Skip to main content
PMC home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1986 Jul;78(1):177–184. doi: 10.1172/JCI112548

Effects of the putative neutrophil-generated toxin, hypochlorous acid, on membrane permeability and transport systems of Escherichia coli.

J M Albrich, J H Gilbaugh 3rd, K B Callahan, J K Hurst
PMCID: PMC329547  PMID: 3013936

Abstract

Titrimetric addition of hypochlorous acid (HOCl) or chloramine (NH2Cl) to suspensions of Escherichia coli decreases their ability to accumulate 14C-labeled glutamine, proline, thiomethylgalactoside, and leucine in a manner that approximately coincides with loss of cell viability; quantitative differences in cellular response are observed with the two oxidants. Inhibition of beta-galactosidase activity in E. coli ML-35, a strain lacking functional lactose permease, is complex and also depends upon the identity of the oxidant. Membrane proton conductivities and glycerol permeabilities are unchanged by addition of HOCl or NH2Cl in excess of that required for inactivation. The combined results are interpreted to indicate that the locus of HOCl attack is the cell envelope, that HOCl inactivation does not occur by loss of membrane structural integrity, that loss of transport function can be identified with either selective oxidative inhibition of the transport proteins or loss of cellular metabolic energy, and that different mechanisms of inactivation may exist for HOCl and NH2Cl.

