The Tat system of Gram-positive bacteria

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 8, 2014, Pages 1698-1706

  Goosens, Vivianne J ^a   Monteferrante, Carmine G ^a   Van Dijl, Jan Maarten ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Bacillus subtilis; EfeB; PhoD; QcrA; YkuE; YwbN

Indexed keywords

BACTERIAL PROTEIN; SEC PROTEIN; SIGNAL PEPTIDASE; TATA PROTEIN; TATB PROTEIN; TATC PROTEIN; TWIN ARGININE PROTEIN TRANSLOCATION; UNCLASSIFIED DRUG; YIDC PROTEIN;

CELL SURVIVAL; CORYNEBACTERIUM; GRAM POSITIVE BACTERIUM; LIPID BILAYER; MYCOBACTERIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REVIEW; STAPHYLOCOCCUS; STREPTOMYCES;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); POSIBACTERIA;

BACILLUS SUBTILIS; EFEB; PHOD; QCRA; YKUE; YWBN;

ARGININE; BACILLUS SUBTILIS; BACTERIAL TRANSLOCATION; CATION TRANSPORT PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION;

EID: 84902305759     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.10.008     Document Type: Review

References (159)

1. DeLisa M.P., Tullman D., Georgiou G. Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:6115-6120.
2. Panahandeh S., Maurer C., Moser M., DeLisa M.P., Muller M. Following the path of a twin-arginine precursor along the TatABC translocase of Escherichia coli. J. Biol. Chem. 2008, 283:33267-33275.
3. Rocco M.A., Waraho-Zhmayev D., DeLisa M.P. Twin-arginine translocase mutations that suppress folding quality control and permit export of misfolded substrate proteins. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:13392-13397.
4. Maurer C., Panahandeh S., Moser M., Muller M. Impairment of twin-arginine-dependent export by seemingly small alterations of substrate conformation. FEBS Lett. 2009, 583:2849-2853.
5. Hatzixanthis K., Palmer T., Sargent F. A subset of bacterial inner membrane proteins integrated by the twin-arginine translocase. Mol. Microbiol. 2003, 49:1377-1390.
6. Goosens V.J., Otto A., Glasner C., Monteferrante C.C., van der Ploeg R., Hecker M., Becher D., van Dijl J.M. Novel twin-arginine translocation pathway-dependent phenotypes of Bacillus subtilis unveiled by quantitative proteomics. J. Proteome Res. 2013, 12:796-807.
7. Keller R., de Keyzer J., Driessen A.J., Palmer T. Co-operation between different targeting pathways during integration of a membrane protein. J. Cell Biol. 2012, 199:303-315.
8. Gohlke U., Pullan L., McDevitt C.A., Porcelli I., de Leeuw E., Palmer T., Saibil H.R., Berks B.C. The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10482-10486.
9. Barnett J.P., Lawrence J., Mendel S., Robinson C. Expression of the bifunctional Bacillus subtilis TatAd protein in Escherichia coli reveals distinct TatA/B-family and TatB-specific domains. Arch. Microbiol. 2011, 193:583-594.
10. Barnett J.P., Eijlander R.T., Kuipers O.P., Robinson C. A minimal Tat system from a Gram-positive organism: a bifunctional TatA subunit participates in discrete TatAC and TatA complexes. J. Biol. Chem. 2008, 283:2534-2542.
11. Jongbloed J.D., Antelmann H., Hecker M., Nijland R., Bron S., Airaksinen U., Pries F., Quax W.J., van Dijl J.M., Braun P.G. Selective contribution of the twin-arginine translocation pathway to protein secretion in Bacillus subtilis. J. Biol. Chem. 2002, 277:44068-44078.
12. Bogsch E.G., Sargent F., Stanley N.R., Berks B.C., Robinson C., Palmer T. An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J. Biol. Chem. 1998, 273:18003-18006.
13. Bogsch E., Brink S., Robinson C. Pathway specificity for a delta pH-dependent precursor thylakoid lumen protein is governed by a 'Sec-avoidance' motif in the transfer peptide and a 'Sec-incompatible' mature protein. EMBO J. 1997, 16:3851-3859.
14. Kikuchi Y., Itaya H., Date M., Matsui K., Wu L.F. Production of Chryseobacterium proteolyticum protein-glutaminase using the twin-arginine translocation pathway in Corynebacterium glutamicum. Appl. Microbiol. Biotechnol. 2008, 78:67-74.
15. Kikuchi Y., Itaya H., Date M., Matsui K., Wu L.F. TatABC overexpression improves Corynebacterium glutamicum Tat-dependent protein secretion. Appl. Environ. Microbiol. 2009, 75:603-607.
16. Barnett J.P., van der Ploeg R., Eijlander R.T., Nenninger A., Mendel S., Rozeboom R., Kuipers O.P., van Dijl J.M., Robinson C. The twin-arginine translocation (Tat) systems from Bacillus subtilis display a conserved mode of complex organization and similar substrate recognition requirements. FEBS J. 2009, 276:232-243.
