Substrate-Dependent Assembly of the Tat Translocase as Observed in Live Escherichia coli Cells

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Rose, Patrick ^a   Fröbel, Julia ^a   Graumann, Peter L ^b   Müller, Matthias ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; TWIN ARGININE TRANSLOCATION A PROTEIN; TWIN ARGININE TRANSLOCATION B PROTEIN; TWIN ARGININE TRANSLOCATION C PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME SUBSTRATE; MOLECULAR IMAGING; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; TRANSPORT KINETICS;

BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CELL MEMBRANE; CYTOPLASM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GREEN FLUORESCENT PROTEINS; MEMBRANE TRANSPORT PROTEINS; MUTATION; PROTEIN TRANSPORT; PROTON-MOTIVE FORCE;

EID: 84880969972     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069488     Document Type: Article

References (68)

1. Celedon JM, Cline K, (2013) Intra-plastid protein trafficking: how plant cells adapted prokaryotic mechanisms to the eukaryotic condition. Biochim Biophys Acta 1833: 341-351. doi:10.1016/j.bbamcr.2012.06.028. PubMed: 22750312.
2. Fröbel J, Rose P, Müller M, (2012) Twin-arginine-dependent translocation of folded proteins. Philos Trans R Soc Lond B Biol Sci 367: 1029-1046. doi:10.1098/rstb.2011.0202. PubMed: 22411976.
3. Palmer T, Berks BC, (2012) The twin-arginine translocation (Tat) protein export pathway. Nat Rev Microbiol 10: 483-496. PubMed: 22683878.
4. Hu Y, Zhao E, Li H, Xia B, Jin C, (2010) Solution NMR structure of the TatA component of the twin-arginine protein transport system from gram-positive bacterium Bacillus subtilis. J Am Chem Soc 132: 15942-15944. doi:10.1021/ja1053785. PubMed: 20726548.
5. Rodriguez F, Rouse SL, Tait CE, Harmer J, De Riso A, et al. (2013) Structural model for the protein-translocating element of the twin-arginine transport system. Proc Natl Acad Sci U.S.A. PubMed: 23471988.
6. Walther TH, Grage SL, Roth N, Ulrich AS, (2010) Membrane alignment of the pore-forming component TatA(d) of the twin-arginine translocase from Bacillus subtilis resolved by solid-state NMR spectroscopy. J Am Chem Soc 132: 15945-15956. doi:10.1021/ja106963s. PubMed: 20977272.
7. Aldridge C, Storm A, Cline K, Dabney-Smith C, (2012) The chloroplast twin arginine transport (tat) component, tha4, undergoes conformational changes leading to tat protein transport. J Biol Chem 287: 34752-34763. doi:10.1074/jbc.M112.385666. PubMed: 22896708.
8. Koch S, Fritsch MJ, Buchanan G, Palmer T, (2012) Escherichia coli TatA and TatB Proteins Have N-out, C-in Topology in Intact Cells. J Biol Chem 287: 14420-14431.
9. Chan CS, Zlomislic MR, Tieleman DP, Turner RJ, (2007) The TatA subunit of Escherichia coli twin-arginine translocase has an N-in topology. Biochemistry 46: 7396-7404. doi:10.1021/bi7005288. PubMed: 17536842.
10. Gouffi K, Gérard F, Santini CL, Wu LF, (2004) Dual topology of the Escherichia coli TatA protein. J Biol Chem 279: 11608-11615. doi:10.1074/jbc.M313187200. PubMed: 14701831.
11. Rollauer SE, Tarry MJ, Graham JE, Jääskeläinen M, Jäger F, et al. (2012) Structure of the TatC core of the twin-arginine protein transport system. Nature 492: 210-214. doi:10.1038/nature11683. PubMed: 23201679.
12. Hicks MG, de Leeuw E, Porcelli I, Buchanan G, Berks BC, et al. (2003) The Escherichia coli twin-arginine translocase: conserved residues of TatA and TatB family components involved in protein transport. FEBS Lett 539: 61-67. doi:10.1016/S0014-5793(03)00198-4. PubMed: 12650927.
13. Sargent F, Stanley NR, Berks BC, Palmer T, (1999) Sec-independent protein translocation in Escherichia coli. A Distinct Pivotal Role TatB Proteins J Biol Chem 274: 36073-36082.
14. Barrett CM, Freudl R, Robinson C, (2007) Twin arginine translocation (Tat)-dependent export in the apparent absence of TatABC or TatA complexes using modified Escherichia coli TatA subunits that substitute for TatB. J Biol Chem 282: 36206-36213. doi:10.1074/jbc.M704127200. PubMed: 17881358.
15. Blaudeck N, Kreutzenbeck P, Müller M, Sprenger GA, Freudl R, (2005) Isolation and characterization of bifunctional Escherichia coli TatA mutant proteins that allow efficient Tat-dependent protein translocation in the absence of TatB. J Biol Chem 280: 3426-3432. PubMed: 15557327.
16. Sargent F, Bogsch EG, Stanley NR, Wexler M, Robinson C, et al. (1998) Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J 17: 3640-3650. doi:10.1093/emboj/17.13.3640. PubMed: 9649434.
17. Baglieri J, Beck D, Vasisht N, Smith CJ, Robinson C, (2012) Structure of TatA paralog, TatE, suggests a structurally homogeneous form of Tat protein translocase that transports folded proteins of differing diameter. J Biol Chem 287: 7335-7344. doi:10.1074/jbc.M111.326355. PubMed: 22190680.
18. Gohlke U, Pullan L, McDevitt CA, Porcelli I, de Leeuw E, et al. (2005) The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter. Proc Natl Acad Sci U S A 102: 10482-10486. doi:10.1073/pnas.0503558102. PubMed: 16027357.
19. White GF, Schermann SM, Bradley J, Roberts A, Greene NP, et al. (2010) Subunit organization in the TatA complex of the twin arginine protein translocase: a site-directed EPR spin labeling study. J Biol Chem 285: 2294-2301. doi:10.1074/jbc.M109.065458. PubMed: 19920142.
20. Greene NP, Porcelli I, Buchanan G, Hicks MG, Schermann SM, et al. (2007) Cysteine scanning mutagenesis and disulfide mapping studies of the TatA component of the bacterial twin arginine translocase. J Biol Chem 282: 23937-23945. doi:10.1074/jbc.M702972200. PubMed: 17565984.
21. Fröbel J, Rose P, Müller M, (2011) Early contacts between substrate proteins and TatA translocase component in twin-arginine translocation. J Biol Chem 286: 43679-43689. doi:10.1074/jbc.M111.292565. PubMed: 22041896.
22. Dabney-Smith C, Cline K, (2009) Clustering of C-terminal stromal domains of Tha4 homo-oligomers during translocation by the Tat protein transport system. Mol Biol Cell 20: 2060-2069. doi:10.1091/mbc.E08-12-1189. PubMed: 19193764.
23. Dabney-Smith C, Mori H, Cline K, (2006) Oligomers of Tha4 organize at the thylakoid Tat translocase during protein transport. J Biol Chem 281: 5476-5483. PubMed: 16407186.
24. Walther TH, Gottselig C, Grage SL, Wolf M, Vargiu AV, et al. (2013) Folding and self-assembly of the TatA translocation pore based on a charge zipper mechanism. Cell 152: 316-326. doi:10.1016/j.cell.2012.12.017. PubMed: 23332763.
25. Brüser T, Sanders C, (2003) An alternative model of the twin arginine translocation system. Microbiol Res 158: 7-17. doi:10.1078/0944-5013-00176. PubMed: 12608575.
26. Bo H, Brüser T, (2011) The Tat-dependent protein translocation pathway. Biomol Concepts 2: 507-523.
27. Behrendt J, Lindenstrauss U, Brüser T, (2007) The TatBC complex formation suppresses a modular TatB-multimerization in Escherichia coli. FEBS Lett 581: 4085-4090. doi:10.1016/j.febslet.2007.07.045. PubMed: 17678896.
28. Kostecki JS, Li H, Turner RJ, DeLisa MP, (2010) Visualizing interactions along the Escherichia coli twin-arginine translocation pathway using protein fragment complementation. PLOS ONE 5: e9225. doi:10.1371/journal.pone.0009225. PubMed: 20169075.
29. Maldonado B, Buchanan G, Müller M, Berks BC, Palmer T, (2011) Genetic evidence for a TatC dimer at the core of the Escherichia coli twin arginine (Tat) protein translocase. J Mol Microbiol Biotechnol 20: 168-175. doi:10.1159/000329076. PubMed: 21709427.
30. Orriss GL, Tarry MJ, Ize B, Sargent F, Lea SM, et al.(2007) TatBC, TatB, and TatC form structurally autonomous units within the twin arginine protein transport system of Escherichia coli. FEBS Lett 581: 4091-4097.
31. Bolhuis A, Mathers JE, Thomas JD, Barrett CM, Robinson C, (2001) TatB and TatC form a functional and structural unit of the twin-arginine translocase from Escherichia coli. J Biol Chem 276: 20213-20219. doi:10.1074/jbc.M100682200. PubMed: 11279240.
32. Zoufaly S, Fröbel J, Rose P, Flecken T, Maurer C, et al. (2012) Mapping Precursor-binding Site on TatC Subunit of Twin Arginine-specific Protein Translocase by Site-specific Photo Cross-linking. J Biol Chem 287: 13430-13441. doi:10.1074/jbc.M112.343798. PubMed: 22362773.
