A dynamin-3 spliced variant modulates the actin/cortactin-dependent morphogenesis of dendritic spines

Journal of Cell Science

Volumn 118, Issue 6, 2005, Pages 1279-1290

  Gray, Noah W ^a,c   Kruchten, Anne E ^b   Chen, Jing ^b   McNiven, Mark A ^a,b  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Actin; Cortactin; Dynamin; Filopodia; Neuron

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; CORTACTIN; DYNAMIN III; GUANOSINE TRIPHOSPHATASE; ISOPROTEIN; MESSENGER RNA;

ANIMAL CELL; ANIMAL TISSUE; ANTIGENIC MODULATION; ARTICLE; BINDING AFFINITY; CELL CULTURE; CELL MATURATION; CULTURE MEDIUM; DENDRITIC SPINE; EMBRYO; ENZYME ACTIVITY; MORPHOGENESIS; NERVE CELL; NERVE CELL GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN VARIANT; RAT; SYNAPTOGENESIS; UPREGULATION;

ACTINS; ALTERNATIVE SPLICING; ANIMALS; BINDING SITES; CORTACTIN; COS CELLS; DENDRITES; DENDRITIC SPINES; DOSE-RESPONSE RELATIONSHIP, DRUG; DYNAMIN III; GREEN FLUORESCENT PROTEINS; GTP PHOSPHOHYDROLASES; HIPPOCAMPUS; IMMUNOPRECIPITATION; MACROMOLECULAR SUBSTANCES; MICROFILAMENT PROTEINS; MICROSCOPY, FLUORESCENCE; NEURONS; PHENOTYPE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, SECONDARY; PSEUDOPODIA; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SYNAPSES; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; UP-REGULATION;

ANIMALIA;

EID: 16244401381     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01711     Document Type: Article

References (52)

