Calcium co-regulates oxidative metabolism and ATP synthase-dependent respiration in pancreatic beta cells

Journal of Biological Chemistry

Volumn 289, Issue 13, 2014, Pages 9182-9194

  De Marchi, Umberto ^a   Thevenet, Jonathan ^a   Hermant, Aurelie ^a   Dioum, Elhadji ^a   Wiederkehr, Andreas ^a  

^a NESTLÉ RESEARCH CENTER   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CYTOLOGY; GLUCOSE; INSULIN; MITOCHONDRIA; PHYSIOLOGY;

CALCIUM SIGNALING; ENERGY METABOLISM; INSULIN SECRETING CELLS; MITOCHONDRIAL ENERGY; MITOCHONDRIAL SUBSTRATES; OXIDATIVE METABOLISM; PANCREATIC BETA CELLS; RESPIRATORY CHAINS;

METABOLISM;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CALCIUM; GLUCOSE; INSULIN; OXIDOREDUCTASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

AEROBIC METABOLISM; ARTICLE; AUTOFLUORESCENCE; CALCIUM SIGNALING; CELL RESPIRATION; CELL STIMULATION; CELL STRAIN INS 1E; CONTROLLED STUDY; ENERGY METABOLISM; HUMAN; HUMAN CELL; INSULIN RELEASE; INSULINOMA CELL; MITOCHONDRION; OXYGEN CONSUMPTION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REGULATORY MECHANISM; RESPIRATORY CHAIN; STEADY STATE; TUMOR CELL; ANIMAL; BIOSYNTHESIS; CYTOLOGY; CYTOSOL; DRUG EFFECTS; METABOLISM; OXIDATION REDUCTION REACTION; RAT; SECRETION (PROCESS);

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; ATP SYNTHETASE COMPLEXES; CALCIUM; CALCIUM SIGNALING; CELL RESPIRATION; CYTOSOL; GLUCOSE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; NADP; OXIDATION-REDUCTION; RATS;

EID: 84897410083     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.513184     Document Type: Article

References (46)