17. Scheele S., Oertel D., Bongaerts J., Evers S., Hellmuth H., Maurer K.H., Bott M., Freudl R. Secretory production of an FAD cofactor-containing cytosolic enzyme (sorbitol-xylitol oxidase from Streptomyces coelicolor) using the twin-arginine translocation (Tat) pathway of Corynebacterium glutamicum. Microb. Biotechnol. 2013, 6:202-206.
18. van Bloois E., Winter R.T., Janssen D.B., Fraaije M.W. Export of functional Streptomyces coelicolor alditol oxidase to the periplasm or cell surface of Escherichia coli and its application in whole-cell biocatalysis. Appl. Microbiol. Biotechnol. 2009, 83:679-687.
19. Tjalsma H., Bolhuis A., Jongbloed J.D., Bron S., van Dijl J.M. Signal peptide-dependent protein transport in Bacillus subtilis: a genome-based survey of the secretome. Microbiol. Mol. Biol. Rev. 2000, 64:515-547.
20. Berks B.C. A common export pathway for proteins binding complex redox cofactors?. Mol. Microbiol. 1996, 22:393-404.
21. Cristobal S., de Gier J.W., Nielsen H., von Heijne G. Competition between Sec- and TAT-dependent protein translocation in Escherichia coli. EMBO J. 1999, 18:2982-2990.
22. Robinson C., Matos C.F., Beck D., Ren C., Lawrence J., Vasisht N., Mendel S. Transport and proofreading of proteins by the twin-arginine translocation (Tat) system in bacteria. Biochim. Biophys. Acta 2011, 1808:876-884.
23. Freudl R. Leaving home ain't easy: protein export systems in Gram-positive bacteria. Res. Microbiol. 2013, 64:664-674.
24. Wu L.F., Chanal A., Rodrigue A. Membrane targeting and translocation of bacterial hydrogenases. Arch. Microbiol. 2000, 173:319-324.
25. Rodrigue A., Chanal A., Beck K., Muller M., Wu L.F. Co-translocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial Tat pathway. J. Biol. Chem. 1999, 274:13223-13228.
26. Palmer T., Berks B.C. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 2012, 10:483-496.
27. Whitaker N., Bageshwar U.K., Musser S.M. Kinetics of precursor interactions with the bacterial Tat translocase detected by real-time FRET. J. Biol. Chem. 2012, 287:11252-11260.
28. Bolhuis A., Mathers J.E., Thomas J.D., Barrett C.M., Robinson C. TatB and TatC form a functional and structural unit of the twin-arginine translocase from Escherichia coli. J. Biol. Chem. 2001, 276:20213-20219.
29. Alami M., Luke I., Deitermann S., Eisner G., Koch H.G., Brunner J., Muller M. Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol. Cell 2003, 12:937-946.
30. Cline K., Mori H. Thylakoid DeltapH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J. Cell Biol. 2001, 154:719-729.
31. Rollauer S.E., Tarry M.J., Graham J.E., Jaaskelainen M., Jager F., Johnson S., Krehenbrink M., Liu S.M., Lukey M.J., Marcoux J., McDowell M.A., Rodriguez F., Roversi P., Stansfeld P.J., Robinson C.V., Sansom M.S., Palmer T., Hogbom M., Berks B.C., Lea S.M. Structure of the TatC core of the twin-arginine protein transport system. Nature 2012, 492:210-214.
32. Papish A.L., Ladner C.L., Turner R.J. The twin-arginine leader-binding protein, DmsD, interacts with the TatB and TatC subunits of the Escherichia coli twin-arginine translocase. J. Biol. Chem. 2003, 278:32501-32506.
33. Frobel J., Rose P., Lausberg F., Blummel A.S., Freudl R., Muller M. Transmembrane insertion of twin-arginine signal peptides is driven by TatC and regulated by TatB. Nat. Commun. 2012, 3:1311.
34. Mori H., Cline K. A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid [Delta]pH/Tat translocase. J. Cell Biol. 2002, 157:205-210.
35. Dabney-Smith C., Mori H., Cline K. Oligomers of Tha4 organize at the thylakoid Tat translocase during protein transport. J. Biol. Chem. 2006, 281:5476-5483.
36. Wu L.F., Ize B., Chanal A., Quentin Y., Fichant G. Bacterial twin-arginine signal peptide-dependent protein translocation pathway: evolution and mechanism. J. Mol. Microbiol. Biotechnol. 2000, 2:179-189.
37. Yen M.R., Tseng Y.H., Nguyen E.H., Wu L.F., Saier M.H. Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system. Arch. Microbiol. 2002, 177. (441647 450).
38. Sargent F., Bogsch E.G., Stanley N.R., Wexler M., Robinson C., Berks B.C., Palmer T. Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 1998, 17:3640-3650.
39. Robinson C., Bolhuis A. Tat-dependent protein targeting in prokaryotes and chloroplasts. Biochim. Biophys. Acta 2004, 1694:135-147.
40. Biswas L., Biswas R., Nerz C., Ohlsen K., Schlag M., Schafer T., Lamkemeyer T., Ziebandt A.K., Hantke K., Rosenstein R., Gotz F. Role of the twin-arginine translocation pathway in Staphylococcus. J. Bacteriol. 2009, 191:5921-5929.
