3,084
Views
4
CrossRef citations to date
0
Altmetric
Reviews

The alteration of drug metabolism enzymes and pharmacokinetic parameters in nonalcoholic fatty liver disease: current animal models and clinical practice

, , , , , , & ORCID Icon show all
Pages 163-180 | Received 01 Feb 2023, Accepted 03 Apr 2023, Published online: 28 Apr 2023

References

  • Ahlström MM, Ridderström M, Zamora I, Luthman K. 2007. CYP2C9 structure-metabolism relationships: optimizing the metabolic stability of COX-2 inhibitors. J Med Chem. 50(18):4444–4452.
  • Almazroo OA, Miah MK, Venkataramanan R. 2017. Drug metabolism in the liver. Clin Liver Dis. 21(1):1–20.
  • Baiges-Gaya G, Fernández-Arroyo S, Luciano-Mateo F, Cabré N, Rodríguez-Tomàs E, Hernández-Aguilera A, Castañé H, Romeu M, Nogués M-R, Camps J, et al. 2021. Hepatic metabolic adaptation and adipose tissue expansion are altered in mice with steatohepatitis induced by high-fat high sucrose diet. J Nutr Biochem. 89:108559.
  • Balogh LM, Le Trong I, Kripps KA, Shireman LM, Stenkamp RE, Zhang W, Mannervik B, Atkins WM. 2010. Substrate specificity combined with stereopromiscuity in glutathione transferase A4-4-dependent metabolism of 4-hydroxynonenal. Biochemistry. 49(7):1541–1548.
  • Bock KW, Köhle C. 2005. UDP-glucuronosyltransferase 1A6: structural, functional, and regulatory aspects. Methods Enzymol. 400:57–75.
  • Bogaards JJ, Venekamp JC, van Bladeren PJ. 1997. Stereoselective conjugation of prostaglandin A2 and prostaglandin J2 with glutathione, catalyzed by the human glutathione S-transferases A1-1, A2-2, M1a-1a, and P1-1. Chem Res Toxicol. 10(3):310–317.
  • Borrie AE, Rose RV, Choi Y-H, Perera FE, Read N, Sexton T, Lock M, Vandenberg TA, Hahn K, Dinniwell R, et al. 2018. Letrozole concentration is associated with CYP2A6 variation but not with arthralgia in patients with breast cancer. Breast Cancer Res Treat. 172(2):371–379.
  • Brunnström A, Hamberg M, Griffiths WJ, Mannervik B, Claesson H-E. 2011. Biosynthesis of 14,15-hepoxilins in human l1236 Hodgkin lymphoma cells and eosinophils. Lipids. 46(1):69–79.
  • Buechler C, Weiss TS. 2011. Does hepatic steatosis affect drug metabolizing enzymes in the liver? Curr Drug Metab. 12(1):24–34.
  • Capi M, Curto M, Lionetto L, de Andrés F, Gentile G, Negro A, Martelletti P. 2016. Eletriptan in the management of acute migraine: an update on the evidence for efficacy, safety, and consistent response. Ther Adv Neurol Disord. 9(5):414–423.
  • Carreira MC, Izquierdo AG, Amil M, Casanueva FF, Crujeiras AB. 2018. Oxidative stress induced by excess of adiposity is related to a downregulation of hepatic SIRT6 expression in obese individuals. Oxid Med Cell Longev. 2018:6256052.
  • Chachay VS, Macdonald GA, Martin JH, Whitehead JP, O'Moore-Sullivan TM, Lee P, Franklin M, Klein K, Taylor PJ, Ferguson M, et al. 2014. Resveratrol does not benefit patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 12(12):2092–2103.e6.
  • Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, Charlton M, Sanyal AJ. 2012. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Gastroenterological Association, American Association for the Study of Liver Diseases, and American College of Gastroenterology. Gastroenterology. 142(7):1592–1609.
  • Chang W-C, Jia H, Aw W, Saito K, Hasegawa S, Kato H. 2014. Beneficial effects of soluble dietary Jerusalem artichoke (Helianthus tuberosus) in the prevention of the onset of type 2 diabetes and non-alcoholic fatty liver disease in high-fructose diet-fed rats. Br J Nutr. 112(5):709–717.
  • Chiba T, Noji K, Shinozaki S, Suzuki S, Umegaki K, Shimokado K. 2016. Diet-induced non-alcoholic fatty liver disease affects expression of major cytochrome P450 genes in a mouse model. J Pharm Pharmacol. 68(12):1567–1576.
  • Cho Y-E, Kim D-K, Seo W, Gao B, Yoo S-H, Song B-J. 2021. Fructose promotes leaky gut, endotoxemia, and liver fibrosis through ethanol-inducible cytochrome P450-2E1-mediated oxidative and nitrative stress. Hepatology. 73(6):2180–2195.
  • Cobbina E, Akhlaghi F. 2017. Non-alcoholic fatty liver disease (NAFLD) - pathogenesis, classification, and effect on drug metabolizing enzymes and transporters. Drug Metab Rev. 49(2):197–211.
  • Cong S, Li Z, Yu L, Liu Y, Hu Y, Bi Y, Cheng M. 2021. Integrative proteomic and lipidomic analysis of Kaili Sour Soup-mediated attenuation of high-fat diet-induced nonalcoholic fatty liver disease in a rat model. Nutr Metab. 18(1):26.
  • Connor F, Rayner TF, Aitken SJ, Feig C, Lukk M, Santoyo-Lopez J, Odom DT. 2018. Mutational landscape of a chemically-induced mouse model of liver cancer. J Hepatol. 69(4):840–850.
  • Cook I, Wang T, Leyh TS. 2019. Isoform-specific therapeutic control of sulfonation in humans. Biochem Pharmacol. 159:25–31.
  • Court MH, Hazarika S, Krishnaswamy S, Finel M, Williams JA. 2008. Novel polymorphic human UDP-glucuronosyltransferase 2A3: cloning, functional characterization of enzyme variants, comparative tissue expression, and gene induction. Mol Pharmacol. 74(3):744–754.
  • Danielson PB. 2002. The cytochrome P450 superfamily: biochemistry, evolution and drug metabolism in humans. Curr Drug Metab. 3(6):561–597.
