Effects of dietary fish oil on cytochrome P450 3A expression in the liver of SHR/NDmcr-cp (cp/cp) rats, an animal model for metabolic syndrome
Pathophysiological and nutritional conditions often affect the expression of drug-metabolizing enzymes. SHR/NDmcr-cp (cp/cp) rats (SHR/NDcp) are highly suitable as a metabolic syndrome (MS) model. Nevertheless, little is known about the expression profile of cytochrome P450 (CYP) in the liver of SHR...
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| Published in | Fundamental Toxicological Sciences Vol. 2; no. 3; pp. 127 - 135 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
The Japanese Society of Toxicology
2015
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| Subjects | |
| Online Access | Get full text |
| ISSN | 2189-115X 2189-115X |
| DOI | 10.2131/fts.2.127 |
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| Abstract | Pathophysiological and nutritional conditions often affect the expression of drug-metabolizing enzymes. SHR/NDmcr-cp (cp/cp) rats (SHR/NDcp) are highly suitable as a metabolic syndrome (MS) model. Nevertheless, little is known about the expression profile of cytochrome P450 (CYP) in the liver of SHR/NDcp. We thus attempted to clarify the expression profile of CYP genes and the effect of fish oil (FO) on this profile in the liver of SHR/NDcp. Lower levels of CYP3A2 mRNA and CYP3A activity (testosterone 6β-hydroxylation) were distinctive features in SHR/NDcp compared with their controls (Wistar Kyoto rats (WKY), spontaneously hypertensive rats (SHR), stroke-prone SHR and lean littermates of SHR/NDcp). Differently from CYP3A2, the expression of other CYP isoforms was largely unchanged in SHR/NDcp. The changes in CYP profile observed in SHR/NDcp are similar to those of patients with diabetes and simple hepatic steatosis. Feeding on FO at a high dose (18.8% in the diet) up-regulated CYP3A2 gene expression and CYP3A activity in the liver; the extent of these increases was greater in SHR/NDcp than in WKY and lean littermates of SHR/NDcp. This effect was not observed with FO at a normal dose (5% in the diet). These results indicate that, in the context of the CYP profile, SHR/NDcp is an animal model that is suitable for studying MS and imply that FO intake is critical in determining the efficacy or adverse effects of drugs in patients with MS. |
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| AbstractList | Pathophysiological and nutritional conditions often affect the expression of drug-metabolizing enzymes. SHR/NDmcr-cp (cp/cp) rats (SHR/NDcp) are highly suitable as a metabolic syndrome (MS) model. Nevertheless, little is known about the expression profile of cytochrome P450 (CYP) in the liver of SHR/NDcp. We thus attempted to clarify the expression profile of CYP genes and the effect of fish oil (FO) on this profile in the liver of SHR/NDcp. Lower levels of CYP3A2 mRNA and CYP3A activity (testosterone 6β-hydroxylation) were distinctive features in SHR/NDcp compared with their controls (Wistar Kyoto rats (WKY), spontaneously hypertensive rats (SHR), stroke-prone SHR and lean littermates of SHR/NDcp). Differently from CYP3A2, the expression of other CYP isoforms was largely unchanged in SHR/NDcp. The changes in CYP profile observed in SHR/NDcp are similar to those of patients with diabetes and simple hepatic steatosis. Feeding on FO at a high dose (18.8% in the diet) up-regulated CYP3A2 gene expression and CYP3A activity in the liver; the extent of these increases was greater in SHR/NDcp than in WKY and lean littermates of SHR/NDcp. This effect was not observed with FO at a normal dose (5% in the diet). These results indicate that, in the context of the CYP profile, SHR/NDcp is an animal model that is suitable for studying MS and imply that FO intake is critical in determining the efficacy or adverse effects of drugs in patients with MS. |
