Skip to main content
NCBI home page
Antimicrobial Agents and Chemotherapy logoLink to Antimicrobial Agents and Chemotherapy
. 1981 Sep;20(3):307–313. doi: 10.1128/aac.20.3.307

Active uptake of tetracycline by membrane vesicles from susceptible Escherichia coli.

L M McMurry, J C Cullinane, R E Petrucci Jr, S B Levy
PMCID: PMC181692  PMID: 7030198

Abstract

A major portion of tetracycline accumulation by susceptible bacterial cells is energy dependent. Inner membrane vesicles prepared from susceptible Escherichia coli cells concentrated tetracycline 2.5 to 5 times above the external concentration when the electron transport substrate D-lactate or reduced phenazine methosulfate was added. This stimulation was reversed by cyanide, 2,4-dinitrophenol, and carbonyl cyanide m-chlorophenyl hydrazone. These vesicles data showed that proton motive force alone could energize tetracycline uptake. The lactate-dependent uptake had a pH optimum of 6.9 and a magnesium optimum of 1 mM and was not saturable up to 400 microM tetracycline. Although the vesicles were not as active as cells in concentrating tetracycline, they were less active to a similar extent in concentrating tetracycline, they were less active to a similar extent in concentrating proline, the transport of which is known to be solely proton motive force dependent. Therefore, we concluded that the active uptake of tetracycline in susceptible cells was largely, if not solely, energized by proton motive force.

