Energetics of SecA dimerization

Journal of Molecular Biology

Volumn 408, Issue 1, 2011, Pages 87-98

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

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

EDTA; ethylenediaminetetraacetic acid

Indexed keywords

BACTERIAL PROTEIN; PROTEIN PRECURSOR; PROTEIN SECA; SIGNAL PEPTIDE; SODIUM CHLORIDE;

ARTICLE; CELL VIABILITY; DIMERIZATION; DISSOCIATION CONSTANT; ESCHERICHIA COLI; LINKAGE ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN TRANSPORT; TEMPERATURE; ULTRACENTRIFUGATION;

ESCHERICHIA COLI;

EID: 79953246902     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.02.006     Document Type: Article

References (82)

1. Sardis M.F., and Economou A. SecA: a tale of two protomers Mol. Microbiol. 76 2010 1070 1081
2. Rusch S.L., and Kendall D.A. Oligomeric states of the SecA and SecYEG core components of the bacterial Sec translocon Biochim. Biophys. Acta 1768 2007 5 12 (Pubitemid 44909078)
3. Driessen A.J., and Nouwen N. Protein translocation across the bacterial cytoplasmic membrane Annu. Rev. Biochem. 77 2008 643 667
4. Papanikou E., Karamanou S., and Economou A. Bacterial protein secretion through the translocase nanomachine Nat. Rev., Microbiol. 5 2007 839 851 (Pubitemid 47578385)
5. Hartl F.U., Lecker S., Schiebel E., Hendrick J.P., and Wickner W. The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane Cell 63 1990 269 279
6. Cabelli R.J., Dolan K.M., Qian L.P., and Oliver D.B. 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 1991 24420 24427 (Pubitemid 21908958)
7. Papanikolau Y., Papadovasilaki M., Ravelli R.B., McCarthy A.A., Cusack S., Economou A., and Petratos K. Structure of dimeric SecA, the Escherichia coli preprotein translocase motor J. Mol. Biol. 366 2007 1545 1557 (Pubitemid 46231228)
8. Cooper D.B., Smith V.F., Crane J.M., Roth H.C., Lilly A.A., and Randall L.L. SecA, the motor of the secretion machine, binds diverse partners on one interactive surface J. Mol. Biol. 382 2008 74 87
9. Randall L.L., Crane J.M., Lilly A.A., Liu G., Mao C., Patel C.N., and Hardy S.J. Asymmetric binding between SecA and SecB two symmetric proteins: implications for function in export J. Mol. Biol. 348 2005 479 489 (Pubitemid 40462110)
10. Osborne A.R., Rapoport T.A., and van den Berg B. Protein translocation by the Sec61/SecY channel Annu. Rev. Cell Dev. Biol. 21 2005 529 550 (Pubitemid 41740645)
11. Hegde R.S., and Bernstein H.D. The surprising complexity of signal sequences Trends Biochem. Sci. 31 2006 563 571 (Pubitemid 44436941)
12. Erlandson K.J., Miller S.B., Nam Y., Osborne A.R., Zimmer J., and Rapoport T.A. A role for the two-helix finger of the SecA ATPase in protein translocation Nature 455 2008 984 987
13. Zimmer J., Nam Y., and Rapoport T.A. Structure of a complex of the ATPase SecA and the protein-translocation channel Nature 455 2008 936 943
14. Gouridis G., Karamanou S., Gelis I., Kalodimos C.G., and Economou A. Signal peptides are allosteric activators of the protein translocase Nature 462 2009 363 367
15. Randall L.L., and Henzl M.T. Direct identification of the site of binding on the chaperone SecB for the amino terminus of the translocon motor SecA Protein Sci. 19 2010 1173 1179
16. Economou A., and Wickner W. SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion Cell 78 1994 835 843 (Pubitemid 24294458)
17. Tomkiewicz D., Nouwen N., van Leeuwen R., Tans S., and Driessen A.J. SecA supports a constant rate of preprotein translocation J. Biol. Chem. 281 2006 15709 15713 (Pubitemid 43848458)
18. van der Wolk J.P., de Wit J.G., and Driessen A.J. The catalytic cycle of the Escherichia coli SecA ATPase comprises two distinct preprotein translocation events EMBO J. 16 1997 7297 7304 (Pubitemid 28010490)
19. Hartl F.U., Lecker S., Schiebel E., Hendrick J.P., and Wickner W. The binding cascade of SecB to SecA to SecY E mediates preprotein targeting to the E. coli plasma membrane Cell 63 1990 269 279
