Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release

doi:10.1083/jcb.200211087

Published 12 May 2003. doi:10.1083/jcb.200211087

This Article

	Full Text
	PDF (Full Text)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Wucherpfennig, T.
	Articles by González-Gaitán, M.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Wucherpfennig, T.
	Articles by González-Gaitán, M.


Social Bookmarking

	What's this?

© The Rockefeller University Press, 0021-9525/2003/5/609 $5.00
The Journal of Cell Biology, Volume 161, Number 3, 609-624

Article

Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release

Tanja Wucherpfennig¹^,2, Michaela Wilsch-Bräuninger¹ and Marcos González-Gaitán¹^,2

¹ Max-Planck Institut für Molekulare Zellbiologie und Genetik, D-01307 Dresden, Germany
² Max-Planck Institut für Biophysikalische Chemie, D-37077 Göttingen, Germany

Address correspondence to Marcos González-Gaitán, Max-Planck Institute, Pfotenhauerstrasse 108, Dresden, D-01307 Germany. Tel.: 49-551-210-2539. Fax: 49-551-210-1389. E-mail: gonzalez{at}mpi-cbg.de

During constitutive endocytosis, internalized membrane trafficsthrough endosomal compartments. At synapses, endocytosis ofvesicular membrane is temporally coupled to action potential–inducedexocytosis of synaptic vesicles. Endocytosed membrane may immediatelybe reused for a new round of neurotransmitter release withouttrafficking through an endosomal compartment. Using GFP-taggedendosomal markers, we monitored an endosomal compartment inDrosophila neuromuscular synapses. We showed that in conditionsin which the synaptic vesicles pool is depleted, the endosomeis also drastically reduced and only recovers from membranederived by dynamin-mediated endocytosis. This suggests thatmembrane exchange takes place between the vesicle pool and thesynaptic endosome. We demonstrate that the small GTPase Rab5is required for endosome integrity in the presynaptic terminal.Impaired Rab5 function affects endo- and exocytosis rates anddecreases the evoked neurotransmitter release probability. Conversely,Rab5 overexpression increases the release efficacy. Therefore,the Rab5-dependent trafficking pathway plays an important rolefor synaptic performance.

Key Words: neuromuscular junction; FYVE domain; small GTPase; shibire; dynamin

^* Abbreviations used in this paper: [Ca²⁺]e, external Ca²⁺ concentration;CNS, central nervous system; CSP, cystein string protein; LTR,long terminal repeat; mEJP, miniature excitatory junction potential;NMJ, neuromuscular junction; NT, neurotransmitter; PI(3), phosphatidylinositol-3;PI(3)P, PI(3)-phosphate; PNS, peripheral nervous system; SV,synaptic vesicles.

Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

This article has been cited by other articles:

