Glucose attenuates impairments in memory and CREB activation produced by an α4β2 but not an α7 nicotinic receptor antagonist

Neuropharmacology

Volumn 67, Issue , 2013, Pages 233-242

  Morris, Ken A ^a   Li, Sisi ^b   Bui, Duat D ^b   Gold, Paul E ^c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c SYRACUSE UNIVERSITY   (United States)

Author keywords

4 2 receptor; 7 receptor; Acetylcholine; Glucose; Memory; Nicotinic

Indexed keywords

BUNGAROTOXIN RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DIHYDRO BETA ERYTHROIDINE; GLUCOSE; METHYLLYCACONITINE; NICOTINIC RECEPTOR ALPHA4BETA2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DISEASE ASSOCIATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LATENT PERIOD; MALE; MEMORY DISORDER; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; TASK PERFORMANCE; WORKING MEMORY;

ANIMALS; CREB-BINDING PROTEIN; GLUCOSE; MALE; MEMORY DISORDERS; NICOTINIC ANTAGONISTS; ORGAN CULTURE TECHNIQUES; RATS; RATS, INBRED F344; RECEPTORS, NICOTINIC;

EID: 84872420164     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.11.008     Document Type: Article

References (85)

1. N.A. Addy, A. Nakijama, and E.D. Levin Nicotinic mechanisms of memory: effects of acute local DHbetaE and MLA infusions in the basolateral amygdala Brain Res. Cogn. Brain Res. 16 2003 51 57
2. C.M. Alberini Transcription factors in long-term memory and synaptic plasticity Physiol. Rev. 89 2009 121 145
3. M. Alkondon, E.F. Pereira, W.S. Cortes, A. Maelicke, and E.X. Albuquerque Choline is a selective agonist of alpha7 nicotinic acetylcholine receptors in the rat brain neurons Eur. J. Neurosci. 9 1997 2734 2742
4. E. Benito, and A. Barco CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models Trends Neurosci. 33 2010 230 240
5. J.H. Bettany, and E.D. Levin Ventral hippocampal alpha 7 nicotinic receptor blockade and chronic nicotine effects on memory performance in the radial-arm maze Pharmacol. Biochem. Behav. 70 2001 467 474
6. J.G. Blanchard, and P.M. Duncan Effect of combinations of insulin, glucose and scopolamine on radial arm maze performance Pharmacol. Biochem. Behav. 58 1997 209 214
7. R. Cannady, R. Weir, B. Wee, E. Gotschlich, N. Kolia, E. Lau, J. Brotherton, and E.D. Levin Nicotinic antagonist effects in the mediodorsal thalamic nucleus: regional heterogeneity of nicotinic receptor involvement in cognitive function Biochem. Pharmacol. 78 2009 788 794
8. W.A. Carlezon Jr., R.S. Duman, and E.J. Nestler The many faces of CREB Trends Neurosci. 28 2005 436 445
9. N.G. Castro, and E.X. Albuquerque alpha-bungarotoxin-sensitive hippocampal nicotinic receptor channel has a high calcium permeability Biophys. J. 68 1995 516 524
10. W.K. Chan, P.T. Wong, and F.S. Sheu Frontal cortical alpha7 and alpha4beta2 nicotinic acetylcholine receptors in working and reference memory Neuropharmacology 52 2007 1641 1649
11. K.T. Chang, and D.K. Berg Voltage-gated channels block nicotinic regulation of CREB phosphorylation and gene expression in neurons Neuron 32 2001 855 865
12. L. Chiappetta, and M.E. Jarvik Comparison of learning impairment and activity depression produced by two classes of cholinergic blocking agents Arch. Int. Pharmacodyn. Ther. 179 1969 161 166
13. S.L. Cincotta, M.S. Yorek, T.M. Moschak, S.R. Lewis, and J.S. Rodefer Selective nicotinic acetylcholine receptor agonists: potential therapies for neuropsychiatric disorders with cognitive dysfunction Curr. Opin. Investig. Drugs 9 2008 47 56
14. P.K. Dash, S.A. Orsi, and A.N. Moore Spatial memory formation and memory-enhancing effect of glucose involves activation of the tuberous sclerosis complex-mammalian target of rapamycin pathway J. Neurosci. 26 2006 8048 8056
15. J.A. Davis, and T.J. Gould The effects of DHBE and MLA on nicotine-induced enhancement of contextual fear conditioning in C57BL/6 mice Psychopharmacology 184 2006 345 352
16. J.A. Davis, and T.J. Gould beta2 subunit-containing nicotinic receptors mediate the enhancing effect of nicotine on trace cued fear conditioning in C57BL/6 mice Psychopharmacology 190 2007 343 352
