All-trans and 9-cis retinoic acids, retinol and β-carotene chemopreventive activities during the initial phases of hepatocarcinogenesis involve distinct actions on glutathione S-transferase positive preneoplastic lesions remodeling and DNA damage

Carcinogenesis

Volumn 26, Issue 11, 2005, Pages 1940-1946

  de Almeida Vasconcelos Fonseca, Elaine Maria ^a   Chagas, Carlos Eduardo Andrade ^a   Mazzantini, Rogério Pietro ^a   Heidor, Renato ^a   Ong, Thomas Prates ^a   Moreno, Fernando Salvador ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ALITRETINOIN; BETA CAROTENE; CORN OIL; GLUTATHIONE TRANSFERASE; RETINOIC ACID; RETINOL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER PREVENTION; CELL COUNT; CELL PROLIFERATION; CHEMOPROPHYLAXIS; CONTROLLED STUDY; DNA STRAND BREAKAGE; IMMUNOHISTOCHEMISTRY; LIVER CANCER; LIVER CARCINOGENESIS; LIVER CELL; MALE; NONHUMAN; PRECANCER; PRIORITY JOURNAL; RAT; TISSUE REPAIR; TISSUE SECTION;

ANIMALS; ANTINEOPLASTIC AGENTS; ANTIOXIDANTS; APOPTOSIS; BETA CAROTENE; BODY WEIGHT; CELL PROLIFERATION; CHEMOPREVENTION; COMET ASSAY; DNA DAMAGE; GLUTATHIONE TRANSFERASE; HEPATOCYTES; INCIDENCE; LIVER NEOPLASMS, EXPERIMENTAL; MALE; ORGAN SIZE; PRECANCEROUS CONDITIONS; RATS; RATS, WISTAR; TRETINOIN; VITAMIN A;

EID: 27744597910     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgi161     Document Type: Article

References (45)