1. Brakeman, P. R., Lanahan, A. A., O'Brien, R., Roche, K., Barnes, C. A., Huganir, R. L. and Worley, P. F. (1997). Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 386, 284-288.
2. Cao, H., Garcia, F. and McNiven, M. A. (1998). Differential distribution of dynamin isoforms in mammalian cells. Mol. Biol. Cell 9, 2595-2609.
3. Cao, H., Orth, J. D., Chen, J., Weller, S. G., Heuser, J. E. and McNiven, M. A. (2003). Cortactin is a component of clathrin-coated pits and participates in receptor-mediated endocytosis. Mol. Cell. Biol. 23, 2162-2170.
4. Cook, T. A., Urrutia, R. and McNiven, M. A. (1994). Identification of dynamin 2, an isoform ubiquitously expressed in fat tissues. Proc. Natl. Acad. Sci. USA 91, 644-648.
5. Cook, T., Mesa, K. and Urrutia, R. (1996). Three dynamin-encoding genes are differently expressed in developing rat brain. J. Neurochem. 67, 927-931.
6. Dailey, M. E. and Smith, S. J. (1996). The dynamics of dendritic structure in developing hippocampal slices. J. Neurosci. 16, 2983-2994.
7. Damke, H., Baba, T., Warnock, D. E. and Schmid, S. L. (1994). Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934.
8. Danino, D., Moon, K. H. and Hinshaw, J. E. (2004). Rapid constriction of lipid bilayers by the mechanochemical enzyme dynamin. J. Struct. Biol. 147, 259-267.
9. Du, Y., Weed, S. A., Xiong, W. C., Marshall, T. D. and Parsons, J. T. (1998). Identification of a novel cortactin SH3 domain-binding protein and its localization to growth cones of cultured neurons. Mol. Cell. Biol. 18, 5838-5851.
10. El-Husseini, A. E., Schnell, E., Chetkovich, D. M., Nicoll, R. A. and Bredt, D. S. (2000). PSD-95 involvement in maturation of excitatory synapses. Science 290, 1364-1368.
11. Feng, J., Yan, Z., Ferreira, A., Tomizawa, K., Liauw, J. A., Zhuo, M., Allen, P. B., Ouimet, C. C. and Greengard, P. (2000). Spinophilin regulates the formation and function of dendritic spines. Proc. Natl. Acad. Sci. USA 97, 9287-9292.
12. Fiala, J. C., Feinberg, M., Popov, V. and Harris, K. M. (1998). Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J. Neurosci. 18, 8900-8911.
13. Gray, N. W., Fourgeaud, L., Huang, B., Chen, J., Cao, H., Oswald, B. J., Hemar, A. and McNiven, M. A. (2003). Dynamin 3 is a component of the postsynapse, where it interacts with mGluR5 and Homer. Curr. Biol. 13, 510-515.
14. Guex, N. and Peitsch, M. C. (1997). SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18, 2714-2723.
15. Hayashi, K. and Shirao, T. (1999). Change in the shape of dendritic spines caused by overexpression of drebrin in cultured cortical neurons. J. Neurosci. 19, 3918-3925.
16. Hering, H. and Sheng, M. (2001). Dendritic spines: structure, dynamics and regulation. Nat. Rev. Neurosci. 2, 880-888.
17. Hering, H. and Sheng, M. (2003). Activity-dependent redistribution and essential role of cortactin in dendritic spine morphogenesis. J. Neurosci. 23, 11759-11769.
18. Hering, H., Lin, C. C. and Sheng, M. (2003). Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J. Neurosci. 23, 3262-3271.
19. Hirokawa, N. (1989). The arrangement of actin filaments in the postsynaptic cytoplasm of the cerebellar cortex revealed by quick-freeze deep-etch electron microscopy. Neurosci. Res. 6, 269-275.
20. Hirshberg, M., Stockley, R. W., Dodson, G. and Webb, M. R. (1997). The crystal structure of human rac1, a member of the Rho-family complexed with a GTP analogue. Nat. Struct. Biol. 4 147-152.
21. Huang, C., Ni, Y., Wang, T., Gao, Y., Haudenschild, C. C. and Zhan, X. (1997). Down-regulation of the filamentous actin cross-linking activity of cortactin by Src-mediated tyrosine phosphorylation. J. Biol. Chem. 272, 13911-13915.
22. Itoh, K., Sakakibara, M., Yamasaki, S., Takeuchi, A., Arase, H., Miyazaki, M., Nakajima, N., Okada, M. and Saito, T. (2002). Cutting edge: negative regulation of immune synapse formation by anchoring lipid raft to cytoskeleton through Cbp-EBP50-ERM assembly. J. Immunol. 168, 541-544.
23. Jontes, J. D. and Smith, S. J. (2000). Filopodia, spines, and the generation of synaptic diversity. Neuron 27, 11-14.
24. Krueger, E. W., Orth, J. D., Cao, H. and McNiven, M. A. (2003). A dynamin-cortactin-Arp2/3 complex mediates actin reorganization in growth factor-stimulated cells. Mol. Biol. Cell 14, 1085-1096.
