Cdc42 and actin control polarized expression of TI-VAMP vesicles to neuronal growth cones and their fusion with the plasma membrane

Molecular Biology of the Cell

Volumn 17, Issue 3, 2006, Pages 1194-1203

  Alberts, Philipp ^a,b,d   Rudge, Rachel ^a,b   Irinopoulou, Theano ^a   Danglot, Lydia ^a,b   Gauthier Rouvière, Cécile ^c   Galli, Thierry ^a,b  

^a INSERM   (France)

^b INSTITUT JACQUES MONOD   (France)

^c CNRS   (France)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CELL ADHESION MOLECULE; F ACTIN; PROTEIN CDC42; PROTEIN TI VAMP; SYNAPTOBREVIN; SYNAPTOBREVIN 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL POLARITY; CONTROLLED STUDY; CYTOSKELETON; EXOCYTOSIS; GROWTH CONE; MEMBRANE TRANSPORT; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL;

ACTINS; ANIMALS; AXONS; CDC42 GTP-BINDING PROTEIN; CELL ADHESION; CELL MEMBRANE; CELL POLARITY; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; EXOCYTOSIS; GROWTH CONES; MEMBRANE FUSION; METALLOENDOPEPTIDASES; PROTEIN TRANSPORT; RATS; RECOMBINANT FUSION PROTEINS; SNARE PROTEINS; TETANUS TOXIN; TRANSPORT VESICLES; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

ANIMALIA;

EID: 33644852316     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-07-0643     Document Type: Article

References (48)

