Investigation of the effects of sulfonylurea exposure on pancreatic beta cell metabolism

FEBS Journal

Volumn 273, Issue 22, 2006, Pages 5160-5168

  Brennan, Lorraine ^a   Hewage, Chandralal ^a   Malthouse, J P G ^a   McClenaghan, Neville H ^b   Flatt, Peter R ^b   Newsholme, Philip ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

Beta cells; Metabolism; Sulfonylurea

Indexed keywords

GLIBENCLAMIDE; PYRUVATE CARBOXYLASE; PYRUVATE DEHYDROGENASE; SULFONYLUREA; TOLBUTAMIDE;

ANIMAL CELL; ARTICLE; CELL METABOLISM; CONTROLLED STUDY; DRUG EFFECT; ENERGY METABOLISM; GLUCOSE METABOLISM; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RAT;

ANIMALS; CARBON RADIOISOTOPES; CELLS, CULTURED; GLUCOSE; GLYBURIDE; HYPOGLYCEMIC AGENTS; INSULIN-SECRETING CELLS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, BIOLOGICAL; RATS; SULFONYLUREA COMPOUNDS; TOLBUTAMIDE;

EID: 33750558924     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05513.x     Document Type: Article

References (48)

1. Aguilar-Bryan L, Nichols CG, Wechsler SW, Clement JPT, Boyd AE 3rd, Gonzalez G, Herrera-Sosa H, Nguy K, Bryan J & Nelson DA (1995) Cloning of the beta cell high-affinity sulfonylurea receptor: a regulator of insulin secretion. Science 268, 423-426.
2. Henquin JC (1998) A minimum of fuel is necessary for tolbutamide to mimic the effects of glucose on electrical activity in pancreatic beta-cells. Endocrinology 139, 993-998.
3. Ashcroft FM & Gribble FM (1998) Correlating structure and function in ATP-sensitive K+ channels. Trends Neurosci 21, 288-294.
4. Eliasson L, Renstrom E, Ammala C, Berggren PO, Bertorello AM, Bokvist K, Chibalin A, Deeney JT, Flatt PR, Gabel J et al. (1996) PKC-dependent stimulation of exocytosis by sulfonylureas in pancreatic beta cells. Science 271, 813-815.
5. Tian YA, Johnson G & Ashcroft SJ (1998) Sulfonylureas enhance exocytosis from pancreatic beta-cells by a mechanism that does not involve direct activation of protein kinase C. Diabetes 47, 1722-1726.
6. Flatt PR, Shibier O, Szecowka J & Berggren PO (1994) New perspectives on the actions of sulphonylureas and hyperglycaemic sulphonamides on the pancreatic beta-cell. Diabete Metab 20, 157-162.
7. Kamp F, Kizilbash N, Corkey BE, Berggren PO & Hamilton JA (2003) Sulfonylureas rapidly cross phospholipid bilayer membranes by a free-diffusion mechanism. Diabetes 52, 2526-2531.
8. Pontiroli AE, Calderara A & Pozza G (1994) Secondary failure of oral hypoglycaemic agents: frequency, possible causes, and management. Diabetes Metab Rev 10, 31-43.
9. Matthews DR, Cull CA, Stratton IM, Holman RR & Turner RC (1998) UKPDS 26: sulphonylurea failure in non-insulin-dependent diabetic patients over six years. UK Prospective Diabetes Study (UKPDS) Group. Diabet Med 15, 297-303.
10. Gullo D, Rabuazzo AM, Vetri M, Gatta C, Vinci C, Buscema M, Vigneri R & Purrello F (1991) Chronic exposure to glibenclamide impairs insulin secretion in isolated rat pancreatic islets. J Endocrinol Invest 14, 287-291.
11. Rabuazzo AM, Buscema M, Vinci C, Caltabiano V, Vetri M, Forte F, Vigneri R & Purrello F (1992) Glyburide and tolbutamide induce desensitization of insulin release in rat pancreatic islets by different mechanisms. Endocrinology 131, 1815-1820.
12. Ball AJ, Flatt PR & McClenaghan NH (2000) Desensitization of sulphonylurea- and nutrient-induced insulin secretion following prolonged treatment with glibenclamide. Eur J Pharmacol 408, 327-333.
