Effects of dapagliflozin and/or insulin glargine on beta cell mass and hepatic steatosis in db/db mice

Metabolism: Clinical and Experimental

Volumn 98, Issue , 2019, Pages 27-36

  Omori, Kazuno ^a   Nakamura, Akinobu ^a   Miyoshi, Hideaki ^b   Takahashi, Kiyohiko ^a   Kitao, Naoyuki ^a   Nomoto, Hiroshi ^a   Kameda, Hiraku ^a   Cho, Kyu Yong ^a,c   Takagi, Ryo ^c   Hatanaka, Kanako C ^c   Terauchi, Yasuo ^d   Atsumi, Tatsuya ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c HOKKAIDO UNIVERSITY HOSPITAL   (Japan)

^d YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

Beta cell mass; Db db mice; Hepatic steatosis; SGLT2 inhibitor

Indexed keywords

DAPAGLIFLOZIN; INSULIN GLARGINE; TRIACYLGLYCEROL; 2-(3-(4-ETHOXYBENZYL)-4-CHLOROPHENYL)-6-HYDROXYMETHYLTETRAHYDRO-2H-PYRAN-3,4,5-TRIOL; ANTIDIABETIC AGENT; BENZHYDRYL DERIVATIVE; FATTY ACID; GLUCOSIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SIZE; CONTROLLED STUDY; DRUG EFFECT; FATTY ACID SYNTHESIS; FATTY LIVER; GENE EXPRESSION; GLUCOSE TOLERANCE; IMMUNOHISTOCHEMISTRY; LIPID LIVER LEVEL; LIPID STORAGE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; ANIMAL; BIOSYNTHESIS; COMPARATIVE STUDY; GLUCOSE INTOLERANCE; LIPID METABOLISM; LIVER; MALE; METABOLISM; NONALCOHOLIC FATTY LIVER; PHARMACOLOGY; ULTRASTRUCTURE;

ANIMALS; BENZHYDRYL COMPOUNDS; FATTY ACIDS; GENE EXPRESSION; GLUCOSE INTOLERANCE; GLUCOSIDES; HYPOGLYCEMIC AGENTS; INSULIN GLARGINE; INSULIN-SECRETING CELLS; LIPID METABOLISM; LIVER; MALE; MICE; NON-ALCOHOLIC FATTY LIVER DISEASE; SODIUM-GLUCOSE TRANSPORTER 2 INHIBITORS; TRIGLYCERIDES;

EID: 85067611098     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2019.06.006     Document Type: Article

References (40)

1. Taylor, S.I., Deconstructing type 2 diabetes. Cell. 97 (1999), 9–12.
2. Butler, A.E., Janson, J., Bonner-Weir, S., Ritzel, R., Rizza, R.A., Butler, P.C., Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52 (2003), 102–110.
3. Ferrannini, E., Gastaldelli, A., Miyazaki, Y., Matsuda, M., Mari, A., DeFronzo, R.A., Beta-cell function in subjects spanning the range from normal glucose tolerance to overt diabetes: a new analysis. J Clin Endocrinol Metab 90 (2005), 493–500.
4. Rhodes, C.J., Type 2 diabetes-a matter of beta-cell life and death?. Science (New York, NY) 307 (2005), 380–384.
5. Prentki, M., Nolan, C.J., Islet beta cell failure in type 2 diabetes. J Clin Invest 116 (2006), 1802–1812.
6. Kendall, D.M., Cuddihy, R.M., Bergenstal, R.M., Clinical application of incretin-based therapy: therapeutic potential, patient selection and clinical use. Am J Med 122 (2009), S37–S50.
7. Salunkhe, V.A., Veluthakal, R., Kahn, S.E., Thurmond, D.C., Novel approaches to restore beta cell function in prediabetes and type 2 diabetes. Diabetologia 61 (2018), 1895–1901.
8. Poitout, V., Robertson, R.P., Glucolipotoxicity: fuel excess and beta-cell dysfunction. Endocr Rev 29 (2008), 351–366.
9. Kaneto, H., Matsuoka, T.A., Kimura, T., Obata, A., Shimoda, M., Kamei, S., et al. Appropriate therapy for type 2 diabetes mellitus in view of pancreatic beta-cell glucose toxicity: “the earlier, the better”. J Diabetes 8 (2016), 183–189.
10. Takahashi, K., Nakamura, A., Miyoshi, H., Nomoto, H., Kitao, N., Omori, K., et al. Effect of the sodium-glucose cotransporter 2 inhibitor luseogliflozin on pancreatic beta cell mass in db/db mice of different ages. Sci Rep, 8, 2018, 6864.
11. Shao, Y., Yuan, G., Feng, Y., Zhang, J., Guo, X., Early liraglutide treatment is better in glucose control, beta-cell function improvement and mass preservation in db/db mice. Peptides. 52 (2014), 134–142.
12. Kimura, T., Kaneto, H., Shimoda, M., Hirukawa, H., Okauchi, S., Kohara, K., et al. Protective effects of pioglitazone and/or liraglutide on pancreatic beta-cells in db/db mice: comparison of their effects between in an early and advanced stage of diabetes. Mol Cell Endocrinol 400 (2015), 78–89.
13. Kimura, T., Obata, A., Shimoda, M., Okauchi, S., Kanda-Kimura, Y., Nogami, Y., et al. Protective effects of the SGLT2 inhibitor luseogliflozin on pancreatic beta-cells in db/db mice: the earlier and longer, the better. Diabetes Obes Metab 20 (2018), 2442–2457.
14. Weng, J., Li, Y., Xu, W., Shi, L., Zhang, Q., Zhu, D., et al. Effect of intensive insulin therapy on beta-cell function and glycaemic control in patients with newly diagnosed type 2 diabetes: a multicentre randomised parallel-group trial. Lancet (London, England) 371 (2008), 1753–1760.
15. Kawashima, S., Matsuoka, T.A., Kaneto, H., Tochino, Y., Kato, K., Yamamoto, K., et al. Effect of alogliptin, pioglitazone and glargine on pancreatic beta-cells in diabetic db/db mice. Biochem Biophys Res Commun 404 (2011), 534–540.
16. Nagata, T., Fukuzawa, T., Takeda, M., Fukazawa, M., Mori, T., Nihei, T., et al. Tofogliflozin, a novel sodium-glucose co-transporter 2 inhibitor, improves renal and pancreatic function in db/db mice. Br J Pharmacol 170 (2013), 519–531.
17. Terami, N., Ogawa, D., Tachibana, H., Hatanaka, T., Wada, J., Nakatsuka, A., et al. Long-term treatment with the sodium glucose cotransporter 2 inhibitor, dapagliflozin, ameliorates glucose homeostasis and diabetic nephropathy in db/db mice. PloS One, 9, 2014, e100777.
18. Okauchi, S., Shimoda, M., Obata, A., Kimura, T., Hirukawa, H., Kohara, K., et al. Protective effects of SGLT2 inhibitor luseogliflozin on pancreatic beta-cells in obese type 2 diabetic db/db mice. Biochem Biophys Res Commun 470 (2016), 772–782.
19. Ferrannini, E., Muscelli, E., Frascerra, S., Baldi, S., Mari, A., Heise, T., et al. Metabolic response to sodium-glucose cotransporter 2 inhibition in type 2 diabetic patients. J Clin Invest 124 (2014), 499–508.
20. Polidori, D., Mari, A., Ferrannini, E., Canagliflozin, a sodium glucose co-transporter 2 inhibitor, improves model-based indices of beta cell function in patients with type 2 diabetes. Diabetologia. 57 (2014), 891–901.
21. 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 64 (2017), 363–367.
22. Obata, A., Kubota, N., Kubota, T., Iwamoto, M., Sato, H., Sakurai, Y., et al. Tofogliflozin improves insulin resistance in skeletal muscle and accelerates lipolysis in adipose tissue in male mice. Endocrinology 157 (2016), 1029–1042.
