C-terminal truncation of a Tat passenger protein affects its membrane translocation by interfering with receptor binding

References

Alami, M., Luke, I., Deitermann, S., Eisner, G., Koch, H.G., Brunner, J., and Müller, M. (2003). Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol. Cell 12, 937–946.10.1016/S1097-2765(03)00398-8Search in Google Scholar

Aldridge, C., Ma, X., Gerard, F., and Cline, K. (2014). Substrate-gated docking of pore subunit Tha4 in the TatC cavity initiates Tat translocase assembly. J. Cell Biol. 205, 51–65.10.1083/jcb.201311057Search in Google Scholar

Annweiler, A., Hipskind, R.A., and Wirth, T. (1991). A strategy for efficient in vitro translation of cDNAs using the rabbit β-globin leader sequence. Nucleic Acids Res. 19, 3750.10.1093/nar/19.13.3750Search in Google Scholar

Bageshwar, U.K. and Musser, S.M. (2007). Two electrical potential-dependent steps are required for transport by the Escherichia coli Tat machinery. J. Cell Biol. 179, 87–99.10.1083/jcb.200702082Search in Google Scholar

Bageshwar, U.K., Whitaker, N., Liang, F.C., and Musser, S.M. (2009). Interconvertibility of lipid- and translocon-bound forms of the bacterial Tat precursor pre-SufI. Mol. Microbiol. 74, 209–226.10.1111/j.1365-2958.2009.06862.xSearch in Google Scholar

Berghöfer, J. and Klösgen, R.B. (1999). Two distinct translocation intermediates can be distinguished during protein transport by the TAT (ΔpH) pathway across the thylakoid membrane. FEBS Lett. 460, 328–332.10.1016/S0014-5793(99)01365-4Search in Google Scholar

Bogdanov, M., Zhang, W., Xie, J., and Dowhan, W. (2005). Transmembrane protein topology mapping by the substituted cysteine accessibility method (SCAM^TM): application to lipid-specific membrane protein topogenesis. Methods 36, 148–171.10.1016/j.ymeth.2004.11.002Search in Google Scholar PubMed PubMed Central

Braun, N.A., Davis, A.W., and Theg, S.M. (2007). The chloroplast Tat pathway utilizes the transmembrane electric potential as an energy source. Biophys. J. 93, 1993–1998.10.1529/biophysj.106.098731Search in Google Scholar PubMed PubMed Central

Brüser, T., Yano, T., Brune, D.C., and Daldal, F. (2003). Membrane targeting of a folded and cofactor-containing protein. Eur. J. Biochem. 270, 1211–1221.10.1046/j.1432-1033.2003.03481.xSearch in Google Scholar PubMed

Celedon, J.M. and Cline, K. (2013). Intra-plastid protein trafficking: how plant cells adapted prokaryotic mechanisms to the eukaryotic condition. Biochim. Biophys. Acta 1833, 341–351.10.1016/j.bbamcr.2012.06.028Search in Google Scholar PubMed PubMed Central

Chaddock, A.M., Mant, A., Karnauchov, I., Brink, S., Herrmann, R.G., Klösgen, R.B., and Robinson, C. (1995). A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the ΔpH-dependent thylakoidal protein translocase. Embo J. 14, 2715–2722.10.1002/j.1460-2075.1995.tb07272.xSearch in Google Scholar

Clausmeyer, S., Klösgen, R.B., and Herrmann, R.G. (1993). Protein import into chloroplasts. The hydrophilic lumenal proteins exhibit unexpected import and sorting specificities in spite of structurally conserved transit peptides. J. Biol. Chem. 268, 13869–13876.10.1016/S0021-9258(19)85183-9Search in Google Scholar

Cline, K. and McCaffery, M. (2007). Evidence for a dynamic and transient pathway through the TAT protein transport machinery. EMBO J. 26, 3039–3049.10.1038/sj.emboj.7601759Search in Google Scholar PubMed PubMed Central

Cline, K. and Mori, H. (2001). Thylakoid ΔpH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J. Cell Biol. 154, 719–729.10.1083/jcb.200105149Search in Google Scholar PubMed PubMed Central

Frielingsdorf, S. and Klösgen, R.B. (2007). Prerequisites for terminal processing of thylakoidal Tat substrates. J. Biol. Chem. 282, 24455–24462.10.1074/jbc.M702630200Search in Google Scholar PubMed

Frielingsdorf, S., Jakob, M., and Klösgen, R.B. (2008). A stromal pool of TatA promotes Tat-dependent protein transport across the thylakoid membrane. J. Biol. Chem. 283, 33838–33845.10.1074/jbc.M806334200Search in Google Scholar PubMed PubMed Central

Fröbel, J., Rose, P., and Müller, M. (2012). Twin-arginine-dependent translocation of folded proteins. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 367, 1029–1046.10.1098/rstb.2011.0202Search in Google Scholar PubMed PubMed Central

Hauer, R.S., Schlesier, R., Heilmann, K., Dittmar, J., Jakob, M., and Klösgen, R.B. (2013). Enough is enough: TatA demand during Tat-dependent protein transport. Biochim. Biophys. Acta 1833, 957–965.10.1016/j.bbamcr.2013.01.030Search in Google Scholar PubMed

Hou, B. and Brüser, T. (2011). The Tat-dependent protein translocation pathway. BioMol. Concepts 2, 507–523.10.1515/BMC.2011.040Search in Google Scholar PubMed

Hou, B., Frielingsdorf, S., and Klösgen, R.B. (2006). Unassisted membrane insertion as the initial step in ΔpH/Tat-dependent protein transport. J. Mol. Biol. 355, 957–967.10.1016/j.jmb.2005.11.029Search in Google Scholar PubMed

Jakob, M., Kaiser, S., Gutensohn, M., Hanner, P., and Klösgen, R.B. (2009). Tat subunit stoichiometry in Arabidopsis thaliana challenges the proposed function of TatA as the translocation pore. Biochim. Biophys. Acta 1793, 388–394.10.1016/j.bbamcr.2008.09.006Search in Google Scholar

Karlsson, A.J., Lim, H.K., Xu, H., Rocco, M.A., Bratkowski, M.A., Ke, A., and DeLisa, M.P. (2012). Engineering antibody fitness and function using membrane-anchored display of correctly folded proteins. J. Mol. Biol. 416, 94–107.10.1016/j.jmb.2011.12.021Search in Google Scholar

Koch, S., Fritsch, M.J., Buchanan, G., and Palmer, T. (2012). Escherichia coli TatA and TatB proteins have N-out, C-in topology in intact cells. J. Biol. Chem. 287, 14420–14431.10.1074/jbc.M112.354555Search in Google Scholar

Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.10.1038/227680a0Search in Google Scholar

Marques, J.P., Dudeck, I., and Klösgen, R.B. (2003). Targeting of EGFP chimeras within chloroplasts. Mol. Genet. Genomics 269, 381–387.10.1007/s00438-003-0846-ySearch in Google Scholar

Maurer C., Panahandeh S., Moser M., and Müller M. (2009). Impairment of twin-arginine-dependent export by seemingly small alterations of substrate conformation. FEBS Lett. 583, 2849–2853.10.1016/j.febslet.2009.07.038Search in Google Scholar

Mori, H. and Cline, K. (2002). A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid ΔpH/Tat translocase. J. Cell Biol. 157, 205–210.10.1083/jcb.200202048Search in Google Scholar

Mori, H., Summer, E.J., and Cline, K. (2001). Chloroplast TatC plays a direct role in thylakoid ΔpH-dependent protein transport. FEBS Lett. 501, 65–68.10.1016/S0014-5793(01)02626-6Search in Google Scholar

Mori, H., Summer, E.J., Ma, X., and Cline, K. (1999). Component specificity for the thylakoidal Sec and ΔpH-dependent protein transport pathways. J. Cell Biol. 146, 45–56.Search in Google Scholar

Motohashi, R., Nagata, N., Ito, T., Takahashi, S., Hobo, T., Yoshida, S., and Shinozaki, K. (2001). An essential role of a TatC homologue of a ΔpH-dependent protein transporter in thylakoid membrane formation during chloroplast development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 98, 10499–10504.10.1073/pnas.181304598Search in Google Scholar PubMed PubMed Central

Palmer, T. and Berks, B.C. (2012). The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 10, 483–496.10.1038/nrmicro2814Search in Google Scholar PubMed

Richter, S. and Brüser, T. (2005). Targeting of unfolded PhoA to the TAT translocon of Escherichia coli. J. Biol. Chem. 280, 42723–42730.10.1074/jbc.M509570200Search in Google Scholar PubMed

Richter, S., Lindenstrauss, U., Lücke, C., Bayliss, R., and Brüser, T. (2007). Functional Tat transport of unstructured, small, hydrophilic proteins. J. Biol. Chem. 282, 33257–33264.10.1074/jbc.M703303200Search in Google Scholar PubMed

Roffey, R.A. and Theg, S.M. (1996). Analysis of the import of carboxyl-terminal truncations of the 23-kilodalton subunit of the oxygen-evolving complex suggests that its structure is an important determinant for thylakoid transport. Plant Physiol. 111, 1329–1338.10.1104/pp.111.4.1329Search in Google Scholar PubMed PubMed Central

Sambrook, J. and Russell, D.W. (2001). Molecular Cloning: A Laboratory manual. 3rd Edition. Cold Spring Harbor, New York: Cold Spring Harbor Laboratories.Search in Google Scholar

Schägger, H. (2006). Tricine-SDS-PAGE. Nat. Protoc. 1, 16–22.10.1038/nprot.2006.4Search in Google Scholar PubMed

Schlesier, R. and Klösgen, R.B. (2010). Twin arginine translocation (Tat)-dependent protein transport: the passenger protein participates in the initial membrane binding step. Biol. Chem. 391, 1411–1417.10.1515/bc.2010.138Search in Google Scholar PubMed

Settles, A.M., Yonetani, A., Baron, A., Bush, D.R., Cline, K., and Martienssen, R. (1997). Sec-independent protein translocation by the maize Hcf106 protein. Science 278, 1467–1470.10.1126/science.278.5342.1467Search in Google Scholar PubMed

Shanmugham, A., Wong Fong Sang, H.W., Bollen, Y.J., and Lill, H. (2006). Membrane binding of twin arginine preproteins as an early step in translocation. Biochemistry 45, 2243–2249.10.1021/bi052188aSearch in Google Scholar PubMed

Theg, S.M., Cline, K., Finazzi, G., and Wollman, F.A. (2005). The energetics of the chloroplast Tat protein transport pathway revisited. Trends Plant Sci. 10, 153–154.10.1016/j.tplants.2005.02.001Search in Google Scholar PubMed

Walker, M.B., Roy, L.M., Coleman, E., Voelker, R., and Barkan, A. (1999). The maize tha4 gene functions in sec-independent protein transport in chloroplasts and is related to hcf106, tatA, and tatB. J. Cell Biol. 147, 267–276.10.1083/jcb.147.2.267Search in Google Scholar PubMed PubMed Central