The role of molecular chaperones in protein transport into the mammalian endoplasmic reticulum

Biological Chemistry

Volumn 379, Issue 3, 1998, Pages 275-282

  Zimmermann, Richard ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

BiP; Grp170; Hsc70; Mtj1p; Sec63p

Indexed keywords

CARRIER PROTEIN; CHAPERONE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; MEMBRANE PROTEIN; PROTEIN; PROTEIN PRECURSOR;

ARTICLE; ENDOPLASMIC RETICULUM; INTRACELLULAR MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TRANSPORT; YEAST;

ANIMALS; BIOLOGICAL TRANSPORT; CYTOSOL; ENDOPLASMIC RETICULUM; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES;

MAMMALIA;

EID: 0031923127     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (100)

1. Adelman, M.R., Sabatini, D.D., and Blobel, G. (1973). Ribosome-membrane interaction. Nondestructive disassembly of rat liver rough microsomes into ribosomes and membranous components. J. Cell Biol. 56, 206-229.
2. Amaya, Y., Nakano, A., Ito, K., and Mori, M. (1990). Isolation of a yeat gene, SRH1, that encodes a homologue of the 54k subunit of mammalian signal recognition particle. J. Biochem. 107, 457-463.
3. Bacher, G., Lütcke, H., Jungnickel, B., Rapoport, T.A., and Dobberstein, B. (1996). Regulation by the ribosome of the GTPase of the signal-recognition particle during protein targeting. Nature 381, 248-251.
4. Borgese, N., Mok, W., Kreibich, G., and Sabatini, D.D. (1974). Ribosome-membrane interaction: In vitro binding of ribosomes to microsomal membranes. J. Mol. Biol. 88, 559-580.
5. Brightman, S.E., Blatch, G.L., and Zetter, B.R. (1995). Isolation of a mouse cDNA encoding MTJ1, a new murine member of the DnaJ family of proteins. Gene 153, 249-254.
6. Brodsky, J.L., Hamamoto, S., Feldheim, D., and Schekman, R. (1993). Reconstitution of protein translocation from solubilized membranes reveals topologically distinct roles for BiP and cytosolic Hsc70. J. Cell Biol. 120, 95-102.
7. Brodsky, J.L., Goeckeler, J., and Schekman, R. (1995). BiP and Sec63p are required for both co- and posttranslational protein translocation into the yeast endoplasmic reticulum. Proc. Natl. Acad.Sci. USA 92, 9643-9646.
8. Caplan, A.J., Cyr, D.M., and Douglas, M.G. (1992). YDJ1p facilitates polypeptide translocation across different intracellular membranes by a conserved mechanism. Cell 71, 1143-1155.
9. Chirico, W.J., Waters, G.M., and Blobel, G. (1988). 70K heat shock related proteins stimulate protein translocation into microsomes. Nature 332, 805-810.
10. Chuck, S.L., and Lingappa, V.R. (1992). Pause transfer: a topogenic sequence in apolipoprotein B mediates stopping and restarting of Translocation. Cell 68, 9-21.
11. Connolly, T., and Gilmore, R. (1986). Formation of a functional ribosome-membrane junction during translocation requires the participation of a GTP-binding protein. J. Cell Biol. 103, 2253-2261.
12. Connolly, T., and Gilmore, R. (1989). The signal recognition particle receptor mediates the GTP-dependent displacement of SRP from the signal sequence of the nascent polypeptide. Cell 57, 599-610.
13. Connolly, T., Rapiejko, P.J., and Gilmore, R. (1991). Requirement of GTP hydrolysis for dissociation of the signal recognition particle from its receptor. Science 252, 1171-1173.
14. Craven, R.A., Egerton, M., and Stirling, C.J. (1996). A novel Hsp70 of the yeast ER lumen is required for the efficient translocation of a number of protein precursors. EMBO J. 15, 2640-2650.
