Home LiteratureArticle Details
PMID: 10844024 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

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

Allison DW, Chervin AS, Gelfand VI, Craig AM

Abstract

The mechanisms responsible for anchoring molecular components of postsynaptic specializations in the mammalian brain are not well understood but are presumed to involve associations with cytoskeletal elements. Here we build on previous studies of neurotransmitter receptors (Allison et al., 1998) to analyze the modes of attachment of scaffolding and signal transducing proteins of both glutamate and GABA postsynaptic sites to either the microtubule or microfilament cytoskeleton. Hippocampal pyramidal neurons in culture were treated with latrunculin A to depolymerize actin, with vincristine to depolymerize microtubules, or with Triton X-100 to extract soluble proteins. The synaptic clustering of PSD-95, a putative NMDA receptor anchoring protein and a core component of the postsynaptic density (PSD), was unaffected by actin depolymerization, microtubule depolymerization, or detergent extraction. The same was largely true for GKAP, a PSD-95-interacting protein. In contrast, the synaptic clustering of Ca(2+)/calmodulin-dependent protein kinase II (CaMKII)alpha, another core component of the PSD, was completely dependent on an intact actin cytoskeleton and was partially disrupted by detergent. Drebrin and alpha-actinin-2, actin-binding proteins concentrated in spines, were also dependent on F-actin for synaptic localization but were unaffected by detergent extraction. Surprisingly, the subcellular distributions of the inhibitory synaptic proteins GABA(A)R and gephyrin, which has a tubulin-binding motif, were unaffected by depolymerization of microtubules or actin or by detergent extraction. These studies reveal an unsuspected heterogeneity in the modes of attachment of postsynaptic proteins to the cytoskeleton and support the idea that PSD-95 and gephyrin may be core scaffolding components independent of the actin or tubulin cytoskeleton.

MeSH Terms
Actins/drug effects,physiology,ultrastructure Animals Bridged Bicyclo Compounds, Heterocyclic/pharmacology Cells, Cultured Disks Large Homolog 4 Protein Evoked Potentials Excitatory Postsynaptic Potentials/physiology Hippocampus/physiology Intracellular Signaling Peptides and Proteins Marine Toxins/pharmacology Membrane Proteins Microtubules/drug effects,physiology,ultrastructure Nerve Tissue Proteins/physiology Neurons/physiology Octoxynol/pharmacology Rats Synapses/physiology Thiazoles/pharmacology Thiazolidines Vincristine/pharmacology
Chemicals
Actins Bridged Bicyclo Compounds, Heterocyclic Disks Large Homolog 4 Protein Dlg4 protein, rat Intracellular Signaling Peptides and Proteins Marine Toxins Membrane Proteins Nerve Tissue Proteins Thiazoles Thiazolidines postsynaptic density proteins Vincristine Octoxynol latrunculin A
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Allison D W
Department of Cell and Structural Biology, University of Illinois, Urbana, Illinois 61801, USA.
Chervin A S
Gelfand V I
Craig A M
References (75)
75 references, click to expand
  1. Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin.
    J Neurosci. 1998 Dec 1;18(23):9835-44 PMID: 9822742
  2. Surface expression of AMPA receptors in hippocampal neurons is regulated by an NSF-dependent mechanism.
    Neuron. 1999 Jun;23(2):365-76 PMID: 10399941
  3. Rat hippocampal neurons in dispersed cell culture.
    Brain Res. 1977 May 13;126(3):397-42 PMID: 861729
  4. GABA(A)-receptor-associated protein links GABA(A) receptors and the cytoskeleton.
    Nature. 1999 Jan 7;397(6714):69-72 PMID: 9892355
  5. Distinct roles for sodium, chloride, and calcium in excitotoxic dendritic injury and recovery.
    Exp Neurol. 1998 Nov;154(1):241-58 PMID: 9875285
  6. A novel neuron-enriched homolog of the erythrocyte membrane cytoskeletal protein 4.1.
    J Neurosci. 1999 Aug 1;19(15):6457-67 PMID: 10414974
  7. Localization of postsynaptic density-93 to dendritic microtubules and interaction with microtubule-associated protein 1A.