33. Ma X, Cline K, (2013) Mapping the signal peptide binding and oligomer contact sites of the core subunit of the pea twin arginine protein translocase. Plant Cell 25: 999-1015. doi:10.1105/tpc.112.107409. PubMed: 23512851.
34. Alami M, Lüke I, Deitermann S, Eisner G, Koch HG, et al. (2003) Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol Cell 12: 937-946. doi:10.1016/S1097-2765(03)00398-8. PubMed: 14580344.
35. Gérard F, Cline K, (2006) Efficient Twin Arginine Translocation (Tat) Pathway Transport of a Precursor Protein Covalently Anchored to Its Initial cpTatC Binding Site. J Biol Chem 281: 6130-6135. doi:10.1074/jbc.M512733200. PubMed: 16407185.
36. Maurer C, Panahandeh S, Jungkamp AC, Moser M, Müller M, (2010) TatB functions as an oligomeric binding site for folded Tat precursor proteins. Mol Biol Cell 21: 4151-4161. doi:10.1091/mbc.E10-07-0585. PubMed: 20926683.
37. Lausberg F, Fleckenstein S, Kreutzenbeck P, Fröbel J, Rose P, et al. (2012) Genetic evidence for a tight cooperation of TatB and TatC during productive recognition of twin-arginine (Tat) signal peptides in Escherichia coli. PLOS ONE 7: e39867. doi:10.1371/journal.pone.0039867. PubMed: 22761916.
38. Kreutzenbeck P, Kröger C, Lausberg F, Blaudeck N, Sprenger GA, et al. (2007) Escherichia coli twin arginine (Tat) mutant translocases possessing relaxed signal peptide recognition specificities. J Biol Chem 282: 7903-7911. doi:10.1074/jbc.M610126200. PubMed: 17229735.
39. Kneuper H, Maldonado B, Jäger F, Krehenbrink M, Buchanan G, et al. (2012) Molecular dissection of TatC defines critical regions essential for protein transport and a TatB-TatC contact site. Mol Microbiol 85: 945-961. doi:10.1111/j.1365-2958.2012.08151.x. PubMed: 22742417.
40. Fröbel J, Rose P, Lausberg F, Blümmel AS, Freudl R, et al. (2012) Transmembrane insertion of twin-arginine signal peptides is driven by TatC and regulated by TatB. Nat Commun 3: 1311. doi:10.1038/ncomms2308. PubMed: 23250441.
41. Celedon JM, Cline K, (2012) Stoichiometry for binding and transport by the twin arginine translocation system. J Cell Biol 197: 523-534. doi:10.1083/jcb.201201096. PubMed: 22564412.
42. Ma X, Cline K, (2010) Multiple precursor proteins bind individual Tat receptor complexes and are collectively transported. EMBO J 29: 1477-1488. doi:10.1038/emboj.2010.44. PubMed: 20339348.
43. Tarry MJ, Schäfer E, Chen S, Buchanan G, Greene NP, et al. (2009) Structural analysis of substrate binding by the TatBC component of the twin-arginine protein transport system. Proc Natl Acad Sci U S A 106: 13284-13289. doi:10.1073/pnas.0901566106. PubMed: 19666509.
44. Stanley NR, Findlay K, Berks BC, Palmer T, (2001) Escherichia coli strains blocked in Tat-dependent protein export exhibit pleiotropic defects in the cell envelope. J Bacteriol 183: 139-144. doi:10.1128/JB.183.1.139-144.2001. PubMed: 11114910.
45. Hou B, Frielingsdorf S, Klösgen RB, (2006) Unassisted membrane insertion as the initial step in DeltapH/Tat-dependent protein transport. J Mol Biol 355: 957-967. doi:10.1016/j.jmb.2005.11.029. PubMed: 16343541.
46. Bageshwar UK, Whitaker N, Liang FC, Musser SM, (2009) Interconvertibility of lipid- and translocon-bound forms of the bacterial Tat precursor pre-SufI. Mol Microbiol 74: 209-226. doi:10.1111/j.1365-2958.2009.06862.x. PubMed: 19732346.
47. Ize B, Stanley NR, Buchanan G, Palmer T, (2003) Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol Microbiol 48: 1183-1193. doi:10.1046/j.1365-2958.2003.03504.x. PubMed: 12787348.
48. Ray N, Nenninger A, Mullineaux CW, Robinson C, (2005) Location and mobility of twin arginine translocase subunits in the Escherichia coli plasma membrane. J Biol Chem 280: 17961-17968. PubMed: 15728576.
49. Berthelmann F, Brüser T, (2004) Localization of the Tat translocon components in Escherichia coli. FEBS Lett 569: 82-88. doi:10.1016/j.febslet.2004.05.054. PubMed: 15225613.
