Effects of metformin on oxidative stress, adenine nucleotides balance, and glucose-induced insulin release impaired by chronic free fatty acids exposure in rat pancreatic islets

Journal of Endocrinological Investigation

Volumn 35, Issue 5, 2012, Pages 504-510

  Piro, S ^a   Rabuazzo, A M ^a   Renis, M ^a   Purrello, F ^a  

^a UNIVERSITY OF CATANIA   (Italy)

Author keywords

FFA; Insulin secretion; Islets; Metformin; Oxidative stress; ROS

Indexed keywords

ADENINE NUCLEOTIDE; ADENOSINE TRIPHOSPHATE; GLUCOSE; HEAT SHOCK PROTEIN 70; INDUCIBLE NITRIC OXIDE SYNTHASE; INSULIN; MALONALDEHYDE; METFORMIN; NITRIC OXIDE; OLEIC ACID; PALMITIC ACID; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DRUG EFFECT; INSULIN RELEASE; LIPID PEROXIDATION; MALE; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET; PROTEIN EXPRESSION; RAT;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL SURVIVAL; FATTY ACIDS, NONESTERIFIED; GLUCOSE; HSP70 HEAT-SHOCK PROTEINS; HYPOGLYCEMIC AGENTS; INSULIN; ISLETS OF LANGERHANS; MALE; MALONDIALDEHYDE; METFORMIN; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; OXIDATIVE STRESS; RATS; RATS, WISTAR;

EID: 84863915541     PISSN: 03914097     EISSN: 17208386     Source Type: Journal    
DOI: 10.3275/7866     Document Type: Article

References (51)