15. Crowley, K.S., Reinhart, G.D., and Johnson, A.E. (1993). The signal sequence moves through a ribosomal tunnel into a non-cytoplasmic aqueous environment at the ER membrane early in translocation. Cell 73, 1101-1115.
16. Crowley, K.S., Lia, S., Worrell, V.E., Reinhart, G.D., and Johnson, A.E. (1994). Secretory proteins move through the endoplasmic reticulum membrane via an aqueous, gated pore. Cell 78, 461-471.
17. Daimon, M., Susa, S., Suzuki, K., Kato, T., Yamatani, K., and Sasaki, H. (1997). Identification of a human cDNA homologue to the Drosophila translocation protein 1 (Dtrp1). Biochem. Biophys. Res. Comm. 230, 100-104.
18. Deshaies, R.J., and Schekman, R. (1987). A yeast mutant defective at an early stage in import of secretory protein precursors into the endoplasmic reticulum. J. Cell Biol. 105, 633-645.
19. Deshaies, R.J., and Schekman, R. (1989). Sec62 encodes a putative membrane protein required for protein translocation into theyeast endoplasmic reticulum. J. Cell Biol. 109, 2653-2664.
20. Deshaies, R.J., Koch, B.D., Werner-Washburne, M., Craig, E.A., and Schekman, R. (1988). A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature 332, 800-805.
21. Deshaies, R.J., Sanders, S. L., Feldheim, D.A., and Schekman, R. (1991). Assembly of yeast Sec proteins involved in translocation into the endoplasmic reticulum into a membrane-bound multisubunit complex. Nature 349, 806-808.
22. Dierks, T., Volkmer, J., Schlenstedt, G., Jung, C., Sandholzer, U., Zachmann, K., Schlotterhose, P., Neifer, K., Schmidt, B., and Zimmermann, R. (1996). A microsomal ATP-binding protein involved in efficient protein transport into the mammalian endoplasmic reticulum. EMBO J. 15, 6931-6942.
23. Feldheim, D., and Schekman, R. (1994). Sec72p contributes to the selective recognition of signal peptides by the secretory polypeptide translocation complex. J. Cell Biol. 126, 935-943.
24. Feldheim, D., Rothblatt, J., and Schekman, R. (1992). Topology and functional domains of Sec63p, an endoplasmic reticulum membrane protein required for secretory protein translocation. Mol. Cell. Biol. 12, 3288-3296.
25. Finke, K., Plath, K., Panzner, S., Prehn, S., Rapoport, T.A., Hartmann, E., and Sommer, T. (1996). A second trimeric complex containing homologs of the Sec61p complex functions in protein transport across the ER membrane of S. cerevisiae. EMBO J. 15, 1482-1494.
26. Freymann, D.M., Keenan, R.J., Stroud, R.M., and Walter, P. (1997). Structure of the conserved GTPase domain of the signal recognition particle. Nature 385, 361-364.
27. Frydman, J., and Höhfeld, J. (1997). Chaperones get in touch: the Hip-Hop connection. Trends Biochem. Sci. 22, 87-92.
28. Gilmore, R., and Blobel, G. (1985). Translocation of secretory proteins across the microsomal membrane occurs through an environment accessible to aqueous perturbants. Cell 42, 497-505.
29. Gilmore, R., Blobel, G., and Walter, P. (1982a). Protein translocation across the endoplasmic reticulum. I. Detection in the microsomal membrane of a receptor for the signal recognition particle. J. Cell Biol. 95, 463-469.
30. Gilmore, R., Walter, P., and Blobel, G. (1982b). Protein translocation across the endoplasmic reticulum. II. Isolation and characterization of the signal recognition particle receptor. J. Cell Biol. 95, 470-477.
31. Görlich, D., and Rapoport, T.A. (1993). Protein translocation into protoliposomes reconstituted from purified components of the endoplasmic reticulum membrane. Cell 75, 615-630.
