DOI: 10.1038/nsmb.1402. Signal sequence–independent membrane targeting of ribosomes containing short nascent peptides within the exit tunnel

Signal sequence–independent membrane targeting of ribosomes containing short nascent peptides within the exit tunnel

10.1038/nsmb.1402

Crossref journal-article

Springer Science and Business Media LLC

Nature Structural & Molecular Biology (297)

Bibliography

Bornemann, T., JÃ¶ckel, J., Rodnina, M. V., & Wintermeyer, W. (2008). Signal sequenceâindependent membrane targeting of ribosomes containing short nascent peptides within the exit tunnel. Nature Structural & Molecular Biology, 15(5), 494â499.

Authors 4

Thomas Bornemann (first)
Johannes Jöckel (additional)
Marina V Rodnina (additional)
Wolfgang Wintermeyer (additional)

References 46 Referenced 155

Koch, H.G. et al. In vitro studies with purified components reveal signal recognition particle (SRP) and SecA/SecB as constituents of two independent protein-targeting pathways of Escherichia coli. Mol. Biol. Cell 10, 2163–2173 (1999). (10.1091/mbc.10.7.2163) / Mol. Biol. Cell by HG Koch (1999)
Ulbrandt, N.D., Newitt, J.A. & Bernstein, H.D. The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell 88, 187–196 (1997). (10.1016/S0092-8674(00)81839-5) / Cell by ND Ulbrandt (1997)
MacFarlane, J. & Müller, M. The functional integration of a polytopic membrane protein of Escherichia coli is dependent on the bacterial signal-recognition particle. Eur. J. Biochem. 233, 766–771 (1995). (10.1111/j.1432-1033.1995.766_3.x) / Eur. J. Biochem. by J MacFarlane (1995)
Luirink, J., von Heijne, G., Houben, E. & de Gier, J.W. Biogenesis of inner membrane proteins in Escherichia coli. Annu. Rev. Microbiol. 59, 329–355 (2005). (10.1146/annurev.micro.59.030804.121246) / Annu. Rev. Microbiol. by J Luirink (2005)
Flanagan, J.J. et al. Signal recognition particle binds to ribosome-bound signal sequences with fluorescence-detected subnanomolar affinity that does not diminish as the nascent chain lengthens. J. Biol. Chem. 278, 18628–18637 (2003). (10.1074/jbc.M300173200) / J. Biol. Chem. by JJ Flanagan (2003)
Van den Berg, B. et al. X-ray structure of a protein-conducting channel. Nature 427, 36–44 (2004). (10.1038/nature02218) / Nature by B Van den Berg (2004)
Walter, P. & Blobel, G. 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 (1981). (10.1083/jcb.91.2.557) / J. Cell Biol. by P Walter (1981)
Wolin, S.L. & Walter, P. Signal recognition particle mediates a transient elongation arrest of preprolactin in reticulocyte lysate. J. Cell Biol. 109, 2617–2622 (1989). (10.1083/jcb.109.6.2617) / J. Cell Biol. by SL Wolin (1989)
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). (10.1093/emboj/19.15.4164) / EMBO J. by N Mason (2000)
Raine, A. et al. Targeting and insertion of heterologous membrane proteins in E. coli. Biochimie 85, 659–668 (2003). (10.1016/S0300-9084(03)00130-5) / Biochimie by A Raine (2003)
de Gier, J.W. et al. Assembly of a cytoplasmic membrane protein in Escherichia coli is dependent on the signal recognition particle. FEBS Lett. 399, 307–309 (1996). (10.1016/S0014-5793(96)01354-3) / FEBS Lett. by JW de Gier (1996)
Nakahigashi, K. et al. HemK, a class of protein methyl transferase with similarity to DNA methyl transferases, methylates polypeptide chain release factors, and hemK knockout induces defects in translational termination. Proc. Natl. Acad. Sci. USA 99, 1473–1478 (2002). (10.1073/pnas.032488499) / Proc. Natl. Acad. Sci. USA by K Nakahigashi (2002)
Buskiewicz, I., Kubarenko, A., Peske, F., Rodnina, M.V. & Wintermeyer, W. Domain rearrangement of SRP protein Ffh upon binding 4.5S RNA and the SRP receptor FtsY. RNA 11, 947–957 (2005). (10.1261/rna.7242305) / RNA by I Buskiewicz (2005)
Buskiewicz, I. et al. Conformations of the signal recognition particle protein Ffh from Escherichia coli as determined by FRET. J. Mol. Biol. 351, 417–430 (2005). (10.1016/j.jmb.2005.06.023) / J. Mol. Biol. by I Buskiewicz (2005)
