Structure-function studies of a protein-transporting transmembrane channel
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1 University of Oxford Department of Biochemistry D.Phil. studentship in Molecular ell Biology Structure-function studies of a protein-transporting transmembrane channel Periplasm Tat TatB TatA ytoplasm Transport of proteins across biological membranes is one of the fundamental problems in molecular cell biology. Proteins destined for transmembrane transport are usually synthesised with -terminal signal sequences, termed signal peptides, which direct the protein to a specific transporter complex in the membrane. Exported proteins in both bacteria and eukaryotic cells are normally transported in an unfolded state by the well-characterised Sec mechanism. However, we and others have demonstrated that bacteria possess a second general pathway for protein transport across the cytoplasmic membrane that is completely distinct from the Sec apparatus. Proteins are targeted to this Sec-independent pathway by signal sequences harbouring consecutive, invariant arginine residues and consequently this protein transport apparatus has been termed the Tat (twin arginine translocation) system. The most remarkable and unusual feature of the Tat pathway is that it functions to transport folded proteins. The Tat translocase thus faces the formidable challenge of moving a structured macromolecular substrate of up to 70Å in diameter across the bacterial cytoplasmic membrane without rendering that membrane freely permeable to protons and other ions. This combination of operating parameters is so demanding that the Tat apparatus is the only known mechanism for moving folded proteins across ionically-tight membranes. Indeed, the Tat proteins show no sequence similarity to the components of other
2 membrane transporters. Taken together these considerations suggest that the Tat system operates by a unique and intriguing mechanism. The substrates of the Tat pathway are often proteins that bind cofactor molecules in the cytoplasm, and are thus folded, prior to export. Such periplasmic cofacto r-containing proteins are essential for most types of bacterial respiratory energy metabolism. The Tat pathway is also involved in cell division, cell motility, symbiotic nitrogen fixation and the virulence of both animal and plant pathogens. Other functions are likely, particularly in organisms such as Streptomycetes and Halobacteria where the majority of exported substrates are Tat-targeted. The Tat system has potential for biotechnological/biomedical exploitation. It is possible to use the Tat pathway to secrete proteins that are recalcitrant to transport by the alternative Sec pathway or that require maturation in the cytoplasm. In addition, since Tat has been shown to be an important virulence determinant for pathogenic bacteria but is not found in humans, it is a potential target for antimicrobial drugs. TatB TatA Tat Figure 1. Predicted secondary structure and topological organisation of the essential Tat components The predicted secondary structures and topological organisation of the essential Tat proteins of our model organism, Escherichia coli, are depicted in Figure 1. Our biochemical studies have allowed overexpression, purification and initial biochemical and structural characterisation (Figure 2) of the transporter complexes formed by these proteins. We now seek a molecular understanding of the unique operational features of the Tat system. To this end we are looking for a highly motivated individual with an interest in structural biology, protein chemistry or molecular cell biology to undertake doctoral studies on the Tat protein translocase in the laboratory of Dr.Ben Berks. The project aims to undertake structural (in the broadest sense) and functional studies of the Tat transporter with special emphasis on the channel-forming TatA component. It is anticipated that the project will involve: Purification and characterisation of membrane proteins.
3 In vitro and in vivo protein transport assays. Protein expression, mutagenesis and engineering Participation in our programme of direct structure determination by crystallographic and single particle electron microscopic methods. However, we operate a problem- rather than techniques-driven approach and are therefore willing to employ any useful methodology. The project can be tailored to a certain extent to the interests of the student and the exact programme of work will take into account the state of research in this fastmoving field. This is a BBSR ommittee studentship and is associated with an enhanced stipend. ote, however, that it does not cover full costs for non-uk students and you need to check your eligibility with the Departmental Graduate Studies Office. The Department of Biochemistry is one of the largest and most successful biochemistry departments in Europe. It is, accordingly, well resourced. The Department is located in the main University Science Area in the historic centre of Oxford and is adjacent to the University Parks (the Berks group is on the 6 th floor of the main tower block and has arguably the best views in Oxford). There are currently three postdoctoral research workers and two D.Phil. students in the Berks group who work on the Tat project. In addition we work closely with external collaborators (including Dr.Tracy Palmer at the John Innes entre in orwich, and Prof.Helen Saibil at Birkbeck ollege, London) and other groups at Oxford. Group members are expected to take part in international scientific meetings. Figure 2. Initial structural analysis of a TatAB complex by negative stain electron microscopy. Six characteristic averaged views (density projections) out of 100 classes are shown. The scale bar has a length of 100Å. From Sargent et al., (2001).
