Competition between the golgin Imh1p and the GAP Gcs1p stabilizes activated Arl1p at the late-Golgi

Journal of Cell Science

Volumn 125, Issue 19, 2012, Pages 4586-4596

  Chen, Kuan Yu ^a   Tsai, Pei Chin ^a   Liu, Ya Wen ^a   Lee, Fang Jen S ^a  

^a NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

ADP ribosylation factor; GTPase; GTPase activating protein; Guanine nucleotide exchange factor; Trans Golgi network

Indexed keywords

ARL1P PROTEIN; CELL PROTEIN; GCS1P PROTEIN; GOLGIN; GUANOSINE TRIPHOSPHATE; IMH1P PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DIMERIZATION; FEEDBACK SYSTEM; GENE DELETION; GOLGI COMPLEX; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; YEAST;

BINDING, COMPETITIVE; DNA-BINDING PROTEINS; ENZYME ACTIVATION; GENE DELETION; GENE KNOCKOUT TECHNIQUES; GOLGI APPARATUS; GTPASE-ACTIVATING PROTEINS; GUANOSINE TRIPHOSPHATE; HYDROLYSIS; MODELS, BIOLOGICAL; MONOMERIC GTP-BINDING PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; TRANS-GOLGI NETWORK; VESICULAR TRANSPORT PROTEINS;

EID: 84872188273     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.107797     Document Type: Article

References (54)

