Sec-dependent protein translocation across biological membranes: Evolutionary conservation of an essential protein transport pathway

Molecular Membrane Biology

Volumn 22, Issue 1-2, 2005, Pages 17-28

  Stephenson, Keith ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Membrane targeting; Protein secretion; Sec61 ; SecYEG; Translocon

Indexed keywords

ADENOSINE TRIPHOSPHATE; CELL PROTEIN; HISTONE; MEMBRANE PROTEIN; PROTEIN FTSY; PROTEIN SEC6; PROTEIN SECA; PROTEIN SECB; PROTEIN SECYEG; SIGNAL PEPTIDE; SIGNAL RECOGNITION PARTICLE; SMALL CYTOPLASMIC RNA; UNCLASSIFIED DRUG;

BACTERIAL MEMBRANE; CELL MEMBRANE TRANSPORT; CELL ORGANELLE; CELL SECRETION; CHANNEL GATING; COMPLEX FORMATION; ENDOPLASMIC RETICULUM; EUKARYOTIC CELL; GENERAL SECRETORY PATHWAY; GENETIC CONSERVATION; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW;

BACTERIAL PROTEINS; CELL MEMBRANE; EUKARYOTIC CELLS; EVOLUTION, MOLECULAR; MEMBRANE PROTEINS; PROTEIN FOLDING; PROTEIN TRANSPORT; PROTEINS;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 18844427294     PISSN: 09687688     EISSN: None     Source Type: Journal    
DOI: 10.1080/09687860500063308     Document Type: Review

References (114)

1. Pugsley AP, Francetic O, Driessen AJ, de Lorenzo V. Getting out: Protein traffic in prokaryotes. Mol Microbiol 2004;52:3-11.
2. Wirth A, Jung M, Bies C, Frien M, Tyedmers J, Zimmermann R, Wagner R. The Sec61p complex is a dynamic precursor activated channel. Mol Cell 2003;12:261-268.
3. Blobel G, Dobberstein B. Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell Biol 1975;67:835-851.
4. Park S, Lui G, Topping TBCWH, Randall LL. Modulation of folding pathways of exported proteins by the leader sequence. Science 1998;239:1033-1035.
5. Akita M, Sasaki S, Matsuyama S, Mizushima S. SecA interacts with secretory proteins by recognizing the positive charge at the amino terminus of the signal peptide in Escherichia coli. J Biol Chem 1990;265:8162-8169.
6. de Vrije T, Batenburg AM, Killian JA, de Kruijff B. Lipid involvement in protein translocation in Escherichia coli. Mol Microbiol 1990;4:143-150.
7. von Heijne G. Patterns of amino acids near signal sequence cleavage sites. Eur J Biochem 1983;133:17-21.
8. von Heijne G. Signal sequences. The limits of variation. J Mol Biol 1985;184:99-105.
9. Martoglio B, Dobberstein B. Signal sequences: More than just greasy peptides. Trend Cell Biol 1998;8:410-415.
10. Humphreys DP, Sehdev M, Chapman AP, Ganesh R, Smith BJ, King LM, Glover DJ, Reeks DG, Stephens PE. High-level periplasmic expression in Escherichia coli using a eukaryotic signal peptide: importance of codon usage at the 5′ end of the coding sequence. Prot Express Purif 2002;20:252-264.
11. Belin D, Guzman L-M, Bost S, Konakova M, Silva F, Beckwith J. Functional activity of eukaryotic signal sequences in Escherichia coli: The ovalbumin family of serine protease inhibitors. J Mol Biol 2003;335:437-453.
12. Johnson AE, van Waes MA. The translocon: A dynamic gateway at the ER membrane. Annu Rev Cell Dev Biol 1999;15:799-842.
13. Keenan RJ, Freymann DM, Stroud RM, Walter P. The signal recognition particle. Annu Rev Biochem 2001;70: 755-775.
14. Stirling CJ. Protein targeting to the endoplasmic reticulum in yeast. Microbiology 1999;145:991-998.
15. Plath K, Rapoport TA. Spontaneous release of cytosolic proteins from post-translational substrates before their transport into the endoplasmic reticulum. J Cell Biol 2000;151:167-178.
