Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform

doi:10.1083/jcb.200110081

PeproTech: Your source for Cell Biology Research Reagents

Published online 11 February 2002. doi:10.1083/jcb.200110081

This Article

	Full Text
	PDF (Full Text)
	PPT slides of all figures
	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 Mallard, F.
	Articles by Johannes, L.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Mallard, F.
	Articles by Johannes, L.


Social Bookmarking

	What's this?

© The Rockefeller University Press, 0021-9525/2002/2/653 $5.00
The Journal of Cell Biology, Volume 156, Number 4, February 18, 2002 653-664

Article

Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform

Frédéric Mallard¹, Bor Luen Tang³, Thierry Galli¹^,2, Danièle Tenza¹, Agnès Saint-Pol¹, Xu Yue³, Claude Antony¹, Wanjin Hong³, Bruno Goud¹ and Ludger Johannes¹

¹ UMR144 Curie/CNRS, Institut Curie, F-75248 Paris Cedex 05, France
² INSERM U536, Institut Curie, F-75248 Paris Cedex 05, France
³ Membrane Biology Laboratory, Institute of Molecular and Cell Biology, Singapore 117609, Republic of Singapore

Address correspondence to Ludger Johannes, Traffic and Signaling Laboratory, UMR144 Institut Curie/CNRS, 26 rue d'Ulm, F-75248 Paris Cedex 05, France. Tel.: 33-1-42346351. Fax: 33-1-42346507. E-mail: johannes{at}curie.fr

The molecular mechanisms underlying early/recycling endosomes-to-TGNtransport are still not understood. We identified interactionsbetween the TGN-localized putative t-SNAREs syntaxin 6, syntaxin16, and Vti1a, and two early/recycling endosomal v-SNAREs, VAMP3/cellubrevin,and VAMP4. Using a novel permeabilized cell system, these proteinswere functionally implicated in the post-Golgi retrograde transportstep. The function of Rab6a' was also required, whereas itsclosely related isoform, Rab6a, has previously been implicatedin Golgi-to-endoplasmic reticulum transport. Thus, our studyshows that membrane exchange between the early endocytic andthe biosynthetic/secretory pathways involves specific componentsof the Rab and SNARE machinery, and suggests that retrogradetransport between early/recycling endosomes and the endoplasmicreticulum is critically dependent on the sequential action oftwo members of the Rab6 subfamily.

Key Words: shiga toxin; early/recycling endosomes; SNARE; Rab protein; retrograde transport

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:

