ER exit sites - Localization and control of COPII vesicle formation

FEBS Letters

Volumn 583, Issue 23, 2009, Pages 3796-3803

  Budnik, Annika ^a   Stephens, David J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

COPII; Endoplasmic reticulum; Golgi; Membrane traffic; Vesicle

Indexed keywords

COAT PROTEIN COMPLEX II; MEMBRANE PROTEIN; PROTEIN SEC16; UNCLASSIFIED DRUG;

BIOSYNTHESIS; CELL DIVISION; CELL MEMBRANE TRANSPORT; CELL STRUCTURE; CELLULAR DISTRIBUTION; COATED VESICLE; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; MAMMAL CELL; MITOSIS; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW;

ANIMALS; COP-COATED VESICLES; ENDOPLASMIC RETICULUM; HUMANS;

MAMMALIA;

EID: 70450225048     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2009.10.038     Document Type: Review

References (108)

1. Voeltz G.K., Rolls M.M., and Rapoport T.A. Structural organization of the endoplasmic reticulum. EMBO Rep. 3 (2002) 944-950
2. Powers E.T., Morimoto R.I., Dillin A., Kelly J.W., and Balch W.E. Biological and chemical approaches to diseases of proteostasis deficiency. Annu. Rev. Biochem. 78 (2009) 959-991
3. Barlowe C., et al. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77 (1994) 895-907
4. Palade G. Intracellular aspects of the process of protein synthesis. Science 189 (1975) 347-358
5. Bannykh S.I., Rowe T., and Balch W.E. The organization of endoplasmic reticulum export complexes. J. Cell Biol. 135 (1996) 19-35
6. Orci L., Ravazzola M., Meda P., Holcomb C., Moore H.P., Hicke L., and Schekman R. Mammalian Sec23p homologue is restricted to the endoplasmic reticulum transitional cytoplasm. Proc. Natl. Acad. Sci. USA 88 (1991) 8611-8615
7. Appenzeller-Herzog C., and Hauri H.P. The ER-Golgi intermediate compartment (ERGIC): in search of its identity and function. J. Cell Sci. 119 (2006) 2173-2183
8. Hughes H., and Stephens D.J. Assembly, organization, and function of the COPII coat. Histochem. Cell Biol. 129 (2008) 129-151
9. Lee M.C., and Miller E.A. Molecular mechanisms of COPII vesicle formation. Semin. Cell Dev. Biol. 18 (2007) 424-434
10. Bi X., Corpina R.A., and Goldberg J. Structure of the Sec23/24-Sar1 pre-budding complex of the COPII vesicle coat. Nature 419 (2002) 271-277
11. Bielli A., Haney C.J., Gabreski G., Watkins S.C., Bannykh S.I., and Aridor M. Regulation of Sar1 NH2 terminus by GTP binding and hydrolysis promotes membrane deformation to control COPII vesicle fission. J. Cell Biol. 171 (2005) 919-924
12. Lee M.C., Orci L., Hamamoto S., Futai E., Ravazzola M., and Schekman R. Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 122 (2005) 605-617
13. Yoshihisa T., Barlowe C., and Schekman R. Requirement for a GTPase-activating protein in vesicle budding from the endoplasmic reticulum. Science 259 (1993) 1466-1468
14. Mossessova E., Bickford L.C., and Goldberg J. SNARE selectivity of the COPII coat. Cell 114 (2003) 483-495
15. Miller E., Antonny B., Hamamoto S., and Schekman R. Cargo selection into COPII vesicles is driven by the Sec24p subunit. EMBO J. 21 (2002) 6105-6113
16. Miller E.A., Beilharz T.H., Malkus P.N., Lee M.C., Hamamoto S., Orci L., and Schekman R. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 114 (2003) 497-509
17. Lederkremer G.Z., Cheng Y., Petre B.M., Vogan E., Springer S., Schekman R., Walz T., and Kirchhausen T. Structure of the Sec23p/24p and Sec13p/31p complexes of COPII. Proc. Natl. Acad. Sci. USA 98 (2001) 10704-10709
18. Stagg S.M., Gurkan C., Fowler D.M., LaPointe P., Foss T.R., Potter C.S., Carragher B., and Balch W.E. Structure of the Sec13/31 COPII coat cage. Nature 439 (2006) 234-238
19. Oka T., and Nakano A. Inhibition of GTP hydrolysis by Sar1p causes accumulation of vesicles that are a functional intermediate of the ER-to-Golgi transport in yeast. J. Cell Biol. 124 (1994) 425-434
