The bacterial protein-translocation complex: SecYEG dimers associate with one or two SecA molecules

Journal of Molecular Biology

Volumn 340, Issue 3, 2004, Pages 513-524

  Tziatzios, Christos ^b   Schubert, Dieter ^b   Lotz, Mirko ^a   Gundogan, Derya ^a   Betz, Heidi ^a   Schägger, Hermann ^c   Haase, Winfried ^a   Duong, Franck ^d   Collinson, Ian ^a  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

BN PAGE, blue native gel electrophoresis; protein translocation; SecA; SecYEG; stoichiometry; TBS, Tris buffered saline

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; MONOCLONAL ANTIBODY; PROTEIN SECA; PROTEIN SECYEG; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; DIMERIZATION; ESCHERICHIA COLI; HYDROLYSIS; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; PROTEOLIPOSOME; RIBOSOME; STOICHIOMETRY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 2942733422     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.04.076     Document Type: Article

References (42)

1. Prinz A., Behrens C., Rapoport T.A., Hartmann E., Kalies K.U. Evolutionarily conserved binding of ribosomes to the translocation channel via the large ribosomal RNA. EMBO J. 19:2000;1900-1906
2. Matlack K.E., Mothes W., Rapoport T.A. Protein translocation: tunnel vision. Cell. 92:1998;381-390
3. Arkowitz R.A., Joly J.C., Wickner W. Translocation can drive the unfolding of a preprotein domain. EMBO J. 12:1993;243-253
4. Müller M., Koch H., Beck K., Schafer U. Protein traffic in bacteria: multiple routes from the ribosome to and across the membrane. Prog. Nucl. Acid Res. Mol. Biol. 66:2001;107-157
5. Hartl F., Lecker S., Schiebel E., Hendrick J., 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. Douville K., Price A., Eichler J., Economou A., Wickner W. SecYEG and SecA are the stoichiometric components of preprotein translocase. J. Biol. Chem. 270:1995;20106-20111
7. Economou A., Wickner W. SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell. 78:1994;835-843
8. Driessen A.J., Fekkes P., van der Wolk J.P. The Sec system. Curr. Opin. Microbiol. 1:1998;216-222
9. Breyton C., Haase W., Rapoport T.A., Kühlbrandt W., Collinson I. Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature. 418:2002;662-665
10. van den Berg L., Clemons W.M.J., Collinson I., Modis Y., Hartmann E., Harrison S.C., Rapoport T.A. X-ray structure of a protein-conducting channel. Nature. 427:2004;36-44
11. Hunt J.F., Weinkauf S., Henry L., Fak J.J., McNicholas P., Oliver D.B., Deisenhofer J. Nucleotide control of interdomain interactions in the conformational reaction cycle of SecA. Science. 297:2002;2018-2026
12. Economou A., Pogliano J., Beckwith J., Oliver D., 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
13. Eichler J., Wickner W. 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. USA. 94:1997;5574-5581
14. Driessen A. SecA, the peripheral subunit of the Escherichia coli precursor protein translocase, is functional as a dimer. Biochemistry. 32:1993;13190-13197
15. Ding H., Hunt J.F., Mukerji I., Oliver D. Bacillus subtilis SecA ATPase exists as an antiparallel dimer in solution. Biochemistry. 42:2003;8729-8738
16. Woodbury R.L., Hardy S.J.S., Randall L.L. Complex behavior in solution of homodimeric SecA. Protein Sci. 11:2002;875-882
17. Bu Z., Wang L., 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
18. Or E., Navon A., Rapoport T.A. Dissociation of the dimeric SecA ATPase during protein translocation across the bacterial membrane. EMBO J. 21:2002;4470-4479
19. 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
20. Yahr T., Wickner W. Evaluating the oligomeric state of SecYEG in preprotein translocase. EMBO J. 19:2000;4393-4401
21. Manting E.H., van der Does C., Remigy H., Engel A., Driessen A.J. SecYEG assembles into a tetramer to form the active protein translocation channel. EMBO J. 19:2000;852-861
