A mutation leading to super-assembly of twin-arginine translocase (Tat) protein complexes

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 9, 2014, Pages 1978-1986

  Patel, Roshani ^a   Vasilev, Cvetelin ^b   Beck, Daniel ^a   Monteferrante, Carmine G ^c   Van Dijl, Jan Maarten ^c   Hunter, C Neil ^b   Smith, Corinne ^a   Robinson, Colin ^d  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d UNIVERSITY OF KENT   (United Kingdom)

Author keywords

AFM; Atomic force microscopy; Signal peptide; Tat; Twin arginine translocation

Indexed keywords

CARRIER PROTEIN; CYTOCHROME P450 2A; MULTIPROTEIN COMPLEX; TWIN ARGININE TRANSLOCASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; BACILLUS SUBTILIS; GEL PERMEATION CHROMATOGRAPHY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; STEADY STATE; TRANSMISSION ELECTRON MICROSCOPY;

AFM; ATOMIC FORCE MICROSCOPY; SIGNAL PEPTIDE; TAT; TWIN-ARGININE TRANSLOCATION;

ARGININE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CHROMATOGRAPHY, GEL; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, ATOMIC FORCE; MULTIPROTEIN COMPLEXES; MUTATION; PROTEIN STRUCTURE, SECONDARY;

EID: 84902438476     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.05.009     Document Type: Article

References (26)

1. Fröbel J., Rose P., Müller M. Twin-arginine-dependent translocation of folded proteins. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2012, 367:1029-1046.
2. Robinson C., Matos C.F.R., Beck D., Chao R., 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.
3. Palmer T., Berks B.C. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 2012, 10:483-496.
4. Santini C.L., Ize B., Chanal A., Müller M., Giordano G., Wu L.F. A novel sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J. 1998, 17:101-102.
5. Weiner J.H., Bilous P.T., Shaw G.M., Lubitz S.P., Frost L., Thomas G.H., Cole J.A., Turner R.J. A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell 1998, 93:93-101.
6. Bolhuis A., Mathers J.E., Thomas J.D., Barrett C.M.L., Robinson C. TatB and TatC form a structural and functional unit of the twin-arginine translocase from Escherichia coli. J. Biol. Chem. 2001, 276:20213-20219.
7. Jongbloed Jan D.H., 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.
8. 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.
9. Jongbloed J.D., Martin U., Antelmann H., Hecker M., Tjalsma H., Venema G., Bron S., van Dijl J.M., Müller J. TatC is a specificity determinant for protein secretion via the twin-arginine translocation pathway. J. Biol. Chem. 2000, 275:41350-41357.
10. 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.
11. 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 organisation and similar substrate recognition requirements. J. Biol. Chem. 2009, 276:232-243.
12. Gohlke L.Pullan, McDevitt C., Porcelli I., de Leeuw E., Palmer T., Saibil H., 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.
13. Baglieri J., Beck D., Vasisht N., Smith C.J., Robinson C. Structure of the 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.
14. Beck D., Vasisht N., Baglieri J., Monteferrante C.G., Robinson C., Smith C.S. Ultrastructural characterisation of Bacillus subtilis TatA complexes suggests they are too small to form homooligomeric translocation pores. Biochim. Biophys. Acta Mol. Cell Res. 2013, 1833:1811-1819.
15. Alami M., Luke I., Deitermann S., Eisner G.H., Koch G., Brunner J., Müller M. Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol. Cell 2003, 12:937-946.
16. Maurer C., Panahandeh S., Jungkamp A.C., Moser M., Müller M. TatB functions as an oligomeric binding site for folded Tat precursor proteins. Mol. Biol. Cell 2010, 21:4151-4161.
17. Fröbel J., Rose P., Lausberg F., Blummel A.S., Freudl R., Müller M. Transmembrane insertion of twin-arginine signal peptides is driven by TatC and regulated by TatB. Nat. Commun. 2012, 3:1311.
18. Zoufaly S., Fröbel J., Rose P., Flecken T., Maurer C., Moser M., Müller 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.
19. 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.
20. Van der Ploeg R., Barnett J.P., Vasisht N., Robinson C., van Dijl J.-M. Salt-sensitivity of minimal TatAC translocases. J. Biol. Chem. 2011, 286:43759-43770.
21. Bongers R.S., Veening J.W., Van Wieringen M., Kuipers O.P., Kleerebezem M. Development and characterization of a subtilin-regulated expression system in Bacillus subtilis: strict control of gene expression by addition of subtilin. Appl. Environ. Microbiol. 2005, 71:8818-8824.
22. Zweers J.C., Wiegert T., van Dijl J.M. Stress-responsive systems set specific limits to the overproduction of membrane proteins in Bacillus subtilis. Appl. Environ. Microbiol. 2009, 75:7356-7364.
23. 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 organisation and similar substrate recognition requirements. FEBS J. 2009, 276:232-243.
24. Fritzsche W., Schaper A., Jovin T.M. Probing chromatin with the scanning force microscope. Chromosoma 1994, 103:231-236.
25. Berthelmann F., Mehner D., Richter S., Lindenstrauss U., Lünsdorf H., Hause G., Brüser 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.
26. Blaudeck N., Kreutzenbeck P., Müller 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.