Co-operation between different targeting pathways during integration of a membrane protein

Journal of Cell Biology

Volumn 199, Issue 2, 2012, Pages 303-315

  Keller, Rebecca ^a   de Keyzer, Jeanine ^b   Driessen, Arnold J M ^b   Palmer, Tracy ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; MEMBRANE PROTEIN; PROTEIN SEC; RIESKE PROTEIN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; STREPTOMYCES COELICOLOR;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CELL MEMBRANE; ELECTRON TRANSPORT COMPLEX III; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; STREPTOMYCES COELICOLOR;

ACTINOBACTERIA; STREPTOMYCES COELICOLOR;

EID: 84869146885     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201204149     Document Type: Article

References (45)

1. Alami, M., D. Trescher, L.F. Wu, and M. Müller. 2002. Separate analysis of twin-arginine translocation (Tat)-specific membrane binding and translocation in Escherichia coli. J. Biol. Chem. 277:20499-20503. http://dx.doi.org/10.1074/jbc.M201711200
2. Amann, E., B. Ochs, and K.J. Abel. 1988. Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene. 69:301-315. http://dx.doi.org/10.1016/0378-1119(88)90440-4
3. Bachmann, J., B. Bauer, K. Zwicker, B. Ludwig, and O. Anderka. 2006. The Rieske protein from Paracoccus denitrificans is inserted into the cytoplasmic membrane by the twin-arginine translocase. FEBS J. 273: 4817-4830. http://dx.doi.org/10.1111/j.1742-4658.2006.05480.x
4. Baneyx, F., and G. Georgiou. 1990. In vivo degradation of secreted fusion proteins by the Escherichia coli outer membrane protease OmpT. J. Bacteriol. 172:491-494.
5. Bartolomé, B., Y. Jubete, E. Martínez, and F. de la Cruz. 1991. Construction and properties of a family of pACYC184-derived cloning vectors compatible with pBR322 and its derivatives. Gene. 102:75-78. http://dx.doi.org/10.1016/0378-1119(91)90541-I
6. Berks, B.C. 1996. A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22:393-404. http://dx.doi.org/10.1046/j.1365-2958.1996.00114.x
7. Blaudeck, N., P. Kreutzenbeck, R. Freudl, and G.A. Sprenger. 2003. Genetic analysis of pathway specificity during posttranslational protein translocation across the Escherichia coli plasma membrane. J. Bacteriol. 185:2811-2819. http://dx.doi.org/10.1128/JB.185.9.2811-2819.2003
8. Caldelari, I., T. Palmer, and F. Sargent. 2008. Escherichia coli tat mutant strains are able to transport maltose in the absence of an active malE gene. Arch. Microbiol. 189:597-604. http://dx.doi.org/10.1007/s00203-008-0356-8
9. Casadaban, M.J., and S.N. Cohen. 1979. Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc. Natl. Acad. Sci. USA. 76:4530-4533. http://dx.doi.org/10.1073/pnas.76.9.4530
10. Cline, K., and S.M. Theg. 2007. The Sec and Tat protein translocation pathways in chloroplasts. In Molecular Machines Involved in Protein Transport Across Cellular Membranes. Vol. XXV. R.E. Dalbey, Koehler, C.M., and Tamanoi, F., editors. Elsevier, London. 463-492.
11. De Buck, E., L. Vranckx, E. Meyen, L. Maes, L. Vandersmissen, J. Anné, and E. Lammertyn. 2007. The twin-arginine translocation pathway is necessary for correct membrane insertion of the Rieske Fe/S protein in Legionella pneumophila. FEBS Lett. 581:259-264. http://dx.doi.org/10.1016/j.febslet.2006.12.022
12. De Keyzer, J., C. van der Does, J. Swaving, and A.J.M. Driessen. 2002. The F286Y mutation of PrlA4 tempers the signal sequence suppressor phenotype by reducing the SecA binding affinity. FEBS Lett. 510:17-21. http://dx.doi.org/10.1016/S0014-5793(01)03213-6