Full text

PDF
307

Selected References

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

  1. ARIMA K., IZAKI K. ACCUMULATION OF OXYTETRACYCLINE RELEVANT TO ITS BACTERICIDAL ACTION IN THE CELLS OF ESCHERICHIA COLI. Nature. 1963 Oct 12;200:192–193. doi: 10.1038/200192a0. [DOI] [PubMed] [Google Scholar]
  2. Adler L. W., Rosen B. P. Functional mosaicism of membrane proteins in vesicles of Escherichia coli. J Bacteriol. 1977 Feb;129(2):959–966. doi: 10.1128/jb.129.2.959-966.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Asleson G. L., Frank C. W. pH dependence of carbon-13 nuclear magnetic resonance shifts of tetracycline. Microscopic dissociation constants. J Am Chem Soc. 1976 Aug 4;98(16):4745–4749. doi: 10.1021/ja00432a009. [DOI] [PubMed] [Google Scholar]
  4. Ball P. R., Shales S. W., Chopra I. Plasmid-mediated tetracycline resistance in Escherichia coli involves increased efflux of the antibiotic. Biochem Biophys Res Commun. 1980 Mar 13;93(1):74–81. doi: 10.1016/s0006-291x(80)80247-6. [DOI] [PubMed] [Google Scholar]
  5. Berger E. A. Different mechanisms of energy coupling for the active transport of proline and glutamine in Escherichia coli. Proc Natl Acad Sci U S A. 1973 May;70(5):1514–1518. doi: 10.1073/pnas.70.5.1514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Colaizzi J. L., Klink P. R. pH-Partition behavior of tetracyclines. J Pharm Sci. 1969 Oct;58(10):1184–1189. doi: 10.1002/jps.2600581003. [DOI] [PubMed] [Google Scholar]
  7. Dockter M. E., Magnuson J. A. Characterization of the active transport of chlorotetracycline in staphylococcus aureus by a fluorescence technique. J Supramol Struct. 1974;2(1):32–44. doi: 10.1002/jss.400020105. [DOI] [PubMed] [Google Scholar]
  8. FRANKLIN T. J., GODFREY A. RESISTANCE OF ESCHERICHIA COLI TO TETRACYCLINES. Biochem J. 1965 Jan;94:54–60. doi: 10.1042/bj0940054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Franklin T. J., Higginson B. Active accumulation of tetracycline by Escherichia coli. Biochem J. 1970 Jan;116(2):287–297. doi: 10.1042/bj1160287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Franklin T. J. Uptake of tetracycline by membrane preparations from Escherichia coli. Biochem J. 1971 Jun;123(2):267–273. doi: 10.1042/bj1230267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. HIEROWSKI M. INHIBITION OF PROTEIN SYNTHESIS BY CHLORTETRACYCLINE IN THE E. COLI IN VITRO SYSTEM. Proc Natl Acad Sci U S A. 1965 Mar;53:594–599. doi: 10.1073/pnas.53.3.594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Harold F. M. Conservation and transformation of energy by bacterial membranes. Bacteriol Rev. 1972 Jun;36(2):172–230. doi: 10.1128/br.36.2.172-230.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hirata H., Altendorf K., Harold F. M. Energy coupling in membrane vesicles of Escherichia coli. I. Accumulation of metabolites in response to an electrical potential. J Biol Chem. 1974 May 10;249(9):2939–2945. [PubMed] [Google Scholar]
  14. Hong J. S., Hunt A. G., Masters P. S., Lieberman M. A. Requirements of acetyl phosphate for the binding protein-dependent transport systems in Escherichia coli. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1213–1217. doi: 10.1073/pnas.76.3.1213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. IZAKI K., ARIMA K. EFFECT OF VARIOUS CONDITIONS ON ACCUMULATION OF OXYTETRACYCLINE IN ESCHERICHIA COLI. J Bacteriol. 1965 May;89:1335–1339. doi: 10.1128/jb.89.5.1335-1339.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kaback H. R., Barnes E. M., Jr Mechanisms of active transport in isolated membrane vesicles. II. The mechanism of energy coupling between D-lactic dehydrogenase and beta-galactoside transport in membrane preparations from Escherichia coli. J Biol Chem. 1971 Sep 10;246(17):5523–5531. [PubMed] [Google Scholar]
  17. Kaback H. R. Transport in isolated bacterial membrane vesicles. Methods Enzymol. 1974;31:698–709. doi: 10.1016/0076-6879(74)31075-0. [DOI] [PubMed] [Google Scholar]
  18. Konings W. N., Barnes E. M., Jr, Kaback H. R. Mechanisms of active transport in isolated membrane vesicles. 2. The coupling of reduced phenazine methosulfate to the concentrative uptake of beta-galactosides and amino acids. J Biol Chem. 1971 Oct 10;246(19):5857–5861. [PubMed] [Google Scholar]
  19. Konings W. N., Freese E. Amino acid transport in membrane vesicles of Bacillus subtilis. J Biol Chem. 1972 Apr 25;247(8):2408–2418. [PubMed] [Google Scholar]
  20. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  21. Lombardi F. J., Kaback H. R. Mechanisms of active transport in isolated bacterial membrane vesicles. 8. The transport of amino acids by membranes prepared from Escherichia coli. J Biol Chem. 1972 Dec 25;247(24):7844–7857. [PubMed] [Google Scholar]
  22. McMurry L., Levy S. B. Two transport systems for tetracycline in sensitive Escherichia coli: critical role for an initial rapid uptake system insensitive to energy inhibitors. Antimicrob Agents Chemother. 1978 Aug;14(2):201–209. doi: 10.1128/aac.14.2.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. McMurry L., Petrucci R. E., Jr, Levy S. B. Active efflux of tetracycline encoded by four genetically different tetracycline resistance determinants in Escherichia coli. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3974–3977. doi: 10.1073/pnas.77.7.3974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Newman E. C., Frank C. W. Circular dichroism spectra of tetracycline complexes with Mg+2 and Ca+2. J Pharm Sci. 1976 Dec;65(12):1728–1732. doi: 10.1002/jps.2600651209. [DOI] [PubMed] [Google Scholar]
  25. Nikaido H. Outer membrane of Salmonella typhimurium. Transmembrane diffusion of some hydrophobic substances. Biochim Biophys Acta. 1976 Apr 16;433(1):118–132. doi: 10.1016/0005-2736(76)90182-6. [DOI] [PubMed] [Google Scholar]
  26. Reynard A. M., Nellis L. F. Uptake of tetracycline by Escherichia coli: lack of binding of tetracycline to the uptake system. Biochem Biophys Res Commun. 1972 Sep 5;48(5):1129–1132. doi: 10.1016/0006-291x(72)90827-3. [DOI] [PubMed] [Google Scholar]
  27. Rottenberg H. The measurement of membrane potential and deltapH in cells, organelles, and vesicles. Methods Enzymol. 1979;55:547–569. doi: 10.1016/0076-6879(79)55066-6. [DOI] [PubMed] [Google Scholar]
  28. Samra Z., Krausz-Steinmetz J., Sompolinsky D. Transport of tetracyclines through the bacterial cell membrane assayed by fluorescence: a study with susceptible and resistant strains of Staphylococcus aureus and Escherichia coli. Microbios. 1978;21(83):7–21. [PubMed] [Google Scholar]
  29. Sarkar S., Thach R. E. Inhibition of formylmethionyl-transfer RNA binding to ribosomes by tetracycline. Proc Natl Acad Sci U S A. 1968 Aug;60(4):1479–1486. doi: 10.1073/pnas.60.4.1479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sompolinsky D., Krausz J. Action of 12 tetracyclines on susceptible and resistant strains of Staphylococcus aureus. Antimicrob Agents Chemother. 1973 Sep;4(3):237–247. doi: 10.1128/aac.4.3.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sompolinsky D., Samra Z. Influence of magnesium and manganese on some biological and physical properties of tetracycline. J Bacteriol. 1972 May;110(2):468–476. doi: 10.1128/jb.110.2.468-476.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Weckesser J., Magnuson J. A. Light-induced tetracycline accumulation by Rhodopseudomonas sphaeroides. J Supramol Struct. 1976;4(4):515–520. doi: 10.1002/jss.400040411. [DOI] [PubMed] [Google Scholar]
  33. Winkler H. H., Wilson T. H. The role of energy coupling in the transport of beta-galactosides by Escherichia coli. J Biol Chem. 1966 May 25;241(10):2200–2211. [PubMed] [Google Scholar]

Articles from Antimicrobial Agents and Chemotherapy are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES