Dietary supplementation of silymarin is associated with decreased cell proliferation, increased apoptosis, and activation of detoxification system in hepatocellular carcinoma

Molecular and Cellular Biochemistry

Volumn 377, Issue 1-2, 2013, Pages 163-176

  Gopalakrishnan, Ramakrishnan ^a   Sundaram, Jagan ^a   Sattu, Kamaraj ^a   Pandi, Anandakumar ^a   Thiruvengadam, Devaki ^a  

^a UNIVERSITY OF MADRAS   (India)

Author keywords

Apoptosis; Hepatocellular carcinoma; Mitochondria; N nitrosodiethylamine; Proliferation; Silymarin

Indexed keywords

CYTOCHROME C; DIETHYLNITROSAMINE; GLUTATHIONE TRANSFERASE; GLYCOCONJUGATE; HEXOSAMINE; HEXOSE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE FERRIHEMOPROTEIN REDUCTASE; SIALIC ACID; SILYMARIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL PROLIFERATION; CHEMOPROPHYLAXIS; CONTROLLED STUDY; CYTOSOL; DETOXIFICATION; DIET SUPPLEMENTATION; DOWN REGULATION; FLOW CYTOMETRY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LIVER CELL; LIVER CELL CARCINOMA; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; RAT; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BETA CATENIN; CARCINOMA, HEPATOCELLULAR; CASPASE 3; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN D1; DIETARY SUPPLEMENTS; DRUG SCREENING ASSAYS, ANTITUMOR; GLYCOPROTEINS; HEXOSAMINES; HEXOSES; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; METABOLIC DETOXICATION, PHASE II; MICROTUBULE-ASSOCIATED PROTEINS; PROLIFERATING CELL NUCLEAR ANTIGEN; RATS; RATS, WISTAR; SIALIC ACIDS; SILYMARIN; TUMOR SUPPRESSOR PROTEIN P53;

RATTUS;

EID: 84875636580     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-013-1582-1     Document Type: Article

References (69)

