Synapses with a segmented, completely partitioned postsynaptic density express more AMPA receptors than other axospinous synaptic junctions

Neuroscience

Volumn 125, Issue 3, 2004, Pages 615-623

  Ganeshina, O ^a   Berry, R W ^a   Petralia, R S ^b   Nicholson, D A ^a   Geinisman, Y ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

Author keywords

amino 3 hydroxy 5 methyl 4 isoxazole propionate receptor; AMPAR; Analysis of covariance; Analysis of variance; ANCOVA; ANOVA; Axospinous synapses; Hippocampus; LTP; NGS; Postembedding immunogold electron microscopy; Synaptic plasticity

Indexed keywords

AMPA RECEPTOR; CALCIUM; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL TISSUE; ARTICLE; CELL SUBPOPULATION; CONTROLLED STUDY; CORRELATION ANALYSIS; COVARIANCE; HIPPOCAMPUS; IMMUNOGOLD ELECTRON MICROSCOPY; LONG TERM POTENTIATION; MALE; MEASUREMENT; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; RECEPTOR DENSITY; SYNAPSE; SYNAPTIC EFFICACY;

ANIMALS; CELL SIZE; DENDRITES; GLUTAMIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LONG-TERM POTENTIATION; MALE; MICROSCOPY, ELECTRON; RATS; RATS, INBRED F344; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC MEMBRANES; SYNAPTIC TRANSMISSION;

EID: 1942424881     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2004.02.025     Document Type: Article

References (56)