16. Deshaies RJ, Sanders SL, Feldheim DA, Schekman R. Assembly of yeast Sec proteins involved in translocation into the endoplasmic reticulum into a membrane-bound multi-subunit complex. Nature 1991;349:806-808.
17. Wilier M, Jermy AJ, Young BP, Stirling CJ. Identification of novel protein-protein interactions at the cytosolic surface of the Sec63 complex in the yeast ER membrane. Yeast 2003;20:133-148.
18. Matlack KE, Misselwitz B, Plath K, Rapoport TA. BiP acts as a molecular ratchet during posttranslational translocation of pre-pro-alpha factor across the ER membrane. Cell 1999;97:553-564.
19. Abell BM, Pool MR, Schlenker O, Sinning I, High S. Signal recognition particle mediates post-translational targeting in eukaryotes. EMBO J 2004;23:2755-2764.
20. Luirink J, Sinning I. SRP-mediated protein targeting: Structure and function revisited. Biochim Biophys Act 2004;1694:17-35.
21. Luirink J, High S, Wood H, Giner A, Tollervey D, Dobberstein B. Signal-sequence recognition by an Escherichia coli ribonucleoprotein complex. Nature 1992;359: 741-743.
22. Luirink J, ten Hagen-Jongman CM, van der Weijden CC, Oudega B, Dobberstein B, Kusters R. An alternative protein targeting pathway in Escherichia coli: on the role of FtsY. EMBO J 1994;13:2289-2296.
23. Valent QA, Scotti PA, High S, de Gier JW, von Heijne G, Lentzen G, Wintermeyer W, Oudega B, Luirink J. The Escherichia coli SRP and SecB targeting pathways converge at the translocon. EMBO J 1998;17:2504-2512.
24. Nakamura K, Nishiguchi M, Honda K, Yamane K. The Bacillus subtilis SRP54 homologue, Ffh, has an intrinsic GTPase activity and forms a ribonucleoprotein complex with small cytoplasmic RNA in vivo. Biochem Biophys Res Commun 1994;199:1394-1399.
25. Nakamura K, Yahagi S, Yamazaki T, Yamane K. Bacillus subtilis histone-like protein, HBsu, is an integral component of an SRP-like particle that can bind to the Alu domain of small cytoplasmic RNA. J Biol Chem 1994;274:13569-13576.
26. Avdeeva ON, Myasnikov AG, Sergiev PV, Bogdanov AA, Brimacombe R, Dontsova OA. Construction of the minimal 'SRP' that interacts with the translating ribosome but not with specific membrane receptors in Escherichia coli. FEBS Lett 2002;514:70-73.
27. Pugsley AP. The complete general secretory pathway in Gram-negative bacteria. Microbiol Rev 1993;57:50-108.
28. Woldringh CL. The role of co-transcriptional translation and protein translocation (transertion) in bacterial chromosome segregation. Mol Microbiol 2002;45:17-29.
29. de Keyzer J, van der Does C, Driessen AJ. The bacterial translocase: A dynamic protein channel complex. Cell Mol Life Sci 2003;60:2034-2052.
30. Ullers RS, Luirink J, Harms N, Schwager F, Georgopoulos C, Genevaux P. SecB is a bona fide generalized chaperone in Escherichia coli. Proc Natl Acad Sci USA 2004;101: 7583-7588.
31. Randall LL, Topping TB, Hardy SJ, Pavlov MY, Freistroffer DV, Ehrenberg M. Binding of SecB to ribosome-bound polypeptides has the same characteristics as binding to full-length, denatured proteins. Proc Natl Acad Sci USA 1997;94:802-807.
32. Knoblauch NT, Rudiger S, Schonfeld HJ, Driessen AJ, Schneider-Mergener J, Bukau B. Substrate specificity of the SecB chaperone. J Biol Chem 1999;274:34219-34225.
33. Dekker C, de Kruijff B, Gros P. Crystal structure of SecB from Escherichia coli. J Struct Biol 2003;144:313-319.
34. Xu Z, Knafels JD, Yoshino K. Crystal structure of the bacterial protein export chaperone SecB. Nat Struct Biol 2000;7:1077-1079.
