What couples glycolysis to mitochondrial signal generation in glucoses- stimulated insulin secretion?

IUBMB Life

Volumn 49, Issue 5, 2000, Pages 391-395

  Ishihara, Hisamitsu ^a   Wollheim, Claes B ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Glycolysis; Lactate dehydrogenase; Mitochondria; Mono carboxylate transporter; NADH shuttles; Pancreatic cell; Pyruvate

Indexed keywords

ANIMAL CELL; CONTROLLED STUDY; EXOCYTOSIS; GLYCOLYSIS; INSULIN RELEASE; MITOCHONDRION; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; RAT; REVIEW; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0033936159     PISSN: 15216543     EISSN: None     Source Type: Journal    
DOI: 10.1080/152165400410236     Document Type: Review

References (40)

1. DeFronzo, R. A. (1988) Lilly Lecture 1987. The triumvirate: β-cell, muscle, liver. A collusion responsible for NIDDM. Diabetes 37, 667-687.
2. Prentki, M. (1996) New insights into pancreatic β-cell metabolic signaling in insulin secretion. Eur. J. Endocrinol. 134, 272-286.
3. Matschinsky, F. M. (1996) Banting Lecture 1995. A lesson in metabolic regulation inspired by the glucokinase glucose sensor paradigm. Diabetes 45, 223-241.
4. Maechler, P., and Wollheim. C. B. (1999) Mitochondrial glutamate acts as a messenger in glucose-induced insulin exocytosis. Nature 402, 685-689.
5. Lembert, N., and Idahl, L. A. (1998) α-Ketoisocaproate is not a true substrate for ATP production by pancreatic β cell mitochondria. Diabetes 47, 339-344.
6. MacDonald, M. J. (1995) Feasibility of a mitochondrial pyruvate malate shuttle in pancreatic islets. Further implication of cytosolic NADPH in insulin secretion. J. Biol. Chem. 270, 20051-20058.
7. 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. J. Biol. Chem. 272, 18572-18579.
8. Sekine, N., Cirulli, V., Regazzi, R., Brown, L. J., Gine, E., Tamarit-Rodriguez, J., Girotti, M., Marie, S., MacDonald, M. J., Wollheim, C. B., and Rutter, G. A. (1994) Low lactate dehydrogenase and high mitochondrial glycerol phosphate dehydrogenase in pancreatic β-cells. J. Biol. Chem. 269, 4895-4902.
9. Hellman, B., Idahl, L.-A., Sehlin, J., and Taljidal, I.-B. (1975) Influence of anoxia on glucose.metabolism in pancreatic islets. Diabetologia 11, 495-500.
10. Hudson, R. C., and Daniel, R. M. (1993) L-Glutamate dehydrogenases: distribution, properties and mechanism. Comp. Biochem. Physiol. B 106, 767-792.
11. MacDonald, M. J. (1993) Estimates of glycolysis, pyruvate (de)carboxylation, pentose phosphate pathway, and methyl succinate metabolism in incapacitated pancreatic islets. Arch. Biochem. Biophys. 305, 205-214.
12. Khan, A., Ling, Z. C., and Landau, B. R. (1996) Quantifying the carboxylation of pyruvate in pancreatic islets. J. Biol. Chem. 271, 2539-2542.
13. MacDonald, M. J., McKenzie, D. I., Walker, T. M., and Kaysen, J. H. (1992) Lack of glyconeogenesis in pancreatic islets: expression of gluconeogenic enzyme genes in islets. Horm. Metab. Res. 24, 158-160.
14. MacDonald, M. J. (1995) Influence of glucose on pyruvate carboxylase expression in pancreatic islets. Arch. Biochem. Biophys. 319, 128-132.
15. Prentki, M., and Corkey, B. E. (1996) Are the beta-cell signaling molecules malonyl-CoA and cystolic long-chain acyl-CoA implicated in multiple tissue defects of obesity and NIDDM? Diabetes 45, 273-283.
16. Antinozzi, P. A., Segall, L., Prentki, M., McGarry, J. D., and Newgard, C. B. (1998) Molecular or pharmacologic perturbation of the link between glucose and lipid metabolism is without effect on glucose-stimulated insulin secretion. A re-evaluation of the long-chain acyl-CoA hypothesis. J. Biol. Chem. 273, 16146-16154.
17. Jijakli, H., Rasschaert, J., Nadi, A. B., Leclercq-Meyer, V., Sener, A., and Malaisse, W. J. (1996) Relevance of lactate dehydrogenase activity to the control of oxidative glycolysis in pancreatic β-cells. Arch. Biochem. Biophys. 327, 260-264.
18. Stryer, L. (1981) Glycolysis. In Biochemistry. pp. 255-279, W. H. Freeman, San Francisco.
19. Ishihara, H., Nakazaki, M., Kanegae, Y., Inukai, K., Asano, T., Katagiri, H., Yazaki, Y., Kikuchi, M., Miyazaki, J.-I., Saito, I., and Oka, Y. (1996) Effect of mitochondrial and/or cytosolic glycerol 3-phosphate dehydrogenase overexpression on glucose-stimulated insulin secretion from MIN6 and HIT cells. Diabetes 45, 1238-1244.
20. MacDonald, M. J. (1982) Evidence for the malate aspartate shuttle in pancreatic islets. Arch. Biochem. Biophys. 213, 643-649.