41. Yamada K., Sanzen I., Ohkura T., Okamoto A., Torii K., Hasegawa T., Ohta M. Analysis of twin-arginine translocation pathway homologue in Staphylococcus aureus. Curr. Microbiol. 2007, 55:14-19.
42. Jongbloed J.D., van der Ploeg R., van Dijl J.M. Bifunctional TatA subunits in minimal Tat protein translocases. Trends Microbiol. 2006, 14:2-4.
43. Kikuchi Y., Date M., Itaya H., Matsui K., Wu L.F. Functional analysis of the twin-arginine translocation pathway in Corynebacterium glutamicum ATCC 13869. Appl. Environ. Microbiol. 2006, 72:7183-7192.
44. Allen S.C., Barrett C.M., Ray N., Robinson C. Essential cytoplasmic domains in the Escherichia coli TatC protein. J. Biol. Chem. 2002, 277:10362-10366.
45. Buchanan G., de Leeuw E., Stanley N.R., Wexler M., Berks B.C., Sargent F., Palmer T. Functional complexity of the twin-arginine translocase TatC component revealed by site-directed mutagenesis. Mol. Microbiol. 2002, 43:1457-1470.
46. Zoufaly S., Frobel J., Rose P., Flecken T., Maurer C., Moser M., Muller M. Mapping precursor-binding site on TatC subunit of twin arginine-specific protein translocase by site-specific photo cross-linking. J. Biol. Chem. 2012, 287:13430-13441.
47. Ma X., Cline K. Mapping the signal peptide binding and oligomer contact sites of the core subunit of the pea twin arginine protein translocase. Plant Cell 2013, 25:999-1015.
48. Strauch E.M., Georgiou G. Escherichia coli TatC mutations that suppress defective twin-arginine transporter signal peptides. J. Mol. Biol. 2007, 374:283-291.
49. Holzapfel E., Eisner G., Alami M., Barrett C.M., Buchanan G., Luke I., Betton J.M., Robinson C., Palmer T., Moser M., Muller M. The entire N-terminal half of TatC is involved in twin-arginine precursor binding. Biochemistry 2007, 46:2892-2898.
50. McDevitt C.A., Buchanan G., Sargent F., Palmer T., Berks B.C. Subunit composition and in vivo substrate-binding characteristics of Escherichia coli Tat protein complexes expressed at native levels. FEBS J. 2006, 273:5656-5668.
51. Behrendt J., Standar K., Lindenstrauss U., Bruser T. Topological studies on the twin-arginine translocase component TatC. FEMS Microbiol. Lett. 2004, 234:303-308.
52. Eijlander R.T., Kolbusz M.A., Berendsen E.M., Kuipers O.P. Effects of altered TatC proteins on protein secretion efficiency via the twin-arginine translocation pathway of Bacillus subtilis. Microbiology 2009, 155:1776-1785.
53. Schreiber S., Stengel R., Westermann M., Volkmer-Engert R., Pop O.I., Muller J.P. Affinity of TatCd for TatAd elucidates its receptor function in the Bacillus subtilis twin arginine translocation (Tat) translocase system. J. Biol. Chem. 2006, 281:19977-19984.
54. Punginelli C., Maldonado B., Grahl S., Jack R., Alami M., Schroder J., Berks B.C., Palmer T. Cysteine scanning mutagenesis and topological mapping of the Escherichia coli twin-arginine translocase TatC component. J. Bacteriol. 2007, 189:5482-5494.
55. Kneuper H., Maldonado B., Jager F., Krehenbrink M., Buchanan G., Keller R., Muller M., Berks B.C., Palmer T. Molecular dissection of TatC defines critical regions essential for protein transport and a TatB-TatC contact site. Mol. Microbiol. 2012, 85:945-961.
56. Jongbloed J.D., Grieger U., Antelmann H., Hecker M., Nijland R., Bron S., van Dijl J.M. Two minimal Tat translocases in Bacillus. Mol. Microbiol. 2004, 54:1319-1325.
57. Baglieri J., Beck D., Vasisht N., Smith C.J., Robinson C. Structure of TatA paralog, TatE, suggests a structurally homogeneous form of Tat protein translocase that transports folded proteins of differing diameter. J. Biol. Chem. 2012, 287:7335-7344.
58. Sargent F., Stanley N.R., Berks B.C., Palmer T. Sec-independent protein translocation in Escherichia coli. A distinct and pivotal role for the TatB protein. J. Biol. Chem. 1999, 274. (36073703 36082).
59. Orriss G.L., Tarry M.J., Ize B., Sargent F., Lea S.M., Palmer T., Berks B.C. TatBC, TatB, and TatC form structurally autonomous units within the twin arginine protein transport system of Escherichia coli. FEBS Lett. 2007, 581:4091-4097.
60. Hicks M.G., de Leeuw E., Porcelli I., Buchanan G., Berks B.C., Palmer T. The Escherichia coli twin-arginine translocase: conserved residues of TatA and TatB family components involved in protein transport. FEBS Lett. 2003, 539:61-67.
61. Barrett C.M., Freudl R., Robinson C. 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. 2007, 282:36206-36213.
62. Blaudeck N., Kreutzenbeck P., Muller M., Sprenger G.A., Freudl R. 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. 2005, 280:3426-3432.