35. Zhou J, Xu Z. Structural determinants of SecB recognition by SecA in bacterial protein translocation. Nat Struct Biol 2003;10:942-947.
36. Fekkes P, Driessen AJ. Protein targeting to the bacterial cytoplasmic membrane. Microbiol Mol Biol Rev 1999;63: 161-173.
37. Hartl FU, Lecker S, Schiebel E, Hendrick JP, Wickner W. The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane. Cell 1990;63:269-279.
38. 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 1990;60:271-280.
39. Vrontou E, Economou A. Structure and function of SecA, the preprotein translocase nanomotor. Biochim Biophys Act 2004;1694:67-80.
40. Hunt JF, Weinkauf S, Henry L, Fak JJ, McNicholas P, Oliver DB, Deisenhofer J. Nucleotide control of interdomain interactions in the conformational reaction cycle of SecA. Science 2002;297:2018-2026.
41. Sharma V, Arockiasamy A, Ronning DR, Sawa CG, Holzenburg A, Braunstein M, Jacobs WR, Jr., Sacchettini JC. Crystal structure of Mycobacterium tuberculosis SecA, a preprotein translocating ATPase. Proc Natl Acad Sci USA 2003;100:2243-2248.
42. Osbourne AR, Clemons WM, Rapoport TA. A large conformational change of the translocation ATPase SecA. Proc Natl Acad Sci USA 2004;101:10937-10942.
43. Matousek WM, Alexandrescu AT. NMR structure of the C-terminal domain of SecA in the free state. Biochim Biophys Act 2004;1702:163-171.
44. Dempsey BR, Wrona M, Moulin JM, Gloor GB, Jalilehvand F, Lajoie G, Shaw GS, Shilton BH. Solution NMR structure and X-ray absorption analysis of the C-terminal zinc-binding domain of the SecA ATPase. Biochemistry 2004;43:9361-9371.
45. Or E, Navon A, Rapoport TA. Dissociation of the dimeric SecA ATPase during protein translocation across the bacterial membrane. EMBO J 2002;21:4470-4479.
46. Duong F. Binding, activation and dissociation of dimeric SecA ATPase at the dimeric SecYEG translocase. EMBO J 2003;22:4375-4384.
47. Benach J, Chou Y-T, Fak JJ, Itkin A, Nicolae DD, Smith PC, Wittrock G, Floyd DL, Golsaz CM, Gierasch LM, Hunt JF. Phospholipid-induced monomerisation and signal peptide induced oligomerisation of SecA. J Biol Chem 2003;278:3628-3638.
48. Bu Z, Wang L, Kendall DA. 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 2003;332:23-30.
49. Fekkes P, de Wit JG, Boorsma A, Friesen RH, Driessen AJ. Zinc stabilizes the SecB binding site of SecA. Biochemistry 1999;38:5111-5116.
50. Randall LL, Crane JM, Liu G, Hardy SJ. Sites of interaction between SecA and the chaperone SecB, two proteins involved in export. Prot Sci 2004;13:1124-1133.
51. Muller JP, Bron S, Venema G, van Dijl JM. Chaperone-like activities of the CsaA protein of Bacillus subtilis. Microbiology 2000;146:77-88.
52. Muller JP, Ozeqowski J, Vettermann S, Swaving J, van Wely KH, Driessen AJ. Interaction of Bacillus subtilis CsaA with SecA and precursor proteins. Biochem J 2000;348:367-373.
53. Bunai K, Yamada K, Hayashi K, Nakamura K, Yamane K. Enhancing effect of Bacillus subtilis Ffh, a homologue of the SRP54 subunit of the mammalian signal recognition particle, on the binding of SecA to precursors of secretory proteins in vitro. J Biochem 1999;125:151-159.
54. Tjalsma H, Bolhuis A, Jongbloed JDH, Bron S, van Dijl JM. Signal peptide-dependent protein transport in Bacillus subtilis: a genome-based survey of the secretome. Microbiol Mol Biol Rev 2000;64:515-547.