1. Baird, G. S., Zacharias, D. A. and Tsien, R. Y. (2000). Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proc. Natl. Acad. Sci. USA 97, 11984-11989.
2. Barr, F. A. (1999). A novel Rab6-interacting domain defines a family of Golgi-targeted coiled-coil proteins. Curr. Biol. 9, 381-384.
3. Behnia, R., Panic, B., Whyte, J. R. and Munro, S. (2004). Targeting of the Arf-like GTPase Arl3p to the Golgi requires N-terminal acetylation and the membrane protein Sys1p. Nat. Cell Biol. 6, 405-413.
4. Benjamin, J. J., Poon, P. P., Drysdale, J. D., Wang, X., Singer, R. A. and Johnston, G. C. (2011). Dysregulated Arl1, a regulator of post-Golgi vesicle tethering, can inhibit endosomal transport and cell proliferation in yeast. Mol. Biol. Cell. 22, 2337-2347.
5. Bigay, J., Casella, J. F., Drin, G., Mesmin, B. and Antonny, B. (2005). ArfGAP1 responds to membrane curvature through the folding of a lipid packing sensor motif. EMBO J. 24, 2244-2253.
6. Brémond, A., Meynet, O., Mahiddine, K., Coito, S., Tichet, M., Scotlandi, K., Breittmayer, J. P., Gounon, P., Gleeson, P. A., Bernard, A. et al. (2009). Regulation of HLA class I surface expression requires CD99 and p230/golgin-245 interaction. Blood 113, 347-357.
7. Chen, K. Y., Tsai, P. C., Hsu, J. W., Hsu, H. C., Fang, C. Y., Chang, L. C., Tsai, Y. T., Yu, C. J. and Lee, F. J. (2010). Syt1p promotes activation of Arl1p at the late Golgi to recruit Imh1p. J. Cell Sci. 123, 3478-3489.
8. Clabecq, A., Henry, J. P. and Darchen, F. (2000). Biochemical characterization of Rab3-GTPase-activating protein reveals a mechanism similar to that of Ras-GAP. J. Biol. Chem. 275, 31786-31791.
9. D'Souza-Schorey, C. and Chavrier, P. (2006). ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347-358.
10. 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.
11. 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.
12. Drin, G., Morello, V., Casella, J. F., Gounon, P. and Antonny, B. (2008). Asymmetric tethering of flat and curved lipid membranes by a golgin. Science 320, 670-673.
13. Gillingham, A. K. and Munro, S. (2003). Long coiled-coil proteins and membrane traffic. Biochim. Biophys. Acta 1641, 71-85.
14. Gillingham, A. K. and Munro, S. (2007a). Identification of a guanine nucleotide exchange factor for Arf3, the yeast orthologue of mammalian Arf6. PLoS ONE 2, e842.
15. Gillingham, A. K. and Munro, S. (2007b). The small G proteins of the Arf family and their regulators. Annu. Rev. Cell Dev. Biol. 23, 579-611.
16. Glick, B. S. and Nakano, A. (2009). Membrane traffic within the Golgi apparatus. Annu. Rev. Cell Dev. Biol. 25, 113-132.
17. Goldberg, J. (1999). Structural and functional analysis of the ARF1-ARFGAP complex reveals a role for coatomer in GTP hydrolysis. Cell 96, 893-902.
18. Golemis, E. A. and Khazak, V. (1997). Alternative yeast two-hybrid systems. The interaction trap and interaction mating. Methods Mol. Biol. 63, 197-218.
19. Harbury, P. B., Zhang, T., Kim, P. S. and Alber, T. (1993). A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262, 1401-1407.
20. Huang, C. F., Buu, L. M., Yu, W. L. and Lee, F. J. (1999). Characterization of a novel ADP-ribosylation factor-like protein (yARL3) in Saccharomyces cerevisiae. J. Biol. Chem. 274, 3819-3827.
21. Ito, H., Fukuda, Y., Murata, K. and Kimura, A. (1983). Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168.
22. Jackson, C. L. (2003). Membrane traffic: Arl GTPases get a GRIP on the Golgi. Curr. Biol. 13, R174-R176.
23. Jackson, C. L. and Casanova, J. E. (2000). Turning on ARF: the Sec7 family of guanine-nucleotide-exchange factors. Trends Cell Biol. 10, 60-67.
24. Kahn, R. A., Cherfils, J., Elias, M., Lovering, R. C., Munro, S. and Schurmann, A. (2006). Nomenclature for the human Arf family of GTP-binding proteins: ARF, ARL, and SAR proteins. J. Cell Biol. 172, 645-650.
25. Kakinuma, T., Ichikawa, H., Tsukada, Y., Nakamura, T. and Toh, B. H. (2004). Interaction between p230 and MACF1 is associated with transport of a glycosyl phosphatidyl inositol-anchored protein from the Golgi to the cell periphery. Exp. Cell Res. 298, 388-398.
26. Kjer-Nielsen, L., Teasdale, R. D., van Vliet, C. and Gleeson, P. A. (1999). A novel Golgi-localisation domain shared by a class of coiled-coil peripheral membrane proteins. Curr. Biol. 9, 385-388.
27. Lee, F. J., Huang, C. F., Yu, W. L., Buu, L. M., Lin, C. Y., Huang, M. C., Moss, J. and Vaughan, M. (1997). Characterization of an ADP-ribosylation factor-like 1 protein in Saccharomyces cerevisiae. J. Biol. Chem. 272, 30998-31005.
28. 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.
