Hippocampal synaptic plasticity and glutamate receptor regulation: Influences of diabetes mellitus

European Journal of Pharmacology

Volumn 490, Issue 1-3, 2004, Pages 177-186

  Trudeau, Francois ^a   Gagnon, Sylvain ^b   Massicotte, Guy ^a  

^a UNIVERSITÉ DU QUÉBEC À TROIS RIVIÈRES   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Diabetes mellitus; Glutamate receptor; Long term potentiation; Synaptic plasticity

Indexed keywords

AMPA RECEPTOR; CALCIUM; GLUCOSE; INSULIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBTYPE; STREPTOZOCIN;

CALCIUM TRANSPORT; CHRONIC DISEASE; DIABETIC NEUROPATHY; DIABETOGENESIS; ELECTROPHYSIOLOGY; HIPPOCAMPUS; HUMAN; HYPERGLYCEMIA; HYPERINSULINEMIA; IMMUNOREACTIVITY; INSULIN BLOOD LEVEL; INSULIN DEFICIENCY; INSULIN DEPENDENT DIABETES MELLITUS; LIPID PEROXIDATION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NERVE DEGENERATION; NEUROTOXICITY; NEUROTRANSMITTER RELEASE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT STRAIN; RECEPTOR INTRINSIC ACTIVITY; REVIEW; STREPTOZOCIN DIABETES; SYNAPTIC TRANSMISSION; WESTERN BLOTTING;

EID: 1842785174     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2004.02.055     Document Type: Article

References (99)