21. Malaisse, W. J., Malaisse-Lagae, F., and Sener, A. (1982) The stimulus-secretion coupling of glucose-induced insulin release: effect of aminooxyacetate upon nutrient-stimulated insulin secretion. Endocrinology 111, 392-397.
22. Mertz, R. J., Worley, J. F., III, Spencer, B., Johnson. J. H., and Dukes, I. D. (1996) Activation of stimulus-secretion coupling in pancreatic β-cells by specific products of glucose metabolism. J. Biol. Chem. 271, 4838-4845.
23. Eto, K., Tsubamoto, Y., Terauchi, Y., Sugiyama, T., Kishimoto, T., Takahashi, N., Yamauchi, N., Kubota, N., Murayama, S., Aizawa, T., Akanuma, Y., Aizawa, S., Kasai, H., Yazaki, Y., and Kadowaki, T. (1999) Role of NADH shuttling system in glucose-induced activation of mitochondrial metabolism and insulin secretion. Science 283, 981-985.
24. Price, N. T., Jackson. V. N., and Halestrap, A. P. (1998) Cloning and sequencing of four new mammalian monocarboxylate transporter (MCT) homologues confirms the existence of a transporter family with an ancient past. Biochem. J. 329, 321-328.
25. Best, L., Trebilcock, R., and Tomlinson, S. (1992) Lactate transport in insulin-secreting β-cells: contrast between rat islets and HIT-T15 insulinoma cells. Mol. Cell. Endocrinol. 86, 49-56.
26. Ishihara, H., Wang, H., Drewes, L. R., and Wollheim, C. B. (1999) Overexpression of monocarboxylate transporter and lactate dehydrogenase alters insulin secretory responses to pyruvate and lactate in beta cells. J. Clin. Invest. 104, 1621-1629.
27. Zhao, C., and Rutter, G. A. (1998) Overexpression of lactate dehydrogenase A attenuates glucose-induced insulin secretion in stable MIN-6 β-cell lines. FEBS Lett. 430, 213-216.
28. Izumi, Y., Benz, A. M., Zurumaski, C. F., and Olney, J. W. (1994) Effects of lactate and pyruvate on glucose deprivation in rat hippocampal slices. Neuroreport 5, 617-620.
29. Pellerin, L., Pellegri, G., Martin, J.-L., and Magistretti, P. (1998) Expression of monocarboxylate transporter mRNAs in mouse brain: support for a distinct role of lactate as an energy substrate for the neonatal vs. adult brain. Proc. Natl. Acad. Sci. U.S.A. 95, 3990-3995.
30. Malaisse, W. J., Kawazu, S., Herchuelz, A., Hutton, J. C., Somers, G., Devis, G., and Sener, A. (1979) The stimulus-secretion coupling of glucose-induced insulin release: effect of exogenous lactate upon islet function. Arch. Biochem, Biophys. 194, 49-62.
31. Lenzen, S., and Panten, U. (1981) Effects of pyruvate, L-lactate and 3-phenylpyruvate on function of ob/ob mouse pancreatic islets. Biochem. Med. 25, 366-372.
32. Sener, A., Kawazu, S., Hutton, J. C., Carlos Boschero, A., Somers, G., Herchuelz, A., and Malaisse, W. J. (1978) The stimulus-secretion coupling of glucose-induced insulin release: effect of exogenous pyruvate on islet function. Biochem. J. 176, 217-232.
33. Lambert, A. E., Junod, A., Stauffacher, W., Jeanrenaud, B., and Renold, A. E. (1969) Organ culture of fetal rat pancreas. Biochim. Biophys. Acta 184, 529-539.
34. Baetens, D., Malaisse-Lagae, F., Perrelet, A., and Orci, L. (1979) Endocrine pancreas: three-dimensional reconstitution shows two type of islets of Langerhans. Science 206, 1323-1325.
35. Malaisse, W. J., Jijakli, H., Ulusoy, S., Cook, L., Best, L., Vinambres, C., Villanueva-Penacarrillo, M. L., Valverde, I., and Sener, A. (1996) Insulinotropic action of methyl pyruvate: enzymatic and metabolic aspects. Arch. Biochem. Biophys. 335, 229-244.
36. Zawalich, W. S., and Zawalich, K. C. (1997) Influence of pyruvic acid methyl ester on rat pancreatic islets. J. Biol. Chem. 272, 3527-3531.
37. -distribution in humans during and after high-intensity exercise: role in muscle fatigue attenuation? J. Appl. Physiol. 78, 765-777.
38. Marliss, E. B., Wollheim, C. B., Blondel, B., Orci, L., Lambert, A. E., Stauffacher, W., Like, A. A., and Renold, A. E. (1973) Insulin and glucagon release from monolayer cell cultures of pancreas from newborn rats. Eur. J. Clin. Invest. 3, 16-26.
39. Leclercq, V., Marchand, J., and Malaisse, W. J. (1977) An arginine-like effect of the "fumarate + glutamate + pyruvate" mixture on glucagon release. Life Sci. 20, 1193-1198.
40. Gerhart, D., Enerson, B. E., Zhdankina, O. Y., Leino, R. L., and Drewes, L. R. (1997) Expression of monocarboxylate transporter MCT1 by brain endothelium and glia in adult and suckling rats. Am. J. Physiol. 273 (Endocrinol. Metab. 36), E207-E213.