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Novel approaches to the mode of action of colicins

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Abstract

According to the theory of Fredericq (1949) and Nomura (1964), colicins are attached by specific receptor sites in the cell walls of sensitive bacteria, which mediate their inhibitive effects. During last years, a great variety of experimental data have been accumulated, some of which cannot be easily interpreted in terms of this theory. There exist considerable discrepancies concerning the chemical nature and molecular weight of isolated receptors. The attachment of a colicin onto its receptor need not be irreversible. The inhibition of numerous membrane-associated functions in colicin-tolerant mutants suggests their pleiotropic deletion nature. The difference between colicin resistance and colicin tolerance does not seem to be clear-cut. Cells of stable L-forms of protoplast type, completely devoid of their walls, retain in most cases the same patterns of sensitivity to colioins as rods of the same strains. Experimental changes in the relationship between the cell wall and the cytoplasmic membrane decrease colicin sensitivity of the cells. Colicin E3 has been found to be a specific endoribonuclease, able to cleave a terminal fragment from the 16 S rRNA also in isolated ribosomesin vitro: not only in ribosomes from sensitivive bacteria, but also in those from resistant ones and from eukaryotic cells. A destabilization of the DNA helix was induced by colicin E2in vitro asin vivo. It seems that there exist two distinct types of colicin receptors with different functions: those in the cell wall, and those in the cytoplasmic membrane. Only the contact of colicins with the latter ones is biologically effective and starts both stages of their inhibitive effect: the reversible and the irreversible ones.

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References

  • Almendinger R., Hager L. P.: Role for endonuclease I in the transmission process of oolicin E2.Nature New Biol. 235, 199 (1972).

    PubMed  CAS  Google Scholar 

  • Beppu T., Arima K.: Dissociating activity of purified colicin E2 on the isolated membrane complex ofEscherichia coli.Biochim. Biophys. Acta 219, 512 (1970).

    Article  PubMed  CAS  Google Scholar 

  • Beppu T., Arima K.: Dissociating activity of purified colicin E2 on the isolated DNA-membrane ofEscherichia coli.Biochim. Biophys. Acta 262, 453 (1972).

    PubMed  CAS  Google Scholar 

  • Beppu T., Kawabata K., Arima K.: Specific inhibition of cell division by colicin E2 without degradation of deoxyribonucleic acid in a new colicin sensitivity mutant ofEscherichia coli.J. Bacteriol. 110, 485 (1972).

    PubMed  CAS  Google Scholar 

  • Bhattacharyya P., Wendt L., Whitney E., Silver S.: Colicin-tolerant mutants ofEscherichia coli: resistance of membranes to colicin El.Science 168, 998 (1970).

    Article  PubMed  CAS  Google Scholar 

  • Boon T.: Inactivation of ribosomesin vitro by colicin E3.Proc. Natl. Acad. Sci. U.S.A. 68, 2421 (1971).

    Article  PubMed  CAS  Google Scholar 

  • Bowman C. M., Sidikaro J., Nomura M.: Specific inactivation of ribosomes by colicine E3in vitro and mechanism of immunity in colicinogenic cells.Nature New Biol. 234, 48 (1971).

    Article  Google Scholar 

  • Braun V., Schaller K., Wolff H.: A common receptor protein for phage T5 and colicin M in the outer membraneof Escherichia coli B.Biochim. Biophys. Acta 323, 87 (1973).

    Article  PubMed  CAS  Google Scholar 

  • Buxton R. S., Holland I. B.: Colicin E2-induced DNA solubilization in mutants ofEscherichia coli deficient in endonuclease I.FEBS Lett. 39, 1 (1974).

    Article  PubMed  CAS  Google Scholar 

  • Chang Y. Y., Hager L. P.: Inhibition of colicin E2 activity by bacterial lipopolysaccharide.J. Bacteriol. 104, 1106 (1970).

