Exciting Times for Pancreatic Islets: Glutamate Signaling in Endocrine Cells

Trends in Endocrinology and Metabolism

Volumn 27, Issue 3, 2016, Pages 177-188

  Otter, Silke ^a,b   Lammert, Eckhard ^a,b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

Author keywords

Diabetes mellitus; Drug; Glutamate; Insulin secretion; NMDA receptor; Pancreatic beta cell

Indexed keywords

4 AMINOBUTYRIC ACID; 4 HYDROXYBUTYRIC ACID; AMPA RECEPTOR; GLUCAGON; GLUCOSE; GLUTAMATE DEHYDROGENASE; GLUTAMATE RECEPTOR ANTAGONIST; GLUTAMIC ACID; INCRETIN; INSULIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; SOMATOSTATIN; AMINO ACID RECEPTOR BLOCKING AGENT; ANTIDIABETIC AGENT; GLUTAMATE RECEPTOR;

CELL FUNCTION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; DIABETES MELLITUS; ENDOCRINE CELL; HUMAN; INSULIN RELEASE; INTRACELLULAR TRANSPORT; NERVE CELL; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REVIEW; SECRETORY GRANULE; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; COMPARATIVE STUDY; DIABETES MELLITUS, TYPE 2; DRUG EFFECTS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SECOND MESSENGER; SECRETION (PROCESS); SECRETORY VESICLE;

ANIMALS; DIABETES MELLITUS, TYPE 2; EXCITATORY AMINO ACID ANTAGONISTS; GLUTAMIC ACID; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; ISLETS OF LANGERHANS; MODELS, BIOLOGICAL; RECEPTORS, GLUTAMATE; SECOND MESSENGER SYSTEMS; SECRETORY VESICLES;

EID: 84958114147     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2015.12.004     Document Type: Review

References (100)

