Diacidic motifs influence the export of transmembrane proteins from the endoplasmic reticulum in plant cells

Plant Cell

Volumn 17, Issue 11, 2005, Pages 3081-3093

  Hanton, Sally L ^a   Renna, Luciana ^a   Bortolotti, Lauren E ^a   Chatre, Laurent ^a   Stefano, Giovanni ^a   Brandizzi, Federica ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; PLANTS (BOTANY);

DIACIDIC MOTIFS; ENDOPLASMIC RETICULUM; PROTEIN TRAFFICKING; TRANSMEMBRANE PROTEINS;

PROTEINS;

AMINO ACIDS; CELLS; PLANTS; PROTEINS;

MAMMALIA;

EID: 33645968400     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.105.034900     Document Type: Article

References (60)

1. Andreeva, A.V., Zheng, H., Saint-Jore, C.M., Kutuzov, M.A., Evans, D.E., and Hawes, C.R. (2000). Organization of transport from endoplasmic reticulum to Golgi in higher plants. Biochem. Soc. Trans. 28, 505-512.
2. Aridor, M., Bannykh, S.I., Rowe, T., and Balch, W.E. (1999). Cargo can modulate COPII vesicle formation from the endoplasmic reticulum. J. Biol. Chem. 274, 4389-4399.
3. 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.
4. Aridor, M., Weissman, J., Bannykh, S., Nuoffer, C., and Balch, W.E. (1998). Cargo selection by the COPII budding machinery during export from the ER. J. Cell Biol. 141, 61-70.
5. Baldwin, T.C., Handford, M.G., Yuseff, M.I., Orellana, A., and Dupree, P. (2001). Identification and characterization of GONST1, a Golgi-localized GDP-mannose transporter in Arabidopsis. Plant Cell 13, 2283-2295.
6. Barlowe, C. (2003). Signals for COPII-dependent export from the ER: What's the ticket out? Trends Cell Biol. 13, 295-300.
7. Batoko, H., Zheng, H.Q., Hawes, C., and Moore, I. (2000). A rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell 12, 2201-2218.
8. Benghezal, M., Wasteneys, G.O., and Jones, D.A. (2000). The C-terminal dilysine motif confers endoplasmic reticulum localization to type I membrane proteins in plants. Plant Cell 12, 1179-1201.
9. Brandizzi, F., Frangne, N., Marc-Martin, S., Hawes, C., Neuhaus, J.M., and Paris, N. (2002a). The destination for single-pass membrane proteins is influenced markedly by the length of the hydrophobic domain. Plant Cell 14, 1077-1092.
10. Brandizzi, F., Hanton, S., DaSilva, L.L., Boevink, P., Evans, D., Oparka, K., Denecke, J., and Hawes, C. (2003). ER quality control can lead to retrograde transport from the ER lumen to the cytosol and the nucleoplasm in plants. Plant J. 34, 269-281.
11. Brandizzi, F., Snapp, E.L., Roberts, A.G., Lippincott-Schwartz, J., and Hawes, C. (2002b). 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.
12. Campbell, J.L., and Schekman, R. (1997). Selective packaging of cargo molecules into endoplasmic reticulum-derived COPII vesicles, Proc. Natl. Acad. Sci. USA 94, 837-842.
13. Contreras, I., Ortiz-Zapater, E., and Aniento, F. (2004a), Sorting signals in the cytosolic tail of membrane proteins involved in the interaction with plant ARF1 and coatomer. Plant J. 38, 685-698.
14. Contreras, I., Yang, Y., Robinson, D.G., and Aniento, F. (2004b). Sorting signals in the cytosolic tail of plant p24 proteins involved in the interaction with the COPII coat. Plant Cell Physiol. 45, 1779-1786.
15. 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.
16. 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.
17. daSilva, L.L., Taylor, J.P., Hadlington, J.L., Hanton, S.L., Snowden, C.J., Fox, S.J., Foresti, O., Brandizzi, F., and Denecke, J. (2005). Receptor salvage from the prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell 17, 132-148.
18. Denecke, J., Botterman, J., and Deblaere, R. (1990). Protein secretion in plant cells can occur via a default pathway. Plant Cell 2, 51-59.
19. Denecke, J., De Rycke, R., and Botterman, J. (1992). Plant and mammalian sorting signals for protein retention in the endoplasmic reticulum contain a conserved epitope. EMBO J. 11, 2345-2355.
