Variations in excitatory and inhibitory postsynaptic protein content in rat cerebral cortex with respect to aging and cognitive status

Neuroscience

Volumn 159, Issue 2, 2009, Pages 896-907

  Majdi, M ^a   Ribeiro da Silva, A ^a   Cuello, A C ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

brain aging; cognitive impairment; excitatory; inhibitory; postsynaptic proteins

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; GEPHYRIN; GLUTAMATE RECEPTOR 2; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; NEUROLIGIN 1;

AGED; AGING; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MAZE TEST; NONHUMAN; PARIETAL LOBE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; WESTERN BLOTTING;

AGE FACTORS; AGING; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CARRIER PROTEINS; CEREBRAL CORTEX; COGNITION DISORDERS; GENE EXPRESSION REGULATION; MALE; MAZE LEARNING; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; RATS; RATS, INBRED F344; REACTION TIME; RECEPTORS, AMPA; RECEPTORS, GABA-A; SYNAPSES;

EID: 61349091634     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.11.034     Document Type: Article

References (92)

1. Adams I., and Jones D.G. Quantitative ultrastructural-changes in rat cortical synapses during early-adulthood and late-adulthood. Brain Res 239 (1982) 349-363
2. Backman C., Rose G.M., Hoffer B.J., Henry M.A., Bartus R.T., Friden P., and Granholm A.C. Systemic administration of a nerve growth factor conjugate reverses age-related cognitive dysfunction and prevents cholinergic neuron atrophy. J Neurosci 16 (1996) 5437-5442
3. Barnes C.A., and McNaughton B.L. An age comparison of the rates of acquisition and forgetting of spatial information in relation to long-term enhancement of hippocampal synapses. Behav Neurosci 99 (1985) 1040-1048
4. Bellone C., and Nicoll R.A. Rapid bidirectional switching of synaptic NMDA receptors. Neuron 55 (2007) 779-785
5. Berninghausen O., Rahman M.A., Silva J.P., Davletov B., Hopkins C., and Ushkaryov Y.A. Neurexin Ibeta and neuroligin are localized on opposite membranes in mature central synapses. J Neurochem 103 (2007) 1855-1863
6. Blum S., Hebert A.E., and Dash P.K. A role for the prefrontal cortex in recall of recent and remote memories. Neuroreport 17 (2006) 341-344
7. Brandeis R., Brandys Y., and Yehuda S. The use of the Morris water maze in the study of memory and learning. Int J Neurosci 48 (1989) 29-69
8. Bruno M.A., Clarke P.B., Seltzer A., Quirion R., Burgess K., Cuello A.C., and Saragovi H.U. Long-lasting rescue of age-associated deficits in cognition and the CNS cholinergic phenotype by a partial agonist peptidomimetic ligand of TrkA. J Neurosci 24 (2004) 8009-8018
9. Burke S.N., and Barnes C.A. Neural plasticity in the ageing brain. Nat Rev Neurosci 7 (2006) 30-40
10. Cassel J.C., Cassel S., Galani R., Kelche C., Will B., and Jarrard L. Fimbria-fornix vs selective hippocampal lesions in rats: Effects on locomotor activity and spatial learning and memory. Neurobiol Learn Mem 69 (1998) 22-45
11. Chubykin A.A., Atasoy D., Etherton M.R., Brose N., Kavalali E.T., Gibson J.R., and Sudhof T.C. Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 54 (2007) 919-931
12. Clarke R.J., and Johnson J.W. NMDA receptor NR2 subunit dependence of the slow component of magnesium unblock. J Neurosci 26 (2006) 5825-5834
13. Craig A.M., and Boudin H. Molecular heterogeneity of central synapses: afferent and target regulation. Nat Neurosci 4 (2001) 569-578
14. Craig A.M., and Kang Y. Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol 17 (2007) 43-52
15. Cruz R., Almaguer M.W., and Bergado Rosado J.A. [Glutathione in cognitive function and neurodegeneration]. Rev Neurol 36 (2003) 877-886
16. Dean C., and Dresbach T. Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci 29 (2006) 21-29
17. Dingledine R., Borges K., Bowie D., and Traynelis S.F. The glutamate receptor ion channels. Pharmacol Rev 51 (1999) 7-61
18. Droge W., and Schipper H.M. Oxidative stress and aberrant signaling in aging and cognitive decline. Aging Cell 6 (2007) 361-370
19. Fallah Z., and Clowry G.J. Gephyrin-like immunoreactivity is a marker for growing axons in the central nervous system of the immature rat. Dev Neurosci 21 (1999) 50-57
20. Fischer W., Bjorklund A., Chen K., and Gage F.H. Ngf improves spatial memory in aged rodents as a function of age. J Neurosci 11 (1991) 1889-1906
21. Frankland P.W., and Bontempi B. The organization of recent and remote memories. Nat Rev Neurosci 6 (2005) 119-130
22. Fritschy J.M., Schweizer C., Brunig I., and Luscher B. Pre- and post-synaptic mechanisms regulating the clustering of type A gamma-aminobutyric acid receptors (GABAA receptors). Biochem Soc Trans 31 (2003) 889-892
23. Gage F.H., Dunnett S.B., and Bjorklund A. Spatial-learning and motor deficits in aged rats. Neurobiol Aging 5 (1984) 43-48
24. Gallagher M., and Burwell R.D. Relationship of age-related decline across several behavioral domains. Neurobiol Aging 10 (1989) 691-708
25. Geinisman Y., Gundersen H.J., van der Zee E., and West M.J. Unbiased stereological estimation of the total number of synapses in a brain region. J Neurocytol 25 (1996) 805-819
26. Graf E.R., Kang Y., Hauner A.M., and Craig A.M. Structure function and splice site analysis of the synaptogenic activity of the neurexin-1 beta LNS domain. J Neurosci 26 (2006) 4256-4265
27. Graf E.R., Zhang X., Jin S.X., Linhoff M.W., and Craig A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119 (2004) 1013-1026
28. Harman D. Free radical theory of aging: an update: increasing the functional life span. Ann N Y Acad Sci 1067 (2006) 10-21
29. Hornung J.P., and Fritschy J.M. Developmental profile of GABAA-receptors in the marmoset monkey: expression of distinct subtypes in pre- and postnatal brain. J Comp Neurol 367 (1996) 413-430
30. Hunt C.A., Schenker L.J., and Kennedy M.B. PSD-95 is associated with the postsynaptic density and not with the presynaptic membrane at forebrain synapses. J Neurosci 16 (1996) 1380-1388
31. Irie M., Hata Y., Takeuchi M., Ichtchenko K., Toyoda A., Hirao K., Takai Y., Rosahl T.W., and Sudhof T.C. Binding of neuroligins to PSD-95. Science 277 (1997) 1511-1515
32. Issa A.M., Rowe W., Gauthier S., and Meaney M.J. Hypothalamic-pituitary-adrenal activity in aged, cognitively impaired and cognitively unimpaired rats. J Neurosci 10 (1990) 3247-3254
33. Izquierdo I., and Medina J.H. Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol Learn Mem 68 (1997) 285-316
34. Kennedy M.B. The postsynaptic density at glutamatergic synapses. Trends Neurosci 20 (1997) 264-268
35. Kew J.N., Richards J.G., Mutel V., and Kemp J.A. Developmental changes in NMDA receptor glycine affinity and ifenprodil sensitivity reveal three distinct populations of NMDA receptors in individual rat cortical neurons. J Neurosci 18 (1998) 1935-1943
36. Kim S., Burette A., Chung H.S., Kwon S.K., Woo J., Lee H.W., Kim K., Kim H., Weinberg R.J., and Kim E. NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat Neurosci 9 (2006) 1294-1301
37. Kneussel M. Dynamic regulation of GABA(A) receptors at synaptic sites. Brain Res Brain Res Rev 39 (2002) 74-83
38. Kneussel M., Brandstatter J.H., Laube B., Stahl S., Muller U., and Betz H. Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice. J Neurosci 19 (1999) 9289-9297
39. Kravitz, Kuffler S.W., and Potter D.D. Gamma-aminobutyric acid and other blocking compounds in Crustacea. III. Their relative concentrations in separated motor and inhibitory axons. J Neurophysiol 26 (1963) 739-751
40. Krnjevic K., and Schwartz S. The action of gamma-aminobutyric acid on cortical neurones. Exp Brain Res 3 (1967) 320-336
41. Kuffler S.W., and Edwards C. Mechanism of gamma aminobutyric acid (GABA) action and its relation to synaptic inhibition. J Neurophysiol 21 (1958) 589-610
42. Laube B., Kuhse J., and Betz H. Evidence for a tetrameric structure of recombinant NMDA receptors. J Neurosci 18 (1998) 2954-2961
43. Levi S., Logan S.M., Tovar K.R., and Craig A.M. Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons. J Neurosci 24 (2004) 207-217
44. Levinson J.N., Chery N., Huang K., Wong T.P., Gerrow K., Kang R., Prange O., Wang Y.T., and El-Husseini A. Neuroligins mediate excitatory and inhibitory synapse formation: involvement of PSD-95 and neurexin-1beta in neuroligin-induced synaptic specificity. J Biol Chem 280 (2005) 17312-17319