55. Woese CR, Fox GE. Phylogenetic structure of the prokaryotic domain: The primary kingdoms. Proc Natl Acad Sci USA 1997;74:5088-5090.
56. Bolhuis A. The archaeal Sec-dependent protein translocation pathway. Philos Trans R Soc 2003;359:919-927.
57. Ring G, Eichler J. Extreme secretion: Protein translocation across the archaeal cytoplasmic membrane. J Bioenerg Biomembr 2004;36:35-45.
58. Rose RW, Pohlschroder M. In vivo analysis of an essential archaeal signal recogition particle in its native host. J Bacteriol 2002;184:3260-3267.
59. Lichi T, Ring G, Eichler J. Membrane binding of SRP pathway components in the halophilic archaea Haloferax volcanii. Eur J Biochem 2004;271:1382-1390.
60. Ha SC, Lee TH, Cha SS, Kim KK. Functional identification of the SecB homologue in Methanococcus jannaschii and direct interaction of SecB with trigger factor. Biochem Biophys Res Commun 2004;315:1039-1044.
61. Bieker KL, Phillips GJ, Silhavy TJ. The sec and prl genes of Eschenchia coli. J Bioenerg Biomembr 1990;22:291-310.
62. Schatz PJ, Beckwith J. Genetic analysis of protein export in Eschenchia coli. Annu Rev Genet 1990;24:215-248.
63. Nishiyama K, Hanada M, Tokuda H. Disruption of the gene encoding p12 (SecG) reveals the direct involvement and important function of SecG in the protein translocation of Eschenchia coli at low temperature. EMBO J 1994;13:3272-3277.
64. Homma T, Yoshihisa T, Ito K. Subunit interactions in the Eschenchia coli protein translocase: SecE and SecG associate independently with SecY. FEBS Lett 1997;408:11-15.
65. Duong F, Wickner W. Distinct catalytic roles of the SecYE, SecG and SecDFYajC subunits of the preprotein translocase holoenzyme. EMBO J 1997;16:2756-2768.
66. Duong F, Wickner W The SecDFYajC domain of the preprotein translocase controls preprotein movement by regulating SecA membrane cycling. EMBO J 1997;16:4871-4879.
67. Bolhuis A, Broekhuizen CP, van Roosmalen ML, Venema G, Bron S, Quax WJ, van Dijl JM. SecDF of Bacillus subtilis, a molecular Siamese twin required for the efficient secretion of proteins. J Biol Chem 1998;273:21217-21224.
68. Taura T, Akiyama K, Ito K. Genetic analysis of SecY: Additional export-defective mutations and factors affecting their phenotypes. Mol Gen Genet 1994;243:261-269.
69. Nouwen N, Driessen AJ. SecDFYajC forms a heterotetrameric complex with YidC. Mol Microbiol 2002;44:1397-1405.
70. Dalbey RE, Kuhn A. YidC family members are involved in the membrane insertion, lateral integration, folding, and assembly of membrane proteins. J Cell Biol 2004;166:769-774.
71. Urbanus ML, Scotti PA, Froderberg L, Saaf A, de Gier JW, Brunner J, Samuelson JC, Dalbey RE, Oudega B, Luirink J. Sec-dependent membrane protein insertion: Sequential interaction of nascent FtsQ with SecY and YidC. EMBO Rep 2001;2:524-529.
72. Sereck J, Bauer-Manz G, Struhalla G, van den Berg L, Kiefer D, Dalbey RE, Kuhn A. Eschenchia coli YidC is a membrane insertase for Sec-independent proteins. EMBO J 2004;23:294-301.
73. Beck K, Eisner G, Trescher D, Dalbey RE, Brunner J, Muller M. YidC, an assembly site for polytopic Eschenchia coli membrane proteins located in immediate proximity to the SecYE translocon and lipids. EMBO Rep 2001;2:709-714.
74. van der Laan M, Urbanus ML, ten Hagen-Jongman CM, Nouwen N, Oudega B, Harms N, Driessen AJ, Luirink J. A conserved function of YidC in the biogenesis of respiratory chain complexes. Proc Natl Acad Sci USA 2003;100: 5801-5806.
