Involvement of SecDF and YidC in the membrane insertion of M13 procoat mutants

Biochemistry

Volumn 44, Issue 31, 2005, Pages 10741-10749

  Chen, Minyong ^a   Xie, Kun ^a   Yuan, Jijun ^a   Yi, Liang ^a   Facey, Sandra J ^b   Pradel, Nathalie ^c   Wu, Long Fei ^c   Kuhn, Andreas ^b   Dalbey, Ross E ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF HOHENHEIM   (Germany)

^c AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHARACTERIZATION; MAPS; MEMBRANES; SENSITIVITY ANALYSIS;

MEMBRANE INSERTION; MUTANTS; TRANSLOCON;

PROTEINS;

BACTERIOPHAGE M13 PROCOAT PROTEIN; COAT PROTEIN; MUTANT PROTEIN; PROTEINASE; SECDF PROTEIN; SECYEG PROTEIN; UNCLASSIFIED DRUG; YIDC PROTEIN;

ARTICLE; BACTERIOPHAGE M13; COLD SENSITIVE MUTANT; COLD SENSITIVITY; CYTOPLASM; GENE TRANSLOCATION; IN VIVO STUDY; MEMBRANE; MUTANT; NONHUMAN; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; BACTERIOPHAGE M13; CAPSID PROTEINS; CELL MEMBRANE; COLD; ESCHERICHIA COLI PROTEINS; HYDROPHOBICITY; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PERIPLASM; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

EID: 23244463743     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047418k     Document Type: Article

References (42)

