KDEL and KKXX retrieval signals appended to the same reporter protein determine different trafficking between endoplasmic reticulum, intermediate compartment, and golgi complex

Molecular Biology of the Cell

Volumn 14, Issue 3, 2003, Pages 889-902

  Stornaiuolo, Mariano ^a   Lotti, Lavinia V ^b   Borgese, Nica ^c   Torrisi, Maria Rosaria ^b   Mottola, Giovanna ^a   Martire, Gianluca ^d   Bonatti, Stefano ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^d UNIVERSITY OF MOLISE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; MEMBRANE PROTEIN; PROTEIN KDEL; PROTEIN KKXX; UNCLASSIFIED DRUG;

ARTICLE; CELL COMPARTMENTALIZATION; ENDOPLASMIC RETICULUM; GLYCOSYLATION; GOLGI COMPLEX; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; STEADY STATE; TRANSPORT VESICLE;

ANIMALS; ANTIGENS, CD8; CELL FRACTIONATION; CELL LINE; ENDOPLASMIC RETICULUM; GENES, REPORTER; GOLGI APPARATUS; HUMANS; MICROSCOPY, ELECTRON, SCANNING; OLIGOPEPTIDES; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; TRANSPORT VESICLES;

EID: 0037339919     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-08-0468     Document Type: Article

References (55)