1. Ametov A.S., Barinov A., Dyck P.J., Hermann R., Kozlova N., Litchy W.J., Low P.A., Nehrdich D., Novosadova M., O'Brien P.C., Reljanovic M., Samigullin R., Schuette K., Strokov I., Tritschler H.J., Wessel K., Yakhno N., Ziegler D., Group S.T.S. The sensory symptoms of diabetic polyneuropathy are improved with alpha-lipoic acid: the SYDNEY trial. Diabetes Care. 26:2003;770-776.
2. Anderson R.J., Freedland K.E., Clouse R.E., Lustman P.J. The prevalence of comorbid depression in adults with diabetes: a meta-analysis. Diabetes Care. 24:2001;1069-1078.
3. Artola A., Brocher S., Singer W. Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature. 347:1990;69-72. (comment).
4. Artola A., Hensch T., Singer W. Calcium-induced long-term depression in the visual cortex of the rat in vitro. J. Neurophysiol. 76:1996;984-994.
5. Artola A., Kamal A., Ramakers G.M., Gardoni F., Di Luca M., Biessels G.J., Cattabeni F., Gispen W.H. Synaptic plasticity in the diabetic brain: advanced aging? Prog. Brain Res. 138:2002;305-314.
6. Baudry M., Lynch G. Remembrance of arguments past: how well is the glutamate receptor hypothesis of LTP holding up after 20 years? Neurobiol. Learn. Mem. 76:2001;284-297.
7. Baudry M., Massicotte G. Physiological and pharmacological relationships between long-term potentiation and mammalian memory. Concr. Neurosci. 3:1992;79-98.
8. Baudry M., Massicotte G., Hauge S. Opposite effects of phospholipase A2 on 3H-AMPA binding in adult and neonatal membranes. Dev. Brain Res. 61:1991;265-267.
9. Bernard J., Lahsaini A., Massicotte G. Potassium-induced long-term potentiation in area CA1 of the hippocampus involves phospholipase activation. Hippocampus. 4:1994;447-453.
10. Bi X., Chang V., Molnar E., McIlhinney R.A., Baudry M. The C-terminal domain of glutamate receptor subunit 1 is a target for calpain-mediated proteolysis. Neuroscience. 73:1996;903-906.
11. Bi R., Bi X., Baudry M. Phosphorylation regulates calpain-mediated truncation of glutamate ionotropic receptors. Brain Res. 797:1998;154-158.
12. Biessels G.J., Kamal A., Ramakers G.M., Urban I.J., Spruijt B.M., Erkelens D.W., Gispen W.H. Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes. 45:1996;1259-1266.
13. Biessels G.J., van der Heide L.P., Kamal A., Bleys R.L., Gispen W.H. Ageing and diabetes: implications for brain function. Eur. J. Pharmacol. 441:2002;1-14.
14. Bitar M., Koulu M., Rapoport S.I., Linnoila M. Diabetes-induced alteration in brain monoamine metabolism in rats. J. Pharmacol. Exp. Ther. 236:1985;432-437.
15. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 361:1993;31-39.
16. Boyle J.P., Honeycutt A.A., Narayan K.M., Hoerger T.J., Geiss L.S., Chen H., Thompson T.J. Projection of diabetes burden through 2050: impact of changing demography and disease prevalence in the U.S. Diabetes Care. 24:2001;1936-1940.
17. Brown M.J., Asbury A.K. Diabetic neuropathy. Ann. Neurol. 15:1984;2-12.
18. Chabot C., Massicotte G., Milot M., Trudeau F., Gagné J. Impaired modulation of AMPA receptors by calcium-dependent processes in streptozotocin-induced diabetic rats. Brain Res. 768:1997;249-256.
19. Chabot C., Bernard J., Normandin M., Ohayon M., Baudry M., Massicotte G. Developmental changes in depolarization-mediated AMPA receptor modifications and potassium-induced long-term potentiation. Dev. Brain Res. 93:1996;70-75.
20. Choi D.W., Rothman S.M. The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu. Rev. Neurosci. 13:1990;161-182.
21. Chu P.C., Lin M.T., Shian L.R., Leu S.Y. Alterations in physiologic functions and in brain monoamine content in streptozotocin-diabetic rats. Diabetes. 35:1986;481-484.
22. Dev K.K., Honore T., Henley J.M. Effects of phospholipase A2 on alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptor subunits. Biochem. Soc. Trans. 25:1997;537S.
23. Dev K.K., Honore T., Henley J.M. Different effects of phospholipase A2 on agonist binding to hippocampal, cortical and recombinant homomeric alpha-amino-3-hydroxy-5-methyl-4-isoxazolpropionate receptors. Neurosci. Lett. 246:1998;25-28.
24. Di Luca M., Ruts L., Gardoni F., Cattabeni F., Biessels G.J., Gispen W.H. NMDA receptor subunits are modified transcriptionally and post-translationally in the brain of streptozotocin-diabetic rats. Diabetologia. 42:1999;693-701.
