Stoichiometry for binding and transport by the twin Arginine translocation system

Journal of Cell Biology

Volumn 197, Issue 4, 2012, Pages 523-534

  Celedon, Jose M ^a,b   Cline, Kenneth ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; OLIGOMER; PROTEIN CPTATC; PROTEIN HCF106; PROTEIN THA4; TWIN ARGININE TRANSLOCATION SYSTEM; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CHLOROPLAST; COMPLEX FORMATION; CONTROLLED STUDY; DISSOCIATION; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; STOICHIOMETRY; THYLAKOID MEMBRANE; TITRIMETRY;

ARGININE; BINDING SITES; KINETICS; MEMBRANE PROTEINS; PEAS; PLANT PROTEINS; PROTEIN TRANSPORT; THYLAKOIDS;

EID: 84862599557     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201201096     Document Type: Article

References (53)

1. Alami, M., I. Lüke, S. Deitermann, G. Eisner, H.-G. Koch, J. Brunner, and M. Müller. 2003. Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol. Cell. 12:937-946. http://dx.doi.org/10.1016/S1097-2765(03)00398-8
2. Alder, N.N., and S.M. Theg. 2003. Protein transport via the cpTat pathway displays cooperativity and is stimulated by transport-incompetent substrate. FEBS Lett. 540:96-100. http://dx.doi.org/10.1016/S0014-5793(03)00231-X
3. Arnon, D.I. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta Vulgaris. Plant Physiol. 24:1-15. http://dx.doi.org/10.1104/pp.24.1.1
4. Auer, S., and D. Kashchiev. 2010. Insight into the correlation between lag time and aggregation rate in the kinetics of protein aggregation. Proteins. 78:2412-2416.
5. Bageshwar, U.K., N. Whitaker, F.-C. Liang, and S.M. Musser. 2009. Interconvertibility of lipid- and translocon-bound forms of the bacterial Tat precursor pre-SufI. Mol. Microbiol. 74:209-226. http://dx.doi.org/10.1111/j.1365-2958.2009.06862.x
6. Berks, B.C., F. Sargent, and T. Palmer. 2000. The Tat protein export pathway. Mol. Microbiol. 35:260-274. http://dx.doi.org/10.1046/j.1365-2958.2000.01719.x
7. Bolhuis, A., J.E. Mathers, J.D. Thomas, C.M.L. Barrett, and C. Robinson. 2001. TatB and TatC form a functional and structural unit of the twin-arginine translocase from Escherichia coli. J. Biol. Chem. 276:20213-20219. http://dx.doi.org/10.1074/jbc.M100682200
8. Brüser, T., and C. Sanders. 2003. An alternative model of the twin arginine translocation system. Microbiol. Res. 158:7-17. http://dx.doi.org/10.1078/0944-5013-00176
9. Chen, Q., L.M. Lauzon, A.E. DeRocher, and E. Vierling. 1990. Accumulation, stability, and localization of a major chloroplast heat-shock protein. J. Cell Biol. 110:1873-1883. http://dx.doi.org/10.1083/jcb.110.6.1873
10. Cline, K. 1986. Import of proteins into chloroplasts. Membrane integration of a thylakoid precursor protein reconstituted in chloroplast lysates. J. Biol. Chem. 261:14804-14810.
11. Cline, K., and H. Mori. 2001. Thylakoid ΔpH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J. Cell Biol. 154:719-729. http://dx.doi.org/10.1083/jcb.200105149
12. Cline, K., and S.M. Theg. 2007. The Sec and Tat Protein Translocation Pathways in Chloroplasts. In The Enzymes: Molecular Machines Involved in Protein Transport across Cellular Membranes. Vol. 25. R.E. Dalbey, C.M. Koehler, and F. Tamanoi, editors. Elsevier, London. 463-492.
13. Cline, K., R. Henry, C. Li, and J. Yuan. 1993. Multiple pathways for protein transport into or across the thylakoid membrane. EMBO J. 12:4105-4114.
14. Connors, K.A. 1990. Chemical Kinetics: The Study of Reaction Rates in Solution. Wiley-VCH, New York. 496 pp.
15. Dabney-Smith, C., and K. Cline. 2009. Clustering of C-terminal stromal domains of Tha4 homo-oligomers during translocation by the Tat protein transport system. Mol. Biol. Cell. 20:2060-2069. http://dx.doi.org/10.1091/mbc.E08-12-1189
16. Dabney-Smith, C., H. Mori, and K. Cline. 2003. Requirement of a Tha4-conserved transmembrane glutamate in thylakoid Tat translocase assembly revealed by biochemical complementation. J. Biol. Chem. 278:43027-43033. http://dx.doi.org/10.1074/jbc.M307923200
17. Dorne, A.J., J. Joyard, and R. Douce. 1990. Do thylakoids really contain phosphatidylcholine? Proc. Natl. Acad. Sci. USA. 87:71-74. http://dx.doi.org/10.1073/pnas.87.1.71
