Sorting signals in the cytosolic tail of membrane proteins involved in the interaction with plant ARF1 and coatomer

Plant Journal

Volumn 38, Issue 4, 2004, Pages 685-698

  Contreras, Inmaculada ^a   Ortiz Zapater, Elena ^a   Aniento, Fernando ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

Author keywords

ARF1; COPI; Dilysine motifs; Endoplasmic reticulum localization; p24 family proteins; Plant coatomer

Indexed keywords

BIOASSAY; CELL MEMBRANES; GAMMA RAYS; HISTOLOGY; PROTEINS; SORTING;

MAMMALS; MEMBRANE PROTEINS;

PLANTS (BOTANY);

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; COATOMER PROTEIN; MEMBRANE PROTEIN; PEPTIDE FRAGMENT; PROTEIN SUBUNIT; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CHEMISTRY; KINETICS; METABOLISM; PHYSIOLOGY; PROTOPLAST; RICE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ADP-RIBOSYLATION FACTOR 1; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BINDING SITES; COATOMER PROTEIN; KINETICS; MEMBRANE PROTEINS; ORYZA SATIVA; PEPTIDE FRAGMENTS; PLANT PROTEINS; PROTEIN SUBUNITS; PROTOPLASTS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 2542632045     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02075.x     Document Type: Article

References (81)

