GLP-1 and exendin-4 transiently enhance gabaa receptor-mediated synaptic and tonic currents in rat hippocampal ca3 pyramidal neurons

Diabetes

Volumn 64, Issue 1, 2015, Pages 79-89

  Korol, Sergiy V ^a   Jin, Zhe ^a   Babateen, Omar ^a   Birnir, Bryndis ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; EXENDIN 4; GLUCAGON LIKE PEPTIDE 1; NEUROTRANSMITTER; TETRODOTOXIN; 4 AMINOBUTYRIC ACID; GLUCAGON RECEPTOR; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; PEPTIDE; SODIUM CHANNEL BLOCKING AGENT; VENOM;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; HIPPOCAMPAL CA3 REGION; NERVE EXCITABILITY; NONHUMAN; POSTSYNAPTIC INHIBITION; PYRAMIDAL NERVE CELL; RAT; SIGNAL TRANSDUCTION; SYNAPTIC POTENTIAL; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; CYTOLOGY; DRUG EFFECTS; INHIBITORY POSTSYNAPTIC POTENTIAL; MEMBRANE POTENTIAL; MEMORY; METABOLISM; ORGAN CULTURE TECHNIQUE; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; SYNAPTIC TRANSMISSION; WISTAR RAT;

ANIMALS; CA3 REGION, HIPPOCAMPAL; GAMMA-AMINOBUTYRIC ACID; GLUCAGON-LIKE PEPTIDE 1; INHIBITORY POSTSYNAPTIC POTENTIALS; MEMBRANE POTENTIALS; MEMORY; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PEPTIDES; PYRAMIDAL CELLS; RATS, WISTAR; RECEPTORS, GABA-A; RECEPTORS, GLUCAGON; SIGNAL TRANSDUCTION; SODIUM CHANNEL BLOCKERS; SYNAPTIC TRANSMISSION; TETRODOTOXIN; VENOMS;

EID: 84920059626     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0668     Document Type: Article

References (51)

