Loss of coupling between calcium influx, energy consumption and insulin secretion associated with development of hyperglycaemia in the UCD-T2DM rat model of type 2 diabetes

Diabetologia

Volumn 56, Issue 4, 2013, Pages 803-813

  Rountree, A M ^a   Reed, B J ^a   Cummings, B P ^b   Jung, S R ^a   Stanhope, K L ^b   Graham, J L ^b   Griffen, S C ^c   Hull, R L ^a   Havel, P J ^b   Sweet, I R ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BRISTOL MYERS SQUIBB   (United States)

Author keywords

Calcium; Hyperglycaemia; Insulin secretion; Islets; Oxygen consumption

Indexed keywords

CALCIUM ION; GLUCOSE; INSULIN; OXYGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DIABETOGENESIS; ENERGY CONSUMPTION; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; INSULIN BLOOD LEVEL; INSULIN RELEASE; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXYGEN CONSUMPTION; PANCREAS ISLET; PRIORITY JOURNAL; RAT;

ANIMALS; CALCIUM; CYTOCHROMES C; CYTOSOL; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; GLUCOSE; HYPERGLYCEMIA; INSULIN; ISLETS OF LANGERHANS; MALE; OXYGEN CONSUMPTION; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 84876500331     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-012-2808-6     Document Type: Article

References (36)

