Demonstration of a specific Escherichia coli SecY - Signal peptide interaction

Biochemistry

Volumn 43, Issue 41, 2004, Pages 13185-13192

  Wang, Ligong ^a,b   Miller, Alexander ^a   Rusch, Sharyn L ^a   Kendall, Debra A ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; ESCHERICHIA COLI; HYDROLYSIS; HYDROPHOBICITY; MICELLES; SIGNAL PROCESSING;

MEMBRANE-EMBEDDED CHANNEL; PROTEIN TRANSLOCATION; PROTEOLYTIC CLEAVAGE; TRANSMEMBRANE DOMAINS;

PROTEINS;

ADENOSINE TRIPHOSPHATASE; CARRIER PROTEIN; MEMBRANE PROTEIN; PROTEIN SECYEG; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ESCHERICHIA COLI; HYDROLYSIS; HYDROPHOBICITY; MICELLE; MOLECULAR BIOLOGY; MOLECULAR INTERACTION; NONHUMAN; PHOTOAFFINITY LABELING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BIOTIN; CROSS-LINKING REAGENTS; ESCHERICHIA COLI PROTEINS; HYDROLYSIS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PHENYLALANINE; PHOTOAFFINITY LABELS; PROTEIN BINDING; PROTEIN PRECURSORS; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; ULTRAVIOLET RAYS;

ESCHERICHIA COLI; NEGIBACTERIA;

EID: 5444259691     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049485k     Document Type: Article

References (59)