20. Fekkes P., van der Does C., and Driessen A.J. The molecular chaperone SecB is released from the carboxy-terminus of SecA during initiation of precursor protein translocation EMBO J. 16 1997 6105 6113 (Pubitemid 27458330)
21. Kimura E., Akita M., Matsuyama S., and Mizushima S. Determination of a region in SecA that interacts with presecretory proteins in Escherichia coli J. Biol. Chem. 266 1991 6600 6606 (Pubitemid 21906259)
22. Papanikou E., Karamanou S., Baud C., Frank M., Sianidis G., and Keramisanou D. Identification of the preprotein binding domain of SecA J. Biol. Chem. 280 2005 43209 43217 (Pubitemid 43049287)
23. Lill R., Dowhan W., and Wickner W. The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins Cell 60 1990 271 280
24. Hendrick J.P., and Wickner W. SecA protein needs both acidic phospholipids and SecY/E protein for functional high-affinity binding to the Escherichia coli plasma membrane J. Biol. Chem. 266 1991 24596 24600 (Pubitemid 21908982)
25. Snyders S., Ramamurthy V., and Oliver D. Identification of a region of interaction between Escherichia coli SecA and SecY proteins J. Biol. Chem. 272 1997 11302 11306 (Pubitemid 27184131)
26. Ramamurthy V., and Oliver D. 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 1997 23239 23246 (Pubitemid 27392459)
27. Economou A., Pogliano J.A., Beckwith J., Oliver D.B., and Wickner W. SecA membrane cycling at SecYEG is driven by distinct ATP binding and hydrolysis events and is regulated by SecD and SecF Cell 83 1995 1171 1181 (Pubitemid 26007808)
28. 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 (Pubitemid 40409604)
29. 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 (Pubitemid 40741002)
30. Wang H.Y., Na B., Yang H., and Tai P.C. 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 2008 1413 1418 (Pubitemid 351215024)
31. Akita M., Shinkai A., Matsuyama S., and Mizushima S. SecA, an essential component of the secretory machinery of Escherichia coli, exists as homodimer Biochem. Biophys. Res. Commun. 174 1991 211 216
32. 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 (Pubitemid 34984334)
33. Woodbury R.L., Hardy S.J., and Randall L.L. Complex behavior in solution of homodimeric SecA Protein Sci. 11 2002 875 882 (Pubitemid 34241295)
34. 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 (Pubitemid 36899816)
35. Benach J., Chou Y.T., Fak J.J., Itkin A., Nicolae D.D., and Smith P.C. Phospholipid-induced monomerization and signal-peptide-induced oligomerization of SecA J. Biol. Chem. 278 2003 3628 3638 (Pubitemid 36801086)
36. Bu Z., Wang L., and Kendall D.A. Nucleotide binding induces changes in the oligomeric state and conformation of SecA in a lipid environment: a small-angle neutron-scattering study J. Mol. Biol. 332 2003 23 30 (Pubitemid 36999728)
37. Musial-Siwek M., Rusch S.L., and Kendall D.A. Probing the affinity of SecA for signal peptide in different environments Biochemistry 44 2005 13987 13996 (Pubitemid 41507479)
38. Musial-Siwek M., Rusch S.L., and Kendall D.A. Selective photoaffinity labeling identifies the signal peptide binding domain on SecA J. Mol. Biol. 365 2007 637 648 (Pubitemid 44960356)
39. Zimmer J., and Rapoport T.A. Conformational flexibility and peptide interaction of the translocation ATPase SecA J. Mol. Biol. 394 2009 606 612
40. 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
41. Sharma V., Arockiasamy A., Ronning D.R., Savva C.G., Holzenburg A., and Braunstein M. Crystal structure of Mycobacterium tuberculosis SecA, a preprotein translocating ATPase Proc. Natl Acad. Sci. USA 100 2003 2243 2248 (Pubitemid 36297484)
42. 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 (Pubitemid 44715923)