32. Görlich, D., Hartmann, E., Prehn, S., and Rapoport, T.A. (1992a). A protein of the endoplasmic reticulum involved early in polypeptide translocation, Nature 357, 47-52.
33. Görlich, D., Prehn, S., Hartmann, E., Kalies, K.-U., and Rapoport T.A. (1992b). A mammalian homolog of Sec61p and SecYp is associated with ribosomes and nascent polypeotides during translocation. Cell 71, 489-503.
34. Green, N., Fang, H., and Walter, P. (1992). Mutants in three novel complementation groups inhibit membrane protein insertion into and soluble protein translocation across the endoplasmic reticulum membrane of Saccharomyces cerevisiae. J. Cell Biol. 116, 597-604.
35. Hamman, B.D., Chen, J.-C., Johnson, E.E., and Johnson, A.E. (1997). The aqueous pore through the translocon has a diameter of 40-60 Å during contranslational protein translocation at the ER membrane. Cell 89, 535-544.
36. Hanein, D., Matlack, K.E.S., Jungnickel, B., Plath, K., Kalies, K.-U., Miller, K.R., Rapoport, T.A., and Akey, C.W. (1996). Oligomeric rings of the Sec61p complex induced by ligands required for protein translocation. Cell 87, 721-732.
37. Hann, B.C., Stirling, C.J., and Walter, P. (1992). Sec65 gene product is a subunit of the yeast signal recognition particle required for its integrity. Nature 356, 532-533.
38. Hardy, S.J.S., and Randall, L.L. (1991). A kinetic partitioning model of selective binding of nonnative proteins by the bacterial chaperone SecB. Science 251, 439-443.
39. Hartmann, E., Sommer, T., Prehn, S., Görlich, D., Jentsch, S., and Rapoport, T.A. (1994). Evolutionary conservation of components of the protein translocation complex. Nature 367, 654-657.
40. Hedge, R.S., and Lingappa, V.R. (1996). Sequence-specific alteration of the ribosome-membrane junction exposes nascent secretory proteins to the cytosol. Cell 85, 217-228.
41. Höhfeld, J., and Jentsch, S. (1997). GrpE-like regulation of the Hsc70 chaperone by the anti-apoptotic protein BAG-1. EMBO J. 16, 101-108.
42. Jungnickel, B., and Rapoport, T.A. (1995). A posttargeting signal sequence recognition event in the endoplasmic reticulum membrane. Cell 82, 261-270.
43. Klappa, P., Mayinger, P., Pipkorn, R., Zimmermann, M., and Zimmermann, R. (1991). A microsomal protein is involved in ATP-dependent transport of presecretory proteins into mammalian microsomes. EMBO J. 10, 2795-2803.
44. Klappa, P., Freedman, R., and Zimmermann, R. (1995). Protein disulfide isomerase and a lumenal cyclophilin-type peptidyl prolyl cis-trans isomerase are in transient contact with secretory proteins during late stages of translocation. Eur. J. Biochem. 232, 755-764.
45. Krieg, U.C., Walter, P., and Johnson, A.E. (1986). Photocrosslinking of the signal sequence of nascent preprolactin to the 54-kilodalton polypeptide of the signal recognition particle. Proc Natl. Acad. Sci. USA 83, 8604-8608.
46. Kurzchalia, T.V., Wiedman, M., Girshovich, A.S., Bochkareva, E.S., Bielka, H., and Rapoport, T.A. (1986). The signal sequence of nascent preprolactin interacts with the 54K polypeptide of the signal recognition particle. Nature 320, 634-636.
47. Lauffer, L., Garcia, P.D., Harkins, R.N., Coussens, L., Ullrich, A., and Walter, P. (1985). Topology of signal recognition particle receptor in endoplasmic reticulum membrane. Nature 318, 334-338.
48. Lia, S., Lin, J., Do, H., and Johnson, A.E. (1997). Both lumenal and cytosolic gating of the aqueous ER translocon pore are regulated from inside the ribosome during membrane protein integration. Cell 90, 31-41.
