Small GTPase Rab17 regulates dendritic morphogenesis and postsynaptic development of hippocampal neurons

Journal of Biological Chemistry

Volumn 287, Issue 12, 2012, Pages 8963-8973

  Mori, Yasunori ^a   Matsui, Takahide ^a   Furutani, Yutaka ^b   Yoshihara, Yoshihiro ^b   Fukuda, Mitsunori ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AXON GROWTH; DENDRITE GROWTH; DENDRITIC GROWTH; DENDRITIC SPINE; GTPASES; HIPPOCAMPAL NEURONS; MEMBRANE TRAFFICKING; MOLECULAR LINKS; MOLECULAR MECHANISM; NEURONAL FUNCTION;

MORPHOLOGY;

NEURONS;

GUANOSINE TRIPHOSPHATASE; RAB17 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL MATURATION; CELL SPECIFICITY; CONTROLLED STUDY; DENDRITIC CELL; EMBRYO; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME LOCALIZATION; ENZYME REGULATION; FILOPODIUM; GROWTH CONE; HIPPOCAMPUS; MEMBRANE TRANSPORT; MORPHOGENESIS; MOUSE; NERVE FIBER; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; POSTSYNAPTIC DEVELOPMENT; PRIORITY JOURNAL; SPINE;

ANIMALS; CELLS, CULTURED; DENDRITES; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MICE; NEURONS; RAB GTP-BINDING PROTEINS; SYNAPSES;

EID: 84858611096     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.314385     Document Type: Article

References (44)

