1,210
Views
131
CrossRef citations to date
0
Altmetric
Original Article

Membrane insertion: The strategies of toxins (Review)

, , , &
Pages 45-64 | Received 04 Nov 1996, Published online: 09 Jul 2009

References

  • Sandvig K., van Deurs B. Endocytosis and intracellular sorting of ricin and Shiga toxin. FEBS Letters 1994; 3466: 99–102
  • Montecucco C., Papini E., Schiavo G. Bacterial protein toxins penetrate cells via a four-step mechanism. FEBS Letters 1994; 3466: 92–98
  • Schatz G., Dobberstein B. Common principles of protein translocation across membranes. Science 1996; 271: 1519–1526
  • Schiavo G., Benfenati F., Poulain B., Rosseto O., Polverino de Laureto P., DasGupta B. R., Montecucco C. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage by synaptobrevin. Nature 1992; 359: 832–835
  • Li J. Bacterial toxins. Current Opinion in Structural Biology 1992; 2: 545–556
  • Sansom M. S. P. The biophysics of peptide models of ion channels. Progress in Biophysical and Molecular Biology 1991; 55: 139–235
  • Ehrlich P. Chemotherapeutics: scientific principles, methods and results. Lancet 1913; 2: 445–451
  • Holmgren J., Lonnroth I., Mansson J., Svennerholm L. Interaction of cholera toxin and membrane GM1 ganglioside of small intestine. Proceedings of the National Academy of Sciences, USA 1975; 72: 2520–2524
  • Naglich J. G., Metherall J. E., Russell D. W., Eidels L. Expression cloning of a diphtheria toxin receptor: identity with a heparin-binding EGF-like growth factor precursor. Cell 1992; 69: 1051–61
  • Knight P. J., Knowles B. H., Ellar D. J. Molecular cloning of an insect aminopeptidase N that serves as a receptor for Bacillus thuringiensis CrylA(c) toxin. Journal of Biological Chemistry 1995; 270: 17765–17770
  • Parker M. W., van der Goot F. G., Buckley J. T. Aerolysin—the ins and outs of a channel forming toxin. Molecular Microbiology 1996; 19: 205–212
  • Nelson K. L., Raja S. M., Buckley J. T. The GPI-anchored surface glycoprotein Thy-1 is a receptor for the channel-forming toxin aerolysin. Journal of Biological Chemistry 1997, (In press)
  • Lutz F., Mohr M., Grimmig M., Leidolf R., Linder D. Pseudomonas aeruginosa cytotoxin-binding protein in rabbit erythrocyte membranes. An oligomer of 28 kDa with similarity to transmembrane channel proteins. European Journal of Biochemistry 1993; 217: 1123–1128
  • Allured V. S., Collier R. J., Carroll S. F., McKay D. B. Structure of exotoxin A of Pseudomonas aeruginosa at 3.0-Angstrom resolution. Proceedings of the National Academy of Science, USA 1986; 83: 1320–1324
  • Parker M. W., Pattus F., Tucker A. D., Tsernoglou D. Structure of the membrane-pore-forming fragment of colicin A. Nature 1989; 337: 93–96
  • Li J. D., Carroll J., Ellar D. J. Crystal structure of insecticidal delta-endotoxin from Bacillus thuringiensis at 2.5 Å resolution. Nature 1991; 353: 815–821
  • Choe S., Bennett M. J., Fujii G., Curmi P. M., Kantardjieff K. A., Collier R. J., Eisenberg D. The crystal structure of diphtheria toxin. Nature 1992; 357: 216–222
  • Wiener M., Freymann D., Ghosh P., Stroud R. M. Crystal structure of colicin la. Nature 1997; 385: 461–464
  • Parker M. W., Pattus F. Rendering a membrane protein soluble in water: a common packing motif in bacterial protein toxins. Trends in Biochemical Sciences 1993; 18: 391–395
  • Parker M. W., Tucker A. D., Tsernoglou D., Pattus F. Insights into membrane insertion based on studies of colicins. Trends in Biochemical Sciences 1990; 15: 126–129
  • Cramer W. A., Zhang Y. L., Schendel S., Merrill A. R., Song H. Y., Stauffacher C. V., Cohen F. S. Dynamic properties of the colicin E1 ion channel. FEMS Microbiology and Immunology 1992; 5: 71–81
