The selective SGLT2 inhibitor ipragliflozin has a therapeutic effect on nonalcoholic steatohepatitis in mice

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Honda, Yasushi ^a   Imajo, Kento ^a   Kato, Takayuki ^a   Kessoku, Takaomi ^a   Ogawa, Yuji ^a   Tomeno, Wataru ^a   Kato, Shingo ^a   Mawatari, Hironori ^a   Fujita, Koji ^a   Yoneda, Masato ^a   Saito, Satoru ^a   Nakajima, Atsushi ^a  

^a YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLIN; FATTY ACID; IPRAGLIFLOZIN; LIPID; SODIUM GLUCOSE COTRANSPORTER 2 INHIBITOR; ANTIDIABETIC AGENT; GLUCOSIDE; SODIUM GLUCOSE COTRANSPORTER 2; THIOPHENE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL FOOD; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CONTROLLED STUDY; DIET INDUCED OBESITY; DRUG EFFICACY; FATTY ACID BLOOD LEVEL; FATTY LIVER; HEPATITIS; INSULIN RESISTANCE; LIPID LIVER LEVEL; LIVER FIBROSIS; LIVER INJURY; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONALCOHOLIC FATTY LIVER; NONHUMAN; ANIMAL; ANTAGONISTS AND INHIBITORS; COMPLICATION; DISEASE MODEL; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; TREATMENT OUTCOME;

ANIMALS; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; GLUCOSIDES; HYPOGLYCEMIC AGENTS; INSULIN RESISTANCE; MICE; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; SODIUM-GLUCOSE TRANSPORTER 2; THIOPHENES; TREATMENT OUTCOME;

EID: 84953791948     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0146337     Document Type: Article

References (55)

1. Sanyal AJ. AGA technical review on nonalcoholic fatty liver disease. Gastroenterology. 2002; 123(5): 1705-1725. doi: 10.1053/gast.2002.36572
2. Marchesini G, Bugianesi E, Forlani G, Cerrelli F, Lenzi M, Manini R, et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology. 2003; 37(4): 917-923. doi: 10.1053/jhep.2003. 50161
3. Clark JM, Brancati FL, Diehl AM. Nonalcoholic fatty liver disease. Gastroenterology. 2002; 122(6): 1649-1657. doi: 10.1053/gast.2002.33573
4. Angulo P. Nonalcoholic Fatty Liver Disease. New England Journal of Medicine. 2002; 346(16): 1221-1231. doi: 10.1056/NEJMra011775 .
5. Jimba S, Nakagami T, Takahashi M, Wakamatsu T, Hirota Y, Iwamoto Y, et al. Prevalence of non-Alcoholic fatty liver disease and its association with impaired glucose metabolism in Japanese adults. Diabetic Medicine. 2005; 22(9): 1141-1145. doi: 10.1111/j.1464-5491.2005.01582.x
6. Corey KE, Kaplan LM. Obesity and Liver Disease: The Epidemic of the Twenty-First Century. Clinics in Liver Disease. 2014; 18(1): 1-18. doi: 10.1016/j.cld.2013.09.019
7. Yilmaz Y, Younossi ZM. Obesity-Associated Nonalcoholic Fatty Liver Disease. Clinics in Liver Disease. 2014; 18(1): 19-31. doi: 10.1016/j.cld.2013.09.018
8. Neuschwander-Tetri BA, Caldwell SH. Nonalcoholic steatohepatitis: Summary of an AASLD Single Topic Conference. Hepatology. 2003; 37(5): 1202-1219. doi: 10.1053/jhep.2003.50193
9. Dunn W, Schwimmer J. The obesity epidemic and nonalcoholic fatty liver disease in children. Curr Gastroenterol Rep. 2008; 10(1): 67-72. doi: 10.1007/s11894-008-0011-1
10. Matteoni CA, Younossi ZM, Gramlich T, Boparai N, Liu YC, McCullough AJ. Nonalcoholic fatty liver disease: A spectrum of clinical and pathological severity. Gastroenterology. 1999; 116(6): 1413-1419. doi: 10.1016/S0016-5085(99)70506-8
11. Lattuada G, Ragogna F, Perseghin G. Why Does NAFLD Predict Type 2 Diabetes? Curr Diab Rep. 2011; 11(3): 167-172. doi: 10.1007/s11892-011-0190-2
