Orientation of internal signal-anchor sequences at the sec61 translocon

Journal of Molecular Biology

Volumn 424, Issue 5, 2012, Pages 368-378

  Kocik, Lucyna ^a   Junne, Tina ^a   Spiess, Martin ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

hydrophobicity; membrane insertion; membrane protein; topology

Indexed keywords

TRANSLOCON;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; ENDOPLASMIC RETICULUM; HYDROPHOBICITY; INTERNAL SIGNAL ANCHOR SEQUENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN TRANSPORT;

EID: 84869215749     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.10.010     Document Type: Article

References (36)

1. A.R. Osborne, T.A. Rapoport, and B. van den Berg Protein translocation by the Sec61/SecY channel Annu. Rev. Cell Dev. Biol. 21 2005 529 550
2. B.C.S. Cross, I. Sinning, J. Luirink, and S. High Delivering proteins for export from the cytosol Nat. Rev. Mol. Cell. Biol. 10 2009 255 264
3. E.C. Mandon, S.F. Trueman, and R. Gilmore Translocation of proteins through the Sec61 and SecYEG channels Curr. Opin. Cell Biol. 21 2009 501 507
4. P.F. Egea, and R.M. Stroud Lateral opening of a translocon upon entry of protein suggests the mechanism of insertion into membranes Proc. Natl Acad. Sci. USA 2010
5. T. Tsukazaki, H. Mori, S. Fukai, R. Ishitani, T. Mori, and N. Dohmae Conformational transition of Sec machinery inferred from bacterial SecYE structures Nature 455 2008 988 991
6. B. van den Berg, W.M. Clemons, I. Collinson, Y. Modis, E. Hartmann, S.C. Harrison, and T.A. Rapoport X-ray structure of a protein-conducting channel Nature 427 2003 36 44
7. J. Zimmer, Y. Nam, and T.A. Rapoport Structure of a complex of the ATPase SecA and the protein-translocation channel Nature 455 2008 936 943
8. K. Dalal, and F. Duong The SecY complex forms a channel capable of ionic discrimination EMBO Rep. 10 2009 762 768
9. E. Park, and T.A. Rapoport Preserving the membrane barrier for small molecules during bacterial protein translocation Nature 473 2011 239 242
10. T. Hessa, H. Kim, K. Bihlmaier, C. Lundin, J. Boekel, and H. Andersson Recognition of transmembrane helices by the endoplasmic reticulum translocon Nature 433 2005 377 381
11. T. Hessa, N.M. Meindl-Beinker, A. Bernsel, H. Kim, Y. Sato, and M. Lerch-Bader Molecular code for transmembrane-helix recognition by the Sec61 translocon Nature 450 2007 1026 1030
12. T. Junne, L. Kocik, and M. Spiess The hydrophobic core of the Sec61 translocon defines the hydrophobicity threshold for membrane integration Mol. Biol. Cell 21 2010 1662 1670
13. M. Higy, T. Junne, and M. Spiess Topogenesis of membrane proteins at the endoplasmic reticulum Biochemistry 43 2004 12716 12722
14. J.P. Beltzer, K. Fiedler, C. Fuhrer, I. Geffen, C. Handschin, H.P. Wessels, and M. Spiess Charged residues are major determinants of the transmembrane orientation of a signal-anchor sequence J. Biol. Chem. 266 1991 973 978
15. G. von Heijne The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology EMBO J. 5 1986 3021 3027
16. E. Hartmann, T.A. Rapoport, and H.F. Lodish Predicting the orientation of eukaryotic membrane-spanning proteins Proc. Natl Acad. Sci. USA 86 1989 5786 5790
17. A.J. Denzer, C.E. Nabholz, and M. Spiess Transmembrane orientation of signal-anchor proteins is affected by the folding state but not the size of the N-terminal domain EMBO J. 14 1995 6311 6317
18. M. Sakaguchi, R. Tomiyoshi, T. Kuroiwa, K. Mihara, and T. Omura Functions of signal and signal-anchor sequences are determined by the balance between the hydrophobic segment and the N-terminal charge Proc. Natl Acad. Sci. USA 89 1992 16 19