  • Delgado A, Velosa J, Zhang J, Dursun SM, Kapczinski F, de Azevedo Cardoso T. 2020. Clozapine in bipolar disorder: a systematic review and meta-analysis. J Psychiatr Res. 125:21–27.
  • Desmots F, Rissel M, Pigeon C, Loyer P, Loréal O, Guillouzo A. 2002. Differential effects of iron overload on GST isoform expression in mouse liver and kidney and correlation between GSTA4 induction and overproduction of free radicles. Free Radic Biol Med. 32(1):93–101.
  • Duthaler U, Bachmann F, Suenderhauf C, Grandinetti T, Pfefferkorn F, Haschke M, Hruz P, Bouitbir J, Krähenbühl S. 2022. Liver cirrhosis affects the pharmacokinetics of the six substrates of the basel phenotyping cocktail differently. Clin Pharmacokinet. 61(7):1039–1055.
  • El Daibani AA, Alherz FA, Abunnaja MS, Bairam AF, Rasool MI, Kurogi K, Liu M-C. 2021. Impact of human SULT1E1 polymorphisms on the sulfation of 17β-Estradiol, 4-hydroxytamoxifen, and diethylstilbestrol by SULT1E1 allozymes. Eur J Drug Metab Pharmacokinet. 46(1):105–118.
  • Emery MG, Fisher JM, Chien JY, Kharasch ED, Dellinger EP, Kowdley KV, Thummel KE. 2003. CYP2E1 activity before and after weight loss in morbidly obese subjects with nonalcoholic fatty liver disease. Hepatology. 38(2):428–435.
  • Eslam M, Newsome PN, Sarin SK, Anstee QM, Targher G, Romero-Gomez M, Zelber-Sagi S, Wai-Sun Wong V, Dufour J-F, Schattenberg JM, et al. 2020. A new definition for metabolic dysfunction-associated fatty liver disease: an international expert consensus statement. J Hepatol. 73(1):202–209.
  • Faber MS, Jetter A, Fuhr U. 2005. Assessment of CYP1A2 activity in clinical practice: why, how, and when? Basic Clin Pharmacol Toxicol. 97(3):125–134.
  • Fashe M, Yi M, Sueyoshi T, Negishi M. 2021. Sex-specific expression mechanism of hepatic estrogen inactivating enzyme and transporters in diabetic women. Biochem Pharmacol. 190:114662.
  • Fisher CD, Lickteig AJ, Augustine LM, Ranger-Moore J, Jackson JP, Ferguson SS, Cherrington NJ. 2009. Hepatic cytochrome P450 enzyme alterations in humans with progressive stages of nonalcoholic fatty liver disease. Drug Metab Dispos. 37(10):2087–2094.
  • Friedman SL, Neuschwander-Tetri BA, Rinella M, Sanyal AJ. 2018. Mechanisms of NAFLD development and therapeutic strategies. Nat Med. 24(7):908–922.
  • Fuhr LM, Marok FZ, Mees M, Mahfoud F, Selzer D, Lehr T. 2022. A physiologically based pharmacokinetic and pharmacodynamic model of the CYP3A4 substrate felodipine for drug-drug interaction modeling. Pharmaceutics. 14(7):1474.
  • Gagné J-F, Montminy V, Belanger P, Journault K, Gaucher G, Guillemette C. 2002. Common human UGT1A polymorphisms and the altered metabolism of irinotecan active metabolite 7-ethyl-10-hydroxycamptothecin (SN-38). Mol Pharmacol. 62(3):608–617.
  • Gao Y, Zhang W, Zeng L-Q, Bai H, Li J, Zhou J, Zhou G-Y, Fang C-W, Wang F, Qin X-J. 2020. Exercise and dietary intervention ameliorate high-fat diet-induced NAFLD and liver aging by inducing lipophagy. Redox Biol. 36:101635.
  • Ghose R, Omoluabi O, Gandhi A, Shah P, Strohacker K, Carpenter KC, McFarlin B, Guo T. 2011. Role of high-fat diet in regulation of gene expression of drug metabolizing enzymes and transporters. Life Sci. 89(1-2):57–64.
  • Goetz MP, Sangkuhl K, Guchelaar H-J, Schwab M, Province M, Whirl-Carrillo M, Symmans WF, McLeod HL, Ratain MJ, Zembutsu H, et al. 2018. Clinical pharmacogenetics implementation consortium (CPIC) guideline for CYP2D6 and tamoxifen therapy. Clin Pharmacol Ther. 103(5):770–777.
  • Gofton C, Upendran Y, Zheng M-H, George J. 2022. MAFLD: what is different from NAFLD? Clin Mol Hepatol.29(Suppl):S17–S31.
  • Gradinaru J, Romand S, Geiser L, Carrupt P-A, Spaggiari D, Rudaz S. 2015. Inhibition screening method of microsomal UGTs using the cocktail approach. Eur J Pharm Sci. 71:35–45.
  • Griesel R, Maartens G, Chirehwa M, Sokhela S, Akpomiemie G, Moorhouse M, Venter F, Sinxadi P. 2021. CYP2B6 genotype and weight gain differences between dolutegravir and efavirenz. Clin Infect Dis. 73(11):e3902–e3909.
  • Gulcan HO, Duffel MW. 2011. Substrate inhibition in human hydroxysteroid sulfotransferase SULT2A1: studies on the formation of catalytically non-productive enzyme complexes. Arch Biochem Biophys. 507(2):232–240.
  • Guo Y, Li F, Ma X, Cheng X, Zhou H, Klaassen CD. 2011. CYP2D plays a major role in berberine metabolism in liver of mice and humans. Xenobiotica. 41(11):996–1005.
  • Hao H, Lai L, Zheng C, Wang Q, Yu G, Zhou X, Wu L, Gong P, Wang G. 2010. Microsomal cytochrome p450-mediated metabolism of protopanaxatriol ginsenosides: metabolite profile, reaction phenotyping, and structure-metabolism relationship. Drug Metab Dispos. 38(10):1731–1739.
  • Hardwick RN, Ferreira DW, More VR, Lake AD, Lu Z, Manautou JE, Slitt AL, Cherrington NJ. 2013. Altered UDP-glucuronosyltransferase and sulfotransferase expression and function during progressive stages of human nonalcoholic fatty liver disease. Drug Metab Dispos. 41(3):554–561.