50. Ridder AN, de Jong EJ, Jongbloed JD, Kuipers OP, (2009) Subcellular localization of TatAd of Bacillus subtilis depends on the presence of TatCd or TatCy. J Bacteriol 191: 4410-4418. doi:10.1128/JB.00215-09. PubMed: 19395490.
51. Leake MC, Greene NP, Godun RM, Granjon T, Buchanan G, et al. (2008) Variable stoichiometry of the TatA component of the twin-arginine protein transport system observed by in vivo single-molecule imaging. Proc Natl Acad Sci U S A 105: 15376-15381. doi:10.1073/pnas.0806338105. PubMed: 18832162.
52. Mori H, Cline K, (2002) A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid [Delta]pH/Tat translocase. J Cell Biol 157: 205-210. doi:10.1083/jcb.200202048. PubMed: 11956224.
53. Cline K, Mori H, (2001) Thylakoid DeltapH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J Cell Biol 154: 719-729. doi:10.1083/jcb.200105149. PubMed: 11502764.
54. Renner LD, Weibel DB, (2011) Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes. Proc Natl Acad Sci U S A 108: 6264-6269. doi:10.1073/pnas.1015757108. PubMed: 21444798.
55. Huang KC, Ramamurthi KS, (2010) Macromolecules that prefer their membranes curvy. Mol Microbiol 76: 822-832. doi:10.1111/j.1365-2958.2010.07168.x. PubMed: 20444099.
56. Mikhaleva NI, Santini CL, Giordano G, Nesmeyanova MA, Wu LF, (1999) Requirement for phospholipids of the translocation of the trimethylamine N-oxide reductase through the Tat pathway in Escherichia coli. FEBS Lett 463: 331-335. doi:10.1016/S0014-5793(99)01661-0. PubMed: 10606748.
57. Kleerebezem M, Crielaard W, Tommassen J, (1996) Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the protonmotive force under stress conditions. EMBO J 15: 162-171. PubMed: 8598199.
58. Lo SM, Theg SM, (2012) Role of vesicle-inducing protein in plastids 1 in cpTat transport at the thylakoid. Plant J 71: 656-668. doi:10.1111/j.1365-313X.2012.05020.x. PubMed: 22487220.
59. Vrancken K, De Keersmaeker S, Geukens N, Lammertyn E, Anné J, et al. (2007) pspA overexpression in Streptomyces lividans improves both Sec- and Tat-dependent protein secretion. Appl Microbiol Biotechnol 73: 1150-1157. PubMed: 17106680.
60. DeLisa MP, Lee P, Palmer T, Georgiou G, (2004) Phage shock protein PspA of Escherichia coli relieves saturation of protein export via the Tat pathway. J Bacteriol 186: 366-373. doi:10.1128/JB.186.2.366-373.2004. PubMed: 14702305.
61. Mehner D, Osadnik H, Lünsdorf H, Brüser T, (2012) The Tat system for membrane translocation of folded proteins recruits the membrane-stabilizing Psp machinery in Escherichia coli. J Biol Chem 287: 27834-27842. doi:10.1074/jbc.M112.374983. PubMed: 22689583.
62. Yamaguchi S, Reid DA, Rothenberg E, Darwin AJ, (2013) Changes in Psp protein binding partners, localization and behaviour upon activation of the Yersinia enterocolitica phage shock protein response. Mol Microbiol 87: 656-671. doi:10.1111/mmi.12122. PubMed: 23290031.
63. Alami M, Trescher D, Wu LF, Müller M, (2002) Separate analysis of twin-arginine translocation (Tat)-specific membrane binding and translocation in Escherichia coli. J Biol Chem 277: 20499-20503. doi:10.1074/jbc.M201711200. PubMed: 11923313.
64. Lewis PJ, Marston AL, (1999) GFP vectors for controlled expression and dual labelling of protein fusions in Bacillus subtilis. Gene 227: 101-110. doi:10.1016/S0378-1119(98)00580-0. PubMed: 9931458.
65. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, et al. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567-1572. doi:10.1038/nbt1037. PubMed: 15558047.
66. Casadaban MJ, Cohen SN, (1979) Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci U S A 76: 4530-4533. doi:10.1073/pnas.76.9.4530. PubMed: 159458.
67. Wexler M, Sargent F, Jack RL, Stanley NR, Bogsch EG, et al. (2000) TatD is a cytoplasmic protein with DNase activity. No requirement for TatD family proteins in Sec-independent protein export. J Biol Chem 275: 16717-16722. doi:10.1074/jbc.M000800200. PubMed: 10747959.
68. Bogsch EG, Sargent F, Stanley NR, Berks BC, Robinson C, et al. (1998) An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J Biol Chem 273: 18003-18006. doi:10.1074/jbc.273.29.18003. PubMed: 9660752.