Tumor suppression effects of bilberry extracts and enzymatically modified isoquercitrin in early preneoplastic liver cell lesions induced by piperonyl butoxide promotion in a two-stage rat hepatocarcinogenesis model

Experimental and Toxicologic Pathology

Volumn 66, Issue 5-6, 2014, Pages 225-234

  Hara, Shintaro ^a   Morita, Reiko ^a,b   Ogawa, Takashi ^a   Segawa, Risa ^a   Takimoto, Norifumi ^a   Suzuki, Kazuhiko ^a   Hamadate, Naobumi ^c   Hayashi, Shim mo ^d   Odachi, Ayano ^a   Ogiwara, Isao ^a   Shibusawa, Sakae ^a   Yoshida, Toshinori ^a   Shibutani, Makoto ^a  

^a TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^b GIFU UNIVERSITY   (Japan)

^c Egao Co Ltd   (Japan)

^d SAN EI GEN F F I INC   (Japan)

Author keywords

Bilberry extracts (BBE); Cell proliferation; Enzymatically modified isoquercitrin (EMIQ); Liver tumor promotion; Phosphatase and tensin homolog (PTEN) Akt signaling; Transforming growth factor (TGF) Smad signaling

Indexed keywords

ANTINEOPLASTIC AGENT; DIETHYLNITROSAMINE; ENZYMATICALLY MODIFIED ISOQUERCITRIN; GLUTATHIONE S TRANSFERASE PLACENTAL FORM; GLUTATHIONE TRANSFERASE; ISOQUERCITRIN; KI 67 ANTIGEN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOPROTEIN; PIPERONYL BUTOXIDE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; SMAD PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VACCINIUM MYRTILLUS EXTRACT; PLANT EXTRACT; QUERCETIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER MODEL; CANCER PREVENTION; CONTROLLED STUDY; DRUG MEGADOSE; LIVER CANCER; LIVER CARCINOGENESIS; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRECANCER; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; APOPTOSIS; CELL PROLIFERATION; CHEMICALLY INDUCED; CHEMISTRY; COCARCINOGENESIS; DRUG EFFECTS; FISCHER 344 RAT; GLYCOSYLATION; ISOLATION AND PURIFICATION; LIVER NEOPLASMS, EXPERIMENTAL; METABOLISM; PATHOLOGY; PRECANCEROUS CONDITIONS; TOXICITY; VACCINIUM MYRTILLUS;

ANIMALS; ANTICARCINOGENIC AGENTS; APOPTOSIS; CELL PROLIFERATION; COCARCINOGENESIS; DIETHYLNITROSAMINE; GLYCOSYLATION; LIVER NEOPLASMS, EXPERIMENTAL; MALE; OXIDATIVE STRESS; PIPERONYL BUTOXIDE; PLANT EXTRACTS; PRECANCEROUS CONDITIONS; QUERCETIN; RATS, INBRED F344; VACCINIUM MYRTILLUS;

EID: 84901060709     PISSN: 09402993     EISSN: 16181433     Source Type: Journal    
DOI: 10.1016/j.etp.2014.02.002     Document Type: Article

References (40)

