Skip to main content

Pore-Forming Colicins: Unusual Ion Channels – Unusually Regulated

  • Chapter
Electrophysiology of Unconventional Channels and Pores

Part of the book series: Springer Series in Biophysics ((BIOPHYSICS,volume 18))

  • 1007 Accesses

Abstract

Colicins are toxins released by plasmid carrying Escherichia coli bacteria in order to kill bacteria not carrying the same plasmid. This selection is achieved since the plasmid bearing cells have an immunity protein that protects them from their own specific colicin. Colicins kill by peptidoglycan synthesis inhibition, nuclease digestion or pore formation. This review describes how the pore-forming colicins function, with reference to other types as needed. The function involves binding to target cells, translocation across the outer membrane and periplasm, insertion into the inner membrane and voltage gated pore formation. Due to this unusual pathway, the pores have an unusual and minimalist mode of pore formation that is still not fully defined. The immunity protein is an integral membrane protein of the inner membrane, which prevents formation of the open pore and thus protects the cell. Models for the interaction with the colicin pore are discussed which also give insights into protein-protein interactions in the lipid bilayer.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Anderluh G, Lakey JH (eds) (2010) Proteins; membrane binding and pore formation, 1st edn. Springer, Heidelberg

    Google Scholar 

  • Anderluh G, Hong Q, Boetzel R, MacDonald C, Moore GR, Virden R, Lakey JH (2003) Concerted folding and binding of a flexible colicin domain to its periplasmic receptor TolA. J Biol Chem 278:21860–21868

    CAS  PubMed  Google Scholar 

  • Arnold T, Zeth K, Linke D (2009) Structure and function of colicin S4, a colicin with a duplicated receptor-binding domain. J Biol Chem 284(10):6403–6413

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baboolal TG, Conroy MJ, Gill K, Ridley H, Visudtiphole V, Bullough PA, Lakey JH (2008) Colicin N binds to the periphery of its receptor and translocator, outer membrane protein F. Structure 16(3):371–379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barhanin J, Romey G, Lazdunski M (1999) IsK: a novel type of potassium channel regulatory subunit. Potass Ion Chan 46:67–84

    CAS  Google Scholar 

  • Baty D, Lakey J, Pattus F, Lazdunski C (1990) A 136-amino-acid-residue COOH-terminal fragment of colicin-a is endowed with ionophoric activity. Eur J Biochem 189(2):409–413

    CAS  PubMed  Google Scholar 

  • Benedetti H, Frenette M, Baty D, Knibiehler M, Pattus F, Lazdunski C (1991) Individual domains of colicins confer specificity in colicin uptake, in pore-properties and in immunity requirement. J Mol Biol 217(3):429–439

    CAS  PubMed  Google Scholar 

  • Benedetti H, Lloubes R, Lazdunski C, Letellier L (1992) Colicin A unfolds during its translocation in Escherichia coli cells and spans the whole cell envelope when its pore has formed. EMBO J 11(2):441–447

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bishop LJ, Bjes ES, Davidson VL, Cramer WA (1985) Localization of the immunity protein-reactive domain in unmodified and chemically modified COOH-terminal peptides of colicin E1. J Bacteriol 164(1):237–244

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bohme S, Padmavathi PVL, Holterhues J, Ouchni F, Klare JP, Steinhoff HJ (2009) Topology of the amphipathic helices of the colicin A pore-forming domain in E. coli lipid membranes studied by pulse EPR. Phys Chem Chem Phys 11(31):6770–6777

    PubMed  Google Scholar 

  • Buchanan SK, Lukacik P, Grizot S, Ghirlando R, Ali MM, Barnard TJ, Jakes KS, Kienker PK, Esser L (2007) Structure of colicin I receptor bound to the R-domain of colicin Ia: implications for protein import. EMBO J 26:2594–2604

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, Postle K, Riley M, Slatin S, Cavard D (2007) Colicin biology. Microbiol Mol Biol Rev 71(1):158–229

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cavard D (1991) Synthesis and functioning of the colicin E1 lysis protein: comparison with the colicin A lysis protein. J Bacteriol 173(1):191–196

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clifton LA, Johnson CL, Solovyova AS, Callow P, Weiss KL, Ridley H, Le Brun AP, Kinane CJ, Webster JRP, Holt SA, Lakey JH (2012) Low resolution structure and dynamics of a colicin-receptor complex determined by neutron scattering. J Biol Chem 287(1):337–346

    CAS  PubMed  Google Scholar 

  • Clifton LA, Skoda MWA, Daulton EL, Hughes AV, Le Brun AP, Lakey JH, Holt SA (2013) Asymmetric phospholipid: lipopolysaccharide bilayers; a Gram-negative bacterial outer membrane mimic. J R Soc Interface 10(89):20130810

    PubMed  PubMed Central  Google Scholar 

  • Collarini M, Amblard G, Lazdunski C, Pattus F (1987) Gating processes of channels induced by colicin-a, its C-terminal fragment and colicin-E1 in planar lipid bilayers. Eur Biophys J 14(3):147–153

    CAS  PubMed  Google Scholar 

  • Dover LG, Evans LJ, Fridd SL, Bainbridge G, Raggett EM, Lakey JH (2000) Colicin pore-forming domains bind to Escherichia coli trimeric porins. Biochemistry 39(29):8632–8637

    CAS  PubMed  Google Scholar 

  • Drew D, Sjostrand D, Nilsson J, Urbig T, Chin CN, de Gier JW, von Heijne G (2002) Rapid topology mapping of Escherichia coli inner-membrane proteins by prediction and PhoA/GFP fusion analysis. Proc Natl Acad Sci U S A 99(5):2690–2695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duche D (2002) The pore-forming domain of colicin A fused to a signal peptide: a tool for studying pore-formation and inhibition. Biochimie 84(5–6):455–464

    CAS  PubMed  Google Scholar 

  • Duche D, Baty D, Chartier M, Letellier L (1994a) Unfolding of colicin A during its translocation through the Escherichia coli envelope as demonstrated by disulfide bond engineering. J Biol Chem 269(40):24820–24825

    CAS  PubMed  Google Scholar 

  • Duche D, Parker MW, Gonzalezmanas JM, Pattus F, Baty D (1994b) Uncoupled steps of the colicin-a pore formation demonstrated by disulfide bond engineering. J Biol Chem 269(9):6332–6339

    CAS  PubMed  Google Scholar 

  • Espesset D, Corda Y, Cunningham K, Benedetti H, Lloubes R, Lazdunski C, Geli V (1994) The colicin A pore-forming domain fused to mitochondrial intermembrane space sorting signals can be functionally inserted into the Escherichia coli plasma membrane by a mechanism that bypasses the Tol proteins. Mol Microbiol 13(6):1121–1131

    CAS  PubMed  Google Scholar 

  • Espesset D, Duche D, Baty D, Geli V (1996) The channel domain of colicin A is inhibited by its immunity protein through direct interaction in the Escherichia coli inner membrane. EMBO J 15(10):2356–2364

    CAS  PubMed  PubMed Central  Google Scholar 

  • Evans LJA, Goble ML, Hales KA, Lakey JH (1996) Different sensitivities to acid denaturation within a family of proteins; implications for acid unfolding and membrane translocation. Biochemistry 35(40):13180–13185

    CAS  PubMed  Google Scholar 

  • Farrance OE, Hann E, Kaminska R, Housden NG, Derrington SR, Kleanthous C, Radford SE, Brockwell DJ (2013) A force-activated trip switch triggers rapid dissociation of a colicin from its immunity protein. PLoS Biol 11(2):e1001489

    CAS  PubMed  PubMed Central  Google Scholar 

  • Feilmeier BJ, Iseminger G, Schroeder D, Webber H, Phillips GJ (2000) Green fluorescent protein functions as a reporter for protein localization in Escherichia coli. J Bacteriol 182(14):4068–4076

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fridd SL, Lakey JH (2002) Surface aspartate residues are essential for the stability of colicin A P-domain: a mechanism for the formation of an acidic molten-globule. Biochemistry 41(5):1579–1586

    CAS  PubMed  Google Scholar 

  • Fridd SL, Gokce I, Lakey JH (2002) High level expression of His-tagged colicin pore-forming domains and reflections on the sites for pore formation in the inner membrane. Biochimie 84(5–6):477–483

    CAS  PubMed  Google Scholar 

  • Geli V, Lazdunski C (1992) An alpha-helical hydrophobic hairpin as a specific determinant in protein-protein interaction occurring in Escherichia coli colicin A and B immunity systems. J Bacteriol 174(20):6432–6437

    CAS  PubMed  PubMed Central  Google Scholar 

  • Geli V, Baty D, Lazdunski C (1988) Use of a foreign epitope as a tag for the localization of minor proteins within a cell – the case of the immunity protein to colicin-A. Proc Natl Acad Sci U S A 85(3):689–693

    CAS  PubMed  PubMed Central  Google Scholar 

  • Geli V, Baty D, Pattus F, Lazdunski C (1989a) Topology and function of the integral membrane protein conferring immunity to colicin A. Mol Microbiol 3(5):679–687

    CAS  PubMed  Google Scholar 

  • Geli V, Knibiehler M, Bernadac A, Lazdunski C (1989b) Purification and reconstitution into liposomes of an integral membrane-protein conferring immunity to colicin-A. FEMS Microbiol Lett 60(2):239–244

    CAS  Google Scholar 

  • Goldman K, Suit JL, Kayalar C (1985) Identification of the plasmid-encoded immunity protein for colicin E1 in the inner membrane of Escherichia coli. FEBS Lett 190(2):319–323

    CAS  PubMed  Google Scholar 

  • Greig SL, Radjainia M, Mitra AK (2009) Oligomeric structure of colicin Ia channel in lipid bilayer membranes. J Biol Chem 284(24):16126–16134

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guder A, Wiedemann I, Sahl HG (2000) Posttranslationally modified bacteriocins – the lantibiotics. Biopolymers 55(1):62–73

    CAS  PubMed  Google Scholar 

  • Hecht O, Ridley H, Boetzel R, Lewin A, Cull N, Chalton DA, Lakey JH, Moore GR (2008) Self-recognition by an intrinsically disordered protein. FEBS Lett 582(17):2673–2677

    CAS  PubMed  Google Scholar 

  • Hecht O, Macdonald C, Moore GR (2012) Intrinsically disordered proteins: lessons from colicins. Biochem Soc Trans 40:1534–1538

    CAS  PubMed  Google Scholar 

  • Hilsenbeck JL, Park H, Chen G, Youn B, Postle K, Kang C (2004) Crystal structure of the cytotoxic bacterial protein colicin B at 2.5Å resolution. Mol Microbiol 51(3):711–720

    CAS  PubMed  Google Scholar 

  • Honigmann A, Pulagam LP, Sippach M, Bartsch P, Steinhoff HJ, Wagner R (2012) A high resolution electro-optical approach for investigating transition of soluble proteins to integral membrane proteins probed by colicin A. Biochem Biophys Res Commun 427(2):385–391

    CAS  PubMed  Google Scholar 

  • Housden NG, Hopper JTS, Lukoyanova N, Rodriguez-Larrea D, Wojdyla JA, Klein A, Kaminska R, Bayley H, Saibil HR, Robinson CV, Kleanthous C (2013) Intrinsically disordered protein threads through the bacterial outer-membrane porin OmpF. Science 340(6140):1570–1574

    CAS  PubMed  Google Scholar 

  • Huang Y, Le Brun A, Soliakov A, MacDonald C, Moore G, Lakey JH (2012) Helix N-cap Asp are the pH trigger for colicin a membrane insertion. Biophys J 102(3):656A

    Google Scholar 

  • Jakes KS (2014) Daring to be different: colicin N finds another way. Mol Microbiol 92(3):435–439

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jakes KS, Cramer WA (2012) Border crossings: colicins and transporters. Annu Rev Genet 46(46):209–231

    CAS  PubMed  Google Scholar 

  • Jakes KS, Finkelstein A (2010) The colicin Ia receptor, Cir, is also the translocator for colicin Ia. Mol Microbiol 75(3):567–578

    CAS  PubMed  Google Scholar 

  • Jakes KS, Abrams CK, Finkelstein A, Slatin SL (1990) Alteration of the pH-dependent ion selectivity of the colicin E1 channel by site-directed mutagenesis. J Biol Chem 265(12):6984–6991

    CAS  PubMed  Google Scholar 

  • Johnson CL, Ridley H, Marchetti R, Silipo A, Griffin DC, Crawford L, Bonev B, Molinaro A, Lakey JH (2014) The antibacterial toxin colicin N binds to the inner core of lipopolysaccharide and close to its translocator protein. Mol Microbiol 92(3):440–452

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kienker PK, Qiu XQ, Slatin SL, Finkelstein A, Jakes KS (1997) Transmembrane insertion of the colicin Ia hydrophobic hairpin. J Membr Biol 157(1):27–37

    CAS  PubMed  Google Scholar 

  • Kim YC, Tarr AW, Penfold CN (2014) Colicin import into E. coli cells: a model system for insights into the import mechanisms of bacteriocins. Biochim Biophys Acta 1843(8):1717–1731

    CAS  PubMed  Google Scholar 

  • Kleanthous C, Hemmings AM, Moore GR, James R (1998) Immunity proteins and their specificity for endonuclease colicins: telling right from wrong in protein-protein recognition. Mol Microbiol 28(2):227–233

    CAS  PubMed  Google Scholar 

  • Kurisu G, Zakharov SD, Zhalnina MV, Bano S, Eroukova VY, Rokitskaya TI, Antonenko YN, Wiener MC, Cramer WA (2003) The structure of BtuB with bound colicin E3 R-domain implies a translocon. Nat Struct Biol 10(11):948–954

    CAS  PubMed  Google Scholar 

  • Lakey JH, Slatin SL (2001) Pore-forming colicins and their relatives. In: Van Der Goot FG (ed) Pore-forming toxins. Springer, Heidelberg, pp 131–161

    Google Scholar 

  • Lakey JH, Massotte D, Heitz F, Dasseux JL, Faucon JF, Parker MW, Pattus F (1991) Membrane insertion of the pore-forming domain of colicin A. A spectroscopic study. Eur J Biochem 196(3):599–607

    CAS  PubMed  Google Scholar 

  • Lakey JH, Duche D, Gonzalezmanas JM, Baty D, Pattus F (1993) Fluorescence energy-transfer distance measurements – the hydrophobic helical hairpin of colicin-a in the membrane-bound state. J Mol Biol 230(3):1055–1067

    CAS  PubMed  Google Scholar 

  • Lakey JH, Parker MW, Gonzalez Manas JM, Duche D, Vriend G, Baty D, Pattus F (1994a) The role of electrostatic charge in the membrane insertion of colicin A: calculation and mutation. Eur J Biochem 220:155–163

    CAS  PubMed  Google Scholar 

  • Lakey JH, van der Goot FG, Pattus F (1994b) All in the family: the toxic activity of colicins. Toxicology 87:85–108

    CAS  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23(21):2947–2948

    CAS  Google Scholar 

  • Le Brun AP, Clifton LA, Halbert CE, Lin B, Meron M, Holden PJ, Lakey JH, Holt SA (2013) Structural characterization of a model gram-negative bacterial surface using lipopolysaccharides from rough strains of Escherichia coli. Biomacromolecules 14(6):2014–2022

    PubMed  PubMed Central  Google Scholar 

  • Lemmon MA, Treutlein HR, Adams PD, Brunger AT, Engelman DM (1994) A dimerisation motif for transmembrane alpha helices. Nat Struct Biol 1(3):157–163

    CAS  PubMed  Google Scholar 

  • Levisohn R, Konisky J, Nomura M (1968) Interaction of colicins with bacterial cells. IV. Immunity breakdown studied with colicins Ia and Ib. J Bacteriol 96(3):811–821

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lindeberg M, Cramer WA (2001) Identification of specific residues in colicin E1 involved in immunity protein recognition. J Bacteriol 183(6):2132–2136

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lindeberg M, Zakharov SD, Cramer WA (2000) Unfolding pathway of the colicin E1 channel protein on a membrane surface. Biophys J 78(1):176a

    Google Scholar 

  • Lloubes R, Baty D, Lazdunski C (1986) The promoters of the genes for colicin production, release and immunity in the ColA plasmid: effects of convergent transcription and Lex A protein. Nucleic Acids Res 14(6):2621–2636

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mankovich JA, Hsu CH, Konisky J (1986) DNA and amino acid sequence analysis of structural and immunity genes of colicins Ia and Ib. J Bacteriol 168(1):228–236

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mathavan I, Beis K (2012) The role of bacterial membrane proteins in the internalization of microcin MccJ25 and MccB17. Biochem Soc Trans 40:1539–1543

    CAS  PubMed  Google Scholar 

  • Moore GR, Osborne MJ, Whittaker S, Videler H, Lian LY, Pommer A, wallis R, James R, Kleanthous C (1995) Mechanism of action of the cytotoxic domain of colicin e9 and its inhibition by its cognate immunity protein. J Cell Biochem:31. Supplement 21B

    Google Scholar 

  • Mosbahi K, Lemaitre C, Keeble AH, Mobasheri H, Morel B, James R, Moore GR, Lea E, Kleanthous C (2002) The cytotoxic domain of colicin E9 is a channel-forming endonuclease. Nat Struct Biol 9(6):476–484

    CAS  PubMed  Google Scholar 

  • Mosbahi K, Walker D, James R, Moore GR, Kleanthous C (2006) Global structural rearrangement of the cell penetrating ribonuclease colicin E3 on interaction with phospholipid membranes. Protein Sci 15(3):620–627

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muchmore SW, Sattler M, Liang H, Meadows RP, Harlan JE, Yoon HS, Nettesheim D, Chang BS, Thompson CB, Wong SL, Ng SC, Fesik SW (1996) X-ray and nmr structure of human bcl-x(l), an inhibitor of programmed cell-death. Nature 381(6580):335–341

    CAS  PubMed  Google Scholar 

  • Mueller JEN, Papic D, Ulrich T, Grin I, Schuetz M, Oberhettinger P, Tommassen J, Linke D, Dimmer KS, Autenrieth IB, Rapaport D (2011) Mitochondria can recognize and assemble fragments of a beta-barrel structure. Mol Biol Cell 22(10):1638–1647

    CAS  Google Scholar 

  • Mulec J, Podlesek Z, Mrak P, Kopitar A, Ihan A, Zgur-Bertok D (2003) A cka-gfp transcriptional fusion reveals that the colicin K activity gene is induced in only 3 percent of the population. J Bacteriol 185(2):654–659

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nardi A, Corda Y, Baty D, Duche D (2001a) Colicin A immunity protein interacts with the hydrophobic helical hairpin of the colicin A channel domain in the Escherichia coli inner membrane. J Bacteriol 183(22):6721–6725

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nardi A, Slatin SL, Baty D, Duche D (2001b) The C-terminal half of the colicin A pore-forming domain is active in vivo and in vitro. J Mol Biol 307(5):1293–1303

    CAS  PubMed  Google Scholar 

  • Olschlager T, Braun V (1987) Sequence, expression, and localization of the immunity protein for colicin-M. J Bacteriol 169(10):4765–4769

    CAS  PubMed  PubMed Central  Google Scholar 

  • Padmavathi PVL, Steinhoff HJ (2008) Conformation of the closed channel state of colicin a in proteoliposomes: an umbrella model. J Mol Biol 378(1):204–214

    CAS  PubMed  Google Scholar 

  • Parker MW, Feil SC (2005) Pore-forming protein toxins: from structure to function. Prog Biophys Mol Biol 88(1):91–142

    CAS  PubMed  Google Scholar 

  • Parker MW, Pattus F, Tucker AD, Tsernoglou D (1989) Structure of the membrane-pore-forming fragment of colicin A. Nature 337(6202):93–96

    CAS  PubMed  Google Scholar 

  • Parker MW, Postma JPM, Pattus F, Tucker AD, Tsernoglou D (1992) Refined structure of the pore-forming domain of colicin-a at 2-bullet-4 angstrom resolution. J Mol Biol 224(3):639–657

    CAS  PubMed  Google Scholar 

  • Pilsl H, Braun V (1995) Evidence that the immunity protein inactivates colicin-5 immediately prior to the formation of the transmembrane channel. J Bacteriol 177(23):6966–6972

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pilsl H, Smajs D, Braun V (1998) The tip of the hydrophobic hairpin of colicin U is dispensable for colicin U activity but is important for interaction with the immunity protein. J Bacteriol 180(16):4111–4115

