Apocynin and enzymatically modified isoquercitrin suppress the expression of a NADPH oxidase subunit p22phox in steatosis-related preneoplastic liver foci of rats

Experimental and Toxicologic Pathology

Volumn 69, Issue 1, 2017, Pages 9-16

  Yoshida, Toshinori ^a   Murayama, Hirotada ^a   Kawashima, Masahi ^a   Nagahara, Rei ^a   Kangawa, Yumi ^a   Mizukami, Sayaka ^a,b   Kimura, Masayoshi ^a,b   Abe, Hajime ^a,b   Hayashi, Shim mo ^c   Shibutani, Makoto ^a  

^a TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^b GIFU UNIVERSITY   (Japan)

^c SAN EI GEN F F I INC   (Japan)

Author keywords

Apocynin; Enzymatically modified isoquercetin; High fat diet; NADPH oxidase; Preneoplastic liver cell lesions; Two stage hepatocarcinogenesis model

Indexed keywords

ADIPOPHILIN; ALKALINE PHOSPHATASE; APOCYNIN; CASPASE 3; DIETHYLNITROSAMINE; GLUTATHIONE TRANSFERASE; ISOQUERCITRIN; KI 67 ANTIGEN; LC3A PROTEIN; MALACHITE GREEN; MARKER; P22PHOX PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; UNCLASSIFIED DRUG; ACETOPHENONE DERIVATIVE; ENZYME INHIBITOR; P22-PHOX PROTEIN, RAT; QUERCETIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; FATTY LIVER; HYPERLIPIDEMIA; LIVER CANCER; LIVER WEIGHT; MALE; NONHUMAN; PARTIAL HEPATECTOMY; PRECANCER; PRENEOPLASTIC LIVER FOCUS; RAT; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; CARCINOGENESIS; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; EXPERIMENTAL LIVER NEOPLASM; FISCHER 344 RAT; IMMUNOHISTOCHEMISTRY; LIVER; METABOLISM; PATHOLOGY;

ACETOPHENONES; ANIMALS; CARCINOGENESIS; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; FATTY LIVER; IMMUNOHISTOCHEMISTRY; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; MALE; NADPH OXIDASE; PRECANCEROUS CONDITIONS; QUERCETIN; RATS; RATS, INBRED F344;

EID: 85003520604     PISSN: 09402993     EISSN: 16181433     Source Type: Journal    
DOI: 10.1016/j.etp.2016.10.003     Document Type: Article

References (37)