45. Liu B., Liao M., Mielke J.G., Ning K., Chen Y., Li L., El-Hayek Y.H., Gomez E., Zukin R.S., Fehlings M.G., and Wan Q. Ischemic insults direct glutamate receptor subunit 2-lacking AMPA receptors to synaptic sites. J Neurosci 26 (2006) 5309-5319
46. Liu L., Wong T.P., Pozza M.F., Lingenhoehl K., Wang Y., Sheng M., Auberson Y.P., and Wang Y.T. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304 (2004) 1021-1024
47. Luebke J.I., Chang Y.M., Moore T.L., and Rosene D.L. Normal aging results in decreased synaptic excitation and increased synaptic inhibition of layer 2/3 pyramidal cells in the monkey prefrontal cortex. Neuroscience 125 (2004) 277-288
48. Luscher B., and Keller C.A. Regulation of GABAA receptor trafficking, channel activity, and functional plasticity of inhibitory synapses. Pharmacol Ther 102 (2004) 195-221
49. MacDonald J.F., Jackson M.F., and Beazely M.A. Hippocampal long-term synaptic plasticity and signal amplification of NMDA receptors. Crit Rev Neurobiol 18 (2006) 71-84
50. Majdi M., Ribeiro-da-Silva A., and Cuello A.C. Cognitive impairment and transmitter-specific pre- and post- synaptic changes in the rat cerebral cortex during aging. Eur J Neurosci 26 (2007) 3583-3596
51. Mano I., and Teichberg V.I. A tetrameric subunit stoichiometry for a glutamate receptor-channel complex. Neuroreport 9 (1998) 327-331
52. Markus E.J., and Petit T.L. Neocortical synaptogenesis, aging, and behavior: life-span development in the motor sensory system of the rat. Exp Neurol 96 (1987) 262-278
53. Masliah E., Crews L., and Hansen L. Synaptic remodeling during aging and in Alzheimer's disease. J Alzheimers Dis 9 (2006) 91-99
54. Massey P.V., Johnson B.E., Moult P.R., Auberson Y.P., Brown M.W., Molnar E., Collingridge G.L., and Bashir Z.I. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci 24 (2004) 7821-7828
55. Maviel T., Durkin T.P., Menzaghi F., and Bontempi B. Sites of neocortical reorganization critical for remote spatial memory. Science 305 (2004) 96-99
56. McClearn G.E. Biomarkers of age and aging. Exp Gerontol 32 (1997) 87-94
57. McKernan R.M., and Whiting P.J. Which GABAA-receptor subtypes really occur in the brain?. Trends Neurosci 19 (1996) 139-143
58. Meng Y., Zhang Y., and Jia Z. Synaptic transmission and plasticity in the absence of AMPA glutamate receptor GluR2 and GluR3. Neuron 39 (2003) 163-176
59. Meyer G., Varoqueaux F., Neeb A., Oschlies M., and Brose N. The complexity of PDZ domain-mediated interactions at glutamatergic synapses: a case study on neuroligin. Neuropharmacology 47 (2004) 724-733
60. Michels G., and Moss S.J. GABAA receptors: properties and trafficking. Crit Rev Biochem Mol Biol 42 (2007) 3-14
61. Mohler H. GABAA receptors in central nervous system disease: anxiety, epilepsy, and insomnia. J Recept Signal Transduct Res 26 (2006) 731-740
62. Nagy J., Boros A., Dezso P., Kolok S., and Fodor L. Inducible expression and pharmacology of recombinant NMDA receptors, composed of rat NR1a/NR2B subunits. Neurochem Int 43 (2003) 19-29
63. Nam C.I., and Chen L. Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proc Natl Acad Sci U S A 102 (2005) 6137-6142
64. Nguyen T., and Sudhof T.C. Binding properties of neuroligin 1 and neurexin 1beta reveal function as heterophilic cell adhesion molecules. J Biol Chem 272 (1997) 26032-26039
65. Persohn E., Malherbe P., and Richards J.G. Comparative molecular neuroanatomy of cloned GABAA receptor subunits in the rat CNS. J Comp Neurol 326 (1992) 193-216
66. Peters A. Structural changes that occur during normal aging of primate cerebral hemispheres. Neurosci Biobehav Rev 26 (2002) 733-741
67. Peters A., Leahu D., Moss M.B., and McNally K.J. The effects of aging on area 46 of the frontal cortex of the rhesus monkey. Cereb Cortex 4 (1994) 621-635
68. Prange O., Wong T.P., Gerrow K., Wang Y.T., and El-Husseini A. A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin. Proc Natl Acad Sci U S A 101 (2004) 13915-13920