49. Lütcke, H., High, S., Römisch, K., Ashford, A.J., and Dobbertein, B. (1992). The methionine-rich domain of the 54 kDa subunit of signal recognition particle is sufficient for the interacts with signal sequences. EMBO J. 11, 1543-1551
50. Lyman, S.K., and Schekman, R. (1995). Interaction between BiP and Sec63p is required for the completion of protein translocation into the ER of Saccharomyces cerevisiae. J. Cell Biol. 131, 1163-1171.
51. Lyman, S.K., and Schekman, R. (1997). Binding of secretory precursor polypeptides to a translocon subcomplex is regulated by BiP. Cell 88, 85-96.
52. Martoglio, B., Hofmann, M.W., Brunner, J., and Dobberstein, B. (1995) The protein-conducting channel in the membrane of the endoplasmic reticulum is open laterally toward the lipid bilayer. Cell 81, 207-214.
53. Matlack, K.E.S., Plath, K., Misselwitz, B., and Rapoport, T.A. (1997). Protein transport by purified yeast Sec complex and Kar2p without membranes. Science 277, 938-941.
54. Meyer, D.I., and Dobberstein, B. (1980a). A membrane component essential for vectorial translocation of nascent proteins across the endoplasmic reticulum: Requirements for its extraction and reassociation with the membrane. J. Cell Biol. 87, 498-502.
55. Meyer, D.I., and Dobberstein, B. (1980b). Identification and characterization of a membrane component essential for the translocation of nascent proteins across the membrane of the endoplasmic reticulum. J. Cell Biol. 87, 503-508.
56. Meyer, D.I., Krause, E., and Dobberstein, B. (1982). Secretory protein translocation across membranes - the role of the 'docking protein'. Nature 297, 647-650.
57. Montoya, G., Svensson, C., Luirink, J., and Sinning, I. (1997). Crystal structure of the NG domain from the signal-recognition particle receptor FtsY. Nature 385, 365-368.
58. Müller, G., and Zimmermann, R. (1987). Import of honeybee prepromelittin into the endoplasmic reticulum: Structural basis for independence of SRP and docking protein. EMBO J. 6, 2099-2107.
59. Ng, D.T.W., Brown, J.D., and Walter, P. (1996). Signal sequences specify the targeting route to the endoplasmic reticulum membrane. J. Cell Biol. 134, 269-278.
60. Nguyen, T.H., Law, D.T.S., and Williams, D.B. (1991). Binding protein BiP is required for translocation of secretory proteins into the endoplasmic reticulum in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 88, 1565-1569.
61. Nicchitta, C.V., and Blodel, G. (1990). Assembly of translocation-competent proteoliposomes from detergent-solubilized rough microsomes. Cell 60, 259-266.
62. Nicchitta, C.V., and Blodel, G. (1993). Lumenal proteins of the mammalian endoplasmic reticulum are required to complete protein translocation. Cell 73, 989-998.
63. Panzner, S., Dreier, L., Hartmann, E., Kostka, S., and Rapoport, T.A. (1995). Posttranslational protein transport in yeast reconstituted with a purified complex of Sec proteins and Kar2p. Cell 81, 561-570.
64. Perara, E., Rothman, R.E., and Lingappa, V.R. (1986). Uncoupling translocation from translation: Implications for transport of proteins across membranes. Science 232, 348-352.
65. Poritz, M.A., Siegel, V., Hansen, W., and Walter, P. (1988). Small ribonucleoproteins in Schizosaccharomyces pombe and Yarrowia lipolytica homologous to signal recognition particle. Proc. Natl. Acad. Sci. USA 85, 4315-4319.
66. Rapiejko, P.J., and Gilmore, R. (1992). Protein translocation across the ER requires a functional GTP binding site in the α subunit of the signal recognition particle receptor. J. Cell Biol. 117, 493-503.