1. Rutter G.A., et al. Pancreatic beta-cell identity, glucose sensing and the control of insulin secretion. Biochem. J. 2015, 466:203-218.
2. Rorsman P., Braun M. Regulation of insulin secretion in human pancreatic islets. Annu. Rev. Physiol. 2013, 75:155-179.
3. Folias A.E., Hebrok M. Pancreas overview. Metabolism of Human Diseases 2014, 157-162. Springer. E. Lammert, M. Zeeb (Eds.).
4. Eberhard D., Lammert E. The pancreatic beta-cell in the islet and organ community. Curr. Opin. Genet. Dev. 2009, 19:469-475.
5. Drucker D.J., Nauck M.A. The incretin system: glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 2006, 368:1696-1705.
6. El Ouaamari A., et al. Liver-derived systemic factors drive beta cell hyperplasia in insulin-resistant states. Cell Rep. 2013, 3:401-410.
7. Arntfield M.E., van der Kooy D. β-Cell evolution: how the pancreas borrowed from the brain: the shared toolbox of genes expressed by neural and pancreatic endocrine cells may reflect their evolutionary relationship. Bioessays 2011, 33:582-587.
8. Koh D.S., et al. Paracrine interactions within islets of Langerhans. J. Mol. Neurosci. 2012, 48:429-440.
9. Doyle M.E. The role of the endocannabinoid system in islet biology. Curr. Opin. Endocrinol. Diabetes Obes. 2011, 18:153-158.
10. Pin J.P., Duvoisin R. The metabotropic glutamate receptors: structure and functions. Neuropharmacology 1995, 34:1-26.
11. Soltani N., et al. GABA exerts protective and regenerative effects on islet beta cells and reverses diabetes. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:11692-11697.
12. Braun M., et al. Gamma-aminobutyric acid (GABA) is an autocrine excitatory transmitter in human pancreatic beta-cells. Diabetes 2010, 59:1694-1701.
13. Cabrera O., et al. Glutamate is a positive autocrine signal for glucagon release. Cell Metab. 2008, 7:545-554.
14. Lutz T.A., Meyer U. Amylin at the interface between metabolic and neurodegenerative disorders. Front. Neurosci. 2015, 9:216.
15. Eizirik D.L., et al. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr. Rev. 2008, 29:42-61.
16. Brown M.K., Naidoo N. The endoplasmic reticulum stress response in aging and age-related diseases. Front. Physiol. 2012, 3:263.
17. Jain D., et al. DJ-1 protects pancreatic beta cells from cytokine- and streptozotocin-mediated cell death. PLoS ONE 2015, 10:e0138535.
18. Jain D., et al. Age- and diet-dependent requirement of DJ-1 for glucose homeostasis in mice with implications for human type 2 diabetes. J. Mol. Cell Biol. 2012, 4:221-230.
19. Aron L., et al. Pro-survival role for Parkinson's associated gene DJ-1 revealed in trophically impaired dopaminergic neurons. PLoS Biol. 2010, 8:e1000349.
20. Kim J.H., et al. DJ-1 facilitates the interaction between STAT1 and its phosphatase SHP-1, in brain microglia and astrocytes: a novel anti-inflammatory function of DJ-1. Neurobiol. Dis. 2013, 60:1-10.
21. Nassel D.R., et al. Factors that regulate insulin producing cells and their output in Drosophila. Front. Physiol. 2013, 4:252.
22. Caruso M.A., Sheridan M.A. New insights into the signaling system and function of insulin in fish. Gen. Comp. Endocrinol. 2011, 173:227-247.
23. Maechler P., Wollheim C.B. Mitochondrial glutamate acts as a messenger in glucose-induced insulin exocytosis. Nature 1999, 402:685-689.
24. Di Cairano E.S., et al. The glial glutamate transporter 1 (GLT1) is expressed by pancreatic beta-cells and prevents glutamate-induced beta-cell death. J. Biol. Chem. 2011, 286:14007-14018.
25. Marquard J., et al. Characterization of pancreatic NMDA receptors as possible drug targets for diabetes treatment. Nat. Med. 2015, 21:363-372.
26. Simo R., Hernandez C. Neurodegeneration in the diabetic eye: new insights and therapeutic perspectives. Trends Endocrinol. Metab. 2014, 25:23-33.
27. Fan X., et al. The NMDA receptor complex: a multifunctional machine at the glutamatergic synapse. Front. Cell Neurosci. 2014, 8:160.
28. Fava E., et al. Novel standards in the measurement of rat insulin granules combining electron microscopy, high-content image analysis and in silico modelling. Diabetologia 2012, 55:1013-1023.
29. Hu Y., et al. Mean synaptic vesicle size varies among individual excitatory hippocampal synapses. Synapse 2008, 62:953-957.
30. MacDonald P.E., et al. Regulated exocytosis and kiss-and-run of synaptic-like microvesicles in INS-1 and primary rat beta-cells. Diabetes 2005, 54:736-743.
31. Schuit F., et al. Metabolic fate of glucose in purified islet cells. Glucose-regulated anaplerosis in beta cells. J. Biol. Chem. 1997, 272:18572-18579.
32. MacDonald M.J., et al. Differences between human and rodent pancreatic islets: low pyruvate carboxylase ATP citrate lyase, and pyruvate carboxylation and high glucose-stimulated acetoacetate in human pancreatic islets. J. Biol. Chem. 2011, 286:18383-18396.
33. Gheni G., et al. Glutamate acts as a key signal linking glucose metabolism to incretin/cAMP action to amplify insulin secretion. Cell Rep. 2014, 9:661-673.