  • London E. How bacterial protein toxins enter cells; the role of partial unfolding in membrane translocation. Molecular Microbiology 1992; 6: 3277–3282
  • van der Goot F. G., González-Mañas J. M., Lakey J. H., Pattus F. A ‘molten-globule’ membrane-insertion intermediate of the pore-forming domain of colicin A. Nature 1991; 354: 408–410
  • Jiang J. X., London E. Involvement of dentaturation-like changes in Pseudomonas exotoxin. A hydrophobicity and membrane penetration determined by characterization of pH and thermal transitions. Roles of two distinct conformationally altered states. Journal of Biological Chemistry 1990; 265: 8636–8641
  • Feng Q., Becktel W. J. pH-induced conformational transitions of Cry IA(a), Cry IA(c), and Cry IIIA delta-endotoxins in Bacillus thuringiensis. Biochemistry 1994; 33: 8521–8526
  • Schendel S. L., Cramer W. A. 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 Science 1994; 3: 2272–2279
  • Evans L. J. A., Goble M. L., Hales K. A., Lakey J. H. Different sensitivities to acid denaturation within a family of proteins: Implications for acid unfolding and membrane translocation. Biochemistry 1996; 35: 13180–13185
  • Bychkova V. E., Ptitsyn O. B. The molten globule in vitro and in vivo. Chemtracts-Biochemistry and Molecular Biology 1993; 4: 133–163
  • van der Goot F. G., Lakey J. H., Pattus F. The molten globule intermediate for protein insertion or translocation through membranes. Trends in Cell Biology 1992; 2: 343–348
  • Lakey J. H., van der Goot F. G., Pattus F. All in the family: the toxic activity of pore-forming toxins. Toxicology 1994; 87: 85–108
  • Cramer W. A., Heymann J. B., Schendel S. L., Deriy B. N., Cohen F. S., Elkins P. A., Stauffacher C. V. Structure-function of the channel-forming colicins. Annual Reviews in Biophysics and Biomolecular Structures 1995; 24: 611–641
  • Vetter I. R., Parker M. W., Partus F., Tsernoglou D. Insights into membrane insertion based on studies of colicins. Protein Toxin Structure, M. W. Parker. Springer Verlag, Heidelberg 1996; 5–24
  • Wormald M. R., Merrill A. R., Cramer W. A., Williams R. J. P. Solution NMR studies of colicin-E1 C-terminal thermolytic peptide-structural comparison with colicin-A and the effects of pH changes. European Journal of Biochemistry 1990; 191: 155–161
  • Elkins P. A., Song H. Y., Cramer W. A., Stauffacher C. V. Crystallization and characterization of colicin E1 channel-forming polypeptides. Proteins 1994; 19: 150–157
  • Ghosh P., Mel S. F., Stroud R. M. The domain structure of the ion channel-forming protein colicin la. Nature Structural Biology 1995; 1: 597–604
  • Pattus F., Martinez M. C., Dargent B., Cavard D., Verger R., Lazdunski C. Interaction of colicin A with phospholipid monolayers and liposomes. Biochemistry 1983; 22: 5698–5707
  • van der Goot F. G., Didat N., Pattus F., Dowhan W., Letellier L. Role of acidic lipids in the translocation and channel activity of colicins A and N in Escherichia coli cells. European Journal of Biochemistry 1993; 213: 217–221
  • Lakey J. H., Parker M. W., Gonzales-Mañas J-M., Duché D., Vriend G., Baty D., Pattus F. The role of electrostatic charge in the membrane insertion of colicin A. Calculation and mutation. European Journal of Biochemistry 1994; 220: 155–163
  • Brunden K. R., Uratani Y., Cramer W. A. Dependence of the conformation of a colicin E1 channel-forming peptide on acidic pH and solvent polarity. Journal of Biological Chemistry 1984; 259: 7682–7687
  • Merrill A. R., Cohen F. S., Cramer W. A. On the nature of the structural change of the colicin E1 channel peptide necessary for its translocation-competent state. Biochemistry 1990; 29: 5829–5836