67. Rapiejko, P.J., and Gilmore, R. (1997). Empty site forms of the SRP54 and SRα GTPases mediate targeting of ribosome-nascent chain complexes to the endoplasmic reticulum. Cell 89, 703-713.
68. Ribes, V., Dehaux, P., and Tollervey, D. (1988). 7SL RNA from Schizosaccharomyces pombe is encoded by a single copy essential gene. EMBO J. 7, 231-237.
69. Römisch, K., Webb, J., Lingelbach, K., Gausepohl, H., and Dobberstein, B. (1990). The 54-kD protein of signal recognition particle contains a methionine-rich RNA binding domain. J. Cell Biol. 111, 1793-1802.
70. Rothblatt, J.A., Deshaies, R.J., Sanders, S.L., Daum, G., and Schekman, R. (1989). Multiple genes are required for proper insertion of secretory proteins into the endoplasmic reticulum. J. Cell Biol. 109, 2641-2652.
71. Sadler, I., Chiang, A., Kurihara, T., Rothblatt, J.A., Way, J., and Silver, P. (1989). A yeast gene important for protein assembly into the endoplasmic reticulum and the nucleus has homology to DnaJ, an Escherichia coli heat shock protein. J. Cell Biol. 109, 2665-2675.
72. Sanders, S.L., Whitfield, K.M., Vogel, J. P., Rose, M.D., and Schekman, R. (1992). Sec61p and BiP directly facilitate polypeptide translocation into the ER. Cell 69, 353-365.
73. Savitz, A. J., and Meyer, D.I. (1990). Identification of a ribosome receptor in the rough endoplasmic reticulum. Nature 346, 540-544.
74. Savitz, A. J., and Meyer, D.I. (1993). 180-kDa ribosome receptor is essential for both ribosome binding and protein translocation. J. Cell Biol. 120, 853-863.
75. Schlenstedt, G., and Zimmermann, R. (1987). Import of frog prepropeptide GLa into microsomes requires ATP but does not involve docking protein or ribosomes. EMBO J. 6, 699-703.
76. Schlenstedt, G., Gudmundsson, G.H., Boman, H.G., and Zimmermann, R. (1990). A large presecretory protein translocates both cotranslationally, using signal recognition particle and ribosome, and posttranslationally, without these ribonucleoprotein particles, when synthesized in the presence of mammalian microsomes. J. Biol. Chem. 265, 13960-13968.
77. Simon, S.M., and Blobel, G. (1991). A protein-conducting channel in the endoplasmic reticulum. Cell 65, 371-380.
78. Stirling, C.J., and Hewitt, E.W. (1992). The S. cerevisiae Sec65 gene encodes a component of yeast signal recognition particle with homology to human SRP19. Nature 356, 534-537.
79. Stirling, C.J., Rothblatt, J., Hosobuchi, M., Deshaies, R., and Schekman, R. (1992). Protein translocation mutants defective in the insertion of integral membrane proteins into the endoplasmic reticulum. Mol. Biol. Cell 3, 129-142.
80. Tajima, S., Lauffer, L., Rath, V.L., and Walter, P. (1986). The signal recognition particle receptor is a complex that contains two distinct polypeptide chains. J. Cell Biol. 103, 1167-1178.
81. Takayama, S., Bimston, D.N., Matsuzawa, S.-i., Freeman, B.C., Aime-Sempe, C., Xie, Z., Morimoto, R.I., and Reed, J.C. (1997). BAG-1 modulates the chaperone activity of Hsp70/Hsc70. EMBO J. 16, 4887-4896.
82. Toyn, J., Hibbs, A.R., Sanz, P., Crowe, J., and Meyer, D.I. (1988). In vivo and in vitro analysis of ptl1, a yeast ts mutant with a membrane-associated defect in protein translocation. EMBO J. 7, 4347-4353.
83. Vogel, J.P., Misra, L.M., and Rose, M.D. (1990). Loss of BiP/GRP78 function blocks translocation of secretory proteins in yeast. J. Cell Biol. 110, 1885-1895.