1. Alder, N. N., and Theg, S. M. (2003) Energy use by biological protein transport pathways, Trends Biochem. Sci. 28, 442-451.
2. Eichler, J., and Irihimovitch, V. (2003) Move it on over: getting proteins across biological membranes, Bioessays 25, 1154- 1157.
3. Schnell, D. J., and Hebert, D. N. (2003) Protein translocons: multifunctional mediators of protein translocation across membranes, Cell 112, 491-505.
4. Cao, T. B., and Saier, M. H., Jr. (2003) The general protein secretory pathway: phylogenetic analyses leading to evolutionary conclusions, Biochim. Biophys. Acta 1609, 115-125.
5. de Keyzer, J., van der Does, C., and Driessen, A. J. (2003) The bacterial translocase: a dynamic protein channel complex, Cell. Mol. Life Sci. 60, 2034-2052.
6. Cabelli, R. J., Chen, L., Tai, P. C., and Oliver, D. B. (1988) SecA protein is required for secretory protein translocation into E. coli membrane vesicles, Cell 55, 683-692.
7. Cunningham, K., Lill, R., Crooke, E., Rice, M., Moore, K., Wickner, W., and Oliver, D. (1989) SecA protein, a peripheral protein of the Escherichia coli plasma membrane, is essential for the functional binding and translocation of proOmpA, EMBO J. 8, 955-959.
8. 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.
9. Brundage, L., Fimmel, C. J., Mizushima, S., and Wickner, W. (1992) SecY, SecE, and band 1 form the membrane-embedded domain of Escherichia coli preprotein translocase, J. Biol. Chem. 267, 4166-4170.
10. Douville, K., Price, A., Eichler, J., Economou, A., and Wickner, W. (1995) SecYEG and SecA are the stoichiometric components of preprotein translocase, J. Biol. Chem. 270, 20106-20111.
11. Economou, A., and Wickner, W. (1994) SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion, Cell 78, 835-843.
12. 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.
13. Akiyama, Y., and Ito, K. (1987) Topology analysis of the SecY protein, an integral membrane protein involved in protein export in Escherichia coli, EMBO J. 6, 3465-3470.
14. Ito, K. (1990) Structure, function, and biogenesis of SecY, an integral membrane protein involved in protein export, J. Bioenerg. Biomembr. 22, 353-367.
15. Matsuyama, S., Akimaru, J., and Mizushima, S. (1990) SecE-dependent overproduction of SecY in Escherichia coli. Evidence for interaction between two components of the secretory machinery, FEBS Lett. 269, 96-100.
16. Veenendaal, A. K., van der Does, C., and Driessen, A. J. (2001) Mapping the sites of interaction between SecY and SecE by cysteine scanning mutagenesis, J. Biol. Chem. 276, 32559-32566.
17. Nishiyama, K., Suzuki, T., and Tokuda, H. (1996) Inversion of the membrane topology of SecG coupled with SecA-dependent preprotein translocation, Cell 85, 71-81.
18. Simon, S. M., and Blobel, G. (1992) Signal peptides open protein-conducting channels in E. coli, Cell 69, 677-684.
19. Meyer, T. H., Menetret, J. F., Breitling, R., Miller, K. R., Akey, C. W., and Rapoport, T. A. (1999) The bacterial SecY/E translocation complex forms channel-like structures similar to those of the eukaryotic Sec61p complex, J. Mol. Biol. 285, 1789-1800.
20. Yahr, T. L., and Wickner, W. T. (2000) Evaluating the oligomeric state of SecYEG in preprotein translocase, EMBO J. 19, 4393-4401.
21. Bessonneau, P., Besson, V., Collinson, I., and Duong, F. (2002) The SecYEG preprotein translocation channel is a conformationally dynamic and dimeric structure, EMBO J. 21, 995-1003.
22. Manting, E. H., van der Does, C., Remigy, H., Engel, A., and Driessen, A. J. (2000) SecYEG assembles into a tetramer to form the active protein translocation channel, EMBO J. 19, 852-861.
23. Breyton, C., Haase, W., Rapoport, T. A., Kuhlbrandt, W., and Collinson, I. (2002) Three-dimensional structure of the bacterial protein-translocation complex SecYEG, Nature 418, 662-665.
24. 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.
25. van der Sluis, E. O., Nouwen, N., and Driessen, A. J. (2002) SecY-SecY and SecY-SecG contacts revealed by site-specific crosslinking, FEBS Lett. 527, 159-165.
26. Satoh, Y., Matsumoto, G., Mori, H., and Ito, K. (2003) Nearest neighbor analysis of the SecYEG complex. 1. Identification of a SecY-SecG interface, Biochemistry 42, 7434-7441.
27. Baba, T., Taura, T., Shimoike, T., Akiyama, Y., Yoshihisa, T., and Ito, K. (1994) A cytoplasmic domain is important for the formation of a SecY-SecE translocator complex, Proc. Natl. Acad. Sci. U.S.A. 91, 4539-4543.
28. Harris, C. R., and Silhavy, T. J. (1999) Mapping an interface of SecY (PrlA) and SecE (PrlG) by using synthetic phenotypes and in vivo cross-linking, J. Bacteriol. 181, 3438-3444.
29. Satoh, Y., Mori, H., and Ito, K. (2003) Nearest neighbor analysis of the SecYEG complex. 2. Identification of a SecY-SecE cytosolic interface, Biochemistry 42, 7442-7447.
30. Matsumoto, G., Yoshihisa, T., and Ito, K. (1997) SecY and SecA interact to allow SecA insertion and protein translocation across the Escherichia coli plasma membrane, EMBO J. 16, 6384-6393.
