Therapeutic Effects of SGLT2 Inhibitor Ipragliflozin and Metformin on NASH in Type 2 Diabetic Mice

References

• Wattacheril J, Issa D, Sanyal A. Nonalcoholic steatohepatitis (NASH) and hepatic fibrosis: emerging therapies. In: Insel PA, ed. Annual Review of Pharmacology and Toxicology. Vol. 58; 2018: 649–662. doi:10.1146/annurev-pharmtox-010617-052545.
   Google Scholar
• McCullough AJ. Pathophysiology of nonalcoholic steatohepatitis. J Clin Gastroenterol. 2006;40:S17–S29. doi: 10.1097/01.mcg.0000168645.86658.22
   PubMed Web of Science ®Google Scholar
• Marchesini G, Bugianesi E, Forlani G, et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology. 2003;37:917–923. doi:10.1053/jhep.2003.50161.
   PubMed Web of Science ®Google Scholar
• Mavrogiannaki AN, Migdalis IN. Nonalcoholic fatty liver disease, diabetes mellitus and cardiovascular disease: newer data. Int J Endocrinol. 2013;2013:450639. doi: 10.1155/2013/450639.
   PubMedGoogle Scholar
• Barb D, Portillo-Sanchez P, Cusi K. Pharmacological management of nonalcoholic fatty liver disease. Metab Clin Exp. 2016;65:1183–1195. doi:10.1016/j.metabol.2016.04.004.
   PubMed Web of Science ®Google Scholar
• Boettcher E, Csako G, Pucino F, Wesley R, Loomba R. Meta-analysis: pioglitazone improves liver histology and fibrosis in patients with non-alcoholic steatohepatitis. Aliment Pharmacol Ther. 2012;35:66–75. doi:10.1111/j.1365-2036.2011.04912.x.
   PubMed Web of Science ®Google Scholar
• Li Y, Liu L, Wang B, Wang J, Chen D. Metformin in non-alcoholic fatty liver disease: A systematic review and meta-analysis. Biomed Rep. 2013;1:57–64. doi:10.3892/br.2012.18.
   PubMedGoogle Scholar
• Portillo-Sanchez P, Cusi K. Treatment of nonalcoholic fatty liver disease (NAFLD) in patients with type 2 diabetes mellitus. Clin Diabetes Endocrinol. 2016;2:9. doi:10.1186/s40842-016-0027-7.
   PubMedGoogle Scholar
• Chao EC. SGLT-2 Inhibitors: A New Mechanism for Glycemic Control. Clin Diabetes. 2014;32:4–11. doi:10.2337/diaclin.32.1.4.
   PubMedGoogle Scholar
• Kurosaki E, Ogasawara H. Ipragliflozin and other sodium-glucose cotransporter-2 (SGLT2) inhibitors in the treatment of type 2 diabetes: preclinical and clinical data. Pharmacol Ther. 2013;139:51–59. doi:10.1016/j.pharmthera.2013.04.003.
   PubMed Web of Science ®Google Scholar
• Takase T, Nakamura A, Miyoshi H, Yamamoto C, Atsumi T. Amelioration of fatty liver index in patients with type 2 diabetes on ipragliflozin: an association with glucose-lowering effects. Endocr J. 2017;64:363–367. doi:10.1507/endocrj.EJ16-0295.
   PubMed Web of Science ®Google Scholar
• Tahara A, Kurosaki E, Yokono M, et al. Effects of SGLT2 selective inhibitor ipragliflozin on hyperglycemia, hyperlipidemia, hepatic steatosis, oxidative stress, inflammation, and obesity in type 2 diabetic mice. Eur J Pharmacol. 2013;715:246–255. doi:10.1016/j.ejphar.2013.05.014.
   PubMed Web of Science ®Google Scholar
• Hayashizaki-Someya Y, Kurosaki E, Takasu T, et al. Ipragliflozin, an SGLT2 inhibitor, exhibits a prophylactic effect on hepatic steatosis and fibrosis induced by choline-deficient L-amino acid-defined diet in rats. Eur J Pharmacol. 2015;754:19–24. doi:10.1016/j.ejphar.2015.02.009.
