The twin-arginine translocation (Tat) protein export pathway

The twin-arginine translocation (Tat) protein export system is present in the cytoplasmic membranes of most bacteria and archaea and has the highly unusual property of transporting fully folded proteins. The system must therefore provide a transmembrane pathway that is large enough to allow the passage of structured macromolecular substrates of different sizes but that maintains the impermeability of the membrane to ions. In the Gram-negative bacterium Escherichia coli, this complex task can be achieved by using only three small membrane proteins: TatA, TatB and TatC. In this Review, we summarize recent advances in our understanding of how this remarkable machine operates.

[1]  A. Driessen,et al.  Bacterial protein translocation: kinetic and thermodynamic role of ATP and the protonmotive force. , 1992, Trends in biochemical sciences.

[2]  Tracy Palmer,et al.  The twin-arginine translocation pathway is a major route of protein export in Streptomyces coelicolor , 2006, Proceedings of the National Academy of Sciences.

[3]  Neal Whitaker,et al.  Interconvertibility of lipid‐ and translocon‐bound forms of the bacterial Tat precursor pre‐SufI , 2009, Molecular microbiology.

[4]  Anna-Carina Jungkamp,et al.  TatB Functions as an Oligomeric Binding Site for Folded Tat Precursor Proteins , 2010, Molecular biology of the cell.

[5]  T. Brüser,et al.  Targeting of Unfolded PhoA to the TAT Translocon of Escherichia coli* , 2005, Journal of Biological Chemistry.

[6]  W. Doerrler,et al.  Inefficient Tat-Dependent Export of Periplasmic Amidases in an Escherichia coli Strain with Mutations in Two DedA Family Genes , 2009, Journal of bacteriology.

[7]  Y. Kimura,et al.  Myxococcus xanthus twin-arginine translocation system is important for growth and development , 2006, Archives of Microbiology.

[8]  Escherichia coli tatC mutations that suppress defective twin-arginine transporter signal peptides. , 2007, Journal of molecular biology.

[9]  D. Bush,et al.  Sec-independent protein translocation by the maize Hcf106 protein. , 1997, Science.

[10]  R. Bayliss,et al.  Functional Tat Transport of Unstructured, Small, Hydrophilic Proteins* , 2007, Journal of Biological Chemistry.

[11]  P. Kroneck,et al.  N2O binding at a [4Cu:2S] copper–sulphur cluster in nitrous oxide reductase , 2011, Nature.

[12]  B. Berks,et al.  Overlapping functions of components of a bacterial Sec‐independent protein export pathway , 1998, The EMBO journal.

[13]  M. Vasil,et al.  Effects of the twin-arginine translocase on secretion of virulence factors, stress response, and pathogenesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[14]  B. Berks,et al.  TatBC, TatB, and TatC form structurally autonomous units within the twin arginine protein transport system of Escherichia coli , 2007, FEBS letters.

[15]  Romé Voulhoux,et al.  In vivo dissection of the Tat translocation pathway in Escherichia coli. , 2002, Journal of molecular biology.

[16]  R. Herrmann,et al.  The Rieske Fe/S protein of the cytochrome b6/f complex in chloroplasts: missing link in the evolution of protein transport pathways in chloroplasts? , 2001, The Journal of biological chemistry.

[17]  Frank Sargent,et al.  The Tat protein translocation pathway and its role in microbial physiology. , 2003, Advances in microbial physiology.

[18]  Y. Bollen,et al.  Membrane binding of twin arginine preproteins as an early step in translocation. , 2006, Biochemistry.

[19]  G. Condemine,et al.  Novel mechanism of outer membrane targeting of proteins in Gram‐negative bacteria , 2008, Molecular microbiology.

[20]  K. Cline,et al.  Evidence for a loop mechanism of protein transport by the thylakoid Delta pH pathway , 1998, FEBS letters.

[21]  D. Lavrov,et al.  Molecular Phylogeny Restores the Supra-Generic Subdivision of Homoscleromorph Sponges (Porifera, Homoscleromorpha) , 2010, PloS one.

[22]  D. Siddavattam,et al.  Organophosphate Hydrolase in Brevundimonas diminuta Is Targeted to the Periplasmic Face of the Inner Membrane by the Twin Arginine Translocation Pathway , 2009, Journal of bacteriology.