1. Andersson, H., Kappeler, F. and Hauri, H.P. (1999) Protein targeting to endoplasmic reticulum by dilysine signals involves direct retention in addition to retrieval. J. Biol. Chem. 274, 15080-15084.
2. Aniento, F., Gu, F., Parton, R.G. and Gruenberg, J. (1996) An endosomal β-COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J. Cell Biol. 133, 29-41.
3. Aniento, F., Helms, B. and Memon, A. (2003) Howto make a vesicle: coat protein-membrane interactions. In The Golgi Apparatus and the Plant Secretory Pathway. Annual Plant Reviews 9 (Robinson, D.G., ed.). Oxford: Blackwell Publishing, pp. 36-62.
4. Arondel, V., Lemieux, B., Hwang, I., Gibson, S., Goodman, H.M. and Somerville, C.R. (1992) Map-based cloning of a gene controlling omega-3 fatty acid desaturation in Arabidopsis. Science, 258, 1353-1355.
5. Bahaji, A., Cornejo, M.J., Ortiz-Zapater, E., Contreras, I. and Aniento, F. (2001) Uptake of endocytic markers by rice cells: variations related to the growth phase. Eur. J. Cell Biol. 80, 178-186.
6. Barlowe, C. (2002) COPII-dependent transport from the endoplasmic reticulum. Curr. Opin. Cell Biol. 14, 417-422.
7. Beiden, W.J. and Barlowe, C. (1996) Erv25p, a component of COP II-coated vesicles, forms a complex with Emp24 that is required for efficient endoplasmic reticulum to Golgi transport. J. Biol. Chem. 271, 26939-26946.
8. Beiden, W.J. and Barlowe, C. (2001) Distinct roles for the cytoplasmic tail sequences of Emp24p and Erv25p in transport between the endoplasmic reticulum and Golgi complex. J. Biol. Chem. 276, 43040-43048.
9. 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.
10. Bermak, J.C., Li, M., Bullock, C., Weingarten, P. and Zhou, Q.Y. (2002) Interaction of gamma-COP with a transport motif in the D1 receptor C-terminus. Eur. J. Cell Biol. 81, 77-85.
11. Chardin, P. and McCormick, F. (1999) Brefeldin A: the advantage of being uncompetitive. Cell, 97, 153-155.
12. 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.
13. Cosson, P. and Letourneur, F. (1994) Coatomer interaction with dilysine endoplasmic reticulum retention motifs. Science, 263, 1629-1631.
14. Cosson, P., Démollière, C., Hennecke, S., Duden, R. and Letourneur, F. (1996) δ- and ζ-COP, two coatomer subunits homologous to clathrin-associated proteins, are involved in ER-retrieval. EMBO J. 15, 1792-1798.
15. Cosson, P., Lefkir, Y., Démollière, C. and Letourneur, F. (1998) New COP1-binding motifs involved in ER retrieval. EMBO J. 17, 6863-6870.
16. Couchy, I., Bolte, S., Crosnier, M.-T., Brown, S. and Satiat-Jeunemaitre, B. (2003) Identification of a β-COP-like protein involved in the morphodynamics of the plant Golgi apparatus. J. Exp. Bot. 54, 2053-2063.
17. Dogic, D., Dubois, A., de Chassey, B., Lefkir, Y. and Letourneur, F. (2001) ERGIC-53 KKAA signal mediates endoplasmic reticulum retrieval in yeast. Eur. J. Cell Biol. 80, 151-155.
18. 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 COPI and COPII coatomer. J. Cell Biol. 140, 751-765.
19. Emery, G., Rojo, M. and Gruenberg, J. (2000) Coupled transport of p24 family members. J. Cell Sci. 113, 2507-2516.
20. Fiedler, K., Veit, M., Stamnes, M.A. and Rothman, J.E. (1996) Bimodal interaction of coatomer with the p24 family of putative cargo receptors. Science, 273, 1396-1399.
21. Füllerkrug, J., Suganuma, T., Tang, B.L., Hong, W., Storrie, B. and Nilsson, T. (1999) Localization and recycling of gp27 (hp24g3): complex formation with other p24 family members. Mol. Biol. Cell, 10, 1939-1955.
22. 7-sterol-C-5-desaturase from yeast. Plant J. 8, 407-416.
23. Gaynor, E.C., te Heesen, S., Graham, T.R., Aebi, M. and Emr, S. (1994) Signal-mediated retrieval of a membrane protein from the Golgi to the ER in yeast. J. Cell Biol. 127, 653-665.
24. 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.
25. Goldberg, J. (1998) Structural basis for activation of ARF GTPase: mechanisms of guanine nucleotide exchange and GTP-myristoyl switching. Cell, 95, 237-248.
26. Goldberg, J. (2000) Decoding of sorting signals by coatomer through a GTPase switch in the COPI coat complex. Cell, 100, 671-679.
27. Gómez, M., Scales, S.J., Kreis, T.E. and Pérez, F. (2000) Membrane recruitment of coatomer and binding to dilysine signals are separate events. J. Biol. Chem. 275, 29162-29169.
28. Gommel, D., Orci, L., Emig, E.M., Hannah, M.J., Ravazzola, M., Nickel, W., Helms, J.B., Wieland, F.T. and Sohn, K. (1999) p24 and p23, the major transmembrane proteins of COPI-coated vesi- cles, form hetero-oligomeric complexes and cycle between organelles of the early secretory pathway. FEBS Lett. 447, 179-185.
29. Gommel, D., Memon, A.R., Heiss, A., Lottspeich, F., Pfannstiel, J., Lechner, J., Reinhard, C., Helms, J.B., Nickel, W. and Wieland, F.T. (2001) Recruitment to Golgi membranes of ADP-ribosylation factor 1 is mediated by the cytoplasmic domain of p23. EMBO J. 20, 6751-6760.
