Postsynaptic scaffolds of excitatory and inhibitory synapses in hippocampal neurons: Maintenance of core components independent of actin filaments and microtubules

Journal of Neuroscience

Volumn 20, Issue 12, 2000, Pages 4545-4554

  Allison, Daniel W ^a   Chervin, Adam S ^a   Gelfand, Vladimir I ^a   Craig, Ann Marie ^a,b  

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

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin; CaMKII ; Drebrin; GABA receptor; Gephyrin; GKAP; Microtubules; Postsynaptic density; PSD 95; actinin 2

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; ACTIN; ACTIN BINDING PROTEIN; ALPHA ACTININ; DETERGENT; DREBRIN; F ACTIN; GEPHYRIN; GLUTAMIC ACID; LATRUNCULIN A; NEUROTRANSMITTER RECEPTOR; PROTEIN KINASE (CALCIUM,CALMODULIN) II; TRITON X 100; VINCRISTINE;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE;

EID: 0034659732     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-12-04545.2000     Document Type: Article

References (77)

1. Adam G, Matus A (1996) Role of actin in the organisation of brain postsynaptic densities. Brain Res Mol Brain Res 43:246-250.
2. Allen PB, Ouimet CC, Greengard P (1997) Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc Natl Acad Sci USA 94:9956-9961.
3. Allison DW, Gelfand VI, Spector I, Craig AM (1998) Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J Neurosci 18:2423-2436.
4. Banker GA, Cowan WM (1977) Rat hippocampal neurons in dispersed cell culture. Brain Res 126:397-442.
5. Bensch KG, Marantz R, Wisniewski H, Shelanski M (1969) Induction in vitro of microtubular crystals by vinca alkaloids. Science 165:495-496.
6. Blomberg F, Cohen RS, Sickevitz P (1977) The structure of postsynaptic densities isolated from dog cerebral cortex. II. Characterization and arrangement of some of the major proteins within the structure. J Cell Biol 74:204-225.
7. Brcnman JE, Topinka JR, Cooper EC, McGee AW, Rosen J, Milroy T, Ralston HJ, Bredt DS (1998) Localization of postsynaptic density-93 to dendritic microtubules and interaction with microtubule-associated protein 1A. J Neurosci 18:8805-8813.
8. Caceres A, Banker G, Steward O, Binder L, Payne M (1984) MAP2 is localized to the dendrites of hippocampal neurons which develop in culture. Brain Res 315:314-318.
9. Carlin RK, Bartelt DC, Siekevitz P (1983) Identification of fodrin as a major calmodulin-binding protein in postsynaptic density preparations. J Cell Biol 96:443-448.
10. Ciruela F, Robbins MJ, Willis AC, McIlhinney RA (1999) Interactions of the C terminus of metabotropic glutamate receptor type 1α with rat brain proteins: evidence for a direct interaction with tubulin. J Neurochem 72:346-354.
11. Cohen RS, Chung SK, Pfaff DW (1985) Immunocytochemical localization of actin in dendritic spines of the cerebral cortex using colloidal gold as a probe. Cell Mol Neurobiol 5:271-284.
12. Costa MC, Mani F, Santoro Jr W, Espreafico EM, Larson RE (1999) Brain myosin-V, a calmodulin-carrying myosin, binds to calmodulin-dependent protein kinase II and activates its kinase activity. J Biol Chem 274:15811-15819.
13. Craig AM, Blackstone CD, Huganir RL, Banker G (1994) Selective clustering of glutamate and γ-aminobutyric acid receptors opposite terminals releasing the corresponding neurotransmitters. Proc Natl Acad Sci USA 91:12373-12377.
14. Craig AM, Banker G, Chang W, McGrath ME, Serpinskaya AS (1996) Clustering of gephyrin at GABAergic but not glutamatergic synapses in cultured rat hippocampal neurons. J Neurosci 16:3166-3177.
15. Ehlers MD, Fung ET, O'Brien RJ, Huganir RL (1998) Splice variant-specific interaction of the NMDA receptor subunit NR1 with neuronal intermediate filaments. J Neurosci 18:720-730.
16. Engert F, Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399:66-70.
17. Espreafico EM, Cheney RE, Matteoli M, Nascimento AA, De Camilli PV, Larson RE, Mooseker MS (1992) Primary structure and cellular localization of chicken brain myosin-V (p190), an unconventional myosin with calmodulin light chains. J Cell Biol 119:1541-1557.
18. A receptor subtypes requires the γ2 subunit and gephyrin. Nat Ncurosci 1:563-571.
19. Fifková E (1985) Actin in the nervous system. Brain Res 356:187-215.
20. Goslin K, Asmussen H, Banker G (1998) Rat hippocampal neurons in low density culture. In: Culturing nerve cells (Banker G, Goslin K, eds), pp 339-370. Cambridge, MA: MIT.
21. Halpain S, Hipolito A, Saffer L (1998) Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin. J Neurosci 18:9835-9844.
22. c receptors to the cytoskeleton at retinal synapses. Nature 397:66-69.
23. Harris KM, Kater SB (1994) Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 17:341-371.
24. Hasbani MJ, Hyre KL, Faddis BT, Romano C, Goldberg MP (1998) Distinct roles for sodium, chloride, and calcium in excitotoxic dendritic injury and recovery. Exp Neurol 154:241-258.
25. Hayashi K, Shirao T (1999) Change in the shape of dendritic spines caused by overexpression of drebrin in cultured cortical neurons. J Neurosci 19:3918-3925.
26. Hayashi K, Ishikawa R, Ye LH, He XL, Takata K, Kohama K, Shirao T (1996) Modulatory role of drebrin on the cytoskeleton within dendritic spines in the rat cerebral cortex. J Neurosci 16:7161-7170.
27. Howard TH, Oresajo CO (1985) A method for quantifying F-actin in chemotactic peptide activated ncutrophils: study of the effect of tBOC peptide. Cell Motil 5:545-557.
28. Ishikawa R, Hayashi K, Shirao T, Xue Y, Takagi T, Sasaki Y, Kohama K (1994) Drebrin, a development-associated brain protein from rat embryo, causes the dissociation of tropomyosin from actin filaments. J Biol Chem 269:29928-29933.
29. A receptors to tubulin. J Neurochem 63:1119-1125.
30. Jones EG, Huntley GW, Benson DL (1994) α calcium/calmodulin-dependent protein kinase II selectively expressed in a subpopulation of excitatory neurons in monkey sensory-motor cortex: comparison with GAD-67 expression. J Neurosci 14:611-629.
31. Kacch S, Brinkhaus H, Matus A (1999) Volatile anesthetics block actin-based motility in dendritic spines. Proc Natl Acad Sci USA 96:10433-10437.
32. Kennedy MB (1997) The postsynaptic density at glutamatergic synapses. Trends Neurosci 20:264-268.
33. Kennedy MB (1998) Signal transduction molecules at the glutamatergic postsynaptic membrane. Brain Res Brain Res Rev 26:243-257.
34. Kim CH, Lisman JE (1999) A role of actin filament in synaptic transmission and long-term potentiation. J Neurosci 19:4314-4324.
35. Kim E, Naisbitt S, Hsuch YP, Rao A, Rothschild A, Craig AM, Sheng M (1997) GKAP, a novel synaptic protein that interacts with the guanylate kinase-like domain of the PSD-95/SAP90 family of channel clustering molecules. J Cell Biol 136:669-678.
36. Kirov SA, Harris KM (1999) Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated. Nat Neurosci 2:878-883.
