Intestinal sodium glucose cotransporter 1 inhibition enhances glucagon-like peptide-1 secretion in normal and diabetic rodents

Journal of Pharmacology and Experimental Therapeutics

Volumn 354, Issue 3, 2015, Pages 279-289

  Oguma, Takahiro ^a   Nakayama, Keiko ^a   Kuriyama, Chiaki ^a   Matsushita, Yasuaki ^a   Yoshida, Kumiko ^a   Hikida, Kumiko ^a   Obokata, Naoyuki ^a   Tsuda Tsukimoto, Minoru ^a   Saito, Akira ^a   Arakawa, Kenji ^a   Ueta, Kiichiro ^a   Shiotani, Masaharu ^a  

^a MITSUBISHI TANABE PHARMA CORPORATION   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CANAGLIFLOZIN; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; INSULIN; PHLORIZIN; SITAGLIPTIN; SODIUM GLUCOSE COTRANSPORTER 1; SODIUM GLUCOSE COTRANSPORTER INHIBITOR; VOGLIBOSE; ANTIDIABETIC AGENT; DIPEPTIDYL PEPTIDASE IV; SODIUM GLUCOSE COTRANSPORTER 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOHYDRATE ABSORPTION; CARBOHYDRATE ANALYSIS; DIABETES MELLITUS; DRUG EFFICACY; DRUG RESPONSE; DRUG SELECTIVITY; GLUCOSE ABSORPTION; GLUCOSE TOLERANCE; IC50; INSULIN BLOOD LEVEL; INTESTINE ABSORPTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN SECRETION; ZUCKER DIABETIC FATTY RAT; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; C57BL MOUSE; CHO CELL LINE; CRICETULUS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DRUG EFFECTS; HUMAN; HYPERGLYCEMIA; INTESTINE; METABOLISM; RAT; SPRAGUE DAWLEY RAT; ZUCKER RAT;

ANIMALS; CHO CELLS; CRICETULUS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DIPEPTIDYL PEPTIDASE 4; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; HUMANS; HYPERGLYCEMIA; HYPOGLYCEMIC AGENTS; INTESTINAL ABSORPTION; INTESTINES; MALE; MICE; MICE, INBRED C57BL; RATS; RATS, SPRAGUE-DAWLEY; RATS, ZUCKER; SODIUM-GLUCOSE TRANSPORTER 1; SODIUM-GLUCOSE TRANSPORTER 2;

EID: 84941585324     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.115.225508     Document Type: Article

References (54)

1. Abdul-Ghani MA, DeFronzo RA, and Norton L (2013) Novel hypothesis to explain why SGLT2 inhibitors inhibit only 30-50% of filtered glucose load in humans. Diabetes 62:3324-3328.
2. Arakawa K, Ishihara T, Oku A, Nawano M, Ueta K, Kitamura K, Matsumoto M, and Saito A (2001) Improved diabetic syndrome in C57BL/KsJ-db/db mice by oral administration of the Na(1)-glucose cotransporter inhibitor T-1095. Br J Pharmacol 132:578-586.
3. Bennett WL, Odelola OA, Wilson LM, Bolen S, Selvaraj S, Robinson KA, Bass EB, and Puhan MA (2012) Evaluation of guideline recommendations on oral medications for type 2 diabetes mellitus: A systematic review. Ann Intern Med 156: 27-36.
4. Bischoff H (1994) Pharmacology of alpha-glucosidase inhibition. Eur J Clin Invest 24 (Suppl 3):3-10.
5. Blonde L (2010) Current antihyperglycemic treatment guidelines and algorithms for patients with type 2 diabetes mellitus. Am J Med 123 (Suppl):S12-S18.
6. Cefalu WT, Leiter LA, Yoon KH, Arias P, Niskanen L, Xie J, Balis DA, Canovatchel W, and Meininger G (2013) Efficacy and safety of canagliflozin versus glimepiride in patients with type 2 diabetes inadequately controlled with metformin (CANTATA-SU): 52 week results from a randomised, double-blind, phase 3 noninferiority trial. Lancet 382:941-950.
7. Chen J, Williams S, Ho S, Loraine H, Hagan D, Whaley JM, and Feder JN (2010) Quantitative PCR tissue expression profiling of the human SGLT2 gene and related family members. Diabetes Ther 1:57-92.
8. Drucker DJ (2003) Enhancing incretin action for the treatment of type 2 diabetes. Diabetes Care 26:2929-2940.
9. Fleming WW, Westfall DP, De la Lande IS, and Jellett LB (1972) Log-normal distribution of equiefective doses of norepinephrine and acetylcholine in several tissues. J Pharmacol Exp Ther 181:339-345.
10. Franz T and Li X (2012) The OASIS HLB mElution plate as a one-step platform for manual high-throughput in-gel digestion of proteins and peptide desalting. Proteomics 12:2487-2492.
11. Freeman TC, Wood IS, Sirinathsinghji DJ, Beechey RB, Dyer J, and Shirazi-Beechey SP (1993) The expression of the Na1/glucose cotransporter (SGLT1) gene in lamb small intestine during postnatal development. Biochim Biophys Acta 1146: 203-212.
12. Freitas HS, Anhê GF, Melo KF, Okamoto MM, Oliveira-Souza M, Bordin S, and Machado UF (2008) Na(1) -glucose transporter-2 messenger ribonucleic acid expression in kidney of diabetic rats correlates with glycemic levels: involvement of hepatocyte nuclear factor-1alpha expression and activity. Endocrinology 149: 717-724.
13. Fukuda-Tsuru S, Anabuki J, Abe Y, Yoshida K, and Ishii S (2012) A novel, potent, and long-lasting dipeptidyl peptidase-4 inhibitor, teneligliptin, improves postprandial hyperglycemia and dyslipidemia after single and repeated administrations. Eur J Pharmacol 696:194-202.
14. Gerich JE (2010) Role of the kidney in normal glucose homeostasis and in the hyperglycaemia of diabetes mellitus: Therapeutic implications. Diabet Med 27: 136-142.
15. Göke B, Herrmann C, Göke R, Fehmann HC, Berghöfer P, Richter G, and Arnold R (1994) Intestinal effects of alpha-glucosidase inhibitors: Absorption of nutrients and enterohormonal changes. Eur J Clin Invest 24 (Suppl 3):25-30.
16. Gorboulev V, Schürmann A, Vallon V, Kipp H, Jaschke A, Klessen D, Friedrich A, Scherneck S, Rieg T, Cunard R, et al. (2012) Na(1)-D-glucose cotransporter SGLT1 is pivotal for intestinal glucose absorption and glucose-dependent incretin secretion. Diabetes 61:187-196.
17. Grempler R, Thomas L, Eckhardt M, Himmelsbach F, Sauer A, Sharp DE, Bakker RA, Mark M, Klein T, and Eickelmann P (2012) Empagliflozin, a novel selective sodium glucose cotransporter-2 (SGLT-2) inhibitor: characterisation and comparison with other SGLT-2 inhibitors. Diabetes Obes Metab 14:83-90.
18. Gromada J, Holst JJ, and Rorsman P (1998) Cellular regulation of islet hormone secretion by the incretin hormone glucagon-like peptide 1. Pflugers Arch 435: 583-594.
19. Hediger MA, Kanai Y, You G, and Nussberger S (1995) Mammalian ion-coupled solute transporters. J Physiol 482:7S-17S.
20. Hwee DT, Kennedy AR, Hartman JJ, Ryans J, Durham N, Malik FI, and Jasper JR (2015) The small-molecule fast skeletal troponin activator, CK-2127107, improves exercise tolerance in a rat model of heart failure. J Pharmacol Exp Ther 353: 159-168.
21. Inzucchi SE, Bergenstal RM, Buse JB, Diamant M, Ferrannini E, Nauck M, Peters AL, Tsapas A, Wender R, and Matthews DR; American Diabetes Association (ADA); European Association for the Study of Diabetes (EASD) (2012) Management of hyperglycemia in type 2 diabetes: A patient-centered approach: position statement of the American Diabetes Association (ADA) and the European Association for the Study of Diabetes (EASD). Diabetes Care 35:1364-1379.
22. Kahn SE, Haffner SM, Heise MA, Herman WH, Holman RR, Jones NP, Kravitz BG, Lachin JM, O'Neill MC, Zinman B, et al.; ADOPT Study Group (2006) Glycemic durability of rosiglitazone, metformin, or glyburide monotherapy. N Engl J Med 355:2427-2443.
23. Kanai Y, Lee WS, You G, Brown D, and Hediger MA (1994a) The human kidney low affinity Na1/glucose cotransporter SGLT2. Delineation of the major renal reabsorptive mechanism for D-glucose. J Clin Invest 93:397-404.
24. Kanai Y, Nussberger S, Romero MF, Boron WF, Hebert SC, and Hediger MA (1995) Electrogenic properties of the epithelial and neuronal high affinity glutamate transporter. J Biol Chem 270:16561-16568.
25. Kanai Y, Stelzner M, Nussberger S, Khawaja S, Hebert SC, Smith CP, and Hediger MA (1994b) The neuronal and epithelial human high affinity glutamate transporter. Insights into structure and mechanism of transport. J Biol Chem 269: 20599-20606.
26. Kinoshita S and Kondo K (2015) Evaluation of pharmacokinetic and pharmacodynamic interactions of canagliflozin and teneligliptin in Japanese healthy male volunteers. Expert Opin Drug Metab Toxicol 11:7-14.
27. Kuriyama C, Xu JZ, Lee SP, Qi J, Kimata H, Kakimoto T, Nakayama K, Watanabe Y, Taniuchi N, Hikida K, et al. (2014) Analysis of the effect of canagliflozin on renal glucose reabsorption and progression of hyperglycemia in Zucker diabetic Fatty rats. J Pharmacol Exp Ther 351:423-431.
28. Leahy JL, Bonner-Weir S, and Weir GC (1992) Beta-cell dysfunction induced by chronic hyperglycemia. Current ideas on mechanism of impaired glucose-induced insulin secretion. Diabetes Care 15:442-455.
29. Liang Y, Arakawa K, Ueta K, Matsushita Y, Kuriyama C, Martin T, Du F, Liu Y, Xu J, Conway B, et al. (2012) Effect of canagliflozin on renal threshold for glucose, glycemia, and body weight in normal and diabetic animal models. PLoS One 7: e30555.
30. Martin AE and Montgomery PA (1996) Acarbose: An alpha-glucosidase inhibitor. Am J Health Syst Pharm 53:2277-2290.
31. McConnell EL, Basit AW, and Murdan S (2008) Measurements of rat and mouse gastrointestinal pH, fluid and lymphoid tissue, and implications for in-vivo experiments. J Pharm Pharmacol 60:63-70.
32. Mitsumoto Y, Burdett E, Grant A, and Klip A (1991) Differential expression of the GLUT1 and GLUT4 glucose transporters during differentiation of L6 muscle cells. Biochem Biophys Res Commun 175:652-659.
33. Moriya R, Shirakura T, Ito J, Mashiko S, and Seo T (2009) Activation of sodiumglucose cotransporter 1 ameliorates hyperglycemia by mediating incretin secretion in mice. Am J Physiol Endocrinol Metab 297:E1358-E1365.
34. Nathan DM (1993) Long-term complications of diabetes mellitus. N Engl J Med 328: 1676-1685.
35. Nauck MA, Holst JJ, Willms B, and Schmiegel W (1997) Glucagon-like peptide 1 (GLP-1) as a new therapeutic approach for type 2-diabetes. Exp Clin Endocrinol Diabetes 105:187-195.
36. Nomura S, Sakamaki S, Hongu M, Kawanishi E, Koga Y, Sakamoto T, Yamamoto Y, Ueta K, Kimata H, Nakayama K, et al. (2010) Discovery of canagliflozin, a novel C-glucoside with thiophene ring, as sodium-dependent glucose cotransporter 2 inhibitor for the treatment of type 2 diabetes mellitus. J Med Chem 53:6355-6360.
37. Nomura S, Yamamoto Y, Matsumura Y, Ohba K, Sakamaki S, Kimata H, Nakayama K, Kuriyama C, Matsushita Y, Ueta K, et al. (2014) Novel indole-N-glucoside, TA- 1887 as a sodium glucose cotransporter 2 inhibitor for treatment of type 2 diabetes. ACS Med Chem Lett 5:51-55.