| Author | Yamamoto, Asami Okazaki, Mari Sakamoto, Takeshi Taguchi, Hiroki Yamazaki, Tohru Ohki, Takashi Kudo, Naomi Mitsumoto, Atsushi Kawashima, Yoichi |
| Author_xml | – sequence: 1 fullname: Ohki, Takashi organization: School of Pharmaceutical Sciences, Josai University – sequence: 1 fullname: Okazaki, Mari organization: School of Pharmaceutical Sciences, Josai University – sequence: 1 fullname: Mitsumoto, Atsushi organization: Faculty of Pharmaceutical Sciences, Josai International University – sequence: 1 fullname: Yamazaki, Tohru organization: School of Pharmaceutical Sciences, Josai University – sequence: 1 fullname: Kawashima, Yoichi organization: School of Pharmaceutical Sciences, Josai University – sequence: 1 fullname: Yamamoto, Asami organization: School of Pharmaceutical Sciences, Josai University – sequence: 1 fullname: Taguchi, Hiroki organization: School of Pharmaceutical Sciences, Josai University – sequence: 1 fullname: Kudo, Naomi organization: School of Pharmaceutical Sciences, Josai University – sequence: 1 fullname: Sakamoto, Takeshi organization: School of Pharmaceutical Sciences, Josai University |
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| Cites_doi | 10.1016/S0022-3565(25)13127-3 10.1196/annals.1333.086 10.1016/S0090-9556(24)15346-9 10.1007/s11745-013-3786-2 10.1111/j.1476-5381.2011.01270.x 10.1006/bbrc.1999.0202 10.1016/j.etp.2010.09.006 10.1016/j.cgh.2006.12.021 10.1248/bpb.35.184 10.1124/dmd.105.007088 10.1053/jhep.2003.50342 10.1016/S0021-9258(19)52451-6 10.2337/dc09-1235 10.1042/BJ20080740 10.1016/S0140-6736(05)67402-8 10.1016/S0140-6736(05)66378-7 10.1146/annurev.pharmtox.41.1.123 10.1124/dmd.112.045112 10.1248/bpb.30.1586 10.2337/db09-1554 10.1021/mp700114j 10.1007/s11745-013-3839-6 10.1146/annurev.pharmtox.39.1.1 10.1006/abbi.1999.1351 10.1093/ajcn/83.6.1499S 10.1016/j.hepres.2005.10.001 10.1126/science.286.5439.487 10.1079/BJN19860088 10.3945/jn.109.111567 10.1248/bpb.29.1634 |
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| References | Emery, M.G., Fisher, J.M., Chien, J.Y., Kharasch, E.D., Dellinger, E.P., Kowdley, K.V. and Thummel, K.E. (2003): CYP2E1 activity before and after weight loss in morbidly obese subjects with nonalcoholic fatty liver disease. Hepatology, 38, 428-435. Tanaka, S., Yamazaki, T., Asano, S., Mitsumoto, A., Kobayashi, D., Kudo, N. and Kawashima, Y. (2013): Increased lipid synthesis and decreased β-oxidation in the liver of SHR/NDmcr-cp (cp/cp) rats, an animal model of metabolic syndrome. Lipids, 48, 1115-1134. Tanaka, S., Yagi, Y., Yamazaki, T., Mitsumoto, A., Kobayashi, D., Kudo, N. and Kawashima, Y. (2012): Characterization of fatty acid profile in the liver of SHR/NDmcr-cp (cp/cp) rats, a model of the metabolic syndrome. Biol. Pharm. Bull., 35, 184-191. Miyata, T., Yamamoto, M. and Izuhara, Y. (2005): From molecular footprints of disease to new therapeutic interventions in diabetic nephropathy. Ann. N.Y. Acad. Sci., 1043, 740-749. Sueyoshi, T. and Negishi, M. (2001) : Phenobarbital