1. Cavaghan MK, Ehrmann DA, Polonsky KS. Interactions between insulin resistance and insulin secretion in the development of glucose intolerance. J Clin Invest 2000, 106: 329-33. (Pubitemid 30655631)
2. DeFronzo RA, Bonadonna RC, Ferrannini E. Pathogenesis of NIDDM. A balanced overview. Diabetes Care 1992, 15: 318-68.
3. McGarry JD, Dobbins RL. Fatty acids, lipotoxicity and insulin secretion. Diabetologia 1999, 42: 128-38. (Pubitemid 29064233)
4. Unger RH. Lipotoxicity in the pathogenesis of obesity-dependent NIDDM. Genetic and clinical implications. Diabetes 1995, 44: 863-70.
5. Grodsky GM, Bolaffi JL. Desensitization of the insulin-secreting beta cell. J Cell Biochem 1992, 48: 3-11.
6. Leahy JL, Cooper HE, Deal DA, Weir GC. Chronic hyperglycemia is associated with impaired glucose influence on insulin secretion. A study in normal rats using chronic in vivo glucose infusions. J Clin Invest 1986, 77: 908-15. (Pubitemid 16067964)
7. Hoenig M, MacGregor LC, Matschinsky FM. In vitro exhaustion of pancreatic beta-cells. Am J Physiol 1986, 250: E502-11.
8. Purrello F, Vetri M, Gatta C, Gullo D, Vigneri R. Effects of high glucose on insulin secretion by isolated rat islets and purified beta-cells and possible role of glycosylation. Diabetes 1989, 38: 1417-22. (Pubitemid 19271724)
9. Anello M, Rabuazzo AM, Degano C, et al. Fast reversibility of glucose-induced desensitization in rat pancreatic islets. Evidence for an involvement of ionic fluxes. Diabetes 1996, 45: 502-6. (Pubitemid 26110257)
10. Björklund A, Yaney G, McGarry JD, Weir G. Fatty acids and beta-cell function. Diabetologia 1997, 40 (Suppl 3): B21-6. (Pubitemid 27428273)
11. Paolisso G, Gambardella A, Amato L, et al. Opposite effects of short- and long-term fatty acid infusion on insulin secretion in healthy subjects. Diabetologia 1995, 38: 1295-9.
12. Hosokawa H, Corkey BE, Leahy JL. Beta-cell hypersensitivity to glucose following 24-h exposure of rat islets to fatty acids. Diabetologia 1997, 40: 392-7. (Pubitemid 27132609)
13. Elks ML. Chronic perifusion of rat islets with palmitate suppresses glucose-stimulated insulin release. Endocrinology 1993, 133: 208-14. (Pubitemid 23206395)
14. Sako Y, Grill VE. A 48-hour lipid infusion in the rat time-dependently inhibits glucose-induced insulin secretion and B cell oxidation through a process likely coupled to fatty acid oxidation. Endocrinology 1990, 127: 1580-9. (Pubitemid 20315212)
15. Lupi R, Dotta F, Marselli L, et al. Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets: evidence that beta-cell death is caspase mediated, partially dependent on ceramide pathway, and Bcl-2 regulated. Diabetes 2002, 51: 1437-42. (Pubitemid 34826609)
16. Piro S, Anello M, Di Pietro C, et al. Chronic exposure to free fatty acids or high glucose induces apoptosis in rat pancreatic islets: possible role of oxidative stress. Metabolism 2002, 51: 1340-7. (Pubitemid 35174157)
17. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003, 52: 102-10. (Pubitemid 36042113)
18. Patane G, Piro S, Rabuazzo AM, et al. Metformin restores insulin secretion altered by chronic exposure to free fatty acids or high glucose: a direct metformin effect on pancreatic beta-cells. Diabetes 2000, 49: 735-40. (Pubitemid 30339988)
19. Rabinovitch A, Suarez WL, Thomas PD, Strynadka K, Simpson I. Cytotoxic effects of cytokines on rat islets: evidence for involvement of free radicals and lipid peroxidation. Diabetologia 1992, 35: 409-13.
20. Rabinovitch A, Suarez-Pinzon WL, Strynadka K, Lakey JR, Rajotte RV. Human pancreatic islet beta-cell destruction by cytokines involves oxygen free radicals and aldehyde production. J Clin Endocrinol Metab 1996, 81: 3197-202. (Pubitemid 26296188)
21. Li LX, Skorpen F, Egeberg K, Jørgensen IH, Grill V. Uncoupling protein-2 participates in cellular defense against oxidative stress in clonal beta-cells. Biochem Biophys Res Commun 2001, 282: 273-7. (Pubitemid 32924375)
22. Poitout V, Robertson RP. Glucolipotoxicity: fuel excess and beta-cell dysfunction. Endocr Rev 2008, 29: 351-66. (Pubitemid 351679704)
23. Flodström M, Chen MC, Smismans A, Schuit F, Pipeleers DG, Eizirik DL. Interleukin 1beta increases arginine accumulation and activates the citrulline-NO cycle in rat pancreatic beta cells. Cytokine 1999, 11: 400-7. (Pubitemid 29259634)
24. Corbett JA, McDaniel ML. Does nitric oxide mediate autoimmune destruction of beta-cells? Possible therapeutic interventions in IDDM. Diabetes 1992, 41: 897-903.
25. Shimabukuro M, Ohneda M, Lee Y, Unger RH. Role of nitric oxide in obesity-induced beta cell disease. J Clin Invest 1997, 100: 290-5. (Pubitemid 27349075)
26. Bellmann K, Burkart V, Bruckhoff J, Kolb H, Landry J. p38-dependent enhancement of cytokine-induced nitric-oxide synthase gene expression by heat shock protein 70. J Biol Chem 2000, 275: 18172-9. (Pubitemid 30414768)