Batey, R.T., Rambo, R.P., Lucast, L., Rha, B. & Doudna, J.A. Crystal structure of the ribonucleoprotein core of the signal recognition particle. Science 287, 1232–1239 (2000). (10.1126/science.287.5456.1232) / Science by RT Batey (2000)
Ban, N., Nissen, P., Hansen, J., Moore, P.B. & Steitz, T.A. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289, 905–920 (2000). (10.1126/science.289.5481.905) / Science by N Ban (2000)
Houben, E.N., Zarivach, R., Oudega, B. & Luirink, J. Early encounters of a nascent membrane protein: specificity and timing of contacts inside and outside the ribosome. J. Cell Biol. 170, 27–35 (2005). (10.1083/jcb.200503035) / J. Cell Biol. by EN Houben (2005)
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). (10.1016/S0092-8674(04)00169-2) / Cell by CA Woolhead (2004)
Lu, J. & Deutsch, C. Folding zones inside the ribosomal exit tunnel. Nat. Struct. Mol. Biol. 12, 1123–1129 (2005). (10.1038/nsmb1021) / Nat. Struct. Mol. Biol. by J Lu (2005)
Ryan, P. & Edwards, C.O. Systematic introduction of proline in a eukaryotic signal sequence suggests asymmetry within the hydrophobic core. J. Biol. Chem. 270, 27876–27879 (1995). (10.1074/jbc.270.46.27876) / J. Biol. Chem. by P Ryan (1995)
Hessa, T. et al. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433, 377–381 (2005). (10.1038/nature03216) / Nature by T Hessa (2005)
Beha, D., Deitermann, S., Müller, M. & Koch, H.G. Export of β-lactamase is independent of the signal recognition particle. J. Biol. Chem. 278, 22161–22167 (2003). (10.1074/jbc.M300929200) / J. Biol. Chem. by D Beha (2003)
Eitan, A. & Bibi, E. The core Escherichia coli signal recognition particle receptor contains only the N and G domains of FtsY. J. Bacteriol. 186, 2492–2494 (2004). (10.1128/JB.186.8.2492-2494.2004) / J. Bacteriol. by A Eitan (2004)
Jagath, J.R. et al. Important role of the tetraloop region of 4.5S RNA in SRP binding to its receptor FtsY. RNA 7, 293–301 (2001). (10.1017/S1355838201002205) / RNA by JR Jagath (2001)
Peluso, P. et al. Role of 4.5S RNA in assembly of the bacterial signal recognition particle with its receptor. Science 288, 1640–1643 (2000). (10.1126/science.288.5471.1640) / Science by P Peluso (2000)
Halic, M. et al. Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature 427, 808–814 (2004). (10.1038/nature02342) / Nature by M Halic (2004)
Gu, S.Q., Peske, F., Wieden, H.J., Rodnina, M.V. & Wintermeyer, W. The signal recognition particle binds to protein L23 at the peptide exit of the Escherichia coli ribosome. RNA 9, 566–573 (2003). (10.1261/rna.2196403) / RNA by SQ Gu (2003)
Kramer, G. et al. L23 protein functions as a chaperone docking site on the ribosome. Nature 419, 171–174 (2002). (10.1038/nature01047) / Nature by G Kramer (2002)
Raue, U., Oellerer, S. & Rospert, S. Association of protein biogenesis factors at the yeast ribosomal tunnel exit is affected by the translational status and nascent polypeptide sequence. J. Biol. Chem. 282, 7809–7816 (2007). (10.1074/jbc.M611436200) / J. Biol. Chem. by U Raue (2007)
Callender, R.H., Dyer, R.B., Gilmanshin, R. & Woodruff, W.H. Fast events in protein folding: the time evolution of primary processes. Annu. Rev. Phys. Chem. 49, 173–202 (1998). (10.1146/annurev.physchem.49.1.173) / Annu. Rev. Phys. Chem. by RH Callender (1998)
Miller, J.D., Bernstein, H.D. & Walter, P. Interaction of E. coli Ffh/4.5S ribonucleoprotein and FtsY mimics that of mammalian signal recognition particle and its receptor. Nature 367, 657–659 (1994). (10.1038/367657a0) / Nature by JD Miller (1994)
Zheng, N. & Gierasch, L.M. Domain interactions in E. coli SRP: stabilization of M domain by RNA is required for effective signal sequence modulation of NG domain. Mol. Cell 1, 79–87 (1997). (10.1016/S1097-2765(00)80009-X) / Mol. Cell by N Zheng (1997)
Nakatogawa, H. & Ito, K. The ribosomal exit tunnel functions as a discriminating gate. Cell 108, 629–636 (2002). (10.1016/S0092-8674(02)00649-9) / Cell by H Nakatogawa (2002)