63. Lee P.A., Buchanan G., Stanley N.R., Berks B.C., Palmer T. Truncation analysis of TatA and TatB defines the minimal functional units required for protein translocation. J. Bacteriol. 2002, 184:5871-5879.
64. Hu Y., Zhao E., Li H., Xia B., Jin C. Solution NMR structure of the TatA component of the twin-arginine protein transport system from Gram-positive bacterium Bacillus subtilis. J. Am. Chem. Soc. 2010, 132:15942-15944.
65. Muller S.D., De Angelis A.A., Walther T.H., Grage S.L., Lange C., Opella S.J., Ulrich A.S. Structural characterization of the pore forming protein TatAd of the twin-arginine translocase in membranes by solid-state 15N-NMR. Biochim. Biophys. Acta 2007, 1768:3071-3079.
66. Lange C., Muller S.D., Walther T.H., Burck J., Ulrich A.S. Structure analysis of the protein translocating channel TatA in membranes using a multi-construct approach. Biochim. Biophys. Acta 2007, 1768:2627-2634.
67. Walther T.H., Gottselig C., Grage S.L., Wolf M., Vargiu A.V., Klein M.J., Vollmer S., Prock S., Hartmann M., Afonin S., Stockwald E., Heinzmann H., Nolandt O.V., Wenzel W., Ruggerone P., Ulrich A.S. Folding and self-assembly of the TatA translocation pore based on a charge zipper mechanism. Cell 2013, 152:316-326.
68. Greene N.P., Porcelli I., Buchanan G., Hicks M.G., Schermann S.M., Palmer T., Berks B.C. Cysteine scanning mutagenesis and disulfide mapping studies of the TatA component of the bacterial twin arginine translocase. J. Biol. Chem. 2007, 282:23937-23945.
69. van der Ploeg R., Barnett J.P., Vasisht N., Goosens V.J., Pother D.C., Robinson C., van Dijl J.M. Salt sensitivity of minimal twin arginine translocases. J. Biol. Chem. 2011, 286:43759-43770.
70. Barrett C.M., Mangels D., Robinson C. Mutations in subunits of the Escherichia coli twin-arginine translocase block function via differing effects on translocation activity or Tat complex structure. J. Mol. Biol. 2005, 347:453-463.
71. Barrett C.M., Mathers J.E., Robinson C. Identification of key regions within the Escherichia coli TatAB subunits. FEBS Lett. 2003, 537:42-46.
72. Hicks M.G., Lee P.A., Georgiou G., Berks B.C., Palmer T. Positive selection for loss-of-function Tat mutations identifies critical residues required for TatA activity. J. Bacteriol. 2005, 187. (2920747 2925).
73. Oates J., Barrett C.M., Barnett J.P., Byrne K.G., Bolhuis A., Robinson C. The Escherichia coli twin-arginine translocation apparatus incorporates a distinct form of TatABC complex, spectrum of modular TatA complexes and minor TatAB complex. J. Mol. Biol. 2005, 346:295-305.
74. Beck D., Vasisht N., Baglieri J., Monteferrante C.G., van Dijl J.M., Robinson C., Smith C.J. Ultrastructural characterisation of Bacillus subtilis TatA complexes suggests they are too small to form homooligomeric translocation pores. Biochim. Biophys. Acta 2013, 1833:1811-1819.
75. Monteferrante C.G., Baglieri J., Robinson C., van Dijl J.M. The third TatA subunit TatAc of Bacillus subtilis can form active twin-arginine translocases with the TatCd and TatCy subunits. Appl. Environ. Microbiol. 2012, 78:4999-5001.
76. Kolkman M.A., van der Ploeg R., Bertels M., van Dijk M., van der Laan J., van Dijl J.M., Ferrari E. The twin-arginine signal peptide of Bacillus subtilis YwbN can direct either Tat- or Sec-dependent secretion of different cargo proteins: secretion of active subtilisin via the B. subtilis Tat pathway. Appl. Environ. Microbiol. 2008, 74:7507-7513.
77. Matos C.F., Robinson C., Di Cola A. The Tat system proofreads FeS protein substrates and directly initiates the disposal of rejected molecules. EMBO J. 2008, 27:2055-2063.
78. Jack R.L., Buchanan G., Dubini A., Hatzixanthis K., Palmer T., Sargent F. Coordinating assembly and export of complex bacterial proteins. EMBO J. 2004, 23:3962-3972.
79. Tottey S., Waldron K.J., Firbank S.J., Reale B., Bessant C., Sato K., Cheek T.R., Gray J., Banfield M.J., Dennison C., Robinson N.J. Protein-folding location can regulate manganese-binding versus copper- or zinc-binding. Nature 2008, 455:1138-1142.
80. Monteferrante C.G., Miethke M., van der Ploeg R., Glasner C., van Dijl J.M. Specific targeting of the metallophosphoesterase YkuE to the Bacillus cell wall requires the twin-arginine translocation system. J. Biol. Chem. 2012, 287:29789-29800.
81. Buchanan G., Maillard J., Nabuurs S.B., Richardson D.J., Palmer T., Sargent F. Features of a twin-arginine signal peptide required for recognition by a Tat proofreading chaperone. FEBS Lett. 2008, 582:3979-3984.
82. Ribnicky B., Van Blarcom T., Georgiou G. A scFv antibody mutant isolated in a genetic screen for improved export via the twin arginine transporter pathway exhibits faster folding. J. Mol. Biol. 2007, 369:631-639.
83. Kim J.Y., Fogarty E.A., Lu F.J., Zhu H., Wheelock G.D., Henderson L.A., DeLisa M.P. Twin-arginine translocation of active human tissue plasminogen activator in Escherichia coli. Appl. Environ. Microbiol. 2005, 71:8451-8459.
84. Oresnik I.J., Ladner C.L., Turner R.J. Identification of a twin-arginine leader-binding protein. Mol. Microbiol. 2001, 40:323-331.
85. Ray N., Oates J., Turner R.J., Robinson C. DmsD is required for the biogenesis of DMSO reductase in Escherichia coli but not for the interaction of the DmsA signal peptide with the Tat apparatus. FEBS Lett. 2003, 534:156-160.
86. Monteferrante C.G., Mackichan C., Marchadier E., Prejean M.V., Carballido-Lopez R., van Dijl J.M. Mapping the twin-arginine protein translocation network of Bacillus subtilis. Proteomics 2013, 13:800-811.
87. Hoff K.G., Silberg J.J., Vickery L.E. Interaction of the iron-sulfur cluster assembly protein IscU with the Hsc66/Hsc20 molecular chaperone system of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:7790-7795.
88. Homuth G., Masuda S., Mogk A., Kobayashi Y., Schumann W. The dnaK operon of Bacillus subtilis is heptacistronic. J. Bacteriol. 1997, 179:1153-1164.
89. Leake M.C., Greene N.P., Godun R.M., Granjon T., Buchanan G., Chen S., Berry R.M., Palmer T., Berks B.C. 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. 2008, 105:15376-15381.
90. Wexler M., Sargent F., Jack R.L., Stanley N.R., Bogsch E.G., Robinson C., Berks B.C., Palmer T. TatD is a cytoplasmic protein with DNase activity. No requirement for TatD family proteins in Sec-independent protein export. J. Biol. Chem. 2000, 275:16717-16722.
91. Ridder A.N., de Jong E.J., Jongbloed J.D., Kuipers O.P. Subcellular localization of TatAd of Bacillus subtilis depends on the presence of TatCd or TatCy. J. Bacteriol. 2009, 191:4410-4418.
92. Pop O.I., Westermann M., Volkmer-Engert R., Schulz D., Lemke C., Schreiber S., Gerlach R., Wetzker R., Muller J.P. Sequence-specific binding of prePhoD to soluble TatAd indicates protein-mediated targeting of the Tat export in Bacillus subtilis. J. Biol. Chem. 2003, 278:38428-38436.
93. Westermann M., Pop O.I., Gerlach R., Appel T.R., Schlormann W., Schreiber S., Muller J.P. The TatAd component of the Bacillus subtilis twin-arginine protein transport system forms homo-multimeric complexes in its cytosolic and membrane embedded localisation. Biochim. Biophys. Acta 2006, 1758:443-451.
94. De Keersmaeker S., Van Mellaert L., Lammertyn E., Vrancken K., Anne J., Geukens N. Functional analysis of TatA and TatB in Streptomyces lividans. Biochem. Biophys. Res. Commun. 2005, 335:973-982.
95. De Keersmaeker S., Van Mellaert L., Schaerlaekens K., Van Dessel W., Vrancken K., Lammertyn E., Anne J., Geukens N. Structural organization of the twin-arginine translocation system in Streptomyces lividans. FEBS Lett. 2005, 579:797-802.
96. De Keersmaeker S., Vrancken K., Van Mellaert L., Anne J., Geukens N. The Tat pathway in Streptomyces lividans: interaction of Tat subunits and their role in translocation. Microbiology 2007, 153:1087-1094.
97. Berthelmann F., Mehner D., Richter S., Lindenstrauss U., Lunsdorf H., Hause G., Bruser T. Recombinant expression of tatABC and tatAC results in the formation of interacting cytoplasmic TatA tubes in Escherichia coli. J. Biol. Chem. 2008, 283:25281-25289.
98. De Keersmaeker S., Vrancken K., Van Mellaert L., Lammertyn E., Anne J., Geukens N. Evaluation of TatABC overproduction on Tat- and Sec-dependent protein secretion in Streptomyces lividans. Arch. Microbiol. 2006, 186:507-512.
99. Schaerlaekens K., Lammertyn E., Geukens N., De Keersmaeker S., Anne J., Van Mellaert L. Comparison of the Sec and Tat secretion pathways for heterologous protein production by Streptomyces lividans. J. Biotechnol. 2004, 112:279-288.
100. Dalbey R.E., Wang P., van Dijl J.M. Membrane proteases in the bacterial protein secretion and quality control pathway. Microbiol. Mol. Biol. Rev. 2012, 76:311-330.
101. Luke I., Handford J.I., Palmer T., Sargent F. Proteolytic processing of Escherichia coli twin-arginine signal peptides by LepB. Arch. Microbiol. 2009, 191:919-925.