1. Urbanska, M., Blazejczyk, M., and Jaworski, J. (2008) Molecular basis of dendritic arborization. Acta Neurobiol. Exp. 68, 264-288 (Pubitemid 351871143)
2. Yoshihara, Y., De Roo, M., and Muller, D. (2009) Dendritic spine formation and stabilization. Curr. Opin. Neurobiol. 19, 146-153
3. Perin, M. S., Fried, V. A., Mignery, G. A., Jahn, R., and Südhof, T. C. (1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345, 260-263
4. Fei, H., Grygoruk, A., Brooks, E. S., Chen, A., and Krantz, D. E. (2008) Trafficking of vesicular neurotransmitter transporters. Traffic 9, 1425-1436
5. Setou, M., Nakagawa, T., Seog, D. H., and Hirokawa, N. (2000) Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288, 1796-1802 (Pubitemid 30399012)
6. Matsuda, S., Miura, E., Matsuda, K., Kakegawa, W., Kohda, K., Watanabe, M., and Yuzaki, M. (2008) Accumulation of AMPA receptors in autophagosomes in neuronal axons lacking adaptor protein AP-4. Neuron 57, 730-745 (Pubitemid 351335349)
7. Fukuda, M. (2008) Regulation of secretory vesicle traffic by Rab small GTPases. Cell. Mol. Life Sci. 65, 2801-2813
8. Stenmark, H. (2009) Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10, 513-525
9. Fischer von Mollard, G., Mignery, G. A., Baumert, M., Perin, M. S., Hanson, T. J., Burger, P. M., Jahn, R., and Südhof, T. C. (1990) rab3 is a small GTP-binding protein exclusively localized to synaptic vesicles. Proc. Natl. Acad. Sci. U.S.A. 87, 1988-1992
10. Yu, E., Kanno, E., Choi, S., Sugimori, M., Moreira, J. E., Llinás, R. R., and Fukuda, M. (2008) Role of Rab27 in synaptic transmission at the squid giant synapse. Proc. Natl. Acad. Sci. U.S.A. 105, 16003-16008
11. Arimura, N., Kimura, T., Nakamuta, S., Taya, S., Funahashi, Y., Hattori, A., Shimada, A., Ménager, C., Kawabata, S., Fujii, K., Iwamatsu, A., Segal, R. A., Fukuda, M., and Kaibuchi, K. (2009) Anterograde transport of TrkB in axons is mediated by direct interaction with Slp1 and Rab27. Dev. Cell 16, 675-686
12. Gerges, N. Z., Backos, D. S., and Esteban, J. A. (2004) Local control of AMPAreceptor trafficking at the postsynaptic terminal by a small GTPase of the Rab family. J. Biol. Chem. 279, 43870-43878 (Pubitemid 39390694)
13. Park, M., Penick, E. C., Edwards, J. G., Kauer, J. A., and Ehlers, M. D. (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305, 1972-1975 (Pubitemid 39287999)
14. Brown, T. C., Tran, I. C., Backos, D. S., and Esteban, J. A. (2005) NMDA receptor-dependent activation of the small GTPase Rab5 drives the removal of synaptic AMPA receptors during hippocampal LTD. Neuron 45, 81-94 (Pubitemid 40075351)
15. Park, M., Salgado, J. M., Ostroff, L., Helton, T. D., Robinson, C. G., Harris, K. M., and Ehlers, M. D. (2006) Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52, 817-830 (Pubitemid 44828451)
16. Brown, T. C., Correia, S. S., Petrok, C. N., and Esteban, J. A. (2007) Functional compartmentalization of endosomal trafficking for the synaptic delivery of AMPA receptors during long-term potentiation. J. Neurosci. 27, 13311-13315 (Pubitemid 350220476)
17. Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., Müller, S. A., Rammner, B., Gräter, F., Hub, J. S., De Groot, B. L., Mieskes, G., Moriyama, Y., Klingauf, J., Grubmüller, H., Heuser, J., Wieland, F., and Jahn, R. (2006) Molecular anatomy of a trafficking organelle. Cell 127, 831-846 (Pubitemid 44716256)
18. Grønborg, M., Pavlos, N. J., Brunk, I., Chua, J. J., Münster-Wandowski, A., Riedel, D., Ahnert-Hilger, G., Urlaub, H., and Jahn, R. (2010) Quantitative comparison of glutamatergic and GABAergic synaptic vesicles unveils selectivity for few proteins including MAL2, a novel synaptic vesicle protein. J. Neurosci. 30, 2-12
19. 2+-dependent secretion in PC12 cells. J. Biol. Chem. 277, 4601-4604
20. Fukuda, M., and Mikoshiba, K. (1999) A novel alternatively spliced variant of synaptotagmin VI lacking a transmembrane domain. Implications for distinct functions of the two isoforms. J. Biol. Chem. 274, 31428-31434
21. Tsuboi, T., and Fukuda, M. (2006) Rab3A and Rab27A cooperatively regulate the docking step of dense-core vesicle exocytosis in PC12 cells. J. Cell Sci. 119, 2196-2203 (Pubitemid 43960309)