1. Bishayee,A., Sarkar,A. and Chatterjee,M. (2000) Further evidence for chemopreventive potential of β-carotene against experimental carcinogenesis: Diethylnitrosamine-initiated and phenobarbital-promoted hepatocarcinogenesis is prevented more effectively by β-carotene than by retinoic acid. Nutr. Cancer, 37, 89-98.
2. Muto,Y., Moriwaki,H., Ninomiya,M. et al. (1996) Prevention of second primary tumors by an acyclic retinoid, polyprenoic acid, in patients with hepatocellular carcinoma. N. Engl. J. Med., 334, 1561-1567.
3. Muto,Y., Moriwaki H. and Saito,A. (1999) Prevention of second primary tumors by an acyclic retinoid in patients with hepatocellular carcinoma. N. Engl. J. Med., 340, 1046-1047.
4. Muto,Y. and Moriwaki,H. (1984) Antitumor activity of vitamin A and its derivatives. J. Natl. Cancer Inst., 73, 1389-1393.
5. Moreno,F.S., Wu,T.-S., Naves,M.M., Silveira,E.R., Oloris,S.C., da Costa,M.A., Dagli,M.L. and Ong,T.P. (2002) Inhibitory effects of β-carotene and vitamin A during the progression phase of hepatocarcinogenesis involve inhibition of cell proliferation but not alterations in DNA methylation. Nutr. Cancer, 44, 80-88.
6. Moreno,F.S., Rizzi,M.B., Dagli,M.L. and Penteado,M.V. (1991) Inhibitory effects of beta-carotene on preneoplastic lesions induced in Wistar rats by the resistant hepatocyte model. Carcinogenesis, 12, 1817-1822.
7. Moon,R.C., Mehta,R.G. and Rao,K.V.N. (1984) Retinoids and cancer in experimental animals. In Sporn,M.B., Roberts,A.B. and Goodman,D.S. (eds) The Retinoids: Biology, Chemistry and Medicine. Raven Press, New York, pp. 597-630.
8. Baba,M., Iishi,H., Yamamoto,R. and Tatsuta,M. (1991) Inhibition by retinoic acid of hepatocarcinogenesis induced by N-nitrosomorpholine and of expression of myc oncogene protein in Sprague-Dawley rats. Int. J. Cancer, 49, 467-470.
9. Silveira,E.R., Naves,M.M., Vannucchi,H., Jordão,A.A.,Jr, Dagli,M.L. and Moreno,F.S. (2001) Vitamin A and all-trans and 9-cis acids inhibit cell proliferation during the progression phase of hepatocarcinogenesis in Wistar rats. Nutr. Cancer, 39, 244-251.
10. Tamura,K., Nakae,D., Horiguchi,K. et al. (1997) Inhibition by N-(4-hydroxyphenyl)retinamide and all-trans-retinoic acid of exogenous and endogenous development of putative preneoplastic, glutathione S-transferase placental form-positive lesions in the livers of rats. Carcinogenesis, 18, 2133-2141.
11. Ledda-Columbano,G.M., Pibiri,M., Molotzu,F., Cossu,C., Sanna,L., Simbula,G., Perra,A. and Columbano,A. (2004) Induction of hepatocyte proliferation by retinoic acid. Carcinogenesis, 25, 2061-2066.
12. Farber,E. and Rubin,H. (1991) Cellular adaptation in the origin and development of cancer. Cancer Res., 51, 2751-2761.
13. Schulte-Hermann,R., Timmermann-Trosiener,L., Barthel,G. and Bursch,W. (1990) DNA synthesis, apoptosis, and phenotypic expression as determinants of growth of altered foci in rat liver during phenobarbital promotion. Cancer Res., 50, 5127-5135.
14. Farber,E. and Sarma,D.S. (1987) Hepatocarcinogenesis: A dynamic cellular perspective. Lab. Invest., 56, 4-22.
15. Rizzi,M.B.S.L., Dagli,M.L.Z., Jordão,A.A.,Jr, Penteado,M.V.C. and Moreno,F.S. (1997). Beta-carotene inhibit persistent and stimulates remodeling gamma GT-positive preneoplastic lesions during early promotion of hepatocarcinogenesis. Int. J. Vitam. Nutr. Res., 67, 415-422.
16. Hsu,S.M., Raine,L. and Fanger,H. (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between (ABC) and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem., 29, 577-580.
17. Wood,G.A., Sarma,D.S. and Archer,M.C. (1999) Resistance to the promotion of glutathione S-transferase 7-7-positive liver lesions in Copenhagen rats. Carcinogenesis, 20, 1169-1175.
18. Mills,J.J., Chari,R.S., Boyer,I.J., Gould,M.N. and Jirtle,R.L. (1995) Induction of apoptosis in liver tumors by the monoterpene perillyl alcohol. Cancer Res., 55, 979-983.
19. Goldsworthy,T.L., Fransson-Steen,R. and Maronpot,R.R. (1996) Importance of and approaches to quantification of hepatocyte apoptosis. Toxicol. Pathol., 24, 24-35.
20. Toledo,L.P., Ong,T.P., Pinho,A.L., Jordão,A.A.,Jr, Vannucchi,H. and Moreno,F.S. (2003) Inhibitory effects of lutein and lycopene on placental glutathione S-transferase-positive preneoplastic lesions and DNA strand breakage induced in Wistar rats by the resistant hepatocyte model of hepatocarcinogenesis. Nutr. Cancer, 47, 62-69.
21. Nadin,S.B., Vargas-Roig,L.M. and Ciocca,D.R. (2001) A silver staining method for single-cell gel assay. J. Histochem. Cytochem., 49, 1183-1186.
22. Espíndola,R.M., Mazzantini,R.P., Ong,T.P., Conti,A.D., Heidor,R. and Moreno,F.S. (2005) Geranylgeraniol and β-ionone inhibit hepatic preneoplastic lesions, cell proliferation, total plasma cholesterol and DNA damage during the initial phases of hepatocarcinogenesis, but only the former inhibits NF-κB activation. Carcinogenesis, 26, 1091-1099.
