Folding and self-assembly of the TatA translocation pore based on a charge zipper mechanism

Cell

Volumn 152, Issue 1-2, 2013, Pages 316-326

  Walther, Torsten H ^a   Gottselig, Christina ^a   Grage, Stephan L ^a   Wolf, Moritz ^a   Vargiu, Attilio V ^b   Klein, Marco J ^a   Vollmer, Stefanie ^a   Prock, Sebastian ^a   Hartmann, Mareike ^a   Afonin, Sergiy ^a   Stockwald, Eva ^a   Heinzmann, Hartmut ^a   Nolandt, Olga V ^a   Wenzel, Wolfgang ^a   Ruggerone, Paolo ^b   Ulrich, Anne S ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DERMCIDIN; MEMBRANE PROTEIN; MONOMER; OLIGOMER; POLYPEPTIDE ANTIBIOTIC AGENT; TATA PROTEIN; TISB PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SEQUENCE; AMPHIPHILIC HELIX; ARTICLE; BIOFILM; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DENSELY CHARGED REGION; DNA HAIRPIN; LIPID BILAYER; MOLECULAR DYNAMICS; PESTIVIRUS INFECTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN MOTIF; SEQUENCE ALIGNMENT;

EID: 84872579327     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.12.017     Document Type: Article

References (81)

1. N.N. Alder, and S.M. Theg Energetics of protein transport across biological membranes: a study of the thylakoid DeltapH-dependent/cpTat pathway Cell 112 2003 231 242 (Pubitemid 36144112)
2. 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
3. O. Beckstein, E.J. Denning, J.R. Perilla, and T.B. Woolf Zipping and unzipping of adenylate kinase: atomistic insights into the ensemble of open< - >closed transitions J. Mol. Biol. 394 2009 160 176
4. B.C. Berks, T. Palmer, and F. Sargent Protein targeting by the bacterial twin-arginine translocation (Tat) pathway Curr. Opin. Microbiol. 8 2005 174 181 (Pubitemid 40417959)
5. B.C. Berks, F. Sargent, and T. Palmer The Tat protein export pathway Mol. Microbiol. 35 2000 260 274 (Pubitemid 30055224)
6. F. Berthelmann, D. Mehner, S. Richter, U. Lindenstrauss, H. Lünsdorf, G. Hause, and T. Brüser Recombinant expression of tatABC and tatAC results in the formation of interacting cytoplasmic TatA tubes in Escherichia coli J. Biol. Chem. 283 2008 25281 25289
7. M. Bonomi, D. Branduardi, G. Bussi, C. Camilloni, D. Provasi, P. Raiteri, D. Donadio, F. Marinelli, F. Pietrucci, and R.A. Broglia PLUMED: A portable plugin for free-energy calculations with molecular dynamics Comput. Phys. Commun. 180 2009 1961 1972
8. T. Brüser, and C. Sanders An alternative model of the twin arginine translocation system Microbiol. Res. 158 2003 7 17 (Pubitemid 36219354)
9. S. Burrack, D. Aberle, J. Bürck, A.S. Ulrich, and G. Meyers A new type of intracellular retention signal identified in a pestivirus structural glycoprotein FASEB J. 26 2012 3292 3305
10. D.A. Case, T.E. Cheatham 3rd, T. Darden, H. Gohlke, R. Luo, K.M. Merz Jr.; A. Onufriev, C. Simmerling, B. Wang, and R.J. Woods The Amber biomolecular simulation programs J. Comput. Chem. 26 2005 1668 1688 (Pubitemid 43076180)
11. 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)
12. C. Dabney-Smith, H. Mori, and K. Cline Requirement of a Tha4-conserved transmembrane glutamate in thylakoid Tat translocase assembly revealed by biochemical complementation J. Biol. Chem. 278 2003 43027 43033 (Pubitemid 37345917)
13. C. Dabney-Smith, H. Mori, and K. Cline Oligomers of Tha4 organize at the thylakoid Tat translocase during protein transport J. Biol. Chem. 281 2006 5476 5483 (Pubitemid 43847642)
14. K. Dilks, R.W. Rose, E. Hartmann, and M. Pohlschröder Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey J. Bacteriol. 185 2003 1478 1483 (Pubitemid 36176885)
15. T. Dörr, M. Vulić, and K. Lewis Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli PLoS Biol. 8 2010 e1000317
16. Y. Duan, C. Wu, S. Chowdhury, M.C. Lee, G. Xiong, W. Zhang, R. Yang, P. Cieplak, R. Luo, and T. Lee A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations J. Comput. Chem. 24 2003 1999 2012