69. Quirion R., Wilson A., Rowe W., Aubert I., Richard J., Doods H., Parent A., White N., and Meaney M.J. Facilitation of acetylcholine-release and cognitive performance by an M(2)-muscarinic receptor antagonist in aged memory-impaired rats. J Neurosci 15 (1995) 1455-1462
70. Rapp P.R., and Amaral D.G. Individual differences in the cognitive and neurobiological consequences of normal aging. Trends Neurosci 15 (1992) 340-345
71. Resnick S.M., Pham D.L., Kraut M.A., Zonderman A.B., and Davatzikos C. Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J Neurosci 23 (2003) 3295-3301
72. Rosenmund C., Stern-Bach Y., and Stevens C.F. The tetrameric structure of a glutamate receptor channel. Science 280 (1998) 1596-1599
73. Sanchez R.M., Koh S., Rio C., Wang C., Lamperti E.D., Sharma D., Corfas G., and Jensen F.E. Decreased glutamate receptor 2 expression and enhanced epileptogenesis in immature rat hippocampus after perinatal hypoxia-induced seizures. J Neurosci 21 (2001) 8154-8163
74. Schipper H.M. Brain iron deposition and the free radical-mitochondrial theory of ageing. Ageing Res Rev 3 (2004) 265-301
75. Sieghart W. Structure, pharmacology, and function of GABAA receptor subtypes. Adv Pharmacol 54 (2006) 231-263
76. Simpkins K.L., Guttmann R.P., Dong Y., Chen Z., Sokol S., Neumar R.W., and Lynch D.R. Selective activation induced cleavage of the NR2B subunit by calpain. J Neurosci 23 (2003) 11322-11331
77. Snyder E.M., Nong Y., Almeida C.G., Paul S., Moran T., Choi E.Y., Nairn A.C., Salter M.W., Lombroso P.J., Gouras G.K., and Greengard P. Regulation of NMDA receptor trafficking by amyloid-beta. Nat Neurosci 8 (2005) 1051-1058
78. Standley S., Wagle N., and Baudry M. Developmental changes in subcellular AMPA/GluR receptor populations in rat forebrain. Brain Res Dev Brain Res 107 (1998) 277-283
79. Stephenson F.A. The GABAA receptors. Biochem J 310 Pt 1 (1995) 1-9
80. Stephenson F.A. Structure and trafficking of NMDA and GABAA receptors. Biochem Soc Trans 34 (2006) 877-881
81. Takeuchi A., and Takeuchi N. A study of the action of picrotoxin on the inhibitory neuromuscular junction of the crayfish. J Physiol 205 (1969) 377-391
82. Takeuchi A., and Takeuchi N. Electrophysiological studies of the action of GABA on the synaptic membrane. Fed Proc 26 (1967) 1633-1638
83. Talos D.M., Fishman R.E., Park H., Folkerth R.D., Follett P.L., Volpe J.J., and Jensen F.E. Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. I. Rodent cerebral white matter and cortex. J Comp Neurol 497 (2006) 42-60
84. Talos D.M., Follett P.L., Folkerth R.D., Fishman R.E., Trachtenberg F.L., Volpe J.J., and Jensen F.E. Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. II. Human cerebral white matter and cortex. J Comp Neurol 497 (2006) 61-77
85. Terry R.D., and Katzman R. Life span and synapses: will there be a primary senile dementia?. Neurobiol Aging 22 (2001) 347-348
86. Toyoda H., Wu L.J., Zhao M.G., Xu H., and Zhuo M. Time-dependent postsynaptic AMPA GluR1 receptor recruitment in the cingulate synaptic potentiation. Dev Neurobiol 67 (2007) 498-509
87. Wang H., Bedford F.K., Brandon N.J., Moss S.J., and Olsen R.W. GABA(A)-receptor-associated protein links GABA(A) receptors and the cytoskeleton. Nature 397 (1999) 69-72
88. Wenthold R.J., Prybylowski K., Standley S., Sans N., and Petralia R.S. Trafficking of NMDA receptors. Annu Rev Pharmacol Toxicol 43 (2003) 335-358
89. Wiltgen B.J., Brown R.A., Talton L.E., and Silva A.J. New circuits for old memories: the role of the neocortex in consolidation. Neuron 44 (2004) 101-108
90. Wong T.P., Marchese G., Casu M.A., Ribeiro-da-Silva A., Cuello A.C., and De Koninck Y. Imbalance towards inhibition as a substrate of aging-associated cognitive impairment. Neurosci Lett 397 (2006) 64-68
91. Wong T.P., Marchese G., Casu M.A., Ribeiro-da-Silva A., Cuello A.C., and De Koninck Y. Loss of presynaptic and postsynaptic structures is accompanied by compensatory increase in action potential-dependent synaptic input to layer V neocortical pyramidal neurons in aged rats. J Neurosci 20 (2000) 8596-8606
92. Yu W., Jiang M., Miralles C.P., Li R.W., Chen G., and de Blas A.L. Gephyrin clustering is required for the stability of GABAergic synapses. Mol Cell Neurosci 36 (2007) 484-500