27. Purrello F, Buscema M, Rabuazzo AM, et al. Glucose modulates glucose transporter affinity, glucokinase activity, and secretory response in rat pancreatic beta-cells. Diabetes 1993, 42: 199-205. (Pubitemid 23013814)
28. Lee Y, Hirose H, Ohneda M, Johnson JH, McGarry JD, Unger RH. Beta-cell lipotoxicity in the pathogenesis of non-insulin-dependent diabetes mellitus of obese rats: impairment in adipocyte-beta-cell relationships. Proc Natl Acad Sci U S A 1994, 91: 10878-82.
29. Patanè G, Piro S, Anello M, Rabuazzo AM, Vigneri R, Purrello F. Exposure to glibenclamide increases rat beta cells sensitivity to glucose. Br J Pharmacol 2000, 129: 887-92. (Pubitemid 30142899)
30. Anello M, Ucciardello V, Piro S, et al. Chronic exposure to high leucine impairs glucose-induced insulin release by lowering the ATP-to-ADP ratio. Am J Physiol Endocrinol Metab 2001, 281: E1082-7.
31. Anello M, Lupi R, Spampinato D, et al. Functional and morphological alterations of mitochondria in pancreatic beta cells from type 2 diabetic patients. Diabetologia 2005, 48: 282-9. (Pubitemid 40543300)
32. Hampp R. Luminometric method. in: Bergmeyer HU (ed). Methods of enzymatic analysis. Weinheim: VCH Verlagsgesellschaft. 1986: 370-9.
33. Pipeleers DG, Pipeleers-Marichal MA. A method for the purification of single A, B and D cells and for the isolation of coupled cells from isolated rat islets. Diabetologia 1981, 20: 654-63. (Pubitemid 11065788)
34. Shen HM, Shi CY, Shen Y, Ong CN. Detection of elevated reactive oxygen species level in cultured rat hepatocytes treated with aflatoxin B1. Free Radic Biol Med 1996, 21: 139-46. (Pubitemid 26249599)
35. Chanvitayapongs S, Draczynska-Lusiak B, Sun AY. Amelioration of oxidative stress by antioxidants and resveratrol in PC12 cells. Neuroreport 1997, 8: 1499-502. (Pubitemid 27242563)
36. Vinci C, Caltabiano V, Santoro AM, et al. Copper addition prevents the inhibitory effects of interleukin 1-beta on rat pancreatic islets. Diabetologia 1995, 38: 39-45.
37. Rabuazzo AM, Patane G, Anello M, et al. Hexokinase shift to mitochondria is associated with an increased sensitivity to glucose in rat pancreatic islets. Diabetes 1997, 46: 1148-52. (Pubitemid 27271075)
38. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72: 248-54.
39. Detimary P, Dejonghe S, Ling Z, Pipeleers D, Schuit F, Henquin JC. The changes in adenine nucleotides measured in glucose-stimulated rodent islets occur in beta cells but not in alpha cells and are also observed in human islets. J Biol Chem 1998, 273: 33905-8. (Pubitemid 29008852)
40. Detimary P, Van den Berghe G, Henquin JC. Concentration dependence and time course of the effects of glucose on adenine and guanine nucleotides in mouse pancreatic islets. J Biol Chem 1996, 271: 20559-65. (Pubitemid 26281832)
41. Owen MR, Doran E, Halestrap AP. Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem J 2000, 348: 607-14. (Pubitemid 30410251)
42. Lupi R, Del Guerra S, Fierabracci V, et al. Lipotoxicity in human pancreatic islets and the protective effect of metformin. Diabetes 2002, 51 (Suppl 1): S134-7. (Pubitemid 34761508)
43. Jacquot J, Tabary O, Le Rouzic P, Clement A. Airway epithelial cell inflammatory signalling in cystic fibrosis. Int J Biochem Cell Biol 2008, 40: 1703-15.
44. Gruber J, Schaffer S, Halliwell B. The mitochondrial free radical theory of ageing--where do we stand? Front Biosci 2008, 13: 6554-79.
45. Thomas SR, Witting PK, Drummond GR. Redox control of endothelial function and dysfunction: molecular mechanisms and therapeutic opportunities. Antioxid Redox Signal 2008, 10: 1713-65.
46. Nishikawa T, Kukidome D, Sonoda K, et al. Impact of mitochondrial ROS production on diabetic vascular complications. Diabetes Res Clin Pract 2007, 77 (Suppl 1): S41-5. (Pubitemid 47212551)
47. Nishikawa T, Edelstein D, Du XL, et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000, 404: 787-90. (Pubitemid 30212409)
48. Kadirvel G, Kumar S, Kumaresan A. Lipid peroxidation, mitochondrial membrane potential and DNA integrity of spermatozoa in relation to intracellular reactive oxygen species in liquid and frozenthawed buffalo semen. Anim Reprod Sci 2009, 114: 125-34.
49. Hostens K, Pavlovic D, Zambre Y, et al. Exposure of human islets to cytokines can result in disproportionately elevated proinsulin release. J Clin Invest 1999, 104: 67-72. (Pubitemid 29534346)
50. Ihara Y, Toyokuni S, Uchida K, et al. Hyperglycemia causes oxidative stress in pancreatic beta-cells of GK rats, a model of type 2 diabetes. Diabetes 1999, 48: 927-32. (Pubitemid 29153099)
51. Laybutt DR, Glandt M, Xu G, et al. Critical reduction in beta-cell mass results in two distinct outcomes over time. Adaptation with impaired glucose tolerance or decompensated diabetes. J Biol Chem 2003, 278: 2997-3005. (Pubitemid 36801207)