Tetracycline/H+ Antiport and Na+/H+ Antiport Catalyzed by the Bacillus Subtilis TetA(L) Transporter Expressed in Escherichia Coli

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 1995 Aug 1

PMID 7635843

Citations 20

Authors

A A Guffanti

T A Krulwich

Affiliations

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Abstract

The properties of TetA(L)-dependent tetracycline/proton and Na+/proton antiport were studied in energized everted vesicles of Escherichia coli transformed with a cloned tetA(L) gene (pJTA1) from Bacillus subtilis. Inhibition patterns by valinomycin and nigericin indicated that both antiports were electrogenic, in contrast to the tetracycline/proton antiport encoded by gram-negative plasmid tet genes. Tetracycline uptake in the everted system was dependent upon a divalent cation, with cobalt being the preferred one. The apparent Km for tetracycline was markedly increased at pH 8.5 versus pH 7.5, whereas the Vmax was unchanged. The much higher apparent Km for Na+ decreased at pH 8.5 relative to that at pH 7.5, as did the Vmax. Na+ did not affect tetracycline uptake, nor did Co2+ and/or tetracycline affect Na+ uptake; complex patterns of inhibition by amiloride and analogs thereof were observed.

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References

Wilson C, Morgan A . Chromosomal-DNA amplification in Bacillus subtilis. J Bacteriol. 1985; 163(2):445-53. PMC: 219142. DOI: 10.1128/jb.163.2.445-453.1985. View

Yamaguchi A, Ohmori H, Nomura T, Sawai T . Delta pH-dependent accumulation of tetracycline in Escherichia coli. Antimicrob Agents Chemother. 1991; 35(1):53-6. PMC: 244940. DOI: 10.1128/AAC.35.1.53. View

Griffith J, Kogoma T, Corvo D, Anderson W, Kazim A . An N-terminal domain of the tetracycline resistance protein increases susceptibility to aminoglycosides and complements potassium uptake defects in Escherichia coli. J Bacteriol. 1988; 170(2):598-604. PMC: 210696. DOI: 10.1128/jb.170.2.598-604.1988. View

McMurry L, Park B, Burdett V, Levy S . Energy-dependent efflux mediated by class L (tetL) tetracycline resistance determinant from streptococci. Antimicrob Agents Chemother. 1987; 31(10):1648-50. PMC: 175008. DOI: 10.1128/AAC.31.10.1648. View

Kleyman T, Cragoe Jr E . Amiloride and its analogs as tools in the study of ion transport. J Membr Biol. 1988; 105(1):1-21. DOI: 10.1007/BF01871102. View

Ives C, Bott K . Cloned Bacillus subtilis chromosomal DNA mediates tetracycline resistance when present in multiple copies. J Bacteriol. 1989; 171(4):1801-10. PMC: 209825. DOI: 10.1128/jb.171.4.1801-1810.1989. View

Levy S, McMurry L, Burdett V, Courvalin P, Hillen W, Roberts M . Nomenclature for tetracycline resistance determinants. Antimicrob Agents Chemother. 1989; 33(8):1373-4. PMC: 172657. DOI: 10.1128/AAC.33.8.1373. View

Yamaguchi A, Udagawa T, Sawai T . Transport of divalent cations with tetracycline as mediated by the transposon Tn10-encoded tetracycline resistance protein. J Biol Chem. 1990; 265(9):4809-13. View

Salyers A, Speer B, Shoemaker N . New perspectives in tetracycline resistance. Mol Microbiol. 1990; 4(1):151-6. DOI: 10.1111/j.1365-2958.1990.tb02025.x. View

10.

Ives C, Bott K . Characterization of chromosomal DNA amplifications with associated tetracycline resistance in Bacillus subtilis. J Bacteriol. 1990; 172(9):4936-44. PMC: 213148. DOI: 10.1128/jb.172.9.4936-4944.1990. View

11.

Amano H, Ives C, Bott K, Shishido K . A limited number of Bacillus subtilis strains carry a tetracycline-resistance determinant at a site close to the origin of replication. Biochim Biophys Acta. 1991; 1088(2):251-8. DOI: 10.1016/0167-4781(91)90061-p. View

12.

Taglicht D, Padan E, Schuldiner S . Overproduction and purification of a functional Na+/H+ antiporter coded by nhaA (ant) from Escherichia coli. J Biol Chem. 1991; 266(17):11289-94. View

13.

NEYFAKH A, Bidnenko V, Chen L . Efflux-mediated multidrug resistance in Bacillus subtilis: similarities and dissimilarities with the mammalian system. Proc Natl Acad Sci U S A. 1991; 88(11):4781-5. PMC: 51750. DOI: 10.1073/pnas.88.11.4781. View

14.

Levy S . Active efflux mechanisms for antimicrobial resistance. Antimicrob Agents Chemother. 1992; 36(4):695-703. PMC: 189356. DOI: 10.1128/AAC.36.4.695. View

15.

Speer B, Shoemaker N, Salyers A . Bacterial resistance to tetracycline: mechanisms, transfer, and clinical significance. Clin Microbiol Rev. 1992; 5(4):387-99. PMC: 358256. DOI: 10.1128/CMR.5.4.387. View

16.

Pinner E, Kotler Y, Padan E, Schuldiner S . Physiological role of nhaB, a specific Na+/H+ antiporter in Escherichia coli. J Biol Chem. 1993; 268(3):1729-34. View

17.

Nikaido H, Thanassi D . Penetration of lipophilic agents with multiple protonation sites into bacterial cells: tetracyclines and fluoroquinolones as examples. Antimicrob Agents Chemother. 1993; 37(7):1393-9. PMC: 187981. DOI: 10.1128/AAC.37.7.1393. View

18.

Padan E, Schuldiner S . Na+/H+ antiporters, molecular devices that couple the Na+ and H+ circulation in cells. J Bioenerg Biomembr. 1993; 25(6):647-69. DOI: 10.1007/BF00770252. View

19.

Pinner E, Padan E, Schuldiner S . Kinetic properties of NhaB, a Na+/H+ antiporter from Escherichia coli. J Biol Chem. 1994; 269(42):26274-9. View

20.

Kuroda T, Shimamoto T, Inaba K, Tsuda M, Tsuchiya T . Properties and sequence of the NhaA Na+/H+ antiporter of Vibrio parahaemolyticus. J Biochem. 1994; 116(5):1030-8. DOI: 10.1093/oxfordjournals.jbchem.a124624. View