Dejgaard, S. Y., Murshid, A., Erman, A., Kizilay, O., Verbich, D., Lodge, R., Dejgaard, K., Ly-Hartig, T. B. N., Pepperkok, R., Simpson, J. C., Presley, J. F. (2008). Rab18 and Rab43 have key roles in ER-Golgi trafficking. J. Cell Sci. 121: 2768-2781 [Abstract] [Full Text]
Perez-Victoria, F. J., Mardones, G. A., Bonifacino, J. S. (2008). Requirement of the Human GARP Complex for Mannose 6-phosphate-receptor-dependent Sorting of Cathepsin D to Lysosomes. Mol. Biol. Cell 19: 2350-2362 [Abstract] [Full Text]
Lelouvier, B., Tamagno, G., Kaindl, A. M., Roland, A., Lelievre, V., Le Verche, V., Loudes, C., Gressens, P., Faivre-Baumann, A., Lenkei, Z., Dournaud, P. (2008). Dynamics of Somatostatin Type 2A Receptor Cargoes in Living Hippocampal Neurons. J. Neurosci. 28: 4336-4349 [Abstract] [Full Text]
Tiwari, N., Wang, C.-C., Brochetta, C., Ke, G., Vita, F., Qi, Z., Rivera, J., Soranzo, M. R., Zabucchi, G., Hong, W., Blank, U. (2008). VAMP-8 segregates mast cell-preformed mediator exocytosis from cytokine trafficking pathways. Blood 111: 3665-3674 [Abstract] [Full Text]
Chidambaram, S., Zimmermann, J., von Mollard, G. F. (2008). ENTH domain proteins are cargo adaptors for multiple SNARE proteins at the TGN endosome. J. Cell Sci. 121: 329-338 [Abstract] [Full Text]
Williams, D., Pessin, J. E. (2008). Mapping of R-SNARE function at distinct intracellular GLUT4 trafficking steps in adipocytes. J. Cell Biol. 180: 375-387 [Abstract] [Full Text]
Ganley, I. G., Espinosa, E., Pfeffer, S. R. (2008). A syntaxin 10 SNARE complex distinguishes two distinct transport routes from endosomes to the trans-Golgi in human cells. J. Cell Biol. 180: 159-172 [Abstract] [Full Text]
Cortes, C., Rzomp, K. A., Tvinnereim, A., Scidmore, M. A., Wizel, B. (2007). Chlamydia pneumoniae Inclusion Membrane Protein Cpn0585 Interacts with Multiple Rab GTPases. Infect. Immun. 75: 5586-5596 [Abstract] [Full Text]
Lieu, Z. Z., Derby, M. C., Teasdale, R. D., Hart, C., Gunn, P., Gleeson, P. A. (2007). The Golgin GCC88 Is Required for Efficient Retrograde Transport of Cargo from the Early Endosomes to the Trans-Golgi Network. Mol. Biol. Cell 18: 4979-4991 [Abstract] [Full Text]
Januschke, J., Nicolas, E., Compagnon, J., Formstecher, E., Goud, B., Guichet, A. (2007). Rab6 and the secretory pathway affect oocyte polarity in Drosophila. Development 134: 3419-3425 [Abstract] [Full Text]
Sun, Y., Shestakova, A., Hunt, L., Sehgal, S., Lupashin, V., Storrie, B. (2007). Rab6 Regulates Both ZW10/RINT-1 and Conserved Oligomeric Golgi Complex-dependent Golgi Trafficking and Homeostasis. Mol. Biol. Cell 18: 4129-4142 [Abstract] [Full Text]
Saenz, J. B., Doggett, T. A., Haslam, D. B. (2007). Identification and Characterization of Small Molecules That Inhibit Intracellular Toxin Transport. Infect. Immun. 75: 4552-4561 [Abstract] [Full Text]
Fuchs, E., Haas, A. K., Spooner, R. A., Yoshimura, S.-i., Lord, J. M., Barr, F. A. (2007). Specific Rab GTPase-activating proteins define the Shiga toxin and epidermal growth factor uptake pathways. J. Cell Biol. 177: 1133-1143 [Abstract] [Full Text]
Bujny, M. V., Popoff, V., Johannes, L., Cullen, P. J. (2007). The retromer component sorting nexin-1 is required for efficient retrograde transport of Shiga toxin from early endosome to the trans Golgi network. J. Cell Sci. 120: 2010-2021 [Abstract] [Full Text]