[23]  Koreaki Ito,et al.  Post-liberation cleavage of signal peptides is catalyzed by the site-2 protease (S2P) in bacteria , 2011, Proceedings of the National Academy of Sciences.

[24]  W. Neupert,et al.  A pathway of protein translocation in mitochondria mediated by the AAA-ATPase Bcs1. , 2011, Molecular cell.

[25]  F. Sargent Constructing the wonders of the bacterial world: biosynthesis of complex enzymes. , 2007, Microbiology.

[26]  P. Kroneck,et al.  The unprecedented nos gene cluster of Wolinella succinogenes encodes a novel respiratory electron transfer pathway to cytochrome c nitrous oxide reductase , 2004, FEBS letters.

[27]  B. Wallace,et al.  Characterization and membrane assembly of the TatA component of the Escherichia coli twin-arginine protein transport system. , 2002, Biochemistry.

[28]  Gunnar von Heijne,et al.  Competition between Sec‐ and TAT‐dependent protein translocation in Escherichia coli , 1999, The EMBO journal.

[29]  B. Berks,et al.  Cysteine Scanning Mutagenesis and Topological Mapping of the Escherichia coli Twin-Arginine Translocase TatC Component , 2007, Journal of bacteriology.

[30]  A. Bolhuis,et al.  TatB and TatC Form a Functional and Structural Unit of the Twin-arginine Translocase from Escherichia coli * , 2001, The Journal of Biological Chemistry.

[31]  Sierd Bron,et al.  Two minimal Tat translocases in Bacillus , 2004, Molecular microbiology.

[32]  Søren Brunak,et al.  Prediction of twin-arginine signal peptides , 2005, BMC Bioinformatics.

[33]  A. Coelho,et al.  The [NiFeSe] hydrogenase from Desulfovibrio vulgaris Hildenborough is a bacterial lipoprotein lacking a typical lipoprotein signal peptide , 2007, FEBS letters.

[34]  George Georgiou,et al.  Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[35]  J. Palacios,et al.  The twin‐arginine translocation (Tat) system is essential for Rhizobium–legume symbiosis , 2003, Molecular microbiology.

[36]  Matthias Müller,et al.  Co-translocation of a Periplasmic Enzyme Complex by a Hitchhiker Mechanism through the Bacterial Tat Pathway* , 1999, The Journal of Biological Chemistry.

[37]  M. Freeman,et al.  Rhomboid protease AarA mediates quorum-sensing in Providencia stuartii by activating TatA of the twin-arginine translocase , 2007, Proceedings of the National Academy of Sciences.

[38]  S. Mendel,et al.  Expression of the bifunctional Bacillus subtilis TatAd protein in Escherichiacoli reveals distinct TatA/B-family and TatB-specific domains , 2011, Archives of Microbiology.

[39]  K. Cline,et al.  Evidence for a dynamic and transient pathway through the TAT protein transport machinery , 2007, The EMBO journal.

[40]  S. Hall,et al.  Roles of the twin-arginine translocase and associated chaperones in the biogenesis of the electron transport chains of the human pathogen Campylobacter jejuni. , 2010, Microbiology.

[41]  Jessica C Kissinger,et al.  Adaptation of protein secretion to extremely high‐salt conditions by extensive use of the twin‐arginine translocation pathway , 2002, Molecular microbiology.

[42]  Matthias Müller,et al.  Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. , 2003, Molecular cell.

[43]  Si-Yu Li,et al.  Coexpression of TorD enhances the transport of GFP via the TAT pathway. , 2006, Journal of biotechnology.

[44]  K. Cline,et al.  Oligomers of Tha4 Organize at the Thylakoid Tat Translocase during Protein Transport* , 2006, Journal of Biological Chemistry.

[45]  R. Mould,et al.  A proton gradient is required for the transport of two lumenal oxygen-evolving proteins across the thylakoid membrane. , 1991, The Journal of biological chemistry.

[46]  G. Georgiou,et al.  Positive Selection for Loss-of-Function tat Mutations Identifies Critical Residues Required for TatA Activity , 2005, Journal of bacteriology.

[47]  Z. Ding,et al.  Agrobacterium tumefaciens Twin-Arginine-Dependent Translocation Is Important for Virulence, Flagellation, and Chemotaxis but Not Type IV Secretion , 2003, Journal of bacteriology.

