Dis. 9 (2018); https://doi.org/10.1038/s41419-018-0507-z10.1038/s41419-018-0507-z594579529748533Search in Google Scholar

54. T. Maeda, C. Tanabe-Fujimura, Y. Fujita, C. Abe, Y. Nanakida, K. Zou, J. J. Liu, S. Y. Liu, T. Nakajima and H. Komano, NAD(P)H quinone oxidoreductase 1 inhibits the proteasomal degradation of homocysteine-induced endoplasmic reticulum protein, Biochem. Bioph. Res. Co. 473 (2016) 1276–1280; https://doi.org/10.1016/j.bbrc.2016.04.05710.1016/j.bbrc.2016.04.057Search in Google Scholar

55. O. H. Rokah, O. Shpilberg and G. Granot, NAD(P)H quinone oxidoreductase protects TAp63 gamma from proteasomal degradation and regulates TAp63 gamma-dependent growth arrest, Plos One5 (2010); https://doi.org/10.1371/journal.pone.001140110.1371/journal.pone.0011401Search in Google Scholar

56. M. J. Lamberti, N. B. Vittar, C. da Silva Fde, V. F. Ferreira and V. A. Rivarola, Synergistic enhancement of antitumor effect of beta-Lapachone by photodynamic induction of quinone oxidoreductase (NQO1), Phytomedicine20 (2013) 1007–1012; https://doi.org/10.1016/j.phymed.2013.04.01810.1016/j.phymed.2013.04.018Search in Google Scholar

57. H. Z. Zhou, H. Q. Zeng, D. Yuan, J. H. Ren, S. T. Cheng, H. B. Yu, F. Ren, Q. Wang, Y. P. Qin, A. L. Huang and J. Chen, NQO1 potentiates apoptosis evasion and upregulates XIAP via inhibiting proteasome-mediated degradation SIRT6 in hepatocellular carcinoma, Cell Commun. Signal17 (2019) 168; https://doi.org/10.1186/s12964-019-0491-710.1186/s12964-019-0491-7Search in Google Scholar

58. X. Zhang, K. Han, D.H. Yuan and C. Y. Meng, Overexpression of NAD(P)H: Quinone oxidoreductase 1 inhibits hepatocellular carcinoma cell proliferation and induced apoptosis by activating AMPK/PGC-1alpha pathway, DNA Cell Biol. 36 (2017) 256–263; https://doi.org/10.1089/dna.2016.358810.1089/dna.2016.3588Search in Google Scholar

59. M. Hayashi, N. Matsumoto, S. Takenoshita-Nakaya, Y. Takeba, M. Watanabe, T. Kumai, M. Takagi, M. Tanaka, T. Otsubo and S. Kobayashi, Individual metabolic capacity evaluation of cytochrome P450 2C19 by protein and activity in the small intestinal mucosa of Japanese pancreatoduodenectomy patients, Biol. Pharm. Bull. 34 (2011) 71–76; https://doi.org/10.1248/bpb.34.7110.1248/bpb.34.71Search in Google Scholar

60. S. Ohtsuki, O. Schaefer, H. Kawakami, T. Inoue, S. Liehner, A. Saito, N. Ishiguro, W. Kishimoto, E. Ludwig-Schwellinger, T. Ebner and T. Terasaki, Simultaneous absolute protein quantification of transporters, cytochromes P450, and UDP-glucuronosyltransferases as a novel approach for the characterization of individual human liver: comparison with mRNA levels and activities, Drug Metab. Dispos. 40 (2012) 83–92; https://doi.org/10.1124/dmd.111.04225910.1124/dmd.111.042259Search in Google Scholar

61. H. Lin and K. S. Caroll, Introduction: Posttranslational protein modification, Chem. Rev. 118 (2018) 887–888; https://doi.org/10.1021/acs.chemrev.7b0075610.1021/acs.chemrev.7b00756Search in Google Scholar

62. R. D. Traver, T. Horikoshi, K. D. Danenberg, T. H. W. Stadlbauer, P. V. Danenberg, D. Ross and N. W. Gibson, NAD(P)H-quinone oxidoreductase gene-expression in human colon-carcinoma cells: characterization of a mutation which modulates DT-diaphorase activity and mitomycin sensitivity, Cancer Res. 52 (1992) 797–802.Search in Google Scholar

63. X. Zhang, K. Han, D. H. Yuan and C. Y. Meng, Overexpression of NAD(P)H: quinone oxidoreductase 1 inhibits hepatocellular carcinoma cell proliferation and induced apoptosis by activating AMPK/PGC-1alpha pathway, DNA Cell Biol. 36 (2017) 256–263; https://doi.org/10.1089/dna.2016.358810.1089/dna.2016.3588Search in Google Scholar

64. D. Bergamaschi, M. Gasco, L. Hiller, A. Sullivan, N. Syed, G. Trigiante, I. Yulug, M. Merlano, G. Numico, A. Comino, M. Attard, O. Reelfs, B. Gusterson, A. K. Bell, V. Heath, M. Tavassoli, P. J. Farrell, P. Smith, X. Lu and T. Crook, p53 polymorphism influences response in cancer chemotherapy via modulation of p73-dependent apoptosis, Cancer Cell3 (2003) 387–402; https://doi.org/10.1016/s1535-6108(03)00079-510.1016/S1535-6108(03)00079-5Search in Google Scholar