Transport of the cholera toxin B-subunit from recycling endosomes to the Golgi requires clathrin and AP-1

Journal of Cell Science

Volumn 128, Issue 16, 2015, Pages 3131-3142

  Matsudaira, Tatsuyuki ^a   Niki, Takahiro ^a   Taguchi, Tomohiko ^a   Arai, Hiroyuki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Cholera toxin; Clathrin; Endosomes; Retrograde transport; SMAP2

Indexed keywords

CHOLERA TOXIN B SUBUNIT; CLATHRIN; COAT PROTEIN; TRANSCRIPTION FACTOR AP 1; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; CHOLERA TOXIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MEMBRANE PROTEIN; SMAP1L PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOSOME; GOLGI COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; ANIMAL; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; GENE SILENCING; GENETICS; HUMAN; METABOLISM;

ADP-RIBOSYLATION FACTOR 1; ANIMALS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; CHOLERA TOXIN; CLATHRIN; COS CELLS; ENDOSOMES; GENE KNOCKDOWN TECHNIQUES; GOLGI APPARATUS; GTPASE-ACTIVATING PROTEINS; HUMANS; MEMBRANE PROTEINS; TRANSCRIPTION FACTOR AP-1;

EID: 84939497678     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.172171     Document Type: Article

References (66)