25. Landis, D. M. and Reese, T. S. (1983). Cytoplasmic organization in cerebellar dendritic spines. J. Cell Biol. 97 1169-1178.
26. Lee, E. and de Camilli, P. (2002). Dynamin at actin tails. Proc. Natl. Acad. Sci. USA 99, 161-166.
27. Matus, A. (2000). Actin-based plasticity in dendritic spines. Science 290, 754-758.
28. McNiven, M. A., Kim, L., Krueger, E. W., Orth, J. D., Cao, H. and Wong, T. W. (2000). Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J. Cell Biol. 151, 187-198.
29. Naisbitt, S., Kim, E., Tu, J. C., Xiao, B., Sala, C., Valtschanoff, J., Weinberg, R. J., Worley, P. F. and 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.
30. Nakata, T., Iwamoto, A., Noda, Y., Takemura, R., Yoshikura, H. and Hirokawa, N. (1991). Predominant and developmentally regulated expression of dynamin in neurons. Neuron 7, 461-469.
31. Nakata, T., Takemura, R. and Hirokawa, N. (1993). A novel member of the dynamin family of GTP-binding proteins is expressed specifically in the testis. J. Cell Sci. 105, 1-5.
32. Notredame, C., Higgins, D. G. and Heringa, J. (2000). T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217.
33. Ochoa, G. C., Slepnev, V. I., Neff, L., Ringstad, N., Takei, K., Daniell, L., Kim, W., Cao, H., McNiven, M., Baron, R. et al. (2000). A functional link between dynamin and the actin cytoskeleton at podosomes. J. Cell Biol. 150, 377-390.
34. Orth, J. D. and McNiven, M. A. (2003). Dynamin at the actin-membrane interface. Curr. Opin. Cell Biol. 15, 31-39.
35. Orth, J. D., Krueger, E. W., Cao, H. and McNiven, M. A. (2002). The large GTPase dynamin regulates actin comet formation and movement in living cells. Proc. Natl. Acad. Sci. USA 99, 167-172.
36. Pak, D. T., Yang, S., Rudolph-Correia, S., Kim, E. and Sheng, M. (2001). Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP. Neuron 31, 289-303.
37. Papa, M., Bundman, M. C., Greenberger, V. and Segal, M. (1995). Morphological analysis of dendritic spine development in primary cultures of hippocampal neurons. J. Neurosci. 15, 1-11.
38. Peitsch, M. C. (1995). Protein modeling by E-mail. Biotechnology 13, 658-660.
39. Poirot, O., Suhre, K., Abergel, C., O'Toole, E. and Notredame, C. (2004). 3DCoffee: a web server for mixing sequences and structure into multiple sequence alignments. Nucleic Acids Res. 32, W39-W40.
40. Sala, C., Piech, V., Wilson, N. R., Passafaro, M., Liu, G. and Sheng, M. (2001). Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron 31, 115-130.
41. Schafer, D. A. (2002). Coupling actin dynamics and membrane dynamics during endocytosis. Curr. Opin. Cell Biol. 14 76-81.
42. Schafer, D. A., Weed, S. A., Binns, D., Karginov, A. V. and Cooper, J. A. (2002). Dynamin 2 and cortactin regulate actin assembly and filament organization. Curr. Biol. 12, 1852-1857.
43. Schwede, T., Kopp, J., Guex, N. and Peitsch, M. C. (2003). SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31, 3381-3385.
44. Shupliakov, O., Low, P., Grabs, D., Gad, H., Chen, H., David, C., Takei, K., de Camilli, P. and Brodin, L. (1997). Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276, 259-263.
45. Sontag, J.-M., Fykse, E. M., Ushkaryov, Y., Liu, J.-P., Robinson, P. J. and Sudhof, T. C. (1994). Differential expression and regulation of multiple dynamins. J. Biol. Chem. 269, 4547-4554.
46. Sorra, K. E. and Harris, K. M. (2000). Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus 10, 501-511.
47. Takei, K., Mundigl, O., Daniell, L. and de Camilli, P. (1996). The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J. Cell Biol. 133, 1237-1250.
48. Thompson, H. M., Cao, H., Chen, J., Euteneuer, U. and McNiven, M. A. (2004). Dynamin 2 binds gamma-tubulin and participates in centrosome cohesion. Nat. Cell Biol. 6, 335-342.
49. Src substrate, is a filamentous actin-binding protein enriched in the cell cortex. J. Cell Biol. 120, 1417-1426.
50. Zacharias, D. A., Garamszegi, N. and Strehler, E. E. (1994). Characterization of persistent artifacts resulting from RT-PCR of alternatively spliced mRNAs. BioTechniques 17, 652-655.
51. Zhang, P. and Hinshaw, J. E. (2001). Three-dimensional reconstruction of dynamin in the constricted state. Nat. Cell Biol. 3, 922-926.
52. Ziv, N. E. and Smith, S. J. (1996). Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17, 91-102.