Chang, W.-L., Liou, W., Pen, H.-C., Chou, H.-Y., Chang, Y.-W., Li, W.-H., Chiang, W., Pai, L.-M. (2008). The gradient of Gurken, a long-range morphogen, is directly regulated by Cbl-mediated endocytosis. Development 135: 1923-1933 [Abstract] [Full Text]
Juhasz, G., Hill, J. H., Yan, Y., Sass, M., Baehrecke, E. H., Backer, J. M., Neufeld, T. P. (2008). The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J. Cell Biol. 181: 655-666 [Abstract] [Full Text]
Ravikumar, B., Imarisio, S., Sarkar, S., O'Kane, C. J., Rubinsztein, D. C. (2008). Rab5 modulates aggregation and toxicity of mutant huntingtin through macroautophagy in cell and fly models of Huntington disease. J. Cell Sci. 121: 1649-1660 [Abstract] [Full Text]
Ly, C. V., Yao, C.-K., Verstreken, P., Ohyama, T., Bellen, H. J. (2008). straightjacket is required for the synaptic stabilization of cacophony, a voltage-gated calcium channel {alpha}1 subunit. J. Cell Biol. 181: 157-170 [Abstract] [Full Text]
Tanaka, T., Nakamura, A. (2008). The endocytic pathway acts downstream of Oskar in Drosophila germ plasm assembly. Development 135: 1107-1117 [Abstract] [Full Text]
Vaccari, T., Lu, H., Kanwar, R., Fortini, M. E., Bilder, D. (2008). Endosomal entry regulates Notch receptor activation in Drosophila melanogaster. J. Cell Biol. 180: 755-762 [Abstract] [Full Text]
Korolchuk, V. I., Schutz, M. M., Gomez-Llorente, C., Rocha, J., Lansu, N. R., Collins, S. M., Wairkar, Y. P., Robinson, I. M., O'Kane, C. J. (2007). Drosophila Vps35 function is necessary for normal endocytic trafficking and actin cytoskeleton organisation. J. Cell Sci. 120: 4367-4376 [Abstract] [Full Text]
Dyer, N., Rebollo, E., Dominguez, P., Elkhatib, N., Chavrier, P., Daviet, L., Gonzalez, C., Gonzalez-Gaitan, M. (2007). Spermatocyte cytokinesis requires rapid membrane addition mediated by ARF6 on central spindle recycling endosomes. Development 134: 4437-4447 [Abstract] [Full Text]
Vardjan, N., Stenovec, M., Jorgacevski, J., Kreft, M., Zorec, R. (2007). Elementary properties of spontaneous fusion of peptidergic vesicles: fusion pore gating. J. Physiol. 585: 655-661 [Abstract] [Full Text]
Devergne, O., Ghiglione, C., Noselli, S. (2007). The endocytic control of JAK/STAT signalling in Drosophila. J. Cell Sci. 120: 3457-3464 [Abstract] [Full Text]
Blankenship, J. T., Fuller, M. T., Zallen, J. A. (2007). The Drosophila homolog of the Exo84 exocyst subunit promotes apical epithelial identity. J. Cell Sci. 120: 3099-3110 [Abstract] [Full Text]
Uzan-Gafsou, S., Bausinger, H., Proamer, F., Monier, S., Lipsker, D., Cazenave, J.-P., Goud, B., de la Salle, H., Hanau, D., Salamero, J. (2007). Rab11A Controls the Biogenesis of Birbeck Granules by Regulating Langerin Recycling and Stability. Mol. Biol. Cell 18: 3169-3179 [Abstract] [Full Text]
Koh, T.-W., Korolchuk, V. I., Wairkar, Y. P., Jiao, W., Evergren, E., Pan, H., Zhou, Y., Venken, K. J.T., Shupliakov, O., Robinson, I. M., O'Kane, C. J., Bellen, H. J. (2007). Eps15 and Dap160 control synaptic vesicle membrane retrieval and synapse development. J. Cell Biol. 178: 309-322 [Abstract] [Full Text]
Besse, F., Mertel, S., Kittel, R. J., Wichmann, C., Rasse, T. M., Sigrist, S. J., Ephrussi, A. (2007). The Ig cell adhesion molecule Basigin controls compartmentalization and vesicle release at Drosophila melanogaster synapses. J. Cell Biol. 177: 843-855 [Abstract] [Full Text]
Kalesnikoff, J., Rios, E. J., Chen, C.-C., Alejandro Barbieri, M., Tsai, M., Tam, S.-Y., Galli, S. J. (2007). Roles of RabGEF1/Rabex-5 domains in regulating Fc{epsilon}RI surface expression and Fc{epsilon}RI-dependent responses in mast cells. Blood 109: 5308-5317 [Abstract] [Full Text]
Zhang, J., Schulze, K. L., Hiesinger, P. R., Suyama, K., Wang, S., Fish, M., Acar, M., Hoskins, R. A., Bellen, H. J., Scott, M. P. (2007). Thirty-One Flavors of Drosophila Rab Proteins. Genetics 176: 1307-1322 [Abstract] [Full Text]
Vardjan, N., Stenovec, M., Jorgacevski, J., Kreft, M., Zorec, R. (2007). Subnanometer Fusion Pores in Spontaneous Exocytosis of Peptidergic Vesicles. J. Neurosci. 27: 4737-4746 [Abstract] [Full Text]
Ing, B., Shteiman-Kotler, A., Castelli, M., Henry, P., Pak, Y., Stewart, B., Boulianne, G. L., Rotin, D. (2007). Regulation of Commissureless by the Ubiquitin Ligase DNedd4 Is Required for Neuromuscular Synaptogenesis in Drosophila melanogaster. Mol. Cell. Biol. 27: 481-496 [Abstract] [Full Text]
Khodosh, R., Augsburger, A., Schwarz, T. L., Garrity, P. A. (2006). Bchs, a BEACH domain protein, antagonizes Rab11 in synapse morphogenesis and other developmental events. Development 133: 4655-4665 [Abstract] [Full Text]