31. Taura, T., Yoshihisa, T., and Ito, K. (1997) Protein translocation functions of Escherichia coli SecY: in vitro characterization of cold-sensitive secY mutants, Biochimie 79, 517-521.
32. Shimokawa, N., Mori, H., and Ito, K. (2003) Importance of transmembrane segments in Escherichia coli SecY, Mol. Genet. Genomics 269, 180-187.
33. Joly, J. C., and Wickner, W. (1993) The SecA and SecY subunits of translocase are the nearest neighbors of a translocating preprotein, shielding it from phospholipids, EMBO J. 12, 255-263.
34. Plath, K., Mothes, W., Wilkinson, B. M., Stirling, C. J., and Rapoport, T. A. (1998) Signal sequence recognition in posttranslational protein transport across the yeast ER membrane, Cell 94, 795-807.
35. Emr, S. D., Hanley-Way, S., and Silhavy, T. J. (1981) Suppressor mutations that restore export of a protein with a defective signal sequence, Cell 23, 79-88.
36. Bieker, K. L., and Silhavy, T. J. (1989) PrlA is important for the translocation of exported proteins across the cytoplasmic membrane of Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 86, 968-972.
37. Osborne, R. S., and Silhavy, T. J. (1993) PrlA suppressor mutations cluster in regions corresponding to three distinct topological domains, EMBO J. 12, 3391-3398.
38. Izard, J. W., Doughty, M. B., and Kendall, D. A. (1995) Physical and conformational properties of synthetic idealized signal sequences parallel their biological function, Biochemistry 34, 9904-9912.
39. Miller, A., Wang, L., and Kendall, D. A. (1998) Synthetic signal peptides specifically recognize SecA and stimulate ATPase activity in the absence of preprotein, J. Biol. Chem. 273, 11409-11412.
40. Wang, L., Miller, A., and Kendall, D. A. (2000) Signal peptide determinants of SecA binding and stimulation of ATPase activity, J. Biol. Chem. 275, 10154-10159.
41. Mitchell, C., and Oliver, D. (1993) Two distinct ATP-binding domains are needed to promote protein export by Escherichia coli SecA ATPase, Mol. Microbiol. 10, 483-497.
42. de Vrije, T., Tommassen, J., and De Kruijff, B. (1987) 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.
43. Miller, A., Wang, L., and Kendall, D. A. (2002) SecB modulates the nucleotide-bound state of SecA and stimulates ATPase activity, Biochemistry 41, 5325-5332.
44. van der Does, C., Manting, E. H., Kaufmann, A., Lutz, M., and Driessen, A. J. (1998) Interaction between SecA and SecYEG in micellar solution and formation of the membrane-inserted state, Biochemistry 37, 201-210.
45. van der Does, C., Swaving, J., van Klompenburg, W., and Driessen, A. J. (2000) Nonbilayer lipids stimulate the activity of the reconstituted bacterial protein translocase, J. Biol. Chem. 275, 2472-2478.
46. van Voorst, F., van der Does, C., Brunner, I., Driessen, A. I., and de Kruijff, B. (1998) Translocase-bound SecA is largely shielded from the phospholipid acyl chains, Biochemistry 37, 12261-12268.
47. Lill, R., Dowhan, W., and Wickner, W. (1990) The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins, Cell 60, 271-280.
48. Lanzetta, P. A., Alvarez, L. J., Reinach, P. S., and Candia, O. A. (1979) An improved assay for nanomole amounts of inorganic phosphate, Anal. Biochem. 100, 95-97.
49. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
50. Cleveland, D. W., Fischer, S. G., Kirschner, M. W., and Laemmli, U. K. (1977) Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis, J. Biol. Chem. 252, 1102-1106.
51. Pedersen, S. E., Dreyer, E. B., and Cohen, J. B. (1986) Location of ligand-binding sites on the nicotinic acetylcholine receptor alpha-subunit, J. Biol. Chem. 261, 13735-13743.
52. 125I]iodophenyl)diazirine, Biochemistry 27, 8741-8751.
53. Schägger, H., and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa, Anal. Biochem. 166, 368-379.
54. Fontana, A., and Gross, E. (1986) Fragmentation of polypeptides by chemical methods, in Practical Protein Chemistry, A Handbook (Darbre, A., Ed.) pp 67-120, John Wiley and Sons, New York.
55. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72, 248-254.
56. Markwell, M. A., Haas, S. M., Bieber, L. L., and Tolbert, N. E. (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples, Anal. Biochem. 87, 206-210.
57. de Keyzer, J., van der Does, C., Kloosterman, T. G., and Driessen, A. J. (2003) Direct demonstration of ATP-dependent release of SecA from a translocating preprotein by surface plasmon resonance, J. Biol. Chem. 278, 29581-29586.
58. den Blaauwen, T., van der Wolk, J. P., van der Does, C., van Wely, K. H., and Driessen, A. J. (1999) Thermodynamics of nucleotide binding to NBS-I of the Bacillus subtilis preprotein translocase subunit SecA, FEBS Lett. 458, 145-150.
59. Bu, Z., Wang, L., and Kendall, D. A. (2003) Nucleotide binding induces changes in the oligomeric state and conformation of Sec A in a lipid environment: a small-angle neutron-scattering study, J. Mol. Biol. 332, 23-30.