12. Gaggini M, Morelli M, Buzzigoli E, DeFronzo R, Bugianesi E, Gastaldelli A. Non-Alcoholic Fatty Liver Disease (NAFLD) and Its Connection with Insulin Resistance, Dyslipidemia, Atherosclerosis and Coronary Heart Disease. Nutrients. 2013; 5(5): 1544. doi: 10.3390/nu5051544
13. Cusi K. Role of Obesity and Lipotoxicity in the Development of Nonalcoholic Steatohepatitis: Pathophysiology and Clinical Implications. Gastroenterology. 2012; 142(4): 711-725.e6. doi: 10.1053/j. gastro.2012.02.003
14. Musso G, Cassader M, Rosina F, Gambino R. Impact of current treatments on liver disease, glucose metabolism and cardiovascular risk in non-Alcoholic fatty liver disease (NAFLD): a systematic review and meta-Analysis of randomised trials. Diabetologia. 2012; 55(4): 885-904. doi: 10.1007/s00125-011-2446-4
15. Chao EC, Henry RR. SGLT2 inhibition-A novel strategy for diabetes treatment. Nat Rev Drug Discov. 2010; 9(7): 551-559. doi: 10.1038/nrd3180
16. Tahara A, Kurosaki E, Yokono M, Yamajuku D, Kihara R, Hayashizaki Y, et al. Pharmacological profile of ipragliflozin (ASP1941), a novel selective SGLT2 inhibitor, in vitro and in vivo. Naunyn-Schmiedeberg's Arch Pharmacol. 2012; 385(4): 423-436. doi: 10.1007/s00210-011-0713-z
17. Imamura M, Nakanishi K, Suzuki T, Ikegai K, Shiraki R, Ogiyama T, et al. Discovery of Ipragliflozin (ASP1941): A novel C-glucoside with benzothiophene structure as a potent and selective sodium glucose co-Transporter 2 (SGLT2) inhibitor for the treatment of type 2 diabetes mellitus. Bioorganic & Medicinal Chemistry. 2012; 20(10): 3263-3279. doi: 10.1016/j.bmc.2012.03.051
18. Fonseca VA, Ferrannini E, Wilding JP, Wilpshaar W, Dhanjal P, Ball G, et al. Active-And placebo-controlled dose-finding study to assess the efficacy, safety, and tolerability of multiple doses of ipragliflozin in patients with type 2 diabetes mellitus. Journal of Diabetes and its Complications. 2013; 27(3): 268-273. doi: 10.1016/j.jdiacomp.2012.11.005
19. Kashiwagi A, Kazuta K, Goto K, Yoshida S, Ueyama E, Utsuno A. Ipragliflozin in combination with metformin for the treatment of Japanese patients with type 2 diabetes: ILLUMINATE, a randomized, double-blind, placebo-controlled study. Diabetes, Obesity and Metabolism. 2015; 17(3): 304-308. doi: 10. 1111/dom.12331
20. Tahara A, Kurosaki E, Yokono M, Yamajuku D, Kihara R, Hayashizaki Y, et al. Antidiabetic Effects of SGLT2-Selective Inhibitor Ipragliflozin in Streptozotocin-Nicotinamide-Induced Mildly Diabetic Mice. Journal of Pharmacological Sciences. 2012; 120(1): 36-44. doi: 10.1254/jphs.12089FP
21. Tahara A, Kurosaki E, Yokono M, Yamajuku D, Kihara R, Hayashizaki Y, et al. Effects of SGLT2 selective inhibitor ipragliflozin on hyperglycemia, hyperlipidemia, hepatic steatosis, oxidative stress, inflammation, and obesity in type 2 diabetic mice. European Journal of Pharmacology. 2013; 715(1-3): 246-255. doi: 10.1016/j.ejphar.2013.05.014
22. Tahara A, Kurosaki E, Yokono M, Yamajuku D, Kihara R, Hayashizaki Y, et al. Effects of sodium-glucose cotransporter 2 selective inhibitor ipragliflozin on hyperglycaemia, oxidative stress, inflammation and liver injury in streptozotocin-induced type 1 diabetic rats. Journal of Pharmacy and Pharmacology. 2014; 66(7): 975-987. doi: 10.1111/jphp.12223
23. Yokono M, Takasu T, Hayashizaki Y, Mitsuoka K, Kihara R, Muramatsu Y, et al. SGLT2 selective inhibitor ipragliflozin reduces body fat mass by increasing fatty acid oxidation in high-fat diet-induced obese rats. European Journal of Pharmacology. 2014; 727(0): 66-74. doi: 10.1016/j.ejphar.2014.01.040
24. Hayashizaki-Someya Y, Kurosaki E, Takasu T, Mitori H, Yamazaki S, Koide K, 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 .