1. Cook DL, Hales CN (1984) Intracellular ATP directly blocks K+ channels in pancreatic B-cells. Nature 311:271-273
2. Henquin JC (2009) Regulation of insulin secretion: a matter of phase control and amplitude modulation. Diabetologia 52:739-751
3. Prentki M (1996) New insights into pancreatic beta-cell metabolic signaling in insulin secretion. Eur J Endocrinol 134:272-286
4. Ivarsson R, Quintens R, Dejonghe S et al (2005) Redox control of exocytosis: regulatory role of NADPH, thioredoxin, and glutaredoxin. Diabetes 54:2132-2142
5. Corkey BE, Deeney JT, Yaney GC, Tornheim K, Prentki M (2000) The role of long-chain fatty acyl-CoA esters in beta-cell signal transduction. J Nutr 130:299S-304S
6. Gembal M, Detimary P, Gilon P, Gao ZY, Henquin JC (1993) Mechanisms by which glucose can control insulin release independently from its action on adenosine triphosphate-sensitive K+ channels in mouse B cells. J Clin Invest 91:871-880
7. Jung SR, Kuok IT, Couron D et al (2011) Reduced cytochrome c is an essential regulator of sustained insulin secretion by pancreatic islets. J Biol Chem 286:17422-17434
8. Kibbey RG, Pongratz RL, Romanelli AJ, Wollheim CB, Cline GW, Shulman GI (2007) Mitochondrial GTP regulates glucose-stimulated insulin secretion. Cell Metab 5:253-264
9. Pi J, Bai Y, Zhang Q et al (2007) Reactive oxygen species as a signal in glucose-stimulated insulin secretion. Diabetes 56:1783-1791
10. Jensen MV, Joseph JW, Ilkayeva O et al (2006) Compensatory responses to pyruvate carboxylase suppression in islet beta-cells. Preservation of glucose-stimulated insulin secretion. J Biol Chem 281:22342-22351
11. MacDonald MJ, Fahien LA, Brown LJ, Hasan NM, Buss JD, Kendrick MA (2005) Perspective: emerging evidence for signaling roles of mitochondrial anaplerotic products in insulin secretion. Am J Physiol Endocrinol Metab 288:E1-E15
12. Hasan NM, Longacre MJ, Stoker SW et al (2008) Impaired anaplerosis and insulin secretion in insulinoma cells caused by small interfering RNA-mediated suppression of pyruvate carboxylase. J Biol Chem 283:28048-28059
13. Jung SR, Reed BJ, Sweet IR (2009) A highly energetic process couples calcium influx through L-type calcium channels to insulin secretion in pancreatic beta-cells. Am J Physiol Endocrinol Metab 297:E717-E727
14. Gilbert M, Jung SR, Reed BJ, Sweet IR (2008) Islet oxygen consumption and insulin secretion tightly coupled to calcium derived from L-type calcium channels but not from the endoplasmic reticulum. J Biol Chem 283:24334-24342
15. Sweet IR, Gilbert M (2006) Contribution of calcium influx in mediating glucose-stimulated oxygen consumption in pancreatic islets. Diabetes 55:3509-3519
16. Ortsater H, Liss P, Akerman KE, Bergsten P (2002) Contribution of glycolytic and mitochondrial pathways in glucose-induced changes in islet respiration and insulin secretion. Pflugers Arch 444:506-512
17. Cummings BP, Digitale EK, Stanhope KL et al (2008) Development and characterization of a novel rat model of type 2 diabetes mellitus: the UC Davis type 2 diabetes mellitus UCD-T2DM rat. Am J Physiol Regul Integr Comp Physiol 295:R1782-R1793
18. Sweet IR, Cook DL, DeJulio E et al (2004) Regulation of ATP/ADP in pancreatic islets. Diabetes 53:401-409
19. Matsumoto S, Shibata S, Kirchhof N (1999) Immediate reversal of diabetes in primates following intraportal transplantation of porcine islets purified on a new histidine-lactoioniate-iodixanol gradient. Transplantation 67:S220
20. Sweet IR, Cook DL, Wiseman RW et al (2002) Dynamic perifusion to maintain and assess isolated pancreatic islets. Diabetes Technol Ther 4:67-76
21. Sweet IR, Khalil G, Wallen AR et al (2002) Continuous measurement of oxygen consumption by pancreatic islets. Diabetes Technol Ther 4:661-672
22. Jung SR, Reed BJ, Sweet IR (2009) A highly energetic process couples calcium influx through L-type calcium channels to insulin secretion in pancreatic beta-cells. Am J Physiol Endocrinol Metab 297:E717-E727
23. Nobes CD, Brown GC, Olive PN, Brand MD (1990) Non-ohmic proton conductance of the mitochondrial inner membrane in hepatocytes. J Biol Chem 265:12903-12909
24. Abe Y, Sakairi T, Kajiyama H, Shrivastav S, Beeson C, Kopp JB (2010) Bioenergetic characterization of mouse podocytes. Am J Physiol Cell Physiol 299:C464-C476
25. Wikstrom JD, Sereda SB, Stiles L et al (2012) A novel high-throughput assay for islet respiration reveals uncoupling of rodent and human islets. PLoS One 7:e33023
26. Affourtit C, Brand MD (2006) Stronger control of ATP/ADP by proton leak in pancreatic beta-cells than skeletal muscle mitochondria. Biochem J 393:151-159
27. Warnotte C, Gilon P, Nenquin M, Henquin JC (1994) Mechanisms of the stimulation of insulin release by saturated fatty acids. A study of palmitate effects in mouse beta-cells. Diabetes 43:703-711
28. Sener A, Somers G, Devis G, Malaisse WJ (1981) The stimulus-secretion coupling of amino acid-induced insulin release. Biosynthetic and secretory responses of rat pancreatic islet to L-leucine and L-glutamine. Diabetologia 21:135-142
29. Yoshikawa H, Ma Z, Bjorklund A, Grill V (2004) Short-term intermittent exposure to diazoxide improves functional performance of beta-cells in a high-glucose environment. Am J Physiol Endocrinol Metab 287:E1202-E1208
30. Steil GM, Trivedi N, Jonas JC et al (2001) Adaptation of beta-cell mass to substrate oversupply: enhanced function with normal gene expression. Am J Physiol Endocrinol Metab 280:E788-E796
31. Liu YQ, Jetton TL, Leahy JL (2002) Beta-cell adaptation to insulin resistance. Increased pyruvate carboxylase and malate-pyruvate shuttle activity in islets of nondiabetic Zucker fatty rats. J Biol Chem 277:39163-39168
32. Hayek A, Woodside W (1979) Correlation between morphology and function in isolated islets of the Zucker rat. Diabetes 28:565-569
33. Huang CJ, Gurlo T, Haataja L et al (2010) Calcium-activated calpain-2 is a mediator of beta cell dysfunction and apoptosis in type 2 diabetes. J Biol Chem 285:339-348
34. Duchen MR (2004) Roles of mitochondria in health and disease. Diabetes 53(Suppl 1):S96-S102
35. Sargsyan E, Ortsater H, Thorn K, Bergsten P (2008) Diazoxide-induced beta-cell rest reduces endoplasmic reticulum stress in lipotoxic beta-cells. J Endocrinol 199:41-50
36. Gier B, Krippeit-Drews P, Sheiko T et al (2009) Suppression of KATP channel activity protects murine pancreatic beta cells against oxidative stress. J Clin Invest 119:3246-3256