Inhibition of DNA Replication Initiation by Aminoglycoside Antibiotics

Overview

Journal Antimicrob Agents Chemother

Publisher American Society for Microbiology

Specialty Pharmacology

Date 1986 Sep 1

PMID 2430522

Citations 9

Authors

K Matsunaga

H Yamaki

T Nishimura

N Tanaka

Affiliations

Soon will be listed here.

Abstract

The reinitiation of DNA replication induced by a temperature shift in a dnaC(Ts) mutant of Escherichia coli was markedly inhibited by aminoglycoside antibiotics around the MIC in a short period. Protein synthesis continued for several minutes after the addition of aminoglycosides but was immediately blocked by chloramphenicol, suggesting that the inhibition of initiation of replication by aminoglycosides is not a secondary effect due to the interruption of protein synthesis. Aminoglycosides did not significantly affect RNA synthesis, suggesting that primer RNA synthesis for DNA initiation is not blocked by the agents. The lethal action of habekacin was observed simultaneously with the inhibition of DNA reinitiation. DNA elongation demonstrated with a dnaE(Ts) mutant or toluene-treated cells of a polA mutant was not significantly affected by aminoglycosides. The oriC-membrane complex formation was markedly interrupted by habekacin in the dnaC(Ts) mutant, and the in vitro reconstitution of the oriC-membrane complex was completely blocked by aminoglycosides. The present studies show that aminoglycosides block initiation of DNA replication and suggest that the inhibition is caused by the interruption of oriC-membrane attachment.

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References

Stern J, Barner H, COHEN S . The lethality of streptomycin and the stimulation of RNA synthesis in the absence of protein synthesis. J Mol Biol. 1966; 17(1):188-217. DOI: 10.1016/s0022-2836(66)80103-1. View

Treick R, KONETZKA W . PHYSIOLOGICAL STATE OF ESCHERICHIA COLI AND THE INHIBITION OF DEOXYRIBONUCLEIC ACID SYNTHESIS BY PHENETHYL ALCOHOL. J Bacteriol. 1964; 88:1580-4. PMC: 277455. DOI: 10.1128/jb.88.6.1580-1584.1964. View

Freda C, Nass M, COHEN S . T6r+-induced proteins and nucleic acids in Escherichia coli infected in the presence of streptomycin. J Bacteriol. 1968; 96(4):1382-99. PMC: 252464. DOI: 10.1128/jb.96.4.1382-1399.1968. View

Richardson A, Leach F . The effect of phenethyl alcohol on Bacillus subtilis transformation. I. Characterization of the effect. Biochim Biophys Acta. 1969; 174(1):264-75. DOI: 10.1016/0005-2787(69)90250-0. View

Richardson A, Pierson D, Leach F . The effect of phenethyl alcohol on Bacillus subtilis transformation. II. Transport of DNA and precursors. Biochim Biophys Acta. 1969; 174(1):276-81. DOI: 10.1016/0005-2787(69)90251-2. View

DE LUCIA P, Cairns J . Isolation of an E. coli strain with a mutation affecting DNA polymerase. Nature. 1969; 224(5225):1164-6. DOI: 10.1038/2241164a0. View

Gefter M, Hirota Y, Kornberg T, Wechsler J, Barnoux C . Analysis of DNA polymerases II and 3 in mutants of Escherichia coli thermosensitive for DNA synthesis. Proc Natl Acad Sci U S A. 1971; 68(12):3150-3. PMC: 389610. DOI: 10.1073/pnas.68.12.3150. View

Burger R . Toluene-treated Escherichia coli replicate only that DNA which was about to be replicated in vivo. Proc Natl Acad Sci U S A. 1971; 68(9):2124-6. PMC: 389366. DOI: 10.1073/pnas.68.9.2124. View

Burger R, Glaser D . Effect of nalidixic acid on DNA replication by toluene-treated Escherichia coli. Proc Natl Acad Sci U S A. 1973; 70(7):1955-8. PMC: 433641. DOI: 10.1073/pnas.70.7.1955. View

10.

Olsen W, HEIDRICH H, Hannig K, Hofschneider P . Deoxyribonucleic acid-envelope complexes isolated from Escherichia coli by free-flow electrophoresis: biochemical and electron microscope characterization. J Bacteriol. 1974; 118(2):646-53. PMC: 246800. DOI: 10.1128/jb.118.2.646-653.1974. View

11.

Iida K, Koike M . Cell wall alterations of gram-negative bacteria by aminoglycoside antibiotics. Antimicrob Agents Chemother. 1974; 5(1):95-7. PMC: 428926. DOI: 10.1128/AAC.5.1.95. View

12.

Hanna M, Carl P . Reinitiation of deoxyribonucleic acid synthesis by deoxyribonucleic acid initiation mutants of Escherichia coli: role of ribonucleic acid synthesis, protein synthesis, and cell division. J Bacteriol. 1975; 121(1):219-26. PMC: 285634. DOI: 10.1128/jb.121.1.219-226.1975. View

13.

Ryder O, Smith D . Properties of membrane-associated folded chromosomes of E. coli related to initiation and termination of DNA replication. Cell. 1975; 4(4):337-45. DOI: 10.1016/0092-8674(75)90154-3. View

14.

Bryan L, van den Elzen H . Streptomycin accumulation in susceptible and resistant strains of Escherichia coli and Pseudomonas aeruginosa. Antimicrob Agents Chemother. 1976; 9(6):928-38. PMC: 429653. DOI: 10.1128/AAC.9.6.928. View

15.

Pine M . Comparative physiological effects of incorporated amino acid analogs in Escherichia coli. Antimicrob Agents Chemother. 1978; 13(4):676-85. PMC: 352309. DOI: 10.1128/AAC.13.4.676. View

16.

Nicolaidis A, Holland I . Evidence for the specific association of the chromosomal origin with outer membrane fractions isolated from Escherichia coli. J Bacteriol. 1978; 135(1):178-89. PMC: 224803. DOI: 10.1128/jb.135.1.178-189.1978. View

17.

. In vitro replication of a DNA fragment containing the vicinity of the origin of E. coli DNA replication. Mol Gen Genet. 1979; 169(1):35-40. DOI: 10.1007/BF00267542. View

18.

Nagai K, Hendrickson W, Balakrishnan R, Yamaki H, Boyd D, Schaechter M . Isolation of a replication origin complex from Escherichia coli. Proc Natl Acad Sci U S A. 1980; 77(1):262-6. PMC: 348249. DOI: 10.1073/pnas.77.1.262. View

19.

Choi E, Nishimura T, Tanaka N . Mutational alterations of either large or small ribosomal subunit for the kanamycin resistance. Biochem Biophys Res Commun. 1980; 94(3):755-62. DOI: 10.1016/0006-291x(80)91299-1. View

20.

Hancock R . Aminoglycoside uptake and mode of action--with special reference to streptomycin and gentamicin. I. Antagonists and mutants. J Antimicrob Chemother. 1981; 8(4):249-76. DOI: 10.1093/jac/8.4.249. View