Abstract
Heavy metal ions are ubiquitous and have beneficial and deleterious actions at the same time.1,2 For this reason cells frequently have inwardly directed transport systems for their uptake and utilization and outwardly directed systems for extrusion and protection. Salts of arsenic were the first chemotherapeutic agents used in treatment of infectious diseases;3 indeed, Paul Ehrlich was awarded the 1908 Nobel Prize in Medicine for the development of the antimicrobial arsenical salvarsan, the “magic bullet” that cured syphilis. In his Nobel Award address Ehrlich pointed out that to be effective and arsenical had be taken up into the cells by an arsenical receptor. He also noted that, soon after the start of drug therapy, arsenical resistant organisms appeared, and he postulated that these organisms were resistant because they could no longer take up the toxic arsenical. Our studies in the 1990s expand on Ehrlich’s ideas.
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References
Foye WO. Antimicrobial activities of mineral elements. In: Weinberg ED, ed. Microorganisms and Minerals. Microbiology Series, Vol 3. New York: Marcel Dekker; 1977:387.
Knowles FC, Benson AA. The biochemistry of arsenic. Trends Biochem Sei 1983; 8:178–80.
Himmelweit F, ed. On the partial function of the cell. In: Collected Papers of Paul Ehrlich. London: Pergammon Press; 1960:183–194.
Foster TJ. Plasmid-determined resistance to antimicrobial drugs and toxic metal ions in bacteria. Microbiol Rev 1983; 47:361–409.
Tisa LS, Rosen BP. Plasmid-encoded transport mechanisms. J Bioenerg Biomembr 1990; 22:493–507.
McMurry L, Petrucci RE Jr, Levy SB. Active efflux of tetracycline encoded by four genetically different tetracycline resistance determinants in Escherichia coli. Proc Natl Acad Sei USA 1980; 77:3974–3977.
Nucifora G, Chu L, Misra T, Silver S. Cadmium resistance from Staphylococcus aureus plasmid pI258 cadA gene results from a cadmium efflux ATPase. Proc Natl Acad Sei USA 1989; 86:3544–3548.
Kaur P, Rosen BP. Plasmid-encoded resistance to arsenic and antimony. Plasmid 1992; 27:29–40.
Novick RP, Roth C. Plasmid-linked resistance to inorganic salts in Staphylococcus aureus. J Bacteriol 1968; 95:1335–1342.
Hedges RW, Baumberg S. Resistance to arsenic compounds conferred by a plasmid transmissible between strains of Escherichia coli. J Bacteriol 1973; 115:459–460.
Silver S, Budd K, Leahy KM, Shaw WV, Hammond D, Novick RP, Willsky GR, Malamy MH, Rosenberg H. Inducible plasmid-determined resistance to arsenate, arsenite and antimony (III) in Escherichia coli and Staphylococcus aureus. J Bacteriol 1981; 146:983–969.
Mobley HLT, Rosen BP. Energetics of plasmid-mediated arsenate resistance in Escherichia coli. Proc Natl Acad Sei USA 1982; 79:6119–6122.
Silver S, Keach D. Energy-dependent arsenate efflux: The mechanism of plasmid mediated resistance. Proc Natl Acad Sei USA 1982; 79:6114–6118.
Mobley HLT, Chen CM, Silver S, Rosen BP. Cloning and expression of R-factor mediated arsenate resistance in Escherichia coli. Mol Gen Genet 1983; 191:421–426.
Rosen BP, Borbolla MG. A plasmid-encoded arsenite pump produces arsenite resistance in Escherichia coli. Biochem Biophys Res Commun 1984; 124:760–765.
Chen CM, Misra T, Silver S, Rosen BP. Nucleotide sequence of the structural genes for an anion pump: The plasmid-encoded arsenical resistance Operon. J Biol Chem 1986; 261:15030–15038.
Ji G, Silver S. Regulation and expression of the arsenic resistance Operon from Staphylococcus aureus plasmid pI258. J Bacteriol 1992; 174:3684–3694.
Rosenstein R, Peschel P, Wieland B, Götz F. Expression and regulation of the Staphylococcus xylosus antimonite, arsenite and arsenate resistance Operon. J Bacteriol 1992; 174:3676–3683.
Chen CM, Mobley HLT, Rosen BP. Separate resistances to arsenate and arsenite (antimonate) encoded by the arsenical resistance operon of R-factor R773. J Bacteriol 1985; 161:758–763.