Full text

PDF
177

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albrich J. M., Hurst J. K. Oxidative inactivation of Escherichia coli by hypochlorous acid. Rates and differentiation of respiratory from other reaction sites. FEBS Lett. 1982 Jul 19;144(1):157–161. doi: 10.1016/0014-5793(82)80591-7. [DOI] [PubMed] [Google Scholar]
  2. Albrich J. M., McCarthy C. A., Hurst J. K. Biological reactivity of hypochlorous acid: implications for microbicidal mechanisms of leukocyte myeloperoxidase. Proc Natl Acad Sci U S A. 1981 Jan;78(1):210–214. doi: 10.1073/pnas.78.1.210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Alemohammad M. M., Knowles C. J. Osmotically induced volume and turbidity changes of Escherichia coli due to salts, sucrose and glycerol, with particular reference to the rapid permeation of glycerol into the cell. J Gen Microbiol. 1974 May;82(1):125–142. doi: 10.1099/00221287-82-1-125. [DOI] [PubMed] [Google Scholar]
  4. BRINGMANN G. Elektronenmikroskopische Befunde zur Wirkung von Chlor, Brom, Jod, Kupfer, Silber und Wasserstoff-superoxyd auf E. coli. Z Hyg Infektionskr. 1953;138(2):155–166. [PubMed] [Google Scholar]
  5. Babior B. M. Oxygen-dependent microbial killing by phagocytes (second of two parts). N Engl J Med. 1978 Mar 30;298(13):721–725. doi: 10.1056/NEJM197803302981305. [DOI] [PubMed] [Google Scholar]
  6. Beckerdite S., Mooney C., Weiss J., Franson R., Elsbach P. Early and discrete changes in permeability of Escherichia coli and certain other gram-negative bacteria during killing by granulocytes. J Exp Med. 1974 Aug 1;140(2):396–409. doi: 10.1084/jem.140.2.396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Camper A. K., McFeters G. A. Chlorine injury and the enumeration of waterborne coliform bacteria. Appl Environ Microbiol. 1979 Mar;37(3):633–641. doi: 10.1128/aem.37.3.633-641.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Elsbach P., Beckerdite S., Pettis P., Franson R. Persistence of regulation of macromolecular synthesis by Escherichia coli during killing by disrupted rabbit granulocytes. Infect Immun. 1974 Apr;9(4):663–668. doi: 10.1128/iai.9.4.663-668.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Elsbach P. On the interaction between phagocytes and micro-organisms. N Engl J Med. 1973 Oct 18;289(16):846–852. doi: 10.1056/NEJM197310182891610. [DOI] [PubMed] [Google Scholar]
  10. Elsbach P., Pettis P., Beckerdite S., Franson R. Effects of phagocytosis by rabbit granulocytes on macromolecular synthesis and degradation in different species of bacteria. J Bacteriol. 1973 Aug;115(2):490–497. doi: 10.1128/jb.115.2.490-497.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Elsbach P., Weiss J. A reevaluation of the roles of the O2-dependent and O2-independent microbicidal systems of phagocytes. Rev Infect Dis. 1983 Sep-Oct;5(5):843–853. doi: 10.1093/clinids/5.5.843. [DOI] [PubMed] [Google Scholar]
  12. Elsbach P., Weiss J., Franson R. C., Beckerdite-Quagliata S., Schneider A., Harris L. Separation and purification of a potent bactericidal/permeability-increasing protein and a closely associated phospholipase A2 from rabbit polymorphonuclear leukocytes. Observations on their relationship. J Biol Chem. 1979 Nov 10;254(21):11000–11009. [PubMed] [Google Scholar]
  13. FRIBERG L. Further quantitative studies on the reaction of chlorine with bacteria in water disinfection. II. Experimental investigations with C136 and P32. Acta Pathol Microbiol Scand. 1957;40(1):67–80. [PubMed] [Google Scholar]
  14. Fox C. F., Kennedy E. P. Specific labeling and partial purification of the M protein, a component of the beta-galactoside transport system of Escherichia coli. Proc Natl Acad Sci U S A. 1965 Sep;54(3):891–899. doi: 10.1073/pnas.54.3.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Glaser J. H., Conrad H. E. Properties of chick embryo chondrocytes grown in serum-free medium. J Biol Chem. 1984 Jun 10;259(11):6766–6772. [PubMed] [Google Scholar]
  16. Grisham M. B., Jefferson M. M., Melton D. F., Thomas E. L. Chlorination of endogenous amines by isolated neutrophils. Ammonia-dependent bactericidal, cytotoxic, and cytolytic activities of the chloramines. J Biol Chem. 1984 Aug 25;259(16):10404–10413. [PubMed] [Google Scholar]
  17. Heller K. B., Lin E. C., Wilson T. H. Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli. J Bacteriol. 1980 Oct;144(1):274–278. doi: 10.1128/jb.144.1.274-278.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hengge R., Boos W. Maltose and lactose transport in Escherichia coli. Examples of two different types of concentrative transport systems. Biochim Biophys Acta. 1983 Aug 11;737(3-4):443–478. doi: 10.1016/0304-4157(83)90009-6. [DOI] [PubMed] [Google Scholar]
  19. Hurst J. K., Albrich J. M., Green T. R., Rosen H., Klebanoff S. Myeloperoxidase-dependent fluorescein chlorination by stimulated neutrophils. J Biol Chem. 1984 Apr 25;259(8):4812–4821. [PubMed] [Google Scholar]
  20. KOCH A. L. The inactivation of the transport mechanism for beta-galactosides of Escherichia coli under various physiological conditions. Ann N Y Acad Sci. 1963 Jan 21;102:602–620. doi: 10.1111/j.1749-6632.1963.tb13663.x. [DOI] [PubMed] [Google Scholar]
  21. Leive L. Studies on the permeability change produced in coliform bacteria by ethylenediaminetetraacetate. J Biol Chem. 1968 May 10;243(9):2373–2380. [PubMed] [Google Scholar]
  22. Maloney P. C. Membrane H+ conductance of Streptococcus lactis. J Bacteriol. 1979 Oct;140(1):197–205. doi: 10.1128/jb.140.1.197-205.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mitchell P., Moyle J. Acid-base titration across the membrane system of rat-liver mitochondria. Catalysis by uncouplers. Biochem J. 1967 Aug;104(2):588–600. doi: 10.1042/bj1040588. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Passo S. A., Weiss S. J. Oxidative mechanisms utilized by human neutrophils to destroy Escherichia coli. Blood. 1984 Jun;63(6):1361–1368. [PubMed] [Google Scholar]
  25. Pavlasova E., Harold F. M. Energy coupling in the transport of beta-galactosides by Escherichia coli: effect of proton conductors. J Bacteriol. 1969 Apr;98(1):198–204. doi: 10.1128/jb.98.1.198-204.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sanno Y., Wilson T. H., Lin E. C. Control of permeation to glycerol in cells of Escherichia coli. Biochem Biophys Res Commun. 1968 Jul 26;32(2):344–349. doi: 10.1016/0006-291x(68)90392-6. [DOI] [PubMed] [Google Scholar]
  27. Scholes P., Mitchell P. Acid-base titration across the plasma membrane of Micrococcus denitrificans: factors affecting the effective proton conductance and the respiratory rate. J Bioenerg. 1970 Jun;1(1):61–72. doi: 10.1007/BF01516089. [DOI] [PubMed] [Google Scholar]
  28. Segal A. W., Geisow M., Garcia R., Harper A., Miller R. The respiratory burst of phagocytic cells is associated with a rise in vacuolar pH. Nature. 1981 Apr 2;290(5805):406–409. doi: 10.1038/290406a0. [DOI] [PubMed] [Google Scholar]
  29. Sips H. J., Hamers M. N. Mechanism of the bactericidal action of myeloperoxidase: increased permeability of the Escherichia coli cell envelope. Infect Immun. 1981 Jan;31(1):11–16. doi: 10.1128/iai.31.1.11-16.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Thomas E. L. Myeloperoxidase, hydrogen peroxide, chloride antimicrobial system: nitrogen-chlorine derivatives of bacterial components in bactericidal action against Escherichia coli. Infect Immun. 1979 Feb;23(2):522–531. doi: 10.1128/iai.23.2.522-531.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Thomas E. L. Myeloperoxidase-hydrogen peroxide-chloride antimicrobial system: effect of exogenous amines on antibacterial action against Escherichia coli. Infect Immun. 1979 Jul;25(1):110–116. doi: 10.1128/iai.25.1.110-116.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Weiss J., Victor M., Elsbach P. Role of charge and hydrophobic interactions in the action of the bactericidal/permeability-increasing protein of neutrophils on gram-negative bacteria. J Clin Invest. 1983 Mar;71(3):540–549. doi: 10.1172/JCI110798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Weiss S. J., Klein R., Slivka A., Wei M. Chlorination of taurine by human neutrophils. Evidence for hypochlorous acid generation. J Clin Invest. 1982 Sep;70(3):598–607. doi: 10.1172/JCI110652. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES