Exenatide treatment alone improves β-cell function in a canine model of pre-diabetes

PLoS ONE

Volumn 11, Issue 7, 2016, Pages

  Ionut, Viorica ^a   Woolcott, Orison O ^a   Mkrtchyan, Hasmik J ^a   Stefanovski, Darko ^a   Kabir, Morvarid ^a   Iyer, Malini S ^a   Liu, Huiwen ^b   Castro, Ana V B ^a   Wu, Qiang ^a   Broussard, Josiane L ^a   Kolka, Cathryn M ^a   Asare Bediako, Isaac ^a   Bergman, Richard N ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXENDIN 4; GLUCOSE; HEMOGLOBIN A1C; INSULIN; PLACEBO; ANTIDIABETIC AGENT; GLUCAGON; GLUCOSE BLOOD LEVEL; GLYCOSYLATED HEMOGLOBIN; PEPTIDE; VENOM;

ACUTE INSULIN RESPONSE; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DIET RESTRICTION; DISEASE MODEL; DISEASE SEVERITY; DOG BREED; DRUG EFFECT; FOOD INTAKE; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; HYPERGLYCEMIA; HYPERGLYCEMIC CLAMP TECHNIQUE; IMPAIRED GLUCOSE TOLERANCE; IN VITRO STUDY; INSULIN RELEASE; INSULIN RESPONSE; INSULIN SENSITIVITY; INSULINEMIA; INTRAVENOUS GLUCOSE TOLERANCE TEST; LIPID DIET; MALE; MEDICAL PARAMETERS; MONOTHERAPY; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PANCREAS ISLET BETA CELL; RANDOMIZED CONTROLLED TRIAL; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; TREATMENT DURATION; WEIGHT REDUCTION; ANIMAL; BLOOD; BODY COMPOSITION; DOG; DRUG EFFECTS; EATING; ENERGY METABOLISM; GLUCOSE TOLERANCE TEST; INSULIN RESISTANCE; LIVER; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PREDIABETIC STATE;

ANIMALS; BLOOD GLUCOSE; BODY COMPOSITION; DISEASE MODELS, ANIMAL; DOGS; EATING; ENERGY METABOLISM; FASTING; GLUCAGON; GLUCOSE TOLERANCE TEST; HEMOGLOBIN A, GLYCOSYLATED; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; LIVER; MALE; PEPTIDES; PREDIABETIC STATE; VENOMS;

EID: 84978727205     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0158703     Document Type: Article

References (48)

1. Bergman RN. Orchestration of glucose homeostasis: from a small acorn to the California oak. Diabetes. 2007; 56: 1489-501. PMID: 17526912
2. Prasad-Reddy L, Isaacs D. A clinical review of GLP-1 receptor agonists: efficacy and safety in diabetes and beyond. Drugs Context. 2015; 4: 212283. doi: 10.7573/dic.212283 PMID: 26213556
3. Tella SH, Rendell MS. Glucagon-like polypeptide agonists in type 2 diabetes mellitus: efficacy and tolerability, a balance. Ther Adv Endocrinol Metab. 2015; 6: 109-34. doi: 10.1177/2042018815580257 PMID: 26137215
4. Nathan DM, Davidson MB, DeFronzo RA, Heine RJ, Henry RR, Pratley R, et al. Impaired fasting glucose and impaired glucose tolerance: implications for care. Diabetes Care. 2007; 30: 753-9. PMID: 17327355
5. ADA. 2. Classification and Diagnosis of Diabetes. Diabetes Care. 2015; 38: S8-S16.
6. Selph S, Dana T, Blazina I, Bougatsos C, Patel H, Chou R. Screening for type 2 diabetes mellitus: a systematic review for the U.S. Preventive Services Task Force. Ann Intern Med. 2015; 162: 765-76. doi: 10.7326/M14-2221 PMID: 25867111
7. Colagiuri S. Epidemiology of prediabetes. Med Clin North Am. 2011; 95: 299-307, vii. doi: 10.1016/j.mcna.2010.11.003 PMID: 21281834
8. Rosenstock J, Klaff LJ, Schwartz S, Northrup J, Holcombe JH, Wilhelm K, et al. Effects of exenatide and lifestyle modification on body weight and glucose tolerance in obese subjects with and without prediabetes. Diabetes Care. 2010; 33: 1173-5. doi: 10.2337/dc09-1203 PMID: 20332357
9. Armato J, DeFronzo RA, Abdul-Ghani M, Ruby R. Successful treatment of prediabetes in clinical practice: targeting insulin resistance and beta-cell dysfunction. Endocr Pract. 2012; 18: 342-50. doi: 10.4158/EP11194.OR PMID: 22068250
10. Kelly AS, Bergenstal RM, Gonzalez-Campoy JM, Katz H, Bank AJ. Effects of exenatide vs. metformin on endothelial function in obese patients with pre-diabetes: a randomized trial. Cardiovasc Diabetol. 2012; 11: 64. doi: 10.1186/1475-2840-11-64 PMID: 22681705
11. Karve A, Hayward RA. Prevalence, diagnosis, and treatment of impaired fasting glucose and impaired glucose tolerance in nondiabetic U.S. adults. Diabetes Care. 2010; 33: 2355-9. doi: 10.2337/dc09-1957 PMID: 20724649
12. Richey JM, Woolcott OO, Stefanovski D, Harrison LN, Zheng D, Lottati M, et al. Rimonabant prevents additional accumulation of visceral and subcutaneous fat during high-fat feeding in dogs. Am J Physiol Endocrinol Metab. 2009; 296: E1311-1318. doi: 10.1152/ajpendo.90972.2008 PMID: 19366874
13. Ionut V, Liu H, Mooradian V, Castro AV, Kabir M, Stefanovski D, et al. Novel Canine Models of Obese Pre-Diabetes and of Mild Type 2 Diabetes. Am J Physiol Endocrinol Metab. 2010; 298: E38-48. doi: 10.1152/ajpendo.00466.2009 PMID: 19843874
14. Ionut V, Castro AVB, Woolcott OO, Stefanovski D, Iyer MS, Broussard JL, et al. Hepatic portal vein denervation impairs oral glucose tolerance but not exenatide's effect on glycemia. Am J Physiol Endocrinol Metab. 2014; 307: E644-E652. doi: 10.1152/ajpendo.00244.2014 PMID: 25117408
15. Stefanovski D, Richey JM, Woolcott O, Lottati M, Zheng D, Harrison LN, et al. Consistency of the Disposition Index in the Face of Diet Induced Insulin Resistance: Potential Role of FFA. PLoS One. 2011; 6: e18134. doi: 10.1371/journal.pone.0018134 PMID: 21479217
16. Castro AVB, Woolcott OO, Iyer MS, Kabir M, Ionut V, Stefanovski D, et al. Increase in visceral fat per se does not induce insulin resistance in the canine model. Obesity. 2015; 23: 105-11. doi: 10.1002/oby.20906 PMID: 25322680
17. Ader M, Stefanovski D, Kim SP, Richey JM, Ionut V, Catalano KJ, et al. Hepatic insulin clearance is the primary determinant of insulin sensitivity in the normal dog. Obesity (Silver Spring). 2014; 22: 1238-45.
18. Woolcott OO, Richey JM, Kabir M, Chow RH, Iyer MS, Kirkman EL, et al. High-fat diet-induced insulin resistance does not increase plasma anandamide levels or potentiate anandamide insulinotropic effect in isolated canine islets. PLoS One. 2015; 10: e0123558. doi: 10.1371/journal.pone.0123558 PMID: 25855974
19. Woolcott OO, Bergman RN, Richey JM, Kirkman EL, Harrison LN, Ionut V, et al. Simplified method to isolate highly pure canine pancreatic islets. Pancreas. 2012; 41: 31-38. doi: 10.1097/MPA.0b013e318221fd0e PMID: 21792087
20. Woolcott OO, Gustafsson AJ, Dzabic M, Pierro C, Tedeschi P, Sandgren J, et al. Arachidonic acid is a physiological activator of the ryanodine receptor in pancreatic beta-cells. Cell Calcium. 2006; 39: 529-537. PMID: 16620964
21. Hamilton LC. Multilevel and mixed-effects modeling. In: eds. Statistics with STATA: Updated for version 10. Belmont: Brooks/Cole; 2008. pp. 387-421.
22. Bradley DP, Kulstad R, Racine N, Shenker Y, Meredith M, Schoeller DA. Alterations in energy balance following exenatide administration. Appl Physiol Nutr Metab. 2012; 37: 893-9. doi: 10.1139/h2012-068 PMID: 22735035
23. Gallwitz B, Guzman J, Dotta F, Guerci B, Simo R, Basson BR, et al. Exenatide twice daily versus glimepiride for prevention of glycaemic deterioration in patients with type 2 diabetes with metformin failure (EUREXA): an open-label, randomised controlled trial. Lancet. 2012; 379: 2270-8. doi: 10.1016/S0140-6736(12)60479-6 PMID: 22683137
24. Kendall DM, Riddle MC, Rosenstock J, Zhuang D, Kim DD, Fineman MS, et al. Effects of exenatide (exendin-4) on glycemic control over 30 weeks in patients with type 2 diabetes treated with metformin and a sulfonylurea. Diabetes Care. 2005; 28: 1083-91. PMID: 15855571
25. Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev. 2007; 87: 1409-39. PMID: 17928588
26. DeFronzo RA, Triplitt C, Qu Y, Lewis MS, Maggs D, Glass LC. Effects of exenatide plus rosiglitazone on beta-cell function and insulin sensitivity in subjects with type 2 diabetes on metformin. Diabetes Care. 2010; 33: 951-7. doi: 10.2337/dc09-1521 PMID: 20107105
27. Weyer C, Tataranni PA, Bogardus C, Pratley RE. Insulin resistance and insulin secretory dysfunction are independent predictors of worsening of glucose tolerance during each stage of type 2 diabetes development. Diabetes Care. 2001; 24: 89-94. PMID: 11194248
28. Waugh J, Keating GM, Plosker GL, Easthope S, Robinson DM. Pioglitazone: a review of its use in type 2 diabetes mellitus. Drugs. 2006; 66: 85-109. PMID: 16398569
29. Gastaldelli A, Brodows RG, D'Alessio D. The effect of chronic twice daily exenatide treatment on beta-cell function in new onset type 2 diabetes. Clin Endocrinol (Oxf). 2014; 80: 545-53.
30. Zheng D, Ionut V, Mooradian V, Stefanovski D, Bergman RN. Exenatide sensitizes insulin-mediated whole-body glucose disposal and promotes uptake of exogenous glucose by the liver. Diabetes. 2009; 58: 352-9. doi: 10.2337/db08-0875 PMID: 19011168
31. Vella A, Shah P, Reed AS, Adkins AS, Basu R, Rizza RA. Lack of effect of exendin-4 and glucagon-like peptide-1-(7,36)-amide on insulin action in non-diabetic humans. Diabetologia. 2002; 45: 1410-5. PMID: 12378382
32. Gedulin BR, Nikoulina SE, Smith PA, Gedulin G, Nielsen LL, Baron AD, et al. Exenatide (exendin-4) improves insulin sensitivity and {beta}-cell mass in insulin-resistant obese fa/fa Zucker rats independent of glycemia and body weight. Endocrinology. 2005; 146: 2069-76. PMID: 15618356
33. Lotfy M, Singh J, Rashed H, Tariq S, Zilahi E, Adeghate E. Mechanism of the beneficial and protective effects of exenatide in diabetic rats. J Endocrinol. 2014; 220: 291-304. doi: 10.1530/JOE-13-0426 PMID: 24353307
34. Wang L, Guo F, Wei S, Zhao R. Divergent effects of GLP-1 analogs exendin-4 and exendin-9 on the expression of myosin heavy chain isoforms in C2C12 myotubes. Peptides. 2011; 32: 1313-9. doi: 10.1016/j.peptides.2011.03.018 PMID: 21453734
35. Idris I, Patiag D, Gray S, Donnelly R. Exendin-4 increases insulin sensitivity via a PI-3-kinase-dependent mechanism: contrasting effects of GLP-1. Biochem Pharmacol. 2002; 63: 993-6. PMID: 11911852
36. Parkes DG, Pittner R, Jodka C, Smith P, Young A. Insulinotropic actions of exendin-4 and glucagon-like peptide-1 in vivo and in vitro. Metabolism. 2001; 50: 583-9. PMID: 11319721
37. Goke R, Fehmann HC, Linn T, Schmidt H, Krause M, Eng J, et al. Exendin-4 is a high potency agonist and truncated exendin-(9-39)-amide an antagonist at the glucagon-like peptide 1-(7-36)-amide receptor of insulin-secreting beta-cells. J Biol Chem. 1993; 268: 19650-5. PMID: 8396143
38. Lupi R, Mancarella R, Del Guerra S, Bugliani M, Del Prato S, Boggi U, et al. Effects of exendin-4 on islets from type 2 diabetes patients. Diabetes Obes Metab. 2008; 10: 515-9. doi: 10.1111/j.1463-1326.2007.00838.x PMID: 18201204
39. Park YJ, Ao Z, Kieffer TJ, Chen H, Safikhan N, Thompson DM, et al. The glucagon-like peptide-1 receptor agonist exenatide restores impaired pro-islet amyloid polypeptide processing in cultured human islets: implications in type 2 diabetes and islet transplantation. Diabetologia. 2013; 56: 508-19. doi: 10.1007/s00125-012-2802-z PMID: 23262664
40. Cechin SR, Perez-Alvarez I, Fenjves E, Molano RD, Pileggi A, Berggren P-O, et al. Anti-Inflammatory Properties of Exenatide in Human Pancreatic Islets. Cell Transplantation. 2012; 21: 633-648. doi: 10.3727/096368911X576027 PMID: 21669040
41. Kim W, Egan JM. The role of incretins in glucose homeostasis and diabetes treatment. Pharmacol Rev. 2008; 60: 470-512. doi: 10.1124/pr.108.000604 PMID: 19074620
42. Garber AJ. Incretin effects on beta-cell function, replication, and mass: the human perspective. Diabetes Care. 2011; 34 Suppl 2: S258-63. doi: 10.2337/dc11-s230 PMID: 21525465
43. Drucker DJ. Incretin action in the pancreas: potential promise, possible perils, and pathological pitfalls. Diabetes. 2013; 62: 3316-23. doi: 10.2337/db13-0822 PMID: 23818527
44. Bentsi-Barnes K, Doyle ME, Abad D, Kandeel F, Al-Abdullah I. Detailed protocol for evaluation of dynamic perifusion of human islets to assess beta-cell function. Islets. 2011; 3: 284-90. PMID: 21811103
45. Abdul-Ghani MA, DeFronzo RA. Pathophysiology of prediabetes. Curr Diab Rep. 2009; 9: 193-9. PMID: 19490820
46. ADA. Classification and Diagnosis of Diabetes. Diabetes Care. 2016; 39: S13-S22.
47. Bergman RN, Phillips LS, Cobelli C. Physiologic evaluation of factors controlling glucose tolerance in man: measurement of insulin sensitivity and beta-cell glucose sensitivity from the response to intravenous glucose. J Clin Invest. 1981; 68: 1456-67. PMID: 7033284
48. Deeds MC, Anderson JM, Armstrong AS, Gastineau DA, Hiddinga HJ, Jahangir A, et al. Single dose streptozotocin-induced diabetes: considerations for study design in islet transplantation models. Lab Anim. 2011; 45: 131-40. doi: 10.1258/la.2010.010090 PMID: 21478271