25. Rinella ME, Elias MS, Smolak RR, Fu T, Borensztajn J, Green RM. Mechanisms of hepatic steatosis in mice fed a lipogenic methionine choline-deficient diet. J Lipid Res. 2008; 49(5): 1068-1076. doi: 10. 1194/jlr.M800042-JLR200
26. Clapper JR, Hendricks MD, Gu G, Wittmer C, Dolman CS, Herich J, et al. Diet-induced mouse model of fatty liver disease and nonalcoholic steatohepatitis reflecting clinical disease progression and methods of assessment. Am J Physiol Gastrointest Liver Physiol. 2013; 305(7): G483-495. doi: 10.1152/ajpgi. 00079.2013 .
27. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005; 41(6): 1313-1321. doi: 10.1002/hep.20701
28. Ferré P, Foufelle F. Hepatic steatosis: a role for de novo lipogenesis and the transcription factor SREBP-1c. Diabetes, Obesity and Metabolism. 2010; 12: 83-92. doi: 10.1111/j.1463-1326.2010. 01275.x
29. Tailleux A, Wouters K, Staels B. Roles of PPARs in NAFLD: Potential therapeutic targets. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids. 2012; 1821(5): 809-818. doi: 10.1016/j.bbalip.2011.10.016
30. Reddy JK, Sambasiva Rao M. Lipid Metabolism and Liver Inflammation. II. Fatty liver disease and fatty acid oxidation 2006 2006-05-01 00:00:00. G852-G8 p. 10.1152/ajpgi.00521.2005.
31. Lefebvre P, Chinetti G, Fruchart J-C, Staels B. Sorting out the roles of PPARα in energy metabolism and vascular homeostasis. The Journal of Clinical Investigation. 2006; 116(3): 571-580. doi: 10.1172/JCI27989
32. Gordon DA, Jamil H. Progress towards understanding the role of microsomal triglyceride transfer protein in apolipoprotein-B lipoprotein assembly. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids. 2000; 1486(1):72-83. doi: 10.1016/S1388-1981(00)00049-4
33. Feldstein AE, Canbay A, Angulo P, Taniai M, Burgart LJ, Lindor KD, et al. Hepatocyte apoptosis and fas expression are prominent features of human nonalcoholic steatohepatitis. Gastroenterology. 2003; 125(2): 437-443. doi: 10.1016/S0016-5085(03)00907-7
34. Susca M, Grassi A, Zauli D, Volta U, Lenzi M, Marchesini G, et al. Liver inflammatory cells, apoptosis, regeneration and stellate cell activation in non-Alcohol steatohepatitis. Digestive and Liver Disease. 2001; 33(9): 768-777. doi: 10.1016/S1590-8658(01)80694-0
35. Promrat K, Kleiner DE, Niemeier HM, Jackvony E, Kearns M, Wands JR, et al. Randomized controlled trial testing the effects of weight loss on nonalcoholic steatohepatitis. Hepatology. 2010; 51(1): 121-129. doi: 10.1002/hep.23276
36. Vernon G, Baranova A, Younossi ZM. Systematic review: the epidemiology and natural history of nonalcoholic fatty liver disease and non-Alcoholic steatohepatitis in adults. Alimentary Pharmacology & Therapeutics. 2011; 34(3): 274-285. doi: 10.1111/j.1365-2036.2011.04724.x
37. Sanyal AJ, Chalasani N, Kowdley KV, McCullough A, Diehl AM, Bass NM, et al. Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. N Engl J Med. 2010; 362(18): 1675-1685. doi: 10.1056/NEJMoa0907929
38. Lincoff A, Wolski K, Nicholls SJ, Nissen SE. Pioglitazone and risk of cardiovascular events in patients with type 2 diabetes mellitus: A meta-Analysis of randomized trials. JAMA. 2007; 298(10): 1180-1188. doi: 10.1001/jama.298.10.1180
39. Cefalu WT, Leiter LA, Yoon K-H, Arias P, Niskanen L, Xie J, et al. Efficacy and safety of canagliflozin versus glimepiride in patients with type 2 diabetes inadequately controlled with metformin (CANTATASU): 52 week results from a randomised, double-blind, phase 3 non-inferiority trial. The Lancet. 2013; 382(9896): 941-950. doi: 10.1016/s0140-6736(13)60683-2