37. Kirsch J, Betz H (1995) The postsynaptic localization of the glycine receptor-associated protein gephyrin is regulated by the cytoskeleton. J Neurosci 15:4148-4156.
38. Kirsch J, Langosch D, Prior P, Littauer UZ, Schmitt B, Betz H (1991) The 93-kDa glycine receptor-associated protein binds to tubulin. J Biol Chem 266:22242-22245.
39. Kirsch J, Kuhse J, Betz H (1995) Targeting of glycine receptor subunits to gephyrin-rich domains in transfected human embryonic kidney cells. Mol Cell Neurosci 6:450-461.
40. A receptor clustering in gephyrin-deficient mice. J Neurosci 19:9289-9297.
41. Knowles GC, McCulloch CA (1992) Simultaneous localization and quantification of relative G and F actin content: optimization of fluorescence labeling methods. J Histochem Cytochem 40:1605-1612.
42. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH (1995) Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269:1737-1740.
43. 2+-dependent inactivation of NMDA receptors. J Neurosci 19:1165-1178.
44. Lai SL, Ling SC, Kuo LH, Shu YC, Chow WY, Chang YC (1998) Characterization of granular particles isolated from postsynaptic densities. J Neurochem 71:1694-1701.
45. Landis DM, Reese TS (1983) Cytoplasmic organization in cerebellar dendritic spines. J Cell Biol 97:1169-1178.
46. Mandell JW, Banker GA (1996) A spatial gradient of tau protein phosphorylation in nascent axons. J Neurosci 16:5727-5740.
47. Matsuoka Y, Li X, Bennett V (1998) Adducin is an in vivo substrate for protein kinase C: phosphorylation in the MARCKS-related domain inhibits activity in promoting spectrin-actin complexes and occurs in many cells, including dendritic spines of neurons. J Cell Biol 142:485-497.
48. Matus AI, Taff-Jones DH (1978) Morphology and molecular composition of isolated postsynaptic junctional structures. Proc R Soc Lond B Biol Sci 203:135-151.
49. Morales M, Fifková E (1989) In situ localization of myosin and actin in dendritic spines with the immunogold technique. J Comp Neurol 279:666-674.
50. Müller BM, Kistner U, Kindler S, Chung WJ, Kuhlendahl S, Fenster SD, Lau LF, Veh RW, Huganir RL, Gundelfinger ED, Garner CC (1996) SAP102, a novel postsynaptic protein that interacts with NMDA receptor complexes in vivo. Neuron 17:255-265.
51. Naisbitt S, Kim E, Tu JC, Xiao B, Sala C, Valtschanoff J, Weinberg RJ, Worley PF, Sheng M (1999) Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron 23:569-582.
52. Nakanishi H, Obaishi H, Satoh A, Wada M, Mandai K, Satoh K, Nishioka H, Matsuura Y, Mizoguchi A, Takai Y (1997) Neurabin: a novel neural tissue-specific actin filament-binding protein involved in neurite formation. J Cell Biol 139:951-961.
53. Niethammer M, Valtschanoff JG, Kapoor TM, Allison DW, Weinberg TM, Craig AM, Sheng M (1998) CRIPT, a novel postsynaptic protein that binds to the third PDZ domain of PSD-95/SAP90. Neuron 20:693-707.
54. Noel J, Ralph GS, Pickard L, Williams J, Molnar E, Uney JB, Collingridge GL, Henley JM (1999) Surface expression of AMPA receptors in hippocampal neurons is regulated by an NSF-dependent mechanism. Neuron 23:365-376.
55. Park JS, Bateman MC, Goldberg MP (1996) Rapid alterations in dendrite morphology during sublethal hypoxia or glutamate receptor activation. Neurobiol Dis 3:215-227.
56. Pedrotti B, Colombo R, Islam K (1994) Microtubule associated protein MAP1A is an actin-binding and crosslinking protein. Cell Motil Cytoskeleton 29:110-116.