102. Molik S., Karnauchov I., Weidlich C., Herrmann R.G., Klosgen R.B. The Rieske Fe/S protein of the cytochrome b6/f complex in chloroplasts: missing link in the evolution of protein transport pathways in chloroplasts?. J. Biol. Chem. 2001, 276:42761-42766.
103. De Buck E., Vranckx L., Meyen E., Maes L., Vandersmissen L., Anne J., Lammertyn E. The twin-arginine translocation pathway is necessary for correct membrane insertion of the Rieske Fe/S protein in Legionella pneumophila. FEBS Lett. 2007, 581:259-264.
104. Bachmann J., Bauer B., Zwicker K., Ludwig B., Anderka O. The Rieske protein from Paracoccus denitrificans is inserted into the cytoplasmic membrane by the twin-arginine translocase. FEBS J. 2006, 273:4817-4830.
105. Hirose I., Sano K., Shioda I., Kumano M., Nakamura K., Yamane K. Proteome analysis of Bacillus subtilis extracellular proteins: a two-dimensional protein electrophoretic study. Microbiology 2000, 146(Pt 1):65-75.
106. Antelmann H., Tjalsma H., Voigt B., Ohlmeier S., Bron S., van Dijl J.M., Hecker M. A proteomic view on genome-based signal peptide predictions. Genome Res. 2001, 11:1484-1502.
107. Bolhuis A., Tjalsma H., Stephenson K., Harwood C.R., Venema G., Bron S., van Dijl J.M. Different mechanisms for thermal inactivation of Bacillus subtilis signal peptidase mutants. J. Biol. Chem. 1999, 274:15865-15868.
108. Sarvas M., Harwood C.R., Bron S., van Dijl J.M. Post-translocational folding of secretory proteins in Gram-positive bacteria. Biochim. Biophys. Acta 2004, 1694:311-327.
109. Krishnappa L., Monteferrante C.G., van Dijl J.M. Degradation of the twin-arginine translocation substrate YwbN by extracytoplasmic proteases of Bacillus subtilis. Appl. Environ. Microbiol. 2012, 78:7801-7804.
110. Desvaux M., Hebraud M., Talon R., Henderson I.R. Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. Trends Microbiol. 2009, 17:139-145.
111. Hoffmann C., Leis A., Niederweis M., Plitzko J.M., Engelhardt H. Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:3963-3967.
112. Marchand C.H., Salmeron C., Bou Raad R., Meniche X., Chami M., Masi M., Blanot D., Daffe M., Tropis M., Huc E., Le Marechal P., Decottignies P., Bayan N. Biochemical disclosure of the mycolate outer membrane of Corynebacterium glutamicum. J. Bacteriol. 2012, 194:587-597.
113. van Dijl J.M., Braun P.G., Robinson C., Quax W.J., Antelmann H., Hecker M., Muller J., Tjalsma H., Bron S., Jongbloed J.D. Functional genomic analysis of the Bacillus subtilis Tat pathway for protein secretion. J. Biotechnol. 2002, 98:243-254.
114. Graumann P. Bacillus: Cellular and Molecular Biology 2007, Caister Academic Press, Norfold, United Kingdom. First Ed.
115. Buescher J.M., Liebermeister W., Jules M., Uhr M., Muntel J., Botella E., Hessling B., Kleijn R.J., Le Chat L., Lecointe F., Mader U., Nicolas P., Piersma S., Rugheimer F., Becher D., Bessieres P., Bidnenko E., Denham E.L., Dervyn E., Devine K.M., Doherty G., Drulhe S., Felicori L., Fogg M.J., Goelzer A., Hansen A., Harwood C.R., Hecker M., Hubner S., Hultschig C., Jarmer H., Klipp E., Leduc A., Lewis P., Molina F., Noirot P., Peres S., Pigeonneau N., Pohl S., Rasmussen S., Rinn B., Schaffer M., Schnidder J., Schwikowski B., Van Dijl J.M., Veiga P., Walsh S., Wilkinson A.J., Stelling J., Aymerich S., Sauer U. Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism. Science 2012, 335:1099-1103.
116. Nicolas P., Mader U., Dervyn E., Rochat T., Leduc A., Pigeonneau N., Bidnenko E., Marchadier E., Hoebeke M., Aymerich S., Becher D., Bisicchia P., Botella E., Delumeau O., Doherty G., Denham E.L., Fogg M.J., Fromion V., Goelzer A., Hansen A., Hartig E., Harwood C.R., Homuth G., Jarmer H., Jules M., Klipp E., Le Chat L., Lecointe F., Lewis P., Liebermeister W., March A., Mars R.A., Nannapaneni P., Noone D., Pohl S., Rinn B., Rugheimer F., Sappa P.K., Samson F., Schaffer M., Schwikowski B., Steil L., Stulke J., Wiegert T., Devine K.M., Wilkinson A.J., van Dijl J.M., Hecker M., Volker U., Bessieres P., Noirot P. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 2012, 335:1103-1106.
117. Jongbloed J.D., Martin U., Antelmann H., Hecker M., Tjalsma H., Venema G., Bron S., van Dijl J.M., Muller J. TatC is a specificity determinant for protein secretion via the twin-arginine translocation pathway. J. Biol. Chem. 2000, 275:41350-41357.