17. J.A. Davis, J.W. Kenney, and T.J. Gould Hippocampal alpha4beta2 nicotinic acetylcholine receptor involvement in the enhancing effect of acute nicotine on contextual fear conditioning J. Neurosci. 27 2007 10870 10877
18. R. Fabian-Fine, P. Skehel, M.L. Errington, H.A. Davies, E. Sher, M.G. Stewart, and A. Fine Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus J. Neurosci. 21 2001 7993 8003
19. S.D. Glick, and S. Greenstein Differential effects of scopolamine and mecamylamine on passive avoidance behavior Life Sci. I 11 1972 169 179
20. P.E. Gold, and D.L. Korol Hormones and memory G. Koob, M. Le Moal, R.F. Thompson, Encyclopedia of Behavioral Neuroscience vol. 2 2010 Academic Press Oxford 57 64
21. P.E. Gold Coordination of multiple memory systems Neurobiol. Learn. Mem. 80 2004 194 210
22. P.E. Gold Glucose and age-related changes in memory Neurobiol. Aging 26 Suppl. 1 2005 60 64
23. P.E. Gold Memory enhancing drugs H. Eichenbaum, Memory Systems J. Byrne, Learning and Memory: a Comprehensive Reference vol. 3 2008 Elsevier Science Oxford 555 576
24. M.E. Goldberg, K. Sledge, M. Hefner, and R.C. Robichaud Learning impairment after three classes of agents which modify cholinergic function Arch. Int. Pharmacodyn. Ther. 193 1971 226 235
25. C. Gotti, and F. Clementi Neuronal nicotinic receptors: from structure to pathology Prog. Neurobiol. 74 2004 363 396
26. S. Graef, P. Schönknecht, O. Sabri, and U. Hegerl Cholinergic receptor subtypes and their role in cognition, emotion, and vigilance control: an overview of preclinical and clinical findings Psychopharmacology (Berl.) 215 2011 205 229
27. B. Hahn, M. Shoaib, and I.P. Stolerman Selective nicotinic receptor antagonists: effects on attention and nicotine-induced attentional enhancement Psychopharmacology (Berl.) 217 2011 75 82
28. M. Hu, Q.S. Liu, K.T. Chang, and D.K. Berg Nicotinic regulation of CREB activation in hippocampal neurons by glutamatergic and nonglutamatergic pathways Mol. Cell. Neurosci. 21 2002 616 625
29. M.R. Jafari, M.R. Zarrindast, and B. Djahanguiri Effects of different doses of glucose and insulin on morphine state-dependent memory of passive avoidance in mice Psychopharmacology (Berl.) 175 2004 457 462
30. H. Kawai, W. Zago, and D.K. Berg Nicotinic alpha 7 receptor clusters on hippocampal GABAergic neurons: regulation by synaptic activity and neurotrophins J. Neurosci. 22 2002 7903 7912
31. J.W. Kenney, and T.J. Gould Modulation of hippocampus-dependent learning and synaptic plasticity by nicotine Mol. Neurobiol. 38 2008 101 121
32. J.W. Kenney, J.D. Raybuck, and T.J. Gould Nicotinic receptors in the dorsal and ventral hippocampus differentially modulate contextual fear conditioning Hippocampus 22 2012 1681 1690
33. S.R. Kopf, and C.M. Baratti Memory-improving actions of glucose: involvement of a central cholinergic muscarinic mechanism Behav. Neural Biol. 62 1994 237 243
34. S.R. Kopf, M.L. Buchholzer, M. Hilgert, K. Loffelholz, and J. Klein Glucose plus choline improve passive avoidance behaviour and increase hippocampal acetylcholine release in mice Neuroscience 103 2001 365 371
35. D.L. Korol, and P.E. Gold Glucose, memory, and aging Am. J. Clin. Nutr. 67 1998 764S 771S
36. D.L. Korol, and P.E. Gold Modulation of learning and memory by adrenal and ovarian hormones R.P. Kesner, J.L. Martinez, Neurobiology of Learning and Memory 2007 Elsevier Science New York 243 268
37. D.L. Krebs, and M.B. Parent The enhancing effects of hippocampal infusions of glucose are not restricted to spatial working memory Neurobiol. Learn. Mem. 83 2005 168 172
38. D.L. Krebs-Kraft, and M.B. Parent Hippocampal infusions of glucose reverse memory deficits produced by co-infusions of a GABA receptor agonist Neurobiol. Learn. Mem. 89 2008 142 152
39. E.D. Levin, A. Bradley, N. Addy, and N. Sigurani Hippocampal alpha 7 and alpha 4 beta 2 nicotinic receptors and working memory Neuroscience 109 2002 757 765
40. E.D. Levin, F.J. McClernon, and A.H. Rezvani Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization Psychopharmacology (Berl.) 184 2006 523 539
41. E.C. McNay, and P.E. Gold Extracellular glucose concentrations in the rat hippocampus measured by zero-net-flux: effects of microdialysis flow rate, strain, and age J. Neurochem. 72 1999 785 790
