The COG complex interacts directly with Syntaxin 6 and positively regulates endosome-to-TGN retrograde transport

Journal of Cell Biology

Volumn 194, Issue 3, 2011, Pages 459-472

  Laufman, Orly ^a   Hong, WanJin ^b,c   Lev, Sima ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b XIAMEN UNIVERSITY   (China)

^c INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; MEMBRANE PROTEIN; PROTEIN SUBUNIT; PROTEIN VAMP4; PROTEIN VTI1A; SNARE PROTEIN; SYNTAXIN; SYNTAXIN 16; SYNTAXIN 6; UNCLASSIFIED DRUG;

ARTICLE; CELL INTERACTION; CELL MIGRATION; CELL TRANSPORT; CONTROLLED STUDY; ENDOSOME; FEMALE; GOLGI COMPLEX; HELA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; STEADY STATE; TRANS GOLGI NETWORK;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ENDOSOMES; HEK293 CELLS; HELA CELLS; HUMANS; PROTEIN TRANSPORT; QA-SNARE PROTEINS; QB-SNARE PROTEINS; R-SNARE PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SYNTAXIN 16; TRANS-GOLGI NETWORK; VESICULAR TRANSPORT PROTEINS;

MAMMALIA;

EID: 80052572363     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201102045     Document Type: Article

References (72)