17. R.A. Frank, J.V. Pratap, X.Y. Pei, R.N. Perham, and B.F. Luisi The molecular origins of specificity in the assembly of a multienzyme complex Structure 13 2005 1119 1130 (Pubitemid 41111480)
18. J. Fröbel, P. Rose, and M. Müller Twin-arginine-dependent translocation of folded proteins Philos. Trans. R. Soc. Lond. B Biol. Sci. 367 2012 1029 1046
19. N. Go, and H.A. Scheraga On the Use of Classical Statistical Mechanics in the Treatment of Polymer Chain Conformation Macromolecules 9 1976 535 542
20. 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)
21. K. Gouffi, F. Gérard, C.-L. Santini, and L.-F. Wu Dual topology of the Escherichia coli TatA protein J. Biol. Chem. 279 2004 11608 11615 (Pubitemid 38401662)
22. B. Hess, C. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation J. Chem. Theory Comput. 4 2008 435 447
23. Y. Hu, E. Zhao, H. Li, B. Xia, and 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
24. R.L. Jack, F. Sargent, B.C. Berks, G. Sawers, and T. Palmer Constitutive expression of Escherichia coli tat genes indicates an important role for the twin-arginine translocase during aerobic and anaerobic growth J. Bacteriol. 183 2001 1801 1804 (Pubitemid 32172328)
25. J.D.H. 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)
26. H. Kim, J. Hsin, Y. Liu, P.R. Selvin, and K. Schulten Formation of salt bridges mediates internal dimerization of myosin VI medial tail domain Structure 18 2010 1443 1449
27. C. Lange, S.D. Müller, T.H. Walther, J. Bürck, 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)
28. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, and R. Lopez Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948 (Pubitemid 350162903)
29. M.C. Leake, N.P. Greene, R.M. Godun, T. Granjon, G. Buchanan, S. Chen, R.M. Berry, T. Palmer, and B.C. Berks Variable stoichiometry of the TatA component of the twin-arginine protein transport system observed by in vivo single-molecule imaging Proc. Natl. Acad. Sci. USA 105 2008 15376 15381
30. P.A. Lee, G. Buchanan, N.R. Stanley, B.C. Berks, and T. Palmer Truncation analysis of TatA and TatB defines the minimal functional units required for protein translocation J. Bacteriol. 184 2002 5871 5879 (Pubitemid 35168235)
31. Y.D. Li, Z. Zhou, L.X. Lv, X.P. Hou, and Y.Q. Li New approach to achieve high-level secretory expression of heterologous proteins by using Tat signal peptide Protein Pept. Lett. 16 2009 706 710
32. J.W. Mack, A.C. Steven, and P.M. Steinert The mechanism of interaction of filaggrin with intermediate filaments. The ionic zipper hypothesis J. Mol. Biol. 232 1993 50 66 (Pubitemid 23245401)
33. S.S. Mande, S. Sarfaty, M.D. Allen, R.N. Perham, and W.G. Hol Protein-protein interactions in the pyruvate dehydrogenase multienzyme complex: dihydrolipoamide dehydrogenase complexed with the binding domain of dihydrolipoamide acetyltransferase Structure 4 1996 277 286
34. H. Mori, and K. Cline Post-translational protein translocation into thylakoids by the Sec and Delta pH-dependent pathways Biochim. Biophys. Acta 1541 2001 80 90 (Pubitemid 34024830)
35. 15N-NMR Biochim. Biophys. Acta 1768 2007 3071 3079 (Pubitemid 350236094)
36. B. Musafia, V. Buchner, and D. Arad Complex salt bridges in proteins: statistical analysis of structure and function J. Mol. Biol. 254 1995 761 770 (Pubitemid 26001806)
37. 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)
38. J.K. Noel, P.C. Whitford, K.Y. Sanbonmatsu, and J.N. Onuchic SMOG@ctbp: simplified deployment of structure-based models in GROMACS Nucleic Acids Res. 38 Web Server issue 2010 W657-61
39. 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)
40. T. Palmer, and B.C. Berks Moving folded proteins across the bacterial cell membrane Microbiology 149 2003 547 556 (Pubitemid 36395090)
41. T. Palmer, F. Sargent, and B.C. Berks Export of complex cofactor-containing proteins by the bacterial Tat pathway Trends Microbiol. 13 2005 175 180 (Pubitemid 40463319)