1. Jemal ABF, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61:69-90
2. Daniele B, Di Maio M (2009) Target therapy for hepatocellular carcinoma: is sorafenib for everybody? J Clin Gastroenterol 43:389-390
3. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, de Oliveira AC, Santoro A, Raoul JL, Forner A, Schwartz M, Porta C, Zeuzem S, Bolondi L, Greten TF, Galle PR, Seitz JF, Borbath I, Haussinger D, Giannaris T, Shan M, Moscovici M, Voliotis D, Bruix J (2008) Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 359:378-390
4. Hecht SS (1997) Approaches to cancer prevention based on an understanding of N-nitrosamine carcinogenesis. Proc Soc Exp Biol Med 216:181-191
5. Ramakrishnan G, Jagan S, Kamaraj S, Anandakumar P, Devaki T (2009) Silymarin attenuated mast cell recruitment thereby decreased the expressions of matrix metalloproteinases-2 and 9 in rat liver carcinogenesis. Invest New Drugs 27:233-240
6. Joos S, Musselmann B, Szecsenyi J (2011) Integration of complementary and alternative medicine into family practices in Germany: results of a national survey. Evid Based Complement Alternat Med 2011:495813. doi: 10.1093/ecam/nep019
7. Polyak SJ, Morishima C, Lohmann V, Pal S, Lee DY, Liu Y, Graf TN, Oberlies NH (2010) Identification of hepatoprotective flavonolignans from silymarin. Proc Natl Acad Sci 107:5995-5999
8. Katiyar SK (2005) Silymarin and skin cancer prevention: anti-inflammatory, antioxidant and immunomodulatory effects (Review). Int J Oncol 26:169-176
9. Bhatia N, Zhao J, Wolf DM, Agarwal R (1999) Inhibition of human carcinoma cell growth and DNA synthesis by silibinin, an active constituent of milk thistle: comparison with silymarin. Cancer Lett 147:77-84
10. Ramakrishnan G, Augustine TA, Jagan S, Vinodhkumar R, Devaki T (2007) Effect of silymarin on N-nitrosodiethylamine induced hepatocarcinogenesis in rats. Exp Oncol 29:39-44
11. Ploton D, Menager M, Jeannesson P, Himber G, Pigeon F, Adnet JJ (1986) Improvement in the staining and in the visualization of the argyrophilic proteins of the nucleolar organizer region at the optical level. Histochem J 18:5-14
12. Ramakrishnan G, Elinos-Baez CM, Jagan S, Augustine TA, Kamaraj S, Anandakumar P, Devaki T (2008) Silymarin downregulates COX-2 expression and attenuates hyperlipidemia during NDEA-induced rat hepatocellular carcinoma. Mol Cell Biochem 313:53-61
13. Niebes P (1972) Determination of enzymes and degradation products of glycosaminoglycan metabolism in the serum of healthy and varicose subjects. Clin Chim Acta 42:399-408
14. Wagner WD (1979) A more sensitive assay discriminating galactosamine and glucosamine in mixtures. Anal Biochem 94:394-396
15. Warren L (1959) The thiobarbituric acid assay of sialic acids. J Biol Chem 234:1971-1975
16. Fry JR (1981) Preparation of mammalian hepatocytes. Methods Enzymol 77:130-137
17. Omura T, Sato R (1964) The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J Biol Chem 239:2370-2378
18. Phillips AH, Langdon RG (1962) Hepatic triphosphopyridine nucleotide-cytochrome c reductase: isolation, characterization, and kinetic studies. J Biol Chem 237:2652-2660
19. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione-S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130-7139
20. Stoimenov I, Helleday T (2009) PCNA on the crossroad of cancer. Biochem Soc Trans 37:605-613
21. Borzio M, Trere D, Borzio F, Ferrari AR, Bruno S, Roncalli M, Colloredo G, Leandro G, Oliveri F, Derenzini M (1998) Hepatocyte proliferation rate is a powerful parameter for predicting hepatocellular carcinoma development in liver cirrhosis. Mol Pathol 51:96-101
22. Rodrigues OR, Antonangelo L, Yagi N, Minamoto H, Schmidt Junior AF, Capelozzi VL, Goldenberg S, Saldiva PH (1997) Prognostic significance of argyrophilic nucleolar organizer region (AgNOR) in resected non-small cell lung cancer (NSCLC). Jpn J Clin Oncol 27:298-304
23. Trere D, Derenzini M, Sirri V, Montanaro L, Grigioni W, Faa G, Columbano GM, Columbano A (1996) Qualitative and quantitative analysis of AgNOR proteins in chemically induced rat liver carcinogenesis. Hepatology 24:1269-1273