22. Fukuda, M., Aruga, J., Niinobe, M., Aimoto, S., and Mikoshiba, K. (1994) Inositol-1,3,4,5-tetrakisphosphate binding to C2B domain of IP4BP/synaptotagmin II. J. Biol. Chem. 269, 29206-29211 (Pubitemid 24366775)
23. Kuroda, T. S., and Fukuda, M. (2004) Rab27A-binding protein Slp2-a is required for peripheral melanosome distribution and elongated cell shape in melanocytes. Nat. Cell Biol. 6, 1195-1203 (Pubitemid 39625118)
24. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K., and Pease, L. R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59 (Pubitemid 19125653)
25. Hara, T., and Miyajima, A. (1992) Two distinct functional high affinity receptors for mouse interleukin-3 (IL-3). EMBO J. 11, 1875-1884
26. Okabe, S., Kim, H. D., Miwa, A., Kuriu, T., and Okado, H. (1999) Continual remodeling of postsynaptic density and its regulation by synaptic activity. Nat. Neurosci. 2, 804-811 (Pubitemid 30491173)
27. Matsuno, H., Okabe, S., Mishina, M., Yanagida, T., Mori, K., and Yoshihara, Y. (2006) Telencephalin slows spine maturation. J. Neurosci. 26, 1776-1786 (Pubitemid 43236990)
28. Itoh, T., Satoh, M., Kanno, E., and Fukuda, M. (2006) Screening for target Rabs of TBC (Tre-2/Bub2/Cdc16) domain-containing proteins based on their Rab-binding activity. Genes Cells 11, 1023-1037 (Pubitemid 44256383)
29. Tamura, K., Ohbayashi, N., Maruta, Y., Kanno, E., Itoh, T., and Fukuda, M. (2009) Varp is a novel Rab32/38-binding protein that regulates Tyrp1 trafficking in melanocytes. Mol. Biol. Cell 20, 2900-2908
30. Furutani, Y., Matsuno, H., Kawasaki, M., Sasaki, T., Mori, K., and Yoshihara, Y. (2007) Interaction between telencephalin and ERM family proteins mediates dendritic filopodia formation. J. Neurosci. 27, 8866-8876 (Pubitemid 47292762)
31. Ibata, K., Hashikawa, T., Tsuboi, T., Terakawa, S., Liang, F., Mizutani, A., Fukuda, M., and Mikoshiba, K. (2002) Non-polarized distribution of synaptotagmin IV in neurons. Evidence that synaptotagmin IV is not a synaptic vesicle protein. Neurosci. Res. 43, 401-406 (Pubitemid 34828240)
32. 2+/calmodulin-dependent protein kinase CLICK-III/CaMKIγ. Neuron 54, 755-770
33. Meijering, E., Jacob, M., Sarria, J. C., Steiner, P., Hirling, H., and Unser, M. (2004) Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58, 167-176 (Pubitemid 38509178)
34. Malgaroli, A., Ting, A. E., Wendland, B., Bergamaschi, A., Villa, A., Tsien, R. W., and Scheller, R. H. (1995) Presynaptic component of long-term potentiation visualized at individual hippocampal synapses. Science 268, 1624-1628
35. Fukuda, M. (2010) How can mammalian Rab small GTPases be comprehensively analyzed? Development of new tools to comprehensively analyze mammalian Rabs in membrane traffic. Histol. Histopathol. 25, 1473-1480
36. Hunziker, W., and Peters, P. J. (1998) Rab17 localizes to recycling endosomes and regulates receptor-mediated transcytosis in epithelial cells. J. Biol. Chem. 273, 15734-15741 (Pubitemid 28298193)
37. Zacchi, P., Stenmark, H., Parton, R. G., Orioli, D., Lim, F., Giner, A., Mellman, I., Zerial, M., and Murphy, C. (1998) Rab17 regulates membrane trafficking through apical recycling endosomes in polarized epithelial cells. J. Cell Biol. 140, 1039-1053 (Pubitemid 28128865)
38. Beaumont, K. A., Hamilton, N. A., Moores, M. T., Brown, D. L., Ohbayashi, N., Cairncross, O., Cook, A. L., Smith, A. G., Misaki, R., Fukuda, M., Taguchi, T., Sturm, R. A., and Stow, J. L. (2011) The recycling endosome protein Rab17 regulates melanocytic filopodia formation and melanosome trafficking. Traffic 12, 627-643
39. 2+/calmodulin-dependent protein kinase in rat brain. J. Neurosci. 5, 3270-3277
40. Saito, Y., Murakami, F., Song, W. J., Okawa, K., Shimono, K., and Katsumaru, H. (1992) Developing corticorubral axons of the cat form synapses on filopodial dendritic protrusions. Neurosci. Lett. 147, 81-84
41. Ziv, N. E., and Smith, S. J. (1996) Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17, 91-102 (Pubitemid 26251594)
42. Halpain, S. (2000) Actin and the agile spine. How and why do dendritic spines dance? Trends Neurosci. 23, 141-146
43. Pfenninger, K. H. (2009) Plasma membrane expansion. A neuron's Herculean task. Nat. Rev. Neurosci. 10, 251-261
44. Dailey, M. E., and Smith, S. J. (1996) The dynamics of dendritic structure in developing hippocampal slices. J. Neurosci. 16, 2983-2994 (Pubitemid 26121841)