1. Amarilio, R., S. Ramachandran, H. Sabanay, and S. Lev. 2005. Differential regulation of endoplasmic reticulum structure through VAP-Nir protein interaction. J. Biol. Chem. 280:5934-5944
2. Amessou, M., A. Fradagrada, T. Falguières, J.M. Lord, D.C. Smith, L.M. Roberts, C. Lamaze, and L. Johannes. 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
3. Bock, J.B., J. Klumperman, S. Davanger, and R.H. Scheller. 1997. Syntaxin 6 functions in trans-Golgi network vesicle trafficking. Mol. Biol. Cell. 8:1261-1271.
4. Bonifacino, J.S., and R. Rojas. 2006. Retrograde transport from endosomes to the trans-Golgi network. Nat. Rev. Mol. Cell Biol. 7:568-579
5. Braun, S., and S. Jentsch. 2007. SM-protein-controlled ER-associated degradation discriminates between different SNAREs. EMBO Rep. 8:1176-1182
6. Bruinsma, P., R.G. Spelbrink, and S.F. Nothwehr. 2004. Retrograde transport of the mannosyltransferase Och1p to the early Golgi requires a component of the COG transport complex. J. Biol. Chem. 279:39814-39823
7. Bryant, N.J., and D.E. James. 2001. Vps45p stabilizes the syntaxin homologue Tlg2p and positively regulates SNARE complex formation. EMBO J. 20:3380-3388
8. Chatterton, J.E., D. Hirsch, J.J. Schwartz, P.E. Bickel, R.D. Rosenberg, H.F. Lodish, and M. Krieger. 1999. Expression cloning of LDLB, a gene essential for normal Golgi function and assembly of the ldlCp complex. Proc. Natl. Acad. Sci. USA. 96:915-920
9. Foulquier, F., E. Vasile, E. Schollen, N. Callewaert, T. Raemaekers, D. Quelhas, J. Jaeken, P. Mills, B. Winchester, M. Krieger, et al. 2006. Conserved oligomeric Golgi complex subunit 1 deficiency reveals a previously uncharacterized congenital disorder of glycosylation type II. Proc. Natl. Acad. Sci. USA. 103:3764-3769
10. Foulquier, F., D. Ungar, E. Reynders, R. Zeevaert, P. Mills, M.T. García-Silva, P. Briones, B. Winchester, W. Morelle, M. Krieger, et al. 2007. A new inborn error of glycosylation due to a Cog8 deficiency reveals a critical role for the Cog1-Cog8 interaction in COG complex formation. Hum. Mol. Genet. 16:717-730
11. Ganley, I.G., E. Espinosa, and S.R. Pfeffer. 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
12. Ghosh, P., N.M. Dahms, and S. Kornfeld. 2003. Mannose 6-phosphate receptors: new twists in the tale. Nat. Rev. Mol. Cell Biol. 4:202-212
13. Ghosh, R.N., W.G. Mallet, T.T. Soe, T.E. McGraw, and F.R. Maxfield. 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
14. Hong, W. 2005. SNAREs and traffic. Biochim. Biophys. Acta. 1744:120-144.
15. Johannes, L., and V. Popoff. 2008. Tracing the retrograde route in protein trafficking. Cell. 135:1175-1187
16. Klumperman, J., R. Kuliawat, J.M. Griffith, H.J. Geuze, and P. Arvan. 1998. Mannose 6-phosphate receptors are sorted from immature secretory granules via adaptor protein AP-1, clathrin, and syntaxin 6-positive vesicles. J. Cell Biol. 141:359-371
17. Kranz, C., B.G. Ng, L. Sun, V. Sharma, E.A. Eklund, Y. Miura, D. Ungar, V. Lupashin, R.D. Winkel, J.F. Cipollo, et al. 2007. COG8 deficiency causes new congenital disorder of glycosylation type IIh. Hum. Mol. Genet. 16:731-741
18. Laufman, O., A. Kedan, W. Hong, and S. Lev. 2009. Direct interaction between the COG complex and the SM protein, Sly1, is required for Golgi SNARE pairing. EMBO J. 28:2006-2017
19. Lieu, Z.Z., M.C. Derby, R.D. Teasdale, C. Hart, P. Gunn, and P.A. Gleeson. 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
20. Litvak, V., D. Tian, S. Carmon, and S. Lev. 2002. Nir2, a human homolog of Drosophila melanogaster retinal degeneration B protein, is essential for cytokinesis. Mol. Cell. Biol. 22:5064-5075
21. Loh, E., and W. Hong. 2002. Sec34 is implicated in traffic from the endoplasmic reticulum to the Golgi and exists in a complex with GTC-90 and ldlBp. J. Biol. Chem. 277:21955-21961
22. Loh, E., and W. Hong. 2004. The binary interacting network of the conserved oligomeric Golgi tethering complex. J. Biol. Chem. 279:24640-24648
23. Lu, L., G. Tai, and W. Hong. 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
24. Luke, M.R., L. Kjer-Nielsen, D.L. Brown, J.L. Stow, and P.A. Gleeson. 2003. GRIP domain-mediated targeting of two new coiled-coil proteins, GCC88 and GCC185, to subcompartments of the trans-Golgi network. J. Biol. Chem. 278:4216-4226
25. Lupashin, V., and E. Sztul. 2005. Golgi tethering factors. Biochim. Biophys. Acta. 1744:325-339
26. Mallard, F., C. Antony, D. Tenza, J. Salamero, B. Goud, and L. Johannes. 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