response elements of cytochrome P450 genes and nuclear receptors. Annu. Rev. Pharmacol. Toxicol., 41, 123-143. Eckel, R.H., Grundy, S.M. and Zimmet, P.Z. (2005): The metabolic syndrome. Lancet, 365, 1415-1428. Aleksunes, L.M. and Klaassen, C.D. (2012): Coordinated regulation of hepatic phase I and II drug-metabolizing genes and transporters using AhR-, CAR-, PXR-, PPARα-, and Nrf2-null mice. Drug Metab. Dispos., 40, 1366-1379. Carpentier, Y.A., Portois, L. and Malaisse, W.J. (2006): n-3 Fatty acids and the metabolic syndrome. Am. J. Clin. Nutr., 83, 1499S-1504S. Hirunpanich, V., Sethabouppha, B. and Sato, H. (2007): Inhibitory effects of saturated and polyunsaturated fatty acids on the cytochrome P450 3A activity in rat liver microsomes. Biol. Pharm. Bull., 30, 1586-1588. Waxman, D.J. (1999): P450 gene induction by structurally diverse xenochemicals: central role of nuclear receptors CAR, PXR, and PPAR. Arch. Biochem. Biophys., 369, 11-23. Saraswathi, V., Morrow, J.D. and Hasty, A.H. (2009): Dietary fish oil exerts hypolipidemic effects in lean and insulin sensitizing effects in obese LDLR-/- mice. J. Nutr., 139, 2380-2386. Cunnane, S.C., McAdoo, K.R. and Horrobin, D.F. (1986): n-3 Essential fatty acids decrease weight gain in genetically obese mice. Br. J. Nutr., 56, 87-95. Dostalek, M., Court, M.H., Yan, B. and Akhlaghi, F. (2011): Significantly reduced cytochromeP450 3A4 expression and activity in liver from humans with diabetes mellitus. Br. J. Pharmacol., 163, 937-947. Cheng, Q., Aleksunes, L.M., Manautou, J.E., Cherrington, N.J., Scheffer, G.L., Yamasaki, H. and Slitt, A.L. (2008): Drug-metabolizing enzyme and transporter expression in a mouse model of diabetes and obesity. Mol. Pharm., 5, 77-91. Karahashi, M., Ishii, F., Yamazaki, T., Imai, K., Mitsumoto, A., Kawashima,Y. and Kudo, N. (2013): Up-regulation of stearoyl-CoA desaturase 1 increases liver MUFA content in obese Zucker but not Goto-Kakizaki rats. Lipids, 48, 457-467. Guo, L.-Q., Fukuda, K., Ohta, T. and Yamazoe, Y. (2000): Role of furanocoumarin derivatives on grapefruit juice-mediated inhibition of human CYP3A activity. Drug Metab. Dispos., 28, 766-771. Finn, R.D., Henderson, C.J., Scott, C.L. and Wolf, C.R. (2009): Unsaturated fatty acid regulation of cytochrome P450 expression via a CAR-dependent pathway. Biochem. J., 417, 43-54. Alberti, K.G., Zimmet, P., Shaw, J.; IDF Epidemiology Task Force Consensus Group (2005): The metabolic syndrome - a new worldwide definition. Lancet, 366, 1059-1062. Guengerich, F.P. (1999): Cytochrome P-450 3A4: Regulation and role in drug metabolism. Annu. Rev. Pharmacol. Toxicol., 39, 1-17. Sato, A., Kawano, H., Notsu, T., Ohta, M., Nakakuki, M., Mizuguchi, K., Itoh, M., Suganami, T. and Ogawa, Y. (2010): Antiobesity effect of eicosapentaenoic acid in high-fat/high-sucrose diet-induced obesity. Importance of hepatic lipogenesis. Diabetes, 59, 2495-2504. Orellana, M., Rodrigo, R., Valera, N., Araya, J., Poniachik, J., Csendes, A., Smok, G. and Videla, L.A. (2006): Relationship between in vivo chlorzoxazone hydroxylation, hepatic cytochrome P450 2E1 content and liver injury in obese non-alcoholic fatty liver disease patients. Hepatol. Res., 34, 57-63. Hirunpanich, V., Katagi, J., Sethabouppha, B. and Sato, H. (2006): Demonstration of docosahexaenoic acid as a bioavailability enhancer for CYP3A substrates: in vitro and in vivo evidence using cyclosporine in rats. Drug Metab. Dispos., 34, 305-310. Yoshinari, K., Takagi, S., Sugitani, J. and Miwa, M. (2006): Changes in the expression of cytochrome P450 and nuclear receptors in the liver of genetically diabetic db/db mice. Biol. Pharm. Bull., 29, 1634-1638. Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951): Protein measurement with the folin phenol reagent. J. Biol. Chem., 193, 265-275. Kawai, K., Sakairi, T., Harada, S., Shinozuka, J., Ide, M., Sato, H., Tanaka, M., Toriumi, W. and Kume, E. (2012): Diet modification and its influence on metabolic and related pathological alterations in the SHR/NDmcr-cp rat, an animal model of the metabolic syndrome. Exp. Toxicol. Pathol., 64, 333-338. Enriquez, A., Leclercq, I., Farrell, G.C. and Robertson, G. (1999): Altered expression of hepatic CYP2E1 and CYP4A in obese, diabetic ob/ob mice, and fa/fa Zucker rats. Biochem. Biophys. Res. Commun., 255, 300-306. Evans, W.E. and Relling, M.V. (1999): Pharmacogenomics: Translating functional genomics into rational therapeutics. Science, 286, 487-491. Kolwankar, D., Vuppalanchi, R., Ethell, B., Jones, D.R., Wrighton, S.A., Hall, S.D. and Chalasani, N. (2007): Association between nonalcoholic hepatic steatosis and hepatic cytochrome P-450 3A activity. Clin. Gastroenterol. Hepatol., 5, 388-393. Belalcazar, L.M., Reboussin, D.M., Haffner, S.M., Reeves, R.S., Schwenke, D.C., Hoogeveen, R.C., Pi-Sunyer, F.X. and Ballantyne, C.M. (2010): Marine ω-3 fatty acid intake. Associations with cardiometabolic risk and response to weight loss intervention in the Look AHEAD (action for health in diabetes) study. Diabetes Care, 33, 197-199. Brunner, L.J., Bennett, W.M. and Koop, D.R. (1996): Selective suppression of rat hepatic microsomal activity during chronic cyclosporine nephrotoxicity. J. Pharmacol. Exp. Ther., 277, 1710-1718. Koletsky, S. (1975): Pathologic findings and laboratory data in a new strain of obese hypertensive rats. Am. J. Pathol., 80, 129-142. 22 23 24 25 26 27 28 29 30 31 10 11 12 13 14 15 16 17 18 19 1 2 3 4 5 6 7 8 9 20 21 |
| References_xml | – reference: Cheng, Q., Aleksunes, L.M., Manautou, J.E., Cherrington, N.J., Scheffer, G.L., Yamasaki, H. and Slitt, A.L. (2008): Drug-metabolizing enzyme and transporter expression in a mouse model of diabetes and obesity. Mol. Pharm., 5, 77-91. – reference: Miyata, T., Yamamoto, M. and Izuhara, Y. (2005): From molecular footprints of disease to new therapeutic interventions in diabetic nephropathy. Ann. N.Y. Acad. Sci., 1043, 740-749. – reference: Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951): Protein measurement with the folin phenol reagent. J. Biol. Chem., 193, 265-275. – reference: Eckel, R.H., Grundy, S.M. and Zimmet, P.Z. (2005): The metabolic syndrome. Lancet, 365, 1415-1428. – reference: Carpentier, Y.A., Portois, L. and Malaisse, W.J. (2006): n-3 Fatty acids and the metabolic syndrome. Am. J. Clin. Nutr., 83, 1499S-1504S. – reference: Dostalek, M., Court, M.H., Yan, B. and Akhlaghi, F. (2011): Significantly reduced cytochromeP450 3A4 expression and activity in liver from humans with diabetes mellitus. Br. J. Pharmacol., 163, 937-947. – reference: Tanaka, S., Yagi, Y., Yamazaki, T., Mitsumoto, A., Kobayashi, D., Kudo, N. and Kawashima, Y. (2012): Characterization of fatty acid profile in the liver of SHR/NDmcr-cp (cp/cp) rats, a model of the metabolic syndrome. Biol. Pharm. Bull., 35, 184-191. – reference: Orellana, M., Rodrigo, R., Valera, N., Araya, J., Poniachik, J., Csendes, A., Smok, G. and