Co- and post-translational translocation through the protein-conducting channel: analogous mechanisms at work? (original) (raw)
Nelson, W.J. & Yeaman, C. Protein trafficking in the exocytic pathway of polarized epithelial cells. Trends Cell Biol.11, 483–486 (2001). ArticleCASPubMed Google Scholar
Mitra, K., Ubarretxena-Belandia, I., Taguchi, T., Warren, G. & Engelman, D.M. Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol. Proc. Natl. Acad. Sci. USA101, 4083–4088 (2004). ArticleCASPubMedPubMed Central Google Scholar
Simon, S.M. & Blobel, G. A protein-conducting channel in the endoplasmic reticulum. Cell65, 371–380 (1991). ArticleCASPubMed Google Scholar
Wickner, W., Driessen, A.J.M. & Hartl, F.U. The enzymology of protein translocation across the Escherichia coli plasma membrane. Annu. Rev. Biochem.60, 101–124 (1991). ArticleCASPubMed Google Scholar
Osborne, A.R., Rapoport, T.A. & van den Berg, B. Protein translocation by the Sec61/SecY channel. Annu. Rev. Cell Dev. Biol.21, 529–550 (2005). ArticleCASPubMed Google Scholar
Economou, A. & Wickner, W. SecA promotes preprotein translocation by under-going ATP-driven cycles of membrane insertion and deinsertion. Cell78, 835–843 (1994). ArticleCASPubMed Google Scholar
Panzner, S., Dreier, L., Hartmann, E., Kostka, S. & Rapoport, T.A. Post-translational protein transport in yeast reconstituted with a purified complex of Sec proteins and Kar2p. Cell81, 561–570 (1995). ArticleCASPubMed Google Scholar
van den Berg, B. et al. X-ray structure of a protein-conducting channel. Nature427, 36–44 (2004). ArticleCASPubMed Google Scholar
Blobel, G. & Dobberstein, B. Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J. Cell Biol.67, 835–851 (1975). ArticleCASPubMed Google Scholar
Eisner, G., Koch, H.G., Beck, K., Brunner, J. & Mueller, M. Ligand crowding at a nascent signal sequence. J. Cell Biol.163, 35–44 (2003). ArticleCASPubMedPubMed Central Google Scholar
Valent, Q.A. et al. Early events in preprotein recognition in E. coli: interactions of SRP and trigger factor with nascent polypeptides. EMBO J.14, 5494–5505 (1995). ArticleCASPubMedPubMed Central Google Scholar
Ng, D.T.W., Brown, J.D. & Walter, P. Signal sequences specify the targeting route to the endoplasmic reticulum. J. Cell Biol.134, 269–278 (1996). ArticleCASPubMed Google Scholar
Bruch, M.D., McKnight, C.J. & Gierasch, L.M. Helix formation and stability in a signal sequence. Biochemistry28, 8554–8561 (1989). ArticleCASPubMed Google Scholar
Raden, D., Song, W. & Gilmore, R. Role of the cytoplasmic segments of Sec61α in the ribosome-binding and translocation-promoting activities of the Sec61 complex. J. Cell Biol.150, 53–64 (2000). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
Snapp, E.L., Reinhart, G.A., Bogert, B.A., Lippincott-Schwartz, J. & Hegde, R.S. The organization of engaged and quiescent translocons in the endoplasmic reticulum of mammalian cells. J. Cell Biol.164, 997–1007 (2004). ArticleCASPubMedPubMed Central Google Scholar
Bessonneau, P., Besson, V., Collinson, I. & Duong, F. The SecYEG preprotein translocation channel is a conformationally dynamic and dimeric structure. EMBO J.21, 995–1003 (2002). ArticleCASPubMedPubMed Central Google Scholar
Beckmann, R. et al. Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell107, 361–372 (2001). ArticleCASPubMed Google Scholar
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). CASPubMed Google Scholar
Scheuring, J. et al. The oligomeric distribution of SecYEG is altered by SecA and translocation ligands. J. Mol. Biol.354, 258–271 (2005). ArticleCASPubMed Google Scholar
Blobel, G. & Dobberstein, B. Transfer of proteins across membranes. II. Reconstitution of functional rough microsomes from heterologous components. J. Cell Biol.67, 852–862 (1975). ArticleCASPubMed Google Scholar
Martoglio, B., Hofmann, M.W., Brunner, J. & Dobberstein, B. The protein-conducting channel in the membrane of the endoplasmic reticulum is open laterally toward the lipid bilayer. Cell81, 207–214 (1995). ArticleCASPubMed Google Scholar
Tani, K., Tokuda, H. & Mizushima, S. Translocation of ProOmpA possessing an intramolecular disulfide bridge into membrane vesicles of Escherichia coli. Effect of membrane energization. J. Biol. Chem.265, 17341–17347 (1990). CASPubMed Google Scholar