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. Aoe, T., Lee, A.J., van Donselaar, E., Peters, P.J., and Hsu, V.W. (1998). Modulation of intracellular transport by transported proteins: insight from regulation of COPI-mediated transport. Proc. Natl. Acad. Sci. USA 95, 1624-1629.
3. Bannykh, S.I., Rowe, T., and Balch, W.E. (1996). The organization of endoplasmic reticulum export complexes. J. Cell Biol. 135, 19-35.
4. Bonatti, S., Migliaccio, G., and Simons, K. (1989). Palmitylation of viral membrane glycoproteins takes place after exit from the endoplasmic reticulum. J. Biol. Chem. 264, 12590-12595.
5. Cosson, P., Demolliere, C., Hennecke, S., Duden, R., and Letourneur, F. (1996). δ- and ξ-COP, two coatomer subunits homologous to clathrin-associated proteins, are involved in ER retrieval. Embo. J. 15, 1792-1798.
6. Cosson, P., and Letourneur, F. (1994). Coatomer interaction with di-lysine endoplasmic reticulum retention motifs. Science 263, 1629-1631.
7. Dean, N., and Pelham, H.R. (1990). Recycling of proteins from the Golgi compartment to the ER in yeast. J. Cell Biol. 111, 369-377.
8. Dunham I., et al. (1999). The DNA sequence of human chromosome 22. Nature 402, 489-495.
9. Erra, M.C., Iodice, L., Lotti, L.V., and Bonatti, S. (1999). Cell fractionation analysis of human CD8 glycoprotein transport between endoplasmic reticulum, intermediate compartment and Golgi complex in tissue cultured cells. Cell Biol. Int. 23, 571-577.
10. Fu, J., and Kreibich, G. (2000). Retention of subunits of the oligosaccharyl-transferase complex in the endoplasmic reticulum. J. Biol. Chem. 275, 3984-3990.
11. Fu, J., Ren, M., and Kreibich, G. (1997). Interactions among subunits of the oligosaccharyl-transferase complex. J. Biol. Chem. 272, 29687-29692.
12. Gaynor, E.C., Heesen, S.T., Graham, T.R., Aebi, M., and Emr, S.D. (1994). Signal-mediated retrieval of a membrane protein from the Golgi to the ER in the yeast. J. Cell Biol. 127, 636-647.
13. Griffiths, G., Ericsson, M., Krijnse-Locker, J., Nilsson, T., Goud, B., Soling, H.D., Tang, B.L., Hong, S.H., and Hong, W. (1994). Localization of the Lys, Asp, Glu, Leu tetrapeptide receptor to the Golgi complex and the intermediate compartment in mammalian cells. J. Cell Biol. 127, 1557-1574.
14. Griffiths, G., Pepperkok, R., Locker, J.K., and Kreis, T.E. (1995). Immunocytochemical localization of beta-COP to the ER-Golgi boundary and the TGN. J. Cell Sci. 108, 2839-2856.
15. Iodice, L., Sarnataro, S., and Bonatti, S. (2001). The carboxyl-terminal valine is required for the transport of glycoprotein CD8α from the endoplasmic reticulum to the intermediate compartment. J. Biol. Chem. 276, 28920-28926.
16. 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.
17. Jackson, M.R., Nisson, T., and Peterson, P.A. (1993). Retrieval of transmembrane proteins to the endoplasmic reticulum. J. Cell Biol. 121, 317-333.
18. Klumperman, J., Schweizer, A., Clausen, H., Tang, B.L., Hong, W., Oorschot, V., and Hauri, H.P. (1998). The recycling pathway of protein ERGIC-53 and dynamics of the ER-Golgi intermediate compartment. J. Cell Sci. 111, 3411-3425.
19. 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 dilysines-tagged proteins to the endoplasmic reticulum. Cell 79, 1199-1207.
20. Lewis, M.J., and Pelham, H.R. (1990). A human homologue of the yeast HDEL receptor. Nature 348, 162-163.
21. Lewis, M.J., and Pelham, H.R. (1992). Ligand-induced redistribution of a human KDEL receptor from the Golgi complex to the endoplasmic reticulum. Cell 68, 353-364.
22. Lewis, M.J., Sweet, D.J., and Pelham, H.R. (1990). The ERD2 gene determines the specificity of the luminal ER protein retention system. Cell 61, 1359-1363.
23. Lippincott-Schwartz, J., Roberts, T.H., and Hirschberg, K. (2000). Secretory protein trafficking and organelle dynamics in living cells. Annu. Rev. Cell Dev. Biol. 16, 557-589.
24. Lotti, L.V., Mottola, G., Torrisi, M.R., and Bonatti, S. (1999). A different intracellular distribution of a single reporter protein is determined at steady state by KKXX or KDEL retrieval signals. J. Biol. Chem. 274, 10413-10420.
25. Lotti, L.V., Torrisi, M.R., Erra, M.C., and Bonatti, S. (1996). Morphological Analysis of the transfer of VSV ts-045 G glycoprotein from the endoplasmic reticulum to the intermediate compartment in Vero cells. Exp. Cell. Res. 227, 323-331.
26. 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.
27. Martinez-Menàrguez, J.A., Geuze, H.J., Slot, J.W., and Klumperman, J. (1999). Vesicular tubular clusters between the ER and Golgi mediate concentration of soluble secretory proteins by exclusion from COPI-coated vesicles. Cell 98, 81-90.
28. Martire, G., Mottola, G., Pascale, M.C., Malagolini, N., Turrini, I., Serafini-Cessi, F., Jackson, M.R., and Bonatti, S. (1996). Different fate of a single reporter protein containing KDEL or KKXX targeting signals stably expressed in mammalian cells. J. Biol. Chem. 271, 3541-3547.
29. Martire, G., Viola, A., Iodice, L., Lotti, L.V., Gradini, R., and Bonatti, S. (2001). Hepatitis C virus structural proteins reside in the endoplasmic reticulum as well as in the intermediate compartment/cisGolgi complex region of stably transfected cells. Virology 280, 176-182.
30. Miesenböck, G., and Rothman, J.E. (1995). The capacity to retrieve escaped ER proteins extends to the trans-most cisterna of the Golgi stack. J. Cell Biol. 129, 309-319.
31. Mottola, G., Cardinali, G., Ceccacci, A., Trozzi, C., Bartholomew, L., Torrisi, M.R., Pedrazzini, E., Bonatti, S., and Migliaccio, G. (2002). Hepatitis C virus nonstructural proteins are localized in a modified endoplasmic reticulum of cells expressing viral subgenomic replicons. Virology 293, 31-43.
32. Mottola, G., Jourdan, N., Castaldo, G., Malagolini, N., Lahm, A., Serafini-Cessi, F., Migliaccio, G., and Bonatti, S. (2000). A new determinant of endoplasmic reticulum localization is contained in the juxtamembrane region of the ectodomain of hepatitis C virus glycoprotein E1. J. Biol. Chem. 275, 24070-24079.
33. Muniz, M., Morsomme, P., and Riezman, H. (2001). Protein sorting upon exit from the endoplasmic reticulum. Cell 104, 313-320.
34. Munro, S., and Pelham, H.R.B. (1987). A C-terminal signal prevents secretion of luminal ER proteins. Cell 48, 899-907.
35. Nilsson, T., Jackson, M.R., and Peterson, P.A. (1989). Short cytoplasmic sequences serve as retention signals for transmembrane proteins in the endoplasmic reticulum. Cell 58, 707-718.
36. Nohturfft, A., Yabe, D., Goldstein, J.L., Brown, M.S., and Espenshade, P.J. (2000). Regulated step in cholesterol feedback localized to budding of SCAP from ER membranes. Cell 102, 315-323.
37. Oprins, A., Duden, R., Kreis, T.E., Geuze, H.J., and Slot, J.W. (1993). Beta-COP localizes mainly to the cis-Golgi side in exocrine pancreas. J. Cell Biol. 121, 49-59.
38. Oprins, A., Rabouille, C., Posthuma, G., Klumperman, J., Geuze, H.J., and Slot, J.W. (2001). The ER to Golgi interface is the major concentration site of secretory proteins in the exocrine pancreatic cell. Traffic 2, 831-838.
39. Pascale, M.C., Malagolini, N., Serafini-Cessi, F., Leone, A., and Bonatti, S. (1992). Biosynthesis and oligosaccharide structure of human CD8 glycoprotein expressed in a rat epithelial cell line. J. Biol. Chem. 267, 9940-9947.
40. Pelham, H.R.B. (1988). Evidence that luminal ER proteins are sorted from secreted proteins in a post-ER compartment. EMBO J. 7, 913-918.
41. Pelham, H.R.B. (1991). Recycling of proteins between the endoplasmic reticulum and Golgi complex (review). Curr. Opin. Cell Biol. 3, 585-591.
42. Pelham, H.R., Hardwick, K.G., and Lewis, M.J. (1988). Sorting of soluble ER proteins in yeast. EMBO J. 7, 1757-1762.
43. Peter, F., Nguyen, V.P., and Soling, H.D. (1992). Different sorting of Lys-Asp-Glu-Leu proteins in rat liver. J. Biol. Chem. 267, 10631-10637.
44. Rexach, M.F., and Schekman, R.W. (1991). Distinct biochemical requirements for the budding, targeting, and fusion of ER-derived transport vesicles. J. Cell Biol. 114, 219-229.
45. Rowe, T., Aridor, M., McCaffery, J.M., Plutner, H., Nuoffer, C., and Balch, W.E. (1996). COPII vesicles derived from mammalian endoplasmic reticulum microsomes recruit COPI. J. Cell Biol. 135, 895-911.
46. Saraste, J., and Kuismanen, E. (1984). Pre- and post-Golgi vacuoles operate in the transport of Semliki Forest virus membrane glycoproteins to the cell surface. Cell. 38, 535-549.
47. Saraste, J., and Svensson, K. (1991). Distribution of the intermediate elements operating in ER to Golgi transport. J. Cell Sci. 100, 415-430.
48. Semenza, J.C., Hardwick, K.G., Dean, N., and Pelham, H.R. (1990). ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell. 61, 1349-1357.
49. Shima, D.T., Scales, S.J., Kreis, T.E., and Pepperkok, R. (1999). Segregation of COPI-rich and anterograde-cargo-rich domains in endoplasmic reticulum-to-Golgi transport complexes. Curr. Biol. 9, 821-824.
50. Stephens, D.J., Lin-Marq, N., Pagano, A., Pepperkok, R., and Paccaud, J.P. (2000). COPI-coated ER-to-Golgi transport complexes segregate from the COPII in close proximity to ER exit sites. J. Cell Sci. 113, 2177-2185.
51. Spiro, R.G. (2002). Protein glycosylation, nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12, 43R-56R.
52. Tang, B.L., Wong, S.H., Qi, X.L., Low, S.H., and Hong, W. (1993). Molecular cloning, characterization, subcellular localization and dynamics of p23, the mammalian KDEL receptor. J. Cell Biol. 120, 325-328.
53. Townsley, F.M., Wilson, D.W., and Pelham, H.R.B. (1993). Mutational analysis of the human KDEL receptor, distinct structural requirements for Golgi retention, ligand binding and retrograde transport. EMBO J. 12, 2821-2829.
54. Yu, Y., Sabatini, D.D., and Kreibich, G. (1990). Antiribophorin antibodies inhibit the targeting to the ER membrane of ribosome containing nascent secretory polypeptides J. Cell Biol. 111, 1335-1342.
55. Zerangue, N., Malan, M.J., Fried, S.R., Dazin, P.F., Jan, Y.N., Jan, L.Y., and Schwappach, B. (2001). Analysis of endoplasmic reticulum trafficking signals by combinatorial screening in mammalian cells. Proc. Natl. Acad. Sci. USA 98, 2431-2436.