  • Muga A., Conzales-Mañas J-M., Lakey J. H., Pattus F., Surewicz W. K. pH-Dependent stability and membrane interaction of the pore-forming domain of colicin A. Journal of Biological Chemistry 1993; 268: 1553–1557
  • Steer B. A., Merrill A. R. The colicin E1 insertion-competent state: detection of structural changes using fluorescence resonance energy transfer. Biochemistry 1994; 33: 1108–1115
  • Gonzales-Mañas J-M., Lakey J. H., Pattus F. Brominated phospholipids as a tool for monitoring the membrane insertion of colicin A. Biochemistry 1992; 31: 7294–7300
  • Gonzalez-Mañas J-M., Lakey J. H., Pattus F. Interaction of the colicin A pore-forming domain with negatively charged phospholipids. European Journal of Biochemistry 1993; 211: 625–633
  • Engelman D. M., Steitz T. A. The spontaneous insertion of proteins into and across membranes: the helical hairpin hypothesis. Cell 1981; 23: 411–422
  • Bénédetti H., Lloubès R., Lazdunski C., Letellier L. Colicin A unfolds during its translocation in Escherichia coli cells and spans the whole cell envelope when its pore is formed. EMBO Journal 1992; 11: 441–447
  • Duché D., Baty D., Chartier M., Letellier L. Unfolding of colicin A during its translocation through the Escherichia coli envelope as demonstrated by disulfide bond engineering. Journal of Biological Chemistry 1994; 269: 24820–24825
  • Lakey J. H., Massotte D., Heitz F., Dasseux J. L., Faucon J. F., Parker M. W., Pattus F. Membrane insertion of the pore-forming domain of colicin A. A spectroscopic study. European Journal of Biochemistry 1991; 196: 599–607
  • Rath P., Boousche O., Merril A. R., Cramer W. A., Rothschild K. J. Fourier transformed infrared evidence for a predominantly alpha-helical structure of the membrane bound channel forming COOH-terminal peptide of colicin E1. Biophysical Journal 1991; 59: 516–522
  • Lakey J., Duché D., Gonzales-Mañas J-M., Baty D., Pattus F. Fluorescence energy transfer distance measurements. The hydrophobic helical hairpin of colicin A in the membrane bound state. Journal of Molecular Biology 1993; 230: 1055–1067
  • Lakey J., Baty D., Pattus F. Fluorescence energy transfer distance measurements using site-directed single cysteine mutants. The membrane insertion of colicin A. Journal of Molecular Biology 1991; 218: 639–653
  • Duché D., Parker M. W., Gonzales-Mañas J-M., Pattus F., Baty D. Uncoupled steps of the colicin A pore formation demonstrated by disulfide bond engineering. Journal of Biological Chemistry 1994; 269: 6332–6339
  • Shin Y. K., Levinthal C., Levinthal F., Hubbell W. L. Colicin E1 binding to membranes: time-resolved studies of spin-labeled mutants. Science 1993; 259: 960–963
  • Massotte D., Yamamoto M., Scianimanico S., Sorokine O., Van Dorsselaer A. Y., Ourisson G., Pattus F. Structure of the membrane-bound form of the pore-forming domain of colicin A: a partial proteolysis and mass spectrometry study. Biochemistry 1993; 32: 13787–13794
  • Jakes K. S., Finkelstein A., Qiu X. Q., Slatin S. L. Major transmembrane rearrangements associated with gating of the pore-forming colicins. Medical Microbiology and Immunology 1996; 185: 110, (abstract)
  • Slatin S. L., Raymond L., Finkelstein A. Gating of a voltage-dependent channel (colicin E1) in planar lipid bilayers. The role of protein translocation. Journal of Membrane Biology 1986; 92: 247–254
  • Abrams C. K., Jakes K. S., Finkelstein A., Slatin S. L. Identification of a translocated gating charge in a voltage-dependent channel. Colicin E1 channels in planar phospholipid bilayer membranes. Journal of General Physiology 1991; 98: 77–93