43. Vassylyev D.G., Mori H., Vassylyeva M.N., Tsukazaki T., Kimura Y., Tahirov T.H., and Ito K. Crystal structure of the translocation ATPase SecA from Thermus thermophilus reveals a parallel, head-to-head dimer J. Mol. Biol. 364 2006 248 258 (Pubitemid 44717539)
44. Alami M., Dalal K., Lelj-Garolla B., Sligar S.G., and Duong F. Nanodiscs unravel the interaction between the SecYEG channel and its cytosolic partner SecA EMBO J. 26 2007 1995 2004 (Pubitemid 46625796)
45. Driessen A.J. SecA, the peripheral subunit of the Escherichia coli precursor protein translocase, is functional as a dimer Biochemistry 32 1993 13190 13197 (Pubitemid 24005927)
46. de Keyzer J., van der Sluis E.O., Spelbrink R.E., Nijstad N., de Kruijff B., and Nouwen N. Covalently dimerized SecA is functional in protein translocation J. Biol. Chem. 280 2005 35255 35260 (Pubitemid 41532713)
47. Duong F. Binding, activation and dissociation of the dimeric SecA ATPase at the dimeric SecYEG translocase EMBO J. 22 2003 4375 4384 (Pubitemid 37087192)
48. Cole J.L., Lary J.W., Moody T., and Laue T.M. Analytical ultracentrifugation: sedimentation velocity and sedimentation equilibrium Methods Cell Biol. 84 2008 143 179
49. Laue T.M., and Stafford W.F. Modern applications of analytical ultracentrifugation Annu. Rev. Biophys. Biomol. Struct 28 1999 75 100 (Pubitemid 29319253)
50. Lebowitz J., Lewis M.S., and Schuck P. Modern analytical ultracentrifugation in protein science: a tutorial review Protein Sci. 11 2002 2067 2079 (Pubitemid 34919611)
51. MacGregor I.K., Anderson A.L., and Laue T.M. Fluorescence detection for the XLI analytical ultracentrifuge Biophys. Chem. 108 2004 165 185 (Pubitemid 38388487)
52. Kroe R.R., and Laue T.M. NUTS and BOLTS: applications of fluorescence-detected sedimentation Anal. Biochem. 390 2009 1 13
53. Stafford W.F. Boundary analysis in sedimentation transport experiments: a procedure for obtaining sedimentation coefficient distributions using the time derivative of the concentration profile Anal. Biochem. 203 1992 295 301
54. Doyle S.M., Braswell E.H., and Teschke C.M. SecA folds via a dimeric intermediate Biochemistry 39 2000 11667 11676
55. Gold V.A., Robson A., Clarke A.R., and Collinson I. Allosteric regulation of SecA: magnesium-mediated control of conformation and activity J. Biol. Chem. 282 2007 17424 17432 (Pubitemid 47100301)
56. Lemaire P.A., Lary J., and Cole J.L. Mechanism of PKR activation: dimerization and kinase activation in the absence of double-stranded RNA J. Mol. Biol. 345 2005 81 90 (Pubitemid 39572826)
57. Snyder D., Lary J., Chen Y., Gollnick P., and Cole J.L. Interaction of the trp RNA-binding attenuation protein (TRAP) with anti-TRAP J. Mol. Biol. 338 2004 669 682 (Pubitemid 38507413)
58. Xu Y. Characterization of macromolecular heterogeneity by equilibrium sedimentation techniques Biophys. Chem. 108 2004 141 163 (Pubitemid 38396760)
59. Record M.T. Jr, Ha J.H., and Fisher M.A. Analysis of equilibrium and kinetic measurements to determine thermodynamic origins of stability and specificity and mechanism of formation of site-specific complexes between proteins and helical DNA Methods Enzymol. 208 1991 291 343
60. Karamanou S., Sianidis G., Gouridis G., Pozidis C., Papanikolau Y., Papanikou E., and Economou A. Escherichia coli SecA truncated at its termini is functional and dimeric FEBS Lett. 579 2005 1267 1271 (Pubitemid 40248698)
61. 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
62. Wyman J., and Gill S.J. Binding and Linkage 1990 University Science Books Mill Valley, CA
63. Auclair S.M., Moses J.P., Musial-Siwek M., Kendall D.A., Oliver D.B., and Mukerji I. Mapping of the signal peptide-binding domain of Escherichia coli SecA using Forster resonance energy transfer Biochemistry 49 2010 782 792
64. Das S., Stivison E., Folta-Stogniew E., and Oliver D. Reexamination of the role of the amino terminus of SecA in promoting its dimerization and functional state J. Bacteriol. 190 2008 7302 7307