38. Oguma T, Kuriyama C, Nakayama K, Matsushita Y, Yoshida K, Kiuchi S, Ikenaga Y, Nakamaru Y, Hikida K, Saito A, et al. (2015) The effect of combined treatment with canagliflozin and teneligliptin on glucose intolerance in Zucker diabetic fatty rats. J Pharmacol Sci 127:456-461.
39. Oku A, Ueta K, Arakawa K, Ishihara T, Nawano M, Kuronuma Y, Matsumoto M, Saito A, Tsujihara K, Anai M, et al. (1999) T-1095, an inhibitor of renal Na1-glucose cotransporters, may provide a novel approach to treating diabetes. Diabetes 48:1794-1800.
40. Oku A, Ueta K, Nawano M, Arakawa K, Kano-Ishihara T, Matsumoto M, Saito A, Tsujihara K, Anai M, and Asano T (2000) Antidiabetic effect of T-1095, an inhibitor of Na(1)-glucose cotransporter, in neonatally streptozotocin-treated rats. Eur J Pharmacol 391:183-192.
41. Orskov C, Wettergren A, and Holst JJ (1993) Biological effects and metabolic rates of glucagonlike peptide-1 7-36 amide and glucagonlike peptide-1 7-37 in healthy subjects are indistinguishable. Diabetes 42:658-661.
42. Polidori D, Sha S, Mudaliar S, Ciaraldi TP, Ghosh A, Vaccaro N, Farrell K, Rothenberg P, and Henry RR (2013) Canagliflozin lowers postprandial glucose and insulin by delaying intestinal glucose absorption in addition to increasing urinary glucose excretion: results of a randomized, placebo-controlled study. Diabetes Care 36:2154-2161.
43. Powell DR, Smith M, Greer J, Harris A, Zhao S, DaCosta C, Mseeh F, Shadoan MK, Sands A, Zambrowicz B, et al. (2013) LX4211 increases serum glucagon-like peptide 1 and peptide YY levels by reducing sodium/glucose cotransporter 1 (SGLT1)- mediated absorption of intestinal glucose. J Pharmacol Exp Ther 345:250-259.
44. Qaseem A, Humphrey LL, Sweet DE, Starkey M, and Shekelle P; Clinical Guidelines Committee of the American College of Physicians (2012) Oral pharmacologic treatment of type 2 diabetes mellitus: A clinical practice guideline from the American College of Physicians. Ann Intern Med 156:218-231.
45. Rossetti L, Giaccari A, and DeFronzo RA (1990) Glucose toxicity. Diabetes Care 13: 610-630.
46. Scott LJ and Spencer CM (2000) Miglitol: A review of its therapeutic potential in type 2 diabetes mellitus. Drugs 59:521-549.
47. Shibazaki T, Tomae M, Ishikawa-Takemura Y, Fushimi N, Itoh F, Yamada M, and Isaji M (2012) KGA-2727, a novel selective inhibitor of a high-affinity sodium glucose cotransporter (SGLT1), exhibits antidiabetic efficacy in rodent models. J Pharmacol Exp Ther 342:288-296.
48. Stórustovu SI and Ebert B (2006) Pharmacological characterization of agonists at deltacontaining GABAA receptors: Functional selectivity for extrasynaptic receptors is dependent on the absence of gamma2. J Pharmacol Exp Ther 316:1351-1359.
49. Szöcs Z, Brunmair B, Stadlbauer K, Nowotny P, Bauer L, Luger A, and Fürnsinn C (2008) Age-dependent development of metabolic derangement and effects of intervention with pioglitazone in Zucker diabetic fatty rats. J Pharmacol Exp Ther 326:323-329.
50. Takata K, Kasahara T, Kasahara M, Ezaki O, and Hirano H (1992) Immunohistochemical localization of Na(1)-dependent glucose transporter in rat jejunum. Cell Tissue Res 267:3-9.
51. Ueta K, Ishihara T, Matsumoto Y, Oku A, Nawano M, Fujita T, Saito A, and Arakawa K (2005) Long-term treatment with the Na1-glucose cotransporter inhibitor T-1095 causes sustained improvement in hyperglycemia and prevents diabetic neuropathy in Goto-Kakizaki rats. Life Sci 76:2655-2668.
52. Wang B, Yu W, Guo J, Jiang X, Lu W, Liu M, and Pang X (2015) The antiparasitic drug, potassium antimony tartrate, inhibits tumor angiogenesis and tumor growth in nonsmall-cell lung cancer. J Pharmacol Exp Ther 352:129-138.
53. Watanabe Y, Nakayama K, Taniuchi N, Horai Y, Kuriyama C, Ueta K, Arakawa K, Senbonmatsu T, and Shiotani M (2015) Beneficial effects of canagliflozin in combination with pioglitazone on insulin sensitivity in rodent models of obese type 2 diabetes. PLoS One 10:e0116851.
54. You G, Lee WS, Barros EJ, Kanai Y, Huo TL, Khawaja S, Wells RG, Nigam SK, and Hediger MA (1995) Molecular characteristics of Na(1)-coupled glucose transporters in adult and embryonic rat kidney. J Biol Chem 270:29365-29371.