Glutamate acts as a key signal linking glucose metabolism to incretin/cAMP action to amplify insulin secretion

Cell Reports

Volumn 9, Issue 2, 2014, Pages 661-673

  Gheni, Ghupurjan ^a   Ogura, Masahito ^a,b   Iwasaki, Masahiro ^a,h   Yokoi, Norihide ^a   Minami, Kohtaro ^a   Nakayama, Yasumune ^c   Harada, Kazuo ^c   Hastoy, Benoit ^d   Wu, Xichen ^e   Takahashi, Harumi ^a   Kimura, Kazushi ^f   Matsubara, Toshiya ^a,g   Hoshikawa, Ritsuko ^a   Hatano, Naoya ^a   Sugawara, Kenji ^a   Shibasaki, Tadao ^a   Inagaki, Nobuya ^b   Bamba, Takeshi ^c   Mizoguchi, Akira ^f   Fukusaki, Eiichiro ^c   Rorsman, Patrik ^d   Seino, Susumu ^a   more..

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF ALBERTA   (Canada)

^f MIE UNIVERSITY   (Japan)

^g SHIMADZU CORPORATION   (Japan)

^h KANSAI ELECTRIC POWER CO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUTAMIC ACID; INCRETIN; MALIC ACID; GLUCOSE; INSULIN;

AMINO ACID SYNTHESIS; AMINO ACID TRANSPORT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL TRANSPORT; CONTROLLED STUDY; DIABETES MELLITUS; EXOCYTOSIS; GLUCOSE METABOLISM; INSULIN RELEASE; MALE; METABOLOME; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PATHOPHYSIOLOGY; RAT; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CYTOPLASM; DRUG EFFECTS; METABOLISM; SECRETORY VESICLE; TUMOR CELL LINE; WISTAR RAT;

ANIMALIA;

ANIMALS; CELL LINE, TUMOR; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOPLASM; EXOCYTOSIS; GLUCOSE; GLUTAMIC ACID; INCRETINS; INSULIN; INSULIN-SECRETING CELLS; MALE; METABOLOME; MICE; RATS; RATS, WISTAR; SECRETORY VESICLES; SIGNAL TRANSDUCTION;

EID: 84919685379     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.09.030     Document Type: Article

References (62)