22. Bessonneau P., Besson V., Collinson I., Duong F. The SecYEG preprotein translocation channel is a conformationally dynamic and dimeric structure. EMBO J. 21:2002;995-1003
23. 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
24. Duong F. Binding, activation and dissociation of the dimeric SecA ATPase at the dimeric SecYEG translocase. EMBO J. 22:2003;4375-4384
25. Reynolds J.A., Tanford C. Determination of molecular weight of the protein moiety in protein-detergent complexes without direct knowledge of detergent binding. Proc. Natl Acad. Sci. USA. 73:1976;4467-4470
26. Schubert D., Schuck P. Analytical ultracentrifugation as a tool for studying membrane proteins. Prog. Colloid Polym. Sci. 86:1991;12-22
27. von Rückmann B., Huber E., Schuck P., Schubert D. Studying heterologous associations between membrane proteins by analytical ultracentrifugation: experience with erythrocyte band 3. Prog. Colloid Polym. Sci. 99:1995;69-73
28. Dölle F., Schubert D. Dye-labelling as a means to study ternary protein complexes by analytical ultracentrifugation: the band 3/ankyrin/aldolase complex from erythrocyte membranes. Prog. Colloid Polym. Sci. 107:1997;77-81
29. von Rückmann B., Schubert D. The complex of band 3 protein of the human erythrocyte membrane and glyceraldehyde-3-phosphate dehydrogenase: stoichiometry and competition by aldolase. Biochim. Biophys. Acta. 1559:2002;43-55
30. Schuck P. Simultaneous radial and wavelength analysis with the Optima XL-A analytical ultracentrifuge. Prog. Colloid Polym. Sci. 94:1994;1-13
31. Schuck P., Legrum B., Passow H., Schubert D. The influence of two anion-transport inhibitors, 4, 4′-diisothiocyanatodihydrostilbene-2, 2′-disulfonate and 4, 4′-dibenzoylstilbene-2, 2′-disulfonate, on the self-association of erythrocyte band 3 protein. Eur. J. Biochem. 230:1995;806-812
32. Collinson I., Breyton C., Duong F., Tziatzios C., Schubert D., Or E., et al. Projection structure and oligomeric properties of a bacterial core protein translocase. EMBO J. 20:2001;2462-2471
33. Lill R., Dowhan W., 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
34. Dobberstein B., Sinning I. Structural biology: surprising news from the PCC. Science. 303:2004;320-322
35. Huber R., Deisenhofer J., Colman P.M., Matsushima M., Palm W. Crystallographic structure studies of an IgG molecule and an Fc fragment. Nature. 264:1976;415-420
36. Laemmli U. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685
37. Fujimoto K. SDS-digested freeze-fracture replica labeling electron microscopy to study the two-dimensional distribution of integral membrane proteins and phospholipids in biomembranes: practical procedure, interpretation and application. Histochem. Cell Biol. 107:1997;87-96
38. Schubert D., Tziatzios C., van den Broek J.A., Schuck P., Germeroth L., Michel H. Determination of the molar mass of pigment containing complexes of intrinsic membrane proteins: problems, solutions and application to the light-harvesting complex B800/820 of Rhodospirillum molischianum. Prog. Colloid Polym. Sci. 94:1994;14-19
39. Mayer G., Ludwig B., Müller H.-W., van den Broek J.A., Friesen R.H.E., Schubert D. Studying membrane proteins in detergent solution by analytical ultracentrifugation: different methods for density matching. Prog. Colloid Polym. Sci. 113:1999;176-181
40. Schägger H. Blue-native gels to isolate protein complexes from mitochondria. Methods Cell Biol. 65:2001;231-244
41. Branton D., Bullivant S., Gilula N.B., Karnovsky M.J., Moor H., Mühlethaler K., et al. Freeze-etching nomenclature. Science. 190:1975;54-56
42. Lanzetta P.A., Alvarez L.J., Reinach P.S., Candia O.A. An improved assay for nanomole amounts of inorganic phosphate. Anal. Biochem. 100:1979;95-97