   PubMed Web of Science ®Google Scholar
• Tahara A, Matsuyama-Yokono A, Shibasaki M. Effects of antidiabetic drugs in high-fat diet and streptozotocin-nicotinamide-induced type 2 diabetic mice. Eur J Pharmacol. 2011;655:108–116. doi:10.1016/j.ejphar.2011.01.015.
   PubMed Web of Science ®Google Scholar
• Nakhaee A, Bokaeian M, Saravani M, Farhangi A, Akbarzadeh A. Attenuation of oxidative stress in streptozotocin-induced diabetic rats by Eucalyptus globulus. Indian J Clin Biochem. 2009;24:419-425. doi:10.1007/s12291-009-0075-1.
   PubMedGoogle Scholar
• Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care. 1999;22:1462–1470. doi:10.2337/diacare.22.9.1462.
   PubMed Web of Science ®Google Scholar
• Anstee QM, Goldin RD. Mouse models in non-alcoholic fatty liver disease and steatohepatitis research. Int J Exp Pathol. 2006;87:1–16. doi:10.1111/j.0959-9673.2006.00465.x.
   PubMed Web of Science ®Google Scholar
• Ibrahim SH, Hirsova P, Malhi H, Gores GJ. Animal models of nonalcoholic steatohepatitis: eat, delete, and inflame. Dig Dis Sci. 2016;61:1325–1336. doi:10.1007/s10620-015-3977-1.
   PubMed Web of Science ®Google Scholar
• Nakamura A, Terauchi Y. Lessons from mouse models of high-fat diet-induced NAFLD. Int J Mol Sci. 2013;14:21240–21257. doi:10.3390/ijms141121240.
   PubMed Web of Science ®Google Scholar
• Takaki A, Kawai D, Yamamoto K. Multiple Hits, Including Oxidative Stress, as Pathogenesis and Treatment Target in Non-Alcoholic Steatohepatitis (NASH). Int J Mol Sci. 2013;14:20704–20728. doi:10.3390/ijms141020704.
   PubMed Web of Science ®Google Scholar
• Hansen HH, Feigh M, Veidal SS, Rigbolt KT, Vrang N, Fosgerau K. Mouse models of nonalcoholic steatohepatitis in preclinical drug development. Drug Discov Today. 2017;22:1707–1718. doi:10.1016/j.drudis.2017.06.007.
   PubMed Web of Science ®Google Scholar
• Okumura K, Ikejima K, Kon K, et al. Exacerbation of dietary steatohepatitis and fibrosis in obese, diabetic KK-Ay mice. Gastroenterology. 2005;128:A703–A703. doi:10.1016/j.hepres.2006.07.009
   Web of Science ®Google Scholar
• Yokono M, Takasu T, Hayashizaki Y, et al. SGLT2 selective inhibitor ipragliflozin reduces body fat mass by increasing fatty acid oxidation in high-fat diet-induced obese rats. Eur J Pharmacol. 2014;727:66–74. doi:10.1016/j.ejphar.2014.01.040.
   PubMed Web of Science ®Google Scholar
• Bugianesi E, McCullough AJ, Marchesini G. Insulin resistance: A metabolic pathway to chronic liver disease. Hepatology. 2005;42:987–1000. doi:10.1002/hep.v42:5.
   PubMed Web of Science ®Google Scholar
• Thoma C, Day CP, Trenell MI. Lifestyle interventions for the treatment of non-alcoholic fatty liver disease in adults: A systematic review. J Hepatol. 2012;56:255–266. doi:10.1016/j.jhep.2011.06.010.
   PubMed Web of Science ®Google Scholar
• Honda Y, Imajo K, Kato T, et al. The selective SGLT2 inhibitor ipragliflozin has a therapeutic effect on nonalcoholic steatohepatitis in mice. Plos One. 2016;11:e0146337. doi: 10.1371/journal.pone.0146337.
   Web of Science ®Google Scholar
• Obata A, Kubota N, Kubota T, et al. Tofogliflozin improves insulin resistance in skeletal muscle and accelerates lipolysis in adipose tissue in male mice. Endocrinology. 2016;157:1029–1042. doi:10.1210/en.2015-1588.