1. Block, K., Gorin, Y., Aiding and abetting roles of NOX oxidases in cellular transformation. Nat. Rev. Cancer 12 (2012), 627–637.
2. Carmona-Cuenca, I., Roncero, C., Sancho, P., Caja, L., Fausto, N., Fernandez, M., et al. Upregulation of the NADPH oxidase NOX4 by TGF-beta in hepatocytes is required for its pro-apoptotic activity. J. Hepatol. 49 (2008), 965–976.
3. Chatterjee, S., Ganini, D., Tokar, E.J., Kumar, A., Das, S., Corbett, J., et al. Leptin is key to peroxynitrite-mediated oxidative stress and Kupffer cell activation in experimental non-alcoholic steatohepatitis. J. Hepatol. 58 (2013), 778–784.
4. Chirino, Y.I., Sanchez-Gonzalez, D.J., Martinez-Martinez, C.M., Cruz, C., Pedraza-Chaverri, J., Protective effects of apocynin against cisplatin-induced oxidative stress and nephrotoxicity. Toxicology 245 (2008), 18–23.
5. Choi, J., Corder, N.L., Koduru, B., Wang, Y., Oxidative stress and hepatic Nox proteins in chronic hepatitis C and hepatocellular carcinoma. Free Radic. Biol. Med. 72 (2014), 267–284.
6. Culp, S.J., Blankenship, L.R., Kusewitt, D.F., Doerge, D.R., Mulligan, L.T., Beland, F.A., Toxicity and metabolism of malachite green and leucomalachite green during short-term feeding to Fischer 344 rats and B6C3F1 mice. Chem. Biol. Interact. 122 (1999), 153–170.
7. Czaja, M.J., Ding, W.X., Donohue, T.M. Jr., Friedman, S.L., Kim, J.S., Komatsu, M., et al. Functions of autophagy in normal and diseased liver. Autophagy 9 (2013), 1131–1158.
8. de Lima, V.M., Oliveira, C.P., Alves, V.A., Chammas, M.C., Oliveira, E.P., Stefano, J.T., et al. A rodent model of NASH with cirrhosis, oval cell proliferation and hepatocellular carcinoma. J. Hepatol. 49 (2008), 1055–1061.
9. Duval, C., Thissen, U., Keshtkar, S., Accart, B., Stienstra, R., Boekschoten, M.V., et al. Adipose tissue dysfunction signals progression of hepatic steatosis towards nonalcoholic steatohepatitis in C57BL/6 mice. Diabetes 59 (2010), 3181–3191.
10. Fernandes, C., Rao, K.V., Enhanced expression of low molecular weight keratins during progressive diethylnitrosamine-induced hepatocarcinogenesis in rats is associated with the presence of high levels of gamma-glutamyl transpeptidase and glycogen-deficient islands. Cancer Lett. 59 (1991), 211–219.
11. Gabele, E., Dostert, K., Hofmann, C., Wiest, R., Scholmerich, J., Hellerbrand, C., et al. DSS induced colitis increases portal LPS levels and enhances hepatic inflammation and fibrogenesis in experimental NASH. J. Hepatol. 55 (2011), 1391–1399.
12. Gauthier, M.S., Favier, R., Lavoie, J.M., Time course of the development of non-alcoholic hepatic steatosis in response to high-fat diet-induced obesity in rats. Br. J. Nutr. 95 (2006), 273–281.
13. Grasselli, E., Voci, A., Pesce, C., Canesi, L., Fugassa, E., Gallo, G., et al. PAT protein mRNA expression in primary rat hepatocytes: effects of exposure to fatty acids. Int. J. Mol. Med. 25 (2010), 505–512.
14. Gupta, S., Sundarrajan, M., Rao, K.V., Tumor promotion by metanil yellow and malachite green during rat hepatocarcinogenesis is associated with dysregulated expression of cell cycle regulatory proteins. Teratog. Carcinog. Mutagen., 2003, 301–312.
15. Gupte, R.S., Floyd, B.C., Kozicky, M., George, S., Ungvari, Z.I., Neito, V., et al. Synergistic activation of glucose-6-phosphate dehydrogenase and NAD(P)H oxidase by Src kinase elevates superoxide in type 2 diabetic, Zucker fa/fa, rat liver. Free Radic. Biol. Med. 47 (2009), 219–228.
16. Hara, S., Morita, R., Ogawa, T., Segawa, R., Takimoto, N., Suzuki, K., et al. 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. Exp. Toxicol. Pathol. 66 (2014), 225–234.
17. Ibrahim, M.A., Kelleni, M., Geddawy, A., Nonalcoholic fatty liver disease: current and potential therapies. Life Sci. 92 (2013), 114–118.
18. Ito, N., Tamano, S., Shirai, T., A medium-term rat liver bioassay for rapid in vivo detection of carcinogenic potential of chemicals. Cancer Sci. 94 (2003), 3–8.
