Transport and proofreading of proteins by the twin-arginine translocation (Tat) system in bacteria

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 3, 2011, Pages 876-884

  Robinson, Colin ^a   Matos, Cristina F R O ^a   Beck, Daniel ^a   Ren, Chao ^a   Lawrence, Janna ^a   Vasisht, Nishi ^a   Mendel, Sharon ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; PROTEIN DMSA; PROTEIN DMSD; PROTEIN TATA; PROTEIN TATABC; PROTEIN TATB; PROTEIN TATC; PROTEIN TORD; TWIN ARGININE TRANSLOCATION PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BACTERIUM; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; ENZYME SUBSTRATE; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; QUALITY CONTROL; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; THYLAKOID;

AMINO ACID SEQUENCE; ARGININE; BIOLOGICAL TRANSPORT; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA;

EID: 79851514906     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2010.11.023     Document Type: Review

References (80)

1. J.H. Weiner, P.T. Bilous, G.M. Shaw, S.P. Lubitz, L. Frost, G.H. Thomas, J.A. Cole, and R.J. Turner A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins Cell 93 1998 93 101 (Pubitemid 28173555)
2. F. Sargent, E.G. Bogsch, N.R. Stanley, M. Wexler, C. Robinson, B.C. Berks, and T. Palmer Overlapping functions of components of a bacterial Sec-independent protein export pathway EMBO J. 17 1998 3640 3650 (Pubitemid 28327382)
3. E.G. Bogsch, F. Sargent, N.R. Stanley, B.C. Berks, C. Robinson, and T. Palmer An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria J. Biol. Chem. 273 1998 18003 18006 (Pubitemid 28334711)
4. A.M. Settles, A. Yonetani, A. Baron, D.R. Bush, K. Cline, and R. Martienssen Sec-independent protein translocation by the maize Hcf106 protein Science 278 1997 1467 1470 (Pubitemid 27509820)
5. K. Cline, and H. Mori Thylakoid DeltapH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport J. Cell Biol. 154 2001 719 729 (Pubitemid 34292954)
6. M.B. Walker, L.M. Roy, E. Coleman, R. Voelker, and A. Barkan The maize tha4 gene functions in sec-independent protein transport in chloroplasts and is related to hcf106, tatA, and tatB J. Cell Biol. 147 1999 267 276
7. J.D. Jongbloed, U. Grieger, H. Antelmann, M. Hecker, R. Nijland, S. Bron, and J.M. van Dijl Two minimal Tat translocases in Bacillus Mol. Microbiol. 54 2004 1319 1325 (Pubitemid 39578274)
8. J.P. Barnett, R.T. Eijlander, O.P. Kuipers, and C. Robinson A minimal Tat system from a gram-positive organism: a bifunctional TatA subunit participates in discrete TatAC and TatA complexes J. Biol. Chem. 283 2008 2534 2542
9. C. Lange, S.D. Muller, T.H. Walther, J. Burck, and A.S. Ulrich Structure analysis of the protein translocating channel TatA in membranes using a multi-construct approach Biochim. Biophys. Acta 1768 2007 2627 2634 (Pubitemid 47532040)
10. G.F. White, S.M. Schermann, J. Bradley, A. Roberts, N.P. Greene, B.C. Berks, and A.J. Thomson Subunit organization in the TatA complex of the twin arginine protein translocase: a site-directed EPR spin labeling study J. Biol. Chem. 285 2010 2294 2301