1. Samuelson, J. C., Chen, M., Jiang, F., Moller, I., Wiedmann, M., Kuhn, A., Phillips, G. J., and Dalbey, R. E. (2000) YidC mediates membrane protein insertion in bacteria, Nature 406, 637-641.
2. Samuelson, J. C., Jiang, F., Yi, L., Chen, M., de Gier, J. W., Kuhn, A., and Dalbey, R. E. (2001) Function of YidC for the insertion of M13 procoat protein in E. coli: Translocation of mutants that show differences in their membrane potential dependence and Sec requirement, J. Biol. Chem. 276, 34847-34852.
3. Chen, M., Xie, K., Jiang, F., Yi, L., and Dalbey, R. E. (2002) YidC, a newly defined evolutionarily conserved protein, mediates membrane protein assembly in bacteria, Biol. Chem. 383, 1565-1572.
4. Chen, M., Samuelson, J. C., Jiang, F., Muller, M., Kuhn, A., and Dalbey, R. E. (2002) Direct interaction of YidC with the Sec-independent Pf3 coat protein during its membrane protein insertion, J. Biol. Chem. 277, 7670-7675.
5. van Der Laan, M., Urbanus, M. L., Ten Hagen-Jongman, C. M., Nouwen, N., Oudega, B., Harms, N., Driessen, A. J., and Luirink, J. (2003) A conserved function of YidC in the biogenesis of respiratory chain complexes, Proc. Natl. Acad. Sci. U.S.A. 100, 5801-5806.
6. Yi, L., Celebi, N., Chen, M., and Dalbey, R. E. (2004) Sec/SRP requirements and energetics of membrane insertion of subunits a, b, and c of the Escherichia coli F1F0 ATP synthase, J. Biol. Chem. 279, 39260-39267.
7. 0ATP synthase and SecE of the SecYEG translocase, Biochemistry 42, 10537-10544.
8. Froderberg, L., Houben, E., Samuelson, J. C., Chen, M., Park, S. K., Phillips, G. J., Dalbey, R., Luirink, J., and De Gier, J. W. (2003) Versatility of inner membrane protein biogenesis in Escherichia coli, Mol. Microbiol. 47, 1015-1027.
9. Serek, J., Bauer-Manz, G., Struhalla, G., Van Den Berg, L., Kiefer, D., Dalbey, R., and Kuhn, A. (2004) Escherichia coli YidC is a membrane insertase for Sec-independent proteins, EMBO J. 23, 294-301.
10. Van Der Laan, M., Bechtluft, P., Kol, S., Nouwen, N., and Driessen, A. J. (2004) F1F0 ATP synthase subunit c is a substrate of the novel YidC pathway for membrane protein biogenesis, J. Cell Biol. 165, 213-222.
11. Stuart, R. A., and Neupert, W. (2000) Making membranes in bacteria [news], Nature 406, 575, 577.
12. Stuart, R. (2002) Insertion of proteins into the inner membrane of mitochondria: The role of the Oxal complex, Biochim. Biophys. Acta 1592, 79-87.
13. Luirink, J., Samuelsson, T., and de Gier, J. W. (2001) YidC/Oxa1p/AIbS: Evolutionarily conserved mediators of membrane protein assembly, FEBS Lett. 501, 1-5.
14. Kuhn, A., Stuart, R., Henry, R., and Dalbey, R. E. (2003) The Alb3/Oxa1/YidC protein family: Membrane-localized chaperones facilitating membrane protein insertion? Trends Cell Biol. 13, 510-516.
15. Urbanus, M. L., Scotti, P. A., Froderberg, L., Saaf, A., de Gier, J. W., Brunner, J., Samuelson, J. C., Dalbey, R. E., Oudega, B., and Luirink, J. (2001) Sec-dependent membrane protein insertion: Sequential interaction of nascent FtsQ with SecY and YidC, EMBO Rep. 2, 524-529.
16. van der Laan, M., Nouwen, N., and Driessen, A. J. (2004) SecYEG proteoliposomes catalyze the Δψ-dependent membrane insertion of FtsQ, J. Biol. Chem. 279, 1659-1664.
17. Wolfe, P. B., Rice, M., and Wickner, W. (1985) Effects of two sec genes on protein assembly into the plasma membrane of Escherichia coli, J. Biol. Chem. 260, 1836-1841.
18. Houben, E. N., Scotti, P. A., Valent, Q. A., Brunner, J., de Gier, J. L., Oudega, B., and Luirink, J. (2000) Nascent Lep inserts into the Escherichia coli inner membrane in the vicinity of YidC, SecY and SecA, FEBS Lett. 476, 229-233.
19. Koch, H. G., Hengelage, T., Neumann-Haefelin, C., MacFarlane, J., Hoffschulte, H. K., Schimz, K. L., Mechler, B., and Muller, M. (1999) 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.
20. Koch, H. G., Moser, M., Schimz, K. L., and Muller, M. (2002) The integration of YidC into the cytoplasmic membrane of Escherichia coli requires the signal recognition particle, SecA and SecYEG, J. Biol. Chem. 277, 5715-5718.
21. Urbanus, M. L., Froderberg, L., Drew, D., Bjork, P., de Gier, J. W., Brunner, J., Oudega, B., and Luirink, J. (2002) Targeting, insertion, and localization of Escherichia coli YidC, J. Biol. Chem. 277, 12718-12723.