Mitra, K. & Frank, J. A model for co-translational translocation: ribosome-regulated nascent polypeptide translocation at the protein-conducting channel. FEBS Lett.580, 3353–3360 (2006). ArticleCASPubMed Google Scholar
Simon, S.M., Blobel, G. & Zimmerberg, J. Large aqueous channels in membrane vesicles derived from the rough endoplasmic reticulum of canine pancreas or the plasma membrane of Escherichia coli. Proc. Natl. Acad. Sci. USA86, 6176–6180 (1989). ArticleCASPubMedPubMed Central Google Scholar
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. Cell102, 233–244 (2000). ArticleCASPubMed Google Scholar
Romisch, K. et al. Homology of 54K protein of signal-recognition particle, docking protein and two E. coli proteins with putative GTP-binding domains. Nature340, 478–482 (1989). ArticleCASPubMed Google Scholar
Walter, P. & Blobel, G. Purification of a membrane-associated protein complex required for protein translocation across the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA77, 7112–7116 (1980). ArticleCASPubMedPubMed Central Google Scholar
Song, W., Raden, D., Mandon, E.C. & Gilmore, R. Role of Sec61α in the regulated transfer of the ribosome-nascent chain complex from the signal recognition particle to the translocation channel. Cell100, 333–343 (2000). ArticleCASPubMed Google Scholar
Keenan, R.J., Freymann, D.M., Stroud, R.M. & Walter, P. The signal recognition particle. Annu. Rev. Biochem.70, 755–775 (2001). ArticleCASPubMed Google Scholar
Ladefoged, S.A. & Christiansen, G. A GTP-binding protein of Mycoplasma hominis: a small sized homolog to the signal recognition particle receptor FtsY. Gene201, 37–44 (1997). ArticleCASPubMed Google Scholar
Meyer, D.I. & Dobberstein, B. 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 (1980). ArticleCASPubMed Google Scholar
Bacher, G., Lutcke, H., Jungnickel, B., Rapoport, T.A. & Dobberstein, B. Regulation by the ribosome of the GTPase of the signal-recognition particle during protein targeting. Nature381, 248–251 (1996). ArticleCASPubMed Google Scholar
Helmers, J., Schmidt, D., Glavy, J.S., Blobel, G. & Schwartz, T. The β-subunit of the protein-conducting channel of the endoplasmic reticulum functions as the guanine nucleotide exchange factor for the β-subunit of the signal recogntion particle receptor. J. Biol. Chem.278, 23686–23690 (2003). ArticleCASPubMed Google Scholar
Halic, M. et al. Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature427, 808–814 (2004). ArticleCASPubMed Google Scholar
Shan, S.O., Stroud, R.M. & Walter, P. Mechanism of association and reciprocal activation of two GTPases. PLoS Biol.2, e320 (2004). ArticlePubMedPubMed Central Google Scholar
Angelini, S., Deitermann, S. & Koch, H.G. FtsY, the bacterial signal-recognition particle receptor, interacts functionally and physically with the SecYEG translocon. EMBO Rep.6, 476–481 (2005). ArticleCASPubMedPubMed Central Google Scholar
Legate, K.R., Falcone, D. & Andrews, D.W. Nucleotide-dependent bindingj of the GTPase domain of the signal recognition particle receptor β-subunit to the α-subunit. J. Biol. Chem.275, 27439–27446 (2000). CASPubMed Google Scholar
Schwartz, T. & Blobel, G. Structural basis for the function of the β subunit of the eukaryotic signal recognition particle receptor. Cell112, 793–803 (2003). ArticleCASPubMed Google Scholar
Focia, P.J., Shepotinovskaya, I.V., Seidler, J.A. & Freymann, D.M. Heterodimeric GTPase core of the SRP targeting complex. Science303, 373–377 (2004). ArticleCASPubMedPubMed Central Google Scholar
Powers, T. & Walter, P. Reciprocal stimulation of GTP hydrolysis by two directly interacting GTPases. Science269, 1422–1424 (1995). ArticleCASPubMed Google Scholar
Pool, M.R., Stumm, J., Fulga, T.A., Sinning, I. & Dobberstein, B. Distinct modes of signal recognition particle interaction with the ribosome. Science297, 1345–1348 (2002). ArticleCASPubMed Google Scholar
Bacher, G., Pool, M. & Dobberstein, B. The ribosome regulates the GTPase of the beta-subunit of the signal recognition particle receptor. J. Cell Biol.146, 723–730 (1999). ArticleCASPubMedPubMed Central Google Scholar
Fulga, T.A., Sinning, I., Dobberstein, B. & Pool, M.R. SRb coordinates signal sequence release from SRP with ribosome binding to the translocon. EMBO J.20, 2338–2347 (2001). ArticleCASPubMedPubMed Central Google Scholar
Shaw, A.S., Rottier, P.J.M. & Rose, J.K. Evidence for the loop model of signal-sequence insertion into the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA85, 7592–7596 (1988). ArticleCASPubMedPubMed Central Google Scholar
Mitra, K. et al. Elongation arrest by SecM via a cascade of ribosomal RNA rearrangements. Mol. Cell22, 533–543 (2006). ArticleCASPubMed Google Scholar
Rutkowski, D.T., Ott, C.M., Polansky, J.R. & Lingappa, V.R. Signal sequences initiate the pathway of maturation in the endoplasmic reticulum lumen. J. Biol. Chem.278, 30365–30372 (2003). ArticleCASPubMed Google Scholar
Houben, E.N. et al. YidC and SecY mediate membrane insertion of a type I transmembrane domain. J. Biol. Chem.277, 35880–35886 (2002). ArticleCASPubMed Google Scholar
Hunt, J.F. et al. Nucleotide control of interdomain interactions in the conformational reaction cycle of SecA. Science297, 2018–2026 (2002). ArticleCASPubMed Google Scholar
Sharma, V. et al. Crystal structure of Mycobacterium tuberculosis SecA, a preprotein translocating ATPase. Proc. Natl. Acad. Sci. USA100, 2243–2248 (2003). ArticleCASPubMedPubMed Central Google Scholar
Natale, P., Swaving, J., de Keyzer, J., van der Does, C. & Driessen, A.J.M. Binding of SecA to the SecYEG complex accelerates the nucleotide exchange kinetics on SecA. J. Biol. Chem.279, 13769–13777 (2004). ArticleCASPubMed Google Scholar
Lill, R. et al. SecA protein hydrolyzes ATP and is an essential component of the protein translocation ATPase of Escherichia coli. EMBO J.8, 961–966 (1989). ArticleCASPubMedPubMed Central Google Scholar
Schiebel, E., Driessen, A.J.M., Hartl, F.U. & Wickner, W. ΔμH+ and ATP function at different steps of the catalytic cyle of preprotein translocase. Cell64, 927–939 (1991). ArticleCASPubMed Google Scholar
van Der Wolk, J.P., de Wit, J.G. & Driessen, A.J.M. The catalytic cycle of the Escherichia coli SecA ATPase comprises two distinct preprotein translocation events. EMBO J.16, 7297–7304 (1997). ArticleCASPubMedPubMed Central Google Scholar
Xu, Z., Knafels, J.D. & Yoshino, K. Crystal structure of the bactieral protein export chaperone SecB. Nat. Struct. Biol.7, 1172–1177 (2000). ArticleCASPubMed Google Scholar
Knoblauch, N.T. et al. Substrate specificity of the SecB chaperone. J. Biol. Chem.274, 34219–34225 (1999). ArticleCASPubMed Google Scholar
Fekkes, P., van der Does, C. & Driessen, A.J.M. The molecular chaperone SecB is released from the carboxy-terminus of SecA during initiation of precursor protein translocation. EMBO J.16, 6105–6113 (1997). ArticleCASPubMedPubMed Central Google Scholar
Zhou, J. & Xu, Z. Structural determinants of SecB recognition by SecA in bacterial protein translocation. Nat. Struct. Biol.10, 942–947 (2003). ArticleCASPubMed Google Scholar
Hartl, F.U., Lecker, S., Schiebel, E., Hendrick, J.P. & Wickner, W. The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane. Cell63, 269–279 (1990). ArticleCASPubMed Google Scholar
Baud, C. et al. Allosteric communication between signal peptides and the SecA protein DEAD motor ATPase domain. J. Biol. Chem.277, 13724–13731 (2002). ArticleCASPubMed Google Scholar
Vrontou, E., Karamanou, S., Baud, C., Sianidis, G. & Economou, A. Global co-ordination of protein translocation by the SecA IRA1 switch. J. Biol. Chem.279, 22490–22497 (2004). ArticleCASPubMed Google Scholar
van der Sluis, E.O. et al. Identification of two interaction sites in SecY that are important for the functional interaction with SecA. J. Mol. Biol.361, 839–849 (2006). ArticleCASPubMed Google Scholar
Tziatzios, C. et al. The baterial protein-translocation complex: SecYEG dimers associate with one or two SecA molecules. J. Mol. Biol.340, 513–524 (2004). ArticleCASPubMed Google Scholar
de Keyzer, J. et al. Covalently dimerized SecA is functional in protein translocation. J. Biol. Chem.280, 35255–35260 (2005). ArticleCASPubMed Google Scholar
Jilaveanu, L.B., Zito, C.R. & Oliver, D. Dimeric SecA is essential for protein translocation. Proc. Natl. Acad. Sci. USA102, 7511–7516 (2005). ArticleCASPubMedPubMed Central Google Scholar
Natale, P., den Blaauwen, T., van der Does, C. & Driessen, A.J.M. Conformational state of the SecYEG-bound SecA probed by single tryptophan fluorescence spectroscopy. Biochemistry44, 6424–6432 (2005). ArticleCASPubMed Google Scholar
Benach, J. et al. Phospholipid-induced monomerization and signal-peptide-induced oligomerization of SecA. J. Biol. Chem.278, 3628–3638 (2003). ArticleCASPubMed Google Scholar