11. S.D. Muller, A.A. De Angelis, T.H. Walther, S.L. Grage, C. Lange, S.J. Opella, and A.S. Ulrich Structural characterization of the pore forming protein TatAd of the twin-arginine translocase in membranes by solid-state 15N-NMR Biochim. Biophys. Acta 1768 2007 3071 3079 (Pubitemid 350236094)
12. C.S. Chan, M.R. Zlomislic, D.P. Tieleman, and R.J. Turner The TatA subunit of Escherichia coli twin-arginine translocase has an N-in topology Biochemistry 46 2007 7396 7404 (Pubitemid 46986366)
13. F. Sargent, N.R. Stanley, B.C. Berks, and T. Palmer Sec-independent protein translocation in Escherichia coli. A distinct and pivotal role for the TatB protein J. Biol. Chem. 274 1999 36073 36082
14. J. Behrendt, K. Standar, U. Lindenstrauss, and T. Bruser Topological studies on the twin-arginine translocase component TatC FEMS Microbiol. Lett. 234 2004 303 308 (Pubitemid 38595647)
15. O.V. Nolandt, T.H. Walther, S. Roth, J. Burck, and A.S. Ulrich Structure analysis of the membrane protein TatC(d) from the Tat system of B. subtilis by circular dichroism Biochim. Biophys. Acta 1788 2009 2238 2244
16. K. Gouffi, C.L. Santini, and L.F. Wu Topology determination and functional analysis of the Escherichia coli TatC protein FEBS Lett. 525 2002 65 70
17. C. Punginelli, B. Maldonado, S. Grahl, R. Jack, M. Alami, J. Schroder, B.C. Berks, and T. Palmer Cysteine scanning mutagenesis and topological mapping of the Escherichia coli twin-arginine translocase TatC Component J. Bacteriol. 189 2007 5482 5494 (Pubitemid 47206393)
18. A. Bolhuis, J.E. Mathers, J.D. Thomas, C.M. Barrett, and C. Robinson TatB and TatC form a functional and structural unit of the twin- arginine translocase from Escherichia coli J. Biol. Chem. 276 2001 20213 20219
19. P.A. Lee, D. Tullman-Ercek, and G. Georgiou The bacterial twin-arginine translocation pathway Annu. Rev. Microbiol. 60 2006 373 395 (Pubitemid 44627954)
20. J. Oates, C.M. Barrett, J.P. Barnett, K.G. Byrne, A. Bolhuis, and C. Robinson 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. 346 2005 295 305 (Pubitemid 40128322)
21. U. Gohlke, L. Pullan, C.A. McDevitt, I. Porcelli, E. de Leeuw, T. Palmer, H.R. Saibil, and B.C. Berks The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter Proc. Natl Acad. Sci. USA 102 2005 10482 10486 (Pubitemid 41061580)
22. G.L. Orriss, M.J. Tarry, B. Ize, F. Sargent, S.M. Lea, T. Palmer, and B.C. Berks TatBC, TatB, and TatC form structurally autonomous units within the twin arginine protein transport system of Escherichia coli FEBS Lett. 581 2007 4091 4097 (Pubitemid 47212116)
23. D. Mangels, J. Mathers, A. Bolhuis, and C. Robinson The core TatABC complex of the twin-arginine translocase in Escherichia coli: TatC drives assembly whereas TatA is essential for stability J. Mol. Biol. 345 2005 415 423 (Pubitemid 39574861)
24. J. Behrendt, U. Lindenstrauss, and T. Bruser The TatBC complex formation suppresses a modular TatB-multimerization in Escherichia coli FEBS Lett. 581 2007 4085 4090 (Pubitemid 47212117)
25. K. Schaerlaekens, M. Schierova, E. Lammertyn, N. Geukens, J. Anne, and L. Van Mellaert Twin-arginine translocation pathway in Streptomyces lividans J. Bacteriol. 183 2001 6727 6732 (Pubitemid 33064183)