Popoff, V., Mardones, G. A., Tenza, D., Rojas, R., Lamaze, C., Bonifacino, J. S., Raposo, G., Johannes, L. (2007). The retromer complex and clathrin define an early endosomal retrograde exit site. J. Cell Sci. 120: 2022-2031 [Abstract] [Full Text]
Torgersen, M. L., Walchli, S., Grimmer, S., Skanland, S. S., Sandvig, K. (2007). Protein Kinase C{delta} Is Activated by Shiga Toxin and Regulates Its Transport. J. Biol. Chem. 282: 16317-16328 [Abstract] [Full Text]
Sehgal, P. B., Mukhopadhyay, S., Xu, F., Patel, K., Shah, M. (2007). Dysfunction of Golgi tethers, SNAREs, and SNAPs in monocrotaline-induced pulmonary hypertension. Am. J. Physiol. Lung Cell. Mol. Physiol. 292: L1526-L1542 [Abstract] [Full Text]
Sanderfoot, A. (2007). Increases in the Number of SNARE Genes Parallels the Rise of Multicellularity among the Green Plants. Plant Physiol. 144: 6-17 [Abstract] [Full Text]
Zhang, Y., Deng, Q., Barbieri, J. T. (2007). Intracellular Localization of Type III-delivered Pseudomonas ExoS with Endosome Vesicles. J. Biol. Chem. 282: 13022-13032 [Abstract] [Full Text]
Amessou, M., Fradagrada, A., Falguieres, T., Lord, J. M., Smith, D. C., Roberts, L. M., Lamaze, C., Johannes, L. (2007). Syntaxin 16 and syntaxin 5 are required for efficient retrograde transport of several exogenous and endogenous cargo proteins. J. Cell Sci. 120: 1457-1468 [Abstract] [Full Text]
Nyasae, L., Bustos, R., Braiterman, L., Eipper, B., Hubbard, A. (2007). Dynamics of endogenous ATP7A (Menkes protein) in intestinal epithelial cells: copper-dependent redistribution between two intracellular sites. Am. J. Physiol. Gastrointest. Liver Physiol. 292: G1181-G1194 [Abstract] [Full Text]
Tran, T. H. T., Zeng, Q., Hong, W. (2007). VAMP4 cycles from the cell surface to the trans-Golgi network via sorting and recycling endosomes. J. Cell Sci. 120: 1028-1041 [Abstract] [Full Text]
Moorhead, A. R., Rzomp, K. A., Scidmore, M. A. (2007). The Rab6 Effector Bicaudal D1 Associates with Chlamydia trachomatis Inclusions in a Biovar-Specific Manner. Infect. Immun. 75: 781-791 [Abstract] [Full Text]
Scheuber, A., Rudge, R., Danglot, L., Raposo, G., Binz, T., Poncer, J.-C., Galli, T. (2006). Loss of AP-3 function affects spontaneous and evoked release at hippocampal mossy fiber synapses. Proc. Natl. Acad. Sci. USA 103: 16562-16567 [Abstract] [Full Text]
Buvelot Frei, S., Rahl, P. B., Nussbaum, M., Briggs, B. J., Calero, M., Janeczko, S., Regan, A. D., Chen, C. Z., Barral, Y., Whittaker, G. R., Collins, R. N. (2006). Bioinformatic and comparative localization of rab proteins reveals functional insights into the uncharacterized GTPases ypt10p and ypt11p.. Mol. Cell. Biol. 26: 7299-7317 [Abstract] [Full Text]
Reddy, J. V., Burguete, A. S., Sridevi, K., Ganley, I. G., Nottingham, R. M., Pfeffer, S. R. (2006). A Functional Role for the GCC185 Golgin in Mannose 6-Phosphate Receptor Recycling. Mol. Biol. Cell 17: 4353-4363 [Abstract] [Full Text]
Ortiz, P. A. (2006). cAMP increases surface expression of NKCC2 in rat thick ascending limbs: role of VAMP. Am. J. Physiol. Renal Physiol. 290: F608-F616 [Abstract] [Full Text]
