FIP1/RCP binding to Golgin-97 regulates retrograde transport from recycling endosomes to the trans-Golgi network

Molecular Biology of the Cell

Volumn 21, Issue 17, 2010, Pages 3041-3053

  Jing, Jian ^a   Junutula, Jagath R ^b   Wu, Christine ^a   Burden, Jemima ^c   Matern, Hugo ^d   Peden, Andrew A ^e   Prekeris, Rytis ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b GENENTECH INC   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d EXELIXIS INC   (United States)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CARRIER PROTEIN; GOLGIN 97; PROTEIN FIP1; RAB11 PROTEIN; SHIGA TOXIN; SOMATOMEDIN B RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; ENDOSOME; HELA CELL; INTRACELLULAR TRANSPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SEQUENCE ANALYSIS; TRANS GOLGI NETWORK; TRANSPORT VESICLE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; AUTOANTIGENS; ENDOCYTOSIS; ENDOSOMES; GENE KNOCKDOWN TECHNIQUES; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RECEPTORS, TRANSFERRIN; RECOMBINANT FUSION PROTEINS; SHIGA TOXIN; TRANS-GOLGI NETWORK;

EID: 77956259226     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-04-0313     Document Type: Article

References (74)

1. Arighi, C. N., Hartnell, L. M., Aguilar, R. C., Haft, C. R., and Bonifacino, J. S. (2004). Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 165, 123-133. (Pubitemid 38649182)
2. Barbero, P., Bittova, L., and Pfeffer, S. R. (2002). Visualization of Rab9-mediated vesicle transport from endosomes to the trans-Golgi in living cells. J. Cell Biol. 156, 511-518.
3. Belenkaya, T. Y., Wu, Y., Tang, X., Zhou, B., Cheng, L., Sharma, Y. V., Yan, D., Selva, E. M., and Lin, X. (2008). The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev. Cell 14, 120-131.
4. Bonifacino, J. S., and Hurley, J. H. (2008). Retromer. Curr. Opin. Cell Biol. 20, 427-436.
5. Bonifacino, J. S., and Rojas, R. (2006). Retrograde transport from endosomes to the trans-Golgi network. Nat. Rev. Mol. Cell Biol. 7, 568-579.
6. Bujny, M. V., Popoff, V., Johannes, L., and 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, 2010-2121.
7. Burguete, A. S., Fenn, T. D., Brunger, A. T., and Pfeffer, S. R. (2008). Rab and Arl GTPase family members cooperate in the localization of the golgin GCC185. Cell 132, 286-298.
8. Carlton, J., Bujny, M., Peter, B. J., Oorschot, V. M., Rutherford, A., Mellor, H., Klumperman, J., McMahon, H. T., and Cullen, P. J. (2004). Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high- curvature membranes and 3-phosphoinositides. Curr. Biol. 14, 1791-1800.
9. Caswell, P. T., Chan, M., Lindsay, A. J., McCaffrey, M. W., Boettiger, D., and Norman, J. C. (2008). Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments. J. Cell Biol. 183, 143-155.
10. Chidambaram, S., Zimmermann, J., and 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.
11. Coudreuse, D. Y., Roel, G., Betist, M. C., Destree, O., and Korswagen, H. C. (2006). Wnt gradient formation requires retromer function in Wnt-producing cells. Science 312, 921-924.
12. Damiani, M. T., Pavarotti, M., Leiva, N., Lindsay, A. J., McCaffrey, M. W., and Colombo, M. I. (2004). Rab coupling protein associates with phagosomes and regulates recycling from the phagosomal compartment. Traffic 5, 785-797.
13. Del Nery, E., Miserey-Lenkei, S., Falguieres, T., Nizak, C., Johannes, L., Perez, F., and Goud, B. (2006). Rab6A and Rab6A′ GTPases play non-overlapping roles in membrane trafficking. Traffic 7, 394-407. (Pubitemid 43372749)
14. Demaurex, N., Furuya, W., D'Souza, S., Bonifacino, J. S., and Grinstein, S. (1998). Mechanism of acidification of the trans-Golgi network (TGN). In situ measurements of pH using retrieval of TGN38 and furin from the cell surface. J. Biol. Chem. 273, 2044-2051.