23. Komiya, C., Tsuchiya, K., Shiba, K., Miyachi, Y., Furuke, S., Shimazu, N., et al. Ipragliflozin improves hepatic steatosis in obese mice and liver dysfunction in type 2 diabetic patients irrespective of body weight reduction. PloS one, 11, 2016, e0151511.
24. Kuchay, M.S., Krishan, S., Mishra, S.K., Farooqui, K.J., Singh, M.K., Wasir, J.S., et al. Effect of empagliflozin on liver fat in patients with type 2 diabetes and nonalcoholic fatty liver disease: a randomized controlled trial (E-LIFT trial). Diabetes Care 41 (2018), 1801–1808.
25. Kitao, N., Nakamura, A., Miyoshi, H., Nomoto, H., Takahashi, K., Omori, K., et al. The role of glucokinase and insulin receptor substrate-2 in the proliferation of pancreatic beta cells induced by short-term high-fat diet feeding in mice. Metab Clin Exp 85 (2018), 48–58.
26. Nomoto, H., Kondo, T., Miyoshi, H., Nakamura, A., Hida, Y., Yamashita, K., et al. Inhibition of small Maf function in pancreatic beta-cells improves glucose tolerance through the enhancement of insulin gene transcription and insulin secretion. Endocrinology. 156 (2015), 3570–3580.
27. Frantz, E.D., Aguila, M.B., Pinheiro-Mulder Ada, R., Mandarim-de-Lacerda, C.A., Transgenerational endocrine pancreatic adaptation in mice from maternal protein restriction in utero. Mech Ageing Dev 132 (2011), 110–116.
28. Kleiner, D.E., Brunt, E.M., Van Natta, M., Behling, C., Contos, M.J., Cummings, O.W., et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology (Baltimore, MD) 41 (2005), 1313–1321.
29. Marinho, T.S., Kawasaki, A., Bryntesson, M., Souza-Mello, V., Barbosa-da-Silva, S., Aguila, M.B., et al. Rosuvastatin limits the activation of hepatic stellate cells in diet-induced obese mice. Hepatol Res 47 (2017), 928–940.
30. Denechaud, P.D., Lopez-Mejia, I.C., Giralt, A., Lai, Q., Blanchet, E., Delacuisine, B., et al. E2F1 mediates sustained lipogenesis and contributes to hepatic steatosis. J Clin Invest 126 (2016), 137–150.
31. Zaccardi, F., Webb, D.R., Htike, Z.Z., Youssef, D., Khunti, K., Davies, M.J., Efficacy and safety of sodium-glucose co-transporter-2 inhibitors in type 2 diabetes mellitus: systematic review and network meta-analysis. Diabetes Obes Metab 18 (2016), 783–794.
32. Kanno, A., Asahara, S.I., Kawamura, M., Furubayashi, A., Tsuchiya, S., Suzuki, E., et al. Early administration of dapagliflozin preserves pancreatic beta-cell mass through a legacy effect in a mouse model of type 2 diabetes. J Diabetes Investig 10 (2019), 577–590.
33. Kubota, N., Terauchi, Y., Tobe, K., Yano, W., Suzuki, R., Ueki, K., et al. Insulin receptor substrate 2 plays a crucial role in beta cells and the hypothalamus. J Clin Invest 114 (2004), 917–927.
34. Kubota, N., Tobe, K., Terauchi, Y., Eto, K., Yamauchi, T., Suzuki, R., et al. Disruption of insulin receptor substrate 2 causes type 2 diabetes because of liver insulin resistance and lack of compensatory beta-cell hyperplasia. Diabetes. 49 (2000), 1880–1889.
35. Withers, D.J., Gutierrez, J.S., Towery, H., Burks, D.J., Ren, J.M., Previs, S., et al. Disruption of IRS-2 causes type 2 diabetes in mice. Nature. 391 (1998), 900–904.
36. Lee, Y.J., Ko, E.H., Kim, J.E., Kim, E., Lee, H., Choi, H., et al. Nuclear receptor PPARgamma-regulated monoacylglycerol O-acyltransferase 1 (MGAT1) expression is responsible for the lipid accumulation in diet-induced hepatic steatosis. Proc Natl Acad Sci U S A 109 (2012), 13656–13661.
37. Rahimian, R., Masih-Khan, E., Lo, M., van Breemen, C., McManus, B.M., Dube, G.P., Hepatic over-expression of peroxisome proliferator activated receptor gamma2 in the ob/ob mouse model of non-insulin dependent diabetes mellitus. Mol Cell Biochem 224 (2001), 29–37.
38. Schadinger, S.E., Bucher, N.L., Schreiber, B.M., Farmer, S.R., PPARgamma2 regulates lipogenesis and lipid accumulation in steatotic hepatocytes. Am J Physiol Endocrinol Metab 288 (2005), E1195–E1205.
39. Werman, A., Hollenberg, A., Solanes, G., Bjorbaek, C., Vidal-Puig, A.J., Flier, J.S., Ligand-independent activation domain in the N terminus of peroxisome proliferator-activated receptor gamma (PPARgamma). Differential activity of PPARgamma1 and -2 isoforms and influence of insulin. J Biol Chem 272 (1997), 20230–20235.
40. van Raalte, D.H., Verchere, C.B., Improving glycaemic control in type 2 diabetes: stimulate insulin secretion or provide beta-cell rest?. Diabetes Obes Metab 19 (2017), 1205–1213.