  • Hempel N, Gamage N, Martin JL, McManus ME. 2007. Human cytosolic sulfotransferase SULT1A1. Int J Biochem Cell Biol. 39(4):685–689.
  • Henry L, Paik J, Younossi ZM. 2022. Review article: the epidemiologic burden of non-alcoholic fatty liver disease across the world. Aliment Pharmacol Ther. 56(6):942–956.
  • Hoehle SI, Pfeiffer E, Metzler M. 2007. Glucuronidation of curcuminoids by human microsomal and recombinant UDP-glucuronosyltransferases. Mol Nutr Food Res. 51(8):932–938.
  • Hong CH, Ko MS, Kim JH, Cho H, Lee C-H, Yoon JE, Yun J-Y, Baek I-J, Jang JE, Lee SE, et al. 2022. Sphingosine 1-phosphate receptor 4 promotes nonalcoholic steatohepatitis by activating NLRP3 inflammasome. Cell Mol Gastroenterol Hepatol. 13(3):925–947.
  • Hua YQ, Zeng Y, Xu J, Xu XL. 2021. Naringenin alleviates nonalcoholic steatohepatitis in middle-aged Apoemice: role of SIRT1. Phytomedicine. 81:153412.
  • Huang S, Wu Y, Zhao Z, Wu B, Sun K, Wang H, Qin L, Bai F, Leng Y, Tang W. 2021. A new mechanism of obeticholic acid on NASH treatment by inhibiting NLRP3 inflammasome activation in macrophage. Metabolism. 120:154797.
  • Huang X, Li C, Li C, Li Z, Li X, Liao J, Rao T, Chen L, Gao L, Ouyang D. 2021. CYP2C19 genotyping may provide a better treatment strategy when administering escitalopram in Chinese population. Front Pharmacol. 12:730461.
  • Huenchuguala S, Muñoz P, Graumann R, Paris I, Segura-Aguilar J. 2016. DT-diaphorase protects astrocytes from aminochrome-induced toxicity. Neurotoxicology. 55:10–12.
  • Jamwal R, de la Monte SM, Ogasawara K, Adusumalli S, Barlock BB, Akhlaghi F. 2018. Nonalcoholic fatty liver disease and diabetes are associated with decreased CYP3A4 protein expression and activity in human liver. Mol Pharm. 15(7):2621–2632.
  • Jaworski M, Buchmann A, Bauer P, Riess O, Schwarz M. 2005. B-raf and Ha-ras mutations in chemically induced mouse liver tumors. Oncogene. 24(7):1290–1295.
  • Jian T, Yu C, Ding X, Chen J, Li J, Zuo Y, Ren B, Lv H, Li W. 2019. Hepatoprotective effect of seed coat of Euryale ferox extract in non-alcoholic fatty liver disease induced by high-fat diet in mice by increasing IRs-1 and inhibiting CYP2E1. J Oleo Sci. 68(6):581–589.
  • Kasichayanula S, Liu X, Griffen SC, Lacreta FP, Boulton DW. 2013. Effects of rifampin and mefenamic acid on the pharmacokinetics and pharmacodynamics of dapagliflozin. Diabetes Obes Metab. 15(3):280–283.
  • Kaur G, Gupta SK, Singh P, Ali V, Kumar V, Verma M. 2020. Drug-metabolizing enzymes: role in drug resistance in cancer. Clin Transl Oncol. 22(10):1667–1680.
  • Kim TH, Choi D, Kim JY, Lee JH, Koo S-H. 2017. Fast food diet-induced non-alcoholic fatty liver disease exerts early protective effect against acetaminophen intoxication in mice. BMC Gastroenterol. 17(1):124.
  • Koch KM, Corrigan BW, Manzo J, James CD, Scott RJ, Stead AG, Kersey KE. 2004. Alosetron repeat dose pharmacokinetics, effects on enzyme activities, and influence of demographic factors. Aliment Pharmacol Ther. 20(2):223–230.
  • Konopnicki CM, Dickmann LJ, Tracy JM, Tukey RH, Wienkers LC, Foti RS. 2013. Evaluation of UGT protein interactions in human hepatocytes: effect of siRNA down regulation of UGT1A9 and UGT2B7 on propofol glucuronidation in human hepatocytes. Arch Biochem Biophys. 535(2):143–149.
  • Kumar A, Sundaram K, Mu J, Dryden GW, Sriwastva MK, Lei C, Zhang L, Qiu X, Xu F, Yan J, et al. 2021. High-fat diet-induced upregulation of exosomal phosphatidylcholine contributes to insulin resistance. Nat Commun. 12(1):213.
  • Kurogi K, Rasool MI, Alherz FA, El Daibani AA, Bairam AF, Abunnaja MS, Yasuda S, Wilson LJ, Hui Y, Liu M-C. 2021. SULT genetic polymorphisms: physiological, pharmacological and clinical implications. Expert Opin Drug Metab Toxicol. 17(7):767–784.
  • Kvitne KE, Åsberg A, Johnson LK, Wegler C, Hertel JK, Artursson P, Karlsson C, Andersson S, Sandbu R, Skovlund E, et al. 2022. Impact of type 2 diabetes on in vivo activities and protein expressions of cytochrome P450 in patients with obesity. Clin Transl Sci. 15(11):2685–2696.
  • Lad A, Hunyadi J, Connolly J, Breidenbach JD, Khalaf FK, Dube P, Zhang S, Kleinhenz AL, Baliu-Rodriguez D, Isailovic D, et al. 2022. Antioxidant therapy significantly attenuates hepatotoxicity following low dose exposure to microcystin-LR in a murine model of diet-induced non-alcoholic fatty liver disease. Antioxidants. 11(8):1625.
  • Lan T, Hu Y, Hu F, Li H, Chen Y, Zhang J, Yu Y, Jiang S, Weng Q, Tian S, et al. 2022. Hepatocyte glutathione S-transferase mu 2 prevents non-alcoholic steatohepatitis by suppressing ASK1 signaling. J Hepatol. 76(2):407–419.
