Slow translocon gating causes cytosolic exposure of transmembrane and lumenal domains during membrane protein integration (original) (raw)

References

  1. Wilson, C., Connolly, T., Morrison, T. & Gilmore, R. Integration of membrane proteins into the endoplasmic reticulum requires GTP. J. Cell Biol. 107, 69–77 (1988).
    Article CAS Google Scholar
  2. Do, H., Falcone, D., Lin, J., Andrews, D.W. & Johnson, A.E. The cotranslational integration of membrane proteins into the phospholipid bilayer is a multistep process. Cell 85, 369–378 (1996).
    Article CAS Google Scholar
  3. Heinrich, S.U., Mothes, W., Brunner, J. & Rapoport, T.A. The Sec61p complex mediates the integration of a membrane protein by allowing lipid partitioning of the transmembrane domain. Cell 102, 233–244 (2000).
    Article CAS Google Scholar
  4. Beltzer, J.P. et al. Charged residues are major determinants of the transmembrane orientation of a signal-anchor sequence. J. Biol. Chem. 266, 973–978 (1991).
    CAS PubMed Google Scholar
  5. Hartmann, E., Rapoport, T.A. & Lodish, H.F. Predicting the orientation of eukaryotic membrane-spanning proteins. Proc. Natl. Acad. Sci. USA 86, 5786–5790 (1989).
    Article CAS Google Scholar
  6. Wahlberg, J.M. & Spiess, M. Multiple determinants direct the orientation of signal-anchor proteins: the topogenic role of the hydrophobic signal domain. J. Cell Biol. 137, 555–562 (1997).
    Article CAS Google Scholar
  7. Denzer, A.J., Nabholz, C.E. & Spiess, M. Transmembrane orientation of signal anchor proteins is affected by the folding state but not the size of the N-terminal domain. EMBO J. 14, 6311–6317 (1995).
    Article CAS Google Scholar
  8. Mothes, W. et al. Molecular mechanism of membrane protein integration into the endoplasmic reticulum. Cell 89, 523–533 (1997).
    Article CAS Google Scholar
  9. Heinrich, S.U. & Rapoport, T.A. Cooperation of transmembrane segments during the integration of a double-spanning protein into the ER membrane. EMBO J. 22, 3654–3663 (2003).
    Article CAS Google Scholar
  10. McCormick, P.J., Miao, Y., Shao, Y., Lin, J. & Johnson, A.E. Cotranslational protein integration into the ER membrane is mediated by the binding of nascent chains to translocon proteins. Mol. Cell 12, 329–341 (2003).
    Article CAS Google Scholar
  11. Sadlish, H., Pitonzo, D., Johnson, A.E. & Skach, W.R. Sequential triage of transmembrane segments by Sec61alpha during biogenesis of a native multispanning membrane protein. Nat. Struct. Mol. Biol. 12, 870–878 (2005).
    Article CAS Google Scholar
  12. Liao, S., Lin, J., Do, H. & Johnson, A.E. 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 (1997).
    Article CAS Google Scholar
  13. Haigh, N.G. & Johnson, A.E. A new role for BiP: closing the aqueous translocon pore during protein integration into the ER membrane. J. Cell Biol. 156, 261–270 (2002).
    Article CAS Google Scholar
  14. Woolhead, C.A., McCormick, P.J. & Johnson, A.E. Nascent membrane and secretory proteins differ in FRET-detected folding far inside the ribosome and in their exposure to ribosomal proteins. Cell 116, 725–736 (2004).
    Article CAS Google Scholar
  15. Plath, K., Mothes, W., Wilkinson, B.M., Stirling, C.J. & Rapoport, T.A. Signal sequence recognition in posttranslational protein transport across the yeast ER membrane. Cell 94, 795–807 (1998).
    Article CAS Google Scholar
  16. Van den Berg, B. et al. X-ray structure of a protein-conducting channel. Nature 427, 36–44 (2004).
    Article CAS Google Scholar
  17. Rapoport, T.A., Goder, V., Heinrich, S.U. & Matlack, K.E. Membrane-protein integration and the role of the translocation channel. Trends Cell Biol. 14, 568–575 (2004).
    Article CAS Google Scholar
  18. Morgan, D.G., Menetret, J.F., Neuhof, A., Rapoport, T.A. & Akey, C.W. Structure of the mammalian ribosome-channel complex at 17 Å resolution. J. Mol. Biol. 324, 871–886 (2002).
    Article CAS Google Scholar
  19. Beckmann, R. et al. Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 107, 361–372 (2001).
