Defining the Escherichia coli SecA dimer interface residues through in vivo site-specific photo-cross-linking

Journal of Bacteriology

Volumn 195, Issue 12, 2013, Pages 2817-2825

  Yu, Dongmei ^a   Wowor, Andy J ^a,b   Cole, James L ^a   Kendall, Debra A ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b Department of Psychology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SECA;

AMINO ACID SUBSTITUTION; ARTICLE; CYTOSOL; DIMERIZATION; ESCHERICHIA COLI; IN VIVO STUDY; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DOMAIN; ULTRACENTRIFUGATION;

ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; ESCHERICHIA COLI; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MUTANT PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; ULTRACENTRIFUGATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84880012758     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02269-12     Document Type: Article

References (48)

1. Papanikou E, Karamanou S, Economou A. 2007. Bacterial protein secretion through the translocase nanomachine. Nat. Rev. Microbiol. 5:839-851.
2. Fekkes P, de Wit JG, van der Wolk JP, Kimsey HH, Kumamoto CA, Driessen AJ. 1998. Preprotein transfer to the Escherichia coli translocase requires the co-operative binding of SecB and the signal sequence to SecA. Mol. Microbiol. 29:1179-1190.
3. Economou A, Wickner W. 1994. SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78:835-843.
4. Papanikolau Y, Papadovasilaki M, Ravelli RBG, McCarthy AA, Cusack S, Economou A, Petratos K. 2007. Structure of dimeric SecA, the Escherichia coli preprotein translocase motor. J. Mol. Biol. 366:1545-1557.
5. Cabelli RJ, Dolan KM, Qian LP, Oliver DB. 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.
6. Lill R, Dowhan W, 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.
7. Douville K, Price A, Eichler J, Economou A, Wickner W. 1995. SecYEG and SecA are the stoichiometric components of preprotein translocase. J. Biol. Chem. 270:20106-20111.
8. Akita M, Shinkai A, Matsuyama S, Mizushima S. 1991. SecA, an essential component of the secretory machinery of Escherichia coli, exists as homodimer. Biochem. Biophys. Res. Commun. 174:211-216.
9. Woodbury RL, Hardy SJS, Randall LL. 2002. Complex behavior in solution of homodimeric SecA. Protein Sci. 11:875-882.
10. Wowor AJ, Yu DM, Kendall DA, Cole JL. 2011. Energetics of SecA dimerization. J. Mol. Biol. 408:87-98.
11. Bu ZM, Wang LO, Kendall DA. 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.
12. Shin JY, Kim M, Ahn T. 2006. Effects of signal peptide and adenylate on the oligomerization and membrane binding of soluble SecA. J. Biochem. Mol. Biol. 39:319-328.
13. Or E, Navon A, Rapoport T. 2002. Dissociation of the dimeric SecA ATPase during protein translocation across the bacterial membrane. EMBO J. 21:4470-4479.
14. Benach J, Chou YT, Fak JJ, Itkin A, Nicolae DD, Smith PC, Wittrock G, Floyd DL, Golsaz CM, Gierasch LM, Hunt JF. 2003. Phospholipidinduced monomerization and signal-peptide-induced oligomerization of SecA. J. Biol. Chem. 278:3628-3638.
15. Musial-Siwek M, Rusch SL, Kendall DA. 2005. Probing the affinity of SecA for signal peptide in different environments. Biochemistry 44: 13987-13996.
16. Fekkes P, vander Does C, Driessen AJM. 1997. The molecular chaperone SecB is released from the carboxy-terminus of SecA during initiation of precursor protein translocation. EMBO J. 16:6105-6113.
17. Or E, Boyd D, Gon P, Beckwith J, Rapoport T. 2005. The bacterial ATPase SecA functions as a monomer in protein translocation. J. Biol. Chem. 280:9097-9105.
18. de Keyzer J, van der Sluis EO, Spelbrink REJ, Nijstad N, de Kruijff B, Nouwen N, van der Does C, Driessen AJM. 2005. Covalently dimerized SecA is functional in protein translocation. J. Biol. Chem. 280:35255-35260.
19. Jilaveanu LB, Oliver D. 2006. SecA dimer cross-linked at its subunit interface is functional for protein translocation. J. Bacteriol. 188:335-338.
20. Duong F. 2003. Binding, activation and dissociation of the dimeric SecA ATPase at the dimeric SecYEG translocase. EMBO J. 22:4375-4384.
21. Kusters I, van den Bogaart G, Kedrov A, Krasnikov V, Fulyani F, Poolman B, Driessen AJM. 2011. Quaternary structure of SecA in solution and bound to SecYEG probed at the single molecule level. Structure 19:430-439.
22. Zimmer J, Nam YS, Rapoport TA. 2008. Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature 455:936-943.
23. Hunt JF, Weinkauf S, Henry L, Fak JJ, McNicholas P, Oliver DB, Deisenhofer J. 2002. Nucleotide control of interdomain interactions in the conformational reaction cycle of SecA. Science 297:2018-2026.
24. Sharma V, Arockiasamy A, Ronning DR, Savva CG, Holzenburg A, Braunstein M, Jacobs WR, Sacchettini JC. 2003. Crystal structure of Mycobacterium tuberculosis SecA, a preprotein translocating ATPase. Proc. Natl. Acad. Sci. U. S. A. 100:2243-2248.
25. Zimmer J, Li WK, Rapoport TA. 2006. A novel dimer interface and conformational changes revealed by an X-ray structure of B. subtilis SecA. J. Mol. Biol. 364:259-265.
26. Vassylyev DG, Mori H, Vassylyeva MN, Tsukazaki T, Kimura Y, Tahirov TH, Ito K. 2006. Crystal structure of the translocation ATPase SecA from Thermus thermophilus reveals a parallel, head-to-head dimer. J. Mol. Biol. 364:248-258.
27. Ding H, Hunt JF, Mukerji I, Oliver D. 2003. Bacillus subtilis SecA ATPase exists as an antiparallel dimer in solution. Biochemistry 42:8729-8738.
28. Jilaveanu LB, Zito CR, Oliver D. 2005. Dimeric SecA is essential for protein translocation. Proc. Natl. Acad. Sci. U. S. A. 102:7511-7516.
29. Das S, Stivison E, Folta-Stogniew E, Oliver D. 2008. Reexamination of the role of the amino terminus of SecA in promoting its dimerization and functional state. J. Bacteriol. 190:7302-7307.
30. Chin JW, Schultz PG. 2002. In vivo photocrosslinking with unnatural amino acid mutagenesis. Chembiochem 3:1135-1137.
31. Freinkman E, Chng SS, Kahne D. 2011. The complex that inserts lipopolysaccharide into the bacterial outer membrane forms a two-protein plug-and-barrel. Proc. Natl. Acad. Sci. U. S. A. 108:2486-2491.
32. Stanley AM, Carvalho P, Rapoport T. 2011. Recognition of an ERAD-L substrate analyzed by site-specific in vivo photocrosslinking. FEBS Lett. 585:1281-1286.
33. Mohibullah N, Hahn S. 2008. Site-specific cross-linking of TBP in vivo and in vitro reveals a direct functional interaction with the SAGA subunit Spt3. Genes Dev. 22:2994-3006.
34. Mori H, Ito K. 2006. Different modes of SecY-SecA interactions revealed by site-directed in vivo photo-cross-linking. Proc. Natl. Acad. Sci. U. S. A. 103:16159-16164.
35. Das S, Oliver DB. 2011. Mapping of the SecA-SecY and SecA-SecG interfaces by site-directed in vivo photocross-linking. J. Biol. Chem. 286: 12371-12380.
36. Farrell IS, Toroney R, Hazen JL, Mehl RA, Chin JW. 2005. Photo-crosslinking interacting proteins with a genetically encoded benzophenone. Nat. Methods 2:377-384.
37. Schmidt MO, Brosh RM, Oliver DB. 2001. Escherichia coli SecA helicase activity is not required in vivo for efficient protein translocation or autogenous regulation. J. Biol. Chem. 276:37076-37085.
38. Young TS, Ahmad I, Yin JA, Schultz PG. 2010. An enhanced system for unnatural amino acid mutagenesis in E. coli. J. Mol. Biol. 395:361-374.
39. Laue TM, Shah BD, Ridgeway TM, Pelletier SL. 1992. Computer-aided interpretation of analytical sedimentation data for proteins, p 90-125. In Harding SE, Rowe AJ, Horton JC (ed), Analytical ultracentrifugation in biochemistry and polymer science. Royal Society of Chemistry, Cambridge, United Kingdom.
40. Stafford WF, Sherwood PJ. 2004. Analysis of heterologous interacting systems by sedimentation velocity: curve fitting algorithms for estimation of sedimentation coefficients, equilibrium and kinetic constants. Biophys. Chem. 108:231-243.
41. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. 2006. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1:2856-2860.
42. Porollo A, Meller J. 2007. Prediction-based fingerprints of proteinprotein interactions. Proteins 66:630-645.
43. Gold VAM, Robson A, Clarke AR, Collinson I. 2007. Allosteric regulation of SecA-magnesium-mediated control of conformation and activity. J. Biol. Chem. 282:17424-17432.
44. Wang HY, Na B, Yang H, Tai PC. 2008. Additional in vitro and in vivo evidence for SecA functioning as dimers in the membrane: dissociation into monomers is not essential for protein translocation in Escherichia coli. J. Bacteriol. 190:1413-1418.
45. Caldas TD, El Yaagoubi A, Richarme G. 1998. Chaperone properties of bacterial elongation factor EF-Tu. J. Biol. Chem. 273:11478-11482.
46. Chen Y, Pan X, Tang Y, Quan S, Tai PC, Sui SF. 2008. Full-length Escherichia coli SecA dimerizes in a closed conformation in solution as determined by cryo-electron microscopy. J. Biol. Chem. 283:28783-28787.
47. Gelis I, Bonvin AM, Keramisanou D, Koukaki M, Gouridis G, Karamanou S, Economou A, Kalodimos CG. 2007. Structural basis for signalsequence recognition by the translocase motor SecA as determined by NMR. Cell 131:756-769.
48. Erlandson KJ, Miller SBM, Nam Y, Osborne AR, Zimmer J, Rapoport TA. 2008. A role for the two-helix finger of the SecA ATPase in protein translocation. Nature 455:984-987.