  • Lee DH, Han DH, Nam KT, Park JS, Kim SH, Lee M, Kim G, Min BS, Cha B-S, Lee YS, et al. 2016. Ezetimibe, an NPC1L1 inhibitor, is a potent Nrf2 activator that protects mice from diet-induced nonalcoholic steatohepatitis. Free Radic Biol Med. 99:520–532.
  • Lee DH, Park JS, Lee YS, Han J, Lee D-K, Kwon SW, Han DH, Lee Y-H, Bae SH. 2020. SQSTM1/p62 activates NFE2L2/NRF2 via ULK1-mediated autophagic KEAP1 degradation and protects mouse liver from lipotoxicity. Autophagy. 16(11):1949–1973.
  • Lee ES, Kwon M-H, Kim HM, Woo HB, Ahn CM, Chung CH. 2020. Curcumin analog CUR5-8 ameliorates nonalcoholic fatty liver disease in mice with high-fat diet-induced obesity. Metabolism. 103:154015.
  • Lee J-T, Pao L-H, Hsiong C-H, Huang P-W, Shih T-Y, Yoa-Pu Hu O. 2013. Validated liquid chromatography-tandem mass spectrometry method for determination of totally nine probe metabolites of cytochrome P450 enzymes and UDP-glucuronosyltransferases. Talanta. 106:220–228.
  • Lépine J, Bernard O, Plante M, Têtu B, Pelletier G, Labrie F, Bélanger A, Guillemette C. 2004. Specificity and regioselectivity of the conjugation of estradiol, estrone, and their catecholestrogen and methoxyestrogen metabolites by human uridine diphospho-glucuronosyltransferases expressed in endometrium. J Clin Endocrinol Metab. 89(10):5222–5232.
  • Lévesque E, Girard H, Journault K, Lépine J, Guillemette C. 2007. Regulation of the UGT1A1 bilirubin-conjugating pathway: role of a new splicing event at the UGT1A locus. Hepatology. 45(1):128–138.
  • Li H, Canet MJ, Clarke JD, Billheimer D, Xanthakos SA, Lavine JE, Erickson RP, Cherrington NJ. 2017. Pediatric cytochrome P450 activity alterations in nonalcoholic steatohepatitis. Drug Metab Dispos. 45(12):1317–1325.
  • Li H, Clarke JD, Dzierlenga AL, Bear J, Goedken MJ, Cherrington NJ. 2017. In vivo cytochrome P450 activity alterations in diabetic nonalcoholic steatohepatitis mice. J Biochem Mol Toxicol. 31(2):e21840.
  • Li P, Robertson TA, Thorling CA, Zhang Q, Fletcher LM, Crawford DHG, Roberts MS. 2011. Hepatic pharmacokinetics of cationic drugs in a high-fat emulsion-induced rat model of nonalcoholic steatohepatitis. Drug Metab Dispos. 39(4):571–579.
  • Li R, Guo G, Cao Y, Wang Y, Liu F, Zhang X. 2013. Expression of cytochrome P450 2A5 in a C57BL/6J mouse model of nonalcoholic fatty liver disease. Pharmacology. 92(1-2):26–31.
  • Li X, Li S, Chen M, Wang J, Xie B, Sun Z. 2018. (-)-Epigallocatechin-3-gallate (EGCG) inhibits starch digestion and improves glucose homeostasis through direct or indirect activation of PXR/CAR-mediated phase II metabolism in diabetic mice. Food Funct. 9(9):4651–4663.
  • Li Z, Lee SH, Jeong HJ, Kang HE. 2021. Pharmacokinetic changes of clozapine and norclozapine in a rat model of non-alcoholic fatty liver disease induced by orotic acid. Xenobiotica. 51(3):324–334.
  • Lin Q-M, Li Y-H, Lu X-R, Wang R, Pang N-H, Xu R-A, Cai J-P, Hu G-X. 2019. Characterization of genetic variation in CYP3A4 on the metabolism of cabozantinib in vitro. Chem Res Toxicol. 32(8):1583–1590.
  • Lin S, Huang J, Wang M, Kumar R, Liu Y, Liu S, Wu Y, Wang X, Zhu Y. 2020. Comparison of MAFLD and NAFLD diagnostic criteria in real world. Liver Int. 40(9):2082–2089.
  • Liu W, Shang J, Deng Y, Han X, Chen Y, Wang S, Yang R, Dong F, Shang H. 2022. Network pharmacology analysis on mechanism of Jian Pi Qing Gan Yin decoction ameliorating high fat diet-induced non-alcoholic fatty liver disease and validated in vivo. J Ethnopharmacol. 295:115382.
  • Liu Y, Deng J, Fan D. 2019. Ginsenoside Rk3 ameliorates high-fat-diet/streptozocin induced type 2 diabetes mellitus in mice via the AMPK/Akt signaling pathway. Food Funct. 10(5):2538–2551.
  • Liu Y, Xu W, Zhai T, You J, Chen Y. 2019. Silibinin ameliorates hepatic lipid accumulation and oxidative stress in mice with non-alcoholic steatohepatitis by regulating CFLAR-JNK pathway. Acta Pharm Sin B. 9(4):745–757.
  • Locuson CW, Williams P, Adcock JM, Daniels JS. 2016. Evaluation of tizanidine as a marker of canine CYP1A2 activity. J Vet Pharmacol Ther. 39(2):122–130.
  • Lu Y, Zhu J, Chen X, Li N, Fu F, He J, Wang G, Zhang L, Zheng Y, Qiu Z, et al. 2009. Identification of human UDP-glucuronosyltransferase isoforms responsible for the glucuronidation of glycyrrhetinic acid. Drug Metab Pharmacokinet. 24(6):523–528.
  • Maksymchuk O, Shysh A, Stroy D. 2022. Treatment with omega-3 PUFAs does not increase the risk of CYP2E1-dependent oxidative stress and diabetic liver pathology. Front Endocrinol. 13:1004564.
  • Mandel HG. 2002. Update on caffeine consumption, disposition and action. Food Chem Toxicol. 40(9):1231–1234.
  • Marok FZ, Fuhr LM, Hanke N, Selzer D, Lehr T. 2021. Physiologically based pharmacokinetic modeling of bupropion and its metabolites in a CYP2B6 drug-drug-gene interaction network. Pharmaceutics. 13(3):331.