    J Neurosci. 1998 Nov 1;18(21):8805-13 PMID: 9786987
  8. CRIPT, a novel postsynaptic protein that binds to the third PDZ domain of PSD-95/SAP90.
    Neuron. 1998 Apr;20(4):693-707 PMID: 9581762
  9. The postsynaptic localization of the glycine receptor-associated protein gephyrin is regulated by the cytoskeleton.
    J Neurosci. 1995 Jun;15(6):4148-56 PMID: 7790902
  10. A method for quantifying F-actin in chemotactic peptide activated neutrophils: study of the effect of tBOC peptide.
    Cell Motil. 1985;5(6):545-57 PMID: 4075387
  11. Neurabin-II/spinophilin. An actin filament-binding protein with one pdz domain localized at cadherin-based cell-cell adhesion sites.
    J Biol Chem. 1998 Feb 6;273(6):3470-5 PMID: 9452470
  12. Dendritic spine changes associated with hippocampal long-term synaptic plasticity.
    Nature. 1999 May 6;399(6731):66-70 PMID: 10331391
  13. Brain myosin-V, a calmodulin-carrying myosin, binds to calmodulin-dependent protein kinase II and activates its kinase activity.
    J Biol Chem. 1999 May 28;274(22):15811-9 PMID: 10336484
  14. Specific visualization of tubulin-containing structures in tissue culture cells by immunofluorescence. Cytoplasmic microtubules, vinblastine-induced paracrystals, and mitotic figures.
    Exp Cell Res. 1975 Oct 1;95(1):111-20 PMID: 172344
  15. Simultaneous localization and quantification of relative G and F actin content: optimization of fluorescence labeling methods.
    J Histochem Cytochem. 1992 Oct;40(10):1605-12 PMID: 1527379
  16. Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation.
    Science. 1999 Apr 2;284(5411):162-6 PMID: 10102820
  17. Interactions of calmodulin and alpha-actinin with the NR1 subunit modulate Ca2+-dependent inactivation of NMDA receptors.
    J Neurosci. 1999 Feb 15;19(4):1165-78 PMID: 9952395
  18. The protein MAP-1B links GABA(C) receptors to the cytoskeleton at retinal synapses.
    Nature. 1999 Jan 7;397(6714):66-9 PMID: 9892354
  19. CaMKIIbeta functions as an F-actin targeting module that localizes CaMKIIalpha/beta heterooligomers to dendritic spines.
    Neuron. 1998 Sep;21(3):593-606 PMID: 9768845
  20. Stimulation of NMDA receptors induces proteolysis of spectrin in hippocampus.
    Brain Res. 1988 Sep 13;460(1):189-94 PMID: 2905922
  21. Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture.
    J Neurosci. 1998 Feb 15;18(4):1217-29 PMID: 9454832
  22. Cytoskeletal dynamics in dendritic spines: direct modulation by glutamate receptors?
    Trends Neurosci. 1999 Jul;22(7):290-5 PMID: 10370249
  23. A role of actin filament in synaptic transmission and long-term potentiation.
    J Neurosci. 1999 Jun 1;19(11):4314-24 PMID: 10341235
  24. Morphology and molecular composition of isolated postsynaptic junctional structures.
    Proc R Soc Lond B Biol Sci. 1978 Dec 4;203(1151):135-51 PMID: 33388
  25. Microtubule associated protein MAP1A is an actin-binding and crosslinking protein.
    Cell Motil Cytoskeleton. 1994;29(2):110-6 PMID: 7820861
  26. Selective clustering of glutamate and gamma-aminobutyric acid receptors opposite terminals releasing the corresponding neurotransmitters.
    Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12373-7 PMID: 7809044
  27. Identification of fodrin as a major calmodulin-binding protein in postsynaptic density preparations.
    J Cell Biol. 1983 Feb;96(2):443-8 PMID: 6833363
  28. Cytoplasmic organization in cerebellar dendritic spines.
    J Cell Biol. 1983 Oct;97(4):1169-78 PMID: 6684661
  29. Alpha 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. 1994 Feb;14(2):611-29 PMID: 8301355
  30. Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors.
    J Neurosci. 1998 Apr 1;18(7):2423-36 PMID: 9502803
  31. The absence of a major Ca2+ signaling pathway in GABAergic neurons of the hippocampus.
    Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3245-50 PMID: 9501248
  32. Postsynaptic mechanisms for bidirectional control of MAP2 phosphorylation by glutamate receptors.
    Neuron. 1996 Feb;16(2):357-68 PMID: 8789950
  33. Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons.
    Neuron. 1997 Oct;19(4):801-12 PMID: 9354327
  34. In situ localization of myosin and actin in dendritic spines with the immunogold technique.
    J Comp Neurol. 1989 Jan 22;279(4):666-74 PMID: 2918091
  35. Volatile anesthetics block actin-based motility in dendritic spines.
    Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10433-7 PMID: 10468626
  36. Immunocytochemical localization of actin in dendritic spines of the cerebral cortex using colloidal gold as a probe.
    Cell Mol Neurobiol. 1985 Sep;5(3):271-84 PMID: 4064076
  37. Targeting of glycine receptor subunits to gephyrin-rich domains in transfected human embryonic kidney cells.
    Mol Cell Neurosci. 1995 Oct;6(5):450-61 PMID: 8581315
  38. Brain spectrin binding to the NMDA receptor is regulated by phosphorylation, calcium and calmodulin.
    EMBO J. 1998 Jul 15;17(14):3931-9 PMID: 9670010
  39. Signal transduction molecules at the glutamatergic postsynaptic membrane.
    Brain Res Brain Res Rev. 1998 May;26(2-3):243-57 PMID: 9651538
  40. The 93-kDa glycine receptor-associated protein binds to tubulin.
    J Biol Chem. 1991 Nov 25;266(33):22242-5 PMID: 1657993
  41. 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. 1997 Feb 10;136(3):669-78 PMID: 9024696
  42. 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. 1998 Jul 27;142(2):485-97 PMID: 9679146
  43. Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice.
    J Neurosci. 1999 Nov 1;19(21):9289-97 PMID: 10531433
  44. SAP102, a novel postsynaptic protein that interacts with NMDA receptor complexes in vivo.
    Neuron. 1996 Aug;17(2):255-65 PMID: 8780649
  45. 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. 1977 Jul;74(1):204-25 PMID: 406264
  46. SAPAPs. A family of PSD-95/SAP90-associated proteins localized at postsynaptic density.
    J Biol Chem. 1997 May 2;272(18):11943-51 PMID: 9115257
  47. MAP2 is localized to the dendrites of hippocampal neurons which develop in culture.
    Brain Res. 1984 Apr;315(2):314-8 PMID: 6722593
  48. Competitive binding of alpha-actinin and calmodulin to the NMDA receptor.
    Nature. 1997 Jan 30;385(6615):439-42 PMID: 9009191
  49. Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated.
    Nat Neurosci. 1999 Oct;2(10):878-83 PMID: 10491607
  50. Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function.
    Annu Rev Neurosci. 1994;17:341-71 PMID: 8210179
  51. Actin in the nervous system.
    Brain Res. 1985 Jun;356(2):187-215 PMID: 3159464
  52. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin.
    Neuron. 1999 Jul;23(3):569-82 PMID: 10433268
  53. Interactions of the C terminus of metabotropic glutamate receptor type 1alpha with rat brain proteins: evidence for a direct interaction with tubulin.
    J Neurochem. 1999 Jan;72(1):346-54 PMID: 9886087
  54. Drebrin, a development-associated brain protein from rat embryo, causes the dissociation of tropomyosin from actin filaments.
    J Biol Chem. 1994 Nov 25;269(47):29928-33 PMID: 7961990
  55. Change in the shape of dendritic spines caused by overexpression of drebrin in cultured cortical neurons.
    J Neurosci. 1999 May 15;19(10):3918-25 PMID: 10234022
  56. Spatial and sub-cellular localization of the membrane cytoskeleton-associated protein alpha-adducin in the rat brain.
    Brain Res. 1995 Nov 27;700(1-2):13-24 PMID: 8624703
  57. Dynamic interaction between soluble tubulin and C-terminal domains of N-methyl-D-aspartate receptor subunits.
    J Neurochem. 1999 Mar;72(3):962-73 PMID: 10037467
  58. Role of actin in the organisation of brain postsynaptic densities.
    Brain Res Mol Brain Res. 1996 Dec 31;43(1-2):246-50 PMID: 9037539
  59. Binding of gamma-aminobutyric acidA receptors to tubulin.
    J Neurochem. 1994 Sep;63(3):1119-25 PMID: 8051553
  60. The postsynaptic density at glutamatergic synapses.
    Trends Neurosci. 1997 Jun;20(6):264-8 PMID: 9185308
  61. Rapid alterations in dendrite morphology during sublethal hypoxia or glutamate receptor activation.
    Neurobiol Dis. 1996;3(3):215-27 PMID: 8980022
  62. Neurabin: a novel neural tissue-specific actin filament-binding protein involved in neurite formation.
    J Cell Biol. 1997 Nov 17;139(4):951-61 PMID: 9362513
  63. Splice variant-specific interaction of the NMDA receptor subunit NR1 with neuronal intermediate filaments.
    J Neurosci. 1998 Jan 15;18(2):720-30 PMID: 9425014
  64. A spatial gradient of tau protein phosphorylation in nascent axons.
    J Neurosci. 1996 Sep 15;16(18):5727-40 PMID: 8795628
  65. The postsynaptic density: constituent and associated proteins characterized by electrophoresis, immunoblotting, and peptide sequencing.
    J Neurochem. 1992 Aug;59(2):667-78 PMID: 1629737
  66. Induction in vitro of microtubular crystals by vinca alkaloids.
    Science. 1969 Aug 1;165(3892):495-6 PMID: 5793242
  67. Clustering of gephyrin at GABAergic but not glutamatergic synapses in cultured rat hippocampal neurons.
    J Neurosci. 1996 May 15;16(10):3166-77 PMID: 8627355
  68. Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin.
    Nat Neurosci. 1998 Nov;1(7):563-71 PMID: 10196563
  69. Characterization of granular particles isolated from postsynaptic densities.
    J Neurochem. 1998 Oct;71(4):1694-701 PMID: 9751204
  70. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95.
    Science. 1995 Sep 22;269(5231):1737-40 PMID: 7569905
  71. Modulatory role of drebrin on the cytoskeleton within dendritic spines in the rat cerebral cortex.
    J Neurosci. 1996 Nov 15;16(22):7161-70 PMID: 8929425
  72. Calmodulin mediates calcium-dependent inactivation of N-methyl-D-aspartate receptors.
    Neuron. 1998 Aug;21(2):443-53 PMID: 9728925
  73. Primary structure and cellular localization of chicken brain myosin-V (p190), an unconventional myosin with calmodulin light chains.
    J Cell Biol. 1992 Dec;119(6):1541-57 PMID: 1469047
  74. Mechanism of Cdc42-induced actin polymerization in neutrophil extracts.
    J Cell Biol. 1998 Aug 24;142(4):1001-12 PMID: 9722612
  75. Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines.
    Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9956-61 PMID: 9275233
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
2000-06-15
Pages
4545-54
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6772458
Subset
IM
Grants
NIGMS NIH HHS · R01 GM052111 · United States
NINDS NIH HHS · R01 NS033184 · United States
NINDS NIH HHS · NS33184 · United States
NIGMS NIH HHS · GM52111-01 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com