Conformational state of the SecYEG-bound SecA probed by single tryptophan fluorescence spectroscopy

Biochemistry

Volumn 44, Issue 17, 2005, Pages 6424-6432

  Natale, Paolo ^a   Den Blaauwen, Tanneke ^a,b   Van Der Does, Chris ^a,c   Driessen, Arnold J M ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; ESCHERICHIA COLI; MEMBRANES; PROTEINS; SPECTROSCOPY; SPECTRUM ANALYSIS;

ACRYLAMIDE; MOLECULAR MOTORS; MUTANTS;

FLUORESCENCE;

ADENOSINE TRIPHOSPHATE; PROTEIN PRECURSOR; TRYPTOPHAN;

ARTICLE; ESCHERICHIA COLI; FLUORESCENCE SPECTROSCOPY; HYDROLYSIS; MEMBRANE CHANNEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE;

ACRYLAMIDE; ADENOSINE TRIPHOSPHATASES; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; ESCHERICHIA COLI PROTEINS; GENETIC COMPLEMENTATION TEST; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN TRANSPORT; SOLUBILITY; SPECTROMETRY, FLUORESCENCE; TEMPERATURE; TRYPTOPHAN;

ESCHERICHIA COLI;

EID: 17844377305     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047488r     Document Type: Article

References (57)