15. Derby, M. C., Lieu, Z. Z., Brown, D., Stow, J. L., Goud, B., and Gleeson, P. A. (2007). The trans-Golgi network golgin, GCC185, is required for endosome-to-Golgi transport and maintenance of Golgi structure. Traffic 8, 758-773.
16. Diaz, E., and Pfeffer, S. R. (1998). TIP47, a cargo selection device for mannose 6-phosphate receptor trafficking. Cell 93, 433-443.
17. Diaz, E., Schimmoller, F., and Pfeffer, S. R. (1997). A novel Rab9 effector required for endosome-to-TGN transport. J. Cell Biol. 138, 283-290.
18. Fan, G. H., Lapierre, L. A., Goldenring, J. R., Sai, J., and Richmond, A. (2004). Rab11-family interacting protein 2 and myosin Vb are required for CXCR2 recycling and receptor-mediated chemotaxis. Mol. Biol. Cell 15, 2456-2469.
19. Fielding, A. B., Schonteich, E., Matheson, J., Wilson, G., Yu, X., Hickson, G. R., Srivastava, S., Baldwin, S. A., Prekeris, R., and Gould, G. W. (2005). Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J. 24, 3389-3399.
20. Franch-Marro, X., Wendler, F., Guidato, S., Griffith, J., Baena-Lopez, A., Itasaki, N., Maurice, M. M., and Vincent, J. P. (2008). Wingless secretion requires endosome-to-Golgi retrieval of Wntless/Evi/Sprinter by the retromer complex. Nat. Cell Biol. 10, 170-177.
21. Ganley, I. G., Espinosa, E., and 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.
22. 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.
23. Gillingham, A. K., and Munro, S. (2003). Long coiled-coil proteins and membrane traffic. Biochim Biophys Acta 1641, 71-85. (Pubitemid 36952588)
24. Griffiths, G., Hoflack, B., Simons, K., Mellman, I., and Kornfeld, S. (1988). The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell 52, 329-341. (Pubitemid 18057394)
25. Hales, C. M., Griner, R., Hobdy-Henderson, K. C., Dorn, M. C., Hardy, D., Kumar, R., Navarre, J., Chan, E. K., Lapierre, L. A., and Goldenring, J. R. (2001). Identification and characterization of a family of Rab11-interacting proteins. J. Biol. Chem. 276, 39067-39075.
26. Hales, C. M., Vaerman, J. P., and Goldenring, J. R. (2002). Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling. J. Biol. Chem. 277, 50415-50421.
27. Hettema, E. H., Lewis, M. J., Black, M. W., and Pelham, H. R. (2003). Retromer and the sorting nexins Snx4/41/42 mediate distinct retrieval pathways from yeast endosomes. EMBO J. 22, 548-557.
28. Hickson, G. R., Matheson, J., Riggs, B., Maier, V. H., Fielding, A. B., Prekeris, R., Sullivan, W., Barr, F. A., and Gould, G. W. (2003). Arfophilins are dual Arf/Rab 11 binding proteins that regulate recycling endosome distribution and are related to Drosophila nuclear fallout. Mol. Biol. Cell. 14, 2908-2920.
29. Horgan, C. P., Oleksy, A., Zhdanov, A. V., Lall, P. Y., White, I. J., Khan, A. R., Futter, C. E., McCaffrey, J. G., and McCaffrey, M. W. (2007). Rab11-FIP3 is critical for the structural integrity of the endosomal recycling compartment. Traffic 8, 414-430.
30. Inoue, H., Ha, V. L., Prekeris, R., and Randazzo, P. A. (2008). Arf GTPase-activating protein ASAP1 interacts with Rab11 effector FIP3 and regulates pericentrosomal localization of transferrin receptor-positive recycling endosome. Mol. Biol. Cell 19, 4224-4237.
31. Jin, M., and Goldenring, J. R. (2006). The Rab11-FIP1/RCP gene codes for multiple protein transcripts related to the plasma membrane recycling system. Biochim. Biophys. Acta 1759, 281-295.
32. Jing, J., and Prekeris, R. (2009). Polarized endocytic transport: the roles of Rab11 and Rab11-FIPs in regulating cell polarity. Histol. Histopathol. Cell. Mol. Biol. 24(9), 1171-1180.
33. Junutula, J. R., Schonteich, E., Wilson, G. M., Peden, A. A., Scheller, R. H., and Prekeris, R. (2004). Molecular characterization of Rab11 interactions with members of the family of Rab11-interacting proteins. J. Biol. Chem. 279, 33430-33437.
