Characterization of pancreatic NMDA receptors as possible drug targets for diabetes treatment

Nature Medicine

Volumn 21, Issue 4, 2015, Pages 363-376

  Marquard, Jan ^a,b   Otter, Silke ^a,c   Welters, Alena ^a,b,c   Stirban, Alin ^d   Fischer, Annelie ^d   Eglinger, Jan ^a,c   Herebian, Diran ^b   Kletke, Olaf ^b   Klemen, Maša Skelin ^e   Stožer, Andraž ^e   Wnendt, Stephan ^f   Piemonti, Lorenzo ^g   Köhler, Martin ^h   Ferrer, Jorge ^i,j   Thorens, Bernard ^k   Schliess, Freimut ^d   Rupnik, Marjan Slak ^e,l   Heise, Tim ^d   Berggren, Per Olof ^h   Klöcker, Nikolaj ^b   Meissner, Thomas ^b   Mayatepek, Ertan ^b   Eberhard, Daniel ^a   Kragl, Martin ^a,c   Lammert, Eckhard ^a,c   more..

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

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

^d Profil Institute for Metabolic Research   (Germany)

^e UNIVERSITY OF MARIBOR   (Slovenia)

^f MLM Medical Labs GmbH   (Germany)

^g SAN RAFFAELE HOSPITAL   (Italy)

^h KAROLINSKA INSTITUTE   (Sweden)

ⁱ IMPERIAL COLLEGE LONDON   (United Kingdom)

^j ALBA SYNCHROTRON LIGHT SOURCE   (Spain)

^k UNIVERSITY OF LAUSANNE   (Switzerland)

^l MEDICAL UNIVERSITY OF VIENNA   (Austria)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; DEXTROMETHORPHAN; EXENDIN 4; GLUCOSE; GPRIN1 PROTEIN, MOUSE; INSULIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NERVE PROTEIN; PEPTIDE; VENOM;

ADULT; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL LINE; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DIABETES MELLITUS, TYPE 2; DISEASE MODEL; DRUG DESIGN; FEMALE; GENETICS; GLUCOSE TOLERANCE TEST; HUMAN; KNOCKOUT MOUSE; MALE; METABOLISM; MIDDLE AGED; MOUSE; PANCREAS; PANCREAS ISLET; PANCREAS ISLET BETA CELL;

ADULT; ANIMALS; CALCIUM; CELL LINE; CELL SURVIVAL; DEXTROMETHORPHAN; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; DRUG DESIGN; FEMALE; GLUCOSE; GLUCOSE TOLERANCE TEST; HUMANS; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; NERVE TISSUE PROTEINS; PANCREAS; PEPTIDES; RECEPTORS, N-METHYL-D-ASPARTATE; VENOMS;

EID: 84926685729     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3822     Document Type: Article

References (70)