1. Ahrén, B. (2009). Islet G protein-coupled receptors as potential targets for treatment of type 2 diabetes. Nat. Rev. Drug Discov. 8, 369-385.
2. Aspinwall, C.A., Brooks, S.A., Kennedy, R.T., and Lakey, J.R. (1997). Effects of intravesicular H+ and extracellular H+ and Zn2+ on insulin secretion in pancreatic beta cells. J. Biol. Chem. 272, 31308-31314.
3. Bai, L., Zhang, X., and Ghishan, F.K. (2003). Characterization of vesicular glutamate transporter in pancreatic α-and β-cells and its regulation by glucose. Am. J. Physiol. Gastrointest. Liver Physiol. 284, G808-G814.
4. Bellocchio, E.E., Reimer, R.J., Fremeau, R.T., Jr., and Edwards, R.H. (2000). Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289, 957-960.
5. Bertrand, G., Ishiyama, N., Nenquin, M., Ravier, M.A., and Henquin, J.C. (2002). The elevation of glutamate content and the amplification of insulin secretion in glucose-stimulated pancreatic islets are not causally related. J. Biol. Chem. 277, 32883-32891.
6. Bos, J.L. (2006). Epac proteins: multi-purpose cAMP targets. Trends Biochem. Sci. 31, 680-686.
7. Brisson, G.R., Malaisse-Lagae, F., and Malaisse, W.J. (1972). The stimulussecretion coupling of glucose-induced insulin release. VII. A proposed site of action for adenosine-3',5'-cyclic monophosphate. J. Clin. Invest. 51, 232-241.
8. Brozzi, F., Lajus, S., Diraison, F., Rajatileka, S., Hayward, K., Regazzi, R., Molnár, E., and Váradi, A. (2012). MyRIP interaction with MyoVa on secretory granules is controlled by the cAMP-PKA pathway. Mol. Biol. Cell 23, 4444-4455.
9. Carobbio, S., Frigerio, F., Rubi, B., Vetterli, L., Bloksgaard, M., Gjinovci, A., Pournourmohammadi, S., Herrera, P.L., Reith, W., Mandrup, S., and Maechler, P. (2009). Deletion of glutamate dehydrogenase in beta-cells abolishes part of the insulin secretory response not required for glucose homeostasis. J. Biol. Chem. 284, 921-929.
10. Casimir, M., Lasorsa, F.M., Rubi, B., Caille, D., Palmieri, F., Meda, P., and Maechler, P. (2009). Mitochondrial glutamate carrier GC1 as a newly identified player in the control of glucose-stimulated insulin secretion. J. Biol. Chem. 284, 25004-25014.
11. Cataland, S., Crockett, S.E., Brown, J.C., and Mazzaferri, E.L. (1974). Gastric inhibitory polypeptide (GIP) stimulation by oral glucose in man. J. Clin. Endocrinol. Metab. 39, 223-228.
12. Charles, M.A., Fanska, R., Schmid, F.G., Forsham, P.H., and Grodsky, G.M. (1973). Adenosine 3′,5′-monophosphate in pancreatic islets: glucose-induced insulin release. Science 179, 569-571.
13. Delmeire, D., Flamez, D., Hinke, S.A., Cali, J.J., Pipeleers, D., and Schuit, F. (2003). Type VIII adenylyl cyclase in rat beta cells: coincidence signal detector/ generator for glucose and GLP-1. Diabetologia 46, 1383-1393.
14. Drucker, D.J. (2006). The biology of incretin hormones. Cell Metab. 3, 153-165.
15. Drucker, D.J., and Nauck, M.A. (2006). The incretin system: glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 368, 1696-1705.
16. Dyachok, O., Idevall-Hagren, O., Sågetorp, J., Tian, G., Wuttke, A., Arrieumerlou, C., Akusjärvi, G., Gylfe, E., and Tengholm, A. (2008). Glucose-induced cyclic AMP oscillations regulate pulsatile insulin secretion. Cell Metab. 8, 26-37.
17. Eliasson, L., Ma, X., Renström, E., Barg, S., Berggren, P.O., Galvanovskis, J., Gromada, J., Jing, X., Lundquist, I., Salehi, A., et al. (2003). SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic Bcells. J. Gen. Physiol. 121, 181-197.
18. Eto, K., Tsubamoto, Y., Terauchi, Y., Sugiyama, T., Kishimoto, T., Takahashi, N., Yamauchi, N., Kubota, N., Murayama, S., Aizawa, T., et al. (1999). Role of NADH shuttle system in glucose-induced activation of mitochondrial metabolism and insulin secretion. Science 283, 981-985.
19. Gammelsaeter, R., Coppola, T., Marcaggi, P., Storm-Mathisen, J., Chaudhry, F.A., Attwell, D., Regazzi, R., and Gundersen, V. (2011). A role for glutamate transporters in the regulation of insulin secretion. PLoS ONE 6, e22960.
20. Goto, Y., Kakizaki, M., and Masaki, N. (1975). Spontaneous diabetes produced by selective breeding of normal Wistar rats. Proc. Jpn. Acad. 51, 80-85.
