The Sec62-Sec63 translocon facilitates translocation of the C-terminus of membrane proteins

Journal of Cell Science

Volumn 127, Issue 19, 2014, Pages 4270-4278

  Jung, Sung jun ^a   Kim, Ji Eun Hani ^a   Reithinger, Johannes H ^b   Kim, Hyun ^a  

^a Seoul National University   (South Korea)

^b STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Co translational translocation; Endoplasmic reticulum; ER; Sec61; Topology; Yeast

Indexed keywords

MEMBRANE PROTEIN; SEC62 PROTEIN; SEC63 PROTEIN; TRANSLOCON; UNCLASSIFIED DRUG; CARRIER PROTEIN; SEC61 PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CYTOSOL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM MEMBRANE; HYDROPHOBICITY; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; STATIC ELECTRICITY; BACTERIAL TRANSLOCATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN TRANSPORT; YEAST;

AMINO ACID SEQUENCE; BACTERIAL TRANSLOCATION; ENDOPLASMIC RETICULUM; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; YEASTS;

EID: 84913608530     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.153650     Document Type: Article

References (39)

1. 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.
2. Chirico, W. J., Waters, M. G. and Blobel, G. (1988). 70K heat shock related proteins stimulate protein translocation into microsomes. Nature 332, 805-810.
3. Deshaies, R. J. and Schekman, R. (1989). SEC62 encodes a putative membrane protein required for protein translocation into the yeast endoplasmic reticulum. J. Cell Biol. 109, 2653-2664.
4. Deshaies, R. J. and Schekman, R. (1990). Structural and functional dissection of Sec62p, a membrane-bound component of the yeast endoplasmic reticulum protein import machinery. Mol. Cell. Biol. 10, 6024-6035.
5. 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.
6. Do, H., Falcone, D., Lin, J., Andrews, D. W. and Johnson, A. E. (1996). The cotranslational integration of membrane proteins into the phospholipid bilayer is a multistep process. Cell 85, 369-378.
7. Görlich, D. and Rapoport, T. A. (1993). Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane. Cell 75, 615-630.
8. Görlich, D., Prehn, S., Hartmann, E., Kalies, K. U. and Rapoport, T. A. (1992). A mammalian homolog of SEC61p and SECYp is associated with ribosomes and nascent polypeptides during translocation. Cell 71, 489-503.
9. 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.
10. Harada, Y., Li, H., Wall, J. S., Li, H. and Lennarz, W. J. (2011). Structural studies and the assembly of the heptameric post-translational translocon complex. J. Biol. Chem. 286, 2956-2965.
11. Heinrich, S. U., Mothes, W., Brunner, J. and Rapoport, T. A. (2000). The Sec61p complex mediates the integration of a membrane protein by allowing lipid partitioning of the transmembrane domain. Cell 102, 233-244.
12. High, S., Martoglio, B., Görlich, D., Andersen, S. S., Ashford, A. J., Giner, A., Hartmann, E., Prehn, S., Rapoport, T. A., Dobberstein, B. et al. (1993). Sitespecific photocross-linking reveals that Sec61p and TRAM contact different regions of a membrane-inserted signal sequence. J. Biol. Chem. 268, 26745-26751.
13. Kitada, K., Yamaguchi, E. and Arisawa, M. (1995). Cloning of the Candida glabrata TRP1 and HIS3 genes, and construction of their disruptant strains by sequential integrative transformation. Gene 165, 203-206.
14. Lang, S., Benedix, J., Fedeles, S. V., Schorr, S., Schirra, C., Schäuble, N., Jalal, C., Greiner, M., Hassdenteufel, S., Tatzelt, J. et al. (2012). Different effects of Sec61a, Sec62 and Sec63 depletion on transport of polypeptides into the endoplasmic reticulum of mammalian cells. J. Cell Sci. 125, 1958-1969.
15. Longtine, M. S., McKenzie, A., 3rd, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P. and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
16. Lundin, C., Kim, H., Nilsson, I., White, S. H. and von Heijne, G. (2008). Molecular code for protein insertion in the endoplasmic reticulum membrane is similar for N(in)-C(out) and N(out)-C(in) transmembrane helices. Proc. Natl. Acad. Sci. USA 105, 15702-15707.
17. Lyman, S. K. and Schekman, R. (1997). Binding of secretory precursor polypeptides to a translocon subcomplex is regulated by BiP. Cell 88, 85-96.
