Drebrin A is a postsynaptic protein that localizes in vivo to the submembranous surface of dendritic sites forming excitatory synapses

Journal of Comparative Neurology

Volumn 483, Issue 4, 2005, Pages 383-402

  Aoki, Chiye ^a   Sekino, Yuko ^b,c   Hanamura, Kenji ^b   Fujisawa, Sho ^a   Mahadomrongkul, Veeravan ^a   Ren, Yong ^b   Shirao, Tomoaki ^b  

^a NEW YORK UNIVERSITY   (United States)

^b GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Cortex; Electron microscopy; F actin; Hippocampus; NHDA receptor; NR2B; Proto spines; Spinogenesis; Synaptogenesis

Indexed keywords

4 AMINOBUTYRIC ACID; ACTIN; ACTIN BINDING PROTEIN; DREBRIN; DREBRIN A; F ACTIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BRAIN CORTEX; CELL MEMBRANE; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; ELECTRON MICROSCOPY; EXCITATORY SYNAPSE; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; MICROSCOPY; NERVE CELL; NERVE ENDING; NERVE FIBER; NEWBORN; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RAT; SYNAPSE; SYNAPTOGENESIS; WESTERN BLOTTING;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; BRAIN; DENDRITES; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; MICROSCOPY, IMMUNOELECTRON; NEURONS; NEUROPEPTIDES; PRESYNAPTIC TERMINALS; PROTEIN ISOFORMS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC MEMBRANES;

EID: 14644401845     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20449     Document Type: Article

References (58)