13. de Keyzer, J., M. van der Laan, and A.J.M. Driessen. 2007. Membrane protein insertion and secretion in bacteria. Methods Mol. Biol. 390:17-31. http://dx.doi.org/10.1007/978-1-59745-466-7_2
14. Driessen, A.J.M., and N. Nouwen. 2008. Protein translocation across the bacterial cytoplasmic membrane. Annu. Rev. Biochem. 77:643-667. http://dx.doi.org/10.1146/annurev.biochem.77.061606.160747
15. Du Plessis, D.J., N. Nouwen, and A.J.M. Driessen. 2006. Subunit a of cytochrome o oxidase requires both YidC and SecYEG for membrane insertion. J. Biol. Chem. 281:12248-12252. http://dx.doi.org/10.1074/jbc.M600048200
16. Gannon, P.M., P. Li, and C.A. Kumamoto. 1989. The mature portion of Escherichia coli maltose-binding protein (MBP) determines the dependence of MBP on SecB for export. J. Bacteriol. 171:813-818.
17. Guzman, L.M., D. Belin, M.J. Carson, and J. Beckwith. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121-4130.
18. Hatzixanthis, K., T. Palmer, and F. Sargent. 2003. A subset of bacterial inner membrane proteins integrated by the twin-arginine translocase. Mol. Microbiol. 49:1377-1390. http://dx.doi.org/10.1046/j.1365-2958.2003.03642.x
19. Ize, B., N.R. Stanley, G. Buchanan, and T. Palmer. 2003. Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol. Microbiol. 48:1183-1193. http://dx.doi.org/10.1046/j.1365-2958.2003.03504.x
20. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685. http://dx.doi.org/10.1038/227680a0
21. Lee, P.A., G.L. Orriss, G. Buchanan, N.P. Greene, P.J. Bond, C. Punginelli, R.L. Jack, M.S. Sansom, B.C. Berks, and T. Palmer. 2006. Cysteinescanning mutagenesis and disulfide mapping studies of the conserved domain of the twin-arginine translocase TatB component. J. Biol. Chem. 281:34072-34085. http://dx.doi.org/10.1074/jbc.M607295200
22. Molik, S., I. Karnauchov, C. Weidlich, R.G. Herrmann, and R.B. Klösgen. 2001. The Rieske Fe/S protein of the cytochrome b6/f complex in chloroplasts: missing link in the evolution of protein transport pathways in chloroplasts? J. Biol. Chem. 276:42761-42766. http://dx.doi.org/10.1074/jbc.M106690200
23. Nagamori, S., I.N. Smirnova, and H.R. Kaback. 2004. Role of YidC in folding of polytopic membrane proteins. J. Cell Biol. 165:53-62. http://dx.doi.org/10.1083/jcb.200402067
24. Nakamura, M., K. Saeki, and Y. Takahashi. 1999. Hyperproduction of recombinant ferredoxins in escherichia coli by coexpression of the ORF1-ORF2-iscS-iscU-iscA-hscB-hs cA-fdx-ORF3 gene cluster. J. Biochem. 126:10-18. http://dx.doi.org/10.1093/oxfordjournals.jbchem.a022409
25. Niebisch, A., and M. Bott. 2001. Molecular analysis of the cytochrome bc1-aa3 branch of the Corynebacterium glutamicum respiratory chain containing an unusual diheme cytochrome c1. Arch. Microbiol. 175:282-294. http://dx.doi.org/10.1007/s002030100262
26. Niebisch, A., and M. Bott. 2003. Purification of a cytochrome bc-aa3 supercomplex with quinol oxidase activity from Corynebacterium glutamicum. Identification of a fourth subunity of cytochrome aa3 oxidase and mutational analysis of diheme cytochrome c1. J. Biol. Chem. 278:4339-4346. http://dx.doi.org/10.1074/jbc.M210499200
27. Palmer, T., and B.C. Berks. 2012. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 10:483-496.
28. Saller, M.J., F. Fusetti, and A.J.M. Driessen. 2009. Bacillus subtilis SpoIIIJ and YqjG function in membrane protein biogenesis. J. Bacteriol. 191: 6749-6757. http://dx.doi.org/10.1128/JB.00853-09
29. Sargent, F. 2007. Constructing the wonders of the bacterial world: biosynthesis of complex enzymes. Microbiology. 153:633-651. http://dx.doi.org/10.1099/mic.0.2006/004762-0