1. Afaq F., Saleem M., Krueger C.G., Reed J.D., Mukhtar H. Anthocyanin- and hydrolyzable tannin-rich pomegranate fruit extract modulates MAPK and NF-κB pathways and inhibits skin tumorigenesis in CD-1 mice. Int J Cancer 2005, 113:423-433.
2. Aggarwal B.B., Shishodia S. Molecular targets of dietary agents for prevention and therapy of cancer. Biochem Pharmacol 2006, 71:1397-1421.
3. Ajiboye T.O., Salawu N.A., Yakubu M.T., Oladiji A.T., Akanji M.A., Okogun J.I. Antioxidant and drug detoxification potentials of Hibiscus sabdariffa anthocyanin extract. Drug Chem Toxicol 2011, 34:109-115.
4. Akiyama T., Washino T., Yamada T., Koda T., Maitani T. Constituents of enzymatically modified isoquercitrin and enzymatically modified rutin (extract). J Food Hyg Soc Jpn 2000, 41:54-60.
5. Bishayee A., Mbimba T., Thoppil R.J., Háznagy-Radnai E., Sipos P., Darvesh A.S., et al. Anthocyanin-rich black currant (Ribes nigrum L.) extract affords chemoprevention against diethylnitrosamine-induced hepatocellular carcinogenesis in rats. J Nutr Biochem 2011, 22:1035-1046.
6. Bishayee A., Thoppil R.J., Mandal A., Darvesh A.S., Ohanyan V., Meszaros J.G., et al. Black currant phytoconstituents exert chemoprevention of diethylnitrosamine-initiated hepatocarcinogenesis by suppression of the inflammatory response. Mol Carcinog 2013, 52:304-317.
7. Brader S., Eccles S.A. Phosphoinositide 3-kinase signalling pathways in tumor progression, invasion and angiogenesis. Tumori 2004, 90:2-8.
8. Bunea A., Ruginǎ D., Sconţa Z., Pop R.M., Pintea A., Socaciu C., et al. Anthocyanin determination in blueberry extracts from various cultivars and their antiproliferative and apoptotic properties in B16-F10 metastatic murine melanoma cells. Phytochemistry 2013, 95:436-444.
9. Butler W.H., Gabriel K.L., Osimitz T.G., Preiss F.J. Oncogenicity studies of piperonyl butoxide in rats and mice. Hum Exp Toxicol 1998, 17:323-330.
10. Formica J.V., Regelson W. Review of the biology of Quercetin and related bioflavonoids. Food Chem Toxicol 1995, 33:1061-1080.
11. Fujii Y., Kimura M., Ishii Y., Yamamoto R., Morita R., Hayashi S.M., et al. Effect of enzymatically modified isoquercitrin on preneoplastic liver cell lesions induced by thioacetamide promotion in a two-stage hepatocarcinogenesis model using rats. Toxicology 2013, 8:30-40.
12. He J., Giusti M.M. Anthocyanins: natural colorants with health-promoting properties. Annu Rev Food Sci Technol 2010, 1:163-187.
13. Ichimura R., Mizukami S., Takahashi M., Taniai E., Kemmochi S., Mitsumori K., et al. Disruption of Smad-dependent signaling for growth of GST-P-positive lesions from the early stage in a rat two-stage hepatocarcinogenesis model. Toxicol Appl Pharmacol 2010, 246:128-140.
14. Ikushima H., Miyazono K. Cellular context-dependent colors of transforming growth factor-β signaling. Cancer Sci 2010, 101:306-312.
15. Ito N., Tamano S., Shirai T. A medium-term rat liver bioassay for rapid in vivo detection of carcinogenic potential of chemicals. Cancer Sci 2003, 94:3-8.
16. Kawai M., Saegusa Y., Dewa Y., Nishimura J., Kemmochi S., Harada T., et al. Elevation of cell proliferation via generation of reactive oxygen species by piperonyl butoxide contributes to its liver tumor-promoting effects in mice. Arch Toxicol 2010, 84:155-164.
17. Kimura M., Fujii Y., Yamamoto R., Yafune A., Hayashi S.M., Suzuki K., et al. Involvement of multiple cell cycle aberrations in early preneoplastic liver cell lesions by tumor promotion with thioacetamide in a two-stage rat hepatocarcinogenesis model. Exp Toxicol Pathol 2013, 65:979-988.
18. Kinoshita A., Wanibuchi H., Morimura K., Wei M., Shen J., Imaoka S., et al. Phenobarbital at low dose exerts hormesis in rat hepatocarcinogenesis by reducing oxidative DNA damage, altering cell proliferation, apoptosis and gene expression. Carcinogenesis 2003, 24:1389-1399.
19. Kuwata K., Shibutani M., Hayashi H., Shimamoto K., Hayashi S.M., Suzuki K., et al. Concomitant apoptosis and regeneration of liver cells as a mechanism of liver-tumor promotion by β-naphthoflavone involving TNFα-signaling due to oxidative cellular stress in rats. Toxicology 2011, 283:8-17.