1. Balaban, R. S., Kantor, H. L., Katz, L. A., and Briggs, R. W. (1986) Relation between work and phosphate metabolite in the in vivo paced mammalian heart. Science 232, 1121-1123 (Pubitemid 16050798)
2. Lin, A. L., Fox, P. T., Hardies, J., Duong, T. Q., and Gao, J. H. (2010) Nonlinear coupling between cerebral blood flow, oxygen consumption, and ATP production in human visual cortex. Proc. Natl. Acad. Sci. U.S.A. 107, 8446-8451
3. Hellman, B., Idahl, L. A., Lernmark, A., Sehlin, J., and Täljedal, I. B. (1974) The pancreatic beta cell recognition of insulin secretagogues. Effects of calcium and sodium on glucose metabolism and insulin release. Biochem. J. 138, 33-45
4. Sweet, I. R., Cook, D. L., DeJulio, E., Wallen, A. R., Khalil, G., Callis, J., and Reems, J. (2004) Regulation of ATP/ADP in pancreatic islets. Diabetes 53, 401-409 (Pubitemid 38174556)
5. Wiederkehr, A., Szanda, G., Akhmedov, D., Mataki, C., Heizmann, C. W., Schoonjans, K., Pozzan, T., Spät, A., and Wollheim, C. B. (2011) Mitochondrial matrix calcium is an activating signal for hormone secretion. Cell Metab. 13, 601-611
6. Wiederkehr, A., Park, K. S., Dupont, O., Demaurex, N., Pozzan, T., Cline, G. W., and Wollheim, C. B. (2009) Matrix alkalinization. A novel mitochondrial signal for sustained pancreatic beta cell activation. EMBO J. 28, 417-428
7. Detimary, P., Dejonghe, S., Ling, Z., Pipeleers, D., Schuit, F., and Henquin, J. C. (1998) 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. 273, 33905-33908 (Pubitemid 29008852)
8. Doliba, N. M., Wehrli, S. L., Vatamaniuk, M. Z., Qin, W., Buettger, C. W., Collins, H. W., and Matschinsky, F. M. (2007) Metabolic and ionic coupling factors in amino acid stimulated insulin release in pancreatic beta-HC9 cells. Am. J. Physiol. Endocrinol. Metab. 292, E1507-E1519 (Pubitemid 47084684)
9. Duchen, M. R., Smith, P. A., and Ashcroft, F. M. (1993) Substrate-dependent changes in mitochondrial function, intracellular free calcium concentration and membrane channels in pancreatic beta cells. Biochem. J. 294, 35-42 (Pubitemid 23251908)
10. Akhmedov, D., Braun, M., Mataki, C., Park, K. S., Pozzan, T., Schoonjans, K., Rorsman, P., Wollheim, C. B., and Wiederkehr, A. (2010) Mitochondrial matrix pH controls oxidative phosphorylation and metabolism-secretion coupling in INS-1E clonal beta cells. FASEB J. 24, 4613-4626
11. Tarasov, A. I., Semplici, F., Ravier, M. A., Bellomo, E. A., Pullen, T. J., Gilon, P., Sekler, I., Rizzuto, R., and Rutter, G. A. (2012) The mitochondrial Ca2+ uniporter MCU is essential for glucose-induced ATP increases in pancreatic beta cells. PLoS ONE 7, e39722
12. Jouaville, L. S., Pinton, P., Bastianutto, C., Rutter, G. A., and Rizzuto, R. (1999) Regulation of mitochondrial ATP synthesis by calcium. Evidence for a long-term metabolic priming. Proc. Natl. Acad. Sci. U.S.A. 96, 13807-13812
13. Denton, R. M. (2009) Regulation of mitochondrial dehydrogenases by calcium ions. Biochim. Biophys. Acta 1787, 1309-1316
14. Duchen, M. R. (1992) Ca2+-dependent changes in the mitochondrial energetics in single dissociated mouse sensory neurons. Biochem. J. 283, 41-50
15. Liu, T., and O'Rourke, B. (2008) Enhancing mitochondrial Ca2+ uptake in myocytes from failing hearts restores energy supply and demand matching. Circ. Res. 103, 279-288
16. Kennedy, E. D., Rizzuto, R., Theler, J. M., Pralong, W. F., Bastianutto, C., Pozzan, T., and Wollheim, C. B. (1996) Glucose-stimulated insulin secretion correlates with changes in mitochondrial and cytosolic Ca2+ in ae-quorin-expressing INS-1 cells. J. Clin. Invest. 98, 2524-2538
17. Sweet, I. R., and Gilbert, M. (2006) Contribution of calcium influx in mediating glucose-stimulated oxygen consumption in pancreatic islets. Diabetes 55, 3509-3519 (Pubitemid 44923612)
18. Gilon, P., and Henquin, J. C. (1992) Influence of membrane potential changes on cytoplasmic Ca2+ concentration in an electrically excitable cell, the insulin-secreting pancreatic B-cell. J. Biol. Chem. 267, 20713-20720
19. Nicholls, L. I., Ainscow, E. K., and Rutter, G. A. (2002) Glucose-stimulated insulin secretion does not require activation of pyruvate dehydrogenase. Impact of adenovirus-mediated overexpression of PDH kinase and PDH phosphate phosphatase in pancreatic islets. Biochem. Biophys. Res. Commun. 291, 1081-1088 (Pubitemid 34694384)
20. Akhmedov, D., De Marchi, U., Wollheim, C. B., and Wiederkehr, A. (2012) Pyruvate dehydrogenase E1α phosphorylation is induced by glucose but does not control metabolism-secretion coupling in INS-1E clonal beta cells. Biochim. Biophys. Acta 1823, 1815-1824
21. Glancy, B., and Balaban, R. S. (2012) Role of mitochondrial Ca 2+ in the regulation of cellular energetics. Biochemistry 51, 2959-2973
22. Nagai, T., Yamada, S., Tominaga, T., Ichikawa, M., and Miyawaki, A. (2004) Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proc. Natl. Acad. Sci. U.S.A. 101, 10554-10559
23. Palmer, A. E., Giacomello, M., Kortemme, T., Hires, S.A., Lev-Ram, V., Baker, D., and Tsien, R. Y. (2006) Ca2+ indicators based on computationally redesigned calmodulin peptide pairs. Chem. Biol. 13, 521-530
