Genetic evidence for a TatC dimer at the core of the escherichia coli twin arginine (Tat) protein translocase

Journal of Molecular Microbiology and Biotechnology

Volumn 20, Issue 3, 2011, Pages 168-175

  Maldonado, Barbara ^a   Buchanan, Grant ^a   Müller, Matthias ^c   Berks, Ben C ^b   Palmer, Tracy ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Dimer; Genetic fusion; Protein transport; Tat pathway; TatBC complex; Twin arginine signal peptide

Indexed keywords

CARRIER PROTEIN; DIMER; HYBRID PROTEIN; OLIGOMER; TWIN ARGININE PROTEIN TRANSPORT C; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ESCHERICHIA COLI; GENE FUSION; NONHUMAN; POINT MUTATION; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN TRANSPORT; STOICHIOMETRY;

CELL MEMBRANE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE TRANSPORT PROTEINS; MUTATION; PEPTIDYL TRANSFERASES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS;

ESCHERICHIA COLI; PROKARYOTA;

EID: 79959551982     PISSN: 14641801     EISSN: 16602412     Source Type: Journal    
DOI: 10.1159/000329076     Document Type: Article

References (38)

1. Alami M, Luke I, Deitermann S, Eisner G, Koch HG, Brunner J, Muller M: Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli Mol Cell 2003; 12: 937-946. (Pubitemid 37352786)
2. Alami M, Trescher D, Wu LF, Muller M: Separate analysis of twin-arginine translocation (Tat)-specific membrane binding and translocation in Escherichia coli J Biol Chem 2002; 277: 20499-20503. (Pubitemid 34967348)
3. Barrett CM, 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. (Pubitemid 40312470)
4. Berks BC: A common export pathway for proteins binding complex redox cofactors? Mol Microbiol 1996; 22: 393-404. (Pubitemid 26373825)
5. Bogsch EG, Sargent F, Stanley NR, Berks BC, 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. (Pubitemid 28334711)
6. Bolhuis A, Mathers JE, Thomas JD, Barrett CM, 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.
7. Buchanan G, de Leeuw E, Stanley NR, Wexler M, Berks BC, Sargent F, Palmer T: Functional complexity of the twin-arginine translocase TatC component revealed by site-directed mutagenesis. Mol Microbiol 2002; 43: 1457-1470. (Pubitemid 34595538)
8. Cline K, Theg SM: The Sec and Tat protein translocation pathways in chloroplasts; in Dalbey RE, Koehler CM, Tamanoi F (ed): Molecular Machines Involved in Protein Transport Across Cellular Membranes. London, Elsevier, 2007, vol XXV, pp 463-492.
9. 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. (Pubitemid 43847642)
10. de Leeuw E, Granjon T, Porcelli I, Alami M, Carr SB, Muller M, Sargent F, Palmer T, Berks BC: Oligomeric properties and signal peptide binding by Escherichia coli Tat protein transport complexes. J Mol Biol 2002; 322: 1135-1146. (Pubitemid 35266517)
11. Driessen AJ, Nouwen N: Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 2008; 77: 643-667.
12. Gerard F, Cline K: Efficient twin arginine translocation (Tat) pathway transport of a precursor protein covalently anchored to its initial cpTatc binding site. J Biol Chem 2006; 281: 6130-6135. (Pubitemid 43847542)
13. Gohlke U, Pullan L, McDevitt CA, Porcelli I, de Leeuw E, Palmer T, Saibil HR, Berks BC: The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter. Proc Natl Acad Sci USA 2005; 102: 10482-10486. (Pubitemid 41061580)
14. Holzapfel E, Eisner G, Alami M, Barrett CM, Buchanan G, Luke I, Betton JM, Robinson C, Palmer T, Moser M, Muller M: The entire Nterminal half of TatC is involved in twin-arginine precursor binding. Biochemistry 2007; 46: 2892-2898. (Pubitemid 46417927)
15. Ize B, Stanley NR, Buchanan G, Palmer T: Role of the Escherichia col i Tat pathway in outer membrane integrity. Mol Microbiol 2003; 48: 1183-1193. (Pubitemid 36718215)
16. Jones PC, Fillingame RH: Genetic fusions of subunit c in the F 0 sector of H + -transporting ATP synthase. Functional dimers and trimers and determination of stoichiometry by cross-linking analysis. J Biol Chem 1998; 273: 29701-29705. (Pubitemid 28509980)