1. Ahle, S., Mann, A., Eichelsbacher, U. and Ungewickell, E. (1988). Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO J. 7, 919-929.
2. Anitei, M., Stange, C., Parshina, I., Baust, T., Schenck, A., Raposo, G., Kirchhausen, T. and Hoflack, B. (2010). Protein complexes containing CYFIP/Sra/PIR121 coordinate Arf1 and Rac1 signalling during clathrin-AP-1-coated carrier biogenesis at the TGN. Nat. Cell Biol. 12, 330-340.
3. Behnia, R. and Munro, S. (2005). Organelle identity and the signposts for membrane traffic. Nature 438, 597-604.
4. Brodsky, F. M. (2012). Diversity of clathrin function: new tricks for an old protein. Annu. Rev. Cell Dev. Biol. 28, 309-336.
5. Donaldson, J. G. and Jackson, C. L. (2011). ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat. Rev. Mol. Cell Biol. 12, 362-375.
6. D'Souza-Schorey, C. and Chavrier, P. (2006). ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347-358.
7. Eaton, S. (2008). Retromer retrieves wntless. Dev. Cell. 14, 4-6.
8. Folsch, H., Pypaert, M., Schu, P. and Mellman, I. (2001). Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J. Cell Biol. 152, 595-606.
9. Foote, C. and Nothwehr, S. F. (2006). The clathrin adaptor complex 1 directly binds to a sorting signal in Ste13p to reduce the rate of its trafficking to the late endosome of yeast. J. Cell Biol. 173, 615-626.
10. Funaki, T., Kon, S., Ronn, R. E., Henmi, Y., Kobayashi, Y., Watanabe, T., Nakayama, K., Tanabe, K. and Satake, M. (2011). Localization of SMAP2 to the TGN and its function in the regulation of TGN protein transport. Cell Struct. Funct. 36, 83-95.
11. Ghosh, R. N., Mallet, W. G., Soe, T. T., McGraw, T. E. and Maxfield, F. R. (1998). An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells. J. Cell Biol. 142, 923-936.
12. Ghosh, P., Dahms, N. M. and Kornfeld, S. (2003). Mannose 6-phosphate receptors: new twists in the tale. Nat. Rev. Mol. Cell Biol. 4, 202-213.
13. Grant, B. D. and Caplan, S. (2008). Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffic 9, 2043-2052.
14. Gravotta, D., Carvajal-Gonzalez, J. M., Mattera, R., Deborde, S., Banfelder, J. R., Bonifacino, J. S. and Rodriguez-Boulan, E. (2012). The clathrin adaptor AP-1A mediates basolateral polarity. Dev. Cell 22, 811-823.
15. Haberg, K., Lundmark, R. and Carlsson, S. R. (2008). SNX18 is an SNX9 paralog that acts as a membrane tubulator in AP-1-positive endosomal trafficking. J. Cell Sci. 121, 1495-1505.
16. Hayakawa, N., Ogoh, H., Sumiyoshi, M., Matsui, Y., Nishikawa, S., Miyamoto, K., Maede, Y., Kiyonari, H., Suzuki, M. and Watanabe, T. (2014). The ADPribosylation factor 1 gene is indispensable for mouse embryonic development after implantation. Biochem. Biophys. Res. Commun. 453, 748-753.
17. Hirst, J., Motley, A., Harasaki, K., Peak Chew, S. Y. and Robinson, M. S. (2003). EpsinR: an ENTH domain-containing protein that interacts with AP-1. Mol. Biol. Cell 14, 625-641.
18. Ioannou, M. S. and Marat, A. L. (2012). The role of EHD proteins at the neuronal synapse. Sci. Signal. 5, jc1.
19. Ishizaki, R., Shin, H.-W., Mitsuhashi, H. and Nakayama, K. (2008). Redundant roles of BIG2 and BIG1, guanine-nucleotide exchange factors for ADPribosylation factors in membrane traffic between the trans-Golgi network and endosomes. Mol. Biol. Cell 19, 2650-2660.
20. Islam, A., Shen, X., Hiroi, T., Moss, J., Vaughan, M. and Levine, S. J. (2007). The brefeldin A-inhibited guanine nucleotide-exchange protein, BIG2, regulates the constitutive release of TNFR1 exosome-like vesicles. J. Biol. Chem. 282, 9591-9599.
21. Jakobsson, J., Ackermann, F., Andersson, F., Larhammar, D., Low, P. and Brodin, L. (2011). Regulation of synaptic vesicle budding and dynamin function by an EHD ATPase. J. Neurosci. 31, 13972-13980.
22. Johannes, L. and Popoff, V. (2008). Tracing the retrograde route in protein trafficking. Cell 135, 1175-1187.
23. Kalthoff, C., Groos, S., Kohl, R., Mahrhold, S. and Ungewickell, E. J. (2002). Clint: a novel clathrin-binding ENTH-domain protein at the Golgi. Mol. Biol. Cell 13, 4060-4073.
24. Kirchhausen, T. (2000). Clathrin. Annu. Rev. Biochem. 69, 699-727.
25. Kornfeld, S. and Mellman, I. (1989). The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5, 483-525
26. 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.
27. Lee, S., Uchida, Y., Wang, J., Matsudaira, T., Nakagawa, T., Kishimoto, T., Mukai, K., Inaba, T., Kobayashi, T., Molday, R. S. et al. (2015). Transport through recycling endosomes requires EHD1 recruitment by a phosphatidylserine translocase. EMBO J. 34, 669-688.
28. Lencer, W. I. and Tsai, B. (2003). The intracellular voyage of cholera toxin: going retro. Trends Biochem. Sci. 28, 639-645.
29. Li, J., Peters, P. J., Bai, M., Dai, J., Bos, E., Kirchhausen, T., Kandror, K. V. and Hsu, V. W. (2007). An ACAP1-containing clathrin coat complex for endocytic recycling. J. Cell Biol. 178, 453-464.
30. Lin, S. X., Mallet, W. G., Huang, A. Y. and Maxfield, F. R. (2004). Endocytosed cation-independent mannose 6-phosphate receptor traffics via the endocytic recycling compartment en route to the trans-Golgi network and a subpopulation of late endosomes. Mol. Biol. Cell. 15, 721-733.
31. Makpol, S., Zainuddin, A., Chua, K. H., Mohd Yusof, Y. A. and Ngah, W. Z. W. (2013). Gamma-tocotrienol modulated gene expression in senescent human diploid fibroblasts as revealed by microarray analysis. Oxid. Med. Cell Longev. 2013, 454328.
32. Mallard, F., Antony, C., Tenza, D., 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.
33. Matsudaira, T., Uchida, Y., Tanabe, K., Kon, S., Watanabe, T., Taguchi, T. and Arai, H. (2013). SMAP2 regulates retrograde transport from recycling endosomes to the Golgi. PLoS ONE 8, e69145.
34. McKenzie, J., Johannes, L., Taguchi, T. and Sheff, D. (2009). Passage through the Golgi is necessary for Shiga toxin B subunit to reach the endoplasmic reticulum. FEBS J. 276, 1581-1595.
35. McKenzie, J. E., Raisley, B., Zhou, X., Naslavsky, N., Taguchi, T., Caplan, S. and Sheff, D. (2012). Retromer guides STxB and CD8-M6PR from early to recycling endosomes, EHD1 guides STxB from recycling endosome to Golgi. Traffic 13, 1140-1159.
36. Mellman, I. (1996). Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 12, 575-625.
37. Meyer, C., Zizioli, D., Lausmann, S., Eskelinen, E.-L., Hamann, J., Saftig, P., von Figura, K. and Schu, P. (2000). mu1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J. 19, 2193-2203.
38. Mills, I. G., Praefcke, G. J. K., Vallis, Y., Peter, B. J., Olesen, L. E., Gallop, J. L., Butler, P. J. G., Evans, P. R. and McMahon, H. T. (2003). EpsinR: an AP1/clathrin interacting protein involved in vesicle trafficking. J. Cell Biol. 160, 213-222.
39. Misaki, R., Nakagawa, T., Fukuda, M., Taniguchi, N. and Taguchi, T. (2007). Spatial segregation of degradation-and recycling-trafficking pathways in COS-1 cells. Biochem. Biophys. Res. Commun. 360, 580-585.
40. Molloy, S. S., Thomas, L., VanSlyke, J. K., Stenberg, P. E. and Thomas, G. (1994). Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface. EMBO J. 13, 18-33.
41. Motley, A., Bright, N. A., Seaman, M. N. J. and Robinson, M. S. (2003). Clathrinmediated endocytosis in AP-2-depleted cells. J. Cell Biol. 162, 909-918.
42. Mukhopadhyay, S. and Linstedt, A. D. (2012). Manganese blocks intracellular trafficking of Shiga toxin and protects against Shiga toxicosis. Science 335, 332-335.
43. Nakai, W., Kondo, Y., Saitoh, A., Naito, T., Nakayama, K. and Shin, H.-W. (2013). ARF1 and ARF4 regulate recycling endosomal morphology and retrograde transport from endosomes to the Golgi apparatus. Mol. Biol. Cell 24, 2570-2581.
44. Natsume, W., Tanabe, K., Kon, S., Yoshida, N., Watanabe, T., Torii, T. and Satake, M. (2006). SMAP2, a novel ARF GTPase-activating protein, interacts with clathrin and clathrin assembly protein and functions on the AP-1-positive early endosome/trans-Golgi network. Mol. Biol. Cell 17, 2592-2603.
45. Ohno, H., Stewart, J., Fournier, M. C., Bosshart, H., Rhee, I., Miyatake, S., Saito, T., Gallusser, A., Kirchhausen, T. and Bonifacino, J. S. (1995). Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269, 1872-1875.
46. Pearse, B. M. and Robinson, M. S. (1984). Purification and properties of 100-kd proteins from coated vesicles and their reconstitution with clathrin. EMBO J. 3, 1951-1957.
47. Pearse, B. M. F. and Robinson, M. S. (1990). Clathrin, adaptors, and sorting. Annu. Rev. Cell Biol. 6, 151-171.
48. Peden, A. A., Park, G. Y. and Scheller, R. H. (2001). The Di-leucine motif of vesicleassociated membrane protein 4 is required for its localization and AP-1 binding. J. Biol. Chem. 276, 49183-49187.
49. Pfeffer, S. R. (2011). Entry at the trans-face of the Golgi. Cold Spring Harb. Perspect. Biol. 3, a005272.
50. Popoff, V., Mardones, G. A., Tenza, D., Rojas, R., Lamaze, C., Bonifacino, J. S., Raposo, G. and Johannes, L. (2007). The retromer complex and clathrin define an early endosomal retrograde exit site. J. Cell Sci. 120, 2022-2031.
51. Puri, S., Bachert, C., Fimmel, C. J. and Linstedt, A. D. (2002). Cycling of early Golgi proteins via the cell surface and endosomes upon lumenal pH disruption. Traffic 3, 641-653.
52. Rapoport, I., Chen, Y. C., Cupers, P., Shoelson, S. E. and Kirchhausen, T. (1998). Dileucine-based sorting signals bind to the beta chain of AP-1 at a site distinct and regulated differently from the tyrosine-based motif-binding site. EMBO J. 17, 2148-2155.
53. Rotem-Yehudar, R., Galperin, E. and Horowitz, M. (2001). Association of insulinlike growth factor 1 receptor with EHD1 and SNAP29. J. Biol. Chem. 276, 33054-33060.
54. Rothman, J. E. and Wieland, F. T. (1996). Protein sorting by transport vesicles. Science 272, 227-234.
55. Saint-Pol, A., Yélamos, B., Amessou, M., Mills, I. G., 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.
56. Sandvig, K. and van Deurs, B. (2002). Membrane traffic exploited by protein toxins. Annu. Rev. Cell Dev. Biol. 18, 1-24.
57. 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.
58. Shi, A., Sun, L., Banerjee, R., Tobin, M., Zhang, Y. and Grant, B. D. (2009). Regulation of endosomal clathrin and retromer-mediated endosome to Golgi retrograde transport by the J-domain protein RME-8. EMBO J. 28, 3290-3302.Taguchi, T. (2013). Emerging roles of recycling endosomes. J. Biochem. 153, 505-510.
59. Stanley, K. K. and Howell, K. E. (1993). TGN38/41: a molecule on the move. Trends Cell Biol. 3, 252-255.
60. Stearns, T., Willingham, M. C., Botstein, D. and Kahn, R. A. (1990). ADPribosylation factor is functionally and physically associated with the Golgi complex. Proc. Natl. Acad. Sci. USA 87, 1238-1242.
61. Taguchi, T. (2013). Emerging roles of recycling endosomes. J. Biochem. 153, 505-510. Takatsu, H., Yoshino, K., Toda, K. and Nakayama, K. (2002). GGA proteins associate with Golgi membranes through interaction between their GGAH domains and ADP-ribosylation factors. Biochem. J. 365, 369-378
62. Traub, L. M. (2003). Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J. Cell Biol. 163, 203-208.
63. Tsuchiya, M., Price, S. R., Tsai, S. C., Moss, J. and Vaughan, M. (1991). Molecular identification of ADP-ribosylation factor mRNAs and their expression in mammalian cells. J. Biol. Chem. 266, 2772-2777.
64. Uchida, Y., Hasegawa, J., Chinnapen, D., Inoue, T., Okazaki, S., Kato, R., Wakatsuki, S., Misaki, R., Koike, M., Uchiyama, Y. et al. (2011). Intracellular phosphatidylserine is essential for retrograde membrane traffic through endosomes. Proc. Natl. Acad. Sci. USA 108, 15846-15851.
65. Valdivia, R. H., Baggott, D., Chuang, J. S. and Schekman, R. W. (2002). The yeast clathrin adaptor protein complex 1 is required for the efficient retention of a subset of late Golgi membrane proteins. Dev. Cell. 2, 283-294.
66. Volpicelli-Daley, L. A., Li, Y., Zhang, C.-J. and Kahn, R. A. (2005). Isoformselective effects of the depletion of ADP-ribosylation factors 1-5 on membrane traffic. Mol. Biol. Cell 16, 4495-4508.