  • Márquez-Quiroga LV, Arellanes-Robledo J, Vásquez-Garzón VR, Villa-Treviño S, Muriel P. 2022. Models of nonalcoholic steatohepatitis potentiated by chemical inducers leading to hepatocellular carcinoma. Biochem Pharmacol. 195:114845.
  • Matsumoto Y, Fujita S, Yamagishi A, Shirai T, Maeda Y, Suzuki T, Kobayashi K-I, Inoue J, Yamamoto Y. 2021. Brown rice inhibits development of nonalcoholic fatty liver disease in obese Zucker (fa/fa) rats by increasing lipid oxidation via activation of retinoic acid synthesis. J Nutr. 151(9):2705–2713.
  • Meech R, Hu DG, McKinnon RA, Mubarokah SN, Haines AZ, Nair PC, Rowland A, Mackenzie PI. 2019. The UDP-glycosyltransferase (UGT) superfamily: new members, new functions, and novel paradigms. Physiol Rev. 99(2):1153–1222.
  • Miura M, Uchida S, Tanaka S, Inui N, Kawakami J, Watanabe H, Namiki N. 2019. The prediction of the area under the curve and clearance of midazolam from single-point plasma concentration and urinary excretion in healthy volunteers. Biol Pharm Bull. 42(9):1590–1595.
  • Miyata M, Funaki A, Fukuhara C, Sumiya Y, Sugiura Y. 2020. Taurine attenuates hepatic steatosis in a genetic model of fatty liver disease. J Toxicol Sci. 45(2):87–94.
  • Miyata M, Matsushita K, Shindo R, Shimokawa Y, Sugiura Y, Yamashita M. 2020. Selenoneine ameliorates hepatocellular injury and hepatic steatosis in a mouse model of NAFLD. Nutrients. 12(6):1898.
  • Nakanishi K, Kaji K, Kitade M, Kubo T, Furukawa M, Saikawa S, Shimozato N, Sato S, Seki K, Kawaratani H, et al. 2019. Exogenous administration of low-dose lipopolysaccharide potentiates liver fibrosis in a choline-deficient l-amino-acid-defined diet-induced murine steatohepatitis model. Int J Mol Sci. 20(11). DOI:10.3390/ijms20112724
  • Negi CK, Babica P, Bajard L, Bienertova-Vasku J, Tarantino G. 2022. Insights into the molecular targets and emerging pharmacotherapeutic interventions for nonalcoholic fatty liver disease. Metabolism. 126:154925.
  • Nielsen RV, Fomsgaard JS, Siegel H, Martusevicius R, Mathiesen O, Dahl JB. 2016. The effect of chlorzoxazone on acute pain after spine surgery. A randomized, blinded trial. Acta Anaesthesiol Scand. 60(8):1152–1160.
  • Niu Z, Qiang T, Lin W, Li Y, Wang K, Wang D, Wang X. 2022. Evaluation of potential herb-drug interactions between Shengmai injection and losartan potassium in rat and in vitro. Front Pharmacol. 13:878526.
  • Nucifora FC, Mihaljevic M, Lee BJ, Sawa A. 2017. Clozapine as a model for antipsychotic development. Neurotherapeutics. 14(3):750–761.
  • Oh K-S, Park S-J, Shinde DD, Shin J-G, Kim D-H. 2012. High-sensitivity liquid chromatography-tandem mass spectrometry for the simultaneous determination of five drugs and their cytochrome P450-specific probe metabolites in human plasma. J Chromatogr B Analyt Technol Biomed Life Sci. 895-896:56–64.
  • Omura K, Motoki K, Kobashi S, Miyata K, Yamano K, Iwanaga T. 2021. Identification of human UDP-glucuronosyltransferase and sulfotransferase as responsible for the metabolism of dotinurad, a novel selective urate reabsorption inhibitor. Drug Metab Dispos. 49(11):1016–1024.
  • Osabe M, Sugatani J, Fukuyama T, Ikushiro S-i, Ikari A, Miwa M. 2008. Expression of hepatic UDP-glucuronosyltransferase 1A1 and 1A6 correlated with increased expression of the nuclear constitutive androstane receptor and peroxisome proliferator-activated receptor alpha in male rats fed a high-fat and high-sucrose diet. Drug Metab Dispos. 36(2):294–302.
  • Oseini AM, Sanyal AJ. 2017. Therapies in non-alcoholic steatohepatitis (NASH). Liver Int. 37:97–103.
  • Pathania S, Bhatia R, Baldi A, Singh R, Rawal RK. 2018. Drug metabolizing enzymes and their inhibitors’ role in cancer resistance. Biomed Pharmacother. 105:53–65.
  • Piver B, Fer M, Vitrac X, Merillon J-M, Dreano Y, Berthou F, Lucas D. 2004. Involvement of cytochrome P450 1A2 in the biotransformation of trans-resveratrol in human liver microsomes. Biochem Pharmacol. 68(4):773–782.
  • Polyzos SA, Kang ES, Boutari C, Rhee E-J, Mantzoros CS. 2020. Current and emerging pharmacological options for the treatment of nonalcoholic steatohepatitis. Metabolism. 111S:154203.
  • Porras D, Nistal E, Martínez-Flórez S, Pisonero-Vaquero S, Olcoz JL, Jover R, González-Gallego J, García-Mediavilla MV, Sánchez-Campos S. 2017. Protective effect of quercetin on high-fat diet-induced non-alcoholic fatty liver disease in mice is mediated by modulating intestinal microbiota imbalance and related gut-liver axis activation. Free Radic Biol Med. 102:188–202.
  • Ranaweera SS, Natraj P, Rajan P, Dayarathne LA, Mihindukulasooriya SP, Dinh DTT, Jee Y, Han C-H. 2022. Anti-obesity effect of sulforaphane in broccoli leaf extract on 3T3-L1 adipocytes and ob/ob mice. J Nutr Biochem. 100:108885.
  • Riches Z, Stanley EL, Bloomer JC, Coughtrie MWH. 2009. Quantitative evaluation of the expression and activity of five major sulfotransferases (SULTs) in human tissues: the SULT “pie.” Drug Metab Dispos. 37(11):2255–2261.