4 Reviews Berks, B.., Sargent, F., and Palmer, T. (2000) The Tat protein export pathway. Mol. Microbiol. 35: Sargent, F., Berks, B.., and Palmer, T. (2002) Assembly of membrane-bound respiratory complexes by the Tat protein targeting system. Arch.Microbiol. 178: Berks, B.., Palmer, T., and Sargent, F. (2003) The Tat protein translocation pathway and its role in microbial physiology. Adv.Microb.Physiol. 47: Further Tat publications from our group Berks, B.. (1996) A common export pathway for proteins binding complex redox cofactors? Mol.Microbiol. 22: Sargent, F., Bogsch, E., Stanley,.R., Wexler, M., Robinson,., Berks, B.., and Palmer, T. (1998) Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 17: Bogsch, E., Sargent, F., Stanley,.R., Berks, B.., Robinson,., and Palmer, T. (1998) An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria (ommunication). J.Biol.hem. 273: Wexler, M., Bogsch, E., Klösgen, R.B., Palmer, T., Robinson,., and Berks, B.. (1998) Targeting signals for a bacterial Sec-independent export system direct plant thylakoid import by the ph pathway. FEBS Lett. 431: Sargent, F., Stanley,.R., Berks, B.., and Palmer, T. (1999) Sec-independent protein translocation in Escherichia coli: a distinct and pivotal role for the TatB protein. J. Biol. hem. 274: Stanley,.R., Palmer, T., and Berks, B.. (2000) The twin-arginine consensus motif of Tat signal peptides is involved in Sec-independent protein targeting in Escherichia coli. J. Biol. hem. 275: Wexler, M., Sargent, F., Jack, R.L., Stanley,.R., Bogsch, E., Robinson,., Berks, B.., and Palmer, T. (2000) TatD is a metal binding protein with DAse activity. o requirement for TatD-family proteins in Secindependent protein export. J. Biol. hem. 275: Berks, B.., Sargent, F., de Leeuw, E., Hinsley, A.P., Stanley,.R., Jack, R.L., Buchanan, G., and Palmer, T. (2000) A novel protein transport system involved in the biogenesis of bacterial electron transfer chains. Biochim. Biophys. Acta 1459: Stanley,.R., Findlay, K., Berks, B.., and Palmer, T. (2001) Escherichia coli strains blocked in Tat-dependent protein export exhibit a defective cell separation morphology. J.Bacteriol. 183: Jack, R.L., Sargent, F., Berks, B.., Sawers, G., and Palmer, T. (2001) onstituitive expression of the Escherichia coli tat genes indicates an important role for the twin-arginine translocase during aerobic and anaerobic growth. J.Bacteriol. 183: Hinsley, A.P., Stanley,.R., Palmer, T., and Berks, B.. (2001) A naturally-occurring bacterial Tat signal peptide lacking one of the invariant arginine residues of the consensus targeting motif. FEBS Lett. 49:
5 Sargent, F., Gohlke, U., de Leeuw, E., Stanley,.R., Palmer, T., Saibil, H.R., and Berks, B.. (2001) Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure (Priority Publication). Eur.J.Biochem. 268: de Leeuw, E., Porcelli, I., Sargent, F., Palmer, T., and Berks, B.. (2001) Membrane interactions and selfassociation of the TatA and TatB components of the twin-arginine translocation pathway. FEBS Lett. 506: Buchanan, G., Sargent, F., Berks, B.., and Palmer, T. (2001) A genetic screen for suppressors of Escherichia coli Tat signal peptide mutations establishes a critical role for the second arginine within the twin-arginine motif. Arch. Microbiol. 177: Stanley,.R., Sargent, F., Buchanan, G., Shi, J., Stewart, V., Palmer, T., and Berks, B.. (2002) Behaviour of topological marker proteins targeted to the Tat protein transport pathway. Mol Microbiol. 43: Buchanan, G., de Leeuw, E., Berks, B.., Sargent, F., and Palmer, T. (2002) Functional complexity of the twinarginine translocase Tat component revealed by site-directed mutagenesis. Mol Microbiol. 43: de Leeuw, E., Granjon, T., Porcelli, I., Alami, M., arr, S.B., Müller, M., Sargent, F., Palmer, T., and Berks, B.. (2002) Oligomeric properties and signal peptide binding by Escherichia coli Tat protein transport complexes. J.Mol.Biol. 322: Lee, P.A., Buchanan, G., Stanley,.R., Berks, B.., and Palmer, T. (2002) Truncation analysis of TatA and TatB defines the minimal functional units required for protein translocation. J.Bacteriol. 184: Porcelli, I., de Leeuw, E., Wallis, R., van den Brink-van der Laan, E., de Kruijff, B., Wallace, B.A., Palmer, T., and Berks, B.. (2002) haracterisation and membrane assembly of the TatA component of the Escherichia coli twin-arginine protein transport system. Biochemistry 41: Hicks, M.G., de Leeuw, E., Porcelli, I., Buchanan, G., Berks, B.., and Palmer, T. (2003) The Escherichia coli twin-arginine translocase: conserved residues of TatA and TatB family components involved in protein transport. FEBS Lett. 539: Palmer, T., Sargent, F., and Berks, B.. (2004) Light traffic: photo-crosslinking a novel transport system. Trends in Biochemical Sciences 29:
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