The translational regulatory function of SecM requires the precise timing of membrane targeting

Molecular Microbiology

Volumn 81, Issue 2, 2011, Pages 540-553

  Yap, Mee Ngan ^a   Bernstein, Harris D ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN SECA; PROTEIN SECM; SECRETORY PROTEIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE DELETION; GENE INSERTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN SYNTHESIS; PROTEIN TARGETING; RIBOSOME; RNA STRUCTURE; TRANSLATION REGULATION;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CELL MEMBRANE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; INDEL MUTATION; MEMBRANE TRANSPORT PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION, MISSENSE; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN SORTING SIGNALS; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS;

ESCHERICHIA COLI;

EID: 79960199054     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07713.x     Document Type: Article

References (48)

1. Arkowitz, R.A., and Wickner, W. (1994) SecD and SecF are required for the proton electrochemical gradient stimulation of preprotein translocation. EMBO J 13: 954-963.
2. Baba, T., Jacq, A., Brickman, E., Beckwith, J., Taura, T., Ueguchi, C., etal. (1990) Characterization of cold-sensitive secY mutants of Escherichia coli. J Bacteriol 172: 7005-7010.
3. Beha, D., Deitermann, S., Müller, M., and Koch, H.G. (2003) Export of β-lactamase is independent of the signal recognition particle. J Biol Chem 278: 22161-22167.
4. Bendtsen, J.D., Nielsen, H., von Heijne, G., and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
5. Brandt, F., Etchells, S.A., Ortiz, J.O., Elcock, A.H., Hartl, F.U., and Baumeister, W. (2009) The native 3D organization of bacterial polysomes. Cell 136: 261-271.
6. Butkus, M.E., Prundeanu, L.B., and Oliver, D.B. (2003) Translocon 'pulling' of nascent SecM controls the duration of its translational pause and secretion-responsive secA regulation. J Bacteriol 185: 6719-6722.
7. Carlsson, F., Stalhammar-Carlemalm, M., Flardh, K., Sandin, C., Carlemalm, E., and Lindahl, G. (2006) Signal sequence directs localized secretion of bacterial surface proteins. Nature 442: 943-946.
8. Cross, B.C., Sinning, I., Luirink, J., and High, S. (2009) Delivering proteins for export from the cytosol. Nat Rev Mol Cell Biol 10: 255-226.
9. Dalley, J.A., Selkirk, A., and Pool, M.R. (2008) Access to ribosomal protein Rpl25p by the signal recognition particle is required for efficient cotranslational translocation. Mol Biol Cell 19: 2876-2884.
10. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
11. Driessen, A.J., and Nouwen, N. (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77: 643-667.
12. Garza-Sanchez, F., Janssen, B.D., and Hayes, C.S. (2006) Prolyl-tRNA(Pro) in the A-site of SecM-arrested ribosomes inhibits the recruitment of transfer-messenger RNA. J Biol Chem 281: 34258-34268.
13. Hegde, R.S., and Bernstein, H.D. (2006) The surprising complexity of signal sequences. Trends Biochem Sci 31: 563-571.
14. von Heijne, G. (1985) Signal sequences. The limits of variation. J Mol Biol 184: 99-105.
15. Hiss, J.A., and Schneider, G. (2009) Architecture, function and prediction of long signal peptides. Brief Bioinform 10: 569-578.
16. Hiss, J.A., Resch, E., Schreiner, A., Meissner, M., Starzinski-Powitz, A., and Schneider, G. (2008) Domain organization of long signal peptides of single-pass integral membrane proteins reveals multiple functional capacity. PLoS ONE 3: e2767.
17. Huber, D., Boyd, D., Xia, Y., Olma, M.H., Gerstein, M., and Beckwith, J. (2005) Use of thioredoxin as a reporter to identify a subset of Escherichia coli signal sequences that promote signal recognition particle-dependent translocation. J Bacteriol 187: 2983-2991.
18. Keenan, R.J., Freymann, D.M., Stroud, R.M., and Walter, P. (2001) The signal recognition particle. Annu Rev Biochem 70: 755-775.
19. Lee, C., and Beckwith, J. (1986) Cotranslational and posttranslational protein translocation in prokaryotic systems. Annu Rev Cell Biol 2: 315-336.
20. Lee, H.C., and Bernstein, H.D. (2001) The targeting pathway of Escherichia coli presecretory and integral membrane proteins is specified by the hydrophobicity of the targeting signal. Proc Natl Acad Sci USA 98: 3471-3476.
21. Lee, H.C., and Bernstein, H.D. (2002) Trigger factor retards protein export in Escherichia coli. J Biol Chem 277: 43527-43535.
22. Lesley, S.A., Brow, M.D., and Burgess, R.R. (1991) Use of in vitro protein synthesis from polymerase chain reaction-generated templates to study interaction of Escherichia coli transcription factors with core RNA polymerase and for epitope mapping of monoclonal antibodies. J Biol Chem 266: 2632-2638.