34. 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.
35. Lieu, Z. Z., Derby, M. C., Teasdale, R. D., Hart, C., Gunn, P., and 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.
36. Lindsay, A. J., Hendrick, A. G., Cantalupo, G., Senic-Matuglia, F., Goud, B., Bucci, C., and McCaffrey, M. W. (2002). Rab coupling protein (RCP), a novel Rab4 and Rab11 effector protein. J. Biol. Chem. 277, 12190-12199.
37. Lu, L., and Hong, W. (2003). Interaction of Arl1-GTP with GRIP domains recruits autoantigens Golgin-97 and Golgin-245/p230 onto the Golgi. Mol. Biol. Cell 14, 3767-3781.
38. 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.
39. Lu, L., Tai, G., Wu, M., Song, H., and Hong, W. (2006). Multilayer interactions determine the Golgi localization of GRIP golgins. Traffic 7, 1399-1407. (Pubitemid 44364177)
40. Ludwig, T., Ovitt, C. E., Bauer, U., Hollinshead, M., Remmler, J., Lobel, P., Ruther, U., and Hoflack, B. (1993). Targeted disruption of the mouse cation-dependent mannose 6-phosphate receptor results in partial missorting of multiple lysosomal enzymes. EMBO J. 12, 5225-5235. (Pubitemid 23358513)
41. Lupashin, V., and Sztul, E. (2005). Golgi tethering factors. Biochim. Biophys. Acta 1744, 325-339.
42. 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. (Pubitemid 28547397)
43. Mallard, F., Tang, B. L., Galli, T., Tenza, D., Saint-Pol, A., Yue, X., Antony, C., Hong, W., 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. (Pubitemid 34839881)
44. Mallet, W. G., and Maxfield, F. R. (1999). Chimeric forms of furin and TGN38 are transported with the plasma membrane in the trans-Golgi network via distinct endosomal pathways. J. Cell Biol. 146, 345-359.
45. Metcalf, D. J., Calvi, A. A., Seaman, M., Mitchison, H. M., and Cutler, D. F. (2008). Loss of the Batten disease gene CLN3 prevents exit from the TGN of the mannose 6-phosphate receptor. Traffic 9, 1905-1914.
46. Meyers, J. M., and Prekeris, R. (2002). Formation of mutually exclusive Rab11 complexes with members of the family of Rab11-interacting proteins regulates Rab11 endocytic targeting and function. J. Biol. Chem. 277, 49003-49010.
47. Miller, S. E., Collins, B. M., McCoy, A. J., Robinson, M. S., and Owen, D. J. (2007). A SNARE-adaptor interaction is a new mode of cargo recognition in clathrin-coated vesicles. Nature 450, 570-574.
48. Munro, S., and Nichols, B. J. (1999). The GRIP domain - a novel Golgi-targeting domain found in several coiled-coil proteins. Curr. Biol. 9, 377-380.
49. Panic, B., Perisic, O., Veprintsev, D. B., Williams, R. L., and Munro, S. (2003). Structural basis for Arl1-dependent targeting of homodimeric GRIP domains to the Golgi apparatus. Mol. Cell 12, 863-874. (Pubitemid 37352780)
50. Peden, A. A., Schonteich, E., Chun, J., Junutula, J. R., Scheller, R. H., and Prekeris, R. (2004). The RCP-Rab11 complex regulates endocytic protein sorting. Mol. Biol. Cell 15, 3530-3541.
51. 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. (Pubitemid 47009998)
52. Port, F., Kuster, M., Herr, P., Furger, E., Banziger, C., Hausmann, G., and Basler, K. (2008). Wingless secretion promotes and requires retromer-dependent cycling of Wntless. Nat. Cell Biol. 10, 178-185.
53. Prekeris, R., Klumperman, J., and Scheller, R. H. (2000). A Rab11/Rip11 protein complex regulates apical membrane trafficking via recycling endosomes. Mol. Cell 6, 1437-1448.
54. Reddy, J. V., Burguete, A. S., Sridevi, K., Ganley, I. G., Nottingham, R. M., and Pfeffer, S. R. (2006). A functional role for the GCC185 golgin in mannose 6-phosphate receptor recycling. Mol. Biol. Cell 17, 4353-4363.
