Amessou, Mohamed, Fradagrada, Alexandre, Falguières, Thomas, Lord, Mike (J. Mike), Smith, Daniel C., Roberts, Lynne M. , Lamaze, Christophe and Johannes, Ludger. (2007) Syntaxin 16 and syntaxin 5 are required for efficient retrograde transport of several exogenous and endogenous cargo proteins. Journal of Cell Science, Vol.12 (No.8). pp. 1457-1468. ISSN 0021-9533

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Abstract

Retrograde transport allows proteins and lipids to leave the endocytic pathway to reach other intracellular compartments, such as trans-Golgi network (TGN)/Golgi membranes, the endoplasmic reticulum and, in some instances, the cytosol. Here, we have used RNA interference against the SNARE proteins syntaxin 5 and syntaxin 16, combined with recently developed quantitative trafficking assays, morphological approaches and cell intoxication analysis to show that these SNARE proteins are not only required for efficient retrograde transport of Shiga toxin, but also for that of an endogenous cargo protein - the mannose 6-phosphate receptor - and for the productive trafficking into cells of cholera toxin and ricin. We have found that the function of syntaxin 16 was specifically required for, and restricted to, the retrograde pathway. Strikingly, syntaxin 5 RNA interference protected cells particularly strongly against Shiga toxin. Since our trafficking analysis showed that apart from inhibiting retrograde endosome-to-TGN transport, the silencing of syntaxin 5 had no additional effect on Shiga toxin endocytosis or trafficking from TGN/Golgi membranes to the endoplasmic reticulum, we hypothesize that syntaxin 5 also has trafficking-independent functions. In summary, our data demonstrate that several cellular and exogenous cargo proteins use elements of the same SNARE machinery for efficient retrograde transport between early/recycling endosomes and TGN/Golgi membranes.

Item Type:	Journal Article
Subjects:	Q Science > QR Microbiology
Divisions:	Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010)
Library of Congress Subject Headings (LCSH):	Toxins, Golgi apparatus, Biological transport
Journal or Publication Title:	Journal of Cell Science
Publisher:	The Company of Biologists Ltd.
ISSN:	0021-9533
Date:	15 April 2007
Volume:	Vol.12
Number:	No.8
Page Range:	pp. 1457-1468
Identification Number:	10.1242/jcs.03436
Status:	Peer Reviewed
Access rights to Published version:	Restricted or Subscription Access
References:	Amessou, M., Popoff, V., Yelamos, B., Saint-Pol, A. and Johannes, L. (2006). Measuring retrograde transport to the trans-Golgi network. In Current Protocols in Cell Biology (ed. J. Bonifacino et al.). Hoboken, NJ: Wiley. Bennett, M. K., Garcia-Arraras, J. E., Elferink, L. A., Peterson, K., Fleming, A. M., Hazuka, C. D. and Scheller, R. H. (1993). The syntaxin family of vesicular transport receptors. Cell 74, 863-873. Bock, J. B., Lin, R. C. and Scheller, R. H. (1996). A new syntaxin family member implicated in targeting of intracellular transport vesicles. J. Biol. Chem. 271, 17961-17965. Chen, Y. A. and Scheller, R. H. (2001). SNARE-mediated membrane fusion. Nat. Rev. Mol. Cell Biol. 2, 98-106. Dascher, C., Matteson, J. and Balch, W. E. (1994). Syntaxin 5 regulates endoplasmic reticulum to Golgi transport. J. Biol. Chem. 269, 29363-29366. De Haan, L. and Hirst, T. R. (2004). Cholera toxin: a paradigm for multi-functional engagement of cellular mechanisms. Mol. Membr. Biol. 21, 77-92. Diaz, E. and Pfeffer, S. R. (1998). TIP47: a cargo selection device for mannose 6-phosphate receptor trafficking. Cell 93, 433-443. Endo, Y., Mitsui, K., Motizuki, M. and Tsurugi, K. (1987). The mechanism of action of ricin and related toxic lectins on eukaryotic ribosomes. The site and the characteristics of the modification in 28 S ribosomal RNA caused by the toxins. J. Biol. Chem. 262, 5908-5912. Endo, Y., Tsurugi, K., Yutsudo, T., Takeda, Y., Ogasawara, T. and Igarashi, K. (1988). Site of action of a Vero toxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. RNA N-glycosidase activity of the toxins. Eur. J. Biochem. 171, 45-50. Falguières, T., Mallard, F., Baron, C. L., Hanau, D., Lingwood, C., Goud, B., Salamero, J. and Johannes, L. (2001). Targeting of Shiga toxin B-subunit to retrograde transport route in association with detergent resistant membranes. Mol. Biol. Cell 12, 2453-2468. Fujinaga, Y., Wolf, A. A., Rodighiero, C., Wheeler, H., Tsai, B., Allen, L., Jobling, M. G., Rapoport, T., Holmes, R. K. and Lencer, W. I. (2003). Gangliosides that associate with lipid rafts mediate transport of cholera and related toxins from the plasma membrane to the endoplasmic reticulum. Mol. Biol. Cell 14, 4783-4793. Goda, Y. and Pfeffer, S. R. (1988). Selective recycling of the mannose 6-phosphate/IGF-II receptor to the trans Golgi network in vitro. Cell 55, 309-320. Grimmer, S., Iversen, T. G., van Deurs, B. and Sandvig, K. (2000). Endosome to golgi transport of ricin is regulated by cholesterol. Mol. Biol. Cell 11, 4205-4216. Hay, J. C., Chao, D. S., Kuo, C. S. and Scheller, R. H. (1997). Protein interactions regulating vesicle transport between the endoplasmic reticulum and Golgi apparatus in mammalian cells. Cell 89, 149-158. Hay, J. C., Klumperman, J., Oorschot, V., Steegmaier, M., Kuo, C. S. and Scheller, R. H. (1998). Localization, dynamics, and protein interactions reveal distinct roles for ER and Golgi SNAREs. J. Cell Biol. 141, 1489-1502. Iversen, T. G., Skretting, G., Llorente, A., Nicoziani, P., van Deurs, B. and Sandvig, K. (2001). Endosome to golgi transport of ricin is independent of clathrin and of the Rab9 and Rab11 GTPases. Mol. Biol. Cell 12, 2099-2107. Jahn, R. and Grubmuller, H. (2002). Membrane fusion. Curr. Opin. Cell Biol. 14, 488-495. Johannes, L. and Decaudin, D. (2005). Protein toxins: intracellular trafficking for targeted therapy. Gene Ther. 16, 1360-1368. Johannes, L., Tenza, D., Antony, C. and Goud, B. (1997). Retrograde transport of KDEL-bearing B-fragment of Shiga toxin. J. Biol. Chem. 272, 19554-19561. Katagiri, Y. U., Mori, T., Nakajima, H., Katagiri, C., Taguchi, T., Takeda, T., Kiyokawa, N. and Fujimoto, J. (1999). Activation of src family kinase yes induced by shiga toxin binding to globotriaosyl ceramide (Gb3/CD77) in low density, detergent-insoluble microdomains. J. Biol. Chem. 274, 35278-35282. Kirkham, M., Fujita, A., Chadda, R., Nixon, S. J., Kurzchalia, T. V., Sharma, D. K., Pagano, R. E., Hancock, J. F., Mayor, S. and Parton, R. G. (2005). Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J. Cell Biol. 168, 465-476. Kovbasnjuk, O., Edidin, M. and Donowitz, M. (2001). Role of lipid rafts in Shiga toxin 1 interaction with the apical surface of Caco-2 cells. J. Cell Sci. 114, 4025-4031. Lauvrak, S. U., Llorente, A., Iversen, T. G. and Sandvig, K. (2002). Selective regulation of the Rab9-independent transport of ricin to the Golgi apparatus by calcium. J. Cell Sci. 115, 3449-3456. Lauvrak, S. U., Torgersen, M. L. and Sandvig, K. (2004). Efficient endosome-to-Golgi transport of Shiga toxin is dependent on dynamin and clathrin. J. Cell Sci. 117, 2321-2331. Lemichez, E., Bomsel, M., Devilliers, G., vanderSpek, J., Murphy, J. R., Lukianov, E. V., Olsnes, S. and Boquet, P. (1997). Membrane translocation of diphtheria toxin fragment A exploits early to late endosome trafficking machinery. Mol. Microbiol. 23, 445-457. Lin, S. X., Gundersen, G. G. and Maxfield, F. R. (2002). Export from pericentriolar endocytic recycling compartment to cell surface depends on stable, detyrosinated (glu) microtubules and kinesin. Mol. Biol. Cell 13, 96-109. Lingwood, C. A. (1993). Verotoxins and their glycolipid receptors. Adv. Lipid Res. 25, 189-211. Lombardi, D., Soldati, T., Riederer, M. A., Goda, Y., Zerial, M. and Pfeffer, S. R. (1993). Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J. 12, 677-682. Lord, J. M., Deeks, E., Marsden, C. J., Moore, K., Pateman, C., Smith, D. C., Spooner, R. A., Watson, P. and Roberts, L. M. (2003). Retrograde transport of toxins across the endoplasmic reticulum membrane. Biochem. Soc. Trans. 31, 1260-1262. Lu, L., Tai, G. and 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. Mallard, F. and Johannes, L. (2003). Shiga toxin B-subunit as a tool to study retrograde transport. Methods Mol. Med. 73, 209-220. Mallard, F., Tenza, D., Antony, C., Salamero, J., Goud, B. and Johannes, L. (1998). Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of Shiga toxin B-fragment transport. J. Cell Biol. 143, 973-990. Mallard, F., Tang, B. L., Galli, T., Tenza, D., Saint-Pol, A., Yue, X., Antony, C., Hong, W. J., Goud, B. and Johannes, L. (2002). Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J. Cell Biol. 156, 653-664. Natarajan, R. and Linstedt, A. D. (2004). A cycling cis-Golgi protein mediates endosome-to-Golgi traffic. Mol. Biol. Cell 15, 4798-4806. Peacock, E., Jacob, V. W. and Fallone, S. M. (2001). Escherichia coli O157:H7: etiology, clinical features, complications, and treatment. Nephrol. Nurs. J. 28, 547-550, 553-555. Pelham, H. R. B. and Rothman, J. E. (2000). The debate about transport in the Golgi–Two sides of the same coin? Cell 102, 713-719. Pina, D. G. and Johannes, L. (2005). Cholera and Shiga toxin B-subunits: thermodynamic and structural considerations for function and biomedical applications. Toxicon 45, 389-393. Rapak, A., Falnes, P. O. and Olsnes, S. (1997). Retrograde transport of mutant ricin to the endoplasmic reticulum with subsequent translocation to cytosol. Proc. Natl. Acad. Sci. USA 94, 3783-3788. Saint-Pol, A., Yélamos, B., Amessou, M., Mills, I., Dugast, M., Tenza, D., Schu, P., Antony, C., McMahon, H. T., Lamaze, C. et al. (2004). Clathrin adaptor epsinR is required for retrograde sorting on early endosomal membranes. Dev. Cell 6, 525-538. Sandvig, K. and van Deurs, B. (1999). Endocytosis and intracellular transport of ricin: recent discoveries. FEBS Lett. 452, 67-70. Sandvig, K., Olsnes, S., Brown, J. E., Petersen, O. W. and van Deurs, B. (1989). Endocytosis from coated pits of Shiga toxin: a glycolipid-binding protein from Shigella dysenteriae 1. J. Cell Biol. 108, 1331-1343. Sandvig, K., Garred, O., Prydz, K., Kozlov, J. V., Hansen, S. H. and van Deurs, B. (1992). Retrograde transport of endocytosed Shiga toxin to the endoplasmic reticulum. Nature 358, 510-512. Sandvig, K., Spilsberg, B., Lauvrak, S. U., Torgersen, M. L., Iversen, T. G. and van Deurs, B. (2004). Pathways followed by protein toxins into cells. Int. J. Med. Microbiol. 293, 483-490. Scales, S. J., Pepperkok, R. and Kreis, T. E. (1997). Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell 90, 1137-1148. Schapiro, F. B., Lingwood, C., Furuya, W. and Grinstein, S. (1998). pH-independent retrograde targeting of glycolipids to the Golgi complex. Am. J. Physiol. 274, C319-C332. Simpson, J. C., Dascher, C., Roberts, L. M., Lord, J. M. and Balch, W. E. (1995). Ricin cytotoxicity is sensitive to recycling between the endoplasmic reticulum and the Golgi complex. J. Biol. Chem. 270, 20078-20083. Smith, D. C., Lord, J. M., Roberts, L. M. and Johannes, L. (2004). Glycosphingolipids as toxin receptors. Semin. Cell Dev. Biol. 15, 397-408. Smith, D. C., Sillence, D. J., Falguières, T., Jarvis, R. M., Johannes, L., Lord, J. M., Platt, F. M. and Roberts, L. M. (2006a). Lipid raft association of Shiga-like toxin is modulated by glycosylceramide and is an essential requirement in the endoplasmic reticulum for a cytotoxic effect. Mol. Biol. Cell 17, 1375-1387. Smith, D. C., Spooner, R. A., Watson, P. D., Murray, L. J., Hodge, T. W., Johannes, L., Lord, J. M. and Roberts, L. M. (2006b). Internalized Pseudomonas exotoxin A can exploit multiple pathways to reach the endoplasmic reticulum. Traffic 7, 379-393. Suga, K., Hattori, H., Saito, A. and Akagawa, K. (2005). RNA interference-mediated silencing of the syntaxin 5 gene induces Golgi fragmentation but capable of transporting vesicles. FEBS Lett. 579, 4226-4234. Tai, G., Lu, L., Wang, T. L., Tang, B. L., Goud, B., Johannes, L. and Hong, W. (2004). Participation of syntaxin 5/Ykt6/GS28/GS15 SNARE complex in transport from the early/recycling endosome to the TGN. Mol. Biol. Cell 15, 4011-4022. Tai, G., Lu, L., Johannes, L. and Hong, W. (2005). Functional analysis of Arl1 and golgin-97 in endosome-to-TGN transport using recombinant Shiga toxin B fragment. Meth. Enzymol. 404, 442-453. Tang, B. L., Low, D. Y., Lee, S. S., Tan, A. E. and Hong, W. (1998a). Molecular cloning and localization of human syntaxin 16, a member of the syntaxin family of SNARE proteins. Biochem. Biophys. Res. Commun. 242, 673-679. Tang, B. L., Low, D. Y., Tan, A. E. and Hong, W. (1998b). Syntaxin 10, a member of the syntaxin family localized to the trans-Golgi network. Biochem. Biophys. Res. Commun. 242, 345-350. Valdez, A. C., Cabaniols, J. P., Brown, M. J. and Roche, P. A. (1999). Syntaxin 11 is associated with SNAP-23 on late endosomes and the trans-Golgi network. J. Cell Sci. 112, 845-854. Waguri, S., Dewitte, F., Le Borgne, R., Rouille, Y., Uchiyama, Y., Dubremetz, J. F. and Hoflack, B. (2003). Visualization of TGN to endosome trafficking through fluorescently labeled MPR and AP-1 in living cells. Mol. Biol. Cell 14, 142-155. Wang, Y., Tai, G., Johannes, L., Hong, W. and Tang, B. L. (2005). Syntaxin 10 at the trans-Golgi network can potentially interact with, but is functionally distinct from syntaxins 6 and 16. Mol. Membr. Biol. 22, 313-325. Wilcke, M., Johannes, L., Galli, T., Mayau, V., Goud, B. and Salamero, J. (2000). Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J. Cell Biol. 151, 1207-1220. Wiley, H. S. and Burke, P. M. (2001). Regulation of receptor tyrosine kinase signaling by endocytic trafficking. Traffic 2, 12-18. Xu, Y., Martin, S., James, D. E. and 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. Yoshida, T., Chen, C. C., Zhang, M. S. and Wu, H. C. (1991). Disruption of the Golgi apparatus by brefeldin A inhibits the cytotoxicity of ricin, modeccin, and Pseudomonas toxin. Exp. Cell Res. 192, 389-395.
URI:	http://wrap.warwick.ac.uk/id/eprint/668

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