30. Sargent, F., U. Gohlke, E. De Leeuw, N.R. Stanley, T. Palmer, H.R. Saibil, and B.C. Berks. 2001. Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure. Eur. J. Biochem. 268:3361-3367. http://dx.doi.org/10.1046/j.1432-1327.2001.02263.x
31. Scotti, P.A., M.L. Urbanus, J. Brunner, J.W. de Gier, G. von Heijne, C. van der Does, A.J.M. Driessen, B. Oudega, and J. Luirink. 2000. YidC, the Escherichia coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase. EMBO J. 19:542-549. http://dx.doi.org/10.1093/emboj/19.4.542
32. Serek, J., G. Bauer-Manz, G. Struhalla, L. van den Berg, D. Kiefer, R. Dalbey, and A. Kuhn. 2004. Escherichia coli YidC is a membrane insertase for Sec-independent proteins. EMBO J. 23:294-301. http://dx.doi.org/10.1038/sj.emboj.7600063
33. Shuman, H.A. 1982. Active transport of maltose in Escherichia coli K12. Role of the periplasmic maltose-binding protein and evidence for a substrate recognition site in the cytoplasmic membrane. J. Biol. Chem. 257:5455-5461.
34. Stanley, N.R., T. Palmer, and B.C. Berks. 2000. The twin arginine consensus motif of Tat signal peptides is involved in Sec-independent protein targeting in Escherichia coli. J. Biol. Chem. 275:11591-11596. http://dx.doi.org/10.1074/jbc.275.16.11591
35. Summer, E.J., H. Mori, A.M. Settles, and K. Cline. 2000. The thylakoid delta pH-dependent pathway machinery facilitates RR-independent N-tail protein integration. J. Biol. Chem. 275:23483-23490. http://dx.doi.org/10.1074/jbc.M004137200
36. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:4350-4354. http://dx.doi.org/10.1073/pnas.76.9.4350
37. Van den Berg, B., W.M. Clemons Jr., I. Collinson, Y. Modis, E. Hartmann, S.C. Harrison, and T.A. Rapoport. 2004. X-ray structure of a protein-conducting channel. Nature. 427:36-44. http://dx.doi.org/10.1038/nature02218
38. van der Does, C., E.H. Manting, A. Kaufmann, M. Lutz, and A.J.M. Driessen. 1998. Interaction between SecA and SecYEG in micellar solution and formation of the membrane-inserted state. Biochemistry. 37:201-210. http://dx.doi.org/10.1021/bi972105t
39. van der Laan, M., P. Bechtluft, S. Kol, N. Nouwen, and A.J.M. Driessen. 2004a. F1F0 ATP synthase subunit c is a substrate of the novel YidC pathway for membrane protein biogenesis. J. Cell Biol. 165:213-222. http://dx.doi.org/10.1083/jcb.200402100
40. van der Laan, M., N. Nouwen, and A.J. Driessen. 2004b. SecYEG proteoliposomes catalyze the Deltaphi-dependent membrane insertion of FtsQ. J. Biol. Chem. 279:1659-1664. http://dx.doi.org/10.1074/jbc.M306527200
41. Wagener, N., M. Ackermann, S. Funes, and W. Neupert. 2011. A pathway of protein translocation in mitochondria mediated by the AAA-ATPase Bcs1. Mol. Cell. 44:191-202. http://dx.doi.org/10.1016/j.molcel.2011.07.036
42. Weiss, J.B., C.H. MacGregor, D.N. Collier, J.D. Fikes, P.H. Ray, and P.J. Bassford Jr. 1989. Factors influencing the in vitro translocation of the Escherichia coli maltose-binding protein. J. Biol. Chem. 264:3021-3027.
43. Welte, T., R. Kudva, P. Kuhn, L. Sturm, D. Braig, M. Müller, B. Warscheid, F. Drepper, and H.G. Koch. 2012. Promiscuous targeting of polytopic membrane proteins to SecYEG or YidC by the Escherichia coli signal recognition particle. Mol. Biol. Cell. 23:464-479. http://dx.doi.org/10.1091/mbc.E11-07-0590
44. Widdick, D.A., K. Dilks, G. Chandra, A. Bottrill, M. Naldrett, M. Pohlschröder, and T. Palmer. 2006. The twin-arginine translocation pathway is a major route of protein export in Streptomyces coelicolor. Proc. Natl. Acad. Sci. USA. 103:17927-17932. http://dx.doi.org/10.1073/pnas.0607025103
45. Yahr, T.L., and W.T. Wickner. 2001. Functional reconstitution of bacterial Tat translocation in vitro. EMBO J. 20:2472-2479. http://dx.doi.org/10.1093/emboj/20.10.2472