Crystal Structure of the Translocation ATPase SecA from Thermus thermophilus Reveals a Parallel, Head-to-Head Dimer

Journal of Molecular Biology

Volumn 364, Issue 3, 2006, Pages 248-258

  Vassylyev, Dmitry G ^a,b   Mori, Hiroyuki ^c   Vassylyeva, Marina N ^a,b   Tsukazaki, Tomoya ^c   Kimura, Yoshiaki ^d   Tahirov, Tahir H ^e   Ito, Koreaki ^c  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b RIKEN HARIMA INSTITUTE   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d BIOMOL ENG RESEARCH INSTITUTE   (Japan)

^e NEBRASKA MEDICAL CENTER   (United States)

Author keywords

crystal structure; parallel dimer; pre protein; SecA ATPase; translocation

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMINO ACID; ARGININE; BACTERIAL PROTEIN; DIMER; LYSINE; MONOMER; PROTEIN SECA; SODIUM CHLORIDE;

ACIDITY; ARTICLE; BACTERIUM; CRYSTAL STRUCTURE; DIMERIZATION; GENETIC CONSERVATION; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN STRUCTURE; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS; THERMUS THERMOPHILUS;

BACTERIA (MICROORGANISMS); THERMUS THERMOPHILUS;

EID: 33750846046     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.09.061     Document Type: Article

References (35)

1. Veenendaal A.K., van der Does C., and Driessen A.J. The protein-conducting channel SecYEG. Biochim. Biophys. Acta 1694 (2004) 81-95
2. Mori H., and Ito K. The Sec protein-translocation pathway. Trends Microbiol. 9 (2001) 494-500
3. Vrontou E., and Economou A. Structure and function of SecA, the preprotein translocase nanomotor. Biochim. Biophys. Acta 1694 (2004) 67-80
4. Economou A., and Wickner W. SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78 (1994) 835-843
5. Xu Z., Knafels J.D., and Yoshino K. Crystal structure of the bacterial protein export chaperone secB. Nature Struct. Biol. 7 (2000) 1172-1177
6. Manting E.H., van Der Does C., Remigy H., Engel A., and Driessen A.J. SecYEG assembles into a tetramer to form the active protein translocation channel. EMBO J. 19 (2000) 852-861
7. Mori H., Tsukazaki T., Masui R., Kuramitsu S., Yokoyama S., Johnson A.E., et al. Fluorescence resonance energy transfer analysis of protein translocase. SecYE from Thermus thermophilus HB8 forms a constitutive oligomer in membranes. J. Biol. Chem. 278 (2003) 14257-14264
8. Cannon K.S., Or E., Clemons Jr. W.M., Shibata Y., and Rapoport T.A. Disulfide bridge formation between SecY and a translocating polypeptide localizes the translocation pore to the center of SecY. J. Cell Biol. 169 (2005) 219-225
9. Duong F. Binding, activation and dissociation of the dimeric SecA ATPase at the dimeric SecYEG translocase. EMBO J. 22 (2003) 4375-4384
10. Driessen A.J. SecA, the peripheral subunit of the Escherichia coli precursor protein translocase, is functional as a dimer. Biochemistry 32 (1993) 13190-13197
11. Or E., Navon A., and Rapoport T. Dissociation of the dimeric SecA ATPase during protein translocation across the bacterial membrane. EMBO J. 21 (2002) 4470-4479
12. Or E., Boyd D., Gon S., Beckwith J., and Rapoport T. The bacterial ATPase SecA functions as a monomer in protein translocation. J. Biol. Chem. 280 (2005) 9097-9105
13. Jilaveanu L.B., Zito C.R., and Oliver D. Dimeric SecA is essential for protein translocation. Proc. Natl Acad. Sci. USA 102 (2005) 7511-7516
14. de Keyzer J., van der Sluis E.O., Spelbrink R.E., Nijstad N., de Kruijff B., Nouwen N., et al. Covalently dimerized SecA is functional in protein translocation. J. Biol. Chem. 280 (2005) 35255-35260
15. Jilaveanu L.B., and Oliver D. SecA dimer cross-linked at its subunit interface is functional for protein translocation. J. Bacteriol. 188 (2006) 335-338
16. Hunt J.F., Weinkauf S., Henry L., Fak J.J., McNicholas P., Oliver D.B., and Deisenhofer J. Nucleotide control of interdomain interactions in the conformational reaction cycle of SecA. Science 297 (2002) 2018-2026
17. Sharma V., Arockiasamy A., Ronning D.R., Savva C.G., Holzenburg A., Braunstein M., et al. Crystal structure of Mycobacterium tuberculosis SecA, a preprotein translocating ATPase. Proc. Natl Acad. Sci. USA 100 (2003) 2243-2248
18. Osborne A.R., Clemons Jr. W.M., and Rapoport T.A. A large conformational change of the translocation ATPase SecA. Proc. Natl Acad. Sci. USA 101 (2004) 10937-10942
19. Woodbury R.L., Hardy S.J., and Randall L.L. Complex behavior in solution of homodimeric SecA. Protein Sci. 11 (2002) 875-882
20. Benach J., Chou Y.T., Fak J.J., Itkin A., Nicolae D.D., Smith P.C., et al. Phospholipid-induced monomerization and signal-peptide-induced oligomerization of SecA. J. Biol. Chem. 278 (2003) 3628-3638
21. Vassylyev D.G., Sekine S., Laptenko O., Lee J., Vassylyeva M.N., Borukhov S., and Yokoyama S. Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution. Nature 417 (2002) 712-719
22. Zhou J., and Xu Z. Structural determinants of SecB recognition by SecA in bacterial protein translocation. Nature Struct. Biol. 10 (2003) 942-947
23. Zimmer J., Li W., and Rapoport T.A. A novel dimer interface and conformational changes revealed by an X-ray structure of B. subtilis SecA. J. Mol. Biol. 364 (2006) 259-265
24. Mori, H., Ito, K., & Vassylyev, D. G., (2006). Parallel dimer is a major form of SecA in solution. J. Biol. Chem. In the press.
25. Ding H., Hunt J.F., Mukerji I., and Oliver D. Bacillus subtilis SecA ATPase exists as an antiparallel dimer in solution. Biochemistry 42 (2003) 8729-8738
26. Mori H., and Ito K. Biochemical characterization of a mutationally altered protein translocase: proton motive force stimulation of the initiation phase of translocation. J. Bacteriol. 185 (2003) 405-412
27. Park S.K., Kim D.W., Choe J., and Kim H. RNA helicase activity of Escherichia coli SecA protein. Biochem. Biophys. Res. Commun. 235 (1997) 593-597
28. Vassylyeva M.N., Mori H., Tsukazaki T., Yokoyama S., Tahirov T.H., Ito K., and Vassylyev D.G. Cloning, expression, purification, crystallization and initial crystallographic analysis of the preprotein translocation ATPase SecA from Thermus thermophilus. Acta Crystallog. sect. F 62 (2006) 909-912
29. Otwinowski Z., and Minor W. Processing X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
30. Navaza J. Implementation of molecular replacement in AMoRe. Acta Crystallog. sect. D 57 (2001) 1367-1372
31. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard G.J. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A 47 (1991) 110-119
32. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921
33. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24 (1991) 946-950
34. Esnouf R.M. Further additions to MolScript version 1.4, including reading and contouring of electron-density maps. Acta Crystallog. sect. D 55 (1999) 938-940
35. Merrit E.A., and Bacon D.J. Raster3D: photorealistic molecular graphics. Methods Enzymol. 277 (1997) 505-524