Walker JE, Saraste M, Runswick MJ, Gay NJ. Distantly related sequences in the a- and ß-subunits of the ATP synthase, myosin kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1982; 1:945–951.
Pedersen PL, Carafoli E. Ion motive ATPases. I. Ubiquity, properties, and significance to cell function. Trends Biochem Sei 1987; 12:146–150.
Rosen BP, Weigel U, Karkaria C, Gangola P. Molecular characterization of an anion pump. The Ars A gene product is an arsenite (antimonate) stimulated ATPase. J Biol Chem 1988; 263:3067–3070.
Tisa LS, Rosen BP. Molecular characterization of an anion pump: The ArsB protein is the membrane anchor for the Ars A protein. J Biol Chem 1990; 265:190–194.
Hsu CM, Rosen BP. Characterization of the catalytic subunit of an anion pump. J Biol Chem 1989; 264:17349–17354.
Hsu CM, Rosen BP. Structure of the plasmid-encoded anion translocating ATPase. In: Kotyk A, Skoda J, Paces V, Kostka V, eds. Highlights of Modern Biochemistry. Zeist: VSP International Science Publishers; 1989:743–751.
Karkaria CE, Chen CM, Rosen BP. Mutagenesis of a nucleotide binding site of an anion-translocating ATPase. J Biol Chem 1990; 265:7832–7836.
Karkaria CE, Rosen BP. Trinitrophenyl-ATP binding to the wild type and mutant ArsA proteins. Arch Biochem Biophys 1991; 288:107–111.
Hsu CM, Kaur P, Karkaria CE, Steiner RF, Rosen BP. Substrate-induced dimerization of the ArsA protein, the catalytic component of an anion-translocating ATPase. J Biol Chem 1991; 266:2327–2332.
San Francisco MJD, Tisa LS, Rosen BP. Identification of the membrane component of the anion pump encoded by the arsenical resistance operon of R-factor R773. Mol Microbiol 1989; 3:15–21.
Wu J, Tisa LS, Rosen BP. Membrane topology of the ArsB protein, the membrane subunit of an anion-translocating ATPase. J Biol Chem 1992; 267:12570–12576.
Boyd D, Manoil C, Beckwith J. Determinants of membrane protein topology. Proc Natl Acad Sei USA 1987; 84:8525–8529.
Casadaban MJ, Martinez-Arias A, Shapiro SK, Chou J. ß-Galactosidase gene fusions for analyzing gene expression in Escherichia coli and yeast. Meth Enzymol 1983; 100:293–307.
Broome-Smith JK, Spratt BG. A vector for the construction of translational fusions to TEM ß-lactamase and the analysis of protein export signals and membrane protein topology. Gene 1986; 49:341–349.
Cohen GN, Monod J. Bacterial permeases. Bacteriol Rev 1957; 21:169–194.
Rosen BP, Weigel U, Monticello RA, Edwards BPF. Molecular analysis of an anion pump: Purification of the ArsC protein. Arch Biochem Biophys 1991; 284:381–385.
Joerger RD, Bishop PE. Nucleotide sequence and genetic analysis of the nifB-nifQ region from Azotobacter vinelandii. J Bacteriol 1988; 170:1475–1487.
Alloing G, Trombe M-C, Claverys J-P. The amiB locus of the Gram-positive bacterium Streptococcus pneumoniae is similar to binding protein-dependent transport Operons of Gram-negative bacteria. Mol Microbiol 1990; 4:633–644.
Behrmann I, Hillemann D, Puehler A, Strauch E, Wohlleben W. Overexpression of a Streptomyces viridochromogenes gene (glnll) encoding a glutamine synthetase similar to those of eucaryotes confers resistance against the antibiotic phosphinothricyl-alanyl-alanine. J Bacteriol 1990; 172:5326–5334.
Futai M, Kanazawa H. Structure and function of proton-translocating ATPase (FoFx): Biochemical and molecular biological approaches. Microbiol Rev 1983; 47:285–313.
Rosen BP, Kashket ER. Energetics of active transport. In: Rosen BP, ed. Bacterial Transport. New York: Marcel Dekker; 1978:559–620.
Endicott JA, Ling V. The biochemistry of P-glycoprotein-mediated multidrug resistance. Annu Rev Biochem 1989; 58:136–171.
Ouelette M, Fase-Fowler F, Borst P. The amplified H circle of methotrexate-resistant Leishmania tarentolae contains a novel P-glycoprotein gene. EMBO J 1990; 9:1027–1033.
Callahan HL, Beverly SM. Heavy metal resistance: A new role for P-glycoproteins in Leishmania. J Biol Chem 1991; 266:18427–18430.