  • Merrill A. R., Cramer W. A. Identification of a voltage-responsive segment of the potential-gated colicin-E1 ion channel. Biochemistry 1990; 29: 8529–8534
  • Slatin S. L., Qiu X. Q., Jakes K. S., Finkelstein A. Identification of a translocated protein segment in a voltage-dependent channel. Nature 1994; 371: 158–161
  • Qiu X. Q., Jakes K. S., Finkelstein A., Slatin S. L. Site-specific biotinylation of colicin la. A probe for protein conformation in the membrane. Journal of Biological Chemistry 1994; 269: 7483–7488
  • Duché D., Izard J., Gonzales-Mañas J-M., Parker M. W., Crest M., Chartier M., Baty D. Membrane topology of the colicin A pore-forming domain analyzed by disulfide bond engineering. Journal of Biological Chemistry 1996; 271: 15401–15406
  • Geli V., Lazdunski G. An α-helical hydrophobic hairpin as a specific determinant in protein-protein interaction occurring in Escherichia coli colicin A and B immunity systems. Journal of Bacteriology 1992; 174: 6432–6437
  • Zhang Y. L., Cramer W. A. Intra-membrane helix-helix interactions as the basis of inhibition of the colicin E1 ion channel by its immunity protein. Journal of Biological Chemistry 1993; 268: 10176–10184
  • Espesset D., Duché D., Baty D., Geli V. The channel domain of colicin A is inhibited by its immunity protein through direct interaction in the Escherichia coli inner membrane. EMBO Journal 1996; 15: 2356–2364
  • Collier R. J. Diphtheria toxin: structure and function of a cytocidal protein. ADP-ribosylating Toxins and G Proteins: insights into signal transduction, J. M. Vaughan, M. Vaughan. American Society of Microbiology, Washington, DC 1990; 3–19
  • London E. Diphtheria toxin: membrane interaction and membrane translocation. Biochimica et Biophysica Acta 1992; 1113: 25–51
  • Tsuneoka M., Nakayama K., Hatsuzawa K., Komada M., Kitamura N., Mekada E. Evidence for involvement of furin in cleavage and activation of diphtheria toxin. Journal of Biological Chemistry 1993; 268: 26461–26465
  • Tortorella D., Sesardic D., Dawes C. S., London E. Immunochemical analysis shows all three domains of diphtheria toxin penetrate across model membranes. Journal of Biological Chemistry 1995; 270: 27446–27452
  • Zhan H., Choe S., Huynh P. D., Finkelstein A., Eisenberg D., Collier R. J. Dynamic transitions of the transmembrane domain of diphtheria toxin: disulfide trapping and fluorescence proximity studies. Biochemistry 1994; 33: 11254–11263
  • Mindell J. A., Silverman J. A., Collier R. J., Finkelstein A. Locating a residue in the diphtheria toxin channel. Biophysical Journal 1992; 62: 41–44
  • Zhan H., Oh K. J., Shin Y. K., Hubbell W. L, Collier R. J. Interaction of the isolated transmembrane domain of diphtheria toxin with membranes. Biochemistry 1995; 34: 4856–4863
  • Silverman J. A., Mindell J. A., Zhan H., Finkelstein A., Collier R. J. Structure-function relationships in diphtheria toxin channels: I. Determining a minimal channel-forming domain. Journal of Membrane Biology 1994; 137: 17–28
  • Oh K. J., Zhan H., Cui C., Hideg K., Collier R. J., Hubbell W. L. Organization of diphtheria toxin T domain in bilayers: a site-directed spin labeling study. Science 1996; 273: 810–812
  • Lanzrein M., Sand O., Olsnes S. GPI-anchored diphtheria toxin receptor allows membrane translocation of the toxin without detectable ion channel activity. EMBO Journal 1996; 15: 725–734
  • Kagan B. L., Finkelstein A., Colombini M. Diphtheria toxin fragment forms large pores in phospholipid bilayer membranes. Proceedings of the National Academy of Sciences, USA 1981; 78: 4950–4954
  • Martoglio B., Hofmann M. W., Brunner J., Dobberstein B. The protein-conducting channel in the membrane of the endoplasmic reticulum is open laterally toward the lipid bilayer. Cell 1995; 81: 207–214