13. McClenaghan NH, Ball AJ & Flatt PR (2001) Specific desensitization of sulfonylurea- but not imidazoline-induced insulin release after prolonged tolbutamide exposure. Biochem Pharmacol 61, 527-536.
14. Rustenbeck I (2002) Desensitization of insulin secretion. Biochem Pharmacol 63, 1921-1935.
15. Kawaki J, Nagashima K, Tanaka J, Miki T, Miyazaki M, Gonoi T, Mitsuhashi N, Nakajima N, Iwanaga T, Yano H et al. (1999) Unresponsiveness to glibenclamide during chronic treatment induced by reduction of ATP-sensitive K+ channel activity. Diabetes 48, 2001-2006.
16. Anello M, Gilon P & Henquin JC (1999) Alterations of insulin secretion from mouse islets treated with sulphonylureas: perturbations of Ca2+ regulation prevail over changes in insulin content. Br J Pharmacol 127, 1883-1891.
17. MacDonald MJ (1993) Glucose enters mitochondrial metabolism via both carboxylation and decarboxylation of pyruvate in pancreatic islets. Metabolism 42, 1229-1231.
18. Khan A, Ling ZC & Landau BR (1996) Quantifying the carboxylation of pyruvate in pancreatic islets. J Biol Chem 271, 2539-2542.
19. Schuit F, De Vos A, Farfari S, Moens K, Pipeleers D, Brun T & Prentki M (1997) Metabolic fate of glucose in purified islet cells. Glucose-regulated anaplerosis in beta cells. J Biol Chem 272, 18572-18579.
20. McCormack JG, Halestrap AP & Denton RM (1990) Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev 70, 391-425.
21. Rutter GA, Burnett P, Rizzuto R, Brini M, Murgia M, Pozzan T, Tavare JM & Denton RM (1996) Subcellular imaging of intramitochondrial Ca2+ with recombinant targeted aequorin: significance for the regulation of pyruvate dehydrogenase activity. Proc Natl Acad Sci USA 93, 5489-5494.
22. Kennedy HJ, Pouli AE, Ainscow EK, Jouaville LS, Rizzuto R & Rutter GA (1999) Glucose generates sub-plasma membrane ATP microdomains in single islet beta-cells. Potential role for strategically located mitochondria. J Biol Chem 274, 13281-13291.
23. Brennan L, Shine A, Hewage C, Malthouse JP, Brindle KM, McClenaghan N, Flatt PR & Newsholme P (2002) A nuclear magnetic resonance-based demonstration of substantial oxidative 1-alanine metabolism and L-alanine-enhanced glucose metabolism in a clonal pancreatic beta-cell line: metabolism of L-alanine is important to the regulation of insulin secretion. Diabetes 51, 1714-1721.
24. Brennan L, Corless M, Hewage C, Malthouse JP, McClenaghan NH, Flatt PR & Newsholme P (2003) 13C NMR analysis reveals a link between L-glutamine metabolism, D-glucose metabolism and gamma-glutamyl cycle activity in a clonal pancreatic beta-cell line. Diabetologia 46, 1512-1521.
25. Lawson JW & Veech RL (1979) Effects of pH and free Mg2+ on the Keq of the creatine kinase reaction and other phosphate hydrolyses and phosphate transfer reactions. J Biol Chem 254, 6528-6537.
26. Matthews PM, Bland JL, Gadian DG & Radda GK (1982) A 31P-NMR saturation transfer study of the regulation of creatine kinase in the rat heart. Biochim Biophys Acta 721, 312-320.
27. McClenaghan NH, Ball AJ & Flatt PR (2000) Induced desensitization of the insulinotropic effects of antidiabetic drugs, BTS 67 582 and tolbutamide. Br J Pharmacol 130, 478-484.
28. Ball AJ, McCluskey JT, Flatt PR & McClenaghan NH (2004) Chronic exposure to tolbutamide and glibenclamide impairs insulin secretion but not transcription of K(ATP) channel components. Pharmacol Res 50, 41-46.
29. Elmi A, Idahl LA & Sehlin J (2000) Relationships between the Na(+)/K(+) pump and ATP and ADP content in mouse pancreatic islets: effects of meglitinide and glibenclamide. Br J Pharmacol 131, 1700-1706.