Videla, L.A. (2006): Relationship between in vivo chlorzoxazone hydroxylation, hepatic cytochrome P450 2E1 content and liver injury in obese non-alcoholic fatty liver disease patients. Hepatol. Res., 34, 57-63. – reference: Brunner, L.J., Bennett, W.M. and Koop, D.R. (1996): Selective suppression of rat hepatic microsomal activity during chronic cyclosporine nephrotoxicity. J. Pharmacol. Exp. Ther., 277, 1710-1718. – reference: Alberti, K.G., Zimmet, P., Shaw, J.; IDF Epidemiology Task Force Consensus Group (2005): The metabolic syndrome - a new worldwide definition. Lancet, 366, 1059-1062. – reference: Guengerich, F.P. (1999): Cytochrome P-450 3A4: Regulation and role in drug metabolism. Annu. Rev. Pharmacol. Toxicol., 39, 1-17. – reference: Sueyoshi, T. and Negishi, M. (2001) : Phenobarbital response elements of cytochrome P450 genes and nuclear receptors. Annu. Rev. Pharmacol. Toxicol., 41, 123-143. – reference: Evans, W.E. and Relling, M.V. (1999): Pharmacogenomics: Translating functional genomics into rational therapeutics. Science, 286, 487-491. – reference: Kolwankar, D., Vuppalanchi, R., Ethell, B., Jones, D.R., Wrighton, S.A., Hall, S.D. and Chalasani, N. (2007): Association between nonalcoholic hepatic steatosis and hepatic cytochrome P-450 3A activity. Clin. Gastroenterol. Hepatol., 5, 388-393. – reference: Sato, A., Kawano, H., Notsu, T., Ohta, M., Nakakuki, M., Mizuguchi, K., Itoh, M., Suganami, T. and Ogawa, Y. (2010): Antiobesity effect of eicosapentaenoic acid in high-fat/high-sucrose diet-induced obesity. Importance of hepatic lipogenesis. Diabetes, 59, 2495-2504. – reference: Saraswathi, V., Morrow, J.D. and Hasty, A.H. (2009): Dietary fish oil exerts hypolipidemic effects in lean and insulin sensitizing effects in obese LDLR-/- mice. J. Nutr., 139, 2380-2386. – reference: Hirunpanich, V., Sethabouppha, B. and Sato, H. (2007): Inhibitory effects of saturated and polyunsaturated fatty acids on the cytochrome P450 3A activity in rat liver microsomes. Biol. Pharm. Bull., 30, 1586-1588. – reference: Emery, M.G., Fisher, J.M., Chien, J.Y., Kharasch, E.D., Dellinger, E.P., Kowdley, K.V. and Thummel, K.E. (2003): CYP2E1 activity before and after weight loss in morbidly obese subjects with nonalcoholic fatty liver disease. Hepatology, 38, 428-435. – reference: Kawai, K., Sakairi, T., Harada, S., Shinozuka, J., Ide, M., Sato, H., Tanaka, M., Toriumi, W. and Kume, E. (2012): Diet modification and its influence on metabolic and related pathological alterations in the SHR/NDmcr-cp rat, an animal model of the metabolic syndrome. Exp. Toxicol. Pathol., 64, 333-338. – reference: Cunnane, S.C., McAdoo, K.R. and Horrobin, D.F. (1986): n-3 Essential fatty acids decrease weight gain in genetically obese mice. Br. J. Nutr., 56, 87-95. – reference: Karahashi, M., Ishii, F., Yamazaki, T., Imai, K., Mitsumoto, A., Kawashima,Y. and Kudo, N. (2013): Up-regulation of stearoyl-CoA desaturase 1 increases liver MUFA content in obese Zucker but not Goto-Kakizaki rats. Lipids, 48, 457-467. – reference: Hirunpanich, V., Katagi, J., Sethabouppha, B. and Sato, H. (2006): Demonstration of docosahexaenoic acid as a bioavailability enhancer for CYP3A substrates: in vitro and in vivo evidence using cyclosporine in rats. Drug Metab. Dispos., 34, 305-310. – reference: Tanaka, S., Yamazaki, T., Asano, S., Mitsumoto, A., Kobayashi, D., Kudo, N. and Kawashima, Y. (2013): Increased lipid synthesis and decreased β-oxidation in the liver of SHR/NDmcr-cp (cp/cp) rats, an animal model of metabolic syndrome. Lipids, 48, 1115-1134. – reference: Belalcazar, L.M., Reboussin, D.M., Haffner, S.M., Reeves, R.S., Schwenke, D.C., Hoogeveen, R.C., Pi-Sunyer, F.X. and Ballantyne, C.M. (2010): Marine ω-3 fatty acid intake. Associations with cardiometabolic risk and response to weight loss intervention in the Look AHEAD (action for health in diabetes) study. Diabetes Care, 33, 197-199. – reference: Guo, L.-Q., Fukuda, K., Ohta, T. and Yamazoe, Y. (2000): Role of furanocoumarin derivatives on grapefruit juice-mediated inhibition of human CYP3A activity. Drug Metab. Dispos., 28, 766-771. – reference: Koletsky, S. (1975): Pathologic findings and laboratory data in a new strain of obese hypertensive rats. Am. J. Pathol., 80, 129-142. – reference: Finn, R.D., Henderson, C.J., Scott, C.L. and Wolf, C.R. (2009): Unsaturated fatty acid regulation of cytochrome P450 expression via a CAR-dependent pathway. Biochem. J., 417, 43-54. – reference: Enriquez, A., Leclercq, I., Farrell, G.C. and Robertson, G. (1999): Altered expression of hepatic CYP2E1 and CYP4A in obese, diabetic ob/ob mice, and fa/fa Zucker rats. Biochem. Biophys. Res. Commun., 255, 300-306. – reference: Aleksunes, L.M. and Klaassen, C.D. (2012): Coordinated regulation of hepatic phase I and II drug-metabolizing genes and transporters using AhR-, CAR-, PXR-, PPARα-, and Nrf2-null mice. Drug Metab. Dispos., 40, 1366-1379. – reference: Waxman, D.J. (1999): P450 gene induction by structurally diverse xenochemicals: central role of nuclear receptors CAR, PXR, and PPAR. Arch. Biochem. Biophys., 369, 11-23. – reference: Yoshinari, K., Takagi, S., Sugitani, J. and Miwa, M. (2006): Changes in the expression of cytochrome P450 and nuclear receptors in the liver of genetically diabetic db/db mice. Biol. Pharm. Bull., 29, 1634-1638. – ident: 4 doi: 10.1016/S0022-3565(25)13127-3 – ident: 23 doi: 10.1196/annals.1333.086 – ident: 15 doi: 10.1016/S0090-9556(24)15346-9 – ident: 18 doi: 10.1007/s11745-013-3786-2 – ident: 8 doi: 10.1111/j.1476-5381.2011.01270.x – ident: 11 doi: 10.1006/bbrc.1999.0202 – ident: 19 doi: 10.1016/j.etp.2010.09.006 – ident: 21 doi: 10.1016/j.cgh.2006.12.021 – ident: 28 doi: 10.1248/bpb.35.184 – ident: 16 doi: 10.1124/dmd.105.007088 – ident: 10 doi: 10.1053/jhep.2003.50342 – ident: 22 doi: 10.1016/S0021-9258(19)52451-6 – ident: 3 doi: 10.2337/dc09-1235 – ident: 13 doi: 10.1042/BJ20080740 – ident: 1 doi: 10.1016/S0140-6736(05)67402-8 – ident: 9 doi: 10.1016/S0140-6736(05)66378-7 – ident: 27 doi: 10.1146/annurev.pharmtox.41.1.123 – ident: 20 – ident: 2 doi: 10.1124/dmd.112.045112 – ident: 17 doi: 10.1248/bpb.30.1586 – ident: 26 doi: 10.2337/db09-1554 – ident: 6 doi: 10.1021/mp700114j – ident: 29 doi: 10.1007/s11745-013-3839-6 – ident: 14 doi: 10.1146/annurev.pharmtox.39.1.1 – ident: 30 doi: 10.1006/abbi.1999.1351 – ident: 5 doi: 10.1093/ajcn/83.6.1499S – ident: 24 doi: 10.1016/j.hepres.2005.10.001 – ident: 12 doi: 10.1126/science.286.5439.487 – ident: 7 doi: 10.1079/BJN19860088 – ident: 25 doi: 10.3945/jn.109.111567 – ident: 31 doi: 10.1248/bpb.29.1634 |
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| Title | Effects of dietary fish oil on cytochrome P450 3A expression in the liver of SHR/NDmcr-cp (cp/cp) rats, an animal model for metabolic syndrome |
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