Smith, D. C., Sillence, D. J., Falguieres, T., Jarvis, R. M., Johannes, L., Lord, J. M., Platt, F. M., Roberts, L. M. (2006). The Association of Shiga-like Toxin with Detergent-resistant Membranes Is Modulated by Glucosylceramide and Is an Essential Requirement in the Endoplasmic Reticulum for a Cytotoxic Effect. Mol. Biol. Cell 17: 1375-1387 [Abstract] [Full Text]
Kim, T., Loh, Y. P. (2006). Protease Nexin-1 Promotes Secretory Granule Biogenesis by Preventing Granule Protein Degradation. Mol. Biol. Cell 17: 789-798 [Abstract] [Full Text]
Fukuda, H., Nakamura, N., Hirose, S. (2006). MARCH-III Is a Novel Component of Endosomes with Properties Similar to Those of MARCH-II. J Biochem 139: 137-145 [Abstract] [Full Text]
Struck, N. S., de Souza Dias, S., Langer, C., Marti, M., Pearce, J. A., Cowman, A. F., Gilberger, T. W. (2005). Re-defining the Golgi complex in Plasmodium falciparum using the novel Golgi marker PfGRASP. J. Cell Sci. 118: 5603-5613 [Abstract] [Full Text]
Bose, A., Guilherme, A., Huang, S., Hubbard, A. C., Lane, C. R., Soriano, N. A., Czech, M. P. (2005). The v-SNARE Vti1a Regulates Insulin-stimulated Glucose Transport and Acrp30 Secretion in 3T3-L1 Adipocytes. J. Biol. Chem. 280: 36946-36951 [Abstract] [Full Text]
Yoshino, A., Setty, S. R. G., Poynton, C., Whiteman, E. L., Saint-Pol, A., Burd, C. G., Johannes, L., Holzbaur, E. L., Koval, M., McCaffery, J. M., Marks, M. S. (2005). tGolgin-1 (p230, golgin-245) modulates Shiga-toxin transport to the Golgi and Golgi motility towards the microtubule-organizing centre. J. Cell Sci. 118: 2279-2293 [Abstract] [Full Text]
Proux-Gillardeaux, V., Gavard, J., Irinopoulou, T., Mege, R.-M., Galli, T. (2005). Tetanus neurotoxin-mediated cleavage of cellubrevin impairs epithelial cell migration and integrin-dependent cell adhesion. Proc. Natl. Acad. Sci. USA 102: 6362-6367 [Abstract] [Full Text]
Lin, P. J. C., Williams, W. P., Luu, Y., Molday, R. S., Orlowski, J., Numata, M. (2005). Secretory carrier membrane proteins interact and regulate trafficking of the organellar (Na+,K+)/H+ exchanger NHE7. J. Cell Sci. 118: 1885-1897 [Abstract] [Full Text]
Jiang, S., Storrie, B. (2005). Cisternal Rab Proteins Regulate Golgi Apparatus Redistribution in Response to Hypotonic Stress. Mol. Biol. Cell 16: 2586-2596 [Abstract] [Full Text]
Nakamura, N., Fukuda, H., Kato, A., Hirose, S. (2005). MARCH-II Is a Syntaxin-6-binding Protein Involved in Endosomal Trafficking. Mol. Biol. Cell 16: 1696-1710 [Abstract] [Full Text]
Young, J., Stauber, T., del Nery, E., Vernos, I., Pepperkok, R., Nilsson, T. (2005). Regulation of Microtubule-dependent Recycling at the Trans-Golgi Network by Rab6A and Rab6A'. Mol. Biol. Cell 16: 162-177 [Abstract] [Full Text]
Shin, H.-W., Morinaga, N., Noda, M., Nakayama, K. (2004). BIG2, A Guanine Nucleotide Exchange Factor for ADP-Ribosylation Factors: Its Localization to Recycling Endosomes and Implication in the Endosome Integrity. Mol. Biol. Cell 15: 5283-5294 [Abstract] [Full Text]
Natarajan, R., Linstedt, A. D. (2004). A Cycling cis-Golgi Protein Mediates Endosome-to-Golgi Traffic. Mol. Biol. Cell 15: 4798-4806 [Abstract] [Full Text]
Lu, L., Tai, G., Hong, W. (2004). Autoantigen Golgin-97, an Effector of Arl1 GTPase, Participates in Traffic from the Endosome to the Trans-Golgi Network. Mol. Biol. Cell 15: 4426-4443 [Abstract] [Full Text]