84. Volkmer, J., Guth, S., Nastainczyk, W., Knippel, P., Klappa, P., Gnau, V., and Zimmermann, R. (1997). Pancreas specific protein disulfide isomerase, PDlp, is in transient contact with secretory proteins during late stages of translocation. FEBS Letters 406, 291-295.
85. von Heijne, G. (1981). On the hydrophobic nature of signal sequences. Eur. J. Biochem. 116, 419-422.
86. von Heijne, G. (1984). Analysis of the distribution of charged residues in the N-terminal region of signal sequences: implications for protein export in prokaryotic and eukaryotic cells. EMBO J. 3, 2315-2318.
87. von Heijne, G. (1985). Signal sequences. The limits of variation. J. Mol. Biol. 184, 99-105.
88. Walter, P., and Blobel, G. (1981a). Translocation of proteins across the endoplasmic reticulum. II. Signal recognition protein, SRP, mediates the selective binding to microsomal membranes of in-vitro-assembled polysomes synthesizing secretory protein. J. Cell Biol. 91, 551-556.
89. Walter, P., and Blobel, G. (1981b). Translocation of proteins across the endoplasmic reticulum. III. Signal recognition protein, SRP, causes signal sequence-dependent and site-specific arrest of chain elongation that is released by microsomal membranes. J. Cell Biol. 91, 557-561.
90. Walter, P., and Blobel, G. (1982). Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum. Nature 299, 691-698.
91. Walter, P., Ibrahimi, I., and Blobel, G. (1981). Translocation of proteins across the endoplasmic reticulum. I. Signal recognition protein, SRP, binds to in-vitro-assembled polysomes synthesizing secretory protein. J. Cell Biol. 91, 545-550.
92. Wanker, E.E., Sun, Y., Savitz, A.J., and Meyer, D.I. (1995). Functional characterization of the 180 kDa ribosome receptor in vivo. J. Cell Biol. 130, 29-39.
93. Wiech, H., Sagstetter, M., Müller, G., and Zimmermann, R. (1987). The ATP requiring step in assembly of M13 procoat protein into microsomes is related to preservation of transport competence of the precursor protein. EMBO J. 6, 1011-1016.
94. Wiech, H., Buchner, J., Zimmermann, M., Zimmermann, R., and Jakob, U. (1993). Hsc70, Immunoglobulin heavy chain binding protein, and Hsp90 differ in their ability to stimulate transport of precursor proteins into mammalian microsomes. J. Biol. Chem. 268, 7414-7421.
95. Zeiner, M., Gebauer, M., and Gehring, U. (1997). Mammalian protein RAP46: an interaction partner and modulator of 70 kDa heat shock proteins. EMBO J. 16, 5483-5490.
96. Zimmerman, D.L., and Walter, P. (1991). An ATP-binding membrane protein is required for protein translocation across the endoplasmic reticulum membrane. Cell Regulation 2, 851-859.
97. Zimmermann, R., and Meyer, D.I. (1986). 1986: A year of new insights into how proteins cross membranes. Trends Biochem. Sci. 11, 512-515.
98. Zimmermann, R., Sagstetter, M., Lewis, M.J., and Pelham, H.R.B. (1988). Seventy kilodalton heat shock proteins and an additional component from reticulocyte lysate stimulate import of M13 procoat protein into microsomes. EMBO J. 7, 2875-2880.
99. Zimmermann, R., Zimmermann, M., Mayinger, P., and Klappa, P. (1991). Photoaffinity labeling of dog pancreas microsomes with 8-azido-ATP inhibits association of nascent preprolactin with the signal sequence receptor complex. FEBS Lett. 286, 95-99.
100. Zopf, D., Bernstein, H.D., Johnson, A.E., and Walter, P. (1990). The methionine-rich domain of the 54 kd protein subunit of the signal recognition particle contains an RNA binding site and can be crosslinked to a signal sequence. EMBO J. 9, 4511-4517.