42. E.C. McNay, and P.E. Gold Age-related differences in hippocampal extracellular fluid glucose concentration during behavioral testing and following systemic glucose administration J. Gerontol. A Biol. Sci. Med. Sci. 56 2001 B66 B71
43. C. Messier, T. Durkin, O. Mrabet, and C. Destrade Memory-improving action of glucose: indirect evidence for a facilitation of hippocampal acetylcholine synthesis Behav. Brain Res. 39 1990 135 143
44. C. Messier Glucose improvement of memory: a review Eur. J. Pharmacol. 19 2004 33 57
45. J. Micheau, C. Messier, and R. Jaffard Glucose enhancement of scopolamine-induced increase of hippocampal high-affinity choline uptake in mice: relation to plasma glucose levels Brain Res. 685 1995 99 104
46. A. Mike, N.G. Castro, and E.X. Albuquerque Choline and acetylcholine have similar kinetic properties of activation and desensitization on the alpha7 nicotinic receptors in rat hippocampal neurons Brain Res. 882 2000 155 168
47. K.A. Morris, and P.E. Gold Age-related impairments in memory and in CREB and pCREB expression in hippocampus and amygdala following inhibitory avoidance training Mech. Ageing Dev. 133 2012 291 299
48. Morris, K.A., Gold, P.E. Epinephrine and glucose modulate training-related CREB phosphorylation in old rats: relationships to age-related memory impairments. Exp. Gerontol., in press.
49. K.A. Morris, Q. Chang, E.G. Mohler, and P.E. Gold Age-related memory impairments due to reduced blood glucose responses to epinephrine Neurobiol. Aging 31 2010 2136 2145
50. H. Nakayama, T. Numakawa, T. Ikeuchi, and H. Hatanaka Nicotine-induced phosphorylation of extracellular signal-regulated protein kinase and CREB in PC12h cells J. Neurochem. 79 2001 489 498
51. L.A. Newman, D.L. Korol, and P.E. Gold Lactate produced by glycogenolysis in astrocytes regulates memory processing PLoS One 6 2011 e28427
52. A. Nott, and E.D. Levin Dorsal hippocampal alpha7 and alpha4beta2 nicotinic receptors and memory Brain Res. 1081 2006 72 78
53. R.L. Papke, P.R. Sanberg, and R.D. Shytle Analysis of mecamylamine stereoisomers on human nicotinic receptor subtypes J. Pharmacol. Exp. Ther. 297 2001 646 656
54. M.M. Pascual, V. Pastor, and R.O. Bernabeu Nicotine-conditioned place preference induced CREB phosphorylation and Fos expression in the adult rat brain Psychopharmacology (Berl.) 207 2009 57 71
55. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates fifth ed. 2003 Elsevier Academic Press Amsterdam
56. J.C. Pych, M. Kim, and P.E. Gold Effects of injections of glucose into the dorsal striatum on learning of place and response mazes Behav. Brain Res. 167 2006 373 378
57. M.E. Ragozzino, and P.E. Gold Glucose effects on mecamylamine-induced memory deficits and decreases in locomotor activity in mice Behav. Neural Biol. 56 1991 271 282
58. M.E. Ragozzino, and P.E. Gold Glucose injections into the medial septum reverse the effects of intraseptal morphine infusions on hippocampal acetylcholine output and memory Neuroscience 68 1995 981 988
59. M.E. Ragozzino, M.E. Parker, and P.E. Gold Spontaneous alternation and inhibitory avoidance impairments with morphine injections into the medial septum. Attenuation by glucose administration Brain Res. 597 1992 241 249
60. M.E. Ragozzino, G. Arankowsky-Sandoval, and P.E. Gold Glucose attenuates the effect of combined muscarinic-nicotinic receptor blockade on spontaneous alternation Eur. J. Pharmacol. 256 1994 31 36
61. M.E. Ragozzino, K.E. Unick, and P.E. Gold Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose Proc. Natl. Acad. Sci. U. S. A. 93 1996 4693 4698
62. M.E. Ragozzino, S.N. Pal, K. Unick, M.R. Stefani, and P.E. Gold Modulation of hippocampal acetylcholine release and spontaneous alternation scores by intrahippocampal glucose injections J. Neurosci. 18 1998 1595 1601
63. A. Rashidi-Pour ATP-sensitive potassium channels mediate the effects of a peripheral injection of glucose on memory storage in an inhibitory avoidance task Behav. Brain Res. 126 2001 43 48
64. J.D. Raybuck, and T.J. Gould The role of nicotinic acetylcholine receptors in the medial prefrontal cortex and hippocampus in trace fear conditioning Neurobiol. Learn. Mem. 94 2010 353 363