75. 0 ATP synthetase subunit c is a substrate of the novel YidC pathway for membrane protein biogenesis. J Cell Biol 2004;165:213-222.
76. Jeong SM, Yoshikawa H, Takahashi H. Isolization and characterisation of the secE homologue gene of Bacillus subtilis. Mol Microbiol 1993;10:133-142.
77. van Wely KH, Swaving J, Broekhuizen CP, Rose M, Quax WJ, Driessen AJ. Functional identification of the product of the Bacillus subtilis yvaL gene as the SecG homologue. J Bacteriol 1999;181:1786-1792.
78. Swaving J, van Wely KH, Driessen AJ. Host specific functions of preprotein translocase subunits. J Bacteriol 1999;181:7021-7027.
79. Tjalsma H, Bron S, van Dijl JM. Complementary impact of paralogous Oxa1-like proteins of Bacillus subtilis on posttranslocational stages in protein secretion. J Biol Chem 2003;278:15622-15632.
80. Cao TB, Saier MH. The general protein secretory pathway: Phylogenetic analysis leading to evolutionary conclusions. Biochim Biophys Act 2003;1609:115-125.
81. Mothes W, Jungnickel B, Brunner J, Rapoport TA. Signal sequence recognition in cotranslational translocation by protein components of the endoplasmic reticulum membrane. Cell Biol 1998;142:355-364.
82. Kalies KU, Rapoport TA, Hartmann E. The beta subunit of the Sec61 complex facilitates cotranslational protein transport and interacts with the signal peptidase during translocation. J Cell Biol 1998;141:887-894.
83. Fons RD, Bogert BA, Hegde RS. Substrate-specific function of the translocon-associated protein complex during translocation across the ER membrane. J Cell Biol 2003;160:529-539.
84. Young BP, Craven RA, Reid PJ, Wilier M, Stirling CJ. Sec63p and Kar2p are required for the translocation of SRP-dependent precursors into the yeast endoplasmic reticulum in vivo. EMBO J 2001;20:262-271.
85. Kinch LN, Saier MH, Grishin NV. Sec61β-a component of the archaeal protein secretory system. Trend Biochem Sci 2002;27:170-171.
86. Eichler J. Evolution of the prokaryotic protein translocation complex: A comparison of archaeal and bacterial versions of SecDF. Mol Phylogent Evol 2003;27:504-509.
87. van den Berg B, Clemons WM, Collinson I, Modis Y, Hartmann E, Harrison SG, Rapoport TA. X-ray structure of a protein-conducting channel. Nature 2003;427:36-44.
88. Breyton C, Haase W, Rapoport TA, Kuhlbrandt W, Collinson I. Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature 2002;418: 662-665.
89. Manting EH, van der Does C, Remigy H, Engel A, Driessen AJ. SecYEG assembles into a tetramer to form the active protein translocation channel. EMBO J 2000;19:852-861.
90. Mori H, Tsukazaki T, Masui R, Kuramitsu S, Yokoyama S, Johnson AE, Kimura Y, Akiyama Y, Ito K. Fluorescence resonance energy transfer analysis of protein translocase. SecYE from Thermus thermophilus HB8 forms a constitutive oligomer in membranes. J Biol Chem 2003;278:14257-14264.
91. Sarvas M, Harwood CR, Bron S, van Dijl JM. Posttranslocational folding of secretory proteins in Gram-positive bacteria. Biochim Biophys Act 2004;1694:311-327.
92. Stevens FJ, Argon Y. Protein folding in the ER. Sem Cell Devel Biol 1999;10:443-454.
93. Rouviere PE, Gross CA. SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev 1996;10: 3170-3182.
94. Jacobs M, Andersen JB, Kontinen VP, Sarvas M. Bacillus subtilis PrsA is required in vivo as an extracytoplasmic chaperone for secretion of active enzymes synthesized either with or without pre-sequences. Mol Microbiol 1993;8:957-966.
95. Behrens S, Maier R, de Cock H, Schmid FX, Gross CA. The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J 2001;20:285-294.
