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Nuclease colicins and their immunity proteins

  • Grigorios Papadakos (a1), Justyna A. Wojdyla (a1) and Colin Kleanthous (a1)
  • DOI:
  • Published online: 16 November 2011

It is more than 80 years since Gratia first described ‘a remarkable antagonism between two strains of Escherichia coli’. Shown subsequently to be due to the action of proteins (or peptides) produced by one bacterium to kill closely related species with which it might be cohabiting, such bacteriocins have since been shown to be commonplace in the internecine warfare between bacteria. Bacteriocins have been studied primarily from the twin perspectives of how they shape microbial communities and how they penetrate bacteria to kill them. Here, we review the modes of action of a family of bacteriocins that cleave nucleic acid substrates in E. coli, known collectively as nuclease colicins, and the specific immunity (inhibitor) proteins that colicin-producing organisms make in order to avoid committing suicide. In a process akin to targeting in mitochondria, nuclease colicins engage in a variety of cellular associations in order to translocate their cytotoxic domains through the cell envelope to the cytoplasm. As well as informing on the process itself, the study of nuclease colicin import has also illuminated functional aspects of the host proteins they parasitize. We also review recent studies where nuclease colicins and their immunity proteins have been used as model systems for addressing fundamental problems in protein folding and protein–protein interactions, areas of biophysics that are intimately linked to the role of colicins in bacterial competition and to the import process itself.

Corresponding author
*Address for correspondence: Professor C. Kleanthous, Department of Biology, University of York, Wentworth Way, Heslington, York YO10 5DD, UK. Tel.: +44-1904-328820; Fax: +44-1904-328825; Email:
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G. Anderluh & J. H. Lakey (2008). Disparate proteins use similar architectures to damage membranes. Trends in Biochemical Sciences 33, 482490.

T. Arnold , K. Zeth & D. Linke (2009). Structure and function of colicin S4, a colicin with a duplicated receptor-binding domain. Journal of Biological Chemistry 284, 64036413.

T. G. Baboolal , M. J. Conroy , K. Gill , H. Ridley , V. Visudtiphole , P. A. Bullough & J. H. Lakey (2008). Colicin N binds to the periphery of its receptor and translocator, outer membrane protein F. Structure 16, 371379.

A. Barneoud-Arnoulet , H. Barreteau , T. Touze , D. Mengin-Lecreulx , R. Lloubes & D. Duche (2010a). Toxicity of the colicin M catalytic domain exported to the periplasm is FkpA independent. Journal of Bacteriology 192, 52125219.

A. Barneoud-Arnoulet , M. Gavioli , R. Lloubes & E. Cascales (2010b). Interaction of the colicin K bactericidal toxin with components of its import machinery in the periplasm of Escherichia coli. Journal of Bacteriology 192, 59345942.

R. Baron , S. E. Wong , C. A. De Oliveira & J. A. Mccammon (2008). E9-Im9 colicin DNase-immunity protein biomolecular association in water: a multiple-copy and accelerated molecular dynamics simulation study. Journal of Physical Chemistry B 112, 1680216814.

H. Barreteau , A. Bouhss , F. Gerard , D. Duche , B. Boussaid , D. Blanot , R. Lloubes , D. Mengin-Lecreulx & T. Touze (2010). Deciphering the catalytic domain of colicin M, a peptidoglycan lipid II-degrading enzyme. Journal of Biological Chemistry 285, 1237812389.

H. Benedetti , M. Frenette , D. Baty , M. Knibiehler , F. Pattus & C. Lazdunski (1991). Individual domains of colicins confer specificity in colicin uptake, in pore-properties and in immunity requirement. Journal of Molecular Biology 217, 429439.

D. A. Bonsor , O. Hecht , M. Vankemmelbeke , A. Sharma , A. M. Krachler , N. G. Housden , K. J. Lilly , R. James , G. R. Moore & C. Kleanthous (2009a). Allosteric β-propeller signalling in TolB and its manipulation by translocating colicins. EMBO Journal 28, 28462857.

J. P. Bourdineaud , H. P. Fierobe , C. Lazdunski & J. M. Pages (1990b). Involvement of OmpF during reception and translocation steps of colicin N entry. Molecular Microbiology 4, 17371743.

E. Bouveret , A. Rigal , C. Lazdunski & H. Benedetti (1998). Distinct regions of the colicin A translocation domain are involved in the interaction with TolA and TolB proteins upon import into Escherichia coli. Molecular Microbiology 27, 143157.

N. Cadieux , P. G. Phan , D. S. Cafiso & R. J. Kadner (2003). Differential substrate-induced signaling through the TonB-dependent transporter BtuB. Proceedings of the National Academy of Sciences, U. S. A. 100, 1068810693.

E. Cascales , S. K. Buchanan , D. Duche , C. Kleanthous , R. Lloubes , K. Postle , M. Riley , S. Slatin & D. Cavard (2007). Colicin biology. Microbiology and Molecular Biology Review 71, 158229.

E. Cascales , M. Gavioli , J. N. Sturgis & R. Lloubes (2000). Proton motive force drives the interaction of the inner membrane TolA and outer membrane pal proteins in Escherichia coli. Molecular Microbiology 38, 904915.

E. Cascales , R. Lloubes & J. N. Sturgis (2001). The TolQ-TolR proteins energize TolA and share homologies with the flagellar motor proteins MotA–MotB. Molecular Microbiology 42, 795807.

M. Chauleau , L. Mora , J. Serba & M. De Zamaroczy (2011). FtsH-dependent processing of RNase colicins D and E3 means that only the cytotoxic domains are imported into the cytoplasm. Journal of Biological Chemistry 286, 2939729407.

E. S. Collins , S. B. Whittaker , K. Tozawa , C. Macdonald , R. Boetzel , C. N. Penfold , A. Reilly , N. J. Clayden , M. J. Osborne , A. M. Hemmings , C. Kleanthous , R. James & G. R. Moore (2002). Structural dynamics of the membrane translocation domain of colicin E9 and its interaction with TolB. Journal of Molecular Biology 318, 787904.

M. De Zamaroczy & R. H. Buckingham (2002). Importation of nuclease colicins into E coli cells: endoproteolytic cleavage and its prevention by the immunity protein. Biochimie 84, 423432.

C. A. Dennis , H. Videler , R. A. Pauptit , R. Wallis , R. James , G. R. Moore & C. Kleanthous (1998). A structural comparison of the colicin immunity proteins Im7 and Im9 gives new insights into the molecular determinants of immunity-protein specificity. Biochemistry Journal 333, 183191.

R. Derouiche , G. Zeder-Lutz , H. Benedetti , M. Gavioli , A. Rigal , C. Lazdunskil & R. Lloubes (1997). Binding of colicins A and E1 to purified TolA domains. Microbiology 143, 31853192.

L. G. Doudeva , H. Huang , K. C. Hsia , Z. Shi , C. L. Li , Y. Shen , Y. S. Cheng & H. S. Yuan (2006). Crystal structural analysis and metal-dependent stability and activity studies of the ColE7 endonuclease domain in complex with DNA/Zn2+ or inhibitor/Ni2+. Protein Science 15, 269280.

M. El Ghachi , A. Bouhss , H. Barreteau , T. Touze , G. Auger , D. Blanot & D. Mengin-Lecreulx (2006). Colicin M exerts its bacteriolytic effect via enzymatic degradation of undecaprenyl phosphate-linked peptidoglycan precursors. Journal of Biological Chemistry 281, 2276122772.

N. Ferguson , A. P. Capaldi , R. James , C. Kleanthous & S. E. Radford (1999). Rapid folding with and without populated intermediates in the homologous four-helix proteins Im7 and Im9. Journal of Molecular Biology 286, 15971608.

N. Ferguson , W. Li , A. P. Capaldi , C. Kleanthous & S. E. Radford (2001). Using chimeric immunity proteins to explore the energy landscape for alpha-helical protein folding. Journal of Molecular Biology 307, 393405.

L. Foit , G. J. Morgan , M. J. Kern , L. R. Steimer , A. A. Von Hacht , J. Titchmarsh , S. L. Warriner , S. E. Radford & J. C. Bardwell (2009). Optimizing protein stability in vivo. Molecular Cell 36, 861871.

C. T. Friel , G. S. Beddard & S. E. Radford (2004). Switching two-state to three-state kinetics in the helical protein Im9 via the optimisation of stabilising non-native interactions by design. Journal of Molecular Biology 342, 261273.

E. A. Galburt & B. L. Stoddard (2002). Catalytic mechanisms of restriction and homing endonucleases. Biochemistry 41, 1385113860.

F. Gerard , M. A. Brooks , H. Barreteau , T. Touze , M. Graille , A. Bouhss , D. Blanot , H. Van Tilbeurgh & D. Mengin-Lecreulx (2010). X-ray structure and site-directed mutagenesis analysis of the Escherichia coli colicin M immunity protein. Journal of Bacteriology 193, 205214.

S. A. Gorski , A. P. Capaldi , C. Kleanthous & S. E. Radford (2001). Acidic conditions stabilise intermediates populated during the folding of Im7 and Im9. Journal of Molecular Biology 312, 849863.

S. A. Gorski , C. S. Le Duff , A. P. Capaldi , A. P. Kalverda , G. S. Beddard , G. R. Moore & S. E. Radford (2004). Equilibrium hydrogen exchange reveals extensive hydrogen bonded secondary structure in the on-pathway intermediate of Im7. Journal of Molecular Biology 337, 183193.

M. Graille , L. Mora , R. H. Buckingham , H. Van Tilbeurgh & M. De Zamaroczy (2004). Structural inhibition of the colicin D tRNase by the tRNA-mimicking immunity protein. EMBO Journal 23, 14741482.

J. Gsponer , H. Hopearuoho , S. B. Whittaker , G. R. Spence , G. R. Moore , E. Paci , S. E. Radford & M. Vendruscolo (2006). Determination of an ensemble of structures representing the intermediate state of the bacterial immunity protein Im7. Proceedings of the National Academy of Sciences, U. S. A. 103, 99104.

G. Hale (2006). Therapeutic antibodies – delivering the promise? Advanced Drug Delivery Review 58(5–6), 633639.

S. L. Hands , L. E. Holland , M. Vankemmelbeke , L. Fraser , C. J. Macdonald , G. R. Moore , R. James & C. N. Penfold (2005). Interactions of TolB with the translocation domain of colicin E9 require an extended TolB box. Journal of Bacteriology 187, 67336741.

O. Hecht , H. Ridley , R. Boetzel , A. Lewin , N. Cull , D. A. Chalton , J. H. Lakey & G. R. Moore (2008). Self-recognition by an intrinsically disordered protein. FEBS Letters 582, 26732677.

O. Hecht , H. Ridley , J. H. Lakey & G. R. Moore (2009b). A common interaction for the entry of colicin N and filamentous phage into Escherichia coli. Journal of Molecular Biology 388, 880893.

O. Hecht , Y. Zhang , C. Li , C. N. Penfold , R. James & G. R. Moore (2010). Characterisation of the interaction of colicin A with its co-receptor TolA. FEBS Letters 584, 22492252.

N. G. Housden & C. Kleanthous (2011). Thermodynamic dissection of colicin interactions. Methods in Enzymology 488, 123145.

N. G. Housden , S. R. Loftus , G. R. Moore , R. James & C. Kleanthous (2005). Cell entry mechanism of enzymatic bacterial colicins: porin recruitment and the thermodynamics of receptor binding. Proceedings of the National Academy of Sciences, U. S. A. 102, 1384913854.

N. G. Housden , J. A. Wojdyla , J. Korczynska , I. Grishkovskaya , N. Kirkpatrick , A. M. Brzozowski & C. Kleanthous (2010). Directed epitope delivery across the Escherichia coli outer membrane through the porin OmpF. Proceedings of the National Academy of Sciences, U.S.A 107, 2141221417.

K. C. Hsia , K. F. Chak , P. H. Liang , Y. S. Cheng , W. Y. Ku & H. S. Yuan (2004). DNA binding and degradation by the HNH protein ColE7. Structure 12, 205214.

K. S. Jakes & A. Finkelstein (2010). The colicin Ia receptor, Cir, is also the translocator for colicin Ia. Molecular Microbiology 75, 567578.