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pugsley AP (1988) The immunity and lysis genes of ColN plasmid pCHAP4. Mol Gen Genet 211(2):335–341

    PubMed  Google Scholar 

  • Qiu XQ, Jakes KS, Kienker PK, Finkelstein A, Slatin SL (1996) Major transmembrane movement associated with colicin Ia channel gating. J Gen Physiol 107(3):313–328

    CAS  PubMed  Google Scholar 

  • Renner LD, Weibel DB (2011) Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes. Proc Natl Acad Sci U S A 108(15):6264–6269

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riley MA (1993) Positive selection for colicin diversity in bacteria. Mol Biol Evol 10(5):1048–1059

    CAS  PubMed  Google Scholar 

  • Riley MA, Cadavid L, Collett MS, Neely MN, Adams MD, Phillips CM, Neel JV, Friedman D (2000) The newly characterized colicin Y provides evidence of positive selection in pore-former colicin diversification. Microbiology 146:1671–1677

    CAS  PubMed  Google Scholar 

  • Schendel SL, Cramer WA (1994) On the nature of the unfolded intermediate in the in-vitro transition of the colicin E1 channel domain from the aqueous to the membrane phase. Protein Sci 3(12):2272–2279

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schramm E, Olschlager T, Troger W, Braun V (1988) Sequence, expression and localization of the immunity protein for colicin B. Mol Gen Genet 211(1):176–182

    CAS  PubMed  Google Scholar 

  • Shirabe K, Yamada M, Merrill AR, Cramer WA, Nakazawa A (1993) Overproduction and purification of the colicin-E1 immunity protein. Plasmid 29(3):236–240

    CAS  PubMed  Google Scholar 

  • Slatin SL, Qiu XQ, Jakes KS, Finkelstein A (1994) Identification of a translocated protein segment in a voltage-dependent channel. Nature 371:158–161

    CAS  PubMed  Google Scholar 

  • Slatin SL, Duche D, Kienker PK, Baty D (2004) Gating movements of colicin A and colicin Ia are different. J Membr Biol 202(2):73–83

    CAS  PubMed  Google Scholar 

  • Smajs D, Matejkova P, Weinstock GM (2006) Recognition of pore-forming colicin Y by its cognate immunity protein. FEMS Microbiol Lett 258(1):108–113

    CAS  PubMed  Google Scholar 

  • Smajs D, Dolezalova M, Macek P, Zidek L (2008) Inactivation of colicin Y by intramembrane helix-helix interaction with its immunity protein. FEBS J 275(21):5325–5331

    CAS  PubMed  Google Scholar 

  • Sobko AA, Kotova EA, Antonenko YN, Zakharov SD, Cramer WA (2004) Effect of lipids with different spontaneous curvature on the channel activity of colicin E1: evidence in favor of a toroidal pore. FEBS Lett 576(1–2):205–210

    CAS  PubMed  Google Scholar 

  • Sobko AA, Kotova EA, Antonenko YN, Zakharov SD, Cramer WA (2006) Lipid dependence of the channel properties of a colicin E1-lipid toroidal pore. J Biol Chem 281(20):14408–14416

    CAS  PubMed  Google Scholar 

  • Sobko AA, Rokitskaya TI, Kotova EA (2009) Histidine 440 controls the opening of colicin E1 channels in a lipid-dependent manner. Biochim Biophys Acta 1788(9):1962–1966

    CAS  PubMed  Google Scholar 

  • Sobko AA, Kovalchuk SI, Kotova EA, Antonenko YN (2010) Induction of lipid flip-flop by colicin E1-a hallmark of proteolipidic pore formation in liposome membranes. Biochemistry (Mosc) 75(6):728–733

    CAS  Google Scholar 

  • Soelaiman S, Jakes K, Wu N, Li CM, Shoham M (2001) Crystal structure of colicin E3: implications for cell entry and ribosome inactivation. Mol Cell 8(5):1053–1062

    CAS  PubMed  Google Scholar 

  • Song HY, Cramer WA (1991) Membrane topography of Cole1 gene-products – the immunity protein. J Bacteriol 173(9):2935–2943

    CAS  PubMed  PubMed Central  Google Scholar 

  • Song HY, Cohen FS, Cramer WA (1991) Membrane topography of Cole1 gene-products – the hydrophobic anchor of the colicin-E1 channel is a helical hairpin. J Bacteriol 173(9):2927–2934

    CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor RM, Zakharov SD, Heymann JB, Girvin ME, Cramer WA (2000) Folded state of the integral membrane colicin E1 immunity protein in solvents of mixed polarity. Biochemistry 39(40):12131–12139

    CAS  PubMed  Google Scholar 

  • Udho E, Jakes KS, Buchanan SK, James KJ, Jiang XX, Klebba PE, Finkelstein A (2009) Reconstitution of bacterial outer membrane TonB-dependent transporters in planar lipid bilayer membranes. Proc Natl Acad Sci U S A 106(51):21990–21995

    CAS  PubMed  PubMed Central  Google Scholar 

  • van der Goot FG, González-Mañas JM, Lakey JH, Pattus F (1991) A ‘molten-globule’ membrane-insertion intermediate of the pore-forming domain of colicin A. Nature 354(6352):408–410

    PubMed  Google Scholar 

  • van der Goot FG, Didat N, Pattus F, Dowhan W, Letellier L (1993) Role of acidic lipids in the translocation and channel activity of colicins A and N in Escherichia coli cells. Eur J Biochem 213:217–221

    PubMed  Google Scholar 

  • Vandergoot FG, Gonzalezmanas JM, Lakey JH, Pattus F (1991) A molten-globule membrane-insertion intermediate of the pore-forming domain of colicin-A. Nature 354(6352):408–410

    CAS  Google Scholar 

  • Vetter IR, Parker MW, Tucker AD, Lakey JH, Pattus F, Tsernoglou D (1998) Crystal structure of a colicin N fragment suggests a model for toxicity. Structure 6:863–874

    CAS  PubMed  Google Scholar 

  • Wiener M, Freymann D, Ghosh P, Stroud RM (1997) Crystal structure of colicin Ia. Nature 385(6615):461–464

    CAS  PubMed  Google Scholar 

  • Zakharov SD, Cramer WA (2002) Insertion intermediates of pore-forming colicins in membrane two-dimensional space. Biochimie 84(5–6):465–475

    CAS  PubMed  Google Scholar 

  • Zakharov SD, Lindeberg M, Cramer WA (1998a) Kinetic phases in membrane binding-insertion of the colicin E1 channel domain. Biophys J 74(2):A228

    Google Scholar 

  • Zakharov SD, Lindeberg M, Griko Y, Salamon Z, Tollin G, Cramer WA (1998b) Conformational changes of the colicin E1 channel domain at the membrane surface. Biophys J 74(2):A228

    Google Scholar 

  • Zakharov SD, Lindeberg M, Griko Y, Salamon Z, Tollin G, Prendergast FG, Cramer WA (1998c) Membrane-bound state of the colicin E1 channel domain as an extended two-dimensional helical array. Proc Natl Acad Sci U S A 95(8):4282–4287

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zakharov SD, Eroukova VY, Rokitskaya TI, Zhalnina MV, Sharma O, Loll PJ, Zgurskaya HI, Antonenko YN, Cramer WA (2004) Colicin occlusion of OmpF and TolC channels: outer membrane translocons for colicin import. Biophys J 87(6):3901–3911

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zeth K, Roemer C, Patzer SI, Braun V (2008) Crystal structure of colicin M, a novel phosphatase specifically imported by Escherichia coli. J Biol Chem 283(37):25324–25331

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YL, Cramer WA (1993) Intramembrane helix-helix interactions as the basis of inhibition of the colicin E1 ion channel by its immunity protein. J Biol Chem 268(14):10176–10184

    CAS  PubMed  Google Scholar 

  • Zhang XYZ, Lloubes R, Duche D (2010) Channel domain of colicin A modifies the dimeric organization of its immunity protein. J Biol Chem 285(49):38053–38061

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daria Stroukova .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Stroukova, D., Lakey, J.H. (2015). Pore-Forming Colicins: Unusual Ion Channels – Unusually Regulated. In: Delcour, A.H. (eds) Electrophysiology of Unconventional Channels and Pores. Springer Series in Biophysics, vol 18. Springer, Cham. https://doi.org/10.1007/978-3-319-20149-8_8

Download citation

Publish with us

Policies and ethics