  • Richter JE, Kahrilas PJ, Johanson J, Maton P, Breiter JR, Hwang C, Marino V, Hamelin B, Levine JG. 2001. Efficacy and safety of esomeprazole compared with omeprazole in GERD patients with erosive esophagitis: a randomized controlled trial. Am J Gastroenterology. 96(3):656–665.
  • Rodolà F. 2006. Midazolam as an anti-emetic. Eur Rev Med Pharmacol Sci. 10(3):121–126.
  • Sakurai Y, Kubota N, Yamauchi T, Kadowaki T. 2021. Role of insulin resistance in MAFLD. Int J Mol Sci. 22(8). DOI:10.3390/ijms22084156
  • Sawynok J. 2011. Methylxanthines and pain. Handb Exp Pharmacol. 200:311–329.
  • Sharma L, Gupta D, Abdullah ST. 2019. Thioacetamide potentiates high cholesterol and high fat diet induced steato-hepatitic changes in livers of C57BL/6J mice: a novel eight weeks model of fibrosing NASH. Toxicol Lett. 304:21–29.
  • Sharma RS, Harrison DJ, Kisielewski D, Cassidy DM, McNeilly AD, Gallagher JR, Walsh SV, Honda T, McCrimmon RJ, Dinkova-Kostova AT, et al. 2018. Experimental nonalcoholic steatohepatitis and liver fibrosis are ameliorated by pharmacologic activation of Nrf2 (NF-E2 p45-related factor 2). Cell Mol Gastroenterol Hepatol. 5(3):367–398.
  • Silva Barbosa AC, Zhou D, Xie Y, Choi Y-J, Tung H-C, Chen X, Xu M, Gibbs RB, Poloyac SM, Liu S, et al. 2020. Inhibition of estrogen sulfotransferase (/EST) ameliorates ischemic acute kidney injury in mice. J Am Soc Nephrol. 31(7):1496–1508.
  • Siu YA, Hao M-H, Dixit V, Lai WG. 2018. Celecoxib is a substrate of CYP2D6: impact on celecoxib metabolism in individuals with CYP2C9*3 variants. Drug Metab Pharmacokinet. 33(5):219–227.
  • Song Y, Li C, Liu G, Liu R, Chen Y, Li W, Cao Z, Zhao B, Lu C, Liu Y. 2021. Drug-metabolizing cytochrome P450 enzymes have multifarious influences on treatment outcomes. Clin Pharmacokinet. 60(5):585–601.
  • Stowers SJ, Wiseman RW, Ward JM, Miller EC, Miller JA, Anderson MW, Eva A. 1988. Detection of activated proto-oncogenes in N-nitrosodiethylamine-induced liver tumors: a comparison between B6C3F1 mice and Fischer 344 rats. Carcinogenesis. 9(2):271–276.
  • Suga T, Yamaguchi H, Ogura J, Shoji S, Maekawa M, Mano N. 2019. Altered bile acid composition and disposition in a mouse model of non-alcoholic steatohepatitis. Toxicol Appl Pharmacol. 379:114664.
  • Suzuki S, Nishijima C, Sato Y, Umegaki K, Murata M, Chiba T. 2020. Coleus forskohlii extract attenuated the beneficial effect of diet-treatment on NASH in mouse model. J Nutr Sci Vitaminol. 66(2):191–199.
  • Sylvester Darvin S, Toppo E, Esakkimuthu S, Ajeesh Krishna TP, Ceasar SA, Stalin A, Balakrishna K, Muniappan N, Pazhanivel N, Mahaprabhu R, et al. 2018. Hepatoprotective effect of bisbenzylisoquinoline alkaloid tiliamosine from Tiliacora racemosa in high-fat diet/diethylnitrosamine-induced non-alcoholic steatohepatitis. Biomed Pharmacother. 108:963–973.
  • Takahashi Y, Soejima Y, Fukusato T. 2012. Animal models of nonalcoholic fatty liver disease/nonalcoholic steatohepatitis. World J Gastroenterol. 18(19):2300–2308.
  • Tarantino G, Balsano C, Santini SJ, Brienza G, Clemente I, Cosimini B, Sinatti G. 2021. It is high time physicians thought of natural products for alleviating NAFLD. Is there sufficient evidence to use them? Int J Mol Sci. 22(24). DOI:10.3390/ijms222413424
  • Tarantino G, Conca P, Capone D, Gentile A, Polichetti G, Basile V. 2006. Reliability of total overnight salivary caffeine assessment (TOSCA) for liver function evaluation in compensated cirrhotic patients. Eur J Clin Pharmacol. 62(8):605–612.
  • Tsuchida T, Lee YA, Fujiwara N, Ybanez M, Allen B, Martins S, Fiel MI, Goossens N, Chou H-I, Hoshida Y, et al. 2018. A simple diet- and chemical-induced murine NASH model with rapid progression of steatohepatitis, fibrosis and liver cancer. J Hepatol. 69(2):385–395.
  • Tung Y-T, Huang C-Z, Lin J-H, Yen G-C. 2018. Effect of Phyllanthus emblica L. fruit on methionine and choline-deficiency diet-induced nonalcoholic steatohepatitis. J Food Drug Anal. 26(4):1245–1252.
  • van Oijen MGH, Huybers S, Peters WHM, Drenth JPH, Laheij RJF, Verheugt FWA, Jansen JBMJ. 2005. Polymorphisms in genes encoding acetylsalicylic acid metabolizing enzymes are unrelated to upper gastrointestinal health in cardiovascular patients on acetylsalicylic acid. Br J Clin Pharmacol. 60(6):623–628.
  • Verbeeck RK. 2008. Pharmacokinetics and dosage adjustment in patients with hepatic dysfunction. Eur J Clin Pharmacol. 64(12):1147–1161.
  • Vogel CFA, Van Winkle LS, Esser C, Haarmann-Stemmann T. 2020. The aryl hydrocarbon receptor as a target of environmental stressors - implications for pollution mediated stress and inflammatory responses. Redox Biol. 34:101530.
  • Wahlang B, Song M, Beier JI, Cameron Falkner K, Al-Eryani L, Clair HB, Prough RA, Osborne TS, Malarkey DE, States JC, et al. 2014. Evaluation of Aroclor 1260 exposure in a mouse model of diet-induced obesity and non-alcoholic fatty liver disease. Toxicol Appl Pharmacol. 279(3):380–390.
  • Wang C, Tao Q, Wang X, Wang X, Zhang X. 2016. Impact of high-fat diet on liver genes expression profiles in mice model of nonalcoholic fatty liver disease. Environ Toxicol Pharmacol. 45:52–62.
  • Wang J, Zhai T, Chen Y. 2018. Effects of honokiol on CYP450 activity and transporter mRNA expression in type 2 diabetic rats. Int J Mol Sci. 19(3). DOI:10.3390/ijms19030815
  • Wang K, Chen X, Ward SC, Liu Y, Ouedraogo Y, Xu C, Cederbaum AI, Lu Y. 2019. CYP2A6 is associated with obesity: studies in human samples and a high fat diet mouse model. Int J Obes. 43(3):475–486.
  • Wang P, Shao X, Bao Y, Zhu J, Chen L, Zhang L, Ma X, Zhong X-B. 2020. Impact of obese levels on the hepatic expression of nuclear receptors and drug-metabolizing enzymes in adult and offspring mice. Acta Pharm Sin B. 10(1):171–185.
  • Wang X-H, Cui X-X, Sun X-Q, Wang X-H, Li X-C, Qi Y, Li W, Han M-Y, Muhammad I, Zhang X-Y. 2017. High fat diet-induced hepatic 18-carbon fatty acids accumulation up-regulates CYP2A5/CYP2A6 via NF-E2-related factor 2. Front Pharmacol. 8:233.
  • Wang Y, You Y, Tian Y, Sun H, Li X, Wang X, Wang Y, Liu J. 2020. Pediococcus pentosaceus PP04 Ameliorates high-fat diet-induced hyperlipidemia by regulating lipid metabolism in C57BL/6N mice. J Agric Food Chem. 68(51):15154–15163.
  • Wang Y-C, Hsieh T-C, Chou C-L, Wu J-L, Fang T-C. 2016. Risks of adverse events following coprescription of statins and calcium channel blockers: a nationwide population-based study. Medicine. 95(2):e2487.
  • Wang Z, Wong T, Hashizume T, Dickmann LZ, Scian M, Koszewski NJ, Goff JP, Horst RL, Chaudhry AS, Schuetz EG, et al. 2014. Human UGT1A4 and UGT1A3 conjugate 25-hydroxyvitamin D3: metabolite structure, kinetics, inducibility, and interindividual variability. Endocrinology. 155(6):2052–2063.
  • Wegman P, Vainikka L, Stål O, Nordenskjöld B, Skoog L, Rutqvist L-E, Wingren S. 2005. Genotype of metabolic enzymes and the benefit of tamoxifen in postmenopausal breast cancer patients. Breast Cancer Res. 7(3):R284–R290.
  • Woolsey SJ, Mansell SE, Kim RB, Tirona RG, Beaton MD. 2015. CYP3A activity and expression in nonalcoholic fatty liver disease. Drug Metab Dispos. 43(10):1484–1490.
  • Wu J, Lou Y-G, Yang X-l, Wang R, Zhang R, Aa J-Y, Wang G-J, Xie Y. 2023. Silybin regulates P450s activity by attenuating endoplasmic reticulum stress in mouse nonalcoholic fatty liver disease. Acta Pharmacol Sin. 44(1):133–144.
  • Wu Z, Zhang Y, Gong X, Cheng G, Pu S, Cai S. 2020. The preventive effect of phenolic-rich extracts from Chinese sumac fruits against nonalcoholic fatty liver disease in rats induced by a high-fat diet. Food Funct. 11(1):799–812.
  • Xu J, Kulkarni SR, Li L, Slitt AL. 2012. UDP-glucuronosyltransferase expression in mouse liver is increased in obesity- and fasting-induced steatosis. Drug Metab Dispos. 40(2):259–266.
  • Xu J, Peng Y, Zeng Y, Hua Y-Q, Xu X-l. 2019. 2, 3, 4', 5-Tetrahydroxystilbene-2-0-β-d glycoside attenuates age- and diet-associated non-alcoholic steatohepatitis and atherosclerosis in LDL receptor knockout mice and its possible mechanisms. Int J Mol Sci. 20(7). DOI:10.3390/ijms20071617
  • Xu L, Yin L, Qi Y, Tan X, Gao M, Peng J. 2021. 3D disorganization and rearrangement of genome provide insights into pathogenesis of NAFLD by integrated Hi-C, Nanopore, and RNA sequencing. Acta Pharm Sin B. 11(10):3150–3164.
  • Xu Y, Lu J, Guo Y, Zhang Y, Liu J, Huang S, Zhang Y, Gao L, Wang X. 2022. Hypercholesterolemia reduces the expression and function of hepatic drug metabolizing enzymes and transporters in rats. Toxicol Lett. 364:1–11.
  • Yan C, Zhang Y, Zhang X, Aa J, Wang G, Xie Y. 2018. Curcumin regulates endogenous and exogenous metabolism via Nrf2-FXR-LXR pathway in NAFLD mice. Biomed Pharmacother. 105:274–281.
  • Yang Z-Z, Li L, Wang L, Yuan L-M, Xu M-C, Gu J-K, Jiang H-d, Yu L-S, Zeng S. 2017. The regioselective glucuronidation of morphine by dimerized human UGT2B7, 1A1, 1A9 and their allelic variants. Acta Pharmacol Sin. 38(8):1184–1194.
  • Yao H, Bai R, Ren T, Wang Y, Gu J, Guo Y. 2019. Enhanced platelet response to clopidogrel in Zucker diabetic fatty rats due to impaired clopidogrel inactivation by carboxylesterase 1 and increased exposure to active metabolite. Drug Metab Dispos. 47(8):794–801.
  • Yao H, Gu J, Shan Y, Wang Y, Chen X, Sun D, Guo Y. 2020. Type 2 diabetes mellitus decreases systemic exposure of clopidogrel active metabolite through upregulation of P-glycoprotein in rats. Biochem Pharmacol. 180:114142.
  • Yao X, Xia F, Tang W, Xiao C, Yang M, Zhou B. 2018. Isobaric tags for relative and absolute quantitation (iTRAQ)-based proteomics for the investigation of the effect of Hugan Qingzhi on non-alcoholic fatty liver disease in rats. J Ethnopharmacol. 212:208–215.