40. Samuel Varman T, Shulman Gerald I. Mechanisms for Insulin Resistance: Common Threads and Missing Links. Cell. 2012; 148(5): 852-871. doi: 10.1016/j.cell.2012.02.017
41. Tilg H, Moschen AR. Insulin resistance, inflammation, and non-Alcoholic fatty liver disease. Trends in Endocrinology & Metabolism. 2008; 19(10): 371-379. doi: 10.1016/j.tem.2008.08.005
42. Arner P. Insulin resistance in type 2 diabetes: role of fatty acids. Diabetes/Metabolism Research and Reviews. 2002; 18(S2): S5-S9. doi: 10.1002/dmrr.254
43. Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. Journal of Clinical Investigation. 2005; 115(5): 1343-1351. doi: 10.1172/jci200523621
44. Tilg H, Moschen AR. Evolution of inflammation in nonalcoholic fatty liver disease: The multiple parallel hits hypothesis. Hepatology. 2010; 52(5): 1836-1846. doi: 10.1002/hep.24001
45. Malhi H, Gores GJ. Molecular Mechanisms of Lipotoxicity in Nonalcoholic Fatty Liver Disease. Semin Liver Dis. 2008; 28(04): 360-369. doi: 10.1055/s-0028-1091980
46. Listenberger LL, Han X, Lewis SE, Cases S, Farese RV, Ory DS, et al. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proceedings of the National Academy of Sciences of the United States of America. 2003; 100(6): 3077-3082. doi: 10.1073/pnas.0630588100 PMC152249.
47. Brunt EM. Histopathology of Non-Alcoholic Fatty Liver Disease. Clinics in Liver Disease. 2009; 13 (4):533-44. doi: 10.1016/j.cld.2009.07.008
48. Anderson N, Borlak J. Molecular Mechanisms and Therapeutic Targets in Steatosis and Steatohepatitis. Pharmacological Reviews. 2008; 60(3): 311-357. doi: 10.1124/pr.108.00001
49. Tetri LH, Basaranoglu M, Brunt EM, Yerian LM, Neuschwander-Tetri BA. Severe NAFLD with hepatic necroinflammatory changes in mice fed trans fats and a high-fructose corn syrup equivalent. American Journal of Physiology-Gastrointestinal and Liver Physiology. 2008; 295(5): G987-G95. doi: 10.1152/ajpgi.90272.2008
50. Grasselli E, Voci A, Demori I, De Matteis R, Compalati A, Gallo G, et al. Effects of binge ethanol on lipid homeostasis and oxidative stress in a rat model of nonalcoholic fatty liver disease. J Physiol Biochem. 2014; 70(2): 341-353. doi: 10.1007/s13105-013-0308-x
51. Fujita K, Nozaki Y, Wada K, Yoneda M, Fujimoto Y, Fujitake M, et al. Dysfunctional very-low-density lipoprotein synthesis and release is a key factor in nonalcoholic steatohepatitis pathogenesis. Hepatology. 2009; 50(3): 772-780. doi: 10.1002/hep.23094 .
52. Pawlak M, Lefebvre P, Staels B. Molecular mechanism of PPARα action and its impact on lipid metabolism, inflammation and fibrosis in non-Alcoholic fatty liver disease. Journal of Hepatology. 2015; 62(3): 720-733. doi: 10.1016/j.jhep.2014.10.039
53. Bonnefont J-P, Djouadi F, Prip-Buus C, Gobin S, Munnich A, Bastin J. Carnitine palmitoyltransferases 1 and 2: biochemical, molecular and medical aspects. Molecular Aspects of Medicine. 2004; 25(5-6): 495-520. doi: 10.1016/j.mam.2004.06.004
54. Navasa M, Gordon DA, Hariharan N, Jamil H, Shigenaga JK, Moser A, et al. Regulation of microsomal triglyceride transfer protein mRNA expression by endotoxin and cytokines. Journal of Lipid Research. 1998; 39(6): 1220-1230.
55. Zhang L, Feng Y, List J, Kasichayanula S, Pfister M. Dapagliflozin treatment in patients with different stages of type 2 diabetes mellitus: effects on glycaemic control and body weight. Diabetes, Obesity and Metabolism. 2010; 12(6): 510-516. doi: 10.1111/j.1463-1326.2010.01216.x