Home LiteratureArticle Details
PMID: 2019557 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Tobramycin uptake in Escherichia coli is driven by either electrical potential or ATP.

Journal of bacteriology ·Vol. 173 ·No. 9 ·1991-05-00 ·Pages 2800-8

Fraimow HS, Greenman JB, Leviton IM, Dougherty TJ, Miller MH

Abstract

Aminoglycoside antibiotics such as streptomycin and tobramycin must traverse the bacterial cytoplasmic membrane prior to initiating lethal effects. Previous data on Escherichia coli, Staphylococcus aureus, and Bacillus subtilis have demonstrated that transport of aminoglycosides is regulated by delta psi, the electrical component of the proton motive force. However, several laboratories have observed that growth of bacterial cells can occur in the apparent absence of delta psi, and we wished to confirm these studies with E. coli and further investigate whether transport of aminoglycosides could occur in the absence of a membrane potential. Treatment of acrA strain CL2 with the protonophore carbonyl cyanide m-chlorophenylhydrazone (CCCP) dissipated delta psi, decreased intracellular ATP levels, and resulted in cessation of growth; after a variable period of time (3 to 7 h), growth resumed, ultimately achieving growth rates comparable to those of untreated cells. Absence of delta psi in these cells was confirmed by absence of [3H]tetraphenyl phosphonium+ uptake as measured by membrane filtration, lack of flagellar motion, and inability of these cells to transport proline (but not methionine). Regrowth was associated with restoration of normal intracellular ATP as measured by luciferin-luciferase bioluminescence assay. Unlike unacclimatized CL2 cells treated with CCCP, these cells transported [3H]tobramycin similarly to untreated cells; aminoglycoside-induced killing was seen in association with transport. These studies suggest that under certain circumstances aminoglycoside transport can be driven by ATP (or other high-energy activated phosphate donors) alone, in the absence of a measurable delta psi. delta uncBC mutants of CL2 incapable of interconverting delta psi and ATP were treated with CCCP, resulting in dissipation of delta psi but no alteration in ATP content. Despite maintenance of normal ATP, there was no transport of [3H] bramycin, confirming that under normal growth conditions ATP has no role in the transport of aminoglycosides.