24. Jagan S, Ramakrishnan G, Anandakumar P, Kamaraj S, Devaki T (2008) Antiproliferative potential of gallic acid against diethylnitrosamine-induced rat hepatocellular carcinoma. Mol Cell Biochem 319:51-59
25. Pich A, Chiusa L, Navone R (2004) Prognostic relevance of cell proliferation in head and neck tumors. Ann Oncol 15:1319-1329
26. Thirunavukkarasu C, Sakthisekaran D (2003) Influence of sodium selenite on glycoprotein contents in normal and N-nitrosodiethylamine initiated and phenobarbital promoted rat liver tumors. Pharmacol Res 48:167-173
27. Senthilnathan P, Padmavathi R, Magesh V, Sakthisekaran D (2006) Chemotherapeutic efficacy of paclitaxel in combination with Withania somnifera on benzo(a)pyrene-induced experimental lung cancer. Cancer Sci 97:658-664
28. Goldhirsch A, Berger E, Muller O, Maibach R, Misteli S, Buser K, Roesler H, Brunner K (1988) Ovarian cancer and tumor markers: sialic acid, galactosyltransferase and CA-125. Oncology 45:281-286
29. Dabelsteen E (1996) Cell surface carbohydrates as prognostic markers in human carcinomas. J Pathol 179:358-369
30. Manoharan S, Padmanabhan M, Kolanjiappan K, Ramachandran CR, Suresh K (2004) Analysis of glycoconjugates in patients with oral squamous cell carcinoma. Clin Chim Acta 339:91-96
31. Joo M, Lee HK, Kang YK (2003) Expression of beta-catenin in hepatocellular carcinoma in relation to tumor cell proliferation and cyclin D1 expression. J Korean Med Sci 18:211-217
32. Derksen PW, Tjin E, Meijer HP, Klok MD, MacGillavry HD, van Oers MH, Lokhorst HM, Bloem AC, Clevers H, Nusse R, van der Neut R, Spaargaren M, Pals ST (2004) Illegitimate WNT signaling promotes proliferation of multiple myeloma cells. Proc Natl Acad Sci USA 101:6122-6127
33. Saldanha G, Ghura V, Potter L, Fletcher A (2004) Nuclear beta-catenin in basal cell carcinoma correlates with increased proliferation. Br J Dermatol 151:157-164
34. Calvisi DF, Ladu S, Factor VM, Thorgeirsson SS (2004) Activation of beta-catenin provides proliferative and invasive advantages in c-myc/TGF-alpha hepatocarcinogenesis promoted by phenobarbital. Carcinogenesis 25:901-908
35. Deane NG, Parker MA, Aramandla R, Diehl L, Lee WJ, Washington MK, Nanney LB, Shyr Y, Beauchamp RD (2001) Hepatocellular carcinoma results from chronic cyclin D1 overexpression in transgenic mice. Cancer Res 61:5389-5395
36. Ramakrishnan G, Raghavendran HR, Vinodhkumar R, Devaki T (2006) Suppression of N-nitrosodiethylamine induced hepatocarcinogenesis by silymarin in rats. Chem Biol Interact 161:104-114
37. Hara A, Sakata K, Yamada Y, Kuno T, Kitaori N, Oyama T, Hirose Y, Murakami A, Tanaka T, Mori H (2005) Suppression of beta-catenin mutation by dietary exposure of auraptene, a citrus antioxidant, in N,N-diethylnitrosamine- induced hepatocellular carcinomas in rats. Oncol Rep 14:345-351
38. Watson AJ (2004) Apoptosis and colorectal cancer. Gut 53:1701-1709
39. Vousden KH, Ryan KM (2009) p53 and metabolism. Nat Rev Cancer 9:691-700
40. Yonish-Rouach E, Grunwald D, Wilder S, Kimchi A, May E, Lawrence JJ, May P, Oren M (1993) p53-Mediated cell death: relationship to cell cycle control. Mol Cell Biol 13:1415-1423
41. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA Jr, Butel JS, Bradley A (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215-221
42. Harvey M, Vogel H, Morris D, Bradley A, Bernstein A, Donehower LA (1995) A mutant p53 transgene accelerates tumour development in heterozygous but not nullizygous p53-deficient mice. Nat Genet 9:305-311
43. Martins CP, Brown-Swigart L, Evan GI (2006) Modeling the therapeutic efficacy of p53 restoration in tumors. Cell 127:1323-1334
44. Ventura A, Kirsch DG, McLaughlin ME, Tuveson DA, Grimm J, Lintault L, Newman J, Reczek EE, Weissleder R, Jacks T (2007) Restoration of p53 function leads to tumour regression in vivo. Nature 445:661-665
45. Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V, Cordon-Cardo C, Lowe SW (2007) Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 445:656-660
46. Vousden KH, Lane DP (2007) p53 in health and disease. Nat Rev Mol Cell Biol 8:275-283
47. Banks D, Wu M, Higa LA, Gavrilova N, Quan J, Ye T, Kobayashi R, Sun H, Zhang H (2006) L2DTL/CDT2 and PCNA interact with p53 and regulate p53 polyubiquitination and protein stability through MDM2 and CUL4A/DDB1 complexes. Cell Cycle 5:1719-1729
48. Ramakrishnan G, Lo Muzio L, Elinos-Baez CM, Jagan S, Augustine TA, Kamaraj S, Anandakumar P, Devaki T (2009) Silymarin inhibited proliferation and induced apoptosis in hepatic cancer cells. Cell Prolif 42:229-240
49. Vaux DL, Cory S, Adams JM (1988) Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335:440-442
50. Cory S, Adams JM (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2:647-656
51. Cory S, Adams JM (2005) Killing cancer cells by flipping the Bcl-2/Bax switch. Cancer Cell 8:5-6
52. Miyashita T, Krajewski S, Krajewska M, Wang HG, Lin HK, Liebermann DA, Hoffman B, Reed JC (1994) Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9:1799-1805
53. Altieri DC (2003) Validating survivin as a cancer therapeutic target. Nat Rev Cancer 3:46-54
54. Ambrosini G, Adida C, Altieri DC (1997) A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 3:917-921
55. Ikeguchi M, Ueta T, Yamane Y, Hirooka Y, Kaibara N (2002) Inducible nitric oxide synthase and survivin messenger RNA expression in hepatocellular carcinoma. Clin Cancer Res 8:3131-3136
56. Hoffman WH, Biade S, Zilfou JT, Chen J, Murphy M (2002) Transcriptional repression of the anti-apoptotic survivin gene by wild type p53. J Biol Chem 277:3247-3257
57. Mirza A, McGuirk M, Hockenberry TN, Wu Q, Ashar H, Black S, Wen SF, Wang L, Kirschmeier P, Bishop WR, Nielsen LL, Pickett CB, Liu S (2002) Human survivin is negatively regulated by wild-type p53 and participates in p53-dependent apoptotic pathway. Oncogene 21:2613-2622
58. Mesri M, Wall NR, Li J, Kim RW, Altieri DC (2001) Cancer gene therapy using a survivin mutant adenovirus. J Clin Invest 108:981-990
59. Hockenbery, D. M. Targeting mitochondria for cancer therapy. Environ Mol Mutagen 51, 476-89.
60. Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C, Kroemer G (2006) Mechanisms of cytochrome c release from mitochondria. Cell Death Differ 13:1423-1433
61. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275:1132-1136
62. Smith DJ, Ng H, Kluck RM, Nagley P (2008) The mitochondrial gateway to cell death. IUBMB Life 60:383-389
63. Gonzalez FJ, Yu AM (2006) Cytochrome P450 and xenobiotic receptor humanized mice. Annu Rev Pharmacol Toxicol 46:41-64
64. Steinkellner H, Rabot S, Freywald C, Nobis E, Scharf G, Chabicovsky M, Knasmuller S, Kassie F (2001) Effects of cruciferous vegetables and their constituents on drug metabolizing enzymes involved in the bioactivation of DNA-reactive dietary carcinogens. Mutat Res 480-481:285-297
65. Verna L, Whysner J, Williams GM (1996) N-nitrosodiethylamine mechanistic data and risk assessment: bioactivation, DNA-adduct formation, mutagenicity, and tumor initiation. Pharmacol Ther 71:57-81
66. Selvendiran K, Thirunavukkarasu C, Singh JP, Padmavathi R, Sakthisekaran D (2005) Chemopreventive effect of piperine on mitochondrial TCA cycle and phase-I and glutathione-metabolizing enzymes in benzo(a)pyrene induced lung carcinogenesis in Swiss albino mice. Mol Cell Biochem 271:101-106
67. Talalay P, Fahey JW, Holtzclaw WD, Prestera T, Zhang Y (1995) Chemoprotection against cancer by phase 2 enzyme induction. Toxicol Lett 82-83:173-179
68. Kohno H, Tanaka T, Kawabata K, Hirose Y, Sugie S, Tsuda H, Mori H (2002) Silymarin, a naturally occurring polyphenolic antioxidant flavonoid, inhibits azoxymethane-induced colon carcinogenesis in male F344 rats. Int J Cancer 101:461-468
69. Yannai S, Day AJ, Williamson G, Rhodes MJ (1998) Characterization of flavonoids as monofunctional or bifunctional inducers of quinone reductase in murine hepatoma cell lines. Food Chem Toxicol 36:623-630