1. Alberts, P., et al. (2003). Cross talk between tetanus neurotoxin-insensitive vesicle-associated membrane protein-mediated transport and L1-mediated adhesion. Mol. Biol. Cell 14, 4207-4220.
2. Allen, W. E., Zicha, D., Ridley, A. J., and Jones, G. E. (1998). A role for Cdc42 in macrophage chemotaxis. J. Cell Biol. 141, 1147-1157.
3. Bradke, F., and Dotti, C. G. (1999). The role of local actin instability in axon formation. Science 283, 1931-1934.
4. Braun, V., Fraisier, V., Raposo, G., Hurbain, I., Sibarita, J. B., Chavrier, P., Galli, T., and Niedergang, F. (2004). TI-VAMP/VAMP7 is required for optimal phagocytosis of opsonised particles in macrophages. EMBO J. 23, 4166-4176.
5. Brown, M. D., Cornejo, B. J., Kuhn, T. B., and Barnburg, J. R. (2000). Cdc42 stimulates neurite outgrowth and formation of growth cone filopodia and lamellipodia. J. Neurobiol. 43, 352-364.
6. Chang, S., and De Camilli, P. (2001). Glutamate regulates actin-based motility in axonal filopodia. Nat. Neurosci. 4, 787-793.
7. Coco, S., Raposo, G., Martinez, S., Fontaine, J. J., Takamori, S., Zahraoui, A., Jahn, R., Matteoli, M., Louvard, D., and Galli, T. (1999). Subcellular localization of tetanus neurotoxin-insensitive vesicle-associated membrane protein (VAMP)/VAMP7 in neuronal cells: evidence for a novel membrane compartment. J. Neurosci. 19, 9803-9812.
8. Cohen, N. R., Taylor, J. S., Scott, L. B., Guillery, R. W., Soriano, P., and Furley, A. J. (1998). Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Curr. Biol. 8, 26-33.
9. da Silva, J. S., and Dotti, C. G. (2002). Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat. Rev. Neurosci. 3, 694-704.
10. Dent, E. W., and Kalil, K. (2001). Axon branching requires interactions between dynamic microtubules and actin filaments. J. Neurosci. 21, 9757-9769.
11. Dickson, B. J. (2002). Molecular mechanisms of axon guidance. Science 298, 1959-1964.
12. Etienne-Manneville, S., and Hall, A. (2001). Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106, 489-498.
13. Filippini, F., Rossi, V., Galli, T., Budillon, A., D'Urso, M., and D'Esposito, M. (2001). Longins: a new evolutionary conserved VAMP family sharing a novel SNARE domain. Trends Biochem. Sci. 26, 407-409.
14. Formstecher, E., et al. (2005). Protein interaction mapping: a Drosophila case study. Genome Res. 15, 376-384.
15. Gasman, S., ChasserotGolaz, S., Malacombe, M., Way, M., and Bader, M. F. (2004). Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments. Mol. Biol. Cell 15, 520-531.
16. Gauthier-Rouviere, C., Vignal, E., Meriane, M., Roux, P., Montcourier, P., and Fort, P. (1998). RhoG GTPase controls a pathway that independently activates Rac1 and Cdc42Hs. Mol. Biol. Cell 9, 1379-1394.
17. Grosse, G., Grosse, J., Tapp, R., Kuchinke, J., Gorsieben, M., Fetter, I., HohneZell, B., Gratzl, M., and Bergmann, M. (1999). SNAP-25 requirement for dendritic growth of hippocampal neurons. J. Neurosci. Res. 56, 539-546.
18. Guirland, C., Suzuki, S., Kojima, M., Lu, B., and Zheng, J. Q. (2004). Lipid rafts mediate chemotropic guidance of nerve growth cones. Neuron 42, 51-62.
19. HongGeller, E., and Cerione, R. A. (2000). Cdc42 and Rac stimulate exocytosis of secretory granules by activating the IP3/calcium pathway in RBL-2H3 mast cells. J. Cell Biol. 148, 481-493.
20. Hoppe, A. D., and Swanson, J. A. (2004). Cdc42, Rac1, and Rac2 display distinct patterns of activation during phagocytosis. Mol. Biol. Cell 15, 3509-3519.
21. Li, Z., Van Aelst, L., and Cline, H. T. (2000). Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo. Nat. Neurosci. 3, 217-225.
22. Lin, C. H., and Forscher, P. (1993). Cytoskeletal remodeling during growth cone-target interactions. J. Cell Biol. 121, 1369-1383.
23. Luo, L., Hensch, T. K., Ackerman, L., Barbel, S., Jan, L. Y., and Jan, Y. N. (1996). Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines. Nature 379, 837-840.
24. Martinez-Arca, S., Alberts, P., Zahraoui, A., Louvard, D., and Galli, T. (2000). Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neunte outgrowth. J. Cell Biol. 149, 889-899.
25. Martinez-Arca, S., Coco, S., Mainguy, G., Schenk, U., Alberts, P., Bouille, P., Mezzina, M., Prochiantz, A., Matteoli, M., Louvard, D., and Galli, T. (2001). A common exocytotic mechanism mediates axonal and dendritic outgrowth. J. Neurosci. 21, 3830-3838.
26. Martinez-Arca, S., Proux-Gillardeaux, V., Alberts, P., Louvard, D., and Galli, T. (2003a). Ectopic expression of syntaxin 1 in the ER redirects TI-VAMP- and cellubrevin-containing vesicles. J. Cell Sci. 116, 2805-2816.
27. Martinez-Arca, S., et al. (2003b). A dual mechanism controlling the localization and function of exocytic v-SNAREs. Proc. Natl. Acad. Sci. USA 100, 9011-9016.
28. May, R. C., and Machesky, L. M. (2001). Phagocytosis and the actin cytoskeleton. J. Cell Sci. 114, 1061-1077.
29. Miesenbock, G., DeAngelis, D. A., and Rothman, J. E. (1998). Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195.
30. Murthy, M., Garza, D., Scheller, R. H., and Schwarz, T. L. (2003). Mutations in the exocyst component Sec5 disrupt neuronal membrane traffic, but neurotransmitter release persists. Neuron 37, 433-447.
31. Muzerelle, A., Alberts, P., Martinez-Arca, S., Jeannequin, O., Lafaye, P., Mazie, J.-C., Galli, T., and Gaspar, P. (2003). Tetanus neurotoxin- insensitive vesicle-associated membrane protein localizes to a presynapric membrane compartment in selected terminal subsets of the rat brain. Neuroscience 122, 59-75.
32. Osen-Sand, A., Staple, J. K., Naldi, E., Schiavo, G., Rossetto, O., Petitpierre, S., Malgaroli, A., Montecucco, C., and Catsicas, S. (1996). Common and distinct fusion proteins in axonal growth and transmitter release. J. Comp. Neurol. 367, 222-234.
33. Rajnicek, A., and McCaig, C. (1997). Guidance of CNS growth cones by substratum grooves and ridges: effects of inhibitors of the cytoskeleton, calcium channels and signal transduction pathways. J. Cell Sci. 110, 2915-2924.
34. Rossi, V., Banfield, D. K., Vacca, M., Dietrich, L. E., Ungermann, C., D'Esposito, M., Galli, T., and Filippini, F. (2004). Longins and their longin domains: regulated SNAREs and multifunctional SNARE regulators. Trends Biochem. Sci. 29, 682-688.
35. Rothman, J. E. (2002). The machinery and principles of vesicle transport in the cell. Nat. Med. 8, 1059-1062.
36. Sabo, S. L., and McAllister, A. K. (2003). Mobility and cycling of synaptic protein-containing vesicles in axonal growth cone filopodia. Nat. Neurosci. 6, 1254-1269.
37. Sandilands, E., Cans, C., Fincham, V. J., Brunton, V. G., Mellor, H., Prendergast, G. C., Norman, J. C., Superti-Furga, G., and Frame, M. C. (2004). RhoB and actin polymerization coordinate Src activation with endosome-mediated delivery to the membrane. Dev. Cell 7, 855-869.
38. Sankaranarayanan, S., DeAngelis, D., Rothman, J. E., and Ryan, T. A. (2000). The use of pHluorins for optical measurements of presynaptic activity. Biophys. J. 79, 2199-2208.
39. Sankaranarayanan, S., and Ryan, T. A. (2000). Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat. Cell Biol. 2, 197-204.
40. Schenk, U., Verderio, C., Benfenati, F., and Matteoli, M. (2003). Regulated delivery of AMPA receptor subunits to the presynaptic membrane. EMBO J. 22, 558-568.
41. Schoch, S., Deak, F., Konigstorfer, A., Mozhayeva, M., Sara, Y., Sudhof, T. C., and Kavalali, E. T. (2001). SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 294, 1117-1122.
42. Schwamborn, J. C., and Puschel, A. W. (2004). The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat. Neurosci. 7, 923-929.
43. Song, H., and Poo, M. (2001). The cell biology of neuronal navigation. Nat. Cell Biol. 3, E81-88.
44. Sudhof, T. C. (2004). The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509-547.
45. Suter, D. M., Errante, L. D., Belotserkovsky, V., and Forscher, P. (1998). The immunoglobulin superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J. Cell Biol. 141, 227-240.
46. Van Aelst, L., and Cline, H. T. (2004). Rho GTPases and activity-dependent dendrite development. Curr. Opin. Neurobiol. 14, 297-304.
47. Yuan, X. B., Jin, M., Xu, X., Song, Y. Q., Wu, C. P., Poo, M. M., and Duan, S. (2003). Signalling and crosstalk of Rho GTPases in mediating axon guidance. Nat. Cell Biol. 5, 38-45.
48. Zheng, J. Q., Wan, J. J., and Poo, M. M. (1996). Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J. Neurosci. 16, 1140-1149.