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PMID: 2643104 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Cloned diphtheria toxin within the periplasm of Escherichia coli causes lethal membrane damage at low pH.

O'Keefe D, Collier RJ

Abstract

Acidic pH within endosomal vesicles of sensitive animal cells triggers a conformational change in diphtheria toxin (DT) that is believed to cause the B chain to insert into the vesicular membrane and the enzymic A chain to be released into the cytosol. In artificial lipid bilayers, DT forms ion-conductive channels under mildly acidic conditions (pH approximately 5). Here we report a related phenomenon in Escherichia coli strains that secrete certain cloned DT-related proteins into their periplasm: the cells are rapidly killed at pH 5 but remain unharmed at pH 7. Expression of full-length DT (an active-site mutant, to comply with the National Institutes of Health recombinant DNA guidelines) causes acid-sensitivity, whereas expression of the A chain alone does not. The killed cells are not lysed, but inner-membrane functions are impaired (membrane potential, active transport, and ion impermeability). We propose that acidification of DT within the periplasm induces its insertion into the inner membrane, lethally damaging the permeability barrier. This discovery provides a potentially important selection procedure for mutations affecting the membrane insertion function of DT. Similar approaches may be useful in studying other proteins that undergo condition-dependent interaction with membranes.

MeSH Terms
Biological Transport Cell Membrane/drug effects,physiology Cloning, Molecular Diphtheria Toxin/genetics,pharmacology Escherichia coli/drug effects,genetics Hydrogen-Ion Concentration Kinetics Membrane Potentials Plasmids Proline/metabolism Recombinant Proteins/pharmacology Rubidium/metabolism
Chemicals
Diphtheria Toxin Recombinant Proteins Proline Rubidium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
O'Keefe D
Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, MA 02115.
Collier R J
References (33)
33 references, click to expand
  1. Reduced temperature alters Pseudomonas exotoxin A entry into the mouse LM cell.
    Infect Immun. 1986 May;52(2):445-53 PMID: 3699892
  2. Effect of pH on the conformation of diphtheria toxin and its implications for membrane penetration.
    Biochemistry. 1985 Sep 24;24(20):5458-64 PMID: 4074708
  3. Ion-conducting channels produced by botulinum toxin in planar lipid membranes.
    Biochemistry. 1986 May 20;25(10):2872-6 PMID: 2424493
  4. Pseudomonas exotoxin A. Membrane binding, insertion, and traversal.
    J Biol Chem. 1986 Aug 25;261(24):11404-8 PMID: 3733757
  5. Fusion of phospholipid vesicles induced by alpha-lactalbumin at acidic pH.
    Biochemistry. 1986 Dec 2;25(24):7867-74 PMID: 3026464
  6. Expression of a mutant, full-length form of diphtheria toxin in Escherichia coli.
    Infect Immun. 1987 Jul;55(7):1647-51 PMID: 3110068
  7. Exotoxin A of Pseudomonas aeruginosa: active, cloned toxin is secreted into the periplasmic space of Escherichia coli.
    J Bacteriol. 1987 Nov;169(11):4962-6 PMID: 3117768
  8. Binding of triton X-100 to diphtheria toxin, crossreacting material 45, and their fragments.
    Proc Natl Acad Sci U S A. 1976 Dec;73(12):4449-53 PMID: 63947
  9. Diphtheria toxin and related proteins. I. Isolation and properties of mutant proteins serologically related to diphtheria toxin.
    J Biol Chem. 1973 Jun 10;248(11):3838-44 PMID: 4196584
  10. Inhibitors of receptor-mediated endocytosis block the entry of Bacillus anthracis adenylate cyclase toxin but not that of Bordetella pertussis adenylate cyclase toxin.
    Infect Immun. 1988 May;56(5):1066-9 PMID: 2895741
  11. Periplasmic space in Salmonella typhimurium and Escherichia coli.
    J Biol Chem. 1977 Nov 10;252(21):7850-61 PMID: 334768