65. C. Rendeiro, D. Vauzour, R.J. Kean, L.T. Butler, M. Rattray, J.P. Spencer, and C.M. Williams Blueberry supplementation induces spatial memory improvements and region-specific regulation of hippocampal BDNF mRNA expression in young rats Psychopharmacology (Berl.) 223 2012 319 330
66. D.K. Rush, and K. Streit Memory modulation with peripherally acting cholinergic drugs Psychopharmacology (Berl.) 106 1992 375 382
67. J.A. Salinas, and P.E. Gold Glucose regulation of memory for reward reduction in young and aged rats Neurobiol. Aging 26 2005 45 52
68. P. Séguéla, J. Wadiche, K. Dineley-Miller, J.A. Dani, and J.W. Patrick Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium J. Neurosci. 13 1993 596 604
69. J.X. Shen, and J.L. Yakel Nicotinic acetylcholine receptor-mediated calcium signaling in the nervous system Acta Pharmacol. Sin. 30 2009 673 680
70. E. Sher, Y. Chen, T.J. Sharples, L.M. Broad, G. Benedetti, R. Zwart, G.I. McPhie, K.H. Pearson, T. Baldwinson, and G. De Filippi Physiological roles of neuronal nicotinic receptor subtypes: new insights on the nicotinic modulation of neurotransmitter release, synaptic transmission and plasticity Curr. Top. Med. Chem. 4 2004 283 297
71. A.J. Silva, J.H. Kogan, P.W. Frankland, and S. Kida CREB and memory Annu. Rev. Neurosci. 21 1998 127 148
72. M.R. Stefani, and P.E. Gold Intra-septal injections of glucose and glibenclamide attenuate galanin-induced spontaneous alternation performance deficits in the rat Brain Res. 813 1998 50 56
73. M.R. Stefani, and P.E. Gold Intrahippocampal infusions of K-ATP channel modulators influence spontaneous alternation performance: relationships to acetylcholine release in the hippocampus J. Neurosci. 21 2001 609 614
74. M.R. Stefani, G.M. Nicholson, and P.E. Gold ATP-sensitive potassium channel blockade enhances spontaneous alternation performance in the rat: a potential mechanism for glucose-mediated memory enhancement Neuroscience 93 1999 557 563
75. W.S. Stone, C.E. Croul, and P.E. Gold Attenuation of scopolamine-induced amnesia in mice Psychopharmacology (Berl.) 96 1988 417 420
76. W.S. Stone, B. Walser, S.D. Gold, and P.E. Gold Scopolamine- and morphine-induced impairments of spontaneous alternation performance in mice: reversal with glucose and with cholinergic and adrenergic agonists Behav. Neurosci. 105 1991 264 271
77. W.S. Stone, R.J. Rudd, and P.E. Gold Glucose attenuation of atropine-induced deficits in paradoxical sleep and memory Brain Res. 694 1995 133 138
78. A. Suzuki, S.A. Stern, O. Bozdagi, G.W. Huntley, R.H. Walker, P.J. Magistretti, and C.M. Alberini Astrocyte-neuron lactate transport is required for long-term memory formation Cell 144 2011 810 823
79. K. Tang, H. Wu, S.K. Mahata, and D.T. O'Connor A crucial role for the mitogen-activated protein kinase pathway in nicotinic cholinergic signaling to secretory protein transcription in pheochromocytoma cells Mol. Pharmacol. 54 1998 59 69
80. E. Tribollet, D. Bertrand, A. Marguerat, and M. Raggenbass Comparative distribution of nicotinic receptor subtypes during development, adulthood and aging: an autoradiographic study in the rat brain Neuroscience 124 2004 405 420
81. V.V. Uteshev, E.M. Meyer, and R.L. Papke Regulation of neuronal function by choline and 4OH-GTS-21 through alpha 7 nicotinic receptors J. Neurophysiol. 89 2003 1797 1806
82. C.M. Williams, M.A. El Mohsen, D. Vauzour, C. Rendeiro, L.T. Butler, J.A. Ellis, M. Whiteman, and J.P. Spencer Blueberry-induced changes in spatial working memory correlate with changes in hippocampal CREB phosphorylation and brain-derived neurotrophic factor (BDNF) levels Free Radic. Biol. Med. 45 2008 295 305
83. S. Wonnacott, J. Barik, J. Dickinson, and I.W. Jones Nicotinic receptors modulate transmitter cross talk in the CNS: nicotinic modulation of transmitters J. Mol. Neurosci. 30 2006 137 140
84. J.C. Yin, and T. Tully CREB and the formation of long-term memory Curr. Opin. Neurobiol. 6 1996 264 268
85. M.M. Zarei, K.A. Radcliffe, D. Chen, J.W. Patrick, and J.A. Dani Distributions of nicotinic acetylcholine receptor alpha7 and beta2 subunits on cultured hippocampal neurons Neuroscience 88 1999 755 764