18. McCormick, P. J., Miao, Y., Shao, Y., Lin, J. and Johnson, A. E. (2003). Cotranslational protein integration into the ER membrane is mediated by the binding of nascent chains to translocon proteins. Mol. Cell 12, 329-341.
19. Meyer, H. A., Grau, H., Kraft, R., Kostka, S., Prehn, S., Kalies, K. U. and Hartmann, E. (2000). Mammalian Sec61 is associated with Sec62 and Sec63. J. Biol. Chem. 275, 14550-14557.
20. Mothes, W., Prehn, S. and Rapoport, T. A. (1994). Systematic probing of the environment of a translocating secretory protein during translocation through the ER membrane. EMBO J. 13, 3973-3982.
21. Müller, L., de Escauriaza, M. D., Lajoie, P., Theis, M., Jung, M., Müller, A., Burgard, C., Greiner, M., Snapp, E. L., Dudek, J. et al. (2010). Evolutionary gain of function for the ER membrane protein Sec62 from yeast to humans. Mol. Biol. Cell 21, 691-703.
22. Ng, D. T., Brown, J. D. andWalter, P. (1996). Signal sequences specify the targeting route to the endoplasmic reticulum membrane. J. Cell Biol. 134, 269-278.
23. Öjemalm, K., Halling, K. K., Nilsson, I. and von Heijne, G. (2012). Orientational preferences of neighboring helices can drive ER insertion of a marginally hydrophobic transmembrane helix. Mol. Cell 45, 529-540.
24. 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.
25. Plath, K. and Rapoport, T. A. (2000). Spontaneous release of cytosolic proteins from posttranslational substrates before their transport into the endoplasmic reticulum. J. Cell Biol. 151, 167-178.
26. Plath, K., Mothes, W., Wilkinson, B. M., Stirling, C. J. and Rapoport, T. A. (1998). Signal sequence recognition in posttranslational protein transport across the yeast ER membrane. Cell 94, 795-807.
27. Plath, K., Wilkinson, B. M., Stirling, C. J. and Rapoport, T. A. (2004). Interactions between Sec complex and prepro-alpha-factor during posttranslational protein transport into the endoplasmic reticulum. Mol. Biol. Cell 15, 1-10.
28. Rapoport, T. A. (2007). Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450, 663-669.
29. Reithinger, J. H., Kim, J. E. and Kim, H. (2013). Sec62 protein mediates membrane insertion and orientation of moderately hydrophobic signal anchor proteins in the endoplasmic reticulum (ER). J. Biol. Chem. 288, 18058-18067.
30. 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 in yeast. J. Cell Biol. 109, 2641-2652.
31. Saurí, A., McCormick, P. J., Johnson, A. E. and Mingarro, I. (2007). Sec61alpha and TRAM are sequentially adjacent to a nascent viral membrane protein during its ER integration. J. Mol. Biol. 366, 366-374.
32. Sommer, N., Junne, T., Kalies, K. U., Spiess, M. and Hartmann, E. (2013). TRAP assists membrane protein topogenesis at the mammalian ER membrane. Biochim. Biophys. Acta 1833, 3104-3111.
33. Tyedmers, J., Lerner, M., Bies, C., Dudek, J., Skowronek, M. H., Haas, I. G., Heim, N., Nastainczyk,W., Volkmer, J. and Zimmermann, R. (2000). Homologs of the yeast Sec complex subunits Sec62p and Sec63p are abundant proteins in dog pancreas microsomes. Proc. Natl. Acad. Sci. USA 97, 7214-7219.
34. van den Berg, B., Clemons, W. M., Jr, Collinson, I., Modis, Y., Hartmann, E., Harrison, S. C. and Rapoport, T. A. (2004). X-ray structure of a proteinconducting channel. Nature 427, 36-44.
35. Voigt, S., Jungnickel, B., Hartmann, E. and Rapoport, T. A. (1996). Signal sequence-dependent function of the TRAM protein during early phases of protein transport across the endoplasmic reticulum membrane. J. Cell Biol. 134, 25-35.
36. Willer, M., Jermy, A. J., Young, B. P. and Stirling, C. J. (2003). Identification of novel protein-protein interactions at the cytosolic surface of the Sec63 complex in the yeast ER membrane. Yeast 20, 133-148.
37. Wittke, S., Dünnwald, M. and Johnsson, N. (2000). Sec62p, a component of the endoplasmic reticulum protein translocation machinery, contains multiple binding sites for the Sec-complex. Mol. Biol. Cell 11, 3859-3871.
38. Young, B. P., Craven, R. A., Reid, P. J., Willer, M. and Stirling, C. J. (2001). Sec63p and Kar2p are required for the translocation of SRP-dependent precursors into the yeast endoplasmic reticulum in vivo. EMBO J. 20, 262-271.
39. Zimmermann, R., Sagstetter, M., Lewis, M. J. and Pelham, H. R. (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.