20. Antonny B., Gounon P., Schekman R., and Orci L. Self-assembly of minimal COPII cages. EMBO Rep. 4 (2003) 419-424
21. Bi X., Mancias J.D., and Goldberg J. Insights into COPII coat nucleation from the structure of Sec23*Sar1 complexed with the active fragment of Sec31. Dev. Cell 13 (2007) 635-645
22. Futai E., Hamamoto S., Orci L., and Schekman R. GTP/GDP exchange by Sec12p enables COPII vesicle bud formation on synthetic liposomes. EMBO J. 23 (2004) 4146-4155
23. Sato K., and Nakano A. Dissection of COPII subunit-cargo assembly and disassembly kinetics during Sar1p-GTP hydrolysis. Nat. Struct. Mol. Biol. 12 (2005) 167-174
24. Antonny B. Membrane deformation by protein coats. Curr. Opin. Cell Biol. 18 (2006) 386-394
25. Townley A.K., and Stephens D.J. Vesicle coating and uncoating - controlling the formation of large COPII-coated carriers. F1000 Biol. Rep. 1 (2009) 65
26. Matsuoka K., Orci L., Amherdt M., Bednarek S.Y., Hamamoto S., Schekman R., and Yeung T. COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. Cell 93 (1998) 263-275
27. Aridor M., and Balch W.E. Kinase signaling initiates coat complex II (COPII) recruitment and export from the mammalian endoplasmic reticulum. J. Biol. Chem. 275 (2000) 35673-35676
28. Lee T.H., and Linstedt A.D. Potential role for protein kinases in regulation of bidirectional endoplasmic reticulum-to-Golgi transport revealed by protein kinase inhibitor H89. Mol. Biol. Cell 11 (2000) 2577-2590
29. Aridor M., Weissman J., Bannykh S., Nuoffer C., and Balch W.E. Cargo selection by the COPII budding machinery during export from the ER. J. Cell Biol. 141 (1998) 61-70
30. Kuehn M.J., Herrmann J.M., and Schekman R. COPII-cargo interactions direct protein sorting into ER-derived transport vesicles. Nature 391 (1998) 187-190
31. Appenzeller C., Andersson H., Kappeler F., and Hauri H.P. The lectin ERGIC-53 is a cargo transport receptor for glycoproteins. Nat. Cell Biol. 1 (1999) 330-334
32. Nichols W.C., et al. Mutations in the ER-Golgi intermediate compartment protein ERGIC-53 cause combined deficiency of coagulation factors V and VIII. Cell 93 (1998) 61-70
33. Mitrovic S., Ben-Tekaya H., Koegler E., Gruenberg J., and Hauri H.P. The cargo receptors Surf4, endoplasmic reticulum-Golgi intermediate compartment (ERGIC)-53, and p25 are required to maintain the architecture of ERGIC and Golgi. Mol. Biol. Cell 19 (2008) 1976-1990
34. Kappeler F., Klopfenstein D.R., Foguet M., Paccaud J.P., and Hauri H.P. The recycling of ERGIC-53 in the early secretory pathway. ERGIC-53 carries a cytosolic endoplasmic reticulum-exit determinant interacting with COPII. J. Biol. Chem. 272 (1997) 31801-31808
35. Itin C., Schindler R., and Hauri H.P. Targeting of protein ERGIC-53 to the ER/ERGIC/cis-Golgi recycling pathway. J. Cell Biol. 131 (1995) 57-67
36. Schindler R., Itin C., Zerial M., Lottspeich F., and Hauri H.P. ERGIC-53, a membrane protein of the ER-Golgi intermediate compartment, carries an ER retention motif. Eur. J. Cell Biol. 61 (1993) 1-9
37. Belden W.J., and Barlowe C. Role of Erv29p in collecting soluble secretory proteins into ER-derived transport vesicles. Science 294 (2001) 1528-1531
38. Fromme J.C., and Schekman R. COPII-coated vesicles: flexible enough for large cargo?. Curr. Opin. Cell Biol. 17 (2005) 345-352
39. Saito K., et al. TANGO1 facilitates cargo loading at endoplasmic reticulum exit sites. Cell 136 (2009) 891-902
40. Boyadjiev S.A., et al. Cranio-lenticulo-sutural dysplasia is caused by a SEC23A mutation leading to abnormal endoplasmic-reticulum-to-Golgi trafficking. Nat. Genet. 38 (2006) 1192-1197
41. Fromme J.C., et al. The genetic basis of a craniofacial disease provides insight into COPII coat assembly. Dev. Cell 13 (2007) 623-634
42. Townley A.K., Feng Y., Schmidt K., Carter D.A., Porter R., Verkade P., and Stephens D.J. Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development. J. Cell Sci. 121 (2008) 3025-3034
43. Rossanese O.W., Soderholm J., Bevis B.J., Sears I.B., O'Connor J., Williamson E.K., and Glick B.S. Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae. J. Cell Biol. 145 (1999) 69-81
44. Zeuschner D., Geerts W.J., van Donselaar E., Humbel B.M., Slot J.W., Koster A.J., and Klumperman J. Immuno-electron tomography of ER exit sites reveals the existence of free COPII-coated transport carriers. Nat. Cell Biol. 8 (2006) 377-383
45. Mironov A.A., et al. ER-to-Golgi carriers arise through direct en bloc protrusion and multistage maturation of specialized ER exit domains. Dev. Cell 5 (2003) 583-594
46. Stephens D.J., and Pepperkok R. Illuminating the secretory pathway: when do we need vesicles?. J. Cell Sci. 114 (2001) 1053-1059
47. Aridor M., Fish K.N., Bannykh S., Weissman J., Roberts T.H., Lippincott-Schwartz J., and Balch W.E. The Sar1 GTPase coordinates biosynthetic cargo selection with endoplasmic reticulum export site assembly. J. Cell Biol. 152 (2001) 213-229
48. Stephens D.J., Lin-Marq N., Pagano A., Pepperkok R., and Paccaud J.P. COPI-coated ER-to-Golgi transport complexes segregate from COPII in close proximity to ER exit sites. J. Cell Sci. 113 (2000) 2177-2185
49. Hammond A.T., and Glick B.S. Dynamics of transitional endoplasmic reticulum sites in vertebrate cells. Mol. Biol. Cell 11 (2000) 3013-3030
50. Gupta, V., Palmer, K.J., Spence, P., Hudson, A. and Stephens, D.J. (in press). Kinesin-1 (uKHC/Kif5b) is required for bidirectional motility of ER exit sites and efficient ER-to-Golgi transport. Traffic 9, 1850-1866.
51. Balch W.E., McCaffery J.M., Plutner H., and Farquhar M.G. Vesicular stomatitis virus glycoprotein is sorted and concentrated during export from the endoplasmic reticulum. Cell 76 (1994) 841-852
52. Schweizer A., Matter K., Ketcham C.M., and Hauri H.P. The isolated ER-Golgi intermediate compartment exhibits properties that are different from ER and cis-Golgi. J. Cell Biol. 113 (1991) 45-54
53. Oprins A., Duden R., Kreis T.E., Geuze H.J., and Slot J.W. Beta-COP localizes mainly to the cis-Golgi side in exocrine pancreas. J. Cell Biol. 121 (1993) 49-59
54. Scales S.J., Pepperkok R., and Kreis T.E. Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell 90 (1997) 1137-1148
55. Duden R. ER-to-Golgi transport: COP I and COP II function. Mol. Membr. Biol. 20 (2003) 197-207
56. Novick P., Field C., and Schekman R. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21 (1980) 205-215
57. Novick P., Ferro S., and Schekman R. Order of events in the yeast secretory pathway. Cell 25 (1981) 461-469
58. Kaiser C.A., and Schekman R. Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway. Cell 61 (1990) 723-733
59. Espenshade P., Gimeno R.E., Holzmacher E., Teung P., and Kaiser C.A. Yeast SEC16 gene encodes a multidomain vesicle coat protein that interacts with Sec23p. J. Cell Biol. 131 (1995) 311-324
60. Gimeno R.E., Espenshade P., and Kaiser C.A. COPII coat subunit interactions: Sec24p and Sec23p bind to adjacent regions of Sec16p. Mol. Biol. Cell 7 (1996) 1815-1823
61. Shaywitz D.A., Espenshade P.J., Gimeno R.E., and Kaiser C.A. COPII subunit interactions in the assembly of the vesicle coat. J. Biol. Chem. 272 (1997) 25413-25416
62. Supek F., Madden D.T., Hamamoto S., Orci L., and Schekman R. Sec16p potentiates the action of COPII proteins to bud transport vesicles. J. Cell Biol. 158 (2002) 1029-1038
63. Connerly P.L., Esaki M., Montegna E.A., Strongin D.E., Levi S., Soderholm J., and Glick B.S. Sec16 is a determinant of transitional ER organization. Curr. Biol. 15 (2005) 1439-1447
64. Watson P., Townley A.K., Koka P., Palmer K.J., and Stephens D.J. Sec16 defines endoplasmic reticulum exit sites and is required for secretory cargo export in mammalian cells. Traffic 7 (2006) 1678-1687