65. Richey B., Cayley D.S., Mossing M.C., Kolka C., Anderson C.F., Farrar T.C., and Record M.T. Jr Variability of the intracellular ionic environment of Escherichia coli. Differences between in vitro and in vivo effects of ion concentrations on protein-DNA interactions and gene expression J. Biol. Chem. 262 1987 7157 7164
66. Record M.T. Jr, Courtenay E.S., Cayley D.S., and Guttman H.J. Responses of E. coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water Trends Biochem. Sci. 23 1998 143 148 (Pubitemid 28189526)
67. Zhao H., Streaker E., Pan W., and Beckett D. Protein-protein interactions dominate the assembly thermodynamics of a transcription repression complex Biochemistry 46 2007 13667 13676 (Pubitemid 350209962)
68. Gelis I., Bonvin A.M., Keramisanou D., Koukaki M., Gouridis G., and Karamanou S. Structural basis for signal-sequence recognition by the translocase motor SecA as determined by NMR Cell 131 2007 756 769 (Pubitemid 350087200)
69. Chen Y., Pan X., Tang Y., Quan S., Tai P.C., and Sui S.F. Full-length Escherichia coli SecA dimerizes in a closed conformation in solution as determined by cryo-electron microscopy J. Biol. Chem. 283 2008 28783 28787
70. Prabhu N.V., and Sharp K.A. Heat capacity in proteins Annu. Rev. Phys. Chem. 56 2005 521 548 (Pubitemid 41156887)
71. Osborne A.R., Clemons W.M. Jr., and Rapoport T.A. A large conformational change of the translocation ATPase SecA Proc. Natl Acad. Sci. USA 101 2004 10937 10942 (Pubitemid 38989563)
72. Bailey M.F., Angley L.M., and Perugini M.A. Methods for sample labeling and meniscus determination in the fluorescence-detected analytical ultracentrifuge Anal. Biochem. 390 2009 218 220
73. Kingsbury J.S., Laue T.M., Klimtchuk E.S., Theberge R., Costello C.E., and Connors L.H. The modulation of transthyretin tetramer stability by cysteine 10 adducts and the drug diflunisal. Direct analysis by fluorescence-detected analytical ultracentrifugation J. Biol. Chem. 283 2008 11887 11896
74. Sianidis G., Karamanou S., Vrontou E., Boulias K., Repanas K., and Kyrpides N. Cross-talk between catalytic and regulatory elements in a DEAD motor domain is essential for SecA function EMBO J. 20 2001 961 970 (Pubitemid 32186787)
75. Mitchell C., and Oliver D. Two distinct ATP-binding domains are needed to promote protein export by Escherichia coli SecA ATPase Mol. Microbiol. 10 1993 483 497 (Pubitemid 23334430)
76. Doyle S.M., Bilsel O., and Teschke C.M. SecA folding kinetics: a large dimeric protein rapidly forms multiple native states J. Mol. Biol. 341 2004 199 214 (Pubitemid 39090645)
77. Laue T.M., Shah B., Ridgeway T.M., and Pelletier S.L. Computer-aided interpretation of sedimentation data for proteins S.E. Harding, J.C. Horton, A.J. Rowe, Analytical Ultracentrifugation in Biochemistry and Polymer Science 1992 Royal Society of Chemistry Cambridge, England 90 125
78. Selo I., Negroni L., Creminon C., Grassi J., and Wal J.M. Preferential labeling of alpha-amino N-terminal groups in peptides by biotin: application to the detection of specific anti-peptide antibodies by enzyme immunoassays J. Immunol. Methods 199 1996 127 138 (Pubitemid 26412942)
79. Musial-Siwek M., Yeagle P.L., and Kendall D.A. A small subset of signal peptidase residues are perturbed by signal peptide binding Chem. Biol. Drug Des. 72 2008 140 146
80. Philo J.S. Improved methods for fitting sedimentation coefficient distributions derived by time-derivative techniques Anal. Biochem. 354 2006 238 246
81. Stafford W.F., and Sherwood P.J. Analysis of heterologous interacting systems by sedimentation velocity: curve fitting algorithms for estimation of sedimentation coefficients, equilibrium and kinetic constants Biophys. Chem. 108 2004 231 243 (Pubitemid 38388491)
82. Krissinel E., and Henrick K. Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797 (Pubitemid 47321791)