20. Lala G., Malik M., Zhao C., He J., Kwon Y., Giusti M.M., et al. Anthocyanin-rich extracts inhibit multiple biomarkers of colon cancer in rats. Nutr Cancer 2006, 54:84-93.
21. Lankinen M., Schwab U., Kolehmainen M., Paananen J., Poutanen K., Mykkänen H., et al. Whole grain products, fish and bilberries alter glucose and lipid metabolism in a randomized, controlled trial: the Sysdimet study. PLoS ONE 2011, 6:e22646.
22. T method. Methods 2001, 25:402-408.
23. Maehama T., Taylor G.S., Dixon J.E. PTEN and myotubularin: novel phosphoinositide phosphatases. Annu Rev Biochem 2001, 70:247-279.
24. Morita R., Shimamoto K., Ishii Y., Kuwata K., Ogawa B., Imaoka M., et al. Suppressive effect of enzymatically modified isoquercitrin on phenobarbital-induced liver tumor promotion in rats. Arch Toxicol 2011, 85:1475-1484.
25. Muguruma M., Unami A., Kanki M., Kuroiwa Y., Nishimura J., Dewa Y., et al. Possible involvement of oxidative stress in piperonyl butoxide induced hepatocarcinogenesis in rats. Toxicology 2007, 236:61-75.
26. Nishikawa T., Wanibuchi H., Ogawa M., Kinoshita A., Morimura K., Hiroi T., et al. Promoting effects of monomethylarsonic acid, dimethylarsinic acid and trimethylarsine oxide on induction of rat liver preneoplastic glutathione S-transferase placental form positive foci: a possible reactive oxygen species mechanism. Int J Cancer 2002, 100:136-139.
27. Nishimura J., Saegusa Y., Dewa Y., Jin M., Kawai M., Kemmochi S., et al. Antioxidant enzymatically modified isoquercitrin or melatonin supplementation reduces oxidative stress-mediated hepatocellular tumor promotion of oxfendazole in rats. Arch Toxicol 2010, 84:143-153.
28. Ogawa K., Oyagi A., Tanaka J., Kobayashi S., Hara H. The protective effect and action mechanism of Vaccinium myrtillus L. on gastric ulcer in mice. Phytother Res 2011, 25:1160-1165.
29. Puntarulo S., Cederbaum A.I. Production of reactive oxygen species by microsomes enriched in specific human cytochrome P450 enzymes. Free Radic Biol Med 1998, 24:1324-1330.
30. Rossmanith W., Schulte-Hermann R. Biology of transforming growth factor β in hepatocarcinogenesis. Microsc Res Tech 2000, 52:430-436.
31. Serron S.C., Dwivedi N., Backes W.L. Ethylbenzene induces microsomal oxygen free radical generation: antibody-directed characterization of the responsible cytochrome P450 enzymes. Toxicol Appl Pharmacol 2000, 164:305-311.
32. Shimada Y., Dewa Y., Ichimura R., Suzuki T., Mizukami S., Hayashi S.M., et al. Antioxidant enzymatically modified isoquercitrin suppresses the development of liver preneoplastic lesions in rats induced by β-naphthoflavone. Toxicology 2010, 268:213-218.
33. Surh Y.J. Cancer chemoprevention with dietary phytochemicals. Nat Rev Cancer 2003, 3:768-780.
34. Takahashi O., Oishi S., Fujitani T., Tanaka T., Yoneyama M. Piperonyl butoxide induces hepatocellular carcinoma in male CD-1 mice. Arch Toxicol 1994, 68:467-469.
35. Taniai E., Kawai M., Dewa Y., Nishimura J., Harada T., Saegusa Y., et al. Crosstalk between PTEN/Akt2 and TGFβ signaling involving EGF receptor down-regulation during the tumor promotion process from the early stage in a rat two-stage hepatocarcinogenesis model. Cancer Sci 2009, 100:813-820.
36. Tasaki M., Umemura T., Suzuki Y., Hibi D., Inoue T., Okamura T., et al. Oxidative DNA damage and reporter gene mutation in the livers of gpt delta rats given non-genotoxic hepatocarcinogens with cytochrome P450-inducible potency. Cancer Sci 2010, 101:2525-2530.
37. Waxman D.J., Azaroff L. Phenobarbital induction of cytochrome P-450 gene expression. Biochem J 1992, 281:577-592.
38. West K.A., Castillo S.S., Dennis P.A. Activation of the PI3K/Akt pathway and chemotherapeutic resistance. Drug Resist Updat 2002, 5:234-248.
39. Yang F., Chen H., Liu Y., Yin K., Wang Y., Li X., et al. Doxorubicin caused apoptosis of mesenchymal stem cells via p38, JNK and p53 pathway. Cell Physiol Biochem 2013, 32:1072-1082.
40. Yoshihara S., Makishita M., Suauki N., Ohta S. Metabolic activation of bisphenol A by rat liver S9 fraction. Toxicol Sci 2001, 62:221-227.