65. Bhattacharyya D., and Glick B.S. Two mammalian Sec16 homologues have nonredundant functions in endoplasmic reticulum (ER) export and transitional ER organization. Mol. Biol. Cell 18 (2007) 839-849
66. Iinuma T., Shiga A., Nakamoto K., O'Brien M.B., Aridor M., Arimitsu N., Tagaya M., and Tani K. Mammalian Sec16/p250 plays a role in membrane traffic from the endoplasmic reticulum. J. Biol. Chem. 282 (2007) 17632-17639
67. Hughes H., et al. Organisation of human ER-exit sites: requirements for the localisation of Sec16 to transitional ER. J. Cell Sci. 122 (2009) 2924-2934
68. Yamaguchi M. Novel protein RGPR-p117: its role as the regucalcin gene transcription factor. Mol. Cell Biochem. 327 (2009) 53-63
69. Ivan V., de Voer G., Xanthakis D., Spoorendonk K.M., Kondylis V., and Rabouille C. Drosophila Sec16 mediates the biogenesis of tER sites upstream of Sar1 through an arginine-rich motif. Mol. Biol. Cell 19 (2008) 4352-4365
70. Ben-Tekaya H., Miura K., Pepperkok R., and Hauri H.P. Live imaging of bidirectional traffic from the ERGIC. J. Cell Sci. 118 (2005) 357-367
71. Ronchi P., Colombo S., Francolini M., and Borgese N. Transmembrane domain-dependent partitioning of membrane proteins within the endoplasmic reticulum. J. Cell Biol. 181 (2008) 105-118
72. Abrami L., Kunz B., Iacovache I., and van der Goot F.G. Palmitoylation and ubiquitination regulate exit of the Wnt signaling protein LRP6 from the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 105 (2008) 5384-5389
73. Hager K.M., Striepen B., Tilney L.G., and Roos D.S. The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. J. Cell Sci. 112 (1999) 2631-2638
74. He C.Y., Ho H.H., Malsam J., Chalouni C., West C.M., Ullu E., Toomre D., and Warren G. Golgi duplication in Trypanosoma brucei. J. Cell Biol. 165 (2004) 313-321
75. Ralston E., Ploug T., Kalhovde J., and Lomo T. Golgi complex, endoplasmic reticulum exit sites, and microtubules in skeletal muscle fibers are organized by patterned activity. J. Neurosci. 21 (2001) 875-883
76. da Silva L.L., Snapp E.L., Denecke J., Lippincott-Schwartz J., Hawes C., and Brandizzi F. Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant cell 16 (2004) 1753-1771
77. Hanton S.L., Matheson L.A., Chatre L., and Brandizzi F. Dynamic organization of COPII coat proteins at endoplasmic reticulum export sites in plant cells. Plant J. 57 (2009) 963-974
78. Hawes C., Osterrieder A., Hummel E., and Sparkes I. The plant ER-Golgi interface. Traffic 9 (2008) 1571-1580
79. Yano H., et al. Distinct functional units of the Golgi complex in Drosophila cells. Proc. Natl. Acad. Sci. USA 102 (2005) 13467-13472
80. Herpers B., and Rabouille C. MRNA localization and ER-based protein sorting mechanisms dictate the use of transitional endoplasmic reticulum-golgi units involved in gurken transport in Drosophila oocytes. Mol. Biol. Cell 15 (2004) 5306-5317
81. Kondylis, V. and Rabouille, C. (2009). The Golgi apparatus: lessons from Drosophila. FEBS Lett., doi:10.1016/j.febslet.2009.09.048.
82. Bevis B.J., Hammond A.T., Reinke C.A., and Glick B.S. De novo formation of transitional ER sites and Golgi structures in Pichia pastoris. Nat. Cell Biol. 4 (2002) 750-756
83. Aridor M., Bannykh S.I., Rowe T., and Balch W.E. Cargo can modulate COPII vesicle formation from the endoplasmic reticulum. J. Biol. Chem. 274 (1999) 4389-4399
84. Forster R., Weiss M., Zimmermann T., Reynaud E.G., Verissimo F., Stephens D.J., and Pepperkok R. Secretory cargo regulates the turnover of COPII subunits at single ER exit sites. Curr. Biol. 16 (2006) 173-179
85. Guo Y., and Linstedt A.D. COPII-Golgi protein interactions regulate COPII coat assembly and Golgi size. J. Cell Biol. 174 (2006) 53-63
86. Stephens D.J. De novo formation, fusion and fission of mammalian COPII-coated endoplasmic reticulum exit sites. EMBO Rep. 4 (2003) 210-217
87. Heinzer S., Worz S., Kalla C., Rohr K., and Weiss M. A model for the self-organization of exit sites in the endoplasmic reticulum. J. Cell Sci. 121 (2008) 55-64
88. Farhan H., Weiss M., Tani K., Kaufman R.J., and Hauri H.P. Adaptation of endoplasmic reticulum exit sites to acute and chronic increases in cargo load. EMBO J. 27 (2008) 2043-2054
89. Prescott A.R., et al. Evidence for prebudding arrest of ER export in animal cell mitosis and its role in generating Golgi partitioning intermediates. Traffic 2 (2001) 321-335
90. Altan-Bonnet N., Sougrat R., Liu W., Snapp E.L., Ward T., and Lippincott-Schwartz J. Golgi inheritance in mammalian cells is mediated through endoplasmic reticulum export activities. Mol. Biol. Cell 17 (2006) 990-1005
91. Farmaki T., Ponnambalam S., Prescott A.R., Clausen H., Tang B.L., Hong W., and Lucocq J.M. Forward and retrograde trafficking in mitotic animal cells. ER-Golgi transport arrest restricts protein export from the ER into COPII-coated structures. J. Cell Sci. 112 Pt 5 (1999) 589-600
92. Wei J.H., and Seemann J. Mitotic division of the mammalian Golgi apparatus. Semin. Cell Dev. Biol. 20 (2009) 810-816
93. Altan-Bonnet N., Phair R.D., Polishchuk R.S., Weigert R., and Lippincott-Schwartz J. A role for Arf1 in mitotic Golgi disassembly, chromosome segregation, and cytokinesis. Proc. Natl. Acad. Sci. USA 100 (2003) 13314-13319
94. Pecot M.Y., and Malhotra V. Golgi membranes remain segregated from the endoplasmic reticulum during mitosis in mammalian cells. Cell 116 (2004) 99-107
95. Bartz R., Sun L.P., Bisel B., Wei J.H., and Seemann J. Spatial separation of Golgi and ER during mitosis protects SREBP from unregulated activation. EMBO J. 27 (2008) 948-955
96. Palmer K.J., Konkel J.E., and Stephens D.J. PCTAIRE protein kinases interact directly with the COPII complex and modulate secretory cargo transport. J. Cell Sci. 118 (2005) 3839-3847
97. Wang L., and Lucocq J.M. P38 MAPK regulates COPII recruitment. Biochem. Biophys. Res. Commun. 363 (2007) 317-321
98. Rismanchi N., Puertollano R., and Blackstone C. STAM adaptor proteins interact with COPII complexes and function in ER-to-Golgi trafficking. Traffic 10 (2009) 201-217
99. Tani K., Mizoguchi T., Iwamatsu A., Hatsuzawa K., and Tagaya M. P125 is a novel mammalian Sec23p-interacting protein with structural similarity to phospholipid-modifying proteins. J. Biol. Chem. 274 (1999) 20505-20512
100. Kapetanovich L., Baughman C., and Lee T.H. Nm23H2 facilitates coat protein complex II assembly and endoplasmic reticulum export in mammalian cells. Mol Biol Cell 16 (2005) 835-848
101. Blumental-Perry A., Haney C.J., Weixel K.M., Watkins S.C., Weisz O.A., and Aridor M. Phosphatidylinositol 4-phosphate formation at ER exit sites regulates ER export. Dev. Cell 11 (2006) 671-682
102. 2+-dependent manner. Biochem. Biophys. Res. Commun. 353 (2007) 756-763
103. 2+-binding protein ALG-2 is recruited to endoplasmic reticulum exit sites by Sec31A and stabilizes the localization of Sec31A. Mol. Biol. Cell 17 (2006) 4876-4887
104. la Cour J.M., Mollerup J., and Berchtold M.W. ALG-2 oscillates in subcellular localization, unitemporally with calcium oscillations. Biochem. Biophys. Res. Commun. 353 (2007) 1063-1067
105. Watson P., Forster R., Palmer K.J., Pepperkok R., and Stephens D.J. Coupling of ER exit to microtubules through direct interaction of COPII with dynactin. Nat. Cell Biol. 7 (2005) 48-55
106. Higashio H., Sato K., and Nakano A. Smy2p participates in COPII vesicle formation through the interaction with Sec23p/Sec24p subcomplex. Traffic 9 (2008) 79-93
107. Salama N.R., Chuang J.S., and Schekman R.W. Sec31 encodes an essential component of the COPII coat required for transport vesicle budding from the endoplasmic reticulum. Mol. Biol. Cell 8 (1997) 205-217
108. Sheff D., Lowe M., Kreis T.E., and Mellman I. Biochemical heterogeneity and phosphorylation of coatomer subunits. J. Biol. Chem. 271 (1996) 7230-7236