Tai, G., Lu, L., Wang, T. L., Tang, B. L., Goud, B., Johannes, L., Hong, W. (2004). Participation of the Syntaxin 5/Ykt6/GS28/GS15 SNARE Complex in Transport from the Early/Recycling Endosome to the Trans-Golgi Network. Mol. Biol. Cell 15: 4011-4022 [Abstract] [Full Text]
Kagan, J. C., Stein, M.-P., Pypaert, M., Roy, C. R. (2004). Legionella Subvert the Functions of Rab1 and Sec22b to Create a Replicative Organelle. J. Exp. Med. 199: 1201-1211 [Abstract] [Full Text]
Bauer, R. A., Overlease, R. L., Lieber, J. L., Angleson, J. K. (2004). Retention and stimulus-dependent recycling of dense core vesicle content in neuroendocrine cells. J. Cell Sci. 117: 2193-2202 [Abstract] [Full Text]
Kuliawat, R., Kalinina, E., Bock, J., Fricker, L., McGraw, T. E., Kim, S. R., Zhong, J., Scheller, R., Arvan, P. (2004). Syntaxin-6 SNARE Involvement in Secretory and Endocytic Pathways of Cultured Pancreatic {beta}-Cells. Mol. Biol. Cell 15: 1690-1701 [Abstract] [Full Text]
Chidambaram, S., Mullers, N., Wiederhold, K., Haucke, V., von Mollard, G. F. (2004). Specific Interaction between SNAREs and Epsin N-terminal Homology (ENTH) Domains of Epsin-related Proteins in trans-Golgi Network to Endosome Transport. J. Biol. Chem. 279: 4175-4179 [Abstract] [Full Text]
Yoshino, A., Bieler, B. M., Harper, D. C., Cowan, D. A., Sutterwala, S., Gay, D. M., Cole, N. B., McCaffery, J. M., Marks, M. S. (2003). A role for GRIP domain proteins and/or their ligands in structure and function of the trans Golgi network. J. Cell Sci. 116: 4441-4454 [Abstract] [Full Text]
Rzomp, K. A., Scholtes, L. D., Briggs, B. J., Whittaker, G. R., Scidmore, M. A. (2003). Rab GTPases Are Recruited to Chlamydial Inclusions in Both a Species-Dependent and Species-Independent Manner. Infect. Immun. 71: 5855-5870 [Abstract] [Full Text]
Umeda, A., Fujita, H., Kuronita, T., Hirosako, K., Himeno, M., Tanaka, Y. (2003). Distribution and trafficking of MPR300 is normal in cells with cholesterol accumulated in late endocytic compartments: evidence for early endosome-to-TGN trafficking of MPR300. J. Lipid Res. 44: 1821-1832 [Abstract] [Full Text]
Chen, A., AbuJarour, R. J., Draper, R. K. (2003). Evidence that the transport of ricin to the cytoplasm is independent of both Rab6A and COPI. J. Cell Sci. 116: 3503-3510 [Abstract] [Full Text]
Atlashkin, V., Kreykenbohm, V., Eskelinen, E.-L., Wenzel, D., Fayyazi, A., Fischer von Mollard, G. (2003). Deletion of the SNARE vti1b in Mice Results in the Loss of a Single SNARE Partner, Syntaxin 8. Mol. Cell. Biol. 23: 5198-5207 [Abstract] [Full Text]
Martinez-Arca, S., Rudge, R., Vacca, M., Raposo, G., Camonis, J., Proux-Gillardeaux, V., Daviet, L., Formstecher, E., Hamburger, A., Filippini, F., D'Esposito, M., Galli, T. (2003). A dual mechanism controlling the localization and function of exocytic v-SNAREs. Proc. Natl. Acad. Sci. USA 100: 9011-9016 [Abstract] [Full Text]
Marz, K. E., Lauer, J. M., Hanson, P. I. (2003). Defining the SNARE Complex Binding Surface of {alpha}-SNAP: IMPLICATIONS FOR SNARE COMPLEX DISASSEMBLY. J. Biol. Chem. 278: 27000-27008 [Abstract] [Full Text]