1. Polonsky, K.S. The past 200 years in diabetes. N. Engl. J. Med. 367, 1332-1340 (2012).
2. Kahn, S.E., Hull, R.L. & Utzschneider, K.M. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444, 840-846 (2006).
3. Cavaghan, M.K., Ehrmann, D.A. & Polonsky, K.S. Interactions between insulin resistance and insulin secretion in the development of glucose intolerance. J. Clin. Invest. 106, 329-333 (2000).
4. Ferrannini, E. The stunned beta cell: a brief history. Cell Metab. 11, 349-352 (2010).
5. Rorsman, P. & Braun, M. Regulation of insulin secretion in human pancreatic islets. Annu. Rev. Physiol. 75, 155-179 (2013).
6. Talchai, C., Xuan, S., Lin, H.V., Sussel, L. & Accili, D. Pancreatic beta cell dedifferentiation as a mechanism of diabetic beta cell failure. Cell 150, 1223-1234 (2012).
7. Tahrani, A.A., Bailey, C.J., Del Prato, S. & Barnett, A.H. Management of type 2 diabetes: new and future developments in treatment. Lancet 378, 182-197 (2011).
8. DeFronzo, R.A. Overview of newer agents: where treatment is going. Am. J. Med. 123, S38-S48 (2010).
9. Amiel, S.A., Dixon, T., Mann, R. & Jameson, K. Hypoglycaemia in type 2 diabetes. Diabet. Med. 25, 245-254 (2008).
10. Cryer, P.E. Mechanisms of hypoglycemia-associated autonomic failure in diabetes. N. Engl. J. Med. 369, 362-372 (2013).
11. Kahn, S.E., Cooper, M.E. & Del Prato, S. Pathophysiology and treatment of type 2 diabetes: perspectives on the past, present, and future. Lancet 383, 1068-1083 (2014).
12. Retnakaran, R., Kramer, C.K., Choi, H., Swaminathan, B. & Zinman, B. Liraglutide and the preservation of pancreatic beta-cell function in early type 2 diabetes: the LIBRA trial. Diabetes Care 37, 3270-3278 (2014).
13. Jain, R. et al. Pharmacological inhibition of Eph receptors enhances glucose-stimulated insulin secretion from mouse and human pancreatic islets. Diabetologia 56, 1350-1355 (2013).
14. Burris, R.E. & Hebrok, M. Pancreatic innervation in mouse development and beta-cell regeneration. Neuroscience 150, 592-602 (2007).
15. Rodriguez-Diaz, R. & Caicedo, A. Novel approaches to studying the role of innervation in the biology of pancreatic islets. Endocrinol. Metab. Clin. North Am. 42, 39-56 (2013).
16. Soltani, N. et al. GABA exerts protective and regenerative effects on islet beta cells and reverses diabetes. Proc. Natl. Acad. Sci. USA 108, 11692-11697 (2011).
17. Rodriguez-Diaz, R. et al. Real-time detection of acetylcholine release from the human endocrine pancreas. Nat. Protoc. 7, 1015-1023 (2012).
18. Maechler, P. & Wollheim, C.B. Mitochondrial glutamate acts as a messenger in glucose-induced insulin exocytosis. Nature 402, 685-689 (1999).
19. Cabrera, O. et al. Glutamate is a positive autocrine signal for glucagon release. Cell Metab. 7, 545-554 (2008).
20. 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. 286, 14007-14018 (2011).
21. Feldmann, N. et al. Reduction of plasma membrane glutamate transport potentiates insulin but not glucagon secretion in pancreatic islet cells. Mol. Cell. Endocrinol. 338, 46-57 (2011).
22. Inagaki, N. et al. Expression and role of ionotropic glutamate receptors in pancreatic islet cells. FASEB 9, 686-691 (1995).
23. Garnock-Jones, K.P. Dextromethorphan/quinidine: in pseudobulbar affect. CNS Drugs 25, 435-445 (2011).
24. Hamosh, A., Maher, J.F., Bellus, G.A., Rasmussen, S.A. & Johnston, M.V. Long-term use of high-dose benzoate and dextromethorphan for the treatment of nonketotic hyperglycinemia. J. Pediatr. 132, 709-713 (1998).