26. Y. Yu, E. Zhao, H. Li, B. Xia, C. Jin, 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 (2010) 15942 - 15944.
27. K. Cline, W.F. Ettinger, and S.M. Theg Protein-specific energy requirements for protein transport across or into thylakoid membranes. Two lumenal proteins are transported in the absence of ATP J. Biol. Chem. 267 1992 2688 2696
28. R.B. Klosgen, I.W. Brock, R.G. Herrmann, and C. Robinson Proton gradient-driven import of the 16 kDa oxygen-evolving complex protein as the full precursor protein by isolated thylakoids Plant Mol. Biol. 18 1992 1031 1034
29. R.M. Mould, and C. Robinson A proton gradient is required for the transport of two lumenal oxygen-evolving proteins across the thylakoid membrane J. Biol. Chem. 266 1991 12189 12193
30. M. Alami, I. Luke, S. Deitermann, G. Eisner, H.G. Koch, J. Brunner, and M. Muller Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli Mol. Cell 12 2003 937 946 (Pubitemid 37352786)
31. M.J. Tarry, E. Schaefer, S. Chena, G. Buchanan, N.P. Greene, S.M. Lead, T. Palmer, H.R. Saibil, and B.C. Berks Structural analysis of substrate binding by the TatBC component of the twin-arginine protein transport system Proc. Natl Acad. Sci. 106 2009 13284 13289
32. H. Mori, and K. Cline A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid [Delta]pH/Tat translocase J. Cell Biol. 157 2002 205 210 (Pubitemid 34839817)
33. I. Porcelli, E. de Leeuw, R. Wallis, and E. van den Brink-van Test Characterization and membrane assembly of the TatA component of the Escherichia coli twin-arginine protein transport system Biochemistry 41 2002 13690 13697 (Pubitemid 35332706)
34. B.C. Berks, F. Sargent, and T. Palmer The Tat protein export pathway Mol. Microbiol. 35 2000 260 274 (Pubitemid 30055224)
35. F. Sargent, B.C. Berks, and T. Palmer Assembly of membrane-bound respiratory complexes by the Tat protein-transport system Arch. Microbiol. 178 2002 77 84 (Pubitemid 34762248)
36. F. Gérard, and K. Cline Efficient twin arginine translocation (Tat) pathway transport of a precursor protein covalently anchored to its initial cpTatC binding site J. Biol. Chem. 281 2005 6130 6135 (Pubitemid 43847542)
37. C. Dabney-Smith, H. Mori, and K. Cline Oligomers of Tha4 organize at the thylakoid Tat translocase during protein transport J. Biol. Chem. 281 2005 5476 5483 (Pubitemid 43847642)
38. M. Moser, S. Panahandeh, E. Holzapfel, and M. Muller In vitro analysis of the bacterial twin-arginine-dependent protein export Methods Mol. Biol. 390 2007 63 79 (Pubitemid 350183652)
39. O. Pop, U. Martin, C. Abel, and J.P. Muller The twin-arginine signal peptide of PhoD and the TatAd/Cd proteins of Bacillus subtilis form an autonomous Tat translocation system J. Biol. Chem. 277 2002 3268 3273 (Pubitemid 34953191)
40. J.D. Jongbloed, H. Antelmann, M. Hecker, R. Nijland, S. Bron, U. Airaksinen, F. Pries, W.J. Quax, J.M. van Dijl, and P.G. Braun Selective contribution of the twin-arginine translocation pathway to protein secretion in Bacillus subtilis J. Biol. Chem. 277 2002 44068 44078 (Pubitemid 36157834)
41. J.D. Jongbloed, U. Martin, H. Antelmann, M. Hecker, H. Tjalsma, G. Venema, S. Bron, J.M. van Dijl, and J. Muller TatC is a specificity determinant for protein secretion via the twin-arginine translocation pathway J. Biol. Chem. 275 2000 41350 41357 (Pubitemid 32054969)
42. N. Blaudeck, P. Kreutzenbeck, M. Muller, G.A. Sprenger, and R. Freudl Isolation and characterisation of bifunctional Escherichia coli TatA mutant proteins that allow efficient tat-dependent protein translocation in the absence of TatB J. Biol. Chem. 280 2005 3426 3432 (Pubitemid 40223806)
43. M. Westermann, O.I. Pop, R. Gerlach, T.R. Appel, W. Schlormann, S. Schreiber, and J.P. Muller 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 1758 2006 443 451 (Pubitemid 43767733)
