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

Karakurt, Serdar; Kandir, Sinan; Gökçek-Saraç, Çiğdem

doi:10.2478/acph-2021-0036

Abstract

The present study’s objective is to clarify the molecular mechanisms of tannic acid effects on the viability of human colorectal carcinoma (CRC). Tannic acid is stable for up to 48 h and is localized in both cytoplasm and nucleus. It dose-dependently inhibited the viability of CRC cell lines; SW-620 and HT-29 with IC₅₀ values of 7.2 ± 0.8 and 37.6 ± 1.4 µmol L^–1. Besides, metastatic, invasive, and colony formation properties of CRC cells were significantly inhibited following the tannic acid treatment (p < 0.001). Tannic acid has been found to modulate enzyme, protein, and gene expressions of NQO1 in different levels and the upregulation of protein/gene expressions of p53 (p < 0.001), which leads the cells to trigger apoptosis. In conclusion, the present in vitro study may supply a significant background for in vivo studies in which the molecular mechanisms of antioxidant and chemopreventive activities of tannic acid will completely clarify.

References

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.1495157
Search in Google Scholar Back to article
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.2139528248415
Search in Google Scholar Back to article
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.5888474721726543234
Search in Google Scholar Back to article
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.24760361972619998273
Search in Google Scholar Back to article
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/s12906-018-2412-5630717430587184
Search in Google Scholar Back to article
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.2018.09.16930466981
Search in Google Scholar Back to article
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.2015.11.00826776960
Search in Google Scholar Back to article
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.2014.07.025414668425058905
Search in Google Scholar Back to article
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/10.1186/2050-6511-14-1810.1186/2050-6511-14-18363717223521834
Search in Google Scholar Back to article
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/s12906-019-2487-7645122530952208
Search in Google Scholar Back to article
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/molecules15107313625914620966876
Search in Google Scholar Back to article
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.2019.03.017
Search in Google Scholar Back to article
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 Back to article
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.201000044
Search in Google Scholar Back to article
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.2016.06.022
Search in Google Scholar Back to article
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.2016.03.006
Search in Google Scholar Back to article
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.2018.8197
Search in Google Scholar Back to article
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.2018.12.007
Search in Google Scholar Back to article
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.2015.06.048
Search in Google Scholar Back to article
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.200410517
Search in Google Scholar Back to article
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)00117-8
Search in Google Scholar Back to article
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)90997-6
Search in Google Scholar Back to article
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)00273-4
Search in Google Scholar Back to article
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/s10147020001312018106
Search in Google Scholar Back to article
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.6601779241028215138483
Search in Google Scholar Back to article
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.2010.03.019293003820361926
Search in Google Scholar Back to article
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.31990554650915687255
Search in Google Scholar Back to article
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.2005.01.02015749015
Search in Google Scholar Back to article
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.x59219499818026
Search in Google Scholar Back to article
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-x30631929
Search in Google Scholar Back to article
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/10.2174/187152061666615111111580910.2174/187152061666615111111580926555610
Search in Google Scholar Back to article
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-2002-30758515733110363
Search in Google Scholar Back to article
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)90101-2
Search in Google Scholar Back to article
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)90442-7
Search in Google Scholar Back to article
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.2001.126211846609
Search in Google Scholar Back to article
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/jf9506287
Search in Google Scholar Back to article
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/BF02702656
Search in Google Scholar Back to article
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.00033.201324186932
Search in Google Scholar Back to article
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.03652519726629
Search in Google Scholar Back to article
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.1725808260076719056882
Search in Google Scholar Back to article
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.e14-01-0697
Search in Google Scholar Back to article
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_2328819859
Search in Google Scholar Back to article
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.a003009
Search in Google Scholar Back to article
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/10.3791/5272710.3791/52727
Search in Google Scholar Back to article
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/10.3791/5199810.3791/51998
Search in Google Scholar Back to article
46. S. Elmore, Apoptosis: a review of programmed cell death, Toxicol Pathol. 35 (2007) 495–516; https://doi.org/10.1080/0192623070132033710.1080/01926230701320337
Search in Google Scholar Back to article
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-X
Search in Google Scholar Back to article
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)90412-3
Search in Google Scholar Back to article
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/s12885-018-4613-1602941129970031
Search in Google Scholar Back to article
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/s41388-017-0060-8644859529343849
Search in Google Scholar Back to article
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.2017.09.05329069577
Search in Google Scholar Back to article
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.18-04-01363.1998
Search in Google Scholar Back to article
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-z594579529748533
Search in Google Scholar Back to article
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.2016.04.057
Search in Google Scholar Back to article
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.0011401
Search in Google Scholar Back to article
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.2013.04.018
Search in Google Scholar Back to article
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/s12964-019-0491-7
Search in Google Scholar Back to article
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.2016.3588
Search in Google Scholar Back to article
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.34.71
Search in Google Scholar Back to article
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.111.042259
Search in Google Scholar Back to article
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.7b00756
Search in Google Scholar Back to article
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 Back to article
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.2016.3588
Search in Google Scholar Back to article
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)00079-5
Search in Google Scholar Back to article

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

Abstract

Paradigm

My account