34. Vetterli L., et al. Delineation of glutamate pathways and secretory responses in pancreatic islets with beta-cell-specific abrogation of the glutamate dehydrogenase. Mol. Biol. Cell 2012, 23:3851-3862.
35. Hawkins R.A. The blood-brain barrier and glutamate. Am. J. Clin. Nutr. 2009, 90:867S-874S.
36. Featherstone D.E., Shippy S.A. Regulation of synaptic transmission by ambient extracellular glutamate. Neuroscientist 2008, 14:171-181.
37. Lammert E., et al. Role of VEGF-A in vascularization of pancreatic islets. Curr. Biol. 2003, 13:1070-1074.
38. Traynelis S.F., et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 2010, 62:405-496.
39. Thorens B. GLUT2, glucose sensing and glucose homeostasis. Diabetologia 2015, 58:221-232.
40. Gilon P., et al. Calcium signaling in pancreatic beta-cells in health and in type 2 diabetes. Cell Calcium 2014, 56:340-361.
41. Yang S.N., et al. Ionic mechanisms in pancreatic beta cell signaling. Cell. Mol. Life Sci. 2014, 71:4149-4177.
42. Satin L.S., et al. Pulsatile insulin secretion, impaired glucose tolerance and type 2 diabetes. Mol. Aspects Med. 2015, 42:61-77.
43. Feldmann N., et al. Reduction of plasma membrane glutamate transport potentiates insulin but not glucagon secretion in pancreatic islet cells. Mol. Cell. Endocrinol. 2011, 338:46-57.
44. Schousboe A., et al. Astrocytic control of biosynthesis and turnover of the neurotransmitters glutamate and GABA. Front. Endocrinol. (Lausanne) 2013, 4:102.
45. Casimir M., et al. Mitochondrial glutamate carrier GC1 as a newly identified player in the control of glucose-stimulated insulin secretion. J. Biol. Chem. 2009, 284:25004-25014.
46. Zhou Y., et al. Proteome analysis and conditional deletion of the EAAT2 glutamate transporter provide evidence against a role of EAAT2 in pancreatic insulin secretion in mice. J. Biol. Chem. 2014, 289:1329-1344.
47. Jenstad M., Chaudhry F.A. The amino acid transporters of the glutamate/GABA-glutamine cycle and their impact on insulin and glucagon secretion. Front. Endocrinol. (Lausanne) 2013, 4:199.
48. Gammelsaeter R., et al. A role for glutamate transporters in the regulation of insulin secretion. PLoS ONE 2011, 6:e22960.
49. Maechler P. Mitochondrial function and insulin secretion. Mol. Cell. Endocrinol. 2013, 379:12-18.
50. Fahien L.A., Macdonald M.J. The complex mechanism of glutamate dehydrogenase in insulin secretion. Diabetes 2011, 60:2450-2454.
51. Prentki M., et al. Metabolic signaling in fuel-induced insulin secretion. Cell Metab. 2013, 18:162-185.
52. Plaitakis A., et al. Deregulation of glutamate dehydrogenase in human neurologic disorders. J. Neurosci. Res. 2013, 91:1007-1017.
53. Cho J.H., et al. Characteristics and functions of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptors expressed in mouse pancreatic α-cells. Endocrinology 2010, 151:1541-1550.
54. Hayashi M., et al. Secretory granule-mediated co-secretion of l-glutamate and glucagon triggers glutamatergic signal transmission in islets of Langerhans. J. Biol. Chem. 2003, 278:1966-1974.
55. Muroyama A., et al. A novel variant of ionotropic glutamate receptor regulates somatostatin secretion from delta-cells of islets of Langerhans. Diabetes 2004, 53:1743-1753.
56. Liu Y., et al. Emerging regulatory paradigms in glutathione metabolism. Adv. Cancer Res. 2014, 122:69-101.
57. Merry T.L., et al. High-fat-fed obese glutathione peroxidase 1-deficient mice exhibit defective insulin secretion but protection from hepatic steatosis and liver damage. Antioxid. Redox Signal. 2014, 20:2114-2129.
58. Mahadevan J., et al. Ebselen treatment prevents islet apoptosis, maintains intranuclear Pdx-1 and MafA levels, and preserves beta-cell mass and function in ZDF rats. Diabetes 2013, 62:3582-3588.
59. Kanaani J., et al. Compartmentalization of GABA synthesis by GAD67 differs between pancreatic beta cells and neurons. PLoS ONE 2015, 10:e0117130.
60. Reetz A., et al. GABA and pancreatic beta-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion. EMBO J. 1991, 10:1275-1284.
61. Li C., et al. Regulation of glucagon secretion in normal and diabetic human islets by gamma-hydroxybutyrate and glycine. J. Biol. Chem. 2013, 288:3938-3951.
62. Chevassus H., et al. Effects of oral monosodium (l)-glutamate on insulin secretion and glucose tolerance in healthy volunteers. Br. J. Clin. Pharmacol. 2002, 53:641-643.
63. Graham T.E., et al. Glutamate ingestion: the plasma and muscle free amino acid pools of resting humans. Am. J. Physiol. Endocrinol. Metab. 2000, 278:E83-E89.
64. Mook-Kanamori D.O., et al. Type 2 diabetes is associated with postprandial amino acid measures. Arch. Biochem. Biophys. 2015, Published online August 10, 2015. 10.1016/j.abb.2015.08.003.
65. Bertrand G., et al. Evidence for a glutamate receptor of the AMPA subtype which mediates insulin release from rat perfused pancreas. Br. J. Pharmacol. 1992, 106:354-359.
66. Lerma J., Marques J.M. Kainate receptors in health and disease. Neuron 2013, 80:292-311.