23. Barbisan,L.F., Scolastici,C., Miyamoto,M., Salvadori,D.M., Ribeiro,L.R., da Eira,A.F. and Camargo,J.L. (2003) Effects of crude extracts of Agaricus blazei on DNA damage and on rat liver carcinogenesis induced by diethylnitrosamine. Genet. Mol. Res., 2, 295-308.
24. Vaghef,H. and Hellman,B. (1998) Detection of styrene and styrene oxide-induced DNA damage in various organs of mice using the comet assay. Pharmacol. Toxicol., 83, 69-74.
25. Tatematsu,M., Mera,Y., Ito,N., Satoh,K. and Sato,K. (1985) Relative merits of immunohistochemical demonstrations of placental, A, B and C forms of glutathione S-transferase and histochemical demonstration of gamma-glutamyl transferase as markers of altered foci during liver carcinogenesis in rats. Carcinogenesis, 11, 1621-1626.
26. Kong,J. and Ringer,D.P. (1996) Quantitative analysis of changes in cell proliferation and apoptosis during preneoplastic and neoplastic stages of hepatocarcinogenesis in rat. Cancer Lett., 105, 241-248.
27. Grasl-Kraupp,B., Ruttkay-Nedecky,B., Mullauer,L., Tarper,H., Huber,W., Bursch,W. and Schulte-Hermann,R. (1997) Inherent increase of apoptosis in liver tumors: Implications for carcinogenesis and tumor regression. Hepatology, 25, 906-912.
28. Okuno,M., Kojima,S. and Moriwaki,H. (2001) Chemoprevention of hepatocellular carcinoma: Concept, progress and perspectives. J. Gastroenterol. Hepatol., 16, 1329-1335.
29. Moreno,F.S., Wu,T.-S., Penteado,M.V.C., Rizzi,M.B.S.L., Jordão,A.A.,Jr, Almeida-Muradian,L.B. and Dagli,M.L. (1995) A comparison of beta-carotene and vitamin A effects on a hepatocarcinogenesis model. Int. J. Vit. Nutr. Res., 65, 1-8.
30. Lotan,R. (1996) Retinoids in cancer chemoprevention. FASEB J., 10, 1031-1039.
31. De Miglio,M.R., Pascale,R.M., Simile,M.M. et al. (2004) Polygenic control of hepatocarcinogenesis in Copenhagen X F344 rats. Int. J. Cancer, 111, 9-16.
32. Garcea,R., Daino,L., Pascale,R., Símile,M.M., Puddu,M., Frassetto,S., Cozzolino,P., Seddaiu,M.A., Gaspa,L. and Feo,F. (1989) Inhibition of promotion and persistent nodule growth by S-adenosyl-L-methionine in rat liver carcinogenesis: Role of remodeling and apoptosis. Cancer Res., 49, 1850-1856.
33. Simile,M.M., Pagnan,G., Pastorino,F. et al. (2005) Chemopreventive N-(4-hydroxyphenyl)retinamide (fenretinide) targets deregulated NF-kB and Mat1A genes in the early stages of rat liver carcinogenesis. Carcinogenesis, 26, 417-427.
34. Bird,R.P. and Good,C.K. The significance of aberrant crypt foci in understanding the pathogenesis of colon cancer. Toxicol. Lett., 112-113, 395-402.
35. Wood,G.A., Korkola,J.E. and Archer,M.C. (2002) Tissue-specific resistance to cancer development in the rat: Phenotypes of tumor-modifier genes. Carcinogenesis, 23, 1-9.
36. Takatsuka,J., Takahashi,N. and De Lucca,L.M. (1996) Retinoic acid metabolism and inhibition of cell proliferation: An unexpected liaison. Cancer Res., 56, 675-678.
37. Briviba,K., Schnabele,K., Schwertle,E., Blockhaus,M. and Rechkemmer,G. (2001) Beta-carotene inhibits growth of human colon carcinoma cells in vitro by induction of apoptosis. Biol. Chem., 382, 1663-1668.
38. Ledda-Columbano,G.M., Perra,A., Loi,R., Shinozuka,H. and Columbano,A. (2000) Cell proliferation induced by triiodothyronine in rat liver is associated with nodule regression and reduction of hepatocellular carcinomas. Cancer Res., 60, 603-609.
39. Simile,M.M., De Miglio,M.R., Calvisi,D., Muroni,M.R., Frau,M., Asara,G., Daino,L., Deiana,L., Pascale,R.M. and Feo,F. (2001) Long-term dehydroepiandroesterone and 16α-fluoro-5-androsten-17-dione administration enhances DNA synthesis and induces expression of c-fos and c-Ha-ras in a selected population of preneoplastic lesions in liver of diethylnitrosamine-initiated rats. Carcinogenesis, 21, 301-308.
40. De Miglio,M.R., Simile,M.M., Muroni,M.R. et al. (2003) Phenotypic reversion of rat neoplastic liver nodules is under genetic control. Int. J. Cancer, 105, 70-75.
41. 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. and Feo,F. (2002) Cell cycle deregulation in liver lesions of rats with and without genetic predisposition to hepatocarcinogenesis. Hepatology, 35, 1341-1350.
42. Sanchez-Perez,Y., Carrasco-Legleu,C., Garcia-Cuellar,C., Perez-Carreon,J., Hernandez-Garcia,S., Salcido-Neyoy,M., Aleman-Lazarini,L. and Villa-Trevino,S. (2005) Oxidative stress in carcinogenesis. Correlation between lipid peroxidation and induction of preneoplastic lesions in rat hepatocarcinogenesis. Cancer Lett., 217, 25-32.
43. Uemura,T., Sai-Kato,K., Takagi,A., Hasegawa,R. and Kurokawa,Y. (1996) Oxidative DNA damage and cell proliferation in the livers of B6C3F1 mice exposed to pentachlorophenol in their diet. Fundam. Appl. Toxicol., 30, 285-289.
44. Collins,A.R. and Horváthová,E. (2001) Oxidative DNA damage, antioxidants and DNA repair: Applications of the comet assay. Biochem. Soc. Trans., 29, 337-341.
45. Palace,V.P., Khaper,N., Qin,Q. and Singal,P.K. (1999) Antioxidant potentials of vitamin A and carotenoids and their relevance to heart disease. Free Radic. Biol. Med., 26, 746-761.