20. Denecke, J., Goldman, M.H., Demolder, J., Seurinck, J., and Botterman, J. (1991). The tobacco luminal binding protein is encoded by a multigene family. Plant Cell 3, 1025-1035.
21. Dominguez, M., Dejgaard, K., Fullekrug, J., Dahan, S., Fazel, A., Paccaud, J.P., Thomas, D.Y., Bergeron, J.J., and Nilsson, T. (1998). gp25L/emp24/p24 protein family members of the cis-Golgi network bind both COP I and II coatomer. J. Cell Biol. 140, 751-765.
22. Driouich, A., Zhang, G.F., and Staehelin, L.A. (1993). Effect of brefeldin A on the structure of the Golgi apparatus and on the synthesis and secretion of proteins and polysaccharides in sycamore maple (Acer pseudoplatanus) suspension-cultured cells. Plant Physiol. 101, 1363-1373.
23. Epping, E.A., and Moye-Rowley, W.S. (2002). Identification of interdependent signals required for anterograde traffic of the ATP-binding cassette transporter protein Yor1p. J. Biol. Chem. 277, 34860-34869.
24. Fiedler, K., and Rothman, J.E. (1997). Sorting determinants in the transmembrane domain of p24 proteins. J. Biol. Chem. 272, 24739-24742.
25. Gillingham, A.K., and Munro, S. (2003). Long coiled-coil proteins and membrane traffic. Biochim. Biophys. Acta 1641, 71-85.
26. Gillingham, A.K., Pfeifer, A.C., and Munro, S. (2002). CASP, the alternatively spliced product of the gene encoding the CCAAT-displacement protein transcription factor, is a Golgi membrane protein related to giantin. Mol. Biol. Cell 13, 3761-3774.
27. Giraudo, C.G., and Maccioni, H.J. (2003). Endoplasmic reticulum export of glycosyltransferases depends on interaction of a cytoplasmic dibasic motif with Sar1. Mol. Biol. Cell 14, 3753-3766.
28. Gomez, L., and Chrispeels, M.J. (1993). Tonoplast and soluble vacuolar proteins are targeted by different mechanisms. Plant Cell 5, 1113-1124.
29. Handford, M.G., Sicilia, F., Brandizzi, F., Chung, J.H., and Dupree, P. (2004). Arabidopsis thaliana expresses multiple Golgi-localised nucleotide-sugar transporters related to GONST1. Mol. Genet. Genomics 272, 397-410.
30. Hanton, S.L., Bortolotti, L.E., Renna, L., Stefano, G., and Brandizzi, F. (2005). Crossing the divide-transport between the endoplasmic reticulum and Golgi apparatus in plants. Traffic 6, 267-277.
31. Haseloff, J., Siemering, K.R., Prasher, D.C., and Hodge, S. (1997). Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl. Acad. Sci. USA 94, 2122-2127.
32. Hofte, H., and Chrispeels, M.J. (1992). Protein sorting to the vacuolar membrane. Plant Cell 4, 995-1004.
33. Jiang, L.W., and Rogers, J.C. (1998). Integral membrane protein sorting to vacuoles in plant cells: Evidence for two pathways. J. Cell Biol. 143, 1183-1199.
34. Kappeler, F., Klopfenstein, D.R., Foguet, M., Paccaud, J.P., and Hauri, H.P. (1997). 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, 31801-31808.
35. Kuehn, M.J., Herrmann, J.M., and Schekman, R. (1998). COPII-cargo interactions direct protein sorting into ER-derived transport vesicles. Nature 391, 187-190.
36. Lee, H.I., Gal, S., Newman, T.C., and Raikhel, N.V. (1993). The Arabidopsis endoplasmic reticulum retention receptor functions in yeast. Proc. Natl. Acad. Sci. USA 90, 11433-11437.
37. Lee, M.H., Min, M.K., Lee, Y.J., Jin, J.B., Shin, D.H., Kim, D.H., Lee, K.H., and Hwang, I. (2002). ADP-ribosylation factor 1 of Arabidopsis plays a critical role in intracellular trafficking and maintenance of endoplasmic reticulum morphology in Arabidopsis. Plant Physiol. 129, 1507-1520.
38. Ma, D., Zerangue, N., Lin, Y.F., Collins, A., Yu, M., Jan, Y.N., and Jan, L.Y. (2001). Role of ER export signals in controlling surface potassium channel numbers. Science 291, 316-319.
39. Malkus, P., Jiang, F., and Schekman, R. (2002). Concentrative sorting of secretory cargo proteins into COPII-coated vesicles. J. Cell Biol. 159, 915-921.
