Drebrin-dependent actin clustering in dendritic filopodia governs synaptic targeting of postsynaptic density-95 and dendritic spine morphogenesis

Journal of Neuroscience

Volumn 23, Issue 16, 2003, Pages 6586-6595

  Takahashi, Hideto ^a   Sekino, Yuko ^a,b   Tanaka, Satoshi ^a   Mizui, Toshiyuki ^a   Kishi, Shoji ^a   Shirao, Tomoaki ^a,c  

^a GUNMA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Actin cytoskeleton; Antisense oligonucleotide; Dendritic spine; Drebrin; Hippocampus; Microinjection; Postsynaptic density; Synaptogenesis

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; DREBRIN; DREBRIN A; F ACTIN; GREEN FLUORESCENT PROTEIN; ISOPROTEIN; NERVE PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; DENDRITIC SPINE; EMBRYO; FILOPODIUM; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; MORPHOGENESIS; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; RAT; SYNAPSE; SYNAPTOGENESIS; UPREGULATION;

EID: 0041342023     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-16-06586.2003     Document Type: Article

References (59)

1. 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.
2. Allison DW, Chervin AS, Gelfand VI, Craig AM (2000) Postsynaptic scaffolds of excitatory and inhibitory synapses in hippocampal neurons: maintenance of core components independent of actin filaments and microtubules. J Neurosci 20:4545-4554.
3. Asada H, Uyemura K, Shirao T (1994) Actin-binding protein, drebrin, accumulates in submembranous regions in parallel with neuronal differentiation. J Neurosci Res 38:149-159.
4. Colicos MA, Collins BE, Sailor MJ, Goda Y (2001) Remodeling of synaptic actin induced by photoconductive stimulation. Cell 107:605-616.
5. Dailey ME, Smith SJ (1996) The dynamics of dendritic structure in developing hippocampal slices. J Neurosci 16:2983-2994.
6. DeCamilli P, Cameron R, Greengard P (1983) Synapsin I (protein I), a nerve terminal specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections. J Cell Biol 96:1337-1354.
7. Dunaevsky A, Tashiro A, Majewska A, Mason C, Yuste R (1999) Developmental regulation of spine motility in the mammalian central nervous system. Proc Natl Acad Sci USA 96:13438-13443.
8. El-Husseini AE, Schnell E, Chetkovich DM, Nicoll RA, Bredt DS (2000) PSD-95 involvement in maturation of excitatory synapses. Science 290:1364-1368.
9. El-Husseini AE, Schnell E, Dakoji S, Sweeney N, Zhou Q, Prange O, Gauthier-Campbell C, Aguilera-Moreno A, Nicoll RA, Bredt DS (2002) Synaptic strength regulated by palmitate cycling on PSD-95. Cell 108:849-863.
10. Ethell IM, Irie F, Kalo MS, Couchman JR, Pasquale EB, Yamaguchi Y (2001) EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron 31:1001-1013.
11. Fiala JC, Feinberg M, Popov V, Harris KM (1998) Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci 18:8900-8911.
12. Fifkova E, Delay RJ (1982) Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity. J Cell Biol 95:345-350.
13. Fischer M, Kaech S, Knutti D, Matus A (1998) Rapid actin-based plasticity in dendritic spines. Neuron 20:847-854.
14. Friedman HV, Bresler T, Garner CC, Ziv NE (2000) Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27:57-69.
15. Fucini RV, Navarrete A, Vadakkan C, Lacomis L, Erdjument-Bromage H, Tempst P, Stamnes M (2000) Activated ADP-ribosylation factor assembles distinct pools of actin on Golgi membranes. J Biol Chem 275:18824-18829.
16. Goslin K, Asumussen 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.
17. Hall A (1998) G proteins and small GTPases: distant relatives keep in touch. Science 280:2074-2075.
18. 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.
19. Harris KM (1999) Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol 9:343-348.
20. Harris KM, Kater SB (1994) Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 17:341-371.
21. 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.
22. 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.
23. Hayashi K, Suzuki K, Shirao T (1998) Rapid conversion of drebrin isoforms during synapse formation in primary culture of cortical neurons. Brain Res Dev Brain Res 111:137-141.
24. Ikeda K, Kaub PA, Asada H, Uyemura K, Toya S, Shirao T (1996) Stabilization of adhesion plaques by the expression of drebrin A in fibroblasts. Brain Res Dev Brain Res 91:227-236.
25. Irie F, Yamaguchi Y (2002) EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP. Nat Neurosci 5:1117-1118.
26. 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.
27. Keon BH, Jedrzejewski PT, Paul DL, Goodenough DA (2000) Isoform specific expression of the neuronal F-actin binding protein, drebrin, in specialized cells of stomach and kidney epithelia. J Cell Sci 113:325-336.
28. Luna JE, Pestonjamasp NK, Cheney ER, Stassel PC, Lu HT, Chia PC, Hitt LA, Fechheimer M, Furthmayr H, Mooseker SM (1996) Actin-binding membrane proteins identified by F-actin blot overlays. In: Cytoskeletal regulation of membrane function: society of general physiologists series (Froehner SC, Bennett V, eds), Vol 52, pp 3-18. New York: Rockefeller UP.