   PubMed Web of Science ®Google Scholar
• Basaranoglu M, Basaranoglu G, Senturk H. From fatty liver to fibrosis: A tale of “second hit”. World J Gastroenterol. 2013;19:1158–1165. doi:10.3748/wjg.v19.i8.1158.
   PubMed Web of Science ®Google Scholar
• Wu CW, Chu ES, Lam CN, et al. PPARgamma is essential for protection against nonalcoholic steatohepatitis. Gene Ther. 2010;17:790–798. doi:10.1038/gt.2010.41.
   PubMed Web of Science ®Google Scholar
• Sumida Y, Niki E, Naito Y, Yoshikawa T. Special issue on “Oxidative stress and redox signaling in the gastrointestinal tract and related organs” for free radical research involvement of free radicals and oxidative stress in NAFLD/NASH. Free Radic Res. 2013;47:869–880. doi:10.3109/10715762.2013.837577.
   PubMed Web of Science ®Google Scholar
• Nair S, Diehl AM, Wiseman M, Farr GH, Perrillo RP. Metformin in the treatment of non-alcoholic steatohepatitis: a pilot open label trial. Aliment Pharmacol Ther. 2004;20:23–28. doi:10.1111/apt.2004.20.issue-1.
   PubMed Web of Science ®Google Scholar
• Van Wagner LB, Rinella ME. The role of insulin-sensitizing agents in the treatment of nonalcoholic steatohepatitis. Therap Adv Gastroenterol. 2011;4:249–263. doi:10.1177/1756283X11403809.
   PubMedGoogle Scholar
• Xu H, Zhou Y, Liu YX, et al. Metformin improves hepatic IRS2/PI3K/Akt signaling in insulin-resistant rats of NASH and cirrhosis. J Endocrinol. 2016;229:133–144. doi:10.1530/JOE-15-0409.
   PubMed Web of Science ®Google Scholar
• Mazza A, Fruci B, Garinis GA, Giuliano S, Malaguarnera R, Belfiore A. The role of metformin in the management of NAFLD. Exp Diabetes Res. 2012. doi:10.1155/2012/716404.
   PubMedGoogle Scholar
• Marchesini G, Brizi M, Bianchi G, et al. Nonalcoholic fatty liver disease - A feature of the metabolic syndrome. Diabetes. 2001;50:1844–1850. doi:10.2337/diabetes.50.8.1844.
   PubMed Web of Science ®Google Scholar
• Yki-Jarvinen H, Nikkila K, Makimattila S. Metformin prevents weight gain by reducing dietary intake during insulin therapy in patients with type 2 diabetes mellitus. Drugs. 1999;58:53–54. doi:10.2165/00003495-199958001-00012.
   PubMed Web of Science ®Google Scholar
• Kita Y, Takamura T, Misu H, et al. Metformin prevents and reverses inflammation in a non-diabetic mouse model of nonalcoholic steatohepatitis. Plos One. 2012;7:e43056. doi:10.1371/journal.pone.0043056 .
   Web of Science ®Google Scholar
• Tahara A, Takasu T, Yokono M, Imamura M, Kurosaki E. Effects of the combination of SGLT2 selective inhibitor ipragliflozin and various antidiabetic drugs in type 2 diabetic mice. Arch Pharm Res. 2016;39:259–270. doi:10.1007/s12272-015-0621-8.
   PubMed Web of Science ®Google Scholar
• Takasu T, Hayashizaki Y, Tahara A, Kurosaki E, Takakura S. Antihyperglycemic effect of ipragliflozin, a sodium-glucose co-transporter 2 inhibitor, in combination with oral antidiabetic drugs in mice. Clin Exp Pharmacol Physiol. 2015;42:87–93. doi:10.1111/cep.2014.42.issue-1.
   PubMed Web of Science ®Google Scholar
• Haukeland JW, Konopski Z, Eggesbo HB, et al. Metformin in patients with non-alcoholic fatty liver disease: a randomized, controlled trial. Scand J Gastroenterol. 2009;44:853-860. doi:10.1080/00365520902845268
   PubMed Web of Science ®Google Scholar