25. Nelson, K.A., Park, K.M., Robinovitz, E., Tsigos, C. & Max, M.B. High-dose oral dextromethorphan versus placebo in painful diabetic neuropathy and postherpetic neuralgia. Neurology 48, 1212-1218 (1997).
26. Pechnick, R.N. & Poland, R.E. Comparison of the effects of dextromethorphan, dextrorphan, and levorphanol on the hypothalamo-pituitary-adrenal axis. J. Pharmacol. Exp. Ther. 309, 515-522 (2004).
27. Yashiro, K. & Philpot, B.D. Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology 55, 1081-1094 (2008).
28. Lee, C.H. et al. NMDA receptor structures reveal subunit arrangement and pore architecture. Nature 511, 191-197 (2014).
29. Kalia, L.V., Kalia, S.K. & Salter, M.W. NMDA receptors in clinical neurology: excitatory times ahead. Lancet Neurol. 7, 742-755 (2008).
30. Ngo-Anh, T.J. et al. SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines. Nat. Neurosci. 8, 642-649 (2005).
31. Isaacson, J.S. & Murphy, G.J. Glutamate-mediated extrasynaptic inhibition: direct coupling of NMDA receptors to Ca(2+)-activated K+ channels. Neuron 31, 1027-1034 (2001).
32. Hardingham, G.E. & Bading, H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 11, 682-696 (2010).
33. Bartlett, T.E. & Wang, Y.T. The intersections of NMDAR-dependent synaptic plasticity and cell survival. Neuropharmacology 74, 59-68 (2013).
34. Rodríguez-Moreno, A., Banerjee, A. & Paulsen, O. Presynaptic NMDA receptors and spike timing-dependent depression at cortical synapses. Front. Synaptic Neurosci. 2, 18 (2010).
35. Gonoi, T. et al. Functional neuronal ionotropic glutamate receptors are expressed in the non-neuronal cell line MIN6. J. Biol. Chem. 269, 16989-16992 (1994).
36. Molnár, E., Varadi, A., McIlhinney, R.A. & Ashcroft, S.J. Identification of functional ionotropic glutamate receptor proteins in pancreatic beta-cells and in islets of Langerhans. FEBS Lett. 371, 253-257 (1995).
37. Garrino, M.G. & Henquin, J.C. Adamantane derivatives: a new class of insulin secretagogues. Br. J. Pharmacol. 90, 583-591 (1987).
38. Konrad, D., Sobetzko, D., Schmitt, B. & Schoenle, E.J. Insulin-dependent diabetes mellitus induced by the antitussive agent dextromethorphan. Diabetologia 43, 261-262 (2000).
39. 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. 2, 203-213 (2009).
40. Ashcroft, F.M., Kerr, A.J., Gibson, J.S. & Williams, B.A. Amantadine and sparteine inhibit ATP-regulated K-currents in the insulin-secreting beta-cell line, HIT-T15. Br. J. Pharmacol. 104, 579-584 (1991).
41. Wong, E.H.F. et al. The anticonvulsant Mk-801 is a potent N-methyl-D-aspartate Antagonist. Proc. Natl. Acad. Sci. USA 83, 7104-7108 (1986).
42. Li, L. & Hanahan, D. Hijacking the neuronal NMDAR signaling circuit to promote tumor growth and invasion. Cell 153, 86-100 (2013).
43. Olney, J.W., Labruyere, J. & Price, M.T. Pathological changes induced in cerebrocortical neurons by phencyclidine and related drugs. Science 244, 1360-1362 (1989).
44. Gheni, G. et al. Glutamate acts as a key signal linking glucose metabolism to incretin/cAMP action to amplify insulin secretion. Cell Reports 9, 661-673 (2014).
45. Speier, S. & Rupnik, M. A novel approach to in situ characterization of pancreatic beta-cells. Pflugers Arch. 446, 553-558 (2003).
46. Miki, T. et al. Defective insulin secretion and enhanced insulin action in KATP channel-deficient mice. Proc. Natl. Acad. Sci. USA 95, 10402-10406 (1998).
47. Begenisich, T. et al. Physiological roles of the intermediate conductance, Ca2+-activated potassium channel Kcnn4. J. Biol. Chem. 279, 47681-47687 (2004).
48. Düfer, M. et al. Enhanced glucose tolerance by SK4 channel inhibition in pancreatic beta-cells. Diabetes 58, 1835-1843 (2009).