21. Gras, C., Herzog, E., Bellenchi, G.C., Bernard, V., Ravassard, P., Pohl, M., Gasnier, B., Giros, B., and El Mestikawy, S. (2002). A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J. Neurosci. 22, 5442-5451.
22. Grill, V., and Cerasi, E. (1973). Activation by glucose of adenyl cyclase in pancreatic islets of the rat. FEBS Lett. 33, 311-314.
23. Henquin, J.C. (2000). Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes 49, 1751-1760.
24. Holst, J.J. (2007). The physiology of glucagon-like peptide 1. Physiol. Rev. 87, 1409-1439.
25. Holst, J.J., Knop, F.K., Vilsbøll, T., Krarup, T., and Madsbad, S. (2011). Loss of incretin effect is a specific, important, and early characteristic of type 2 diabetes. Diabetes Care 34 (Suppl 2), S251-S257.
26. Høy, M., Maechler, P., Efanov, A.M., Wollheim, C.B., Berggren, P.O., and Gromada, J. (2002). Increase in cellular glutamate levels stimulates exocytosis in pancreatic beta-cells. FEBS Lett. 531, 199-203.
27. Iwasaki, M., Minami, K., Shibasaki, T., Miki, T., Miyazaki, J., and Seino, S. (2010). Establishment of new clonal pancreatic β-cell lines (MIN6-K) useful for study of incretin/cyclic adenosine monophosphate signaling. J. Diabetes Investig. 1, 137-142.
28. Kanno, T., Ma, X., Barg, S., Eliasson, L., Galvanovskis, J., Göpel, S., Larsson, M., Renström, E., and Rorsman, P. (2004). Large dense-core vesicle exocytosis in pancreatic beta-cells monitored by capacitance measurements. Methods 33, 302-311.
29. Kreymann, B., Williams, G., Ghatei, M.A., and Bloom, S.R. (1987). Glucagonlike peptide-1 7-36: a physiological incretin in man. Lancet 2, 1300-1304.
30. Kubota, A., Maeda, H., Kanamori, A., Matoba, K., Jin, Y., Minagawa, F., Obana, M., Iemitsu, K., Ito, S., Amamiya, H., et al. (2012). Efficacy and safety of sitagliptin monotherapy and combination therapy in Japanese type 2 diabetes patients. J. Diabetes Investig. 3, 503-509.
31. Li, D.Q., Jing, X., Salehi, A., Collins, S.C., Hoppa, M.B., Rosengren, A.H., Zhang, E., Lundquist, I., Olofsson, C.S., Mörgelin, M., et al. (2009). Suppression of sulfonylurea-and glucose-induced insulin secretion in vitro and in vivo in mice lacking the chloride transport protein ClC-3. Cell Metab. 10, 309-315.
32. MacDonald, M.J. (1982). Evidence for the malate aspartate shuttle in pancreatic islets. Arch. Biochem. Biophys. 213, 643-649.
33. MacDonald, M.J., and Fahien, L.A. (2000). Glutamate is not a messenger in insulin secretion. J. Biol. Chem. 275, 34025-34027.
34. Maechler, P., and Wollheim, C.B. (1999). Mitochondrial glutamate acts as a messenger in glucose-induced insulin exocytosis. Nature 402, 685-689.
35. Matsubara, T., Mita, A., Minami, K., Hosooka, T., Kitazawa, S., Takahashi, K., Tamori, Y., Yokoi, N., Watanabe, M., Matsuo, E., et al. (2012). PGRN is a key adipokine mediating high fat diet-induced insulin resistance and obesity through IL-6 in adipose tissue. Cell Metab. 15, 38-50.
36. Naito, S., and Ueda, T. (1983). Adenosine triphosphate-dependent uptake of glutamate into protein I-associated synaptic vesicles. J. Biol. Chem. 258, 696-699.
37. Nauck, M.A., Heimesaat, M.M., Orskov, C., Holst, J.J., Ebert, R., and Creutzfeldt, W. (1993). Preserved incretin activity of glucagon-like peptide 1 [7-36 amide] but not of synthetic human gastric inhibitory polypeptide in patients with type-2 diabetes mellitus. J. Clin. Invest. 91, 301-307.
38. Omote, H., Miyaji, T., Juge, N., and Moriyama, Y. (2011). Vesicular neurotransmitter transporter: bioenergetics and regulation of glutamate transport. Biochemistry 50, 5558-5565.
39. Ostenson, C.G., Khan, A., Abdel-Halim, S.M., Guenifi, A., Suzuki, K., Goto, Y., and Efendic, S. (1993). Abnormal insulin secretion and glucose metabolism in pancreatic islets from the spontaneously diabetic GK rat. Diabetologia 36, 3-8.
40. Peyot, M.L., Gray, J.P., Lamontagne, J., Smith, P.J., Holz, G.G., Madiraju, S.R., Prentki, M., and Heart, E. (2009). Glucagon-like peptide-1 induced signaling and insulin secretion do not drive fuel and energy metabolism in primary rodent pancreatic β-cells. PLoS ONE 4, e6221.