L. A. Joachimiak , T. Kortemme , B. L. Stoddard & D. Baker (2006). Computational design of a new hydrogen bond network and at least a 300-fold specificity switch at a protein–protein interface. Journal of Molecular Biology 361, 195208.

A. E. Johnson & M. A. Van Waes (1999). The translocon: a dynamic gateway at the ER membrane. Annual Review of Cell Development Biology 15, 799842.

A. H. Keeble , L. A. Joachimiak , M. J. Mate , N. Meenan , N. Kirkpatrick , D. Baker & C. Kleanthous (2008). Experimental and computational analyses of the energetic basis for dual recognition of immunity proteins by colicin endonucleases. Journal of Molecular Biology 379, 745759.

A. H. Keeble , N. Kirkpatrick , S. Shimizu & C. Kleanthous (2006). Calorimetric dissection of colicin DNase–immunity protein complex specificity. Biochemistry 45, 32433254.

A. H. Keeble , M. J. Maté & C. Kleanthous (2005). HNH endonucleases. In Homing Endonucleases and Inteins, vol. 16 (eds. M. Belfort V. Derbyshire B. Stoddard & D. Wood ), pp. 4965. Berlin: Springer-Verlag.

R. J. Keenan , D. M. Freymann , R. M. Stroud & P. Walter (2001). The signal recognition particle. Annual Review of Biochemistry 70, 755775.

P. D. Kiely & D. M. Johnson (2002). Infliximab and leflunomide combination therapy in rheumatoid arthritis: an open-label study. Rheumatology (Oxford) 41, 631637.

B. C. Kirkup & M. A. Riley (2004). Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo. Nature 428, 412.

C. Kleanthous & D. Walker (2001). Immunity proteins: enzyme inhibitors that avoid the active site. Trends in Biochemical Sciences 26, 624631.

S. E. Knowling , A. M. Figueiredo , S. B. Whittaker , G. R. Moore & S. E. Radford (2009). Amino acid insertion reveals a necessary three-helical intermediate in the folding pathway of the colicin E7 immunity protein Im7. Journal of Molecular Biology 392, 10741086.

U. C. Kuhlmann , A. J. Pommer , G. R. Moore , R. James & C. Kleanthous (2000). Specificity in protein–protein interactions: the structural basis for dual recognition in endonuclease colicin-immunity protein complexes. Journal of Molecular Biology 301, 1163.

G. Kurisu , S. D. Zakharov , M. V. Zhalnina , S. Bano , V. Y. Eroukova , T. I. Rokitskaya , Y. N. Antonenko , M. C. Wiener & W. A. Cramer (2003). The structure of BtuB with bound colicin E3 R-domain implies a translocon. Nature Structural Biology 10, 948954.

L. E. Lancaster , A. Savelsbergh , C. Kleanthous , W. Wintermeyer & M. V. Rodnina (2008). Colicin E3 cleavage of 16S rRNA impairs decoding and accelerates tRNA translocation on Escherichia coli ribosomes. Molecular Microbiology 69, 390401.

J. C. Lazzaroni , J. F. Dubuisson & A. Vianney (2002). The Tol proteins of Escherichia coli and their involvement in the translocation of group A colicins. Biochimie 84, 391397.

K. B. Levin , O. Dym , S. Albeck , S. Magdassi , A. H. Keeble , C. Kleanthous & D. S. Tawfik (2009). Following evolutionary paths to protein–protein interactions with high affinity and selectivity. Nature Structural and Molecular Biology 16, 10491055.

W. Li , S. J. Hamill , A. M. Hemmings , G. R. Moore , R. James & C. Kleanthous (1998). Dual recognition and the role of specificity-determining residues in colicin E9 DNase-immunity protein interactions. Biochemistry 37, 1177111779.

S. R. Loftus , D. Walker , M. J. Mate , D. A. Bonsor , R. James , G. R. Moore & C. Kleanthous (2006). Competitive recruitment of the periplasmic translocation portal TolB by a natively disordered domain of colicin E9. Proceedings of the National Academy of Sciences, U. S. A. 103, 1235312358.

J. Lubkowski , F. Hennecke , A. Pluckthun & A. Wlodawer (1999). Filamentous phage infection: crystal structure of g3p in complex with its coreceptor, the C-terminal domain of TolA. Structure 7, 711722.

C. Luna-Chavez , Y. L. Lin & R. H. Huang (2006). Molecular basis of inhibition of the ribonuclease activity in colicin E5 by its cognate immunity protein. Journal of Molecular Biology 358, 571579.

M. J. Mate & C. Kleanthous (2004). Structure-based analysis of the metal-dependent mechanism of H-N-H endonucleases. Journal of Biological Chemistry 279, 3476334769.

N. A. Meenan , A. Sharma , S. J. Fleishman , C. J. Macdonald , B. Morel , R. Boetzel , G. R. Moore , D. Baker & C. Kleanthous (2010). The structural and energetic basis for high selectivity in a high-affinity protein–protein interaction. Proceedings of the National Academy of Sciences, U. S. A. 107, 1008010085.

G. Meng , N. K. Surana , J. W. St Geme III & G. Waksman (2006). Structure of the outer membrane translocator domain of the Haemophilus influenzae Hia trimeric autotransporter. EMBO Journal 25, 22972304.

K. Mosbahi , C. Lemaitre , A. H. Keeble , H. Mobasheri , B. Morel , R. James , G. R. Moore , E. J. Lea & C. Kleanthous (2002). The cytotoxic domain of colicin E9 is a channel-forming endonuclease. Nature Structural Biology 9, 476484.

K. Mosbahi , D. Walker , E. Lea , G. R. Moore , R. James & C. Kleanthous (2004). Destabilization of the colicin E9 Endonuclease domain by interaction with negatively charged phospholipids: implications for colicin translocation into bacteria. Journal of Biological Chemistry 279, 2214522151.

C. L. Ng , K. Lang , N. A. Meenan , A. Sharma , A. C. Kelley , C. Kleanthous & V. Ramakrishnan (2010b). Structural basis for 16S ribosomal RNA cleavage by the cytotoxic domain of colicin E3. Nature Structural and Molecular Biology 17, 12411246.

T. Ogawa , S. Inoue , S. Yajima , M. Hidaka & H. Masaki (2006). Sequence-specific recognition of colicin E5, a tRNA-targeting ribonuclease. Nucleic Acids Research 34, 60656073.

R. K. Oldham & R. O. Dillman (2008). Monoclonal antibodies in cancer therapy: 25 years of progress. Journal of Clinical Oncology 26, 17741777.

E. Paci , C. T. Friel , K. Lindorff-Larsen , S. E. Radford , M. Karplus & M. Vendruscolo (2004). Comparison of the transition state ensembles for folding of Im7 and Im9 determined using all-atom molecular dynamics simulations with phi value restraints. Proteins 54, 513525.

C. N. Penfold , B. Healy , N. G. Housden , R. Boetzel , M. Vankemmelbeke , G. R. Moore , C. Kleanthous & R. James (2004a). Flexibility in the receptor-binding domain of the enzymatic colicin E9 is required for toxicity against Escherichia coli cells. Journal of Bacteriology 186, 45204527.

H. Pilsl & V. Braun (1998). The Ton system can functionally replace the TolB protein in the uptake of mutated colicin U. FEMS Microbiology Letters 164, 363367.

M. Pohlschroder , W. A. Prinz , E. Hartmann & J. Beckwith (1997). Protein translocation in the three domains of life: variations on a theme. Cell 91, 563566.

N. Pokala & T. M. Handel (2001). Review: protein design – where we were, where we are, where we're going. Journal of Structural Biology 134, 269281.

A. J. Pommer , S. Cal , A. H. Keeble , D. Walker , S. J. Evans , U. C. Kuhlmann , A. Cooper , B. A. Connolly , A. M. Hemmings , G. R. Moore , R. James & C. Kleanthous (2001). Mechanism and cleavage specificity of the H-N-H endonuclease colicin E9. Journal of Molecular Biology 314, 735.

K. Postle & R. J. Kadner (2003). Touch and go: tying TonB to transport. Molecular Microbiology 49, 869882.

H. Ridley , C. L. Johnson & J. H. Lakey (2010). Interfacial interactions of pore-forming colicins. Advances in Experimental Medicine and Biology 677, 8190.