118. Eder S., Shi L., Jensen K., Yamane K., Hulett F.M. A Bacillus subtilis secreted phosphodiesterase/alkaline phosphatase is the product of a Pho regulon gene, phoD. Microbiology 1996, 142(Pt 8):2041-2047.
119. Link T.A., Saynovits M., Assmann C., Iwata S., Ohnishi T., von Jagow G. Isolation, characterisation and crystallisation of a water-soluble fragment of the Rieske iron-sulfur protein of bovine heart mitochondrial bc1 complex. Eur. J. Biochem. 1996, 237:71-75.
120. Iwata S., Saynovits M., Link T.A., Michel H. Structure of a water soluble fragment of the 'Rieske' iron-sulfur protein of the bovine heart mitochondrial cytochrome bc1 complex determined by MAD phasing at 1.5 A resolution. Structure 1996, 4:567-579.
121. Schneider D., Schmidt C.L. Multiple Rieske proteins in prokaryotes: where and why?. Biochim. Biophys. Acta 2005, 1710:1-12.
122. Schmidt C.L., Shaw L. A comprehensive phylogenetic analysis of Rieske and Rieske-type iron-sulfur proteins. J. Bioenerg. Biomembr. 2001, 33:9-26.
123. Hunsicker-Wang L.M., Heine A., Chen Y., Luna E.P., Todaro T., Zhang Y.M., Williams P.A., McRee D.E., Hirst J., Stout C.D., Fee J.A. High-resolution structure of the soluble, respiratory-type Rieske protein from Thermus thermophilus: analysis and comparison. Biochemistry 2003, 42. (7303900 7317).
124. Eijlander R.T., Jongbloed J.D., Kuipers O.P. Relaxed specificity of the Bacillus subtilis TatAdCd translocase in Tat-dependent protein secretion. J. Bacteriol. 2009, 191:196-202.
125. van der Ploeg R., Monteferrante C.G., Piersma S., Barnett J.P., Kouwen T.R., Robinson C., van Dijl J.M. High-salinity growth conditions promote Tat-independent secretion of Tat substrates in Bacillus subtilis. Appl. Environ. Microbiol. 2012, 78:7733-7744.
126. Monteferrante C.G., Baglieri J., Robinson C., van Dijl J.M. TatAc, the third TatA subunit of Bacillus subtilis, can form active twin-arginine translocases with the TatCd and TatCy subunits. Appl. Environ. Microbiol. 2012, 78:4999-5001.
127. Miethke M., Monteferrante C.G., Marahiel M.A., van Dijl J.M. The Bacillus subtilis EfeUOB transporter is essential for high-affinity acquisition of ferrous and ferric iron. Biochim. Biophys. Acta 2013, 1833:2267-2278.
128. van der Ploeg R., Mader U., Homuth G., Schaffer M., Denham E.L., Monteferrante C.G., Miethke M., Marahiel M.A., Harwood C.R., Winter T., Hecker M., Antelmann H., van Dijl J.M. Environmental salinity determines the specificity and need for Tat-dependent secretion of the YwbN protein in Bacillus subtilis. PLoS One 2011, 6:e18140.
129. Anne J., Maldonado B., Van Impe J., Van Mellaert L., Bernaerts K. Recombinant protein production and streptomycetes. J. Biotechnol. 2012, 158:159-167.
130. Widdick D.A., Dilks K., Chandra G., Bottrill A., Naldrett M., Pohlschroder M., Palmer T. The twin-arginine translocation pathway is a major route of protein export in Streptomyces coelicolor. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:17927-17932.
131. Schaerlaekens K., Van Mellaert L., Lammertyn E., Geukens N., Anne J. The importance of the Tat-dependent protein secretion pathway in Streptomyces as revealed by phenotypic changes in Tat deletion mutants and genome analysis. Microbiology 2004, 150:21-31.
132. Joshi M.V., Mann S.G., Antelmann H., Widdick D.A., Fyans J.K., Chandra G., Hutchings M.I., Toth I., Hecker M., Loria R., Palmer T. The twin arginine protein transport pathway exports multiple virulence proteins in the plant pathogen Streptomyces scabies. Mol. Microbiol. 2010, 77:252-271.
133. Schaerlaekens K., Schierova M., Lammertyn E., Geukens N., Anne J., Van Mellaert L. Twin-arginine translocation pathway in Streptomyces lividans. J. Bacteriol. 2001, 183:6727-6732.
134. Vrancken K., De Keersmaeker S., Geukens N., Lammertyn E., Anne J., Van Mellaert L. pspA overexpression in Streptomyces lividans improves both Sec- and Tat-dependent protein secretion. Appl. Microbiol. Biotechnol. 2007, 73:1150-1157.
135. DeLisa M.P., Lee P., Palmer T., Georgiou G. Phage shock protein PspA of Escherichia coli relieves saturation of protein export via the Tat pathway. J. Bacteriol. 2004, 186:366-373.
136. Kobayashi R., Suzuki T., Yoshida M. Escherichia coli phage-shock protein A (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes. Mol. Microbiol. 2007, 66:100-109.
137. Mehner D., Osadnik H., Lunsdorf H., Bruser T. The Tat system for membrane translocation of folded proteins recruits the membrane-stabilizing Psp machinery in Escherichia coli. J. Biol. Chem. 2012, 287:27834-27842.