42. M. Paulmann, T. Arnold, D. Linke, S. Özdirekcan, A. Kopp, T. Gutsmann, H. Kalbacher, I. Wanke, V.J. Schuenemann, and M. Habeck Structure-activity analysis of the dermcidin-derived peptide DCD-1L, an anionic antimicrobial peptide present in human sweat J. Biol. Chem. 287 2012 8434 8443
43. O. Pop, U. Martin, C. Abel, and J.P. Müller 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)
44. I. Porcelli, E. de Leeuw, R. Wallis, E. van den Brink-van der Laan, B. de Kruijff, B.A. Wallace, T. Palmer, and B.C. Berks Characterization and membrane assembly of the TatA component of the Escherichia coli twin-arginine protein transport system Biochemistry 41 2002 13690 13697 (Pubitemid 35332706)
45. C. Robinson, and A. Bolhuis Tat-dependent protein targeting in prokaryotes and chloroplasts Biochim. Biophys. Acta 1694 2004 135 147 (Pubitemid 39535066)
46. K.J. Rosenberg, J.L. Ross, H.E. Feinstein, S.C. Feinstein, and J. Israelachvili Complementary dimerization of microtubule-associated tau protein: Implications for microtubule bundling and tau-mediated pathogenesis Proc. Natl. Acad. Sci. USA 105 2008 7445 7450 (Pubitemid 351830037)
47. F. Sargent, U. Gohlke, E. De Leeuw, N.R. Stanley, T. Palmer, H.R. Saibil, and B.C. Berks Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure Eur. J. Biochem. 268 2001 3361 3367 (Pubitemid 32862927)
48. H. Schägger, and G. von Jagow Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form Anal. Biochem. 199 1991 223 231
49. B. Schittek, R. Hipfel, B. Sauer, J. Bauer, H. Kalbacher, S. Stevanovic, M. Schirle, K. Schroeder, N. Blin, and F. Meier Dermcidin: a novel human antibiotic peptide secreted by sweat glands Nat. Immunol. 2 2001 1133 1137 (Pubitemid 33130147)
50. T. Steinbrecher, S. Prock, J. Reichert, P. Wadhwani, B. Zimpfer, J. Bürck, M. Berditsch, M. Elstner, and A.S. Ulrich Peptide-lipid interactions of the stress-response peptide TisB that induces bacterial persistence Biophys. J. 103 2012 1460 1469
51. rns is anchored in plane in the membrane via an amphipathic helix J. Biol. Chem. 282 2007 32730 32741 (Pubitemid 350159277)
52. C. Unoson, and E.G.H. Wagner A small SOS-induced toxin is targeted against the inner membrane in Escherichia coli Mol. Microbiol. 70 2008 258 270
53. B.P. Uberuaga, M. Anghel, and A.F. Voter Synchronization of trajectories in canonical molecular-dynamics simulations: observation, explanation, and exploitation J. Chem. Phys. 120 2004 6363 6374
54. R. van der Ploeg, J.P. Barnett, N. Vasisht, V.J. Goosens, D.C. Pöther, C. Robinson, and J.M. van Dijl Salt sensitivity of minimal twin arginine translocases J. Biol. Chem. 286 2011 43759 43770
55. d) of the twin-arginine translocase from Bacillus subtilis resolved by solid-state NMR spectroscopy J. Am. Chem. Soc. 132 2010 15945 15956
56. G. Warren, J. Oates, C. Robinson, and A.M. Dixon Contributions of the transmembrane domain and a key acidic motif to assembly and function of the TatA complex J. Mol. Biol. 388 2009 122 132
57. A.M. Waterhouse, J.B. Procter, D.M.A. Martin, M. Clamp, and G.J. Barton Jalview Version 2 - a multiple sequence alignment editor and analysis workbench Bioinformatics 25 2009 1189 1191
58. M. Westermann, O.I. Pop, R. Gerlach, T.R. Appel, W. Schlörmann, S. Schreiber, and J.P. Müller 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)
59. 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
60. P.C. Whitford, J.K. Noel, S. Gosavi, A. Schug, K.Y. Sanbonmatsu, and J.N. Onuchic An all-atom structure-based potential for proteins: bridging minimal models with all-atom empirical forcefields Proteins 75 2009 430 441
61. I. Wittig, H.P. Braun, and H. Schägger Blue native PAGE Nat. Protoc. 1 2006 418 428
62. L. Zhang, Z. Zhu, H. Jing, J. Zhang, Y. Xiong, M. Yan, S. Gao, L.F. Wu, J. Xu, and B. Kan Pleiotropic effects of the twin-arginine translocation system on biofilm formation, colonization, and virulence in Vibrio cholerae BMC Microbiol. 9 2009 114
63. Abramoff, M.D.; Magalhaes, P.J.; and Ram, S.J. (2004). Image Processing with ImageJ. Biophotonics International 11, 36-42.