23. Miroux, B., and Walker, J.E. (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol 260: 289-298.
24. Moser, M., Panahandeh, S., Holzapfel, E., and Müller, M. (2007) In vitro analysis of the bacterial twin-arginine-dependent protein export. Methods Mol Biol 390: 63-79.
25. Munavar, H., Zhou, Y., and Gottesman, S. (2005) Analysis of the Escherichia coli Alp phenotype: heat shock induction in ssrA mutants. J Bacteriol 187: 4739-4751.
26. Murakami, A., Nakatogawa, H., and Ito, K. (2004) Translation arrest of SecM is essential for the basal and regulated expression of SecA. Proc Natl Acad Sci USA 101: 12330-12335.
27. Muto, H., Nakatogawa, H., and Ito, K. (2006) Genetically encoded but nonpolypeptide prolyl-tRNA functions in the A site for SecM-mediated ribosomal stall. Mol Cell 22: 545-552.
28. Nakatogawa, H., and Ito, K. (2001) Secretion monitor, SecM, undergoes self-translation arrest in the cytosol. Mol Cell 7: 185-192.
29. Nakatogawa, H., and Ito, K. (2002) The ribosomal exit tunnel functions as a discriminating gate. Cell 108: 629-636.
30. Nakatogawa, H., Murakami, A., Mori, H., and Ito, K. (2005) SecM facilitates translocase function of SecA by localizing its biosynthesis. Genes Dev 19: 436-444.
31. Neumann-Haefelin, C., Schafer, U., Müller, M., and Koch, H.G. (2000) SRP-dependent co-translational targeting and SecA-dependent translocation analyzed as individual steps in the export of a bacterial protein. EMBO J 19: 6419-6426.
32. Oliver, D., Norman, J., and Sarker, S. (1998) Regulation of Escherichia coli secA by cellular protein secretion proficiency requires an intact gene X signal sequence and an active translocon. J Bacteriol 180: 5240-5242.
33. Peterson, J.H., Woolhead, C.A., and Bernstein, H.D. (2003) Basic amino acids in a distinct subset of signal peptides promote interaction with the signal recognition particle. J Biol Chem 278: 46155-46162.
34. Peterson, J.H., Szabady, R.L., and Bernstein, H.D. (2006) An unusual signal peptide extension inhibits the binding of bacterial presecretory proteins to the signal recognition particle, trigger factor, and the SecYEG complex. J Biol Chem 281: 9038-9048.
35. Randall, L.L. (1983) Translocation of domains of nascent periplasmic proteins across the cytoplasmic membrane is independent of elongation. Cell 33: 231-240.
36. Sarker, S., and Oliver, D. (2002) Critical regions of secM that control its translation and secretion and promote secretion-specific secA regulation. J Bacteriol 184: 2360-2369.
37. Schiebel, E., Driessen, A.J.M., Hartl, F.-U., and Wickner, W. (1991) DmH+ and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell 64: 927-939.
38. Schierle, C.F., Berkmen, M., Huber, D., Kumamoto, C., Boyd, D., and Beckwith, J. (2003) The DsbA signal sequence directs efficient, cotranslational export of passenger proteins to the Escherichia coli periplasm via the signal recognition particle pathway. J Bacteriol 185: 5706-5713.
39. Steitz, J.A. (1969) Polypeptide chain initiation: nucleotide sequences of the three ribosomal binding sites in bacteriophage R17 RNA. Nature 224: 957-964.
40. van Stelten, J., Silva, F., Belin, D., and Silhavy, T.J. (2009) Effects of antibiotics and a proto-oncogene homolog on destruction of protein translocator SecY. Science 325: 753-756.
41. Szabady, R.L., Peterson, J.H., Skillman, K.M., and Bernstein, H.D. (2005) An unusual signal peptide facilitates late steps in the biogenesis of a bacterial autotransporter. Proc Natl Acad Sci USA 102: 221-226.
42. Tanner, D.R., Cariello, D.A., Woolstenhulme, C.J., Broadbent, M.A., and Buskirk, A.R. (2009) Genetic identification of nascent peptides that induce ribosome stalling. J Biol Chem 284: 34809-34818.
43. Tenson, T., and Ehrenberg, M. (2002) Regulatory nascent peptides in the ribosomal tunnel. Cell 108: 591-594.
44. Ulbrandt, N.D., Newitt, J.A., and Bernstein, H.D. (1997) The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell 88: 187-196.
45. Underwood, K.A., Swartz, J.R., and Puglisi, J.D. (2005) Quantitative polysome analysis identifies limitations in bacterial cell-free protein synthesis. Biotechnol Bioeng 91: 425-435.
46. Woolhead, C.A., Johnson, A.E., and Bernstein, H.D. (2006) Translation arrest requires two-way communication between a nascent polypeptide and the ribosome. Mol Cell 22: 587-598.
47. Yap, M.-N., and Bernstein, H.D. (2009) The plasticity of a translation arrest motif yields insights into nascent polypeptide recognition inside the ribosome tunnel. Mol Cell 34: 201-211.
48. Zimmer, J., Nam, Y., and Rapoport, T.A. (2008) Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature 455: 936-943.