57. Peters A, Palay SL, Webster H (1991) Synapses. In: The fine structure of the nervous system: neurons and their supporting cells, pp 138-211. New York: Oxford UP.
58. Quinlan EM, Halpain S (1996) Postsynaptic mechanisms for bidirectional control of MAP2 phosphorylation by glutamate receptors. Neuron 16:357-368.
59. Rao A, Craig AM (1997) Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron 19:801-812.
60. Rao A, Kim E, Sheng M, Craig AM (1998) Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J Neurosci 18:1217-1229.
61. Satoh A, Nakanishi H, Obaishi H, Wada M, Takahashi K, Satoh K, Hirao K, Nishioka H, Hata Y, Mizoguchi A, Takai Y (1998) Neurabin-II/ spinophilin. An actin filament-binding protein with one PDZ domain localized at cadherin-based cell-cell adhesion sites. J Biol Chem 273:3470-3475.
62. Seidel B, Zuschratter W, Wex H, Garner CC, Gundelfinger ED (1995) Spatial and sub-cellular localization of the membrane cytoskeleton-associated protein α-adducin in the rat brain. Brain Res 700:13-24.
63. Seubert P, Larson J, Oliver M, Jung MW, Baudry M, Lynch G (1988) Stimulation of NMDA receptors induces proteolysis of spectrin in hippocampus. Brain Res 460:189-194.
64. Shen K, Meyer T (1999) Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Science 284:162-166.
65. Shen K, Teruel MN, Subramanian K, Meyer T (1998) CaMKIIβ functions as an F-actin targeting module that localizes CaMKIIα/β heterooligomers to dendritic spines. Neuron 21:593-606.
66. 2+ signaling pathway in GABAerg c neurons of the hippocampus. Proc Natl Acad Sci USA 95:3245-3250.
67. Takeuchi M, Hata Y, Hirao K, Toyoda A, Irie M, Takai Y (1997) SAPAPs. A family of PSD-95/SAP90-associated proteins localized at postsynaptic density. J Biol Chem 272:11943-11951.
68. van Rossum D, Hanisch UK (1999) Cytoskeletal dynamics in dendritic spines: direct modulation by glutamate receptors? Trends Neurosci 22:290-295.
69. van Rossum D, Kuhse J, Betz H (1999) Dynamic interaction between soluble tubulin and C-terminal domains of N-methyl-D-aspartate receptor subunits. J Neurochem 72:962-973.
70. Walensky LD, Blackshaw S, Liao D, Watkins CC, Weier HU, Parra M, Huganir RL, Conboy JG, Mohandas N, Snyder SH (1999) A novel neuron-enriched homolog of the erythrocyte membrane cytoskeletal protein 4.1. J Neurosci 19:6457-6467.
71. Walsh MJ, Kuruc N (1992) The postsynapt c density: constituent and associated proteins characterized by electrophoresis, immunoblotting, and peptide sequencing. J Neurochem 59:657-678.
72. A receptors and the cytoskeleton. Nature 397:69-72.
73. Weber K, Bibring T, Osborn M (1975) Specific visualization of tubulin-containing structures in tissue culture cels by immunofluorescence. Cytoplasmic microtubules, vinblastine-induced paracrystals, and mitotic figures. Exp Cell Res 95:111-120.
74. Wechsler A, Teichberg VI (1998) Brain spectrin binding to the NMDA receptor is regulated by phosphorylation, calcium and calmodulin. EMBO J 17:3931-3939.
75. Wyszynski M, Lin J, Rao A, Nigh E, Beggs AH, Craig AM, Sheng M (1997) Competitive binding of α-actinin and calmodulin to the NMDA receptor. Nature 385:439-442.
76. Zhang S, Ehlers MD, Bernhardt JP, Su CT Huganir RL (1998) Calmodulin mediates calcium-dependent inactivation of N-methyl-D-aspartate receptors. Neuron 21:443-453.
77. Zigmond SH, Joyce M, Yang C, Brown K, Huang M, Pring M (1998) Mechanism of Cdc42-induced actin polymerization in neutrophil extracts. J Cell Biol 142:1001-1012.