64. Bonomi, M.; Branduardi, D.; Bussi, G.; Camilloni, C.; Provasi, D.; Raiteri, P.; Donadio, D.; Marinelli, F.; Pietrucci, F.; Broglia, R.A.; et al. (2009). PLUMED: A portable plugin for free-energy calculations with molecular dynamics. Comput. Phys. Commun. 180, 1961-1972.
65. Case, D.A.; Cheatham, T.E.; 3rd, Darden, T.; Gohlke, H.; Luo, R.; Merz, K.M.; Jr.; Onufriev, A.; Simmerling, C.; Wang, B.; and Woods, R.J. (2005). The Amber biomolecular simulation programs. J. Comput. Chem. 26, 1668-1688. (Pubitemid 43076180)
66. Chavez, L.L.; Gosavi, S.; Jennings, P.A.; and Onuchic, J.N. (2006). Multiple routes lead to the native state in the energy landscape of the β-trefoil family. Proc. Natl. Acad. Sci. USA 103, 10254-10258. (Pubitemid 44051153)
67. Clementi, C.; García, A.E.; and Onuchic, J.N. (2003). Interplay among tertiary contacts, secondary structure formation and side-chain packing in the protein folding mechanism: all-atom representation study of protein L. J. Mol. Biol. 326, 933-954. (Pubitemid 36284722)
68. Dabney-Smith, C.; Mori, H.; and Cline, K. (2003). Requirement of a Tha4-conserved transmembrane glutamate in thylakoid Tat translocase assembly revealed by biochemical complementation. J. Biol. Chem. 278, 43027-43033. (Pubitemid 37345917)
69. Duan, Y.; Wu, C.; Chowdhury, S.; Lee, M.C.; Xiong, G.; Zhang, W.; Yang, R.; Cieplak, P.; Luo, R.; Lee, T.; et al. (2003). A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem. 24, 1999-2012.
70. Hess, B.; Kutzner, C.; van der Spoel, D.; and Lindahl, E. (2008). GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation. J. Chem. Theory Comput. 4, 435-447.
71. Lange, C.; Müller, S.D.; Walther, T.H.; Bürck, J.; and Ulrich, A.S. (2007). Structure analysis of the protein translocating channel TatA in membranes using a multi-construct approach. Biochim. Biophys. Acta 1768, 2627-2634. (Pubitemid 47532040)
72. Lee, P.A.; Buchanan, G.; Stanley, N.R.; Berks, B.C.; and Palmer, T. (2002). Truncation analysis of TatA and TatB defines the minimal functional units required for protein translocation. J. Bacteriol. 184, 5871-5879. (Pubitemid 35168235)
73. Mongan, J.; Simmerling, C.; McCammon, J.A.; Case, D.A.; and Onufriev, A. (2007). Generalized Born model with a simple, robust molecular volume correction. J. Chem. Theory Comput. 3, 156-169.
74. Noel, J.K.; Whitford, P.C.; Sanbonmatsu, K.Y.; and Onuchic, J.N. (2010). SMOG@ctbp: simplified deployment of structure-based models in GROMACS. Nucleic Acids Res. 38(Web Server issue), W657-61.
75. Schägger, H.; and von Jagow, G. (1991). Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199, 223-231.
76. Schug, A.; Weigt, M.; Onuchic, J.N.; Hwa, T.; and Szurmant, H. (2009). High-resolution protein complexes from integrating genomic information with molecular simulation. Proc. Natl. Acad. Sci. USA 106, 22124-22129.
77. Schug, A.; Whitford, P.C.; Levy, Y.; and Onuchic, J.N. (2007). Mutations as trapdoors to two competing native conformations of the Rop-dimer. Proc. Natl. Acad. Sci. USA 104, 17674-17679. (Pubitemid 350210893)
78. Uberuaga, B.P.; Anghel, M.; and Voter, A.F. (2004). Synchronization of trajectories in canonical molecular-dynamics simulations: observation, explanation, and exploitation. J. Chem. Phys. 120, 6363-6374.
79. Warren, G.; Oates, J.; Robinson, C.; and Dixon, A.M. (2009). Contributions of the transmembrane domain and a key acidic motif to assembly and function of the TatA complex. J. Mol. Biol. 388, 122-132.
80. Whitford, P.C.; Noel, J.K.; Gosavi, S.; Schug, A.; Sanbonmatsu, K.Y.; and Onuchic, J.N. (2009). An all-atom structure-based potential for proteins: bridging minimal models with all-atom empirical forcefields. Proteins 75, 430-441.
81. Wittig, I.; Braun, H.P.; and Schägger, H. (2006). Blue native PAGE. Nat. Protoc. 1, 418-428.