1. Roberts RO, Knopman DS, Przybelski SA, et al. Association of type 2 diabetes with brain atrophy and cognitive impairment. Neurology 2014;82:1132-1141
2. Tuligenga RH, Dugravot A, Tabák AG, et al. Midlife type 2 diabetes and poor glycaemic control as risk factors for cognitive decline in early old age: A post-hoc analysis of the Whitehall II cohort study. Lancet Diabetes Endocrinol 2014;2:228-235
3. Marder TJ, Flores VL, Bolo NR, et al. Task-induced brain activity patterns in type 2 diabetes: A potential biomarker for cognitive decline. Diabetes. 4 April 2014 [Epub ahead of print]
4. Zhou X, Zhang J, Chen Y, et al. Aggravated cognitive and brain functional impairment in mild cognitive impairment patients with type 2 diabetes: A restingstate functional MRI study. J Alzheimers Dis 2014;41:925-935
5. Qiu C, Sigurdsson S, Zhang Q, et al. Diabetes, markers of brain pathology and cognitive function: The Age, Gene/Environment Susceptibility-Reykjavik Study. Ann Neurol 2014;75:138-146
6. Patrone C, Eriksson O, Lindholm D. Diabetes drugs and neurological disorders: new views and therapeutic possibilities. Lancet Diabetes Endocrinol 2014;2:256-262
7. Duarte AI, Candeias E, Correia SC, et al. Crosstalk between diabetes and brain: glucagon-like peptide-1 mimetics as a promising therapy against neurodegeneration. Biochim Biophys Acta 2013;1832:527-541
8. Biessels GJ, Strachan MW, Visseren FL, Kappelle LJ, Whitmer RA. Dementia and cognitive decline in type 2 diabetes and prediabetic stages: Towards targeted interventions. Lancet Diabetes Endocrinol 2014;2:246-255
9. Deuker L, Doeller CF, Fell J, Axmacher N. Human neuroimaging studies on the hippocampal CA3 region - integrating evidence for pattern separation and completion. Front Cell Neurosci 2014;8:64
10. Lathe R. Hormones and the hippocampus. J Endocrinol 2001;169:205-231
11. Risold PY, Swanson LW. Structural evidence for functional domains in the rat hippocampus. Science 1996;272:1484-1486
12. Davidson TL, Kanoski SE, Schier LA, Clegg DJ, Benoit SC. A potential role for the hippocampus in energy intake and body weight regulation. Curr Opin Pharmacol 2007;7:613-616
13. Holst JJ. The physiology of glucagon-like peptide Physiol Rev 2007;87: 1409-1439
14. Orci L, Pictet R, Forssmann WG, Renold AE, Rouiller C. Structural evidence for glucagon producing cells in the intestinal mucosa of the rat. Diabetologia 1968;4:56-67
15. Jin SL, Han VK, Simmons JG, Towle AC, Lauder JM, Lund PK. Distribution of glucagonlike peptide I (GLP-I), glucagon, and glicentin in the rat brain: An immunocytochemical study. J Comp Neurol 1988;271:519-532
16. Merchenthaler I, Lane M, Shughrue P. Distribution of pre-pro-glucagon and glucagon-like peptide-1 receptor messenger RNAs in the rat central nervous system. J Comp Neurol 1999;403:261-280
17. Hamilton A, Hölscher C. Receptors for the incretin glucagon-like peptide-1 are expressed on neurons in the central nervous system. Neuroreport 2009;20: 1161-1166
18. Mojsov S, Heinrich G, Wilson IB, Ravazzola M, Orci L, Habener JF. Preproglucagon gene expression in pancreas and intestine diversifies at the level of post-translational processing. J Biol Chem 1986;261:11880-11889
19. Vilsbøll T, Agersø H, Krarup T, Holst JJ. Similar elimination rates of glucagon-like peptide-1 in obese type 2 diabetic patients and healthy subjects. J Clin Endocrinol Metab 2003;88:220-224
20. Widmann C, Dolci W, Thorens B. Agonist-induced internalization and recycling of the glucagon-like peptide-1 receptor in transfected fibroblasts and in insulinomas. Biochem J 1995;310:203-214
21. Widmann C, Dolci W, Thorens B. Desensitization and phosphorylation of the glucagon-like peptide-1 (GLP-1) receptor by GLP-1 and 4-phorbol 12-myristate 13-Acetate. Mol Endocrinol 1996;10:62-75
22. Widmann C, Dolci W, Thorens B. Internalization and homologous desensitization of the GLP-1 receptor depend on phosphorylation of the receptor carboxyl tail at the same three sites. Mol Endocrinol 1997;11:1094-1102
23. Roed SN, Wismann P, Underwood CR, et al. Real-time trafficking and signaling of the glucagon-like peptide-1 receptor. Mol Cell Endocrinol 2014;382: 938-949
24. Richards P, Parker HE, Adriaenssens AE, et al. Identification and characterization of GLP-1 receptor-expressing cells using a new transgenic mouse model. Diabetes 2014;63:1224-1233
25. Isacson R, Nielsen E, Dannaeus K, et al. The glucagon-like peptide 1 receptor agonist exendin-4 improves reference memory performance and decreases immobility in the forced swim test. Eur J Pharmacol 2011;650:249-255
