Dynamics of COPII vesicles and the Golgi apparatus in cultured Nicotiana tabacum BY-2 cells provides evidence for transient association of Golgi stacks with endoplasmic reticulum exit sites

Plant Cell

Volumn 17, Issue 5, 2005, Pages 1513-1531

  Yang, Yao Dong ^a   Elamawi, Rabab ^b   Bubeck, Julia ^a   Pepperkok, Rainer ^c   Ritzenthaler, Christophe ^b   Robinson, David G ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b INST DE BIOL MOLEC DES PLANTES   (France)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

IMAGING SYSTEMS; MORPHOLOGY; MUTAGENESIS; PERTURBATION TECHNIQUES; PLANTS (BOTANY); TOBACCO; YEAST;

ENDOPLASMIC RETICULUM (ER); GOLGI APPARATUS; GOLGI STACKS; IMAGING DATA;

CELLS;

ANATOMY; CELLS; IMAGE ANALYSIS; MUTAGENS; PLANTS; TOBACCO; YEASTS;

EUKARYOTA; MAMMALIA; NICOTIANA TABACUM;

EID: 26844472700     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.104.026757     Document Type: Article

References (85)

1. An, G., Ebert, P.R., Mitra, A., and Ho, S. B. (1988). Binary vectors. In Plant Molecular Biology Manual, S.B. Gelvin and R.A. Schilperoort, eds (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 3-7.
2. Andreeva, A.V., Kutuzov, M.A., Evans, D.E., and Hawes, C.R. (1998). Proteins involved in membrane transport between the ER and the Golgi apparatus: 21 putative plant homologues revealed by dbEST searching. Cell Biol. Int. 22, 145-160.
3. Antonny, B., and Schekman, R. (2001). ER export: Public transportation by the COPII coach. Curr. Opin. Cell Biol. 13, 438-443.
4. Aoyama, T., and Chua, N. (1997). A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11, 605-612.
5. Aridor, M., and Balch, W.E. (2000). Kinase signaling initiates coat complex II (COPII) recruitment and export from the mammalian endoplasmic reticulum. J. Biol. Chem. 275, 35673-35676.
6. Aridor, M., Fish, K.N., Bannykh, S., Weissman, J., Roberts, T.H., Lippincott-Schwartz, J., and Balch, W.E. (2001). The Sar1 GTPase coordinates biosynthetic cargo selection with endoplasmic reticulum export site assembly. J. Cell Biol. 152, 213-229.
7. Bannykh, S.I., Rowe, T., and Balch, W.E. (1996). The organization of endoplasmic reticulum export complexes. J. Cell Biol. 135, 19-35.
8. Barlowe, C. (1998). COPII and selective export from the endoplasmic reticulum. Biochim. Biophys. Acta 1404, 67-76.
9. Barlowe, C. (2002). COPII-dependent transport from the endoplasmic reticulum. Curr. Opin. Cell Biol. 14, 417-422.
10. Barlowe, C. (2003). Signals for COPII-dependent export from the ER: What's the ticket out? Trends Cell Biol. 13, 295-300.
11. Barlowe, C., Orci, L., Yeung, T., Hosobuchi, M., Hamamoto, S., Salama, N., Rexach, M.F., Ravazzola, M., Amherdt, M., and Schekman, R. (1994). COPII: A membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895-907.
12. Barlowe, C., and Schekman, R. (1993). SEC12 encodes a guanine-nucleotide-exchange factor essential for transport vesicle budding from the ER. Nature 365, 347-349.
13. Bar-Peled, M., and Raikhel, N.V. (1997). Characterization of AtSEC12 and AtSAR1. Proteins likely involved in endoplasmic reticulum and Golgi transport. Plant Physiol. 114, 315-324.
14. Bevis, B.J., Hammond, A.T., Reinke, C.A., and Glick, B.S. (2002). De novo formation of transitional ER sites and Golgi structures in Pichia pastoris. Nat. Cell Biol. 4, 750-756.
15. Bi, X., Corpina, R.A., and Goldberg, J. (2002). Structure of the Sec23/24-Sar1 pre-budding complex of the COPII vesicle coat. Nature 419, 271-277.
16. Boevink, P., Oparka, K., Santa Cruz, S., Martin, B., Betteridge, A., and Hawes, C. (1998). Stacks on tracks: The plant Golgi apparatus traffics on an actin/ER network. Plant J. 15, 441-447.
17. Bonifacino, J.S., and Glick, B.S. (2004). The mechanisms of vesicle budding and fusion. Cell 116, 153-166.
18. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
19. Brandizzi, F., and Hawes, C. (2004). A long and winding road: Symposium on membrane trafficking in plants. EMBO Rep. 5, 245-249.
20. Brandizzi, F., Snapp, E.L., Roberts, A.G., Lippincott-Schwartz, J., and Hawes, C. (2002). Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: Evidence from selective photobleaching. Plant Cell 14, 1293-1309.
21. Campbell, R.E., Tour, O., Palmer, A.E., Steinbach, P.A., Baird, G.S., Zacharias, D.A., and Tsien, R.Y. (2002). A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99, 7877-7882.
22. Contreras, I., Ortiz-Zapater, E., and Aniento, F. (2004). Sorting signals in the cytosolic tail of membrane proteins involved in the interaction with plant ARF1 and coatomer. Plant J. 38, 685-698.
23. Contreras, I., Ortiz-Zapater, E., Castilho, L.M., and Aniento, F. (2000). Characterization of Cop I coat proteins in plant cells. Biochem. Biophys. Res. Commun. 273, 176-182.
24. Craig, S., and Staehelin, L.A. (1988). High pressure freezing of intact plant tissues. Evaluation and characterization of novel features of the endoplasmic reticulum and associated membrane systems. Eur. J. Cell Biol. 46, 81-93.
25. Crofts, A.J., Leborgne-Castel, N., Hillmer, S., Robinson, D.G., Phillipson, B., Carlsson, L.E., Ashford, D.A., and Denecke, J. (1999). Saturation of the endoplasmic reticulum retention machinery reveals anterograde bulk flow. Plant Cell 11, 2233-2248.
26. daSilva, L.L., Snapp, E.L., Denecke, J., Lippincott-Schwartz, J., Hawes, C., and Brandizzi, F. (2004). Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant Cell 16, 1753-1771.
27. Denecke, J., Botterman, J., and Deblaere, R. (1990). Protein secretion in plant cells can occur via a default pathway. Plant Cell 2, 51-59.
28. Duden, R. (2003). ER-to-Golgi transport: COP I and COP II function (Review). Mol. Membr. Biol. 20, 197-207.
29. Enninga, J., Levay, A., and Fontoura, B.M. (2003). Sec13 shuttles between the nucleus and the cytoplasm and stably interacts with Nup96 at the nuclear pore complex. Mol. Cell. Biol. 23, 7271-7284.
30. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., Delbarre, A., Ueda, T., Nakano, A., and Jurgens, G. (2003). The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219-230.
31. Geldner, N., Richter, S., Vieten, A., Marquardt, S., Torres-Ruiz, R.A., Mayer, U., and Jurgens, G. (2004). Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development 131, 389-400.
32. Hammond, A.T., and Glick, B.S. (2000). Dynamics of transitional endoplasmic reticulum sites in vertebrate cells. Mol. Biol. Cell 11, 3013-3030.
33. Hawes, C., and Brandizzi, F. (2004). The Golgi apparatus - Still causing problems after all these years! Cell. Mol. Life Sci. 61, 131-132.
34. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S., and Mollineaux, P.M. (2000). pGreen: A versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819-832.
35. Horstmann, H., Ng, C.P., Tang, B.L., and Hong, W. (2002). Ultrastructural characterization of endoplasmic reticulum-Golgi transport containers (EGTC). J. Cell Sci. 115, 4263-4273.
36. Jürgens, G. (2004). Membrane trafficking in plants. Annu. Rev. Cell Dev. Biol. 20, 481-504.
37. Klumperman, J. (2000). Transport between ER and Golgi. Curr. Opin. Cell Biol. 12, 445-449.
38. Ladinsky, M.S., Mastronarde, D.N., McIntosh, J.R., Howell, K.E., and Staehelin, L.A. (1999). Golgi structure in three dimensions: Functional insights from the normal rat kidney cell. J. Cell Biol. 144, 1135-1149.
39. Laporte, C., Vetter, G., Loudes, A.M., Robinson, D.G., Hillmer, S., Stussi-Garaud, C., and Ritzenthaler, C. (2003). Involvement of the secretory pathway and the cytoskeleton in intracellular targeting and tubule assembly of Grapevine fanleaf virus movement protein in tobacco BY-2 cells. Plant Cell 15, 2058-2075.
40. Lee, M.C.S., Miller, E.A., Goldberg, J., Orci, L., and Schekman, R. (2004). Bi-directional protein transport between the ER and Golgi. Annu. Rev. Cell Dev. Biol. 20, 87-123.
41. Miller, E., Antonny, B., Hamamoto, S., and Schekman, R. (2002). Cargo selection into COPII vesicles is driven by the Sec24p subunit. EMBO J. 21, 6105-6113.
42. Mogelsvang, S., Gomez-Ospina, N., Soderholm, J., Glick, B.S., and Staehelin, L.A. (2003). Tomographic evidence for continuous turnover of Golgi cisternae in Pichia pastoris. Mol. Biol. Cell 14, 2277-2291.
43. Mossessova, E., Bickford, L.C., and Goldberg, J. (2003). SNARE selectivity of the COPII coat. Cell 114, 483-495.
44. Movafeghi, A., Happel, N., Pimpl, P., Tai, G.H., and Robinson, D.G. (1999). Arabidopsis Sec21p and Sec23p homologs. Probable coat proteins of plant COP-coated vesicles. Plant Physiol. 119, 1437-1446.
45. Murshid, A., and Presley, J.F. (2004). ER-to-Golgi transport and cytoskeletal interactions in animal cells. Cell. Mol. Life Sci. 61, 133-145.
46. Nebenführ, A., Frohlick, J.A., and Staehelin, L.A. (2000). Redistribution of Golgi stacks and other organelles during mitosis and cytokinesis in plant cells. Plant Physiol. 124, 135-151.
47. Nebenführ, A., Gallagher, L.A., Dunahay, T.G., Frohlick, J.A., Mazurkiewicz, A.M., Meehl, J.B., and Staehelin, L.A. (1999). Stop-and-go movements of plant Golgi stacks are mediated by the actomyosin system. Plant Physiol. 121, 1127-1142.
48. Nebenführ, A., Ritzenthaler, C., and Robinson, D.G. (2002). Brefeldin A: Deciphering an enigmatic inhibitor of secretion. Plant Physiol. 130, 1102-1108.
49. Neumann, U., Brandizzi, F., and Hawes, C. (2003). Protein transport in plant cells: In and out of the Golgi. Ann. Bot. (Lond.) 92, 167-180.
50. Orci, L., Ravazzola, M., Meda, P., Holcomb, C., Moore, H.P., Hicke, L., and Schekman, R. (1991). Mammalian Sec23p homologue is restricted to the endoplasmic reticulum transitional cytoplasm. Proc. Natl. Acad. Sci. USA 88, 8611-8615.
51. Otte, S., and Barlowe, C. (2002). The Erv41p-Erv46p complex: Multiple export signals are required in trans for COPII-dependent transport from the ER. EMBO J. 21, 6095-6104.
52. Otte, S., Belden, W.J., Heidtman, M., Liu, J., Jensen, O.N., and Barlowe, C. (2001). Erv41p and Erv46p: New components of COPII vesicles involved in transport between the ER and Golgi complex. J. Cell Biol. 152, 503-518.
53. Palade, G. (1975). Intracellular aspects of the process of protein synthesis. Science 189, 347-358.
54. Pavelka, M., and Robinson, D.G. (2003). The Golgi apparatus in mammalian and higher plant cells: A comparison. In The Golgi Apparatus and the Plant Secretory Pathway, D.G. Robinson, ed (Oxford: Blackwell Publishing), pp. 16-35.
55. Peyroche, A., Antonny, B., Robineau, S., Acker, J., Cherfils, J., and Jackson, C.L. (1999). Brefeldin A acts to stabilize an abortive ARF-GDP-Sec7 domain protein complex: Involvement of specific residues of the Sec7 domain. Mol. Cell 3, 275-285.
56. Phair, R.D., and Misteli, T. (2000). High mobility of proteins in the mammalian cell nucleus. Nature 404, 604-609.
57. Phillipson, B.A., Pimpl, P., daSilva, L.L., Crofts, A.J., Taylor, J.P., Movafeghi, A., Robinson, D.G., and Denecke, J. (2001). Secretory bulk flow of soluble proteins is efficient and COPII dependent. Plant Cell 13, 2005-2020.
58. Pimpl, P., Movafeghi, A., Coughlan, S., Denecke, J., Hillmer, S., and Robinson, D.G. (2000). In situ localization and in vitro induction of plant COPI-coated vesicles. Plant Cell 12, 2219-2236.
59. Prescott, A.R., Farmaki, T., Thomson, C., James, J., Paccaud, J.P., Tang, B.L., Hong, W., Quinn, M., Ponnambalam, S., and Lucocq, J. (2001). Evidence for prebudding arrest of ER export in animal cell mitosis and its role in generating Golgi partitioning intermediates. Traffic 2, 321-335.
60. Puri, S., and Linstedt, A.D. (2003). Capacity of the Golgi apparatus for biogenesis from the endoplasmic reticulum. Mol. Biol. Cell 14, 5011-5018.
61. Ritzenthaler, C., Laporte, C., Gaire, F., Dunoyer, P., Schmitt, C., Duval, S., Piequet, A., Loudes, A.M., Rohfritsch, O., Stussi-Garaud, C., and Pfeiffer, P. (2002b). Grapevine fanleaf virus replication occurs on endoplasmic reticulum-derived membranes. J. Virol. 76, 8808-8819.
62. Ritzenthaler, C., Nebenführ, A., Movafeghi, A., Stussi-Garaud, C., Behnia, L., Pimpl, P., Staehelin, L.A., and Robinson, D.G. (2002a). Reevaluation of the effects of brefeldin A on plant cells using tobacco Bright Yellow 2 cells expressing Golgi-targeted green fluorescent protein and COPI antisera. Plant Cell 14, 237-261.
63. Rossanese, O.W., Soderholm, J., Bevis, B.J., Sears, I.B., O'Connor, J., Williamson, E.K., and Glick, B.S. (1999). Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae. J. Cell Biol. 145, 69-81.
64. Rust, R.C., Landmann, L., Gosert, R., Tang, B.L., Hong, W., Hauri, H.P., Egger, D., and Bienz, K. (2001). Cellular COPII proteins are involved in production of the vesicles that form the poliovirus replication complex. J. Virol. 75, 9808-9818.
65. Seemann, J., Pypaert, M., Taguchi, T., Malsam, J., and Warren, G. (2002). Partitioning of the matrix fraction of the Golgi apparatus during mitosis in animal cells. Science 295, 848-851.
66. Segui-Simarro, J.M., Austin II, J.R., White, E., and Staehelin, L.A. (2004). Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16, 836-856.
67. Sesso, A., de Faria, F.P., Iwamura, E.S., and Correa, H. (1994). A three-dimensional reconstruction study of the rough ER-Golgi interface in serial thin sections of the pancreatic acinar cell of the rat. J. Cell Sci. 107, 517-528.
68. Shorter, J., and Warren, G. (2002). Golgi architecture and inheritance. Annu. Rev. Cell Dev. Biol. 18, 379-420.
69. Shugrue, C.A., Kolen, E.R., Peters, H., Czernik, A., Kaiser, C., Matovcik, L., Hubbard, A.L., and Gorelick, F. (1999). Identification of the putative mammalian orthologue of Sec31P, a component of the COPII coat. J. Cell Sci. 112, 4547-4556.
70. Siniossoglou, S., Lutzmann, M., Santos-Rosa, H., Leonard, K., Mueller, S., Aebi, U., and Hurt, E. (2000). Structure and assembly of the Nup84p complex. J. Cell Biol. 149, 41-54.
71. Soderholm, J., Bhattacharyya, D., Strongin, D., Markovitz, V., Connerly, P.L., Reinke, C.A., and Glick, B.S. (2004). The transitional ER localization mechanism of Pichia pastoris Sec12. Dev. Cell 6, 649-659.
72. Staehelin, L.A. (1997). The plant ER: A dynamic organelle composed of a large number of discrete functional domains. Plant J. 11, 1151-1165.
73. Stephens, D.J. (2003). De novo formation, fusion and fission of mammalian COPII-coated endoplasmic reticulum exit sites. EMBO Rep. 4, 210-217.
74. Stephens, D.J., Lin-Marq, N., Pagano, A., Pepperkok, R., and Paccaud, J.P. (2000). COPI-coated ER-to-Golgi transport complexes segregate from COPII in close proximity to ER exit sites. J. Cell Sci. 113, 2177-2185.
75. Stephens, D.J., and Pepperkok, R. (2001). Illuminating the secretory pathway: When do we need vesicles? J. Cell Sci. 114, 1053-1059.
76. Supek, F., Madden, D.T., Hamamoto, S., Orci, L., and Schekman, R. (2002). Sec16p potentiates the action of COPII proteins to bud transport vesicles. J. Cell Biol. 158, 1029-1038.
77. Takeuchi, M., Ueda, T., Sato, K., Abe, H., Nagata, T., and Nakano, A. (2000). A dominant negative mutant of sar1 GTPase inhibits protein transport from the endoplasmic reticulum to the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J. 23, 517-525.
78. Tang, B.L., Ong, Y.S., Huang, B., Wei, S., Wong, E.T., Qi, R., Horstmann, H., and Hong, W. (2001). A membrane protein enriched in endoplasmic reticulum exit sites interacts with COPII. J. Biol. Chem. 276, 40008-40017.
79. Tang, B.L., Zhang, T., Low, D.Y., Wong, E.T., Horstmann, H., and Hong, W. (2000). Mammalian homologues of yeast sec31p. An ubiquitously expressed form is localized to endoplasmic reticulum (ER) exit sites and is essential for ER-Golgi transport. J. Biol. Chem. 275, 13597-13604.
80. Vetter, G., Hily, J.M., Klein, E., Schmidlin, L., Haas, M., Merkle, T., and Gilmer, D. (2004). Nucleo-cytoplasmic shuttling of the beet necrotic yellow vein virus RNA-3-encoded p25 protein. J. Gen. Virol. 85, 2459-2469.
81. Ward, T.H., and Brandizzi, F. (2004). Dynamics of proteins in Golgi membranes: Comparisons between mammalian and plant cells highlighted by photobleaching techniques. Cell. Mol. Life Sci. 61, 172-185.
82. Ward, T.H., Polishchuk, R.S., Caplan, S., Hirschberg, K., and Lippincott-Schwartz, J. (2001). Maintenance of Golgi structure and function depends on the integrity of ER export. J. Cell Biol. 155, 557-570.
83. Weissman, J.T., Plutner, H., and Balch, W.E. (2001). The mammalian guanine nucleotide exchange factor mSec12 is essential for activation of the Sari GTPase directing endoplasmic reticulum export. Traffic 2, 465-475.
84. Wessel, D., and Flügge, U.I. (1984). A method for the quantitative recovery of proteins in dilute solutions in the presence of detergents and lipids. Ann. Biochem. 138, 141-143.
85. Zhang, Y.-H., and Robinson, D.G. (1986). The endomembranes of Chlamydomonas reinhardtii. A comparison of the wild type with the wall mutants CW2 and CW15. Protoplasma 133, 186-194.