  12. Dye indicators of membrane potential.
    Annu Rev Biophys Bioeng. 1979;8:47-68 PMID: 383007
  13. Aerotaxis in Salmonella typhimurium: role of electron transport.
    J Bacteriol. 1981 Feb;145(2):990-1001 PMID: 6257658
  14. Diphtheria toxin entry into cells is facilitated by low pH.
    J Cell Biol. 1980 Dec;87(3 Pt 1):828-32 PMID: 7462324
  15. The entry of diphtheria toxin into the mammalian cell cytoplasm: evidence for lysosomal involvement.
    J Cell Biol. 1980 Dec;87(3 Pt 1):849-54 PMID: 7462326
  16. Diphtheria toxin forms transmembrane channels in planar lipid bilayers.
    Proc Natl Acad Sci U S A. 1981 Jan;78(1):172-6 PMID: 6264431
  17. Rapid entry of nicked diphtheria toxin into cells at low pH. Characterization of the entry process and effects of low pH on the toxin molecule.
    J Biol Chem. 1981 Sep 10;256(17):9068-76 PMID: 7263699
  18. Diphtheria toxin fragment forms large pores in phospholipid bilayer membranes.
    Proc Natl Acad Sci U S A. 1981 Aug;78(8):4950-4 PMID: 6272284
  19. Entry of the toxic proteins abrin, modeccin, ricin, and diphtheria toxin into cells. II. Effect of pH, metabolic inhibitors, and ionophores and evidence for toxin penetration from endocytotic vesicles.
    J Biol Chem. 1982 Jul 10;257(13):7504-13 PMID: 7085634
  20. Colicins and other bacteriocins with established modes of action.
    Annu Rev Microbiol. 1982;36:125-44 PMID: 6184011
  21. Construction and analysis of in vivo activity of E. coli promoter hybrids and promoter mutants that alter the -35 to -10 spacing.
    Gene. 1982 Dec;20(2):231-43 PMID: 6299890
  22. Cloned fragment A of diphtheria toxin is expressed and secreted into the periplasmic space of Escherichia coli K12.
    Science. 1983 Apr 29;220(4596):515-7 PMID: 6403984
  23. Ammonium chloride and methylamine hydrochloride antagonize clostridial neurotoxins.
    J Pharmacol Exp Ther. 1983 Jun;225(3):546-52 PMID: 6864519
  24. Nucleotide sequence and expression of the diphtheria tox228 gene in Escherichia coli.
    Science. 1983 Aug 26;221(4613):855-8 PMID: 6348945
  25. Localization in diphtheria toxin fragment B of a region that induces pore formation in planar lipid bilayers at low pH.
    FEBS Lett. 1983 Aug 22;160(1-2):82-6 PMID: 6309569
  26. Molecular cloning and expression of gene fragments from corynebacteriophage beta encoding enzymatically active peptides of diphtheria toxin.
    J Bacteriol. 1983 Nov;156(2):680-5 PMID: 6313613
  27. Nucleotide sequence of the structural gene for diphtheria toxin carried by corynebacteriophage beta.
    Proc Natl Acad Sci U S A. 1983 Nov;80(22):6853-7 PMID: 6316330
  28. Membrane fusion proteins of enveloped animal viruses.
    Q Rev Biophys. 1983 May;16(2):151-95 PMID: 6359230
  29. Evidence for penetration of diphtheria toxin to the cytosol through a prelysosomal membrane.
    Infect Immun. 1984 Apr;44(1):145-50 PMID: 6706404
  30. Dependence of the activity of colicin E1 in artificial membrane vesicles on pH, membrane potential, and vesicle size.
    J Biol Chem. 1984 Jan 10;259(1):594-600 PMID: 6706954
  31. Identification of a cold-sensitive step in the mechanism of modeccin action.
    J Biol Chem. 1984 Apr 10;259(7):4083-8 PMID: 6706992
  32. Interaction of tetanus toxin with lipid vesicles at low pH. Protection of specific polypeptides against proteolysis.
    J Biol Chem. 1985 Jun 10;260(11):6827-35 PMID: 3922981
  33. Macrophages are sensitive to anthrax lethal toxin through an acid-dependent process.
    J Biol Chem. 1986 Jun 5;261(16):7123-6 PMID: 3711080
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1989-01-00
Pages
343-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC286461
Subset
IM
Grants
NIAID NIH HHS · AI-22021 · United States
NIAID NIH HHS · AI-22848 · United States
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