Mitra, K. et al. Elongation arrest by SecM via a cascade of ribosomal RNA rearrangements. Mol. Cell 22, 533–543 (2006). (10.1016/j.molcel.2006.05.003) / Mol. Cell by K Mitra (2006)
Cruz-Vera, L.R., Gong, M. & Yanofsky, C. Changes produced by bound tryptophan in the ribosome peptidyl transferase center in response to TnaC, a nascent leader peptide. Proc. Natl. Acad. Sci. USA 103, 3598–3603 (2006). (10.1073/pnas.0600082103) / Proc. Natl. Acad. Sci. USA by LR Cruz-Vera (2006)
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). (10.1016/S0092-8674(00)80311-6) / Cell by S Liao (1997)
Ullers, R.S. et al. Interplay of signal recognition particle and trigger factor at L23 near the nascent chain exit site on the Escherichia coli ribosome. J. Cell Biol. 161, 679–684 (2003). (10.1083/jcb.200302130) / J. Cell Biol. by RS Ullers (2003)
Hsu, L.M., Zagorski, J. & Fournier, M.J. Cloning and sequence analysis of the Escherichia coli 4.5 S RNA gene. J. Mol. Biol. 178, 509–531 (1984). (10.1016/0022-2836(84)90236-5) / J. Mol. Biol. by LM Hsu (1984)
Jensen, C.G. & Pedersen, S. Concentrations of 4.5S RNA and Ffh protein in Escherichia coli: the stability of Ffh protein is dependent on the concentration of 4.5S RNA. J. Bacteriol. 176, 7148–7154 (1994). (10.1128/jb.176.23.7148-7154.1994) / J. Bacteriol. by CG Jensen (1994)
Golding, I. & Cox, E.C. Physical nature of bacterial cytoplasm. Phys. Rev. Lett. 96, 098102 (2006). (10.1103/PhysRevLett.96.098102) / Phys. Rev. Lett. by I Golding (2006)
Jagath, J.R., Rodnina, M.V. & Wintermeyer, W. Conformational changes in the bacterial SRP receptor FtsY upon binding of guanine nucleotides and SRP. J. Mol. Biol. 295, 745–753 (2000). (10.1006/jmbi.1999.3427) / J. Mol. Biol. by JR Jagath (2000)
De Vrije, T., Tommassen, J. & De Kruijff, B. Optimal posttranslational translocation of the precursor of PhoE protein across Escherichia coli membrane vesicles requires both ATP and the protonmotive force. Biochim. Biophys. Acta 900, 63–72 (1987). (10.1016/0005-2736(87)90278-1) / Biochim. Biophys. Acta by T De Vrije (1987)
Müller, M. & Blobel, G. In vitro translocation of bacterial proteins across the plasma membrane of Escherichia coli. Proc. Natl. Acad. Sci. USA 81, 7421–7425 (1984). (10.1073/pnas.81.23.7421) / Proc. Natl. Acad. Sci. USA by M Müller (1984)
Rodnina, M.V. & Wintermeyer, W. GTP consumption of elongation factor Tu during translation of heteropolymeric mRNAs. Proc. Natl. Acad. Sci. USA 92, 1945–1949 (1995). (10.1073/pnas.92.6.1945) / Proc. Natl. Acad. Sci. USA by MV Rodnina (1995)
Gu, S.Q. et al. Conformation of 4.5S RNA in the signal recognition particle and on the 30S ribosomal subunit. RNA 11, 1374–1384 (2005). (10.1261/rna.7219805) / RNA by SQ Gu (2005)
Laskey, R.A. & Mills, A.D. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Eur. J. Biochem. 56, 335–341 (1975). (10.1111/j.1432-1033.1975.tb02238.x) / Eur. J. Biochem. by RA Laskey (1975)

Dates

Type	When
Created	17 years, 4 months ago (April 6, 2008, 4:30 p.m.)
Deposited	2 years, 3 months ago (May 19, 2023, 12:22 a.m.)
Indexed	1 month ago (July 25, 2025, 6:30 a.m.)
Issued	17 years, 4 months ago (April 6, 2008)
Published	17 years, 4 months ago (April 6, 2008)
Published Online	17 years, 4 months ago (April 6, 2008)
Published Print	17 years, 3 months ago (May 1, 2008)

Funders 0

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BibTeX

@article{Bornemann_2008, title={Signal sequence–independent membrane targeting of ribosomes containing short nascent peptides within the exit tunnel}, volume={15}, ISSN={1545-9985}, url={http://dx.doi.org/10.1038/nsmb.1402}, DOI={10.1038/nsmb.1402}, number={5}, journal={Nature Structural & Molecular Biology}, publisher={Springer Science and Business Media LLC}, author={Bornemann, Thomas and Jöckel, Johannes and Rodnina, Marina V and Wintermeyer, Wolfgang}, year={2008}, month=apr, pages={494–499} }

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