19. Kalyanaraman, B., Teaching the basics of redox biology to medical and graduate students: oxidants, antioxidants and disease mechanisms. Redox Biol. 1 (2013), 244–257.
20. Kleiner, D.E., Brunt, E.M., Van Natta, M., Behling, C., Contos, M.J., Cummings, O.W., et al. Nonalcoholic Steatohepatitis Clinical Research Network: design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41 (2005), 1313–1321.
21. Kojima, S., Sasaki, J., Tomita, M., Saka, M., Ishizuka, K., Kawakatsu, H., et al. Multiple organ toxicity, including hypochromic anemia, following repeated dose oral administration of phenobarbital (PB) in rats. J. Toxicol. Sci. 34 (2009), 527–539.
22. 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 beta-naphthoflavone involving TNFalpha-signaling due to oxidative cellular stress in rats. Toxicology 283 (2011), 8–17.
23. Lalles, J.P., Orozco-Solis, R., Bolanos-Jimenez, F., de Coppet, P., Le Drean, G., Segain, J.P., Perinatal undernutrition alters intestinal alkaline phosphatase and its main transcription factors KLF4 and Cdx1 in adult offspring fed a high-fat diet. J. Nutr. Biochem. 23 (2012), 1490–1497.
24. Levin, I., Petrasek, J., Szabo, G., The presence of p47phox in liver parenchymal cells is a key mediator in the pathogenesis of alcoholic liver steatosis. Alcohol. Clin. Exp. Res. 36 (2012), 1397–1406.
25. Makino, T., Shimizu, R., Kanemaru, M., Suzuki, Y., Moriwaki, M., Mizukami, H., Enzymatically modified isoquercitrin, alpha-oligoglucosyl quercetin 3-O-glucoside, is absorbed more easily than other quercetin glycosides or aglycone after oral administration in rats. Biol. Pharm. Bull. 32 (2009), 2034–2040.
26. Marcolin, E., San-Miguel, B., Vallejo, D., Tieppo, J., Marroni, N., Gonzalez-Gallego, J., et al. Quercetin treatment ameliorates inflammation and fibrosis in mice with nonalcoholic steatohepatitis. J. Nutr. 142 (2012), 1821–1828.
27. Montezano, A.C., Touyz, R.M., Reactive oxygen species, vascular Noxs, and hypertension: focus on translational and clinical research. Antioxid. Redox Signal. 20 (2014), 164–182.
28. 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. 85 (2011), 1475–1484.
29. Murota, K., Matsuda, N., Kashino, Y., Fujikura, Y., Nakamura, T., Kato, Y., et al. alpha-Oligoglucosylation of a sugar moiety enhances the bioavailability of quercetin glucosides in humans. Arch. Biochem. Biophys. 501 (2010), 91–97.
30. 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. 84 (2010), 143–153.
31. Pan, M.H., Lai, C.S., Tsai, M.L., Ho, C.T., Chemoprevention of nonalcoholic fatty liver disease by dietary natural compounds. Mol. Nutr. Food Res. 58 (2014), 147–171.
32. Pisonero-Vaquero, S., Martinez-Ferreras, A., Garcia-Mediavilla, M.V., Martinez-Florez, S., Fernandez, A., Benet, M., et al. Quercetin ameliorates dysregulation of lipid metabolism genes via the PI3K/AKT pathway in a diet-induced mouse model of nonalcoholic fatty liver disease. Mol. Nutr. Food Res. 59 (2015), 879–893.
33. Sheedfar, F., Di Biase, S., Koonen, D., Vinciguerra, M., Liver diseases and aging: friends or foes?. Aging Cell 12 (2013), 950–954.
34. 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 beta-naphthoflavone. Toxicology 268 (2010), 213–218.
35. Sundarrajan, M., Fernandis, A.Z., Subrahmanyam, G., Prabhudesai, S., Krishnamurthy, S.C., Rao, K.V., Overexpression of G1/S cyclins and PCNA and their relationship to tyrosine phosphorylation and dephosphorylation during tumor promotion by metanil yellow and malachite green. Toxicol. Lett. 116 (2000), 119–130.
36. Sundarrajan, M., Prabhudesai, S., Krishnamurthy, S.C., Rao, K.V., Effect of metanil yellow and malachite green on DNA synthesis in N-nitrosodiethylamine induced preneoplastic rat livers. Indian J. Exp. Biol. 39 (2001), 845–852.
37. Younossi, Z.M., Review article: current management of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis. Aliment. Pharmacol. Ther. 28 (2008), 2–12.