The Chemopreventive Capacity of Quercetin to Induce Programmed Cell Death in Hepatocarcinogenesis

Toxicologic Pathology

Volumn 41, Issue 6, 2013, Pages 857-865

  Vásquez Garzón, Verónica Rocío ^a   Macias Pérez, José Roberto ^a   Jiménez García, Mónica Noemí ^a   Villegas, Vanessa ^b   Fattel Fazenta, Samia ^a   Villa Treviño, Saúl ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

apoptosis mechanisms; carcinogenesis; chemoprevention; hepatic cancer; quercetin

Indexed keywords

CASPASE 3; CASPASE 8; CASPASE 9; DIETHYLNITROSAMINE; N (2 FLUORENYL)ACETAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROCASPASE 3; QUERCETIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CHEMOPROPHYLAXIS; CONTROLLED STUDY; ENZYME ACTIVATION; LIPID PEROXIDATION; LIVER CARCINOGENESIS; LIVER CELL; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SINGLE DRUG DOSE; WESTERN BLOTTING;

APOPTOSIS MECHANISMS; CARCINOGENESIS.; CHEMOPREVENTION; HEPATIC CANCER; QUERCETIN;

ANIMALS; ANTICARCINOGENIC AGENTS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOGENESIS; CASPASES; CHEMOPREVENTION; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; MALE; OXIDATIVE STRESS; PRECANCEROUS CONDITIONS; QUERCETIN; RATS; RATS, INBRED F344;

EID: 84880424677     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623312467522     Document Type: Article

References (39)