Loewen, C. A., Lee, S.-M., Shin, Y.-K., Reist, N. E. (2006). C2B Polylysine Motif of Synaptotagmin Facilitates a Ca2+-independent Stage of Synaptic Vesicle Priming In Vivo. Mol. Biol. Cell 17: 5211-5226 [Abstract] [Full Text]
Schmid, A., Qin, G., Wichmann, C., Kittel, R. J., Mertel, S., Fouquet, W., Schmidt, M., Heckmann, M., Sigrist, S. J. (2006). Non-NMDA-Type Glutamate Receptors Are Essential for Maturation But Not for Initial Assembly of Synapses at Drosophila Neuromuscular Junctions.. J. Neurosci. 26: 11267-11277 [Abstract] [Full Text]
Rusten, T. E., Rodahl, L. M.W., Pattni, K., Englund, C., Samakovlis, C., Dove, S., Brech, A., Stenmark, H. (2006). Fab1 Phosphatidylinositol 3-Phosphate 5-Kinase Controls Trafficking but Not Silencing of Endocytosed Receptors. Mol. Biol. Cell 17: 3989-4001 [Abstract] [Full Text]
Devon, R. S., Orban, P. C., Gerrow, K., Barbieri, M. A., Schwab, C., Cao, L. P., Helm, J. R., Bissada, N., Cruz-Aguado, R., Davidson, T.-L., Witmer, J., Metzler, M., Lam, C. K., Tetzlaff, W., Simpson, E. M., McCaffery, J. M., El-Husseini, A. E., Leavitt, B. R., Hayden, M. R. (2006). Als2-deficient mice exhibit disturbances in endosome trafficking associated with motor behavioral abnormalities. Proc. Natl. Acad. Sci. USA 103: 9595-9600 [Abstract] [Full Text]
Kittel, R. J., Wichmann, C., Rasse, T. M., Fouquet, W., Schmidt, M., Schmid, A., Wagh, D. A., Pawlu, C., Kellner, R. R., Willig, K. I., Hell, S. W., Buchner, E., Heckmann, M., Sigrist, S. J. (2006). Bruchpilot Promotes Active Zone Assembly, Ca2+ Channel Clustering, and Vesicle Release. Science 312: 1051-1054 [Abstract] [Full Text]
Ataman, B., Ashley, J., Gorczyca, D., Gorczyca, M., Mathew, D., Wichmann, C., Sigrist, S. J., Budnik, V. (2006). Nuclear trafficking of Drosophila Frizzled-2 during synapse development requires the PDZ protein dGRIP. Proc. Natl. Acad. Sci. USA 103: 7841-7846 [Abstract] [Full Text]
Hagedorn, E. J., Bayraktar, J. L., Kandachar, V. R., Bai, T., Englert, D. M., Chang, H. C. (2006). Drosophila melanogaster auxilin regulates the internalization of Delta to control activity of the Notch signaling pathway. J. Cell Biol. 173: 443-452 [Abstract] [Full Text]
Seto, E. S., Bellen, H. J. (2006). Internalization is required for proper Wingless signaling in Drosophila melanogaster.. J. Cell Biol. 173: 95-106 [Abstract] [Full Text]
Phillips, M. D., Thomas, G. H. (2006). Brush border spectrin is required for early endosome recycling in Drosophila. J. Cell Sci. 119: 1361-1370 [Abstract] [Full Text]
Kavalali, E. T. (2006). Synaptic Vesicle Reuse and Its Implications. Neuroscientist 12: 57-66 [Abstract]
Star, E. N., Newton, A. J., Murthy, V. N. (2005). Real-time imaging of Rab3a and Rab5a reveals differential roles in presynaptic function. J. Physiol. 569: 103-117 [Abstract] [Full Text]
Bao, H., Daniels, R. W., MacLeod, G. T., Charlton, M. P., Atwood, H. L., Zhang, B. (2005). AP180 Maintains the Distribution of Synaptic and Vesicle Proteins in the Nerve Terminal and Indirectly Regulates the Efficacy of Ca2+-Triggered Exocytosis. J. Neurophysiol. 94: 1888-1903 [Abstract] [Full Text]
Marzesco, A.-M., Janich, P., Wilsch-Brauninger, M., Dubreuil, V., Langenfeld, K., Corbeil, D., Huttner, W. B. (2005). Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J. Cell Sci. 118: 2849-2858 [Abstract] [Full Text]
Medioni, C., Noselli, S. (2005). Dynamics of the basement membrane in invasive epithelial clusters in Drosophila. Development 132: 3069-3077 [Abstract] [Full Text]
Qin, G., Schwarz, T., Kittel, R. J., Schmid, A., Rasse, T. M., Kappei, D., Ponimaskin, E., Heckmann, M., Sigrist, S. J. (2005). Four Different Subunits Are Essential for Expressing the Synaptic Glutamate Receptor at Neuromuscular Junctions of Drosophila. J. Neurosci. 25: 3209-3218 [Abstract] [Full Text]
Ganley, I. G., Carroll, K., Bittova, L., Pfeffer, S. (2004). Rab9 GTPase Regulates Late Endosome Size and Requires Effector Interaction for Its Stability. Mol. Biol. Cell 15: 5420-5430 [Abstract] [Full Text]
Kanaani, J., Diacovo, M. J., El-Husseini, A. E.-D., Bredt, D. S., Baekkeskov, S. (2004). Palmitoylation controls trafficking of GAD65 from Golgi membranes to axon-specific endosomes and a Rab5a-dependent pathway to presynaptic clusters. J. Cell Sci. 117: 2001-2013 [Abstract] [Full Text]
Chang, H. C., Hull, M., Mellman, I. (2004). The J-domain protein Rme-8 interacts with Hsc70 to control clathrin-dependent endocytosis in Drosophila. J. Cell Biol. 164: 1055-1064 [Abstract] [Full Text]
Thiagarajan, R., Tewolde, T., Li, Y., Becker, P. L., Rich, M. M., Engisch, K. L. (2004). Rab3A negatively regulates activity-dependent modulation of exocytosis in bovine adrenal chromaffin cells. J. Physiol. 555: 439-457 [Abstract] [Full Text]