19. J.M. Wahlberg, and M. Spiess Multiple determinants direct the orientation of signal-anchor proteins: the topogenic role of the hydrophobic signal domain J. Cell Biol. 137 1997 555 562
20. V. Goder, and M. Spiess Molecular mechanism of signal sequence orientation in the endoplasmic reticulum EMBO J. 22 2003 3645 3653
21. P.K. Devaraneni, B. Conti, Y. Matsumura, Z. Yang, A.E. Johnson, and W.R. Skach Stepwise insertion and inversion of a type II signal anchor sequence in the ribosome-Sec61 translocon complex Cell 146 2011 134 147
22. K. Rösch, D. Naeher, V. Laird, V. Goder, and M. Spiess The topogenic contribution of uncharged amino acids on signal sequence orientation in the endoplasmic reticulum J. Biol. Chem. 275 2000 14916 14922
23. J. Frauenfeld, J. Gumbart, E.O. van der Sluis, S. Funes, M. Gartmann, and B. Beatrix Cryo-EM structure of the ribosome-SecYE complex in the membrane environment Nat. Struct. Mol. Biol. 18 2011 614 621
24. T. Becker, S. Bhushan, A. Jarasch, J.-P. Armache, S. Funes, and F. Jossinet Structure of monomeric yeast and mammalian Sec61 complexes interacting with the translating ribosome Science 326 2009 1369 1373
25. F. Bonardi, E. Halza, M. Walko, F. Du Plessis, N. Nouwen, B.L. Feringa, and A.J.M. Driessen Probing the SecYEG translocation pore size with preproteins conjugated with sizable rigid spherical molecules Proc. Natl Acad. Sci. USA 108 2011 7775 7780
26. V. Goder, C. Bieri, and M. Spiess Glycosylation can influence topogenesis of membrane proteins and reveals dynamic reorientation of nascent polypeptides within the translocon J. Cell Biol. 147 1999 257 266
27. Y. Kida, F. Morimoto, and M. Sakaguchi Two translocating hydrophilic segments of a nascent chain span the ER membrane during multispanning protein topogenesis J. Cell Biol. 179 2007 1441 1452
28. P.-J. Lin, C.G. Jongsma, S. Liao, and A.E. Johnson Transmembrane segments of nascent polytopic membrane proteins control cytosol/ER targeting during membrane integration J. Cell Biol. 195 2011 41 54
29. P.-J. Lin, C.G. Jongsma, M.R. Pool, and A.E. Johnson Polytopic membrane protein folding at L17 in the ribosome tunnel initiates cyclical changes at the translocon J. Cell Biol. 195 2011 55 70
30. T. Junne, T. Schwede, V. Goder, and M. Spiess Mutations in the Sec61p channel affecting signal sequence recognition and membrane protein topology J. Biol. Chem. 282 2007 33201 33209
31. M.A. Smith, W.M. Clemons, C.J. DeMars, and A.M. Flower Modeling the effects of prl mutations on the Escherichia coli SecY complex J. Bacteriol. 187 2005 6454 6465
32. M. Higy, S. Gander, and M. Spiess Probing the environment of signal-anchor sequences during topogenesis in the endoplasmic reticulum Biochemistry 44 2005 2039 2047
33. T.A. Rapoport, V. Goder, S.U. Heinrich, and K.E.S. Matlack Membrane-protein integration and the role of the translocation channel Trends Cell Biol. 14 2004 568 575
34. Y. Kida, F. Morimoto, and M. Sakaguchi Signal anchor sequence provides motive force for polypeptide chain translocation through the endoplasmic reticulum membrane J. Biol. Chem. 284 2009 2861 2866
35. E. Wallin, and G. von Heijne Properties of N-terminal tails in G-protein coupled receptors: a statistical study Protein Eng. 8 1995 693 698
36. H. Andersson, A.M. D'Antona, D.A. Kendall, G. von Heijne, and C.-N. Chin Membrane assembly of the cannabinoid receptor 1: impact of a long N-terminal tail Mol. Pharmacol. 64 2003 570 577