1. Aoki C. 1997. Postnatal changes in the laminar and subcellular distribution of NMDA-R1 subunits in the cat visual cortex as revealed by immuno-electron microscopy. Brain Res Dev Brain Res 98:41-59.
2. Aoki C, Venkatesan C, Go CG, Mong JA, Dawson TM. 1994. Cellular and subcellular localization of NMDA-R1 subunit immunoreactivity in the visual cortex of adult and neonatal rats. J Neurosci 14:5202-5222.
3. Aoki C, Rodrigues S, Kurose H. 2000. Use of electron microscopy in the detection of adrenergic receptors. Methods Mol Biol 126:535-563.
4. Aoki C, Miko I, Oviedo H, Mikeladze-Dvali T, Alexandre L, Sweeney N, Bredt DS. 2001. Electron microscopic immunocytochemical detection of PSD-95, PSD-93, SAP-102, and SAP-97 at postsynaptic, presynaptic, and nonsynaptic sites of adult and neonatal rat visual cortex. Synapse 40:239-257.
5. 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.
6. Bonhoeffer T, Yuste R. 2002. Spine motility. Phenomenology, mechanisms, and function. Neuron 35:1019-1027.
7. Butkevich E, Hulsmann S, Wenzel D, Shirao T, Duden R, Majoul I. 2004. Drebrin is a novel connexin-43 binding partner that links gap junctions to the submembrane cytoskeleton. Curr Biol 14:650-658.
8. Crosbie R, Adams S, Chalovich JM, Reisler E. 1991. The interaction of caldesmon with the COOH terminus of actin. J Biol Chem 266:20001-20006.
9. Descarries L. 1991. Non junctional relationships of monoamine axon terminals in the cerebral cortex of adult rat. Volume transmission in the brain: novel mechanisms for neural transmission. Adv Neurosci 1:53-62.
10. Erisir A, Levey AI, Aoki C. 2001. Muscarinic receptor M(2) in cat visual cortex: laminar distribution, relationship to gamma-aminobutyric acidergic neurons, and effect of cingulate lesions. J Comp Neurol 441:168-185.
11. Farb CR, Aoki C, Ledoux JE. 1995. Differential localization of NMDA and AMPA receptor subunits in the lateral and basal nuclei of the amygdala: a light and electron microscopic study. J Comp Neurol 362:86-108.
12. Fox JE. 1985. Identification of actin-binding protein as the protein linking the membrane skeleton to glycoproteins on platelet plasma membranes. J Biol Chem 260:11970-11977.
13. Fritschy JM, Brunig I. 2003. Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol Ther 98:299-323.
14. Fujisawa S, Aoki C. 2003. In vivo blockade of N-methyl-D-aspartate receptors induces rapid trafficking of NR2B subunits away from synapses and out of spines and terminals in adult cortex. Neuroscience 121:51-63.
15. Glenney JR Jr, Glenney P, Weber K. 1982. F-actin-binding and cross-linking properties of porcine brain fodrin, a spectrin-related molecule. J Biol Chem 257:9781-9787.
16. Gould E, Woolley CS, Frankfurt M, McEwen BS. 1990. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10:1286-1291.
17. Harris KM. 1999. Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol 9:343-348.
18. 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.
19. 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.
20. 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.
21. He Y, Janssen WG, Morrison JH. 1998. Synaptic coexistence of AMPA and NMDA receptors in the rat hippocampus: a postembedding immunogold study. J Neurosci Res 54:444-449.
22. Ikeda K, Shirao T, Toda M, Asada H, Toya S, Uyemura K. 1995. Effect of a neuron-specific actin-binding protein, drebrin A, on cell-substratum adhesion. Neurosci Lett 194:197-200.
23. 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.
24. Imamura K, Shirao T, Mori K, Obata K. 1992. Changes of drebrin expression in the visual cortex of the cat during development. Neurosci Res 13:33-41.
25. 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.
26. Jontes JD, Buchanan J, Smith SJ. 2000. Growth cone and dendrite dynamics in zebrafish embryos: early events in synaptogenesis imaged in vivo. Nat Neurosci 3:231-237.
27. Kojima N, Shirao T, Obata K. 1993. Molecular cloning of a developmentally regulated brain protein, chicken drebrin A and its expression by alternative splicing of the drebrin gene. Brain Res Mol Brain Res 19:101-114.
28. Konur S, Yuste R. 2004. Developmental regulation of spine and filopodial motility in primary visual cortex: reduced effects of activity and sensory deprivation. J Neurobiol 59:236-246.
29. Lendvai B, Stern EA, Chen B, Svoboda K. 2000. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404:876-881.
30. Leranth C, Hajszan T, MacLusky NJ. 2004. Androgens increase spine synapse density in the CA1 hippocampal subfield of ovariectomized female rats. J Neurosci 24:495-499.
31. Levy RB, Aoki C. 2002. Alpha7 nicotinic acetylcholine receptors occur at postsynaptic densities of AMPA receptor-positive and -negative excitatory synapses in rat sensory cortex. J Neurosci 22:5001-5015.
32. Majewska A, Sur M. 2003. Motility of dendritic spines in visual cortex in vivo: changes during the critical period and effects of visual deprivation. Proc Natl Acad Sci U S A 100:16024-16029.
33. Marty S, Wehrle R, Alvarez-Leefmans FJ, Gasnier B, Sotelo C. 2002. Postnatal maturation of Na+, K+, 2Cl- cotransporter expression and inhibitory synaptogenesis in the rat hippocampus: an immunocytochemical analysis. Eur J Neurosci 15:233-245.
34. Matus A. 2000. Actin-based plasticity in dendritic spines. Science 290:754-758.
35. Megias M, Emri Z, Freund TF, Gulyas AI. 2001. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102:527-540.
36. Minelli A, Alonso-Nanclares L, Edwards RH, DeFelipe J, Conti F. 2003. Postnatal development of the vesicular GABA transporter in rat cerebral cortex. Neuroscience 117:337-346.
37. Mizutani A, Shiraishi Y, Mikoshiba K, Furuichi T. 1999. Characterization of Cupidin-binding proteins. Soc Neurosci Abst 25:805.807.
38. 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.
39. 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.
40. Peters A. 2002. Examining neocortical circuits: some background and facts. J Neurocytol 31:183-193.
41. Petralia RS, Wenthold RJ. 1992. Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol 318:329-354.
42. Phend KD, Rustioni A, Weinberg RJ. 1995. An osmium-free method of Epon embedment that preserves both ultrastructure and antigenicity for post-embedding immunocytochemistry. J Histochem Cytochem 43: 283-292.
43. Purpura DP, Pappas GD. 1972. Structure and function of synapses. New York: Raven Press.
44. Sal 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.
45. Shirao T. 1995. The roles of microfilament-associated proteins, drebrins, in brain morphogenesis: a review. J Biochem (Tokyo) 117:231-236.
46. Shirao T, Sekino Y. 2001. Clustering and anchoring mechanisms of molecular constituents of postsynaptic scaffolds in dendritic spines. Neurosci Res 40:1-7.
47. Shirao T, Obata K. 1986. Immunochemical homology of 3 developmentally regulated brain proteins and their developmental change in neuronal distribution. Dev Brain Res 29:233-244.
48. 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.
49. 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.
50. Shirao T, Kojima N, Nabeta Y, Obata K. 1989. Two forms of drebrins, developmentally regulated brain proteins, in rat. Proc Jpn Acad 65: 169-172.
51. Shirao T, Kojima N, Obata K. 1992. Cloning of drebrin A and induction of neurite-like processes in drebrin-transfected cells. Neuroreport 3:109-112.
52. 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.
53. Star EN, Kwiatkowski DJ, Murthy VN. 2002. Rapid turnover of actin in dendritic spines and its regulation by activity. Nat Neurosci 5:239-246.
54. Takahashi H, Sekino Y, Tanaka S, Mizui T, Kishi S, Shirao T. 2003. Drebrin-dependent actin clustering in dendritic filopodia governs synaptic targeting of postsynaptic density-95 and dendritic spine morphogenesis. J Neurosci 23:6586-6595.
55. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, Svoboda K. 2002. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420:788-794.
56. Vaughn JE. 1989. Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 3:255-285.
57. Woolley CS, Gould E, Frankfurt M, McEwen BS. 1990. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10:4035-4039.
58. Yamashiro-Matsumura S, Matsumura F. 1985. Purification and characterization of an F-actin-bundling 55-kilodalton protein from HeLa cells. J Biol Chem 260:5087-5097.