1. Hartl, F. U., Lecker, S., Schiebel, E., Hendrick, J. P., and Wickner, W. (1990) The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane, Cell 63, 269-279.
2. 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.
3. Ulbrandt, N. D., London, E., and Oliver, D. B. (1992) Deep penetration of a portion of Escherichia coli SecA protein into model membranes is promoted by anionic phospholipids and by partial unfolding, J. Biol. Chem. 267, 15184-15192.
4. Cabelli, R. J., Dolan, K. M., Qian, L. P., and Oliver, D. B. (1991) Characterization of membrane-associated and soluble states of SecA protein from wild-type and SecA51(TS) mutant strains of Escherichia coli, J. Biol. Chem. 266, 24420-24427.
5. van der Does, C., den Blaauwen, T., de Wit, J. G., Manting, E. H., Groot, N. A., Fekkes, P., and Driessen, A. J. M. (1996) SecA is an intrinsic subunit of the Escherichia coli preprotein translocase and exposes its carboxyl terminus to the periplasm, Mol. Microbiol. 22, 619-629.
6. Manting, E. H., and Driessen, A. J. M. (2000) Escherichia coli translocase: The unravelling of a molecular machine, Mol. Microbiol. 37, 226-238.
7. Driessen, A. J. M., Manting, E. H., and van der Does, C. (2001) The structural basis of protein targeting and translocation in bacteria, Nat. Struct. Biol. 8, 492-498.
8. de Keyzer, J., van der Does, C., and Driessen, A. J. M. (2003) The bacterial translocase: A dynamic protein channel complex, Cell Mol. Life Sci. 60, 2034-2052.
9. Clemons, W. M., Jr., Menetret, J. F., Akey, C. W., and Rapoport, T. (1904) Structural insight into the protein translocation channel, Curr. Opin. Struct. Biol. 14, 390-396.
10. Economou, A., and Wickner, W. (1994) SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion, Cell 78, 835-843.
11. Schiebel, E., Driessen, A. J. M., Hartl, F. U., and Wickner, W. (1991) Delta mu H+ and ATP function at different steps of the catalytic cycle of preprotein translocase, Cell 64, 927-939.
12. van der Wolk, J. P., de Wit, J. G., and Driessen, A. J. M. (1997) The catalytic cycle of the Escherichia coli SecA ATPase comprises two distinct preprotein translocation events, EMBO J. 16, 7297-7304.
13. Hunt, J. F., Weinkauf, S., Henry, L., Fak, J. J., McNicholas, P., Oliver, D. B., and Deisenhofer, J. (2002) Nucleotide control of interdomain interactions in the conformational reaction cycle of SecA, Science 297, 2018-2026.
14. Osborne, A. R., Clemons, W. M., Jr., and Rapoport, T. A. (2004) A large conformational change of the translocation ATPase SecA, Proc. Natl. Acad. Sci. U.S.A. 101, 10937-10942.
15. Sharma, V., Arockiasamy, A., Ronning, D. R., Savva, C. G., Holzenburg, A., Braunstein, M., Jacobs, W. R., Jr., and Sacchettini, J. C. (2003) Crystal structure of Mycobacterium tuberculosis SecA, a preprotein translocating ATPase, Proc. Natl. Acad. Sci. U.S.A. 100, 2243-2248.
16. Kimura, E., Akita, M., Matsuyama, S., and Mizushima, S. (1991) Determination of a region in SecA that interacts with presecretory proteins in Escherichia coli, J. Biol. Chem. 266, 6600-6606.
17. 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.
18. van der Wolk, J. P., Boorsma, A., Knoche, M., Schafer, H. J., and Driessen, A. J. M. (1997) The low-affinity ATP binding site of the Escherichia coli SecA dimer is localized at the subunit interface, Biochemistry 36, 14924-14929.
19. Karamanou, S., Vrontou, E., Sianidis, G., Baud, C., Roos, T., Kuhn, A., Politou, A. S., and Economou, A. (1999) A molecular switch in SecA protein couples ATP hydrolysis to protein translocation, Mol. Microbiol. 34, 1133-1145.
20. Dapic, V., and Oliver, D. (2000) Distinct membrane binding properties of N- and C-terminal domains of Escherichia coli SecA ATPase, J. Biol. Chem. 275, 25000-25007.
21. Sianidis, G., Karamanou, S., Vrontou. E., Boulias, K., Repanas, K., Kyrpides, N., Politou, A. S., and Economou, A. (2001) Cross-talk between catalytic and regulatory elements in a DEAD motor domain is essential for SecA function, EMBO J. 20, 961-970.
22. van der Wolk, J. P., Klose, M., Breukink, E., Demel, R. A., de Kruijff, B., Freudl, R., and Driessen, A. J. M. (1993) Characterization of a Bacillus subtilis SecA mutant protein deficient in translocation ATPase and release from the membrane, Mol. Microbiol. 8, 31-42.
23. Rajapandi, T., and Oliver, D. (1996) Integration of SecA protein into the Escherichia coli inner membrane is regulated by its aminoterminal ATP-binding domain, Mol. Microbiol. 20, 43-51.
24. Breukink, E., Keller, R. C., and de Kruijff, B. (1993) Nucleotide and negatively charged lipid-dependent vesicle aggregation caused by SecA. Evidence that SecA contains two lipid-binding sites, FEBS Lett. 331, 19-24.
25. de Keyzer, J., van der Does, C., Kloosterman, T. G., and Driessen, A. J. M. (2003) Direct demonstration of ATP-dependent release of SecA from a translocating preprotein by surface plasmon resonance, J. Biol. Chem. 278, 29581-29586.
26. Song, M., and Kim, H. (1997) Stability and solvent accessibility of SecA protein of Escherichia coli, J. Biochem. 122, 1010-1018.
27. 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.
28. Vrontou, E., Karamanou, S., Baud, C., Sianidis, G., and Economou, A. (2004) Global coordination of protein translocation by the SecA IRA1 switch, J. Biol. Chem.