  • Yin H, Huang L, Ouyang T, Chen L. 2018. Baicalein improves liver inflammation in diabetic db/db mice by regulating HMGB1/TLR4/NF-κB signaling pathway. Int Immunopharmacol. 55:55–62.
  • Yin OQP, Lam SSL, Lo CMY, Chow MSS. 2004. Rapid determination of five probe drugs and their metabolites in human plasma and urine by liquid chromatography/tandem mass spectrometry: application to cytochrome P450 phenotyping studies. Rapid Commun Mass Spectrom. 18(23):2921–2933.
  • Yokota H, Iwano H, Endo M, Kobayashi T, Inoue H, Ikushiro S, Yuasa A. 1999. Glucuronidation of the environmental oestrogen bisphenol A by an isoform of UDP-glucuronosyltransferase, UGT2B1, in the rat liver. Biochem J. 340(2):405–409.
  • Yoon HY, Cho YA, Yee J, Gwak HS. 2020. Effects of CYP2B6 polymorphisms on plasma nevirapine concentrations: a systematic review and meta-analysis. Sci Rep. 10(1):17390.
  • Zhang C, Deng J, Liu D, Tuo X, Xiao L, Lai B, Yao Q, Liu J, Yang H, Wang N. 2018. Nuciferine ameliorates hepatic steatosis in high-fat diet/streptozocin-induced diabetic mice through a PPARα/PPARγ coactivator-1α pathway. Br J Pharmacol. 175(22):4218–4228.
  • Zhang L, Chu X, Wang H, Xie H, Guo C, Cao L, Zhou X, Wang G, Hao H. 2013. Dysregulations of UDP-glucuronosyltransferases in rats with valproic acid and high fat diet induced fatty liver. Eur J Pharmacol. 721(1-3):277–285.
  • Zhang L, Xu P, Cheng Y, Wang P, Ma X, Liu M, Wang X, Xu F. 2019. Diet-induced obese alters the expression and function of hepatic drug-metabolizing enzymes and transporters in rats. Biochem Pharmacol. 164:368–376.
  • Zhang M-H, Li J, Zhu X-Y, Zhang Y-Q, Ye S-T, Leng Y-R, Yang T, Zhang H, Kong L-Y. 2021. Physalin B ameliorates nonalcoholic steatohepatitis by stimulating autophagy and NRF2 activation mediated improvement in oxidative stress. Free Radic Biol Med. 164:1–12.
  • Zhang S, Song N, Li Q, Fan H, Liu C. 2008. Liquid chromatography/tandem mass spectrometry method for simultaneous evaluation of activities of five cytochrome P450s using a five-drug cocktail and application to cytochrome P450 phenotyping studies in rats. J Chromatogr B Analyt Technol Biomed Life Sci. 871(1):78–89.
  • Zhang Y, Hou K, Liu F, Luo X, He S, Hu L, Yang C, Huang L, Feng Y. 2021. The influence of CYP2C19 polymorphisms on voriconazole trough concentrations: systematic review and meta-analysis. Mycoses. 64(8):860–873.
  • Zhang Y, Wen J, Liu D, Qiu Z, Zhu Q, Li R, Zhang Y. 2021. Demethylenetetrahydroberberine alleviates nonalcoholic fatty liver disease by inhibiting the NLRP3 inflammasome and oxidative stress in mice. Life Sci. 281:119778.
  • Zhao K, Ding M, Cao H, Cao Z-X. 2012. In-vitro metabolism of glycyrrhetinic acid by human and rat liver microsomes and its interactions with six CYP substrates. J Pharm Pharmacol. 64(10):1445–1451.
  • Zhao M, Ma J, Li M, Zhang Y, Jiang B, Zhao X, Huai C, Shen L, Zhang N, He L, et al. 2021. Cytochrome P450 enzymes and drug metabolism in humans. Int J Mol Sci. 22(23). DOI:10.3390/ijms222312808
  • Zheng W, Song Z, Li S, Hu M, Shaukat H, Qin H. 2021. Protective effects of sesamol against liver oxidative stress and inflammation in high-fat diet-induced hepatic steatosis. Nutrients. 13(12):4484.
  • Zheng Z-G, Zhu S-T, Cheng H-M, Zhang X, Cheng G, Thu PM, Wang SP, Li H-J, Ding M, Qiang L, et al. 2021. Discovery of a potent SCAP degrader that ameliorates HFD-induced obesity, hyperlipidemia and insulin resistance via an autophagy-independent lysosomal pathway. Autophagy. 17(7):1592–1613.
  • Zhong X, Liu H. 2018. Honokiol attenuates diet-induced non-alcoholic steatohepatitis by regulating macrophage polarization through activating peroxisome proliferator-activated receptor γ. J Gastroenterol Hepatol. 33(2):524–532.
  • Zhou J, Zhou F, Wang W, Zhang X-J, Ji Y-X, Zhang P, She Z-G, Zhu L, Cai J, Li H. 2020. Epidemiological features of NAFLD from 1999 to 2018 in China. Hepatology. 71(5):1851–1864.
  • Zhou L, Sharma P, Yeo KR, Higashimori M, Xu H, Al-Huniti N, Zhou D. 2019. Assessing pharmacokinetic differences in Caucasian and East Asian (Japanese, Chinese and Korean) populations driven by CYP2C19 polymorphism using physiologically-based pharmacokinetic modelling. Eur J Pharm Sci. 139:105061.
  • Zhou W, Johnson TN, Bui KH, Cheung SYA, Li J, Xu H, Al-Huniti N, Zhou D. 2018. Predictive performance of physiologically based pharmacokinetic (PBPK) modeling of drugs extensively metabolized by major cytochrome P450s in children. Clin Pharmacol Ther. 104(1):188–200.
  • Zhou X, Li Z, Qi M, Zhao P, Duan Y, Yang G, Yuan L. 2020. Brown adipose tissue-derived exosomes mitigate the metabolic syndrome in high fat diet mice. Theranostics. 10(18):8197–8210.
  • Zou Y, Li J, Lu C, Wang J, Ge J, Huang Y, Zhang L, Wang Y. 2006. High-fat emulsion-induced rat model of nonalcoholic steatohepatitis. Life Sci. 79(11):1100–1107.