Martinez-Arca, S., Proux-Gillardeaux, V., Alberts, P., Louvard, D., Galli, T. (2003). Ectopic expression of syntaxin 1 in the ER redirects TI-VAMP- and cellubrevin-containing vesicles. J. Cell Sci. 116: 2805-2816 [Abstract] [Full Text]
Perera, H. K. I., Clarke, M., Morris, N. J., Hong, W., Chamberlain, L. H., Gould, G. W. (2003). Syntaxin 6 Regulates Glut4 Trafficking in 3T3-L1 Adipocytes. Mol. Biol. Cell 14: 2946-2958 [Abstract] [Full Text]
Zeng, Q., Tran, T. T. H., Tan, H.-X., Hong, W. (2003). The Cytoplasmic Domain of Vamp4 and Vamp5 Is Responsible for Their Correct Subcellular Targeting: THE N-TERMINAL EXTENSION OF VAMP4 CONTAINS A DOMINANT AUTONOMOUS TARGETING SIGNAL FOR THE TRANS-GOLGI NETWORK. J. Biol. Chem. 278: 23046-23054 [Abstract] [Full Text]
Nizak, C., Monier, S., del Nery, E., Moutel, S., Goud, B., Perez, F. (2003). Recombinant Antibodies to the Small GTPase Rab6 as Conformation Sensors. Science 300: 984-987 [Abstract] [Full Text]
Fratti, R. A., Chua, J., Vergne, I., Deretic, V. (2003). Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc. Natl. Acad. Sci. USA 100: 5437-5442 [Abstract] [Full Text]
Shewan, A. M., van Dam, E. M., Martin, S., Luen, T. B., Hong, W., Bryant, N. J., James, D. E. (2003). GLUT4 Recycles via a trans-Golgi Network (TGN) Subdomain Enriched in Syntaxins 6 and 16 But Not TGN38: Involvement of an Acidic Targeting Motif. Mol. Biol. Cell 14: 973-986 [Abstract] [Full Text]
Stedman, T. T., Sussmann, A. R., Joiner, K. A. (2003). Toxoplasma gondii Rab6 Mediates a Retrograde Pathway for Sorting of Constitutively Secreted Proteins to the Golgi Complex. J. Biol. Chem. 278: 5433-5443 [Abstract] [Full Text]
Luo, Z., Gallwitz, D. (2003). Biochemical and Genetic Evidence for the Involvement of Yeast Ypt6-GTPase in Protein Retrieval to Different Golgi Compartments. J. Biol. Chem. 278: 791-799 [Abstract] [Full Text]
Grimberg, E., Peng, Z., Hammel, I., Sagi-Eisenberg, R. (2003). Synaptotagmin III is a critical factor for the formation of the perinuclear endocytic recycling compartment and determination of secretory granules size. J. Cell Sci. 116: 145-154 [Abstract] [Full Text]
Xu, Y., Martin, S., James, D. E., Hong, W. (2002). GS15 Forms a SNARE Complex with Syntaxin 5, GS28, and Ykt6 and Is Implicated in Traffic in the Early Cisternae of the Golgi Apparatus. Mol. Biol. Cell 13: 3493-3507 [Abstract] [Full Text]
Mukherjee, K., Parashuraman, S., Krishnamurthy, G., Majumdar, J., Yadav, A., Kumar, R., Basu, S. K., Mukhopadhyay, A. (2002). Diverting intracellular trafficking of Salmonella to the lysosome through activation of the late endocytic Rab7 by intracellular delivery of muramyl dipeptide. J. Cell Sci. 115: 3693-3701 [Abstract] [Full Text]
Chen, J.-L., Ahluwalia, J. P., Stamnes, M. (2002). Selective Effects of Calcium Chelators on Anterograde and Retrograde Protein Transport in the Cell. J. Biol. Chem. 277: 35682-35687 [Abstract] [Full Text]
Johannes, L. (2002). The Epithelial Cell Cytoskeleton and Intracellular Trafficking: I. Shiga toxin B-subunit system: retrograde transport, intracellular vectorization, and more. Am. J. Physiol. Gastrointest. Liver Physiol. 283: G1-G7 [Abstract] [Full Text]
Xu, H., Boulianne, G. L., Trimble, W. S. (2002). Drosophila syntaxin 16 is a Q-SNARE implicated in Golgi dynamics. J. Cell Sci. 115: 4447-4455 [Abstract] [Full Text]