25. Di Mario U., Morano S., Valle E., Pozzessere G. Electrophysiological alterations of the central nervous system in diabetes mellitus. Diabetes/Metab. Rev. 11:1995;259-277.
26. Dingledine R., Borges K., Bowie D., Traynelis S.F. The glutamate receptor ion channels. Pharmacol. Rev. 51:1999;7-61.
27. Dyck P.J., Kratz K.M., Karnes J.L., Litchy W.J., Klein R., Pach J.M., Wilson D.M., O'Brien P.C., Melton L.J. 3rd, Service F.J. The prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study. [erratum appears in Neurology 1993 Nov;43(11):2345] Neurology. 43:1993;817-824.
28. Franceshi M., Cecchetto R., Minicucci F., Smizne S., Baio G., Canal N. Cognitive processes in insulin-dependent diabetes. Diabetes Care. 7:1984;228-231.
29. Gagné J., Milot M., Gélinas S., Lahsaïni A., Trudeau F., Martinoli M.G., Massicotte G. Binding properties of glutamate receptors in streptozotocin-induced diabetes in rats. Diabetes. 46:1997;841-846.
30. Gagné J., Gélinas S., Martinoli M.G., Foster T.C., Ohayon M., Thompson R.F., Baudry M., Massicotte G. AMPA receptor properties in adult rat hippocampus following environmental enrichment. Brain Res. 799:1998;16-25.
31. Gardoni F., Kamal A., Bellone C., Biessels G.J., Ramakers G.M., Cattabeni F., Gispen W.H., Di Luca M. Effects of streptozotocin-diabetes on the hippocampal NMDA receptor complex in rats. J. Neurochem. 80:2002;438-447.
32. Gasparini L., Netzer W.J., Greengard P., Xu H. Does insulin dysfunction play a role in Alzheimer's disease? Trends Pharmacol. Sci. 23:2002;288-293.
33. Gispen W.H., Biessels G.J. Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci. 23:2000;542-549.
34. Grodstein F., Chen J., Wilson R.S., Manson J.E., Nurses' Health S. Type 2 diabetes and cognitive function in community-dwelling elderly women. Diabetes Care. 24:2001;1060-1065.
35. Hayashi Y., Shi S.H., Esteban J.A., Piccini A., Poncer J.C., Malinow R. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science. 287:2000;2262-2267.
36. Isaac J.T.R., Nicoll R.A., Malenka R.C. Evidence for silent synapses: Implications for the expression of LTP. Neuron. 15:1995;427-434.
37. Ito I., Futai K., Katagiri H., Watanabe M., Sakimura K., Mishina M., Sugiyama H. Synapse-selective impairment of NMDA receptor functions in mice lacking NMDA receptor epsilon 1 or epsilon 2 subunit. J. Physiol. 500:1997;401-408.
38. Kamal A., Biessels G.J., Urban I.J., Gispen W.H. Hippocampal synaptic plasticity in streptozotocin-diabetic rats: impairment of long-term potentiation and facilitation of long-term depression. Neuroscience. 90:1999;737-745.
39. Kamal A., Biessels G.J., Duis S.E., Gispen W.H. Learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: interaction of diabetes and ageing. Diabetologia. 43:2000;500-506.
40. Kamal A., Artola A., Biessels G.J., Gispen W.H., Ramakers G.M. Increased spike broadening and slow afterhyperpolarization in CA1 pyramidal cells of streptozotocin-induced diabetic rats. Neuroscience. 118:2003;577-583.
41. Knopman D., Boland L.L., Mosley T., Howard G., Liao D., Szklo M., McGovern P., Folsom A.R. Cardiovascular risk factors and cognitive decline in middle-aged adults. Neurology. 56:2001;42-48.
42. Lackovic Z., Salkovic M., Kuci S., Relja M. Effect of long-lasting diabetes mellitus on rat and human brain monoamines. J. Neurochem. 54:1990;143-147.
43. Lapierre L., Valastro B., Miceli D., Massicotte G. AMPA receptor modulation in previously frozen mouse brain sections: Opposite effects of calcium in the cortex and hippocampus. Hippocampus. 10:2000;645-653.
44. Leibson C.L., Rocca W.A., Hanson V.A., Cha R., Kokmen E., O'Brien P.C., Palumbo P.J. Risk of dementia among persons with diabetes mellitus: a population-based cohort study. Am. J. Epidemiol. 145:1997;301-308.
45. Li N., Young M.M., Bailey C.J., Smith M.E. NMDA and AMPA glutamate receptor subtypes in the thoracic spinal cord in lean and obese-diabetic ob/ob mice. Brain Res. 849:1999;34-44.
46. Li X.L., Aou S., Hori T., Oomura Y. Spatial memory deficit and emotional abnormality in OLETF rats. Physiol. Behav. 75:2002;15-23.
47. Liao D., Hessler N.A., Malinow R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature. 375:1995;400-404.
48. Lipton S.A., Rosenberg P.A. Excitatory amino acids as a final common pathway for neurologic disorders. New Engl. J. Med. 330:1994;613-622.
49. Liu L., Brown J.C., Webster W.W., Morrisett R.A., Monaghan D.T. Insulin potentiates N-methyl-D-aspartate receptor activity in Xenopus oocytes and rat hippocampus. Neurosci. Lett. 192:1995;5-8.
50. Magarinos A.M., McEwen B.S. Experimental diabetes in rats causes hippocampal dendritic and synaptic reorganization and increased glucocorticoid reactivity to stress. Proc. Natl. Acad. Sci. U. S. A. 97:2000;11056-11061.
51. Makar T.K., Hungund B.L., Cook G.A., Kashfi K., Cooper A.J.L. Lipid metabolism and membrane composition are altered in the brains of type II diabetic mice. J. Neurochem. 64:1995;2159-2168.
52. Malenka R.C. Synaptic plasticity in the hippocampus: LTP and LTD. Cell. 78:1994;535-538.
53. Malinow R., Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25:2002;103-126.
54. Man H.E., Lin J.W., Ju W.H., Ahmadian G., Liu L., Becker L.E., Sheng M., Wang Y.T. Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron. 25:2000;649-662.
55. Manabe T., Renner P., Nicholl R.A. Postsynaptic contribution to long-term potentiation revealed by the analysis of miniature synaptic currents. Nature. 355:1992;50-55.
56. Mandrup-Poulsen T. Diabetes. BMJ. 316:1998;1221-1225.
57. Maren S., Tocco G., Standley S., Baudry M., Thompson R.F. Postsynaptic factors in the expression of long-term potentiation (LTP): increased glutamate receptor binding following LTP induction in vivo. Proc. Natl. Acad. Sci. U. S. A. 90:1993;9654-9658.
58. Massicotte G. Modification of glutamate receptors by phospholipase A2: its role in adaptive neural plasticity. Cell. Mol. Life Sci. 57:2000;1542-1550.
59. Massicotte G., Baudry M. Triggers and substrates of hippocampal synaptic plasticity. Neurosci. Biobehav. Rev. 15:1991;415-423.
60. Massicotte G., Vanderklish P., Lynch G., Baudry M. Modulation of AMPA/Quisqualate receptors by phospholipase A2: A necessary step in long-term potentiation. Proc. Natl. Acad. Sci. U. S. A. 88:1991;1893-1897.
61. Massicotte G., Bernard J., Baudry M. Postnatal changes in AMPA receptor regulation by phospholipase A2 treatment of synaptic membranes: temporally differential effects on agonist and antagonist binding. Dev. Brain Res. 66:1992;203-208.
62. McCall A.L. The impact of diabetes on the CNS. Diabetes. 41:1992;557-570.
63. McCarthy A.M., Lindgren S., Mengeling M.A., Tsalikian E., Engvall J.C. Effects of diabetes on learning in children. Pediatrics. 109:2002;E9.
64. McCarthy A.M., Lindgren S., Mengeling M.A., Tsalikian E., Engvall J. Factors associated with academic achievement in children with type 1 diabetes. Diabetes Care. 26:2003;112-117.
65. Medina I., Filippova N., Charton G., Rougeole S., Ben-Ari Y., Khrestchatisky M., Bregestovski P. Calcium-dependent inactivation of heteromeric NMDA receptor-channels expressed in human embryonic kidney cells. J. Physiol. 482:1995;567-573.
66. Messier C., Gagnon M. Glucose regulation and cognitive functions: Relation to Alzheimer's disease and diabetes. Behav. Brain Res. 75:1996;1-11.
67. Michaelis E.K. Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog. Neurobiol. 54:1998;369-415.
68. Mooradian A.D., Dickerson F., Smith T.L. Lipid order and composition of synaptic membranes in experimental diabetes mellitus. Neurochem. Res. 15:1990;981-985.
69. Mulkey R.M., Herron C.E., Malenka R.C. An essential role for protein phosphatases in hippocampal long-term depression. Science. 261:1993;1051-1055.
70. Mulkey R.M., Endo S., Shenollkar S.S., Malenka R.C. Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature. 1994;486-488.
71. Northam E.A., Anderson P.J., Jacobs R., Hughes M., Warne G.L., Werther G.A. Neuropsychological profiles of children with Type 1 diabetes 6 years after disease onset. Diabetes Care. 24:2001;1541-1546.
72. O'Dell T.J., Kandel E.R. Low-frequency stimulation erases LTP through an NMDA receptor-mediated activation of protein phosphatases. Learn. Mem. 1:1994;129-139.
73. Ott A., Stolk R.P., van Harskamp F., Pols H.A., Hofman A., Breteler M.M. Diabetes mellitus and the risk of dementia: the Rotterdam Study. Neurology. 53:1999;1937-1942. (comment).
74. Peila R., Rodriguez B.L., Launer L.J., Honolulu-Asia Aging S. Type 2 diabetes, APOE gene, and the risk for dementia and related pathologies: the Honolulu-Asia Aging Study. Diabetes. 51:2002;1256-1262.
75. Rosello-Catafau J., Closa D., Hotter G., Bulbena O., Ortiz M.A., Pou-Torello J.M., Gimeno M.A.F., Gelpi E. Pancreas lipoxygenase arachidonic acid metabolites production in streptozotocin-induced diabetes in rats. Horm. Metab. Res. 26:1994;387-388.