138. Vrancken K., Van Mellaert L., Anne J. Characterization of the Streptomyces lividans PspA response. J. Bacteriol. 2008, 190:3475-3481.
139. Darwin A.J. The phage-shock-protein response. Mol. Microbiol. 2005, 57:621-628.
140. Meissner D., Vollstedt A., van Dijl J.M., Freudl R. Comparative analysis of twin-arginine (Tat)-dependent protein secretion of a heterologous model protein (GFP) in three different Gram-positive bacteria. Appl. Microbiol. Biotechnol. 2007, 76:633-642.
141. Zuber B., Chami M., Houssin C., Dubochet J., Griffiths G., Daffe M. Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 2008, 190:5672-5680.
142. Crellin P.K., Luo C.Y., Morita Y.S. Metabolism of plasma membrane lipids in mycobacteria and corynebacteria. Lipid Metabolism 2013, Intech, Online. R. Valenzuela Baez (Ed.).
143. Hermann T. Industrial production of amino acids by coryneform bacteria. J. Biotechnol. 2003, 104:155-172.
144. Ikeda M., Nakagawa S. The Corynebacterium glutamicum genome: features and impacts on biotechnological processes. Appl. Microbiol. Biotechnol. 2003, 62:99-109.
145. Kalinowski J., Bathe B., Bartels D., Bischoff N., Bott M., Burkovski A., Dusch N., Eggeling L., Eikmanns B.J., Gaigalat L., Goesmann A., Hartmann M., Huthmacher K., Kramer R., Linke B., McHardy A.C., Meyer F., Mockel B., Pfefferle W., Puhler A., Rey D.A., Ruckert C., Rupp O., Sahm H., Wendisch V.F., Wiegrabe I., Tauch A. The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of L-aspartate-derived amino acids and vitamins. J. Biotechnol. 2003, 104:5-25.
146. Nishio Y., Nakamura Y., Kawarabayasi Y., Usuda Y., Kimura E., Sugimoto S., Matsui K., Yamagishi A., Kikuchi H., Ikeo K., Gojobori T. Comparative complete genome sequence analysis of the amino acid replacements responsible for the thermostability of Corynebacterium efficiens. Genome Res. 2003, 13:1572-1579.
147. WHO Global Tuberculosis Report 2012 2012.
148. Posey J.E., Shinnick T.M., Quinn F.D. Characterization of the twin-arginine translocase secretion system of Mycobacterium smegmatis. J. Bacteriol. 2006, 188:1332-1340.
149. Saint-Joanis B., Demangel C., Jackson M., Brodin P., Marsollier L., Boshoff H., Cole S.T. Inactivation of Rv2525c, a substrate of the twin arginine translocation (Tat) system of Mycobacterium tuberculosis, increases beta-lactam susceptibility and virulence. J. Bacteriol. 2006, 188:6669-6679.
150. Pickering B.S., Oresnik I.J. The twin arginine transport system appears to be essential for viability in Sinorhizobium meliloti. J. Bacteriol. 2010, 192:5173-5180.
151. McDonough J.A., Hacker K.E., Flores A.R., Pavelka M.S., Braunstein M. The twin-arginine translocation pathway of Mycobacterium smegmatis is functional and required for the export of mycobacterial beta-lactamases. J. Bacteriol. 2005, 187:7667-7679.
152. Ligon L.S., Hayden J.D., Braunstein M. The ins and outs of Mycobacterium tuberculosis protein export. Tuberculosis (Edinb) 2012, 92:121-132.
153. Raynaud C., Guilhot C., Rauzier J., Bordat Y., Pelicic V., Manganelli R., Smith I., Gicquel B., Jackson M. Phospholipases C are involved in the virulence of Mycobacterium tuberculosis. Mol. Microbiol. 2002, 45:203-217.
154. Vasil M.L., Tomaras A.P., Pritchard A.E. Identification and evaluation of twin-arginine translocase inhibitors. Antimicrob. Agents Chemother. 2012, 56:6223-6234.
155. Chaddock A.M., Mant A., Karnauchov I., Brink S., Herrmann R.G., Klosgen R.B., Robinson C. A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the delta pH-dependent thylakoidal protein translocase. EMBO J. 1995, 14:2715-2722.
156. Robinson C., Cai D., Hulford A., Brock I.W., Michl D., Hazell L., Schmidt I., Herrmann R.G., Klosgen R.B. The presequence of a chimeric construct dictates which of two mechanisms are utilized for translocation across the thylakoid membrane: evidence for the existence of two distinct translocation systems. EMBO J. 1994, 13:279-285.
157. Henry R., Kapazoglou A., McCaffery M., Cline K. Differences between lumen targeting domains of chloroplast transit peptides determine pathway specificity for thylakoid transport. J. Biol. Chem. 1994, 269:10189-10192.
158. Behrendt J., Lindenstrauss U., Bruser T. The TatBC complex formation suppresses a modular TatB-multimerization in Escherichia coli. FEBS Lett. 2007, 581:4085-4090.
159. Richter S., Bruser T. Targeting of unfolded PhoA to the TAT translocon of Escherichia coli. J. Biol. Chem. 2005, 280:42723-42730.