1. Aggarwal B. B. Van Kuiken M. E. Iyer L. H. Harikumar K. B. Sung B. (2009). Molecular targets of nutraceuticals derived from dietary spices: Potential role in suppression of inflammation and tumorigenesis. Exp Biol Med (Maywood) 234, 825–49.
2. Anisimov V. N. (2007). Biology of aging and cancer. Cancer Control 14, 23–31.
3. Arellanes-Robledo J. Salcido-Neyoy M. E. Marquez-Quinones A. Garcia-Roman R. Beltran-Ramirez O. Le Berre V. Sokol S. Francois J. M. Villa-Trevino S. (2009). Celecoxib activates Stat5 and restores or increases the expression of growth hormone-regulated genes in hepatocarcinogenesis. Anti-cancer drugs 21, 411–22.
4. Beltran-Ramirez O. Aleman-Lazarini L. Salcido-Neyoy M. Hernandez-Garcia S. Fattel-Fazenda S. Arce-Popoca E. Arellanes-Robledo J. Garcia-Roman R. Vazquez-Vazquez P. Sierra-Santoyo A. Villa-Trevino S. (2008). Evidence that the anticarcinogenic effect of caffeic acid phenethyl ester in the resistant hepatocyte model involves modifications of cytochrome P450. Toxicol Sci 104, 100–106.
5. Benetou V. Orfanos P. Lagiou P. Trichopoulos D. Boffetta P. Trichopoulou A. (2008). Vegetables and fruits in relation to cancer risk: Evidence from the Greek EPIC cohort study. Cancer Epidemiol Biomarkers Prev 17, 387–92.
6. Buege J. A. Aust S. D. (1978). Microsomal lipid peroxidation. Methods Enzymol 52, 302–10.
7. Campbell H. A. Xu Y. D. Hanigan M. H. Pitot H. C. (1986). Application of quantitative stereology to the evaluation of phenotypically heterogeneous enzyme-altered foci in the rat liver. J Natl Cancer Inst. 76, 751–67.
8. Carrasco-Legleu C. E. Marquez-Rosado L. Fattel-Fazenda S. Arce-Popoca E. Perez-Carreon J. I. Villa-Trevino S. (2004). Chemoprotective effect of caffeic acid phenethyl ester on promotion in a medium-term rat hepatocarcinogenesis assay. Int J Cancer 108, 488–92.
9. Devipriya S. Ganapathy V. Shyamaladevi C. S. (2006). Suppression of tumor growth and invasion in 9,10 dimethyl benz(a) anthracene induced mammary carcinoma by the plant bioflavonoid quercetin. Chem Biol Interact 162, 106–13.
10. Farber E. (1984). Pre-cancerous steps in carcinogenesis. Their physiological adaptive nature. Biochim Biophys Acta 738, 171–80.
11. Ferlay J. Shin H. R. Bray F. Forman D. Mathers C. Parkin D. M. (2010). Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer, 127, 2893–2917.
12. Freedman N. D. Park Y. Subar A. F. Hollenbeck A. R. Leitzmann M. F. Schatzkin A. Abnet C. C. (2008). Fruit and vegetable intake and head and neck cancer risk in a large United States prospective cohort study. Int J Cancer 122, 2330–336.
13. Gibellini L. Pinti M. Nasi M. Montagna J. P. De Biasi S. Roat E. Bertoncelli L. Cooper E. L. Cossarizza A. (2011). Quercetin and cancer chemoprevention. Evid Based Complement Alternat Med 2011, 591356.
14. Granado-Serrano A. B. Martin M. A. Bravo L. Goya L. Ramos S. (2006). Quercetin induces apoptosis via caspase activation, regulation of Bcl-2, and inhibition of PI-3-kinase/Akt and ERK pathways in a human hepatoma cell line (HepG2). J Nutr 136, 2715–721.
15. Gupta C. Vikram A. Tripathi D. N. Ramarao P. Jena G. B. (2009). Antioxidant and antimutagenic effect of quercetin against DEN induced hepatotoxicity in rat. Phytother Res 24, 119–28.
16. Hanahan D. Weinberg R. A. (2011). Hallmarks of cancer: The next generation. Cell 144, 646–74.
17. Jeong J. H. An J. Y. Kwon Y. T. Rhee J. G. Lee Y. J. (2009). Effects of low dose quercetin: Cancer cell-specific inhibition of cell cycle progression. J Cell Biochem 106, 73–82.
18. Kaldas M. I. Walle U. K. van der Woude H. McMillan J. M. Walle T. (2005). Covalent binding of the flavonoid quercetin to human serum albumin. J Agric Food Chem 53, 4194–97.
19. Kamaraj S. Vinodhkumar R. Anandakumar P. Jagan S. Ramakrishnan G. Devaki T. (2007). The effects of quercetin on antioxidant status and tumor markers in the lung and serum of mice treated with benzo(a)pyrene. Biol Pharm Bull 30, 2268–73.
20. Kim H. J. Kim S. K. Kim B. S. Lee S. H. Park Y. S. Park B. K. Kim S. J. Kim J. Choi C. Kim J. S. Cho S. D. Jung J. W. Roh K. H. Kang K. S. Jung J. Y. (2010). Apoptotic effect of quercetin on HT-29 colon cancer cells via the AMPK signaling pathway. J Agri Food Chem 58, 8643–50.