18. Douce, R., and J. Joyard. 1982. Purification of the Chloroplast Envelope. In Methods in Chloroplast Molecular Biology. M. Edelman, N.-H., and R.B. Hallick, editors. Elsevier, Amsterdam. 239-256.
19. Fincher, V., C. Dabney-Smith, and K. Cline. 2003. Functional assembly of thylakoid deltapH-dependent/Tat protein transport pathway components in vitro. Eur. J. Biochem. 270:4930-4941. http://dx.doi.org/10.1046/j.1432-1033.2003.03894.x
20. Frielingsdorf, S., M. Jakob, and R.B. Klösgen. 2008. A stromal pool of TatA promotes Tat-dependent protein transport across the thylakoid membrane. J. Biol. Chem. 283:33838-33845. http://dx.doi.org/10.1074/jbc.M806334200
21. Fröbel, J., P. Rose, and M. Müller. 2011. Twin-arginine translocation: Early contacts between substrate proteins and TatA. J. Biol. Chem. 286:43679-43689. http://dx.doi.org/10.1074/jbc.M111.292565
22. Gérard, F., and K. Cline. 2006. Efficient twin arginine translocation (Tat) pathway transport of a precursor protein covalently anchored to its initial cpTatC binding site. J. Biol. Chem. 281:6130-6135. http://dx.doi.org/10.1074/jbc.M512733200
23. Gérard, F., and K. Cline. 2007. The thylakoid proton gradient promotes an advanced stage of signal peptide binding deep within the Tat pathway receptor complex. J. Biol. Chem. 282:5263-5272. http://dx.doi.org/10.1074/jbc.M610337200
24. Gettens, R.T.T., and J.L. Gilbert. 2007. Quantification of fibrinogen adsorption onto 316L stainless steel. J. Biomed. Mater. Res. A. 81:465-473.
25. Gohlke, U., L. Pullan, C.A. McDevitt, I. Porcelli, E. de Leeuw, T. Palmer, H.R. Saibil, and B.C. Berks. 2005. The TatA component of the twinarginine protein transport system forms channel complexes of variable diameter. Proc. Natl. Acad. Sci. USA. 102:10482-10486. http://dx.doi.org/10.1073/pnas.0503558102
26. Hashimoto, A., W.F. Ettinger, Y. Yamamoto, and S.M. Theg. 1997. Assembly of newly imported oxygen-evolving complex subunits in isolated chloroplasts: Sites of assembly and mechanism of binding. Plant Cell. 9:441-452. http://dx.doi.org/10.1105/tpc.9.3.441
27. Heuberger, E.H.M.L., L.M. Veenhoff, R.H. Duurkens, R.H.E. Friesen, and B. Poolman. 2002. Oligomeric state of membrane transport proteins analyzed with blue native electrophoresis and analytical ultracentrifugation. J. Mol. Biol. 317:591-600. http://dx.doi.org/10.1006/jmbi.2002.5416
28. Hou, B., S. Frielingsdorf, and R.B. Klösgen. 2006. Unassisted membrane insertion as the initial step in DeltapH/Tat-dependent protein transport. J. Mol. Biol. 355:957-967. http://dx.doi.org/10.1016/j.jmb.2005.11.029
29. Jakob, M., S. Kaiser, M. Gutensohn, P. Hanner, and R.B. Klösgen. 2009. Tat subunit stoichiometry in Arabidopsis thaliana challenges the proposed function of TatA as the translocation pore. Biochim. Biophys. Acta. 1793:388-394. http://dx.doi.org/10.1016/j.bbamcr.2008.09.006
30. Leake, M.C., N.P. Greene, R.M. Godun, T. Granjon, G. Buchanan, S. Chen, R.M. Berry, T. Palmer, and B.C. Berks. 2008. 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. 105:15376-15381. http://dx.doi.org/10.1073/pnas.0806338105
31. Lee, P.A., D. Tullman-Ercek, and G. Georgiou. 2006. The bacterial twin-arginine translocation pathway. Annu. Rev. Microbiol. 60:373-395. http://dx.doi.org/10.1146/annurev.micro.60.080805.142212
32. Ma, X., and K. Cline. 2000. Precursors bind to specific sites on thylakoid membranes prior to transport on the delta pH protein translocation system. J. Biol. Chem. 275:10016-10022. http://dx.doi.org/10.1074/jbc.275.14.10016
33. Ma, X., and J. Browse. 2006. Altered rates of protein transport in Arabidopsis mutants deficient in chloroplast membrane unsaturation. Phytochemistry. 67:1629-1636. http://dx.doi.org/10.1016/j.phytochem.2006.04.008
34. Ma, X., and K. Cline. 2010. Multiple precursor proteins bind individual Tat receptor complexes and are collectively transported. EMBO J. 29:1477-1488. http://dx.doi.org/10.1038/emboj.2010.44
35. Maurer, C., S. Panahandeh, A.-C. Jungkamp, M. Moser, and M. Müller. 2010. TatB functions as an oligomeric binding site for folded Tat precursor proteins. Mol. Biol. Cell. 21:4151-4161. http://dx.doi.org/10.1091/mbc.E10-07-0585