22. Traxler, B., and Murphy, C. (1996) Insertion of the polytopic membrane protein MalF is dependent on the bacterial secretion machinery, J. Biol. Chem. 271, 12394-12400.
23. Newitt, J. A., and Bernstein, H. D. (1998) A mutation in the Escherichia coli secY gene that produces distinct effects on inner membrane protein insertion and protein export, J. Biol. Chem. 273, 12451-12456.
24. Ito, K., and Akiyama, Y. (1991) In vivo analysis of integration of membrane proteins in Escherichia coli, Mol. Microbiol. 5, 2243-2253.
25. Akimaru, J., Matsuyama, S., Tokuda, H., and Mizushima, S. (1991) Reconstitution of a protein translocation system containing purified SecY, SecE, and SecA from Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 88, 6545-6549.
26. Brundage, L., Hendrick, J. P., Schiebel, E., Driessen, A. J., and Wickner, W. (1990) The purified E. coli integral membrane protein SecY/E is sufficient for reconstitution of SecA-dependent precursor protein translocation, Cell 62, 649-657.
27. Van den Berg, B., Clemons, W. M., Jr., Collinson, I., Modis, Y., Hartmann, E., Harrison, S. C., and Rapoport, T. A. (2004) X-ray structure of a protein-conducting channel, Nature 427, 36-44.
28. Pogliano, J. A., and Beckwith, J. (1994) SecD and SecF facilitate protein export in Escherichia coli, EMBO J. 13, 554-561.
29. Duong, F., and Wickner, W. (1997) The SecDFyajC domain of preprotein translocase controls preprotein movement by regulating SecA membrane cycling, EMBO J. 16, 4871-4879.
30. Scotti, P. A., Urbanus, M. L., Brunner, J., de Gier, J. W., von Heijne, G., van der Does, C., Driessen, A. J., Oudega, B., and Luirink, J. (2000) YidC, the Escherichia coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase, EMBO J. 19, 542-549.
31. Nouwen, N., and Driessen, A. J. (2002) SecDFyajC forms a heterotetrameric complex with YidC, Mol. Microbiol. 44, 1397-1405.
32. Chen, M., Xie, K., Nouwen, N., Driessen, A. J., and Dalbey, R. E. (2003) Conditional Lethal Mutations Separate the M13 Procoat and Pf3 Coat Functions of YidC: Different YidC structural requirements for membrane protein insertion, J. Biol. Chem. 278, 23295-23300.
33. Nagamori, S., Smirnova, I. N., and Kaback, H. R. (2004) Role of YidC in folding of polytopic membrane proteins, J. Cell Biol. 165, 53-62.
34. Cao, G., Kuhn, A., and Dalbey, R. E. (1995) The translocation of negatively charged residues across the membrane is driven by the electrochemical potential: Evidence for an electrophoresis-like membrane transfer mechanism, EMBO J. 14, 866-875.
35. Economou, A., Pogliano, J. A., Beckwith, J., Oliver, D. B., and Wickner, W. (1995) SecA membrane cycling at SecYEG is driven by distinct ATP binding and hydrolysis events and is regulated by SecD and SecF, Cell 83, 1171-1181.
36. Kuhn, A. (1988) Alterations in the extracellular domain of M13 procoat protein make its membrane insertion dependent on secA and secY, Eur. J. Biochem. 177, 267-271.
37. Kuhn, A., Zhu, H. Y., and Dalbey, R. E. (1990) Efficient translocation of positively charged residues of M13 procoat protein across the membrane excludes electrophoresis as the primary force for membrane insertion, EMBO J. 9, 2385-2388, 2429, 3413 (published erratum).
38. Schuenemann, T. A., Delgado-Nixon, V. M., and Dalbey, R. E. (1999) Direct evidence that the proton motive force inhibits membrane translocation of positively charged residues within membrane proteins, J. Biol. Chem. 274, 6855-6864.
39. Hashemzadeh-Bonehi, L., Mehraein-Ghomi, F., Mitsopoulos, C., Jacob, J. P., Hennessey, E. S., and Broome-Smith, J. K. (1998) Importance of using lac rather than ara promoter vectors for modulating the levels of toxic gene products in Escherichia coli, Mol. Microbiol. 30, 676-678.
40. Gerard, F., Pradel, N., Ye, C., Ize, B., Yi, L., Xu, J., Dalbey, R. E., and Wu, L. F. (2004) Putative membrane assembly of EtpM-colicin V chimeras, Biochimie 86, 283-286.
41. Miller, J. H. (1972) Experiments in Molecular Genetics, Cold Spring Harbor Laboratory Press, Plainview, NY.
42. de Gier, J. W., Scotti, P. A., Saaf, A., Valent, Q. A., Kuhn, A., Luirink, J., and von Heijne, G. (1998) Differential use of the signal recognition particle translocase targeting pathway for inner membrane protein assembly in Escherichia coli [see comments]. Proc. Natl. Acad. Sci. U.S.A. 95, 14646-14651.