76. Rosello-Catafau J., Hotter G., Closa D., Ortiz M.A., Pou-Torello J.M., Gimeno M., Bioque G., Gelpi E. Liver lipoxygenase arachidonic acid metabolites in streptozotocin-induced diabetes in rats. Prost. Leuk. Essent. Fatty Acids. 51:1994;411-413.
77. Rosen P., Nawroth P.P., King G., Moller W., Tritschler H.J., Packer L. The role of oxidative stress in the onset and progression of diabetes and its complications: a summary of a Congress Series sponsored by UNESCO-MCBN, the American Diabetes Association and the German Diabetes Society. Diabetes/Metab. Res. Rev. 17:2001;189-212.
78. Ryan C.M., Geckle M. Why is learning and memory dysfunction in Type 2 diabetes limited to older adults? Diabetes/Metab. Res. Rev. 16:2000;308-315.
79. Ryan C.M., Geckle M.O. Circumscribed cognitive dysfunction in middle-aged adults with type 2 diabetes. Diabetes Care. 23:2000;1486-1493.
80. Ryan C., Vega A., Drash A. Cognitive deficits in adolescents who developed diabetes early in life. Pediatrics. 75:1985;921-927.
81. Ryan C.M., Williams T.M., Finegog D.N., Orchard T.J. Cognitive dysfunction in adult with Type 1 (insulin dependent) diabetes mellitus of long duration: effects of recurrent hypoglycemia and other chronic complications. Diabetologia. 36:1993;329-334.
82. Schmidt R.E., Dorsey D.A., Beaudet L.N., Peterson R.G. Analysis of the Zucker Diabetic Fatty (ZDF) type 2 diabetic rat model suggests a neurotrophic role for insulin/IGF-I in diabetic autonomic neuropathy. Am. J. Pathol. 163:2003;21-28.
83. Schreiber S.S., Baudry M. Selective neuronal vulnerability in the hippocampus - a role for a gene expression? Trends Neurosci. 18:1995;446-451.
84. Shi S.H., Hayashi Y., Petralia R.S., Zaman S.H., Wenthold R.J., Svoboda K., Malinow R. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science. 284:1999;1811-1816.
85. Siesjö B.K., Zhao Q., Phalmark K., Siesjo P., Katsura K., Folbergrova J. Glutamate, calcium, and free radicals as mediators of ischemic brain damage. Ann. Thorac. Surg. 59:1995;1316-1320.
86. Sima A.A., Sugimoto K. Experimental diabetic neuropathy: an update. Diabetologia. 42:1999;773-788.
87. Skeberdis V.A., Lan J.Y., Zheng X., Zukin R.S., Bennett M.V. Insulin promotes rapid delivery of N-methyl-D-aspartate receptors to the cell surface by exocytosis. Proc. Natl. Acad. Sci. U. S. A. 98:2001;3561-3566.
88. Song I., Huganir R.L. Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci. 25:2002;578-588.
89. Staubli U., Larson J., Lynch G. Mossy fiber potentiation and long-term potentiation involve different expression mechanisms. Synapse. 5:1990;333-335.
90. St-Gelais, F., Ménard, C., Congar, P., Trudeau, L.E., Massicotte, G., in press. Postsynaptic injection of calcium-independent phospholipase A2 inhibitors selectively increases AMPA receptor-mediated synaptic transmission. Hippocampus.
91. Suzuki C., Ozaki I., Tanosaki M., Suda T., Baba M., Matsunaga M. Peripheral and central conduction abnormalities in diabetes mellitus. Neurology. 54:2000;1932-1937.
92. 3H]AMPA binding in rat hippocampus. Brain Res. 573:1992;228-234.
93. Valastro B., Cossette J., Lavoie N., Gagnon S., Trudeau F., Massicotte G. Up-regulation of glutamate receptors is associated with LTP defects in the early stages of diabetes mellitus. Diabetologia. 45:2002;642-650.
94. Vaithianathan T., Bedi D., Kanju P.M., Wang Z., Bahr B.A., Dityatev A., Judd R.L., Suppiramaniam V.D. Evidence of AMPA-glutamate receptor dysfunction in brain of streptozotocin-diabetic rats. Soc. Neurosci. 2003;375.18.
95. Vanderklish P., Neve R., Bahr B.A., Arai A., Hennegrif M., Larson J., Lynch G. Translational suppression of a glutamate receptor subunit impairs long-term potentiation. Synapse. 12:1992;333-337.
96. Wang J., Kelly P.T. The balance between postsynaptic Ca2+-dependent protein kinase and phosphatase activities controlling synaptic strength. Learn. Mem. 3:1996;170-181.
97. Welsh B., Wecker L. Effects of streptozotocin-induced diabetes on acetylcholine metabolism in rat brain. Neurochem. Res. 16:1991;453-460.
98. Yagihashi S. Pathology and pathogenetic mechanisms of diabetic neuropathy. Diabetes/Metab. Res. Rev. 11:1995;193-225.
99. Zucker R.S. Short-term synaptic plasticity. Annu. Rev. Neurosci. 12:1989;13-22.