Prevention by metformin of alterations induced by chronic exposure to high glucose in human islet beta cells is associated with preserved ATP/ADP ratio

Diabetes Research and Clinical Practice

Volumn 104, Issue 1, 2014, Pages 163-170

  Masini, M ^a   Anello, M ^b   Bugliani, M ^a   Marselli, L ^a   Filipponi, F ^a   Boggi, U ^a   Purrello, F ^b   Occhipinti, M ^a   Martino, L ^a   Marchetti, P ^a   De Tata, V ^a  

^a UNIVERSITY OF PISA   (Italy)

^b UNIVERSITY OF CATANIA   (Italy)

Author keywords

Adenine nucleotides; Beta cells; Diabetes; Glucotoxicity; Insulin secretion; Metformin

Indexed keywords

ADENINE NUCLEOTIDE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; GLUCOSE; INSULIN; METFORMIN; MITOCHONDRIAL COMPLEX 2; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG; ANTIDIABETIC AGENT;

ADULT; ARTICLE; CELL CULTURE; CELL DENSITY; CELL ORGANELLE; CELL ULTRASTRUCTURE; CHEMICAL ANALYSIS; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SYNTHESIS; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYPERGLYCEMIA; INSULIN RELEASE; MITOCHONDRION; PANCREAS ISLET BETA CELL; BLOOD; DIABETES MELLITUS; DRUG EFFECTS; FEMALE; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; SECRETION (PROCESS); ULTRASTRUCTURE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CELLS, CULTURED; DIABETES MELLITUS; FEMALE; GLUCOSE; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN-SECRETING CELLS; MALE; METFORMIN; MICROSCOPY, ELECTRON; MIDDLE AGED;

EID: 84898549561     PISSN: 01688227     EISSN: 18728227     Source Type: Journal    
DOI: 10.1016/j.diabres.2013.12.031     Document Type: Article

References (38)