21. Lee J. S. Chu I. S. Heo J. Calvisi D. F. Sun Z. Roskams T. Durnez A. Demetris A. J. Thorgeirsson S. S. (2004). Classification and prediction of survival in hepatocellular carcinoma by gene expression profiling. Hepatology 40, 667–76.
22. Li J. Mottamal M. Li H. Liu K. Zhu F. Cho Y. Y. Sosa C. P. Zhou K. Bowden G. T. Bode A. M. Dong Z. (2012). Quercetin-3-methyl ether suppresses proliferation of mouse epidermal JB6 P+ cells by targeting ERKs. Carcinogenesis 33, 459–65.
23. Marche-Cova A. Fattel-Fazenda S. Rojas-Ochoa A. Arce-Popoca E. Villa-Trevino S. (1995). Follow-up of GST-P during hepatocarcinogenesis with DEN-2AAF in F344 rats. Arch Med Res 26, S169–73.
24. Marquez-Rosado L. Trejo-Solis M. C. Garcia-Cuellar C. M. Villa-Trevino S. (2005). Celecoxib, a cyclooxygenase-2 inhibitor, prevents induction of liver preneoplastic lesions in rats. J Hepatol 43, 653–60.
25. Mikstacka R. Ignatowicz E. (2010). [Chemopreventive and chemotherapeutic effect of trans-resveratrol and its analogues in cancer]. Pol Merkur Lekarski 28, 496–500.
26. Pascale R. M. Simile M. M. De Miglio M. R. Muroni M. R. Calvisi D. F. Asara G. Casabona D. Frau M. Seddaiu M. A. Feo F. (2002). Cell cycle deregulation in liver lesions of rats with and without genetic predisposition to hepatocarcinogenesis. Hepatology 35, 1341–50.
27. Perera F. P. (2000). Molecular epidemiology: On the path to prevention? J Natl Cancer Inst 92, 602–12.
28. Perez-Carreon J. I. Lopez-Garcia C. Fattel-Fazenda S. Arce-Popoca E. Aleman-Lazarini L. Hernandez-Garcia S. Le Berre V. Sokol S. Francois J. M. Villa-Trevino S. (2006). Gene expression profile related to the progression of preneoplastic nodules toward hepatocellular carcinoma in rats. Neoplasia 8, 373–83.
29. Pitot H. C. Dragan Y. P. Teeguarden J. Hsia S. Campbell H. (1996). Quantitation of multistage carcinogenesis in rat liver. Toxicol Pathol 24, 119–28.
30. Rotstein J. Macdonald P. D. Rabes H. M. Farber E. (1984). Cell cycle kinetics of rat hepatocytes in early putative preneoplastic lesions in hepatocarcinogenesis. Canc Res 44, 2913–17.
31. Rutenburg A. M. Kim H. Fischbein J. W. Hanker J. S. Wasserkrug H. L. Seligman A. M. (1969). Histochemical and ultrastructural demonstration of gamma-glutamyl transpeptidase activity. J Histochem Cytochem 17, 517–26.
32. Senthilkumar K. Elumalai P. Arunkumar R. Banudevi S. Gunadharini N. D. Sharmila G. Selvakumar K. Arunakaran J. (2010). Quercetin regulates insulin like growth factor signaling and induces intrinsic and extrinsic pathway mediated apoptosis in androgen independent prostate cancer cells (PC-3). Mol Cell Biochem 344, 173–84.
33. Sivaramakrishnan V. Shilpa P. N. Praveen Kumar V. R. Niranjali Devaraj S. (2008). Attenuation of N-nitrosodiethylamine-induced hepatocellular carcinogenesis by a novel flavonol-Morin. Chem Biol Interact 171, 79–88.
34. Sun Z. J. Chen G. Hu X. Zhang W. Liu Y. Zhu L. X. Zhou Q. Zhao Y. F. (2010). Activation of PI3K/Akt/IKK-alpha/NF-kappaB signaling pathway is required for the apoptosis-evasion in human salivary adenoid cystic carcinoma: Its inhibition by quercetin. Apoptosis 15, 850–63.
35. Vasquez-Garzon V. R. Arellanes-Robledo J. Garcia-Roman R. Aparicio-Rautista D. I. Villa-Trevino S. (2009). Inhibition of reactive oxygen species and pre-neoplastic lesions by quercetin through an antioxidant defense mechanism. Free Radic Res 43, 128–37.
36. Volate S. R. Davenport D. M. Muga S. J. Wargovich M. J. (2005). Modulation of aberrant crypt foci and apoptosis by dietary herbal supplements (quercetin, curcumin, silymarin, ginseng and rutin). Carcinogenesis 26, 1450–56.
37. Weinstein I. B. (1991). Cancer prevention: Recent progress and future opportunities. Cancer Res 51, 5080s–85s.
38. Williamson G. Manach C. (2005). Bioavailability and bioefficacy of polyphenols in humans. II. Review of 93 intervention studies. Am J Clin Nutr 81, 243S–55S.
39. Yamada K. Yamamiya I. Utsumi H. (2006). In vivo detection of free radicals induced by diethylnitrosamine in rat liver tissue. Free Radic Biol Med 40, 2040–46.