MeSH Terms
Adenosine Triphosphate/physiology Arsenates/pharmacology Biological Transport, Active/physiology Carbonyl Cyanide m-Chlorophenyl Hydrazone/pharmacology Cell Division/drug effects Cell Movement Cell Survival/drug effects Escherichia coli/metabolism Membrane Potentials Methionine/metabolism Microscopy, Phase-Contrast Onium Compounds/analysis Organophosphorus Compounds/analysis Proline/metabolism Tobramycin/pharmacokinetics
Chemicals
Arsenates Onium Compounds Organophosphorus Compounds Carbonyl Cyanide m-Chlorophenyl Hydrazone Adenosine Triphosphate Proline Methionine arsenic acid tetraphenylphosphonium Tobramycin
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Fraimow H S
Department of Medicine, Montefiore Hospital and Medical Center, Bronx, New York.
Greenman J B
Leviton I M
Dougherty T J
Miller M H
References (38)
38 references, click to expand
  1. Release of lipopolysaccharide by EDTA treatment of E. coli.
    Biochem Biophys Res Commun. 1965 Nov 22;21(4):290-6 PMID: 4159978
  2. Protein measurement with the Folin phenol reagent.
    J Biol Chem. 1951 Nov;193(1):265-75 PMID: 14907713
  3. Energization of active transport by Escherichia coli.
    J Biol Chem. 1972 Nov 25;247(22):7257-65 PMID: 4264299
  4. Transport across isolated bacterial cytoplasmic membranes.
    Biochim Biophys Acta. 1972 Aug 4;265(3):367-416 PMID: 4581579
  5. Energy coupling for methionine transport in Escherichia coli.
    J Bacteriol. 1975 Sep;123(3):985-91 PMID: 125747
  6. Assay of picomole amounts of ATP, ADP, and AMP using the luciferase enzyme system.
    Anal Biochem. 1975 Nov;69(1):187-206 PMID: 2029
  7. The proton electrochemical gradient in Escherichia coli cells.
    Eur J Biochem. 1976 Apr 1;63(2):533-41 PMID: 4325
  8. Circulation of H+ and K+ across the plasma membrane is not obligatory for bacterial growth.
    Science. 1977 Jul 22;197(4301):372-3 PMID: 69317
  9. Mutants of Bacillus megaterium resistant to uncouplers of oxidative phosphorylation.
    J Biol Chem. 1977 Sep 10;252(17):5936-8 PMID: 408344
  10. The measurement of membrane potential and deltapH in cells, organelles, and vesicles.
    Methods Enzymol. 1979;55:547-69 PMID: 37402
  11. Two mutations which affect the barrier function of the Escherichia coli K-12 outer membrane.
    J Bacteriol. 1979 Sep;139(3):899-910 PMID: 383699
  12. Electrochemical proton gradient in Micrococcus lysodeikticus cells and membrane vesicles.
    J Bacteriol. 1980 May;142(2):651-8 PMID: 7380805
  13. Quantitative measurements of membrane potential in Escherichia coli.
    Biochemistry. 1980 Jul 22;19(15):3585-90 PMID: 6996707
  14. Proton chemical potential, proton electrical potential and bacterial motility.
    J Mol Biol. 1980 Apr 15;138(3):599-614 PMID: 6774100
  15. Gentamicin uptake in wild-type and aminoglycoside-resistant small-colony mutants of Staphylococcus aureus.
    Antimicrob Agents Chemother. 1980 Nov;18(5):722-9 PMID: 7447428
  16. Proton motive force in growing Streptococcus lactis and Staphylococcus aureus cells under aerobic and anaerobic conditions.
    J Bacteriol. 1981 Apr;146(1):369-76 PMID: 6260743
  17. Effects of aerobiosis and nitrogen source on the proton motive force in growing Escherichia coli and Klebsiella pneumoniae cells.
    J Bacteriol. 1981 Apr;146(1):377-84 PMID: 6260744
  18. Use of lipophilic cation-permeable mutants for measurement of transmembrane electrical potential in metabolizing cells of Escherichia coli.
    J Bacteriol. 1981 Nov;148(2):399-405 PMID: 6795176
  19. Role of the membrane potential in bacterial resistance to aminoglycoside antibiotics.
    Antimicrob Agents Chemother. 1981 Dec;20(6):803-8 PMID: 6173015
  20. Membrane potential and gentamicin uptake in Staphylococcus aureus.
    Proc Natl Acad Sci U S A. 1982 Nov;79(21):6693-7 PMID: 6959147
  21. Membrane potential in anaerobically growing Staphylococcus aureus and its relationship to gentamicin uptake.
    Antimicrob Agents Chemother. 1983 Apr;23(4):526-30 PMID: 6859831
  22. Roles of ribosomal binding, membrane potential, and electron transport in bacterial uptake of streptomycin and gentamicin.
    Antimicrob Agents Chemother. 1983 Jun;23(6):835-45 PMID: 6351731
  23. Quantitative association between electrical potential across the cytoplasmic membrane and early gentamicin uptake and killing in Staphylococcus aureus.
    J Bacteriol. 1984 Mar;157(3):863-7 PMID: 6698939
  24. The requirement for energy during export of beta-lactamase in Escherichia coli is fulfilled by the total protonmotive force.
    EMBO J. 1984 Apr;3(4):895-900 PMID: 6327294
  25. Effect of growth rate on streptomycin accumulation by Escherichia coli and Bacillus megaterium.
    J Gen Microbiol. 1984 Aug;130(8):2015-22 PMID: 6432955
  26. Proline uptake through the major transport system of Salmonella typhimurium is coupled to sodium ions.
    J Bacteriol. 1984 Oct;160(1):22-7 PMID: 6090414
  27. Proton motive force is not obligatory for growth of Escherichia coli.
    J Bacteriol. 1984 Dec;160(3):1074-7 PMID: 6389506
  28. ATP is essential for protein translocation into Escherichia coli membrane vesicles.
    Proc Natl Acad Sci U S A. 1985 Jul;82(13):4384-8 PMID: 2861605
  29. Respiration rate, growth rate and the accumulation of streptomycin in Escherichia coli.
    J Gen Microbiol. 1985 Oct;131(10):2573-9 PMID: 3906027
  30. Accumulation of gentamicin by Staphylococcus aureus: the role of the transmembrane electrical potential.
    J Antimicrob Chemother. 1986 Jan;17(1):37-44 PMID: 3949638
  31. Effects of nucleotides on ATP-dependent protein translocation into Escherichia coli membrane vesicles.
    J Bacteriol. 1986 Nov;168(2):828-32 PMID: 3536863
  32. Isolation and characterization of uncoupler-resistant mutants of Bacillus subtilis.
    J Bacteriol. 1987 Oct;169(10):4469-78 PMID: 2820927
  33. Mechanism of bactericidal action of aminoglycosides.
    Microbiol Rev. 1987 Sep;51(3):341-50 PMID: 3312985
  34. Bioenergetics of dihydrostreptomycin transport by Escherichia coli.
    FEBS Lett. 1988 Feb 15;228(2):245-8 PMID: 2449366
  35. Bacterial uptake of aminoglycoside antibiotics.
    Microbiol Rev. 1987 Dec;51(4):439-57 PMID: 3325794
  36. Uncoupler-resistant mutants of bacteria.
    Microbiol Rev. 1990 Mar;54(1):52-65 PMID: 2181259
  37. Uncoupler resistance in Escherichia coli: the role of cellular respiration.
    J Gen Microbiol. 1989 Oct;135(10):2577-87 PMID: 2698912
  38. Effects of streptomycin in bacterial cultures growing at different rates; interaction with bacterial ribosomes in vivo.
    Eur J Biochem. 1969 May 1;9(1):42-9 PMID: 4182130
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1991-05-00
Pages
2800-8
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC207860
Subset
IM
Grants
NIAID NIH HHS · 2-T32-AI07183-06 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com