27. Mallard, F., B.L. Tang, T. Galli, D. Tenza, A. Saint-Pol, X. Yue, C. Antony, W. Hong, B. Goud, and L. Johannes. 2002. Early/recycling endosomesto-TGN transport involves two SNARE complexes and a Rab6 isoform. J. Cell Biol. 156:653-664
28. McNew, J.A., F. Parlati, R. Fukuda, R.J. Johnston, K. Paz, F. Paumet, T.H. Söllner, and J.E. Rothman. 2000. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature. 407:153-159
29. Meyer, C., D. Zizioli, S. Lausmann, E.L. Eskelinen, J. Hamann, P. Saftig, K. von Figura, and P. Schu. 2000. mu1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J. 19:2193-2203
30. Oka, T., D. Ungar, F.M. Hughson, and M. Krieger. 2004. The COG and COPI complexes interact to control the abundance of GEARs, a subset of Golgi integral membrane proteins. Mol. Biol. Cell. 15:2423-2435
31. Oka, T., E. Vasile, M. Penman, C.D. Novina, D.M. Dykxhoorn, D. Ungar, F.M. Hughson, and M. Krieger. 2005. Genetic analysis of the subunit organization and function of the conserved oligomeric golgi (COG) complex: studies of COG5- and COG7-deficient mammalian cells. J. Biol. Chem. 280:32736-32745
32. Paumet, F., B. Brügger, F. Parlati, J.A. McNew, T.H. Söllner, and J.E. Rothman. 2001. A t-SNARE of the endocytic pathway must be activated for fusion. J. Cell Biol. 155:961-968
33. Pérez-Victoria, F.J., and J.S. Bonifacino. 2009. Dual roles of the mammalian GARP complex in tethering and SNARE complex assembly at the trans-golgi network. Mol. Cell. Biol. 29:5251-5263
34. Pérez-Victoria, F.J., G.A. Mardones, and J.S. Bonifacino. 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
35. Pérez-Victoria, F.J., C. Schindler, J.G. Magadán, G.A. Mardones, C. Delevoye, M. Romao, G. Raposo, and J.S. Bonifacino. 2010. Ang2/fat-free is a conserved subunit of the Golgi-associated retrograde protein complex. Mol. Biol. Cell. 21:3386-3395
36. Pfeffer, S.R. 1996. Transport vesicle docking: SNAREs and associates. Annu. Rev. Cell Dev. Biol. 12:441-461
37. Pfeffer, S.R. 2009. Multiple routes of protein transport from endosomes to the trans Golgi network. FEBS Lett. 583:3811-3816
38. Protopopov, V., B. Govindan, P. Novick, and J.E. Gerst. 1993. Homologs of the synaptobrevin/VAMP family of synaptic vesicle proteins function on the late secretory pathway in S. cerevisiae. Cell. 74:855-861
39. Ram, R.J., B. Li, and C.A. Kaiser. 2002. Identification of Sec36p, Sec37p, and Sec38p: components of yeast complex that contains Sec34p and Sec35p. Mol. Biol. Cell. 13:1484-1500
40. Reaves, B., M. Horn, and G. Banting. 1993. TGN38/41 recycles between the cell surface and the TGN: brefeldin A affects its rate of return to the TGN. Mol. Biol. Cell. 4:93-105.
41. Reddy, P., and M. Krieger. 1989. Isolation and characterization of an extragenic suppressor of the low-density lipoprotein receptor-deficient phenotype of a Chinese hamster ovary cell mutant. Mol. Cell. Biol. 9:4799-4806.
42. Saint-Pol, A., B. Yélamos, M. Amessou, I.G. Mills, M. Dugast, D. Tenza, P. Schu, C. Antony, H.T. McMahon, C. Lamaze, and L. Johannes. 2004. Clathrin adaptor epsinR is required for retrograde sorting on early endosomal membranes. Dev. Cell. 6:525-538
43. Sannerud, R., J. Saraste, and B. Goud. 2003. Retrograde traffic in the biosynthetic-secretory route: pathways and machinery. Curr. Opin. Cell Biol. 15:438-445
44. Sapperstein, S.K., D.M. Walter, A.R. Grosvenor, J.E. Heuser, and M.G. Waters. 1995. p115 is a general vesicular transport factor related to the yeast endoplasmic reticulum to Golgi transport factor Uso1p. Proc. Natl. Acad. Sci. USA. 92:522-526
45. Sapperstein, S.K., V.V. Lupashin, H.D. Schmitt, and M.G. Waters. 1996. Assembly of the ER to Golgi SNARE complex requires Uso1p. J. Cell Biol. 132:755-767
46. Shestakova, A., S. Zolov, and V. Lupashin. 2006. COG complex-mediated recycling of Golgi glycosyltransferases is essential for normal protein glycosylation. Traffic. 7:191-204
47. Shestakova, A., E. Suvorova, O. Pavliv, G. Khaidakova, and V. Lupashin. 2007. Interaction of the conserved oligomeric Golgi complex with t-SNARE Syntaxin5a/Sed5 enhances intra-Golgi SNARE complex stability. J. Cell Biol. 179:1179-1192
48. Smith, R.D., R. Willett, T. Kudlyk, I. Pokrovskaya, A.W. Paton, J.C. Paton, and V.V. Lupashin. 2009. The COG complex, Rab6 and COPI define a novel Golgi retrograde trafficking pathway that is exploited by SubAB toxin. Traffic. 10:1502-1517