36. McDevitt, C.A., G. Buchanan, F. Sargent, T. Palmer, and B.C. Berks. 2006. Subunit composition and in vivo substrate-binding characteristics of Escherichia coli Tat protein complexes expressed at native levels. FEBS J. 273:5656-5668. http://dx.doi.org/10.1111/j.1742-4658.2006.05554.x
37. Mori, H., and K. Cline. 2002. A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid? pH/Tat translocase. J. Cell Biol. 157:205-210. http://dx.doi.org/10.1083/jcb.200202048
38. Mori, H., E.J. Summer, X. Ma, and K. Cline. 1999. Component specificity for the thylakoidal Sec and Delta pH-dependent protein transport pathways. J. Cell Biol. 146:45-56.
39. Mori, H., E.J. Summer, and K. Cline. 2001. Chloroplast TatC plays a direct role in thylakoid (Δ)pH-dependent protein transport. FEBS Lett. 501:65-68. http://dx.doi.org/10.1016/S0014-5793(01)02626-6
40. Müller, M., and R.B. Klösgen. 2005. The Tat pathway in bacteria and chloroplasts (review). Mol. Membr. Biol. 22:113-121. http://dx.doi.org/10.1080/09687860500041809
41. Musser, S.M., and S.M. Theg. 2000. Characterization of the early steps of OE17 precursor transport by the thylakoid DeltapH/Tat machinery. Eur. J. Biochem. 267:2588-2598. http://dx.doi.org/10.1046/j.1432-1327.2000.01269.x
42. Orriss, G.L., M.J. Tarry, B. Ize, F. Sargent, S.M. Lea, T. Palmer, and B.C. Berks. 2007. TatBC, TatB, and TatC form structurally autonomous units within the twin arginine protein transport system of Escherichia coli. FEBS Lett. 581:4091-4097. http://dx.doi.org/10.1016/j.febslet.2007.07.044
43. Panahandeh, S., C. Maurer, M. Moser, M.P. DeLisa, and M. Müller. 2008. Following the path of a twin-arginine precursor along the TatABC translocase of Escherichia coli. J. Biol. Chem. 283:33267-33275. http://dx.doi.org/10.1074/jbc.M804225200
44. Patrick, T.D., C.E. Lewer, and V.M. Pain. 1989. Preparation and characterization of cell-free protein synthesis systems from oocytes and eggs of Xenopus laevis. Development. 106:1-9.
45. Reed, J.E., K. Cline, L.C. Stephens, K.O. Bacot, and P.V. Viitanen. 1990. Early events in the import/assembly pathway of an integral thylakoid protein. Eur. J. Biochem. 194:33-42. http://dx.doi.org/10.1111/j.1432-1033.1990.tb19423.x
46. Rodrigue, A., A. Chanal, K. Beck, M. Müller, and L.F. Wu. 1999. Co-translocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial tat pathway. J. Biol. Chem. 274:13223-13228. http://dx.doi.org/10.1074/jbc.274.19.13223
47. Sargent, F., B.C. Berks, and T. Palmer. 2006. Pathfinders and trailblazers: A prokaryotic targeting system for transport of folded proteins. FEMS Microbiol. Lett. 254:198-207. http://dx.doi.org/10.1111/j.1574-6968.2005.00049.x
48. Stanley, N.R., T. Palmer, and B.C. Berks. 2000. The twin arginine consensus motif of Tat signal peptides is involved in Sec-independent protein targeting in Escherichia coli. J. Biol. Chem. 275:11591-11596. http://dx.doi.org/10.1074/jbc.275.16.11591
49. Summer, E.J., H. Mori, A.M. Settles, and K. Cline. 2000. The thylakoid delta pH-dependent pathway machinery facilitates RR-independent N-tail protein integration. J. Biol. Chem. 275:23483-23490. http://dx.doi.org/10.1074/jbc.M004137200
50. Tarry, M.J., E. Schäfer, S. Chen, G. Buchanan, N.P. Greene, S.M. Lea, T. Palmer, H.R. Saibil, and B.C. Berks. 2009. Structural analysis of substrate binding by the TatBC component of the twin-arginine protein transport system. Proc. Natl. Acad. Sci. USA. 106:13284-13289. http://dx.doi.org/10.1073/pnas.0901566106
51. Tossi, A., L. Sandri, and A. Giangaspero. 2000. Amphipathic, α-helical antimicrobial peptides. Biopolymers. 55:4-30. http://dx.doi.org/10.1002/1097-0282(2000)55:1<4::AID-BIP30>3.0.CO;2-M
52. Weimer, P.J., J.M. Lopez-Guisa, and A.D. French. 1990. Effect of cellulose fine structure on kinetics of its digestion by mixed ruminal microorganisms in vitro. Appl. Environ. Microbiol. 56:2421-2429.
53. Whitaker, N., U.K. Bageshwar, and S.M. Musser. 2012. Kinetics of precursor interactions with the bacterial Tat translocase detected by real-time FRET. J. Biol. Chem. In Press.