49. Gilon, P., Shepherd, R.M. & Henquin, J.C. Oscillations of secretion driven by oscillations of cytoplasmic Ca2+ as evidences in single pancreatic islets. J. Biol. Chem. 268, 22265-22268 (1993).
50. Bergsten, P., Grapengiesser, E., Gylfe, E., Tengholm, A. & Hellman, B. Synchronous oscillations of cytoplasmic Ca2+ and insulin release in glucose-stimulated pancreatic islets. J. Biol. Chem. 269, 8749-8753 (1994).
51. Bardy, G. et al. Quercetin induces insulin secretion by direct activation of L-type calcium channels in pancreatic beta cells. Br. J. Pharmacol. 169, 1102-1113 (2013).
52. Dadi, P.K. et al. Inhibition of pancreatic beta-cell Ca2+/calmodulin-dependent protein kinase II reduces glucose-stimulated calcium influx and insulin secretion, impairing glucose tolerance. J. Biol. Chem. 289, 12435-12445 (2014).
53. Dixit, S.S. et al. Effects of CaMKII-mediated phosphorylation of ryanodine receptor type 2 on islet calcium handling, insulin secretion, and glucose tolerance. PLoS ONE 8, e58655 (2013).
54. Maurice, T., Urani, A., Phan, V.L. & Romieu, P. The interaction between neuroactive steroids and the sigma1 receptor function: behavioral consequences and therapeutic opportunities. Brain Res. Brain Res. Rev. 37, 116-132 (2001).
55. 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 368, 1696-1705 (2006).
56. Coleman, D.L. & Hummel, K.P. Studies with the mutation, diabetes, in the mouse. Diabetologia 3, 238-248 (1967).
57. Donath, M.Y. Targeting inflammation in the treatment of type 2 diabetes: time to start. Nat. Rev. Drug Discov. 13, 465-476 (2014).
58. Ashcroft, F.M. & Rorsman, P. Electrophysiology of the pancreatic beta-cell. Prog. Biophys. Mol. Biol. 54, 87-143 (1989).
59. Shen, K.Z. & Johnson, S.W. Ca2+ influx through NMDA-gated channels activates ATP-sensitive K+ currents through a nitric oxide-cGMP pathway in subthalamic neurons. J. Neurosci. 30, 1882-1893 (2010).
60. Schiemann, J. et al. K-ATP channels in dopamine substantia nigra neurons control bursting and novelty-induced exploration. Nat. Neurosci. 15, 1272-1280 (2012).
61. Gu, G., Dubauskaite, J. & Melton, D.A. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 129, 2447-2457 (2002).
62. Thorens, B. et al. Ins1Cre knock-in mice for beta cell-specific gene recombination. Diabetologia 58, 558-565 (2015).
63. Yesil, P. et al. A new collagenase blend increases the number of islets isolated from mouse pancreas. Islets 1, 185-190 (2009).
64. Janjic, D. et al. Free radical modulation of insulin release in INS-1 cells exposed to alloxan. Biochem. Pharmacol. 57, 639-648 (1999).
65. Kopec, C.D., Li, B., Wei, W., Boehm, J. & Malinow, R. Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J. Neurosci. 26, 2000-2009 (2006).
66. Silva, J.P. et al. Impaired insulin secretion and beta-cell loss in tissue-specific knockout mice with mitochondrial diabetes. Nat. Genet. 26, 336-340 (2000).
67. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).
68. Berggren, P.O. et al. Removal of Ca2+ channel beta3 subunit enhances Ca2+ oscillation frequency and insulin exocytosis. Cell 119, 273-284 (2004).
69. Stožer, A., Dolensek, J. & Rupnik, M.S. Glucose-stimulated calcium dynamics in islets of Langerhans in acute mouse pancreas tissue slices. PLoS ONE 8, e54638 (2013).
70. Loos, W.J. et al. Simultaneous quantification of dextromethorphan and its metabolites dextrorphan, 3-methoxymorphinan and 3-hydroxymorphinan in human plasma by ultra performance liquid chromatography/tandem triple-quadrupole mass spectrometry. J. Pharm. Biomed. Anal. 54, 387-394 (2011).