44. O.I. Pop, M. Westermann, R. Volkmer-Engert, D. Schulz, C. Lemke, S. Schreiber, R. Gerlach, R. Wetzker, and J.P. Muller Sequence-specific binding of prePhoD to soluble TatAd indicates protein-mediated targeting of the Tat export in Bacillus subtilis J. Biol. Chem. 278 2003 38428 38436 (Pubitemid 37221736)
45. S. Schreiber, R. Stengel, M. Westermann, R. Volkmer-Engert, O.I. Pop, and J.P. Muller Affinity of TatCd for TatAd elucidates its receptor function in the Bacillus subtilis twin arginine translocation (Tat) translocase system J. Biol. Chem. 281 2006 19977 19984 (Pubitemid 44065771)
46. A.M. Chaddock, A. Mant, I. Karnauchov, S. Brink, R.G. Herrmann, R.B. Klosgen, and C. Robinson 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. 14 1995 2715 2722
47. N.R. Stanley, T. Palmer, and B.C. Berks The twin arginine consensus motif of Tat signal peptides is involved in Sec-independent protein targeting in Escherichia coli J. Biol. Chem. 275 2000 11591 11596 (Pubitemid 30237716)
48. G. Buchanan, F. Sargent, B.C. Berks, and T. Palmer A genetic screen for suppressors of Escherichia coli Tat signal peptide mutations establishes a critical role for the second arginine within the twin-arginine motif Arch. Microbiol. 177 2001 107 112 (Pubitemid 34031241)
49. M.P. DeLisa, P. Samuelson, T. Palmer, and G. Georgiou Genetic analysis of the twin arginine translocator secretion pathway in bacteria J. Biol. Chem. 277 2002 29825 29831
50. S. Mendel, A. McCarthy, J.P. Barnett, R.T. Eijlander, A. Nenninger, O.P. Kuipers, and C. Robinson The Escherichia coli TatABC system and a Bacillus subtilis TatAC-type system recognise three distinct targeting determinants in twin-arginine signal peptides J. Mol. Biol. 375 2008 661 672 (Pubitemid 350297281)
51. B. Ize, F. Gerard, and L.F. Wu In vivo assessment of the Tat signal peptide specificity in Escherichia coli Arch. Microbiol. 178 2002 548 553 (Pubitemid 35340988)
52. C. Sanders, N. Wethkamp, and H. Lill Transport of cytochrome c derivatives by the bacterial Tat protein translocation system Mol. Microbiol. 41 2001 241 246 (Pubitemid 32660999)
53. M.P. DeLisa, D. Tullman, and G. Georgiou Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway Proc. Natl Acad. Sci. USA 100 2003 6115 6120 (Pubitemid 36576940)
54. S. Richter, and T. Bruser Targeting of unfolded PhoA to the TAT translocon of Escherichia coli J. Biol. Chem. 280 2005 42723 42730 (Pubitemid 43049232)
55. H.K. Lim, T.J. Mansell, S.W. Linderman, A.C. Fisher, M.R. Dyson, and M.P. DeLisa Mining mammalian genomes for folding competent proteins using Tat-dependent genetic selection in Escherichia coli Protein Sci. 18 2009 2537 2549
56. S. Richter, U. Lindenstrauss, C. Lucke, R. Bayliss, and T. Bruser Functional Tat transport of unstructured, small, hydrophilic proteins J. Biol. Chem. 282 2007 33257 33264 (Pubitemid 350159532)
57. S. Panahandeh, C. Maurer, M. Moser, M.P. DeLisa, and M. Muller Following the path of a twin-arginine precursor along the TatABC translocase of Escherichia coli J. Biol. Chem. 283 2008 33267 33275
58. C.F. Matos, C. Robinson, and A. Di Cola The Tat system proofreads FeS protein substrates and directly initiates the disposal of rejected molecules EMBO J. 27 2008 2055 2063
59. S.M. Musser, and S.M. Theg Characterization of the early steps of OE17 precursor transport by the thylakoid DeltapH/Tat machinery Eur. J. Biochem. 267 2000 2588 2598 (Pubitemid 30304254)
60. K. Cline, and M. McCaffery Evidence for a dynamic and transient pathway through the TAT protein transport machinery EMBO J. 26 2007 3039 3049 (Pubitemid 47057499)
61. P.J. Hynds, D. Robinson, and C. Robinson The sec-independent twin-arginine translocation system can transport both tightly folded and malfolded proteins across the thylakoid membrane J. Biol. Chem. 273 1998 34868 34874 (Pubitemid 29028181)