41. Polonsky, K.S., Given, B.D., Hirsch, L.J., Tillil, H., Shapiro, E.T., Beebe, C., Frank, B.H., Galloway, J.A., and Van Cauter, E. (1988). Abnormal patterns of insulin secretion in non-insulin-dependent diabetes mellitus. N. Engl. J. Med. 318, 1231-1239.
42. Porte, D., Jr. (1991). Banting lecture 1990. Beta-cells in type II diabetes mellitus. Diabetes 40, 166-180.
43. 2+, cAMP, and phospholipidderived messengers in coupling mechanisms of insulin secretion. Physiol. Rev. 67, 1185-1248.
44. Rorsman, P., and Renström, E. (2003). Insulin granule dynamics in pancreatic beta cells. Diabetologia 46, 1029-1045.
45. Roseth, S., Fykse, E.M., and Fonnum, F. (1995). Uptake of L-glutamate into rat brain synaptic vesicles: effect of inhibitors that bind specifically to the glutamate transporter. J. Neurochem. 65, 96-103.
46. Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., et al. (2003). TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374-378.
47. Seino, S., and Shibasaki, T. (2005). PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol. Rev. 85, 1303-1342.
48. Seino, Y., Fukushima, M., and Yabe, D. (2010). GIP and GLP-1, the two incretin hormones: similarities and differences. J. Diabetes Investig. 1, 8-23.
49. Seino, S., Shibasaki, T., and Minami, K. (2011). Dynamics of insulin secretion and the clinical implications for obesity and diabetes. J. Clin. Invest. 121, 2118-2125.
50. Shibasaki, T., Takahashi, H., Miki, T., Sunaga, Y., Matsumura, K., Yamanaka, M., Zhang, C., Tamamoto, A., Satoh, T., Miyazaki, J., and Seino, S. (2007). Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc. Natl. Acad. Sci. USA 104, 19333-19338.
51. Siegel, E.G., and Creutzfeldt, W. (1985). Stimulation of insulin release in isolated rat islets by GIP in physiological concentrations and its relation to islet cyclic AMP content. Diabetologia 28, 857-861.
52. Song, W.J., Seshadri, M., Ashraf, U., Mdluli, T., Mondal, P., Keil, M., Azevedo, M., Kirschner, L.S., Stratakis, C.A., and Hussain, M.A. (2011). Snapin mediates incretin action and augments glucose-dependent insulin secretion. Cell Metab. 13, 308-319.
53. Sugawara, K., Shibasaki, T., Mizoguchi, A., Saito, T., and Seino, S. (2009). Rab11 and its effector Rip11 participate in regulation of insulin granule exocytosis. Genes Cells 14, 445-456.
54. Susini, S., Roche, E., Prentki, M., and Schlegel, W. (1998). Glucose and glucoincretin peptides synergize to induce c-fos, c-jun, junB, zif-268, and nur-77 gene expression in pancreatic β(INS-1) cells. FASEB J. 12, 1173-1182.
55. Takamori, S., Rhee, J.S., Rosenmund, C., and Jahn, R. (2001). Identification of differentiation-associated brain-specific phosphate transporter as a second vesicular glutamate transporter (VGLUT2). J. Neurosci. 21, RC182.
56. Uehara, S., Jung, S.K., Morimoto, R., Arioka, S., Miyaji, T., Juge, N., Hiasa, M., Shimizu, K., Ishimura, A., Otsuka, M., et al. (2006). Vesicular storage and secretion of L-glutamate from glucagon-like peptide 1-secreting clonal intestinal L cells. J. Neurochem. 96, 550-560.
57. Vetterli, L., Carobbio, S., Pournourmohammadi, S., Martin-Del-Rio, R., Skytt, D.M., Waagepetersen, H.S., Tamarit-Rodriguez, J., and Maechler, P. (2012). Delineation of glutamate pathways and secretory responses in pancreatic islets with β-cell-specific abrogation of the glutamate dehydrogenase. Mol. Biol. Cell 23, 3851-3862.
58. Weir, G.C., Mojsov, S., Hendrick, G.K., and Habener, J.F. (1989). Glucagonlike peptide I (7-37) actions on endocrine pancreas. Diabetes 38, 338-342.
59. Xie, X.S., Stone, D.K., and Racker, E. (1983). Determinants of clathrin-coated vesicle acidification. J. Biol. Chem. 258, 14834-14838.
60. Xie, X.S., Crider, B.P., and Stone, D.K. (1989). Isolation and reconstitution of the chloride transporter of clathrin-coated vesicles. J. Biol. Chem. 264, 18870-18873.
61. Yasuda, T., Shibasaki, T., Minami, K., Takahashi, H., Mizoguchi, A., Uriu, Y., Numata, T., Mori, Y., Miyazaki, J., Miki, T., and Seino, S. (2010). Rim2a determines docking and priming states in insulin granule exocytosis. Cell Metab. 12, 117-129.
62. Zucker, L.M., and Zucker, T.F. (1961). Fatty, a new mutation in the rat. J. Hered. 52, 275-278.