1. Unger R.H., Grundy S. Hyperglycaemia as an inducer as well as a consequence of impaired islet cell function and insulin resistance: implications for the management of diabetes. Diabetologia 1985, 28:119-121.
2. Weir G.C., Marselli L., Marchetti P., Katsuta H., Jung M.H., Bonner-Weir S. Towards better understanding of the contributions of overwork and glucotoxicity to the beta-cell inadequacy of type 2 diabetes. Diabetes Obes Metab 2009, 11(Suppl. 4):82-90.
3. 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, 38:1417-1422.
4. Eizirik D.L., Korbutt G.S., Hellerström C. Prolonged exposure of human pancreatic islets to high glucose concentrations in vitro impairs the beta-cell function. J Clin Invest 1992, 90:1263-1268.
5. Maechler P., Carobbio S., Rubi B. In beta-cells, mitochondria integrate and generate metabolic signals controlling insulin secretion. Int J Biochem Cell Biol 2006, 38:696-709.
6. Anello M., Lupi R., Spampinato D., Piro S., Masini M., Boggi U., et al. Functional and morphological alterations of mitochondria in pancreatic beta cells from type 2 diabetic patients. Diabetologia 2005, 48:282-289.
7. Bailey C.J., Turner R.C. Metformin. N Engl J Med 1996, 334:574-579.
8. Marchetti P., Del Guerra S., Marselli L., Lupi R., Masini M., Pollera M., et al. Pancreatic islets from type 2 diabetic patients have functional defects and increased apoptosis that are ameliorated by metformin. J Clin Endocrinol Metab 2004, 89(November (11)):5535-5541.
9. Irwin N., McKinney J.M., Bailey C.J., Flatt P.R., McClenaghan N.H. Effects of metformin on BRIN-BD11 beta-cell insulin secretory desensitization induced by prolonged exposure to sulphonylureas. Diabetes Obes Metab 2010, 12:1066-1071.
10. Lupi R., Del Guerra S., Tellini C., Giannarelli R., Coppelli A., Lorenzetti M., et al. The biguanide compound metformin prevents desensitization of human pancreatic islets induced by high glucose. Eur J Pharmacol 1999, 364:205-209.
11. Lupi R., Del Guerra S., Fierabracci V., Marselli L., Novelli M., Patanè G., et al. Lipotoxicity in human pancreatic islets and the protective effect of metformin. Diabetes 2002, 51(Suppl. 1):S134-S137.
12. Marchetti P., Dotta F., Ling Z., Lupi R., Del Guerra S., Santangelo C., et al. Function of pancreatic islets isolated from a type 1 diabetic patient. Diabetes Care 2000, 23:701-703.
13. Bugliani M., Liechti R., Cheon H., Suleiman M., Marselli L., Kirkpatrick C., et al. Microarray analysis of isolated human islet transcriptome in type 2 diabetes and the role of the ubiquitin-proteasome system in pancreatic beta cell dysfunction. Mol Cell Endocrinol 2012, pii S0303-7207(12)00513-8. 10.1016/j.mce.2012.12.001.
14. Gatto C., Callegari M., Folin M., Conconi M., Paolin A., Di Falco G., et al. Effects of cryopreservation and coculture with pancreatic ductal epithelial cells on insulin secretion from human pancreatic islets. Int J Mol Med 2003, 12:851-854.
15. Anello M., Ucciardello V., Piro S., Patané G., Frittitta L., Calabrese V., 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-E1087.
16. Hampp R. Luminometric method. Methods of enzymatic analysis 1986, 370-379. Verlagsgesellschaft, Weinheim, Germany. H.U. Bergmeyer (Ed.).
17. Martino L., Masini M., Novelli M., Beffy P., Bugliani M., Marselli L., et al. Palmitate activates autophagy in INS-1E β-cells and in isolated rat and human pancreatic islets. PLoS ONE 2012, 7(5):e36188. 10.1371/journal.pone.0036188.
18. Masini M., Marselli L., Bugliani M., Martino L., Masiello P., Marchetti P., et al. Ultrastructural morphometric analysis of insulin secretory granules in human type 2 diabetes. Acta Diabetol 2012, 49(Suppl. 1):S247-S252.
19. Merglen A., Theander S., Rubi B., Chaffard G., Wollheim C.B., Maechler P. Glucose sensitivity and metabolism-secretion coupling studied during two-year continuous culture in INS-1E insulinoma cells. Endocrinology 2004, 145(February (2)):667-678.
20. Hinke S.A., Martens G.A., Cai Y., Finsi J., Heimberg H., Pipeleers D., et al. Methyl succinate antagonises biguanide-induced AMPK-activation and death of pancreatic beta-cells through restoration of mitochondrial electron transfer. Br J Pharmacol 2007, 150(April (8)):1031-1043.
21. Nolan C.J., Damm P., Prentki M. Type 2 diabetes across generations: from pathophysiology to prevention and management. Lancet 2011, 378:169-181.
22. Ashcroft F.M., Rorsman P. Diabetes mellitus and the β cell: the last ten years. Cell 2012, 148:1160-1171.
23. Del Guerra S., Lupi R., Marselli L., Masini M., Bugliani M., Sbrana S., et al. Functional and molecular defects of pancreatic islets in human type 2 diabetes. Diabetes 2005, 54:727-735.
24. Jonas J.C., Bensellam M., Duprez J., Elouil H., Guiot Y., Pascal S.M. Glucose regulation of islet stress responses and beta-cell failure in type 2 diabetes. Diabetes Obes Metab 2009, 11(Suppl. 4):65-81.
25. Patanè G., Piro S., Rabuazzo A.M., Anello M., Vigneri R., Purrello F. 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, 49:735-740.
26. Mannella C.A. The relevance of mitochondrial membrane topology to mitochondrial function. Biochim Biophys Acta 2006, 1762:140-147.
27. Wakabayashi T., Karbowski M. Structural changes of mitochondria related to apoptosis. Biol Signals Recept 2001, 10:26-56.
28. Knowler W.C., Barrett-Connor E., Fowler S.E., Hamman R.F., Lachin J.M., Walker E.A., et al. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 2002, 346:393-403.
29. Turner R.C., Cull C.A., Frighi V., Holman R.R. Glycemic control with diet, sulfonylurea, metformin, or insulin in patients with type 2 diabetes mellitus: progressive requirement for multiple therapies (UKPDS 49). UK Prospective Diabetes Study (UKPDS) Group. J Am Med Assoc 1999, 281:2005-2012.
30. El-Mir M.Y., Nogueira V., Fontaine E., Avéret N., Rigoulet M., Leverve X. Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. J Biol Chem 2000, 275:223-228.
31. Rena G., Pearson E.R., Sakamoto K. Molecular mechanism of action of metformin: old or new insights. Diabetologia 2013, 56:1898-1906.
32. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001, 414:813-820.
33. Lablanche S., Cottet-Rousselle C., Lamarche F., Benhamou P.Y., Halimi S., Leverve X., et al. Protection of pancreatic INS-1 β-cells from glucose- and fructose-induced cell death by inhibiting mitochondrial permeability transition with cyclosporin A or metformin. Cell Death Dis 2011, 2(March):e134. 10.1038/cddis.2011.15.
34. Jung T.W., Lee M.W., Lee Y.J., Kim S.M. Metformin prevents endoplasmic reticulum stress-induced apoptosis through AMPK-PI3K-c-Jun NH2 pathway. Biochem Biophys Res Commun 2012, 417:147-152.
35. Zhou G., Myers R., Li Y., Chen Y., Shen X., Fenyk-Melody J., et al. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 2001, 108:1167-1174.
36. Winder W.W., Thomson D.M. Cellular energy sensing and signaling by AMP-activated protein kinase. Cell Biochem Biophys 2007, 47:332-347.
37. Turban S., Stretton C., Drouin O., Green C.C.J., Watson M.L., Gray A., et al. Defining the contribution of AMP-activated protein kinase (AMPK) and protein kinase C (PKC) in regulation of glucose uptake by metformin in skeletal muscle cells. J Biol Chem 2012, 287:20088-20099.
38. González-Barroso M.M., Anedda A., Gallardo-Vara E., Redondo-Horcajo M., Rodriguez-Sánchez L., Rial E. Fatty acids revert the inhibition of respiration caused by the antidiabetic drug metformin to facilitate their mitochondrial β-oxidation. Biochim Biophys Acta 2012, 1817:1768-1775.