62. F. Sargent The twin-arginine transport system: moving folded proteins across membranes Biochem. Soc. Trans. 35 2007 835 847 (Pubitemid 350206379)
63. R.J. Turner, A.L. Papish, and F. Sargent Sequence analysis of bacterial redox enzyme maturation proteins (REMPs) Can. J. Microbiol. 50 2004 225 238 (Pubitemid 38903410)
64. R.L. Jack, G. Buchanan, A. Dubini, K. Hatzixanthis, T. Palmer, and F. Sargent Coordinating assembly and export of complex bacterial proteins EMBO J. 23 2004 3962 3972 (Pubitemid 39472418)
65. L.C. Potter, and J.A. Cole Essential roles for the products of the napABCD genes, but not napFGH, in periplasmic nitrate reduction by Escherichia coli K-12 Biochem. J. 344 Pt 1 1999 69 76
66. I.J. Oresnik, C.L. Ladner, and R.J. Turner Identification of a twin-arginine leader-binding protein Mol. Microbiol. 40 2001 323 331 (Pubitemid 32391628)
67. J.H. Weiner, R.A. Rothery, D. Sambasivarao, and C.A. Trieber Molecular analysis of dimethylsulfoxide reductase: a complex iron-sulfur molybdoenzyme of Escherichia coli Biochim. Biophys. Acta 1102 1992 1 18
68. D. Sambasivarao, R.J. Turner, J.L. Simala-Grant, G. Shaw, J. Hu, and J.H. Weiner Multiple roles for the twin arginine leader sequence of dimethyl sulfoxide reductase of Escherichia coli J. Biol. Chem. 275 2000 22526 22531 (Pubitemid 30621842)
69. A.L. Papish, C.L. Ladner, and R.J. Turner The twin-arginine leader-binding protein, DmsD, interacts with the TatB and TatC subunits of the Escherichia coli twin-arginine translocase J. Biol. Chem. 278 2003 32501 32506 (Pubitemid 37055687)
70. N. Ray, J. Oates, R.J. Turner, and C. Robinson 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. 534 2003 156 160 (Pubitemid 36084534)
71. H. Li, L. Chang, J.M. Howell, and R.J. Turner DmsD, a Tat system specific chaperone, interacts with other general chaperones and proteins involved in the molybdenum cofactor biosynthesis Biochim. Biophys. Acta 1804 2010 1301 1309
72. G. Buchanan, J. Maillard, S.B. Nabuurs, D.J. Richardson, T. Palmer, and F. Sargent Features of a twin-arginine signal peptide required for recognition by a Tat proofreading chaperone FEBS Lett. 582 2008 3979 3984
73. O. Genest, F. Seduk, M. Ilbert, V. Mejean, and C. Iobbi-Nivol Signal peptide protection by specific chaperone Biochem. Biophys. Res. Commun. 339 2006 991 995 (Pubitemid 41772909)
74. M. Ilbert, V. Mejean, M.T. Giudici-Orticoni, J.P. Samama, and C. Iobbi-Nivol Involvement of a mate chaperone (TorD) in the maturation pathway of molybdoenzyme TorA J. Biol. Chem. 278 2003 28787 28792 (Pubitemid 36935788)
75. O. Genest, M. Neumann, F. Seduk, W. Stocklein, V. Mejean, S. Leimkuhler, and C. Iobbi-Nivol Dedicated metallochaperone connects apoenzyme and molybdenum cofactor biosynthesis components J. Biol. Chem. 283 2008 21433 21440
76. D. Guymer, J. Maillard, M.F. Agacan, C.A. Brearley, and F. Sargent Intrinsic GTPase activity of a bacterial twin-arginine translocation proofreading chaperone induced by domain swapping FEBS J. 277 2010 511 525
77. K. Hatzixanthis, T.A. Clarke, A. Oubrie, D.J. Richardson, R.J. Turner, and F. Sargent Signal peptide-chaperone interactions on the twin-arginine protein transport pathway Proc. Natl Acad. Sci. USA 102 2005 8460 8465 (Pubitemid 40862758)
78. C.S. Chan, L. Chang, K.L. Rommens, and R.J. Turner Differential Interactions between Tat-specific redox enzyme peptides and their chaperones J. Bacteriol. 191 2009 2091 2101
79. W. Graubner, A. Schierhorn, and T. Bruser DnaK plays a pivotal role in Tat targeting of CueO and functions beside SlyD as a general Tat signal binding chaperone J. Biol. Chem. 282 2007 7116 7124 (Pubitemid 47093664)
80. A. Sturm, A. Schierhorn, U. Lindenstrauss, H. Lilie, and T. Bruser YcdB from Escherichia coli reveals a novel class of Tat-dependently translocated hemoproteins J. Biol. Chem. 281 2006 13972 13978 (Pubitemid 43848323)