24. Langhofer, M., Hopkinson, S. B., and Jones, J. C. (1993) The matrix secreted by 804G cells contains laminin-related components that participate in hemidesmosome assembly in vitro. J. Cell Sci. 105, 753-764 (Pubitemid 23243208)
25. Schultz, V., Sussman, I., Bokvist, K., and Tornheim, K. (1993) Bioluminometricassay of ADP and ATP at high ATP/ADP ratios. Assay of ADP after enzymatic removal of ATP. Anal. Biochem. 215, 302-304 (Pubitemid 23360921)
26. Ohta, M., Nelson, D., Nelson, J., Meglasson, M. D., and Ereciñska, M. (1990) Oxygen and temperature dependence of stimulated insulin secretion in isolated rat islets of Langerhans. J. Biol. Chem. 265, 17525-17532
27. Henquin, J. C., Dufrane, D., and Nenquin, M. (2006) Nutrient control of insulin secretion in isolated normal human islets. Diabetes 55, 3470-3477 (Pubitemid 44923607)
28. Meglasson, M.D., Nelson, J., Nelson, D., and Erecinska, M. (1989) Bioenergetic response of pancreatic islets to stimulation by fuel molecules. Metabolism 38, 1188-1195 (Pubitemid 20015494)
29. Detimary, P., Gilon, P., and Henquin, J.C. (1998) Interplay between cytoplasmic Ca2+ and the ATP/ADP ratio. A feedback control mechanism in mouse pancreatic islets. Biochem. J. 333, 269-274
30. Ohta, M., Nelson, J., Nelson, D., Meglasson, M.D., and Ereciñska, M. (1993) Effect of Ca2+ channel blockers on energy level and stimulated insulin secretion in isolated rat islets of Langerhans. J. Pharmacol. Exp. Ther. 264, 35-40
31. Patterson, G. H., Knobel, S. M., Arkhammar, P., Thastrup, O., and Piston, D. W. (2000) Separation of the glucose-stimulated cytoplasmic and mitochondrial NAD(P)H responses in pancreatic islet beta cells. Proc. Natl. Acad. Sci. U.S.A. 97, 5203-5207 (Pubitemid 30313696)
32. Pralong, W. F., Bartley, C., and Wollheim, C. B. (1990) Single islet beta cell stimulation by nutrients. Relationship between pyridine nucleotides, cytosolic Ca2+, and secretion. EMBO J. 9, 53-60
33. Luciani, D. S., Misler, S., and Polonsky, K. S. (2006) Ca2+ controls slow NAD(P)H oscillations in glucose-stimulated mouse pancreatic islets. J. Physiol. 572, 379-392
34. Braun, M., Ramracheya, R., Bengtsson, M., Zhang, Q., Karanauskaite, J., Partridge, C., Johnson, P. R., and Rorsman, P. (2008) Voltage-gated ion channels in human pancreatic beta cells. electrophysiological characterization and role in insulin secretion. Diabetes 57, 1618-1628
35. Doliba, N. M., Vatamaniuk, M. Z., Buettger, C. W., Qin, W., Collins, H. W., Wehrli, S. L., Carr, R. D., and Matschinsky, F. M. (2003) Differential effects of glucose and glyburide on energetics and Na+ levels of βHC9 cells. Nuclear magnetic resonance spectroscopy and respirometry studies. Diabetes 52, 394-402
36. Schuit, F., De Vos, A., Farfari, S., Moens, K., Pipeleers, D., Brun, T., and Prentki, M. (1997) Metabolic fate of glucose in purified islet cells. Glucose-regulated anaplerosis in beta cells. J. Biol. Chem. 272, 18572-18579 (Pubitemid 27318196)
37. Spégel, P., Malmgren, S., Sharoyko, V. V., Newsholme, P., Koeck, T., and Mulder, H. (2011) Metabolomic analyses reveal profound differences in glycolytic and tricarboxylic acid cycle metabolism in glucose-responsive and -unresponsive clonal beta cell lines. Biochem. J. 435, 277-284
38. Park, K. S., Wiederkehr, A., and Wollheim, C. B. (2012) Defective mitochondrial function and motility due to mitofusin 1 overexpression in insulin secreting cells. Korean J. Physiol. Pharmacol. 16, 71-77
39. Wu, M., Neilson, A., Swift, A. L., Moran, R., Tamagnine, J., Parslow, D., Armistead, S., Lemire, K., Orrell, J., Teich, J., Chomicz, S., and Ferrick, D. A. (2007) Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 292, C125-C136 (Pubitemid 46115126)
40. Affourtit, C., and Brand, M. D. (2008) Uncoupling protein-2 contributes significantly to high mitochondrial proton leak in INS-1E insulinoma cells and attenuates glucose-stimulated insulin secretion. Biochem. J. 409, 199-204
41. Samper, E., Morgado, L., Estrada, J. C., Bernad, A., Hubbard, A., Cadenas, S., and Melov, S. (2009) Increase in mitochondrial biogenesis, oxidative stress, and glycolysis in murine lymphomas. Free Radic. Biol. Med. 46, 387-396
42. Wikstrom, J. D., Sereda, S. B., Stiles, L., Elorza, A., Allister, E. M., Neilson, A., Ferrick, D. A., Wheeler, M. B., and Shirihai, O. S. (2012) A novel high-throughput assay for islet respiration reveals uncoupling of rodent and human islets. PLoS ONE 7, e33023
43. Wiederkehr, A. (2009) Matrix alkalinisation unleashes beta cell mitochondria. Islets 1, 154-156
44. Das, A. M., and Harris, D. A. (1989) Reversible modulation of the mitochondrial ATP synthase with energy demand in cultured rat cardiomyocytes. FEBS Lett. 256, 97-100 (Pubitemid 19246475)
45. Hajnóczky, G., Robb-Gaspers, L. D., Seitz, M. B., and Thomas, A. P. (1995) Decoding of cytosolic calcium oscillations in the mitochondria. Cell 82, 415-424
46. Moreno-Sánchez, R., Hogue, B. A., and Hansford, R. G. (1990) Influence of NAD-linked dehydrogenase activity on flux through oxidative phosphorylation. Biochem. J. 268, 421-428 (Pubitemid 20193983)