[48]  R. Berry,et al.  Variable stoichiometry of the TatA component of the twin-arginine protein transport system observed by in vivo single-molecule imaging , 2008, Proceedings of the National Academy of Sciences.

[49]  M. Krehenbrink,et al.  Identification of protein secretion systems and novel secreted proteins in Rhizobium leguminosarum bv. viciae , 2008, BMC Genomics.

[50]  G. Sprenger,et al.  Genetic Analysis of Pathway Specificity during Posttranslational Protein Translocation across the Escherichia coli Plasma Membrane , 2003, Journal of bacteriology.

[51]  D. Richardson,et al.  Signal peptide-chaperone interactions on the twin-arginine protein transport pathway. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[52]  H. Andrews-Polymenis,et al.  The CpxR/CpxA Two-component System Up-regulates Two Tat-dependent Peptidoglycan Amidases to Confer Bacterial Resistance to Antimicrobial Peptide* , 2010, The Journal of Biological Chemistry.

[53]  K. Cline,et al.  Requirement of a Tha4-conserved Transmembrane Glutamate in Thylakoid Tat Translocase Assembly Revealed by Biochemical Complementation* , 2003, Journal of Biological Chemistry.

[54]  So Iwata,et al.  Molecular Basis of Proton Motive Force Generation: Structure of Formate Dehydrogenase-N , 2002, Science.

[55]  K. Cline,et al.  Localization and integration of thylakoid protein translocase subunit cpTatC. , 2009, The Plant journal : for cell and molecular biology.

[56]  Helen R Saibil,et al.  Structural analysis of substrate binding by the TatBC component of the twin-arginine protein transport system , 2009, Proceedings of the National Academy of Sciences.

[57]  N. Alder,et al.  Energetics of Protein Transport across Biological Membranes A Study of the Thylakoid ΔpH-Dependent/cpTat Pathway , 2003, Cell.

[58]  N. Hand,et al.  Translocation of proteins across archaeal cytoplasmic membranes. , 2004, FEMS microbiology reviews.

[59]  Genetic Evidence for a TatC Dimer at the Core of the Escherichia coli Twin Arginine (Tat) Protein Translocase , 2011, Journal of Molecular Microbiology and Biotechnology.

[60]  Kieran Dilks,et al.  Genetic and Biochemical Analysis of the Twin-Arginine Translocation Pathway in Halophilic Archaea , 2005, Journal of bacteriology.

[61]  G. Sprenger,et al.  Isolation and Characterization of Bifunctional Escherichia coli TatA Mutant Proteins That Allow Efficient Tat-dependent Protein Translocation in the Absence of TatB* , 2005, Journal of Biological Chemistry.

[62]  Michael Hecker,et al.  The twin arginine protein transport pathway exports multiple virulence proteins in the plant pathogen Streptomyces scabies , 2010, Molecular microbiology.

[63]  S. Cole,et al.  Inactivation of Rv2525c, a Substrate of the Twin Arginine Translocation (Tat) System of Mycobacterium tuberculosis, Increases β-Lactam Susceptibility and Virulence , 2006, Journal of bacteriology.

[64]  J. Anné,et al.  The twin‐arginine translocation pathway is necessary for correct membrane insertion of the Rieske Fe/S protein in Legionella pneumophila , 2007, FEBS letters.

[65]  R. Turner,et al.  The Twin-arginine Leader-binding Protein, DmsD, Interacts with the TatB and TatC Subunits of the Escherichia coli Twin-arginine Translocase* , 2003, Journal of Biological Chemistry.

[66]  C. Santini,et al.  Dual Topology of the Escherichia coli TatA Protein* , 2004, Journal of Biological Chemistry.

[67]  S. Létoffé,et al.  Bacteria capture iron from heme by keeping tetrapyrrol skeleton intact , 2009, Proceedings of the National Academy of Sciences.

[68]  Peter D. Newell,et al.  Conservation of the Pho regulon in Pseudomonas fluorescens Pf0-1 , 2006, Applied and Environmental Microbiology.

[69]  K. Cline,et al.  Chloroplast TatC plays a direct role in thylakoid ΔpH‐dependent protein transport , 2001 .

[70]  B. Berks A common export pathway for proteins binding complex redox cofactors? , 1996, Molecular microbiology.

[71]  M. Fontecave,et al.  Cobalt Stress in Escherichia coli , 2007, Journal of Biological Chemistry.

[72]  G. Giordano,et al.  TorD, A Cytoplasmic Chaperone That Interacts with the Unfolded Trimethylamine N-Oxide Reductase Enzyme (TorA) in Escherichia coli * , 1998, The Journal of Biological Chemistry.

[73]  Matthias Müller,et al.  Mapping Precursor-binding Site on TatC Subunit of Twin Arginine-specific Protein Translocase by Site-specific Photo Cross-linking* , 2012, The Journal of Biological Chemistry.

[74]  K. Cline,et al.  A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid ΔpH/Tat translocase , 2002, The Journal of cell biology.

[75]  Frank Sargent,et al.  A subset of bacterial inner membrane proteins integrated by the twin‐arginine translocase , 2003, Molecular microbiology.

[76]  F. Pfeiffer,et al.  Mutational and Bioinformatic Analysis of Haloarchaeal Lipobox-Containing Proteins , 2010, Archaea.

[77]  W. Schliebs,et al.  Peroxisomal protein import and ERAD: variations on a common theme , 2010, Nature Reviews Molecular Cell Biology.

[78]  T. Palmer,et al.  Investigating lipoprotein biogenesis and function in the model Gram‐positive bacterium Streptomyces coelicolor , 2010, Molecular microbiology.

[79]  Hongwei Li,et al.  Solution NMR structure of the TatA component of the twin-arginine protein transport system from gram-positive bacterium Bacillus subtilis. , 2010, Journal of the American Chemical Society.

[80]  S. Grage,et al.  Membrane alignment of the pore-forming component TatA(d) of the twin-arginine translocase from Bacillus subtilis resolved by solid-state NMR spectroscopy. , 2010, Journal of the American Chemical Society.

[81]  C. Lange,et al.  Structure analysis of the protein translocating channel TatA in membranes using a multi-construct approach. , 2007, Biochimica et biophysica acta.

[82]  P. Jagtap,et al.  The Bdellovibrio bacteriovorus twin-arginine transport system has roles in predatory and prey-independent growth. , 2011, Microbiology.

[83]  Helen R Saibil,et al.  The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[84]  K. Cline,et al.  18 - The Sec and Tat Protein Translocation Pathways in Chloroplasts , 2007 .

[85]  M. DeLisa,et al.  Visualizing Interactions along the Escherichia coli Twin-Arginine Translocation Pathway Using Protein Fragment Complementation , 2010, PloS one.

[86]  W. Wickner,et al.  Functional reconstitution of bacterial Tat translocation in vitro , 2001, The EMBO journal.

[87]  Matthias Müller,et al.  Early Contacts between Substrate Proteins and TatA Translocase Component in Twin-arginine Translocation* , 2011, The Journal of Biological Chemistry.

[88]  M. Hecker,et al.  TatC Is a Specificity Determinant for Protein Secretion via the Twin-arginine Translocation Pathway* , 2000, The Journal of Biological Chemistry.

[89]  K. Cline,et al.  Thylakoid ΔpH-dependent precursor proteins bind to a cpTatC–Hcf106 complex before Tha4-dependent transport , 2001, The Journal of cell biology.

[90]  Topological studies on the twin-arginine translocase component TatC. , 2004, FEMS microbiology letters.

[91]  G. W. Vuister,et al.  Structural diversity in twin-arginine signal peptide-binding proteins , 2007, Proceedings of the National Academy of Sciences.

[92]  B. Berks,et al.  A naturally occurring bacterial Tat signal peptide lacking one of the ‘invariant’ arginine residues of the consensus targeting motif , 2001, FEBS letters.

[93]  S. Brink,et al.  Pathway specificity for a ΔpH‐dependent precursor thylakoid lumen protein is governed by a 'sec‐avoidance’ motif in the transfer peptide and a 'sec‐incompatible’ mature protein , 1997, The EMBO journal.

[94]  H. Vogel,et al.  Towards understanding the Tat translocation mechanism through structural and biophysical studies of the amphipathic region of TatA from Escherichia coli. , 2011, Biochimica et biophysica acta.

[95]  T. Palmer,et al.  Coordinating assembly and export of complex bacterial proteins , 2004, The EMBO journal.

[96]  Colin Robinson,et al.  Tat‐dependent targeting of Rieske iron‐sulphur proteins to both the plasma and thylakoid membranes in the cyanobacterium Synechocystis PCC6803 , 2008, Molecular microbiology.

[97]  B. Berks,et al.  Cysteine Scanning Mutagenesis and Disulfide Mapping Studies of the TatA Component of the Bacterial Twin Arginine Translocase* , 2007, Journal of Biological Chemistry.

[98]  T. Lamkemeyer,et al.  Role of the Twin-Arginine Translocation Pathway in Staphylococcus , 2009, Journal of bacteriology.

[99]  Pantelis G. Bagos,et al.  Combined prediction of Tat and Sec signal peptides with hidden Markov models , 2010, Bioinform..

[100]  T. Palmer,et al.  Dissecting the complete lipoprotein biogenesis pathway in Streptomyces scabies , 2011, Molecular microbiology.

[101]  T. Palmer,et al.  Proteolytic processing of Escherichia coli twin-arginine signal peptides by LepB , 2009, Archives of Microbiology.

[102]  J. Anné,et al.  The importance of the twin-arginine translocation pathway for bacterial virulence. , 2008, Trends in microbiology.

[103]  B. Berks,et al.  Oligomeric properties and signal peptide binding by Escherichia coli Tat protein transport complexes. , 2002, Journal of molecular biology.

[104]  T. Palmer,et al.  Role of the Escherichia coli Tat pathway in outer membrane integrity , 2003, Molecular microbiology.

[105]  T. Palmer,et al.  Escherichia coli TatA and TatB Proteins Have N-out, C-in Topology in Intact Cells* , 2012, The Journal of Biological Chemistry.

[106]  S. M. Musser,et al.  Two electrical potential–dependent steps are required for transport by the Escherichia coli Tat machinery , 2007, The Journal of cell biology.

[107]  B. Berks,et al.  The Twin Arginine Consensus Motif of Tat Signal Peptides Is Involved in Sec-independent Protein Targeting in Escherichia coli * , 2000, The Journal of Biological Chemistry.

[108]  B. Berks,et al.  Truncation Analysis of TatA and TatB Defines the Minimal Functional Units Required for Protein Translocation , 2002, Journal of bacteriology.

[109]  D. Newman,et al.  Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[110]  A. Bolhuis,et al.  Bioenergetic requirements of a Tat‐dependent substrate in the halophilic archaeon Haloarcula hispanica , 2008, The FEBS journal.

[111]  F. Tamanoi,et al.  Molecular machines involved in protein transport across cellular membranes , 2007 .

[112]  K. Cline,et al.  Clustering of C-terminal stromal domains of Tha4 homo-oligomers during translocation by the Tat protein transport system. , 2009, Molecular biology of the cell.

[113]  B. Berks,et al.  Sec-independent Protein Translocation in Escherichia coli , 1999, The Journal of Biological Chemistry.

[114]  B. Berks,et al.  The SoxYZ Complex Carries Sulfur Cycle Intermediates on a Peptide Swinging Arm* , 2007, Journal of Biological Chemistry.

[115]  Frank Sargent,et al.  Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. , 2005, Current opinion in microbiology.

[116]  B. Berks,et al.  Subunit Organization in the TatA Complex of the Twin Arginine Protein Translocase , 2009, The Journal of Biological Chemistry.

[117]  B. Berks,et al.  Characterisation of the membrane‐extrinsic domain of the TatB component of the twin arginine protein translocase , 2011, FEBS letters.

[118]  I. Oresnik,et al.  The Twin Arginine Transport System Appears To Be Essential for Viability in Sinorhizobium meliloti , 2010, Journal of bacteriology.

[119]  B. Berks,et al.  Cysteine-scanning Mutagenesis and Disulfide Mapping Studies of the Conserved Domain of the Twin-arginine Translocase TatB Component* , 2006, Journal of Biological Chemistry.

[120]  T. Brüser,et al.  The TatBC complex formation suppresses a modular TatB‐multimerization in Escherichia coli , 2007, FEBS letters.

[121]  Julie Bachmann,et al.  The Rieske protein from Paracoccus denitrificans is inserted into the cytoplasmic membrane by the twin‐arginine translocase , 2006, The FEBS journal.