55. Rohn, W. M., Rouille, Y., Waguri, S., and Hoflack, B. 2000. Bi-directional trafficking between the trans-Golgi network and the endosomal/lysosomal system. J. Cell Sci. 113(Pt 12), 2093-2101. (Pubitemid 30426824)
56. Rojas, R., Kametaka, S., Haft, C. R., and Bonifacino, J. S. (2007). Interchangeable but essential functions of SNX1 and SNX2 in the association of retromer with endosomes and the trafficking of mannose 6-phosphate receptors. Mol. Cell. Biol. 27, 1112-1124.
57. Rojas, R., van Vlijmen, T., Mardones, G. A., Prabhu, Y., Rojas, A. L., Mohammed, S., Heck, A. J., Raposo, G., van der Sluijs, P., and Bonifacino, J. S. (2008). Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol. 183, 513-526.
58. Saint-Pol, A., et al. (2004). Clathrin adaptor epsinR is required for retrograde sorting on early endosomal membranes. Dev. Cell. 6, 525-538.
59. Sandvig, K., and van Deurs, B. (2005). Delivery into cells: lessons learned from plant and bacterial toxins. Gene Ther. 12, 865-872. (Pubitemid 40852204)
60. Schonteich, E., Pilli, M., Simon, G. C., Matern, H. T., Junutula, J. R., Sentz, D., Holmes, R. K., and Prekeris, R. (2007). Molecular characterization of Rab11-FIP3 binding to ARF GTPases. Eur. J. Cell Biol. 86, 417-431.
61. Schonteich, E., Wilson, G. M., Burden, J., Hopkins, C. R., Anderson, K., Goldenring, J. R., and Prekeris, R. (2008). The Rip11/Rab11-FIP5 and kinesin II complex regulates endocytic protein recycling. J. Cell Sci. 121, 3824-3833.
62. Seaman, M. N. (2004). Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165, 111-122.
63. Seaman, M. N. (2005). Recycle your receptors with retromer. Trends Cell Biol. 15, 68-75.
64. Seaman, M. N. (2007). Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J. Cell Sci. 120, 2378-2389.
65. Seaman, M. N., Marcusson, E. G., Cereghino, J. L., and Emr, S. D. (1997). Endosome to Golgi retrieval of the vacuolar protein sorting receptor, Vps10p, requires the function of the VPS29, VPS30, and VPS35 gene products. J. Cell Biol. 137, 79-92.
66. Simon, G. C., Schonteich, E., Wu, C. C., Piekny, A., Ekiert, D., Yu, X., Gould, G. W., Glotzer, M., and Prekeris, R. (2008). Sequential Cyk-4 binding to ECT2 and FIP3 regulates cleavage furrow ingression and abscission during cytokinesis. EMBO J. 27, 1791-1803. (Pubitemid 351960209)
67. Tran, T. H., Zeng, Q., and 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. (Pubitemid 46638516)
68. Utskarpen, A., Slagsvold, H. H., Dyve, A. B., Skanland, S. S., and Sandvig, K. (2007). SNX1 and SNX2 mediate retrograde transport of Shiga toxin. Biochem. Biophys. Res. Commun. 358, 566-570.
69. Welsh, G. I., Leney, S. E., Lloyd-Lewis, B., Wherlock, M., Lindsay, A. J., McCaffrey, M. W., and Tavare, J. M. (2007). Rip11 is a Rab11- and AS160-RabGAP-binding protein required for insulin-stimulated glucose uptake in adipocytes. J. Cell Sci. 120, 4197-4208.
70. 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.
71. Wilson, G. M., Fielding, A. B., Simon, G. C., Yu, X., Andrews, P. D., Hames, R. S., Frey, A. M., Peden, A. A., Gould, G. W., and Prekeris, R. (2005). The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis. Mol. Biol. Cell 16, 849-860.
72. Wu, S., Mehta, S. Q., Pichaud, F., Bellen, H. J., and Quiocho, F. A. (2005). Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo. Nat. Struct. Mol. Biol. 12, 879-885.
73. Yoshino, A., et al. (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. (Pubitemid 40872849)
74. Zhang, X. M., Ellis, S., Sriratana, A., Mitchell, C. A., and Rowe, T. (2004). Sec15 is an effector for the Rab11 GTPase in mammalian cells. J. Biol. Chem. 279, 43027-43034.