    PubMed  CAS  Google Scholar 

  • Cramer W. A., Keenan T. W.: Phospholipase A activity is not associated with early effects of colicin El.Biochim. Biophys. Res. Commun. 56, 60 (1974).

    Article  CAS  Google Scholar 

  • Cramer W. A., Phillips S. K., Keenan T. W.: On the role of membrane phase in the transmission mechanism of colicin El.Biochemistry 12, 1177 (1973).

    Article  PubMed  CAS  Google Scholar 

  • DeGraafF. K., VanVughtM. J. J., Stouthamer A. H.: Cell-envelope changes in mutants ofCitrobacter freundii with altered response to colicin A. Ant. v. LeeuwenhoekJ. Microbiol. Serol. 39, 51 (1973).

    Google Scholar 

  • DiMasiD. R., White J. C., Schnaitman C. A., Bradbeer C.: Transport of vitamin B12 inEscherichia coli: common receptor sites for vitamin B12 and the E colicins on the outer membrane of the cell envelope.J. Bacteriol. 115, 506 (1973).

    Google Scholar 

  • Fredericq P.: Sur la résistance croisée entre colicine E et bactériophage II.C. R. Soc. Biol. 143, 1011 (1949).

    Google Scholar 

  • Guterman S. K.: Colicin B: mode of action and inhibition by enterochelin.J. Bacteriol. 114, 1217 (1973).

    PubMed  CAS  Google Scholar 

  • Guterman S. K., Luria S. E.:Escherichia coli: strains that excrete an inhibitor of colicin B.Science 164, 1414 (1969).

    Article  PubMed  CAS  Google Scholar 

  • Hamon Y., Péron Y.: Sur les propriétés détergentes des molécules de bactériocines.C. R. Acad. Sci. D277, 1401 (1973).

    CAS  Google Scholar 

  • Hill C., Holland I. B.: Genetic basis of colicin E susceptibility inEscherichia coli. I. Isolation and properties of refractory mutants and the preliminary mapping of their mutations.J. Bacteriol. 94, 677 (1967).

    PubMed  CAS  Google Scholar 

  • Holland É. M., Holland I. B.: Induction of DNA breakdown and inhibition of cell division by colicin E2. Nature of some early steps in the process and properties of the E2-specific nuclease system.J. Gen. Microbiol. 64, 223 (1970).

    PubMed  CAS  Google Scholar 

  • Holland I. B., Samson A. C. R., Holland É. M., Senior B. W.: Aspects of membrane structure and function inEscherichia coli. CIBA Found. Symp. Growth Control in Cell Cultures p. 221, 1971.

  • Jetten A. M., Vogels G. D.: Inhibition of amino acid transport in membrane vesicles by colicin A and staphylococcin 1580. Ant. v. LeeuwenhoekJ. Microbiol. Serol. 39, 360 (1973).

    Google Scholar 

  • Koniski J., Liu C. T.: Solubilization and partial characterization of the colicin I receptor ofEscherichia coli.J. Biol. Chem. 249, 835 (1974).

    Google Scholar 

  • Marotel-Schirman J., Barbu E.: Interactions entre colicines et divers constituants de la surface bactérienne.C. R. Acad. Sci. D276, 1779 (1973).

    Google Scholar 

  • Meyhack B., Meyhack I., Apirion D.: Colicin E3: a unique endoribonuclease.Proc. Natl. Acad. Sci. U.S.A. 70, 156 (1973).

    Article  PubMed  CAS  Google Scholar 

  • Nagel de Zwaig R., Luria S. E.: Genetics and physiology of colicin-tolerant mutants ofEscherichia coli.J. Bacteriol. 94, 1112 (1967).

    PubMed  CAS  Google Scholar 

  • Nomura M.: Mechanism of action of colicines.Proc. Nat. Acad. Sci. U.S.A. 52, 1514 (1964).

    Article  CAS  Google Scholar 

  • Ohsumi Y., Maeda A.: Inactivation of ribosomes by a factor induced by colicin E3.J. Biochem. 71, 911 (1972).