29. Lieu, Z. Z., Lock, J. G., Hammond, L. A., La Gruta, N. L., Stow, J. L. and Gleeson, P. A. (2008). A trans-Golgi network golgin is required for the regulated secretion of TNF in activated macrophages in vivo. Proc. Natl. Acad. Sci. USA 105, 3351-3356.
30. Liu, Y. W., Huang, C. F., Huang, K. B. and Lee, F. J. (2005). Role for Gcs1p in regulation of Arl1p at trans-Golgi compartments. Mol. Biol. Cell 16, 4024-4033.
31. Lock, J. G., Hammond, L. A., Houghton, F., Gleeson, P. A. and Stow, J. L. (2005). E-cadherin transport from the trans-Golgi network in tubulovesicular carriers is selectively regulated by golgin-97. Traffic 6, 1142-1156.
32. Lowe, S. L., Wong, S. H. and Hong, W. (1996). The mammalian ARF-like protein 1 (Arl1) is associated with the Golgi complex. J. Cell Sci. 109, 209-220.
33. Lu, L. and Hong, W. J. (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.
34. Lu, L., Horstmann, H., Ng, C. and Hong, W. (2001). Regulation of Golgi structure and function by ARF-like protein 1 (Arl1). J. Cell Sci. 114, 4543-4555.
35. 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.
36. Luke, M. R., Houghton, F., Perugini, M. A. and Gleeson, P. A. (2005). The trans-Golgi network GRIP-domain proteins form alpha-helical homodimers. Biochem. J. 388, 835-841.
37. Matheson, L. A., Hanton, S. L., Rossi, M., Latijnhouwers, M., Stefano, G., Renna, L. and Brandizzi, F. (2007). Multiple roles of ADP-ribosylation factor 1 in plant cells include spatially regulated recruitment of coatomer and elements of the Golgi matrix. Plant Physiol. 143, 1615-1627.
38. Panic, B., Whyte, J. R. and Munro, S. (2003). The ARF-like GTPases Arl1p and Arl3p act in a pathway that interacts with vesicle-tethering factors at the Golgi apparatus. Curr. Biol. 13, 405-410.
39. Poon, P. P., Wang, X., Rotman, M., Huber, I., Cukierman, E., Cassel, D., Singer, R. A. and Johnston, G. C. (1996). Saccharomyces cerevisiae Gcs1 is an ADPribosylation factor GTPase-activating protein. Proc. Natl. Acad. Sci. USA 93, 10074-10077.
40. Puertollano, R., Randazzo, P. A., Presley, J. F., Hartnell, L. M. and Bonifacino, J. S. (2001). The GGAs promote ARF-dependent recruitment of clathrin to the TGN. Cell 105, 93-102.
41. Ramirez, I. B. and Lowe, M. (2009). Golgins and GRASPs: holding the Golgi together. Semin. Cell Dev. Biol. 20, 770-779.
42. 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.
43. Sacchetti, A., Subramaniam, V., Jovin, T. M. and Alberti, S. (2002). Oligomerization of DsRed is required for the generation of a functional red fluorescent chromophore. FEBS Lett. 525, 13-19.
44. Scheffzek, K., Ahmadian, M. R., Kabsch, W., Wiesmüller, L., Lautwein, A., Schmitz, F. and Wittinghofer, A. (1997). The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277, 333-338.
45. Setty, S. R., Shin, M. E., Yoshino, A., Marks, M. S. and Burd, C. G. (2003). Golgi recruitment of GRIP domain proteins by Arf-like GTPase 1 is regulated by Arf-like GTPase 3. Curr. Biol. 13, 401-404.
46. Setty, S. R., Strochlic, T. I., Tong, A. H., Boone, C. and Burd, C. G. (2004). Golgi targeting of ARF-like GTPase Arl3p requires its Nalpha-acetylation and the integral membrane protein Sys1p. Nat. Cell Biol. 6, 414-419.
47. Sherman, F., Fink, G. R. and Hicks, J. B. (1986). Methods in Yeast Genetics. New York, NY: Cold Spring Harbor Laboratory Press.
48. Shin, H. W., Kobayashi, H., Kitamura, M., Waguri, S., Suganuma, T., Uchiyama, Y. and Nakayama, K. (2005). Roles of ARFRP1 (ADP-ribosylation factor-related protein 1) in post-Golgi membrane trafficking. J. Cell Sci. 118, 4039-4048.
49. Singer-Krüger, B., Lasić, M., Bürger, A. M., Hausser, A., Pipkorn, R. and Wang, Y. (2008). Yeast and human Ysl2p/hMon2 interact with Gga adaptors and mediate their subcellular distribution. EMBO J. 27, 1423-1435.
50. Tsukada, M. and Gallwitz, D. (1996). Isolation and characterization of SYS genes from yeast, multicopy suppressors of the functional loss of the transport GTPase Ypt6p. J. Cell Sci. 109, 2471-2481.
51. Tsukada, M., Will, E. and Gallwitz, D. (1999). Structural and functional analysis of a novel coiled-coil protein involved in Ypt6 GTPase-regulated protein transport in yeast. Mol. Biol. Cell 10, 63-75.
52. Wolf, E., Kim, P. S. and Berger, B. (1997). MultiCoil: a program for predicting twoand three-stranded coiled coils. Protein Sci. 6, 1179-1189.
53. Wu, M., Lu, L., Hong, W. and Song, H. (2004). Structural basis for recruitment of GRIP domain golgin-245 by small GTPase Arl1. Nat. Struct. Mol. Biol. 11, 86-94.
54. Zahn, C., Jaschke, A., Weiske, J., Hommel, A., Hesse, D., Augustin, R., Lu, L., Hong, W., Florian, S., Scheepers, A. et al. (2008). ADP-ribosylation factor-like GTPase ARFRP1 is required for trans-Golgi to plasma membrane trafficking of Ecadherin. J. Biol. Chem. 283, 27179-27188.