1. Baude A., Nusser Z., Molnár E., McIlhinney R.A.J., Somogyi P. High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus. Neuroscience. 69:1995;1031-1055.
2. Boyer C., Schikorsky T., Stevens C.F. Comparison of hippocampal dendritic spines in culture and in brain. J Neurosci. 18:1998;5294-5300.
3. Calverley P.K.S., Jones D.G. A serial section study of perforated synapses in rat neocortex. Cell Tissue Res. 247:1987;565-572.
4. Carlin P.K., Siekevitz P. Plasticity in the central nervous system Do synapses divide? Proc Natl Acad Sci USA. 80:1983;3517-3521.
5. Carroll R.C., Beattie E.C., von Zastrow M., Malenka R.C. Role of AMPA receptor endocytosis in synaptic plasticity. Nat Rev Neurosci. 2:2001;315-324.
6. Cohen R.S., Siekevitz P. Form of the postsynaptic density A serial section study. J Cell Biol. 78:1978;36-46.
7. Desmond N.L., Weinberg R.J. Enhanced expression of AMPA receptor protein at perforated axospinous synapses. Neuroreport. 9:1998;857-860.
8. Dingledine R., Borges K., Bowie D., Traynelis S.F. The glutamate receptor ion channels. Pharmacol Rev. 51:1999;7-61.
9. Dyson S.E., Jones D.G. Synaptic remodeling during development and maturation Junction differentiation and slitting as a mechanisms of modifying connectivity. Dev Brain Res. 13:1984;125-137.
10. Edwards F.A. Anatomy and electrophysiology of fast central synapses lead to a structural model for long-term potentiation. Physiol Rev. 75:1995;759-787.
11. Ganeshina O., Berry R.W., Petralia R.S., Nicholson D.A., Geinisman Y. Differences in the expression of AMPA and NMDA receptors between axospinous perforated and nonperforated synapses are related to the configuration and size of postsynaptic densities. J Comp Neurol. 468:2004;86-95.
12. Geinisman Y. Perforated axospinous synapses with multiple, completely partitioned transmission zones Probable structural intermediates in synaptic plasticity. Hippocampus. 3:1993;417-434.
13. Geinisman Y., DeToledo-Morrell L., Morrell F., Heller R.E., Rossi M., Parshall R.F. Structural synaptic correlate of long-term potentiation Formation of axospinous synapses with multiple, completely partitioned transmission zones. Hippocampus. 3:1993;435-446.
14. Geinisman Y., DeToledo-Morrell L., Morrell F., Persina I.S., Beatty M.A. Synapse restructuring associated with the maintenance phase of hippocampal long-term potentiation. J Comp Neurol. 368:1996;413-423.
15. Geinisman Y., DeToledo-Morrell L., Morrell F., Persina I.S., Rossi M. Structural synaptic plasticity associated with the induction of long-term potentiation is preserved in the dentate gyrus of aged rats. Hippocampus. 2:1992;446-456.
16. Geinisman Y., Ganeshina O., Yoshida R., Berry R.W., Disterhoft J.F., Gallagher M. Aging, spatial learning, and total synapse number in the rat CA1 stratum radiatum. Neurobiol Aging. 25:2004;407-416.
17. Geinisman Y., Gundersen H.J.H., Van der Zee E., West M.J. Unbiased stereological estimation of the total number of synapses in a brain region. J Neurocytol. 25:1996;805-819.
18. Geinisman Y., Morrell F., DeToledo-Morrell L. Axospinous synapses with segmented postsynaptic densities A morphologically distinct synaptic subtype contributing to the number of profiles of 'perforated' synapses visualized in random sections. Brain Res. 423:1987;179-188.
19. Greenough W.T., West R.W., de Voogt T.J. Subsynaptic plate perforations Changes with age and experience in the rat. Science. 202:1978;1096-1098.
20. Harris K.M. Structure, development and plasticity of dendritic spines. Curr Opin Neurobiol. 9:1999;343-348.
21. Harris K.M., Jensen F.E., Tsao B. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages Implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci. 12:1992;2685-2705.
22. 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.
23. Hollmann M., Heineman S. Cloned glutamate receptors. Annu Rev Neurosci. 17:1994;31-108.
24. Lüscher C., Frerking M. Restless AMPA receptors Implications for synaptic transmission and plasticity. Trends Neurosci. 24:2001;665-670.
25. Lüscher C., Nicoll R.A., Malenka R.C., Muller D. Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci. 3:2000;545-550.
26. Lynch G., Baudry M. The biochemistry of memory A new and specific hypothesis. Science. 224:1984;1057-1063.
27. Malenka R.C., Nicoll R.A. Long-term potentiation A decade of progress? Science. 285:1999;1870-1874.
28. Malinow R., Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci. 25:2002;103-126.
29. Matsubara A., Laake J.H., Davanger S., Usamu S., Ottersen O.P. Organization of AMPA receptor subunits at a glutamate synapse A quantitative immunogold analysis of hair cell synapses in the rat organ of corti. J Neurosci. 16:1996;4457-4467.
30. Maxwell S.E., Delaney H.D. Designing experiments and analyzing data A model comparison perspective, 2nd ed. 2004;Lawrence Erlbaum Associates, Mahwah, NJ.
31. Nieto-Sampedro M., Hoff S.W., Cotman C.W. Perforated postsynaptic densities Probable intermediates in synapse turnover. Proc Natl Acad Sci USA. 79:1982;5718-5722.
32. Nimchinsky E.A., Sabatini B.L., Svoboda K. Structure and function of dendritic spines. Annu Rev Physiol. 64:2002;313-353.
33. Nusser Z., Lujan R., Laube G., Roberts J.D.B., Molnar E., Somogyi P. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron. 21:1998;545-559.
34. Peters A., Kaiserman-Abramof I.R. The small pyramidal neuron of the rat cerebral cortex The synapses upon dendritic spines. Z Zellforsch. 100:1969;487-506.
35. Peters A., Kaiserman-Abramof I.R. The small pyramidal neuron of the rat cerebral cortex The perikaryon, dendrites and spines. J Anat. 127:1970;321-356.
36. Petralia R.S., Wenthold R.J. Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol. 318:1992;329-354.
37. Petralia R.S., Wenthold R.J. Immunocytochemistry of NMDA receptors. Li M. Methods in molecular biology: NMDA receptor protocols. 1999;73-92 Humana Press, Totowa, NJ.
38. Petralia R.S., Wang Y.-X., Wenthold R.J. The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J Neurosci. 14:1994;6102-6120.
39. Petralia R.S., Yokotani N., Wenthold R.J. Light and electron-microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective antipeptide antibody. J Neurosci. 14:1994;667-696.
40. Petralia R.S., Esteban J.A., Wang Y.-X., Partridge J.G., Zhao H.-M., Wenthold R.J. Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat Neurosci. 2:1999;31-36.
41. Racca C., Stephenson F.A., Streit P., Roberts J.D.B., Somogyi P. NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J Neurosci. 20:2000;2512-2522.
42. Royet J.-P. Stereology A method for analyzing images. Prog Neurobiol. 37:1991;433-474.
43. Scannevin R.H., Huganir R.L. Postsynaptic organization and regulation of excitatory synapses. Nat Rev Neurosci. 1:2000;133-141.
44. Sheng M., Kim M.J. Postsynaptic signaling and plasticity mechanisms. Science. 298:2002;776-780.
45. Shepherd G.M.G., Harris K.M. Three-dimensional structure and composition of CA3 → CA1 axons in rat hippocampal slices Implications for presynaptic connectivity and compartmentalization. J Neurosci. 18:1998;8300-8310.
46. 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.
47. Shi S.-H., Hayashi Y., Esteban J.A., Malinow R. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell. 105:2001;331-343.
48. Sorra K.E., Harris K.M. Stability in synapse number and size 2 hr after long-term potentiation in hippocampal area CA1. J Neurosci. 18:1998;658-671.
49. Sorra K.E., Fiala J.C., Harris K.M. Critical assessment of the involvement of perforations, spinules and spine branching in hippocampal synapse formation. J Comp Neurol. 398:1998;225-240.
50. Spacek J., Hartman M. Three-dimensional analysis of dendritic spines I. quantitative observations related to dendritic spine and synaptic morphology in cerebral and cerebellar cortices. Anat Embryol. 167:1983;289-310.
51. Stein V., House D.R.C., Bredt D.S., Nicoll R.A. Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression. J Neurosci. 23:2003;5503-5506.
52. Takumi Y., Ramírez-León V., Laake P., Rinvik E., Ottersen O.P. Different models of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci. 2:1999;618-624.
53. Toni N., Buchs P.A., Nikonenko I., Povilatite P., Parisi L., Muller D. Remodeling of synaptic membranes after induction of long-term potentiation. J Neurosci. 21:2001;6245-6251.
54. Turrigiano G.G. AMPA receptors unbound Membrane cycling and synaptic plasticity. Neuron. 26:2000;5-8.
55. Wenthold R.J., Yokotani N., Doj K., Wada K. Immunochemical characterization of the non-NMDA glutamate receptor using subunit-specific antibodies Evidence for a hetero-oligomeric structure in rat brain. J Biol Chem. 267:1992;501-507.
56. Ziff E.B. Recent excitement in the ionotropic glutamate receptor field. Ann NY Acad Sci. 868:1999;465-473.