  • Bhakdi S., Tranum-Jensen J. Alpha-toxin of Staphylococcus aureus. Microbiological Reviews 1991; 55: 733–751
  • Braun V., Focareta T. Pore-forming bacterial protein hemolysins (cytolysins). Critical Reviews in Microbiology 1991; 18: 115–158
  • Perelle S., Gibert M., Boquet P., Popoff M. R. Characterization of Clostridium perfringens iota-toxin genes and expression in Escherichia coli. Infection and Immunity 1993; 61: 5147–5156
  • Li J., Koni P. A., Ellar D. J. Structure of the mosquitocidal δ-endotoxin CytB from Bacillus thuringiensis sp. kyushuensis and implications for membrane pore formation. Journal of Molecular Biology 1996; 257: 129–152
  • Petosa C., Collier R. J., Klimpel K. R., Leppla S. H., Liddington R. C. Crystal structure of the anthrax toxin protective antigen. Nature 1997; 385: 833–838
  • Song L., Hobaugh M. R., Shustak C., Cheley S., Bayley H., Gouaux J. E. Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science 1996; 274: 1859–1866
  • Morgan P. J., Varley P. G., Rowe A. J., Andrew P. W., Mitchell T. J. Characterization of the solution properties and conformation of pneumolysin, the membrane-damaging toxin of Streptococcus pneumoniae. Biochemical Journal 1993; 296: 671–674
  • Parker M. W., Buckley J. T., Postma J. P. M., Tucker A. D., Leonard K., Pattus F. T, Tsernoglou D. Structure of the Aeromonas toxin proaerolysin in its water-soluble and membrane-channel states. Nature 1994; 367: 292–295
  • Schulz G. E. Porins: general to specific, native to engineered passive pores. Current Opinion in Structural Biology 1996; 6: 485–490
  • Valeva A., Weisser A., Walker B., Kehoe M., Bayley H., Bhakdi S., Palmer M. Molecular architecture of a toxin pore: a 15-residue sequence lines the transmembrane channel of staphylococcal alpha-toxin. EMBO Journal 1996; 15: 1857–1864
  • Howard S. P., Buckley J. T. Activation of the hole forming toxin aerolysin by extracellular processing. Journal of Bacteriology 1985; 163: 336–340
  • van der Goot F. G., Hardie K. R., Parker M. W., Buckley J. T. The C-terminal peptide produced upon proteolytic activation of the cytolytic toxin aerolysin is not involved in channel formation. Journal of Biological Chemistry 1994; 269: 30496–30501
  • Milne J. C., Collier R. J. pH-dependent permea-bilization of the plasma membrane of mammalian cells by anthrax protective antigen. Molecular Microbiology 1993; 10: 647–653
  • Milne J. C., Furlong D., Hanna P. C., Wall J. S., Collier R. J. Anthrax protective antigen forms oligomers during intoxication of mammalian cells. Journal of Biological Chemistry 1994; 269: 20607–20612
  • Moniatte M., van der Goot F. G., Buckley J. T., Pattus F., Van Dorsselaer A. Characterization of the heptameric pore-forming complex of the Aeromonas toxin aerolysin using MALDI-TOF mass spectrometry. FEBS Letters 1996; 384: 269–272
  • Wilmsen H. U., Leonard K. R., Tichelaar W., Buckley J. T., Pattus F. The aerolysin membrane channel is formed by heptamerization of the monomer. EMBO Journal 1992; 11: 2457–2463
  • Gouaux J. E., Braha O., Hobaugh M. H., Song L., Cheley S., Shustak C., Bayley H. Subunit stoichiometry of staphylococcal α-hemolysin in crystals and on membranes: a heptameric transmembrane pore. Proceedings of the National Academy of Sciences, USA 1994; 91: 12828–12831
  • Morgan P. J., Hyman S. C., Byron O., Andrew P. W., Mitchell T. J., Rowe A. J. Modeling the bacterial protein toxin, pneumolysin, in its monomeric and oligomeric form. Journal of Biological Chemistry 1994; 269: 25315–25320
  • Olofsson A., Hebert H., Thelestam M. The projection structure of perfringolysin O (Clostridium perfringens theta-toxin). FEBS Letters 1993; 319: 125–127