[122]  F. Thompson,et al.  Vibrio2009: the third international conference on the biology of Vibrios , 2010, Molecular microbiology.

[123]  B. Berks,et al.  Novel Phenotypes of Escherichia coli tat Mutants Revealed by Global Gene Expression and Phenotypic Analysis* , 2004, Journal of Biological Chemistry.

[124]  K. Cline,et al.  Component Specificity for the Thylakoidal Sec and Delta Ph–Dependent Protein Transport Pathways , 1999, The Journal of cell biology.

[125]  W. Zumft Biogenesis of the Bacterial Respiratory CuA, Cu-S Enzyme Nitrous Oxide Reductase , 2006, Journal of Molecular Microbiology and Biotechnology.

[126]  O. Kuipers,et al.  A Minimal Tat System from a Gram-positive Organism , 2008, Journal of Biological Chemistry.

[127]  A. Bolhuis,et al.  The tatC gene cluster is essential for viability in halophilic archaea. , 2006, FEMS microbiology letters.

[128]  E. Hartmann,et al.  Prokaryotic Utilization of the Twin-Arginine Translocation Pathway: a Genomic Survey , 2003, Journal of bacteriology.

[129]  K. Cline,et al.  Efficient Twin Arginine Translocation (Tat) Pathway Transport of a Precursor Protein Covalently Anchored to Its Initial cpTatC Binding Site* , 2006, Journal of Biological Chemistry.

[130]  B. Berks,et al.  Escherichia coli Strains Blocked in Tat-Dependent Protein Export Exhibit Pleiotropic Defects in the Cell Envelope , 2001, Journal of bacteriology.

[131]  A. Bolhuis Protein transport in the halophilic archaeon Halobacterium sp. NRC-1: a major role for the twin-arginine translocation pathway? , 2002, Microbiology.

[132]  M. Paetzel,et al.  Crystal structure of a bacterial signal peptidase in complex with a β-lactam inhibitor , 1998, Nature.

[133]  C. Robinson,et al.  Large-scale translocation reversal within the thylakoid Tat system in vivo , 2005, The Journal of cell biology.

[134]  George Georgiou,et al.  A periplasmic fluorescent reporter protein and its application in high-throughput membrane protein topology analysis. , 2004, Journal of molecular biology.

[135]  D. Scanlan,et al.  The Tat protein export pathway and its role in cyanobacterial metalloprotein biosynthesis. , 2011, FEMS microbiology letters.

[136]  Matthias Müller,et al.  Following the Path of a Twin-arginine Precursor along the TatABC Translocase of Escherichia coli* , 2008, Journal of Biological Chemistry.

[137]  K. Cline,et al.  The Thylakoid Proton Gradient Promotes an Advanced Stage of Signal Peptide Binding Deep within the Tat Pathway Receptor Complex* , 2007, Journal of Biological Chemistry.

[138]  N. Vasisht,et al.  Structure of TatA Paralog, TatE, Suggests a Structurally Homogeneous Form of Tat Protein Translocase That Transports Folded Proteins of Differing Diameter , 2011, The Journal of Biological Chemistry.

[139]  Conrad Bessant,et al.  Protein-folding location can regulate manganese-binding versus copper- or zinc-binding , 2008, Nature.

[140]  G. Giordano,et al.  Requirement for phospholipids of the translocation of the trimethylamine N‐oxide reductase through the Tat pathway in Escherichia coli , 1999, FEBS letters.

[141]  M. Saier,et al.  Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system , 2002, Archives of Microbiology.

[142]  Tom A. Rapoport,et al.  Sec61/SecY-Mediated Protein Translocation Across Membranes , 2012 .

[143]  T. Brüser,et al.  An alternative model of the twin arginine translocation system. , 2003, Microbiological research.

[144]  A. Potter,et al.  Salmonella enterica Serovar Enteritidis tatB and tatC Mutants Are Impaired in Caco-2 Cell Invasion In Vitro and Show Reduced Systemic Spread in Chickens , 2010, Infection and Immunity.

[145]  A. Bolhuis,et al.  The Escherichia coli twin-arginine translocation apparatus incorporates a distinct form of TatABC complex, spectrum of modular TatA complexes and minor TatAB complex. , 2005, Journal of molecular biology.