17. Leake MC, Greene NP, Godun RM, Granjon T, Buchanan G, Chen S, Berry RM, Palmer T, Berks BC: Variable stoichiometry of the TatA component of the twin-arginine protein transport system observed by in vivo singlemolecule imaging. Proc Natl Acad Sci USA 2008; 105: 15376-15381.
18. Lee PA, Orriss GL, Buchanan G, Greene NP, Bond PJ, Punginelli C, Jack RL, Sansom MS, Berks BC, Palmer T: Cysteine-scanning mutagenesis and disulfide mapping studies of the conserved domain of the twin-arginine translocase TatB component. J Biol Chem 2006; 281: 34072-34085. (Pubitemid 46036617)
19. Lester RL, DeMoss JA: Effects of molybdate and selenite on formate and nitrate metabolism in Escherichia coli J Bacteriol 1971; 105: 1006-1014.
20. Ma X, Cline K: Multiple precursor proteins bind individual tat receptor complexes and are collectively transported. EMBO J 2010; 29: 1477-1488.
21. Maurer C, Panahandeh S, Jungkamp AC, Moser M, Müller M: TatB functions as an oligomeric binding site for folded Tat precursor proteins. Mol Biol Cell 2010;21:4151-4161.
22. McDevitt CA, Hicks MG, Palmer T, Berks BC: Characterisation of Tat protein transport complexes carrying inactivating mutations. Biochem Biophys Res Comm 2005; 329: 693-698. (Pubitemid 40311799)
23. 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. (Pubitemid 34839817)
24. Mori H, Summer EJ, Cline K: Chloroplast TatC plays a direct role in thylakoid (delta)pH-dependent protein transport. FEBS Letts 2001; 501: 65-68. (Pubitemid 33712488)
25. Muller M: Twin-arginine-specific protein export in Escherichia coli Res Microbiol 2005; 156: 131-136. (Pubitemid 40320948)
26. Oates J, Mathers J, Mangels D, Kuhlbrandt W, Robinson C, Model K: Consensus structural features of purified bacterial TatABC complexes. J Mol Biol 2003; 330: 277-286. (Pubitemid 36773701)
27. Palmer T, Sargent F, and Berks BC: The Tat protein export pathway; in Böck A, Curtiss III R, Kaper JB, Karp PD, Neidhardt FC, Nyström T, Slauch JM, Squires CL, Ussery D (eds): EcoSal - Escherichia coli and Salmonella : Cellular and Molecular Biology. Washington, ASM Press, 2010.
28. Punginelli C: The Escherichia coli Tat protein translocase and its substrates; thesis, University of East Anglia, 2005.
29. Punginelli C, Maldonado B, Grahl S, Jack R, Alami M, Schroder J, Berks BC, Palmer T: Cysteine scanning mutagenesis and topological mapping of the Escherichia coli twin-arginine translocase Tatc component. J Bacteriol 2007; 189: 5482-5494. (Pubitemid 47206393)
30. Richter S, Bruser T: Targeting of unfolded PhoA to the Tat translocon of Escherichia coli. J Biol Chem 2005; 280: 42723-42730. (Pubitemid 43049232)
31. Sargent F, Bogsch EG, Stanley NR, Wexler M, Robinson C, Berks BC, Palmer T: Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J 1998; 17: 3640-3650. (Pubitemid 28327382)
32. Sargent F, Stanley NR, Berks BC, Palmer T: Secindependent protein translocation in Escherichia coli A distinct and pivotal role for the TatB protein. J Biol Chem 1999; 274: 36073-36082.
33. Settles AM, Yonetani A, Baron A, Bush DR, Cline K, Martienssen R: Sec-independent protein translocation by the maize Hcf106 protein. Science 1997; 278: 1467-1470. (Pubitemid 27509820)
34. Silvestro A, Pommier J, Giordano G: The inducible trimethylamine- N -oxide reductase of Escherichia coli K12: Biochemical and immunological studies. Biochim Biophys Acta 1988; 954: 1-13.
35. Stanley NR, Palmer T, Berks BC: The twin arginine consensus motif of Tat signal peptides is involved in Sec-independent protein targeting in Escherichia coli J Biol Chem 2000; 275: 11591-11596. (Pubitemid 30237716)
36. Strauch EM, Georgiou G: Escherichia coli TatC mutations that suppress defective twin-arginine transporter signal peptides. J Mol Biol 2007; 374: 283-291. (Pubitemid 350007660)
37. Tarry MJ, Schafer E, Chen S, Buchanan G, Greene NP, Lea SM, Palmer T, Saibil HR, Berks BC: Structural analysis of substrate binding by the TatBC component of the twin-arginine protein transport system. Proc Natil Acad Sci U S A 2009; 106: 13284-13289.
38. Weiner JH, Bilous PT, Shaw GM, Lubitz SP, Frost L, Thomas GH, Cole JA, Turner RJ: A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell 1998; 93: 93-101. (Pubitemid 28173555)