40. Miller, E.A., Beilharz, T.H., Malkus, P.N., Lee, M.C., Hamamoto, S., Orci, L., and Schekman, R. (2003). Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 114, 497-509.
41. Miranda, M., Sorkina, T., Grammatopoulos, T.N., Zawada, W.M., and Sorkin, A. (2004). Multiple molecular determinants in the carboxyl terminus regulate dopamine transporter export from endoplasmic reticulum. J. Biol. Chem. 279, 30760-30770.
42. Misumi, Y., Sohda, M., Tashiro, A., Sato, H., and Ikehara, Y. (2001). An essential cytoplasmic domain for the Golgi localization of coiled-coil proteins with a COOH-terminal membrane anchor. J. Biol. Chem. 276, 6867-6873.
43. Mossessova, E., Bickford, L.C., and Goldberg, J. (2003). SNARE selectivity of the COPII coat. Cell 114, 483-495.
44. Nakamura, N., Yamazaki, S., Sato, K., Nakano, A., Sakaguchi, M., and Mihara, K. (1998). Identification of potential regulatory elements for the transport of Emp24p. Mol. Biol. Cell 9, 3493-3503.
45. Nishimura, N., and Balch, W.E. (1997). A di-acidic signal required for selective export from the endoplasmic reticulum. Science 277, 556-558.
46. Nishimura, N., Bannykh, S., Slabough, S., Matteson, J., Altschuler, Y., Hahn, K., and Balch, W.E. (1999). A di-acidic (DXE) code directs concentration of cargo during export from the endoplasmic reticulum. J. Biol. Chem. 274, 15937-15946.
47. 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.
48. Paulhe, F., Imhof, B.A., and Wehrle-Haller, B. (2004). A specific endoplasmic reticulum export signal drives transport of stem cell factor (Kitl) to the cell surface. J. Biol. Chem. 279, 55545-55555.
49. 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.
50. Renna, L., Hanton, S.L., Stefano, G., Bortolotti, L., Misra, V., and Brandizzi, F. (2005). Identification and characterization of AtCASP, a plant transmembrane Golgi matrix protein. Plant Mol. Biol. 58, 109-122.
51. Ritzenthaler, C., Nebenführ, A., Movafeghi, A., Stussi-Garaud, C., Behnia, L., Pimpl, P., Staehelin, L.A., and Robinson, D.G. (2002). 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.
52. Saint-Jore, C.M., Evins, J., Batoko, H., Brandizzi, F., Moore, I., and Hawes, C. (2002). Redistribution of membrane proteins between the Golgi apparatus and endoplasmic reticulum in plants is reversible and not dependent on cytoskeletal networks. Plant J. 29, 661-678.
53. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Press).
54. Sato, K., and Nakano, A. (2002). Emp47p and its close homolog Emp46p have a tyrosine-containing endoplasmic reticulum exit signal and function in glycoprotein secretion in Saccharomyces cerevisiae. Mol. Biol. Cell 13, 2518-2532.
55. Sevier, C.S., Weisz, O.A., Davis, M., and Machamer, C.E. (2000). Efficient export of the vesicular stomatitis virus G protein from the endoplasmic reticulum requires a signal in the cytoplasmic tail that includes both tyrosine-based and di-acidic motifs. Mol. Biol. Cell 11, 13-22.
56. Stockklausner, C., Ludwig, J., Ruppersberg, J.P., and Klocker, N. (2001). A sequence motif responsible for ER export and surface expression of Kir2.0 inward rectifier K(+) channels. FEBS Lett. 493, 129-133.
57. 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.
58. Votsmeier, C., and Gallwitz, D. (2001). An acidic sequence of a putative yeast Golgi membrane protein binds COPII and facilitates ER export. EMBO J. 20, 6742-6750.
59. Wang, X., Mattesern, J., An, Y., Moyer, B., Yoo, J.S., Bannykh, S., Wilson, I.A., Riordan, J.R., and Balch, W.E. (2004). COPII-dependent export of cystic fibrosis transmembrane conductance regulator from the ER uses a di-acidic exit code. J. Cell Biol. 167, 65-74.
60. Yuasa, K., Toyooka, K., Fukuda, H., and Matsuoka, K. (2005). Membrane-anchored prolyl hydroxylase with an export signal from the endoplasmic reticulum. Plant J. 41, 81-94.