    Article CAS Google Scholar
  20. Johnsson, N. & Varshavsky, A. Ubiquitin-assisted dissection of protein transport across membranes. EMBO J. 13, 2686–2698 (1994).
    Article CAS Google Scholar
  21. Ng, D.T., Brown, J.D. & Walter, P. Signal sequences specify the targeting route to the endoplasmic reticulum. J. Cell Biol. 134, 269–278 (1996).
    Article CAS Google Scholar
  22. Mason, N., Ciufo, L.F. & Brown, J.D. Elongation arrest is a physiologically important function of signal recognition particle. EMBO J. 19, 4164–4174 (2000).
    Article CAS Google Scholar
  23. Jungnickel, B. & Rapoport, T.A. A posttranslational signal sequence recognition event in the endoplasmic reticulum membrane. Cell 82, 261–270 (1995).
    Article CAS Google Scholar
  24. Belin, D., Bost, S., Vassalli, J.D. & Strub, K. A two-step recognition of signal sequences determines the translocation efficiency of proteins. EMBO J. 15, 468–478 (1996).
    Article CAS Google Scholar
  25. Goder, V. & Spiess, M. Molecular mechanism of signal sequence orientation in the endoplasmic reticulum. EMBO J. 22, 3645–3653 (2003).
    Article CAS Google Scholar
  26. Ogg, S.C., Barz, W.P. & Walter, P. A functional GTPase domain, but not its transmembrane domain, is required for function of the SRP receptor β-subunit. J. Cell Biol. 142, 341–354 (1998).
    Article CAS Google Scholar
  27. Cheng, Z., Jiang, Y., Mandon, E.C. & Gilmore, R. Identification of cytoplasmic residues of Sec61p involved in ribosome binding and cotranslational translocation. J. Cell Biol. 168, 67–77 (2005).
    Article CAS Google Scholar
  28. Johnsson, N. & Varshavsky, A. Split ubiquitin as a sensor of protein interactions in vivo. Proc. Natl. Acad. Sci. USA 91, 10340–10344 (1994).
    Article CAS Google Scholar
  29. Goder, V., Crottet, P. & Spiess, M. In vivo kinetics of protein targeting to the endoplasmic reticulum determined by site-specific phosphorylation. EMBO J. 19, 6704–6712 (2000).
    Article CAS Google Scholar
  30. Connolly, T., Collins, P. & Gilmore, R. Access of proteinase K to partially translocated nascent polypeptides in intact and detergent-solubilized membranes. J. Cell Biol. 108, 299–307 (1989).
    Article CAS Google Scholar
  31. Crowley, K.S., Reinhart, G.D. & Johnson, A.E. The signal sequence moves through a ribosomal tunnel into a noncytoplasmic aqueous environment at the ER membrane early in translocation. Cell 73, 1101–1115 (1993).
    Article CAS Google Scholar
  32. Braakman, I., Hoover-Litty, H., Wagner, K.R. & Helenius, A. Folding of influenza hemagglutinin in the endoplasmic reticulum. J. Cell Biol. 114, 401–411 (1991).
    Article CAS Google Scholar
  33. Hershey, J.W. Translational control in mammalian cells. Annu. Rev. Biochem. 60, 717–755 (1991).
    Article CAS Google Scholar
  34. Crowley, K.S., Liao, S., Worrell, V.E., Reinhart, G.D. & Johnson, A.E. Secretory proteins move through the endoplasmic reticulum via an aqueous, gated pore. Cell 78, 461–471 (1994).
    Article CAS Google Scholar
  35. Buck, T.M. & Skach, W.R. Differential stability of biogenesis intermediates reveals a common pathway for aquaporin-1 topological maturation. J. Biol. Chem. 280, 261–269 (2005).
    Article CAS Google Scholar
  36. Hessa, T. et al. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433, 377–381 (2005).
    Article CAS Google Scholar
  37. Green, N. & Walter, P. C-terminal sequences can inhibit the insertion of membrane proteins into the endoplasmic reticulum of Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 276–282 (1992).
    Article CAS Google Scholar
  38. Kim, H., Melen, K. & von Heijne, G. Topology models for 37 Saccharomyces cerevisiae membrane proteins based on C-terminal reporter fusions and predictions. J. Biol. Chem. 278, 10208–10213 (2003).
    Article CAS Google Scholar
  39. Rothblatt, J. & Schekman, R. A hitchhiker's guide to the analysis of the secretory pathway in yeast. Methods Cell Biol. 32, 3–36 (1989).
    Article CAS Google Scholar

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