49. Spelbrink, R.G., and S.F. Nothwehr. 1999. The yeast GRD20 gene is required for protein sorting in the trans-Golgi network/endosomal system and for polarization of the actin cytoskeleton. Mol. Biol. Cell. 10:4263-4281.
50. Subramaniam, V.N., J. Krijnse-Locker, B.L. Tang, M. Ericsson, A.R. Yusoff, G. Griffiths, and W. Hong. 1995. Monoclonal antibody HFD9 identifies a novel 28 kDa integral membrane protein on the cis-Golgi. J. Cell Sci. 108:2405-2414.
51. Südhof, T.C., and J.E. Rothman. 2009. Membrane fusion: grappling with SNARE and SM proteins. Science. 323:474-477
52. Sun, Y., A. Shestakova, L. Hunt, S. Sehgal, V. Lupashin, and B. Storrie. 2007. Rab6 regulates both ZW10/RINT-1 and conserved oligomeric Golgi complex-dependent Golgi trafficking and homeostasis. Mol. Biol. Cell. 18:4129-4142
53. Suvorova, E.S., R.C. Kurten, and V.V. Lupashin. 2001. Identification of a human orthologue of Sec34p as a component of the cis-Golgi vesicle tethering machinery. J. Biol. Chem. 276:22810-22818
54. Suvorova, E.S., R. Duden, and V.V. Lupashin. 2002. The Sec34/Sec35p complex, a Ypt1p effector required for retrograde intra-Golgi trafficking, interacts with Golgi SNAREs and COPI vesicle coat proteins. J. Cell Biol. 157:631-643
55. Tai, G., L. Lu, T.L. Wang, B.L. Tang, B. Goud, L. Johannes, and W. Hong. 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
56. Tran, T.H., Q. Zeng, and W. Hong. 2007. VAMP4 cycles from the cell surface to the trans-Golgi network via sorting and recycling endosomes. J. Cell Sci. 120:1028-1041
57. Ungar, D., T. Oka, E.E. Brittle, E. Vasile, V.V. Lupashin, J.E. Chatterton, J.E. Heuser, M. Krieger, and M.G. Waters. 2002. Characterization of a mammalian Golgi-localized protein complex, COG, that is required for normal Golgi morphology and function. J. Cell Biol. 157:405-415
58. Ungar, D., T. Oka, M. Krieger, and F.M. Hughson. 2006. Retrograde transport on the COG railway. Trends Cell Biol. 16:113-120
59. VanRheenen, S.M., X. Cao, V.V. Lupashin, C. Barlowe, and M.G. Waters. 1998. Sec35p, a novel peripheral membrane protein, is required for ER to Golgi vesicle docking. J. Cell Biol. 141:1107-1119
60. VanRheenen, S.M., X. Cao, S.K. Sapperstein, E.C. Chiang, V.V. Lupashin, C. Barlowe, and M.G. Waters. 1999. Sec34p, a protein required for vesicle tethering to the yeast Golgi apparatus, is in a complex with Sec35p. J. Cell Biol. 147:729-742
61. Walter, D.M., K.S. Paul, and M.G. Waters. 1998. Purification and characterization of a novel 13 S hetero-oligomeric protein complex that stimulates in vitro Golgi transport. J. Biol. Chem. 273:29565-29576
62. Wang, Y., G. Tai, L. Lu, L. Johannes, W. Hong, and B.L. Tang. 2005. Trans-Golgi network syntaxin 10 functions distinctly from syntaxins 6 and 16. Mol. Membr. Biol. 22:313-325
63. Wendler, F., and S. Tooze. 2001. Syntaxin 6: the promiscuous behaviour of a SNARE protein. Traffic. 2:606-611
64. Whyte, J.R., and S. Munro. 2001. The Sec34/35 Golgi transport complex is related to the exocyst, defining a family of complexes involved in multiple steps of membrane traffic. Dev. Cell. 1:527-537
65. Whyte, J.R., and S. Munro. 2002. Vesicle tethering complexes in membrane traffic. J. Cell Sci. 115:2627-2637.
66. Wiederkehr, A., J.O. De Craene, S. Ferro-Novick, and P. Novick. 2004. Functional specialization within a vesicle tethering complex: bypass of a subset of exocyst deletion mutants by Sec1p or Sec4p. J. Cell Biol. 167:875-887
67. Wu, X., R.A. Steet, O. Bohorov, J. Bakker, J. Newell, M. Krieger, L. Spaapen, S. Kornfeld, and H.H. Freeze. 2004. Mutation of the COG complex subunit gene COG7 causes a lethal congenital disorder. Nat. Med. 10:518-523
68. Wuestehube, L.J., R. Duden, A. Eun, S. Hamamoto, P. Korn, R. Ram, and R. Schekman. 1996. New mutants of Saccharomyces cerevisiae affected in the transport of proteins from the endoplasmic reticulum to the Golgi complex. Genetics. 142:393-406.
69. Yoshino, A., S.R. Setty, C. Poynton, E.L. Whiteman, A. Saint-Pol, C.G. Burd, L. Johannes, E.L. Holzbaur, M. Koval, J.M. McCaffery, and M.S. Marks. 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
70. Zeevaert, R., F. Foulquier, J. Jaeken, and G. Matthijs. 2008. Deficiencies in subunits of the Conserved Oligomeric Golgi (COG) complex define a novel group of Congenital Disorders of Glycosylation. Mol. Genet. Metab. 93:15-21
71. Zeng, Q., T.T. Tran, H.X. Tan, and W. Hong. 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
72. Zolov, S.N., and V.V. Lupashin. 2005. Cog3p depletion blocks vesicle-mediated Golgi retrograde trafficking in HeLa cells. J. Cell Biol. 168:747-75