M. A. Riley (1998). Molecular mechanisms of bacteriocin evolution. Annual Review of Genetics 32, 255278.

C. Roodveldt , A. Aharoni & D. S. Tawfik (2005). Directed evolution of proteins for heterologous expression and stability. Current Opinion in Structural Biology 15, 5056.

O. Sharma , K. A. Datsenko , S. C. Ess , M. V. Zhalnina , B. L. Wanner & W. A. Cramer (2009). Genome-wide screens: novel mechanisms in colicin import and cytotoxicity. Molecular Microbiology 73, 571585.

O. Sharma , E. Yamashita , M. V. Zhalnina , S. D. Zakharov , K. A. Datsenko , B. L. Wanner & W. A. Cramer (2007). Structure of the complex of the colicin E2 R-domain and its BtuB receptor. The outer membrane colicin translocon. Journal of Biological Chemistry 282, 2316323170.

D. A. Shub , H. Goodrich-Blair & S. R. Eddy (1994). Amino acid sequence motif of group I intron endonucleases is conserved in open reading frames of group II introns. Trends in Biochemical Sciences 19, 402404.

C. R. Smallwood , A. G. Marco , Q. Xiao , V. Trinh , S. M. Newton & P. E. Klebba (2009). Fluoresceination of FepA during colicin B killing: effects of temperature, toxin and TonB. Molecular Microbiology 72, 11711180.

S. Soelaiman , K. Jakes , N. Wu , C. Li & M. Shoham (2001). Crystal structure of colicin E3: implications for cell entry and ribosome inactivation. Molecular Cell 8, 10531062.

L. Sutto , J. Latzer , J. A. Hegler , D. U. Ferreiro & P. G. Wolynes (2007). Consequences of localized frustration for the folding mechanism of the IM7 protein. Proceedings of the National Academy of Sciences, U. S. A. 104, 1982519830.

C. Tanford (1970). Protein denaturation. C. Theoretical models for the mechanism of denaturation. Advanced Protein Chemistry 24, 195.

N. Tokuriki & D. S. Tawfik (2009). Protein dynamism and evolvability. Science 324, 203207.

K. Tomita , T. Ogawa , T. Uozumi , K. Watanabe & H. Masaki (2000). A cytotoxic ribonuclease which specifically cleaves four isoaccepting arginine tRNAs at their anticodon loops. Proceedings of the National Academy of Sciences, U. S. A. 97, 82788283.

E. T. Van Den Bremer , A. H. Keeble , W. Jiskoot , R. E. Spelbrink , C. S. Maier , A. Van Hoek , A. J. Visser , R. James , G. R. Moore , C. Kleanthous & A. J. Heck (2004). Distinct conformational stability and functional activity of four highly homologous endonuclease colicins. Protein Science 13, 13911401.

M. Vankemmelbeke , B. Healy , G. R. Moore , C. Kleanthous , C. N. Penfold & R. James (2005). Rapid detection of colicin E9-induced DNA damage using Escherichia coli cells carrying SOS promoter–lux fusions. Journal of Bacteriology 187, 49004907.

M. Vankemmelbeke , Y. Zhang , G. R. Moore , C. Kleanthous , C. N. Penfold & R. James (2009). Energy-dependent immunity protein release during tol-dependent nuclease colicin translocation. Journal of Biological Chemistry 284, 1893218941.

I. R. Vetter , M. W. Parker , A. D. Tucker , J. H. Lakey , F. Pattus & D. Tsernoglou (1998). Crystal structure of a colicin N fragment suggests a model for toxicity. Structure 6, 863874.

D. Walker , L. Lancaster , R. James & C. Kleanthous (2004a). Identification of the catalytic motif of the microbial ribosome inactivating cytotoxin colicin E3. Protein Science 13, 16031611.

D. Walker , G. R. Moore , R. James & C. Kleanthous (2003). Thermodynamic consequences of bipartite immunity protein binding to the ribosomal ribonuclease colicin E3. Biochemistry 42, 4161.

D. Walker , K. Mosbahi , M. Vankemmelbeke , R. James & C. Kleanthous (2007). The role of electrostatics in colicin nuclease domain translocation into bacterial cells. Journal of Biological Chemistry 282, 3138931397.

D. Walker , M. Rolfe , A. Thompson , G. R. Moore , R. James , J. C. Hinton & C. Kleanthous (2004b). Transcriptional profiling of colicin-induced cell death of Escherichia coli MG1655 identifies potential mechanisms by which bacteriocins promote bacterial diversity. Journal of Bacteriology 186, 866.

R. Wallis , K. Y. Leung , M. J. Osborne , R. James , G. R. Moore & C. Kleanthous (1998). Specificity in protein–protein recognition: conserved Im9 residues are the major determinants of stability in the colicin E9 DNase–Im9 complex. Biochemistry 37, 476.

R. Wallis , G. R. Moore , R. James & C. Kleanthous (1995). Protein–protein interactions in colicin E9 DNase-immunity protein complexes. 1. Diffusion-controlled association and femtomolar binding for the cognate complex. Biochemistry 34, 1374313750.

R. Wallis , A. Reilly , K. Barnes , C. Abell , D. G. Campbell , G. R. Moore , R. James & C. Kleanthous (1994). Tandem overproduction and characterisation of the nuclease domain of colicin E9 and its cognate inhibitor protein Im9. European Journal of Biochemistry 220, 447.

R. E. Webster (1991). The tol gene products and the import of macromolecules into Escherichia coli. Molecular Microbiology 5, 10051011.

S. B. Whittaker , G. R. Spence , J. Gunter Grossmann , S. E. Radford & G. R. Moore (2007). NMR analysis of the conformational properties of the trapped on-pathway folding intermediate of the bacterial immunity protein Im7. Journal of Molecular Biology 366, 10011015.

E. Yamashita , M. V. Zhalnina , S. D. Zakharov , O. Sharma & W. A. Cramer (2008). Crystal structures of the OmpF porin: function in a colicin translocon. EMBO Journal 27, 21712180.

S. D. Zakharov , V. Y. Eroukova , T. I. Rokitskaya , M. V. Zhalnina , O. Sharma , P. J. Loll , H. I. Zgurskaya , Y. N. Antonenko & W. A. Cramer (2004a). Colicin occlusion of OmpF and TolC channels: outer membrane translocons for colicin import. Biophysical Journal 87, 39013911.

S. D. Zakharov , E. A. Kotova , Y. N. Antonenko & W. A. Cramer (2004b). On the role of lipid in colicin pore formation. Biochimica Biophysica Acta 1666, 239249.

S. D. Zakharov , O. Sharma , M. V. Zhalnina & W. A. Cramer (2008). Primary events in the colicin translocon: FRET analysis of colicin unfolding initiated by binding to BtuB and OmpF. Biochemistry 47, 1280212809.

S. D. Zakharov , M. V. Zhalnina , O. Sharma & W. A. Cramer (2006). The colicin E3 outer membrane translocon: immunity protein release allows interaction of the cytotoxic domain with OmpF porin. Biochemistry 45, 1019910207.

K. Zeth , C. Romer , S. I. Patzer & V. Braun (2008). Crystal structure of colicin M, a novel phosphatase specifically imported by Escherichia coli. Journal of Biological Chemistry 283, 2532425331.

X. Y. Zhang , E. L. Goemaere , N. Seddiki , H. Celia , M. Gavioli , E. Cascales & R. Lloubes (2011). Mapping the interactions between Escherichia coli TolQ transmembrane segments. Journal of Biological Chemistry 286, 1175611764.

Y. Zhang , M. Vankemmelbeke , P. Baardelang , M. Paoli , C. N. Penfold & R. James (2009b). The crystal structure of the TolB box of Colicin A in complex with TolB reveals important differences in the recruitment of the common TolB translocation portal used by group A colicins. Molecular Microbiology 75, 623636.

Y. Zhang , M. N. Vankemmelbeke , L. E. Holland , D. C. Walker , R. James & C. N. Penfold (2008). Investigating early events in receptor binding and translocation of colicin E9 using synchronized cell killing and proteolytic cleavage. Journal of Bacteriology 190, 43424350.

Y. L. Zhang & W. A. Cramer (1992). Constraints imposed by protease accessibility on the trans-membrane and surface topography of the colicin E1 ion channel. Protein Science 1, 16661676.

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