30. Cline GW, Lepine RL, Papas KK, Kibbey RG & Shulman GI (2004) 13C NMR isotopomer analysis of anaplerotic pathways in INS-1 cells. J Biol Chem 279, 44370-44375.
31. Lu D, Mulder H, Zhao P, Burgess SC, Jensen MV, Kamzolova S, Newgard CB & Sherry AD (2002) 13C NMR isotopomer analysis reveals a connection between pyruvate cycling and glucose-stimulated insulin secretion (GSIS). Proc Natl Acad Sci USA 99, 2708-2713.
32. Fransson U, Rosengren AH, Schuit FC, Renstrom E & Mulder H (2006) Anaplerosis via pyruvate carboxylase is required for the fuel-induced rise in the ATP:ADP ratio in rat pancreatic islets. Diabetologia 49, 1578-1586.
33. Panten U, Burgfeld J, Goerke F, Rennicke M, Schwanstecher M, Wallasch A, Zunkler BJ & Lenzen S (1989) Control of insulin secretion by sulfonylureas, meglitinide and diazoxide in relation to their binding to the sulfonylurea receptor in pancreatic islets. Biochem Pharmacol 38, 1217-1229.
34. McClenaghan NH & Flatt PR (1999) Physiological and pharmacological regulation of insulin release: insights offered through exploitation of insulin-secreting cell lines. Diabetes Obes Metab 1, 137-150.
35. Groop LC (1992) Sulfonylureas in NIDDM. Diabetes Care 15, 737-754.
36. Hellman B, Idahl LA & Danielsson A (1969) Adenosine triphosphate levels of mammalian pancreatic B cells after stimulation with glucose and hypoglycemic sulfonylureas. Diabetes 18, 509-516.
37. Welsh M (1983) The effects of glibenclamide on rat islet radioactive nucleotide efflux, ATP contents and respiratory rates. Biochem Pharmacol 32, 2903-2908.
38. Detimary P, Gilon P & Henquin JC (1998) Interplay between cytoplasmic Ca2+ and the ATP/ADP ratio: a feedback control mechanism in mouse pancreatic islets. Biochem J 333, 269-274.
39. Doliba NM, Vatamaniuk MZ, Buettger CW, Qin W, Collins HW, Wehrli SL, Carr RD & Matschinsky FM (2003) Differential effects of glucose and glyburide on energetics and Na+ levels of betaHC9 cells: nuclear magnetic resonance spectroscopy and respirometry studies. Diabetes 52, 394-402.
40. Ainscow EK & Rutter GA (2001) Mitochondrial priming modifies Ca2+ oscillations and insulin secretion in pancreatic islets. Biochem J 353, 175-180.
41. McClenaghan NH, Barnett CR, Ah-Sing E, Abdel-Wahab YH, O'Harte FP, Yoon TW, Swanston-Flatt SK & Flatt PR (1996) Characterization of a novel glucose-responsive insulin-secreting cell line, BRINBD11, produced by electrofusion. Diabetes 45, 1132-1140.
42. Lowry OH, Rosebrough NJ, Farr AL & Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265-275.
43. Thelwall PE & Brindle KM (1999) Analysis of CHO-K1 cell growth in a fixed bed bioreactor using magnetic resonance spectroscopy and imaging. Cytotechnology 30, 121-132.
44. Fan TWM (1996) Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog Nucl Magnet Reson Spectrosc 28, 161-219.
45. Chateil J, Biran M, Thiaudiere E, Canioni P & Merle M (2001) Metabolism of [1-(13)C) glucose and [2-(13)C]acetate in the hypoxic rat brain. Neurochem Int 38, 399-407.
46. Lapidot A & Gopher A (1994) Cerebral metabolic compartmentation. Estimation of glucose flux via pyruvate carboxylase/pyruvate dehydrogenase by 13C NMR isotopomer analysis of D-[U-13C]glucose metabolites. J Biol Chem 269, 27198-27208.
47. Malloy CR, Sherry AD & Jeffrey FM (1990) Analysis of tricarboxylic acid cycle of the heart using 13C isotope isomers. Am J Physiol 259, H987-H995.
48. Haber S & Lapidot A (2001) Energy fuel utilization by fetal versus young rabbit brain: a 13C MRS isotopomer analysis of [U-(13)C]glucose metabolites. Brain Res 896, 102-117.