96. Vitikainen M, Lappalainen I, Seppala R, Antelmann H, Boer H, Taira S, Savilahti H, Hecker M, Sarvas M, Kontinen VP. Structure-function analysis of PrsA reveals roles for the parvulin-like and flanking N- and C-terminal domains in protein folding and secretion in Bacillus subtilis. J Biol Chem 2004;279:19302-19314.
97. Jessop CE, Chakravarthi S, Watkins RH, Bulleid NJ. Oxidative protein folding in the mammalian endoplasmic reticulum. Biochem Soc Trans 2004;32:655-658.
98. Ritz D, Beckwith J. Roles of thiol-redox pathways in bacteria. Annu Rev Microbiol 2001;55:21-48.
99. Bolhuis A, Venema G, Quax WJ, Bron S, van Dijl JM. Functional analysis of paralogous thiol-disulphide oxidoreductases in Bacillus subtilis. J Biol Chem 1999;274:24531-24538.
100. Meima R, Eschevins C, Fillinger S, Bolhuis A, Hamoen LW, Dorenbos R, Quax WJ, van Dijl JM, Prowedi R, Chen I, Dubnau D, Bron S. The bdbDC operon of Bacillus subtilis encodes thiol disulphide oxidoreductases required for competence development. J Biol Chem 2001;277:6994-7001.
101. 2+-handling proteins. J Cell Biol 2003;160:475-479.
102. Stephenson K, Carter NM, Harwood CR, Petit-Glatron MF, Chambert R. The influence of protein folding on late stages of the secretion of alpha-amylases from Bacillus subtilis. FEBS Lett 1998;430:385-389.
103. Stephenson K, Jensen CL, Jorgensen ST, Lakey JH, Harwood CR. The influence of secretory protein charge on late stages of secretion from the Gram-positive bacterium Bacillus subtilis. Biochem J 2000;350 Pt 1:31-39.
104. Hyyrylainen HL, Vitikainen M, Thwaite J, Wu H, Sarvas M, Harwood CR, Kontinen VP, Stephenson K. D-Alanine substitution of teichoic acids as a modulator of protein folding and stability at the cytoplasmic membrane/cell wall interface of Bacillus subtilis. J Biol Chem 2000;275:26696-26703.
105. Bolhuis A, Tjalsma H, Stephenson K, Harwood CR, Venema G, Bron S, van Dijl JM. Different mechanisms for thermal inactivation of Bacillus subtilis signal peptidase mutants. J Biol Chem 1999;274:15865-15868.
106. Stephenson K, Harwood CR. Influence of a cell-wall-associated protease on production of alpha- amylase by Bacillus subtilis. Appl Environ Microbiol 1998;64:2875-2881.
107. Stephenson K, Jensen CL, Jorgensen ST, Harwood CR. Simultaneous inactivation of the wprA and dltB genes of Bacillus subtilis reduces the yield of alpha-amylase. Lett Appl Microbiol 2002;34:394-397.
108. Thwaite J, Baillie LW, Carter NM, Stephenson K, Rees M, Harwood CR, Emmerson PT. Optimising the cell wall microenvironment allows increased production of recombinant Bacillus anthracis protective antigen from Bacillus subtilis. Appl Environ Microbiol 2002;68:227-234.
109. Ellgaard L, Helenius A. Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 2003;4:181-191.
110. Spiess C, Beil A, Ehrmann M. A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 1999;97:339-347.
111. Jensen CL, Stephenson K, Jorgensen ST, Harwood C. Cell-associated degradation affects the yield of secreted engineered and heterologous proteins in the Bacillus subtilis expression system. Microbiology 2000;146 (Pt 10):2583-2594.
112. Noone D, Howell A, Collery R, Devine KM. YkdA and YvtA, HtrA-like serine proteases in Bacillus subtilis engage in negative autoregulation and reciprocal cross-regulation of ykdA and yvtA gene expression. J Bacteriol 2001;183: 654-663.
113. Driessen AJ. Precursor protein translocation by the Escherichia coli translocase is directed by the protonmotive force. EMBO J 1992;11:847-853.
114. Neumann-Haefelin C, Schafer U, Muller M, Koch H-G. SRP-dependent co-translational targeting and SecA-dependent translocation analyzed as individual steps in the export of a bacterial protein. EMBO J 2000;19:6419-6426.