29. Maekawa S, Sakai H (1988) Isolation of 110K actin binding protein from mammalian brain and its immunocytochemical localization within cultured cells. Exp Cell Res 178:127-142.
30. Marrs GS, Green SH, Dailey ME (2001) Rapid formation and remodeling of postsynaptic densities in developing dendrites. Nat Neurosci 4:1006-1013.
31. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H (2001) Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4:1086-1092.
32. Matus A (2000) Actin-based plasticity in dendritic spines. Science 290:754-758.
33. Matus A, Ackermann M, Pehling G, Byers HR, Fujiwara K (1982) High actin concentrations in brain dendritic spines and postsynaptic densities. Proc Natl Acad Sci USA 79:7590-7594.
34. McGee AW, Dakoji SR, Olsen O, Bredt DS, Lim WA, Prehoda KE (2001) Structure of the SH3-guanylate kinase module from PSD-95 suggests a mechanism for regulated assembly of MAGUK scaffolding proteins. Mol Cell 8:1291-1301.
35. Meng Y, Zhang Y, Tregoubov V, Janus C, Cruz L, Jackson M, Lu WY, MacDonald JF, Wang JY, Falls DL, Jia Z (2002) Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 35:121-133.
36. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, He Y, Ramsay MF, Morris RG, Morrison JH, O'Dell TJ, Grant SG (1998) Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396:433-439.
37. Nakayama AY, Harms MB, Luo L (2000) Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J Neurosci 20:5329-5338.
38. Okabe S, Miwa A, Okado H (2001) Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J Neurosci 21:6105-6114.
39. Pak DT, Yang S, Rudolph-Correia S, Kim E, Sheng M (2001) Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP. Neuron 31:289-303.
40. Papa M, Bundman MC, Greenberger V, Segal M (1995) Morphological analysis of dendritic spine development in primary cultures of hippocampal neurons. J Neurosci 15:1-11.
41. Peitsch WK, Grund C, Kuhn C, Schnolzer M, Spring H, Schmelz M, Franke WW (1999) Drebrin is a widespread actin-associating protein enriched at junctional plaques, defining a specific microfilament anchorage system in polar epithelial cells. Eur J Cell Biol 78:767-778.
42. Prange O, Murphy TH (2001) Modular transport of postsynaptic density-95 clusters and association with stable spine precursors during early development of cortical neurons. J Neurosci 21:9325-9333.
43. Rao A, Craig AM (2000) Signaling between the actin cytoskeleton and the postsynaptic density of dendritic spines. Hippocampus 10:527-541.
44. 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.
45. Sala C, Piech V, Wilson NR, Passafaro M, Liu G, Sheng M (2001) Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron 31:115-130.
46. Sasaki Y, Hayashi K, Shirao T, Ishikawa R, Kohama K (1996) Inhibition by drebrin of the actin-bundling activity of brain fascin, a protein localized in filopodia of growth cones. J Neurochem 66:980-988.
47. Sheng M, Pak DT (1999) Glutamate receptor anchoring proteins and the molecular organization of excitatory synapses. Ann NY Acad Sci 868:483-493.
48. Shirao T (1995) The roles of microfilament-associated proteins, drebrins, in brain morphogenesis: a review. J Biochem (Tokyo) 117:231-236.
49. Shirao T, Obata K (1985) Two acidic proteins associated with brain development in chick embryo. J Neurochem 44:1210-1216.
50. Shirao T, Obata K (1986) Immunochemical homology of 3 developmentally regulated brain proteins and their developmental change in neuronal distribution. Brain Res 394:233-244.
51. Shirao T, Sekino Y (2001) Clustering and anchoring mechanisms of molecular constituents of postsynaptic scaffolds in dendritic spines. Neurosci Res 40:1-7.
52. Shirao T, Inoue HK, Kano Y, Obata K (1987) Localization of a developmentally regulated neuron-specific protein S54 in dendrites as revealed by immunoelectron microscopy. Brain Res 413:374-378.
53. Shirao T, Kojima N, Kato Y, Obata K (1988) Molecular cloning of a cDNA for the developmentally regulated brain protein, drebrin. Brain Res 464:71-74.
54. Shirao T, Hayashi K, Ishikawa R, Isa K, Asada H, Ikeda K, Uyemura K (1994) Formation of thick, curving bundles of actin by drebrin A expressed in fibroblasts. Exp Cell Res 215:145-153.
55. Togashi H, Abe K, Mizoguchi A, Takaoka K, Chisaka O, Takeichi M (2002) Cadherin regulates dendritic spine morphogenesis. Neuron 35:77-89.
56. Washbourne P, Bennett JE, McAllister AK (2002) Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nat Neurosci 5:751-759.
57. Yuste R, Bonhoeffer T (2001) Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24:1071-1089.
58. Zhang W, Benson DL (2001) Stages of synapse development defined by dependence on F-actin. J Neurosci 21:5169-5181.
59. Ziv NE, Smith SI (1996) Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17:91-102.