    CAS  Google Scholar 

  • Plate C. A., Luria S. E.: Stages in colicin K action, as revealed by the action of trypsin.Proc. Natl. Acad. Sci. U.S.A. 69, 2030 (1972).

    Article  PubMed  CAS  Google Scholar 

  • Reeves P.: Mutants resistant to colicin CA 42-E2: cross resistance and genetic mapping of a special class of mutants.Austral. J. Exp. Biol. Med. Sci. 44, 301 (1966).

    Article  CAS  Google Scholar 

  • Reynolds B. L., Reeves P. R.: Kinetics of adsorption of colicin CA 42-E2 and reversal of its bactericidal activity.J. Bacteriol. 100, 301 (1969).

    PubMed  CAS  Google Scholar 

  • Ringrose P. S.: Interaction between colicin E2 and DNAin vitro.FEBS Lett. 23, 241 (1972).

    Article  PubMed  CAS  Google Scholar 

  • Ringrose P. S.: Effects of colicin E2 on DNA and the bacterial membranein vivo.Biochim. Biophys. Acta 312, 656 (1973).

    PubMed  CAS  Google Scholar 

  • Sabet S. F., Schnaitman C. A.: Purification and properties of the colicin E3 receptor ofEscherichia coli.J. Biol. Chem. 248, 1797 (1973).

    PubMed  CAS  Google Scholar 

  • Shannon R., Hedges A. J.: Reversibility of the specific adsorption of colicin E2-P9 to cells of eolicinsensitive strainsof Escherichia coli.J. Bacteriol. 116, 1136 (1973).

    PubMed  CAS  Google Scholar 

  • Sidikaro J., Nomura M.: Colicin E3-inducedin vitro inactivation of ribosomes from colicin-insensitive bacterial species.FEBS Lett. 29, 15 (1973).

    Article  PubMed  CAS  Google Scholar 

  • Šmabda J., Ebringer L., Mach J.: The effect of colicin E2 on the flagellateEuglena gracilis.J. Gen. Microbiol. 86, 363 (1975).

    Google Scholar 

  • Šmarda J., Kousalík J., Pavlák I.: Adsorption and effect of colicins on sensitive bacteriaEscherichia coli with altered cell surface.Folia Microbiol. 20, 64 (1975).

    Google Scholar 

  • Šmarda J., Laněk B.: Possibility of use of colicin-refractory mutants in the study of localization of colicin receptors.Folia Microbiol. 16, 481 (1971).

    Article  Google Scholar 

  • Šmarda J., Schuhmann E.: An ambiguous effect of colicin E3 on wall-less stable L-form cellsof Escherichia coli.Z. Allg. Mikrobiol. 14, 241 (1974).

    Article  PubMed  Google Scholar 

  • Smarda J., Taubeneck U.: Situation of colicin receptors in surface layers of bacterial cells.J. Gen. Microbiol. 52, 161 (1968).

    Google Scholar 

  • Takagaki Y., Kunugita K., Matsuhashi M.: Evidence for the direct action of colicin K on aerobic32P1 uptake inEscherichia coli in vivo andin vitro.J. Bacteriol. 113, 42 (1973).

    PubMed  CAS  Google Scholar 

  • Tubnowsky F., Högknauek G.: Colicin E3, an inactivating agent of the ribosomal A-site.Biochem. Biophys. Res. Commun. 55, 1246 (1973).

    Article  Google Scholar 

  • Weltzien H. U., Jesaitis M. A.: The nature of the colicin K receptor ofEscherichia coli Cullen.J. Exp. Med. 133, 534 (1971).

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Biology, Medical Faculty, J. E. Purkyně University, 662 43, Brno

    J. Šmarda

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Dedicated to Prof. O. Necas on the occasion of his 50th birthday

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Šmarda, J. Novel approaches to the mode of action of colicins. Folia Microbiol 20, 264–271 (1975). https://doi.org/10.1007/BF02876789

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