  • Sekiya K., Satoh R., Danbara H., Futaesaku Y. A ring-shaped structure with a crown formed by streptolysin O on the erythrocyte membrane. Journal of Bacteriology 1993; 175: 5953–5961
  • van der Goot F. G., Wong K. R., Pattus F., Buckley J. T. Oligomerization of the channel-forming toxin aerolysin precedes its insertion into lipid bilayer. Biochemistry 1993; 32: 2636–2642
  • Thelestam M., Olofsson A., Blomqvist L., Hebert H. Oligomereisation of cell-bound staphylococcal alpha-toxin in relation to membrane permeabilisation. Biochimica et Biophysica Acta 1991; 1062: 245–254
  • Walker B., Krishnasastry M., Zorn L., Bayley H. Assembly of the oligomeric membrane pore formed by staphylococcal alpha-hemolysin examined by truncation mutagenesis. Journal of Biological Chemistry 1992; 267: 21782–21786
  • Vecsey-Semjen B., Möllby R., van der Goot F. G. Partial C-terminal unfolding is required for channel formation by staphylococcal alpha-toxin. Journal of Biological Chemistry 1996; 271: 8655–8660
  • Vecsey-Semjen B., Lesieur C., Möllby R., van der Goot F. G. Conformational changes due to membrane binding and channel formation by staphylococcal α-toxin. Journal of Biological Chemistry 1997; 272: 5709–5717
  • de Cock H., Tommassen J. Lipopolysaccharides and divalent cations are involved in the formation of an assembly-competent intermediate of outer-membrane protein PhoE of E. coli. EMBO Journal 1996; 15: 5567–5573
  • Menestrina G. Ionic channels formed by Staphylococcus aureus alpha toxin: voltage-dependent inhibition by divalent and trivalent cations. Journal of Membrane Biology 1986; 90: 177–190
  • Wilmsen H. U., Partus F., Buckley J. T. Aerolysin, a hemolysin from Aeromonas hydrophila, forms voltage-gated channels in planar bilayers. Journal of Membrane Biology 1990; 115: 71–81
  • Blaustein R. O., Koehler T. M., Collier R. J., Finkelstein A. Anthrax toxin: channel-forming activity of protective antigen in planar phospholipid bilayers. Proceedings of the National Academy of Sciences, USA 1989; 86: 2209–2213
  • van der Goot F., Ausio J., Wong K., Partus F., Buckley J. Dimerization stabilizes the pore-forming toxin aerolysin in solution. Journal of Biological Chemistry 1993; 268: 18272–18279
  • Ballard J., Crabtree J., Roe B. A., Tweten R. K. The primary structure of Clostridium septicum alpha-toxin exhibits similarity with that of Aeromonas hydrophila aerolysin. Infection and Immunity 1995; 63: 340–344
  • Gruber H. J., Wilmsen H. U., Cowell S., Schindler H., Buckley J. T. Partial purification of the rat erythrocyte receptor for the channel-forming toxin aerolysin and reconstitution into planar lipid bilayers. Molecular Microbiology 1994; 14: 1093–1101
  • Zhang F., Crise B., Su B., Hou Y., Rose J. K., Bothwell A., Jacobson K. Lateral diffusion of membrane-spanning and glycosylphosphatidylinositol-linked proteins: toward establishing rules governing the lateral mobility of membrane proteins. Journal of Cell Biology 1991; 115: 75–84
  • Parton R. G. Caveolin and caveolins. Current Opinion in Cell Biology 1996; 8: 542–548
  • Bhakdi S., Bayley H., Valeva A., Walev I., Walker B., Kehoe M., Palmer M. Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins. Archives in Microbiology 1996; 165: 73–79
  • Walker B., Bayley H. Key residues for membrane binding, oligomerization, and pore forming activity of staphylococcal α-hemolysin identified by cystein scanning mutagenesis and targeted chemical modification. Journal of Biological Chemistry 1995; 270: 23065–23071
  • Walker B., Braha O., Cheley S., Bayley H. An intermediate in the assembly of a pore-forming protein trapped with genetically-engineered switches. Chemistry and Biology 1995; 2: 99–105
  • Panchal R. G., Bayley H. Interactions between residues in staphylococcal α-hemolysin revealed by reversion mutagenesis. Journal of Biological Chemistry 1995; 270: 23072–23076
  • Tobkes N., Wallace B. A., Bayley H. Secondary structure and assembly mechanism of an oligomeric channel protein. Biochemistry 1985; 24: 1915–1920
  • Ikigai H., Nakae T. Conformational alteration in alpha-toxin from Staphylococcus aureus concomitant with the transformation of the water soluble monomer to the membrane oligomer. Biochemical and Biophysical Research Communications 1985; 130: 175–181
  • Ward R. J., Palmer M., Leonard K., Bhakdi S. Identification of a putative membrane-inserted segment in the alpha-toxin of Staphylococcus aureus. Biochemistry 1994; 33: 7477–7484
  • Leppla S. H. The anthrax toxin complex. Sourcebook of Bacterial Protein Toxins, J. Alouf, J. H. Freer. Academic Press, New York 1991; 277–302
  • Petosa C., Liddington R. C. The anthrax toxin. Protein Toxin Structure, M. W. Parker. Springer Verlag, Heidelberg 1996; 97–121
  • Klimpel K. R., Arora N., Leppla S. H. Anthrax toxin lethal factor contains a zinc metalloprotease consensus sequence which is required for lethal toxin activity. Molecular Microbiology 1994; 13: 1093–1100
  • Escuyer V., Collier R. J. Anthrax protective antigen interacts with a specific receptor on the surface of CHO-K1 cells. Infection and Immunity 1991; 59: 3381–3386
  • Klimpel K. R., Molloy S. S., Thomas G., Leppla S. H. Anthrax toxin protective antigen is activated by a cell surface protease with the sequence specificity and catalytic properties of furin. Proceedings of the National Academy of Science, USA 1992; 89: 10277–10281
  • Gordon V. M., Klimpel K. R., Arora N., Henderson M. A., Leppla S. H. Proteolytic activation of bacterial toxins by eukaryotic cells is performed by furin and by additional cellular proteases. Infection and Immunity 1995; 63: 82–87
  • Singh Y., Klimpel K. R., Quinn C. P., Chaudhary V. K., Leppla S. H. The carboxyl-terminal end of protective antigen is required for receptor binding and anthrax toxin activity. Journal of Biological Chemistry 1991; 266: 15493–15497
  • Koehler T. M., Collier R. J. Anthrax toxin protective antigen: low pH induced hydrophobicity and channel formation in liposomes. Molecular Microbiology 1991; 5: 1501–1506
  • Kochi S. K., Martin I., Schiavo G., Mock M., Cabiaux V. The effects of pH on the interaction of anthrax toxin lethal and edema factors with phospholipid vesicles. Biochemistry 1994; 33: 2604–9
  • Zhao J., Milne J. C., Collier R. J. Effect of anthrax toxin's lethal factor on ion channels formed by the protective antigen. Journal of Biological Chemistry 1995; 270: 18626–18630
  • Blanke S. R., Milne J. C., Benson E. L., Collier R. J. Fused polycationic peptide mediates delivery of diphtheria toxin A chain to the cytosol in the presence of anthrax protective antigen. Proceedings of the National Academy of Sciences, USA 1996; 93: 8437–8442
  • Milne J. C., Blanke S. R., Hanna P. C., Collier R. J. Protective antigen-binding domain of anthrax lethal factor mediates translocation of a heterologous protein fused to its amino- or carboxy-terminus. Molecular Microbiology 1995; 15: 661–666
  • Novak J. M., Stein M.-P., Little S. F., Leppla S. H., Friedlander A. M. Functional characterization of protease-treated Bacillus anthracis protective antigen. Journal of Biological Chemistry 1992; 267: 17186–17193
  • Singh Y., Klimpel K. R., Arora N., Sharma M., Leppla S. H. The chymotrypsin-sensitive site, FFD315, in anthrax toxin protective antigen is required for translocation of lethal factor. Journal of Biological Chemistry 1994; 269: 29039–29046