30. Grebenok, R.J., Ohnmeiss, T.E., Yamamoto, A., Huntley, E.D., Galbraith, D.W. and Della Penna, D. (1998) Isolation and characterization of an Arabidopsis thaliana C-8,7 sterol isomerase: functional and structural similarities to mammalian C-8,7 sterol isomerase/emopanil-binding protein. Plant Mol. Biol. 38, 807-815.
31. Gu, F., Aniento, F., Parton, R.G. and Gruenberg, J. (1997) Functional dissection of COP-1 subunits in the biogenesis of multi-vesicular endosomes. J. Cell. Biol. 139, 1183-1195.
32. Guo, Q., Vasile, E. and Krieger, M. (1994) Disruptions in Golgi structure and membrane traffic in a conditional lethal mammalian cell mutant are corrected by epsilon-COP. J. Cell Biol. 125, 1213-1224.
33. Hardt, B. and Bause, E. (2002) Lysine can be replaced by histidine but not by arginine as the ER retrieval motif for type I membrane proteins. Biochem. Biophys. Res. Commun. 291, 751-757.
34. Harter, C. and Wieland, F.T. (1998) A single binding site for dilysine retrieval motifs and p23 within the γ-subunits of coatomer. Proc. Natl. Acad. Sci. USA, 95, 11649-11654.
35. Harter, C., Pavel, J., Coccia, F., Draken, E., Wegehingel, S., Tschochner, H. and Wieland, F. (1996) Nonclathrin coat protein γ, a subunit of coatomer, binds to the cytoplasmic dilysine motif of membrane proteins of the early secretory pathway. Proc. Natl. Acad. Sci. USA, 93, 1902-1906.
36. Hobbie, L., Fisher, A.S., Lee, S., Flint, A. and Krieger. M. (1994) Isolation of three classes of conditional lethal Chinese hamster ovary cell mutants with temperature-dependent defects in low density lipoprotein receptor stability and intracellular membrane transport. J. Biol. Chem. 269, 20958-20970.
37. Jackson, M.R., Nilsson, T. and Peterson, P.A. (1990) Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum. EMBO J. 9, 3153-3162.
38. Jackson, M.R., Nilsson, T. and Peterson, P.A. (1993) Retrieval of transmembrane proteins to the endoplasmic reticulum. J. Cell Biol. 121, 317-333.
39. Jenne, N., Frey, K., Brügger, B. and Wieland, F.T. (2002) Oligomeric state and stoichiometry of p24 proteins in the early secretory pathway. J. Biol. Chem. 277, 46504-46511.
40. Jones, D.A., Thomas, C.M., Hammond-Kosack, K.E., Balint-Kurti, P.J. and Jones, J.D.G. (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science, 266, 789-793.
41. Kappeler, F., Klopfenstein, D.R.C., 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.
42. Kopka, J., Ludewig, M. and Müller-Röber, B. (1997) Complementary DNAs encoding eukaryotic-type cytidine-5′-diphosphate- diacylglycerol synthases of two plant species. Plant Physiol. 113, 997-1002.
43. Lanoix, J., Ouwendijk, J., Lin, C.C., Stark, A., Love, H.D., Ostermann, J. and Nilsson, T. (1999) GTP hydrolysis by arf-1 mediates sorting and concentration of Golgi resident enzymes into functional COPI vesicles. EMBO J. 18, 4935-4948.
44. Lanoix, J., Ouwendijk, J., Stark, A., Szafer, E., Cassel, D., Dejgaard, K., Weiss, M. and Nilsson, T. (2001) Sorting of Golgi resident proteins into different subpopulations of COPI vesicles: a role for ArfGAP. J. Cell Biol. 155, 1199-1212.
45. 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.
46. Letourneur, F., Gaynor, E.C., Hennecke, S., Demolliere, C., Duden, R., Emr, S.D., Riezman, H. and Cosson, P. (1994) Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell, 79, 1199-1207.
47. 2+-ATPase in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA, 94, 8579-8584.
48. Lowe, M. and Kreis, T.E. (1995) In vitro assembly and disassembly of coatomer. J. Biol. Chem. 270, 31364-31371.
49. Majoul, I., Straub, M., Hell, S.W., Duden, R. and Soling, H.D. (2001) KDEL-cargo regulates interactions between proteins involved in COPI vesicle traffic: measurements in living cells using FRET. Dev. Cell. 1, 139-153.
50. Martínez-Menárguez, J.A., Prekeris, R., Oorschot, V.M.J., Scheller, R., Slot, J.W., Geuze, H.J. and Klumperman, J. (2001) Peri-Golgi vesicles contain retrograde but not anterograde proteins consistent with the cisternal progression model of intra-Golgi transport. J. Cell Biol. 155, 1213-1224.
51. Marzioch, M., Henthorn, D.C., Herrmann, J.M., Wilson, R., Thomas, D.Y., Bergeron, J.J., Solari, R.C. and Rowley, A. (1999) Erp1p and Erp2p, partners for Emp24p and Erv25p in a yeast p24 complex. Mol. Biol. Cell, 10, 1923-1938.
52. 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, 1437-1445.
53. Nebenführ, A. (2003) Intra-Golgi transport: escalator or bucket brigade? In The Golgi Apparatus and the Plant Secretory Pathway. Annual Plant Reviews 9 (Robinson, D.G. ed.). Oxford: Blackwell Publishing, pp. 76-89.
54. Nebenführ, A., Ritzenthaler, C. and Robinson, D.G. (2002) Brefeldin A: deciphering an enigmatic inhibitor of secretion. Plant Physiol. 130, 1102-1108.
55. Nickel, W., Sohn, K., Bunning, C. and Wieland, F. (1997) p23, a major COPI-vesicle membrane protein, constitutively cycles through the early secretory pathway. Proc. Natl. Acad. Sci. USA, 94, 11393-11398.
56. Nickel, W., Brugger, B. and Wieland, F. (2002) Vesicular transport: the core machinery of COPI recruitment and budding. J. Cell Sci. 115, 3235-3240.