26. Tang-Christensen M, Vrang N, Larsen PJ. Glucagon-like peptide 1(7-36) amide's central inhibition of feeding and peripheral inhibition of drinking are abolished by neonatal monosodium glutamate treatment. Diabetes 1998;47:530-537
27. During MJ, Cao L, Zuzga DS, et al. Glucagon-like peptide-1 receptor is involved in learning and neuroprotection. Nat Med 2003;9:1173-1179
28. Campbell JE, Drucker DJ. Pharmacology, physiology, and mechanisms of incretin hormone action. Cell Metab 2013;17:819-837
29. Ma T, Du X, Pick JE, Sui G, Brownlee M, Klann E. Glucagon-like peptide-1 cleavage product GLP-1(9-36) amide rescues synaptic plasticity and memory deficits in Alzheimer's disease model mice. J Neurosci 2012;32:13701-13708
30. Oka JI, Goto N, Kameyama T. Glucagon-like peptide-1 modulates neuronal activity in the rat's hippocampus. Neuroreport 1999;10:1643-1646
31. Porter D, Faivre E, Flatt PR, Hölscher C, Gault VA. Actions of incretin metabolites on locomotor activity, cognitive function and in vivo hippocampal synaptic plasticity in high fat fed mice. Peptides 2012;35:1-8
32. Iwai T, Suzuki M, Kobayashi K, Mori K, Mogi Y, Oka J. The influences of juvenile diabetes on memory and hippocampal plasticity in rats: improving effects of glucagon-like peptide-1. Neurosci Res 2009;64:67-74
33. Semyanov A, Walker MC, Kullmann DM, Silver RA. Tonically active GABA A receptors: modulating gain and maintaining the tone. Trends Neurosci 2004;27: 262-269
34. Palovcik RA, Phillips MI, Kappy MS, Raizada MK. Insulin inhibits pyramidal neurons in hippocampal slices. Brain Res 1984;309:187-191
35. Wan Q, Xiong ZG, Man HY, et al. Recruitment of functional GABA(A) receptors to postsynaptic domains by insulin. Nature 1997;388:686-690
36. Jin Z, Jin Y, Kumar-Mendu S, Degerman E, Groop L, Birnir B. Insulin reduces neuronal excitability by turning on GABA(A) channels that generate tonic current. PLoS ONE 2011;6:e16188
37. Birnir B, Everitt AB, Gage PW. Characteristics of GABAA channels in rat dentate gyrus. J Membr Biol 1994;142:93-102
38. Bai D, Zhu G, Pennefather P, Jackson MF, MacDonald JF, Orser BA. Distinct functional and pharmacological properties of tonic and quantal inhibitory postsynaptic currents mediated by gamma-Aminobutyric acid(A) receptors in hippocampal neurons. Mol Pharmacol 2001;59:814-824
39. Farrant M, Nusser Z. Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 2005;6:215-229
40. Rossi DJ, Hamann M, Attwell D. Multiple modes of GABAergic inhibition of rat cerebellar granule cells. J Physiol 2003;548:97-110
41. Richerson GB, Wu Y. Dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J Neurophysiol 2003;90:1363-1374
42. Kozlov AS, Angulo MC, Audinat E, Charpak S. Target cell-specific modulation of neuronal activity by astrocytes. Proc Natl Acad Sci U S A 2006;103:10058-10063
43. Amaral DG, Witter MP. The three-dimensional organization of the hippocampal formation: A review of anatomical data. Neuroscience 1989;31:571-591
44. Benedict C, Hallschmid M, Schultes B, Born J, Kern W. Intranasal insulin to improve memory function in humans. Neuroendocrinology 2007;86:136-142
45. Tschritter O, Hennige AM, Preissl H, et al. Cerebrocortical beta activity in overweight humans responds to insulin detemir. PLoS ONE 2007;2:e1196
46. Rönnemaa E, Zethelius B, Sundelöf J, et al. Impaired insulin secretion increases the risk of Alzheimer disease. Neurology 2008;71:1065-1071
47. McClean PL, Gault VA, Harriott P, Hölscher C. Glucagon-like peptide-1 analogues enhance synaptic plasticity in the brain: A link between diabetes and Alzheimer's disease. Eur J Pharmacol 2010;630:158-162
48. Gilman CP, Perry T, Furukawa K, Grieg NH, Egan JM, Mattson MP. Glucagon-like peptide 1 modulates calcium responses to glutamate and membrane depolarization in hippocampal neurons. J Neurochem 2003;87:1137-1144
49. Abbas T, Faivre E, Hölscher C. Impairment of synaptic plasticity and memory formation in GLP-1 receptor KO mice: Interaction between type 2 diabetes and Alzheimer's disease. Behav Brain Res 2009;205:265-271
50. Luttrell LM, Lefkowitz RJ. The role of beta-Arrestins in the termination and transduction of G-protein-coupled receptor signals. J Cell Sci 2002;115:455-465
51. McClean PL, Holscher C. Liraglutide can reverse memory impairment, synaptic loss and reduce plaque load in aged APP/PS1 mice, a model of Alzheimer's disease. Neuropharmacology 2014;76:57-67