  • Li J. Insecticidal δ-endotoxins from Bacillus thuringiensis. Protein Toxin Structure, R. G. L. C. Michael, M. W. Parker. Springer-Verlag, Heidelberg 1996; 49–77
  • Koni P. A., Ellar D. J. Biochemical characterization of Bacillus thuringiensis cytolytic delta-endotoxins. Microbiology 1994; 140: 1869–1880
  • Drobniewski F. A., Ellar D. J. Toxin-membrane interactions of Bacillus thuringiensis δ-endotoxins. Biochemical Society Transactions 1988; 16: 39–40
  • Maddrell S. H., Lane N. J., Harrison J. B., Overton J. A., Moreton R. B. The initial stages in the action of an insecticidal delta-endotoxin of Bacillus thuringiensis var. israelensis on the epithelial cells of the Malpighian tubules of the insect, Rhodnius prolixus. Journal of Cell Science 1988; 90: 131–144
  • Chow E., Singh F. J. P., Gill S. S. Binding and aggregation of the 25 kilodalton toxin of Bacillus thuringiensis subsp. israelensis to cell membranes and alteration by monoclonal antibodies and amino acid modifiers. Applied Environmental Microbiology 1989; 55: 2779–2788
  • McLachlan A. D. Gene duplication in the structural evolution of chymotrypsin. Journal of Molecular Biology 1979; 128: 49–79
  • Protein Toxin Structure, M. W. Parker. Springer Verlag, Heidelberg 1996
  • Sixma T. K., Pronk S. E., Kalk K. H., Wartna E. S., van Zanten B. A., Witholt B., Hol W. G. Crystal structure of a cholera toxin-related heat-labile enterotoxin from E. coli. Nature 1991; 351: 371–377
  • Fraser M. E., Chemaia M. M., Kozlov Y. V., James M. N. Crystal structure of the holotoxin from Shigella dysentehae at 2.5 Å resolution. Nature Structural Biology 1994; 1: 59–64
  • Merritt E. A., Sarfaty S., van den Akker F., L'Hoir C., Martial J. A., Hoi W. G. Crystal structure of cholera toxin B-pentamer bound to receptor GM1 pentasaccharide. Protein Science 1994; 3: 166–175
  • Unwin N. Acetylcholine receptor channel imaged in the open state. Nature 1995; 373: 37–43
  • Walker J. E., Saraste M. Editorial overview: membrane protein structure. Current Opinion in Structural Biology 1996; 6: 457–459
  • Montal M. Protein fold in channel structure. Current Opinion in Structural Biology 1996; 6: 499–510
  • Peitsch M., Tschopp J. Assembly of the macro-molecular pores by immune defense systems. Current Opinion in Cell Biology 1991; 3: 710–716
  • Liu C. C., Walsh C. M., Young J. D. Perforin: structure and function. Immunology Today 1995; 16: 194–201
  • Muchmore S. W., Sattler M., Liang H., Meadows R. P., Harlan J. E., Yoon H. S., Nettesheim D., Chang B. S, Thompson C. B., Wong S. L., Ng S. C., Fesik S. W. X-ray and NMR structure of human Bcl-XL, an inhibitor of programmed cell death. Nature 1996; 381: 335–341
  • Minn A. J., Vélez P., Schendel S. L., Liang H., Muchmore S. W., Fesik S. W., Fill M., Thompson C. B. Bcl-XL forms an ion channel in synthetic lipid membranes. Nature 1997; 385: 353–357
  • Korsmeyer S. J. Regulators of cell death. Trends in Genetics 1995; 11: 101–105
  • Gajewski T. F., Thompson C. B. Apoptosis meets signal transduction: elimination of a BAD influence. Cell 1996; 87: 589–592
  • Kounnas M. Z., Morris R. E., Thompson M. R., Fitzgerald D. J., Strickland D. K., Saelinger C. B. The alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein binds and internalizes Pseudomonas exotoxin A. Journal of Biological Chemistry 1992; 267: 12420–12423
  • Morgan P. J., Hyman S. C., Rowe A. J., Mitchell T. J., Andrew P. W., Saibil H. R. Subunit organization and symmetry of pore-forming, oligomeric pneumolysis. FEBS Letters 1995; 371: 77–80

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.