57. Nilsson, T., Jackson, M. and Peterson, P.A. (1989) Short cytoplasmic sequences serve as retention signals for transmembrane proteins in the endoplasmic reticulum. Cell, 58, 707-718.
58. Orci, L., Stammes, M., Ravazzola, M., Amhert, M., Perrelet, A., Sollner, T.H. and Rothman, J.E. (1997) Bidirectional transport by distinct populations of COPI-coated vesicles. Cell, 90, 335-349.
59. Orci, L., Amherdt, M., Ravazzola, M., Perrelet, A. and Rothman, J.E. (2000) Exclusion of Golgi residents from transport vesicles budding from Golgi cisternae in intact cells. J. Cell Biol. 150, 1263-1270.
60. Ostermann, J., Orci, L., Tani, K., Amherdt, M., Ravazzola, M., Elazar, Z. and Rothman, J.E. (1993) Stepwise assembly of functionally active transport vesicles. Cell, 75, 1015-1025.
61. Pavel, J., Harter, C. and Wieland, F.T. (1998) Reversible dissociation of coatomer: functional characterization of a β/δ-coat protein subcomplex. Proc. Natl. Acad. Sci. USA, 95, 2140-2145.
62. Pepperkok, R., Scheel, J., Horstmann, H., Hauri, H.P., Griffiths, G. and Kreis, T.E. (1993) β-COP is essential for biosynthetic membrane transport from the endoplasmic reticulum to the Golgi complex in vivo. Cell, 74, 71-82.
63. 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, 2219-2235.
64. Ritzenthaler, C., Nebenführ, A., Movafeghi, A., Stussi-Garaud, C., Behnia, L., Pimpl, P., Staehelin, 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.
65. Rojo, M., Peperkok, R., Emery, G., Kellner, R., Stang, E., Parton, R.G. and Gruenberg, J. (1997) Involvement of the transmembrane protein p23 in biosynthetic protein transport. J. Cell Biol. 139, 1119-1135.
66. Rojo, M., Emery, G., Marjomäki, V., McDowall, A., Parton, R.G. and Gruenberg, J. (2000) The transmembrane protein p23 contributes to the organization of the Golgi apparatus. J. Cell Sci. 113, 1043-1057.
67. Scales, S.J., Pepperkok, R. and Kreis, T.E. (1997) Visualization of ER to Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell, 90, 1137-1148.
68. Schimmöller, F., Singer-Krüger, B., Schröder, S., Krüger, U., Barlowe, C. and Riezman, H. (1995) The absence of Em24p, a component of ER-derived COPII-coated vesicles, causes a defect in transport of selected proteins to the Golgi. EMBO J. 14, 1329-1339.
69. Schutze, M.-P., Peterson, P.A. and Jackson, M.R. (1994) An N-terminal double-arginine motif maintains type II membrane proteins in the endoplasmic reticulum. EMBO J. 13, 1696-1705.
70. Serafini, T., Stenbeck, G., Brecht, A., Lottspeich, F., Orci, L., Rothman, J.E. and Wieland, F.T. (1991) A coat subunit of Golgi-derived non-clathrin-coated vesicles with homology to the clathrin-coated vesicle coat protein beta-adaptin. Nature, 349, 215-220.
71. Sohn, K., Orci, L., Ravazzola, M., Amherdt, M., Brunner, M., Kahn, R.A. and Rothman, J.E. (1996) A major transmembrane protein of Golgi-derived COPI-coated vesicles involved in coatomer binding. J. Cell Biol. 135, 1239-1248.
72. Stamnes, M.A., Craighead, M.W., Hoe, M.H., Lampen, N., Geromanos, S., Tempst, P. and Rothman, J.E. (1995) An integral membrane components of coatomer-coated transport vesicles defines a family of proteins involved in budding. Proc. Natl. Acad. Sci. USA, 92, 8011-8015.
73. Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, C.L., Paris, S., Gälweiler, L., Palme, K. and Jürgens, G. (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science, 286, 316-318.
74. Takeuchi, M., Ueda, T., Yahara, N. and Nakano, A. (2002) Arf1 GTPase plays roles in the protein traffic between the endoplasmic reticulum and the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J. 31, 499-515.
75. Thomas, C.M., Jones, D.A., Parniske, M., Harrison, K., Balint-Kurti, P.J., Hatzixanthis, K. and Jones, J.D.G. (1997) Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell, 9, 2209-2224.
76. Waters, M.G., Serafini, T. and Rothman, J.E. (1991) A cytosolic protein complex containing subunits of non-clathrin coated Golgi transport vesicles. Nature, 349, 248-251.
77. Whitney, J.A., Gómez, M., Sheff, D., Kreis, T.E. and Mellman, I. (1995) Cytoplasmic coat proteins involved in endosome function. Cell, 83, 703-713.
78. 2+-ATPase: primary structure and regulation of mRNA abundance by salt. Proc. Natl. Acad. Sci. USA, 89, 9205-9209.
79. Yadav, N.S., Wierzbicki, A., Aegerter, M., Caster, C.S., Pérez-Grau, L., Kinney, A.J., Hitz, W.D., Booth, J.R., Jr, Schweiger, B. and Stecca, K.L. (1993) Cloning of higher plant ω-3 fatty acid desaturases. Plant Physiol. 103, 467-476.
80. Zhao, L., Helms, J.B., Brugger, B., Harter, C., Martoglio, B., Graf, R., Brunner, J. and Wieland, F.T. (1997) Direct and GTP-dependent interaction of ADP ribosylation factor 1 with coatomer subunit beta. Proc. Natl. Acad. Sci. USA, 94, 4418-4423.
81. Zhao, L., Helms, J.B., Brunner, J. and Wieland, F.T. (1999) GTP-dependent binding of ADP-ribosylation factor to coatomer in close proximity to the binding site for dilysine retrieval motifs and p23. J. Biol. Chem. 274, 14198-14203.