67. Bertrand G., et al. Glutamate stimulates insulin secretion and improves glucose tolerance in rats. Am. J. Physiol. 1995, 269:E551-E556.
68. Huypens P., et al. Glucagon receptors on human islet cells contribute to glucose competence of insulin release. Diabetologia 2000, 43:1012-1019.
69. Omar B., et al. Conditional glucagon receptor overexpression has multi-faceted consequences for beta-cell function. Metabolism 2014, 63:1568-1576.
70. Gelling R.W., et al. Pancreatic beta-cell overexpression of the glucagon receptor gene results in enhanced beta-cell function and mass. Am. J. Physiol. Endocrinol. Metab. 2009, 297:E695-E707.
71. Wu Z.Y., et al. AMPA receptors regulate exocytosis and insulin release in pancreatic beta cells. Traffic 2012, 13:1124-1139.
72. Kailey B., et al. SSTR2 is the functionally dominant somatostatin receptor in human pancreatic beta- and alpha-cells. Am. J. Physiol. Endocrinol. Metab. 2012, 303:E1107-E1116.
73. Bosco D., et al. Unique arrangement of alpha- and beta-cells in human islets of Langerhans. Diabetes 2010, 59:1202-1210.
74. Cabrera O., et al. The unique cytoarchitecture of human pancreatic islets has implications for islet cell function. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:2334-2339.
75. Molina J., et al. Control of insulin secretion by cholinergic signaling in the human pancreatic islet. Diabetes 2014, 63:2714-2726.
76. van der Meulen T., et al. Urocortin 3 mediates somatostatin-dependent negative feedback control of insulin secretion. Nat. Med. 2015, 21:769-776.
77. Almaca J., et al. Young capillary vessels rejuvenate aged pancreatic islets. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:17612-17617.
78. Dufer M., et al. Enhanced glucose tolerance by SK4 channel inhibition in pancreatic beta-cells. Diabetes 2009, 58:1835-1843.
79. + currents through a nitric oxide-cGMP pathway in subthalamic neurons. J. Neurosci. 2010, 30:1882-1893.
80. Schiemann J., et al. K-ATP channels in dopamine substantia nigra neurons control bursting and novelty-induced exploration. Nat. Neurosci. 2012, 15:1272-1280.
81. Uehara S., et al. Metabotropic glutamate receptor type 4 is involved in autoinhibitory cascade for glucagon secretion by alpha-cells of islet of Langerhans. Diabetes 2004, 53:998-1006.
82. Storto M., et al. Insulin secretion is controlled by mGlu5 metabotropic glutamate receptors. Mol. Pharmacol. 2006, 69:1234-1241.
83. Soni A., et al. GPRC5B a putative glutamate-receptor candidate is negative modulator of insulin secretion. Biochem. Biophys. Res. Commun. 2013, 441:643-648.
84. Fowler S.W., et al. Functional interaction of mGlu5 and NMDA receptors in aversive learning in rats. Neurobiol. Learn. Mem. 2011, 95:73-79.
85. Dicpinigaitis P.V. Clinical perspective - cough: an unmet need. Curr. Opin. Pharmacol. 2015, 22:24-28.
86. Garnock-Jones K.P. Dextromethorphan/quinidine: in pseudobulbar affect. CNS Drugs 2011, 25:435-445.
87. Hamosh A., et al. Long-term use of high-dose benzoate and dextromethorphan for the treatment of nonketotic hyperglycinemia. J. Pediatr. 1998, 132:709-713.
88. Kalia L.V., et al. NMDA receptors in clinical neurology: excitatory times ahead. Lancet Neurol. 2008, 7:742-755.
89. Nguyen L., et al. Involvement of sigma-1 receptors in the antidepressant-like effects of dextromethorphan. PLoS ONE 2014, 9:e89985.
90. Marquard J., et al. Effects of dextromethorphan as add-on to sitagliptin on blood glucose and serum insulin concentrations in individuals with type 2 diabetes mellitus: a randomized, placebo-controlled, double-blinded, multiple crossover, single-dose clinical trial. Diabetes Obes. Metab. 2015, Published online September 12, 2015. 10.1111/dom.12576.
91. Lechin F., et al. Amantadine reduces glucagon and enhances insulin secretion throughout the oral glucose tolerance test: central plus peripheral nervous system mechanisms. Diabetes Metab. Syndr. Obes. 2009, 2:203-213.
92. Paoletti P., et al. NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat. Rev. Neurosci. 2013, 14:383-400.
93. + channels. Neuron 2001, 31:1027-1034.
94. Lai T.W., et al. Excitotoxicity and stroke: identifying novel targets for neuroprotection. Prog. Neurobiol. 2014, 115:157-188.
95. Pinheiro P.S., Mulle C. Presynaptic glutamate receptors: physiological functions and mechanisms of action. Nat. Rev. Neurosci. 2008, 9:423-436.
96. Sihra T.S., Rodriguez-Moreno A. Presynaptic kainate receptor-mediated bidirectional modulatory actions: mechanisms. Neurochem. Int. 2013, 62:982-987.
97. Lebrun-Julien F., et al. Excitotoxic death of retinal neurons in vivo occurs via a non-cell-autonomous mechanism. J. Neurosci. 2009, 29:5536-5545.
98. 3H]MK-801 in heterologously expressed NMDA receptors. Neuropharmacology 2005, 49:1-16.
99. Nelson K.A., et al. High-dose oral dextromethorphan versus placebo in painful diabetic neuropathy and postherpetic neuralgia. Neurology 1997, 48:1212-1218.
100. Liu S.L., et al. Dextromethorphan reduces oxidative stress and inhibits atherosclerosis and neointima formation in mice. Cardiovasc. Res. 2009, 82:161-169.