29. Fekkes, P., de Wit, J. G., Boorsma, A., Friesen, R. H., and Driessen, A. J. M. (1999) Zinc stabilizes the SecB binding site of SecA, Biochemistry 38, 5111-5116.
30. Ding, H., Hunt, J. F., Mukerji, I., and Oliver, D. (2003) Bacillus subtilis SecA ATPase exists as an antiparallel dimer in solution, Biochemistry 42, 8729-8738.
31. van den Berg, B., Clemons, W. M., 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.
32. 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.
33. Manting, E. H., van der Does, C., Remigy, H., Engel, A., and Driessen, A. J. M. (2000) SecYEG assembles into a tetramer to form the active protein translocation channel, EMBO J. 19, 852-861.
34. Wang, H. W., Chen, Y., Yang, H., Chen, X., Duan, M. X., Tai, P. C., and Sui, S. F. (2003) Ring-like pore structures of SecA: Implication for bacterial protein-conducting channels, Proc. Natl. Acad. Sci. U.S.A. 100, 4221-4226.
35. Yahr, T. L., and Wickner, W. T. (2000) Evaluating the oligomeric state of SecYEG in preprotein translocase, EMBO J. 19, 4393-4401.
36. Duong, F. (2003) Binding, activation, and dissociation of the dimeric SecA ATPase at the dimeric SecYEG translocase, EMBO J. 22, 4375-4384.
37. Tziatzios, C., Schubert, D., Lotz, M., Gundogan, D., Betz, H., Schagger, H., Haase, W., Duong, F., and Collinson, I. (2004) The bacterial protein-translocation complex: SecYEG dimers associate with one or two SecA molecules, J. Mol. Biol. 340, 513-524.
38. Natale, P., Swaving, J., van Der, D. C., de Keyzer, J., and Driessen. A. J. M. (2004) Binding of SecA to the SecYEG complex accelerates the rate of nucleotide exchange on SecA, J. Biol. Chem. 279, 13769-13777.
39. Schmidt, M. G., Rollo, E. E., Grodberg, J., and Oliver, D. B. (1988) Nucleotide sequence of the secA gene and secA(Ts) mutations preventing protein export in Escherichia coli, J. Bacteriol. 170, 3404-3414.
40. Fak, J. J., Itkin, A., Ciobanu, D. D., Lin, E. C., Song, X. J., Chou, Y. T., Gierasch, L. M., and Hunt, J. F. (2004) Nucleotide exchange from the high-affinity ATP-binding site in SecA is the rate-limiting step in the ATPase cycle of the soluble enzyme and occurs through a specialized conformational state, Biochemistry 43, 7307-7327.
41. den Blaauwen, T., Fekkes, P., de Wit, J. G., Kuiper, W., and Driessen, A. J. M. (1996) Domain interactions of the peripheral preprotein translocase subunit SecA, Biochemistry 35, 11994-12004.
42. Kourtz, L., and Oliver, D. (2000) Tyr-326 plays a critical role in controlling SecA-preprotein interaction, Mol. Microbiol. 37, 1342-1356.
43. Ding, H., Mukerji, I., and Oliver, D. (2001) Lipid and signal peptide-induced conformational changes within the C-domain of Escherichia coli SecA protein, Biochemistry 40, 1835-1843.
44. Weaver, A. J. M., McDowall, A. W., Oliver, D. B., and Deisenhofer, J. (1992) Electron microscopy of thin-sectioned three-dimensional crystals of SecA protein from Escherichia coli: Structure in projection at 40 Å resolution, J. Struct. Biol. 109, 87-96.
45. Song, W., Raden, D., Mandon, E. C., and Gilmore, R. (2000) Role of Sec61α in the regulated transfer of the ribosome-nascent chain complex from the signal recognition particle to the translocation channel, Cell 100, 333-343.
46. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Habor Laboratory Press, Cold Spring Habor, New York.
47. Yanisch-Perron, C., Vieira, J., and Messing, J. (1985) Improved M13 phage cloning vectors and host strains: Nucleotide sequences of the M13mp18 and pUC19 vectors, Gene 33, 103-119.
48. Oliver, D. B., and Beckwith, J. (1982) Regulation of a membrane component required for protein secretion in Escherichia coli, Cell 30, 311-319.
49. Klose, M., Schimz, K. L., van der Wolk, J., Driessen, A. J. M., and Freudl, R. (1993) Lysine 106 of the putative catalytic ATP-binding site of the Bacillus subtilis SecA protein is required for functional complementation of Escherichia coli secA mutants in vivo, J. Biol. Chem. 268, 4504-4510.
50. Or, E., Navon, A., and Rapoport, T. (2002) Dissociation of the dimeric SecA ATPase during protein translocation across the bacterial membrane, EMBO J. 21, 4470-4479.
51. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, 2nd ed., Kluwer Academic/Plenum Publishers, New York.
52. de Keyzer, J., van der Does, C., and Driessen, A. J. M. (2002) Kinetic analysis of the translocation of fluorescent precursor proteins into Escherichia coli membrane vesicles, J. Biol. Chem. 277, 46059-46065.
53. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling, Electrophoresis 18, 2714-2723.
54. Burstein, E. A. (1976) Luminescence of protein chromophores. Model Studies, in Advances in Science and Technology (Itogi Nauki i Tekhniki) 6th ed., VINITI, Moscow, Russia.
55. Ramamurthy, V., and Oliver, D. (1997) Topology of the integral membrane form of Escherichia coli SecA protein reveals multiple periplasmically exposed regions and modulation by ATP binding, J. Biol. Chem. 272, 23239-23246.
56. van der Does, C., Manting, E. H., Kaufmann, A., Lutz, M., and Driessen, A. J. M. (1998) Interaction between SecA and SecYEG in micellar solution and formation of the membrane-inserted state, Biochemistry 37, 201-210.
57. Eichler, J., and Wickner, W. (1997) Both an N-terminal 65-kDa domain and a C-terminal 30-kDa domain of SecA cycle into the membrane at SecYEG during translocation, Proc. Natl. Acad. Sci. U.S.A. 94, 5574-5581.