Rosteck PR, Reynolds PA, Hershberger CL. Homology between proteins controlling Streptomyces fradiae tylosin resistance and ATP-binding transport. Gene 1991; 102:27–32.
Guilfoile PG, Hutchinson CR. A bacterial analog of the mdr gene of mammalian tumor cells is present in Streptomyces peucetius, the producer of daunorubicin and doxorubicin. Proc Natl Acad Sei USA 1991; 88:8553–8557.
Smith K, Novick RP. Genetic studies on plasmid-linked cadmium resistance in Staphylococcus aureus. J Bacteriol 1972; 112:761–727.
Perry RD, Silver S. Cadmium and manganese transport in Staphylococcus aureus membrane vesicles. J Bacteriol 1982; 150:973–976.
Witte W, Green L, Misra TK, Silver S. Resistance to mercury and to cadmium in chromosomally resistant Staphylococcus aureus. Antimicro Agents Chemother 1986; 29:663–669.
Chopra I. Decreased uptake of cadmium by a resistant strain of Staphylococcus aureus. J Gen Microbiol 1970; 63:265–267.
Tynecka Z, Zajac J, Gos Z. Plasmid dependent impermeability barrier to cadmium ions in Staphylococcus aureus. Acta Microbiol Pol 1975; 7:11–20.
Chopra I. Mechanism of plasmid-mediated resistance to cadmium in Staphylococcus aureus. Antimicro Agents Chemother 1975; 7:8–14.
Weiss AA, Silver S, Kinscherf TG. Cation transport alteration associated with plasmid-determined resistance to cadmium in Staphylococcus aureus. Antimicro Agents Chemother 1978; 14:856–865.
Tynecka Z, Gos Z, Zajac J. Reduced cadmium transport determined by a resistance plasmid in Staphylococcus aureus. J Bacteriol 1981; 147:305–312.
Tynecka Z, Gos Z, Zajac J. Energy-dependent efflux of cadmium coded by a plasmid resistance determinant in Staphylococcus aureus. J Bacteriol 1981; 147:313–319.
Silver S, Nucifora G, Chu L, Misra T. Bacterial resistance ATPases: Primary pumps for exporting toxic cations and anions. Trends Biochem Sei 1989; 14:76–80.
Silver S, Walderhaug M. Gene regulation of plasmid and chromosomal-determined inorganic ion transport in bacteria. Microbiol Rev 1992; 56:195–228.
Walderhaug MO, Post RL, Saccomani G, Leonard RT, Briskin DP. Structural relatedness of three ion-transport adenosine triphosphatases around their active sites of phosphorylation. J Biol Chem 1985; 260:3852–3859.
Serrano R, Portillo F. Catalytic and regulatory sites of yeast plasma membrane H+-ATPase studied by directed mutagenesis. Biochim Biophys Acta 1990; 1018:195–199.
Snavely MD, Miller CG, Maguire ME. The mgtB Mg2+ transport locus of Salmonella typhimurium encodes a P-type ATPase. J Biol Chem 1991; 266:815–823.
Solioz M, Mathews S, Fürst P. Cloning of the K+-ATPase of Streptococcus faecalis. J Biol Chem 1987; 262:7358–7362.
Hesse JE, Wieczorek L, Altendorf K, Reicin AS, Dorus E, Epstein W. Sequence homology between two membrane transport ATPases, the Kdp-ATPase of Escherichia coli and the Ca2+-ATPase of sarcoplasmic reticulum. Proc Natl Acad Sei USA 1984; 81:4746–4750.
Yoon KP, Silver S. A second gene in the Staphylococcus aureus cad A cadmium resistance determinant of plasmid pI258. J Bacteriol 1991; 173:7636–7642.
Tynecka Z, Skwarek T, Malm A. Anaerobic 109Cd accumulation by cadmium-resistant and -sensitive Staphylococcus aureus. FEMS Microbiol Letts 1990; 69:159–164.
Tsai K-J, Yoon KP, Lynn AR. ATP-dependent cadmium transport by the cadA cadmium resistance determinant in everted membrane vesicles of Bacillus subtilis. J Bacteriol 1992; 174:116–121.
Bowman EJ, Siebers A, Altendorf K. Bafilomycins: A class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sei USA 1988; 85:7972–7976.
Yoon KP, Misra T, Silver S. Regulation of the cadA cadmium resistance determinant of Staphylococcus aureus plasmid pI258. J Bacteriol 1991; 173:7643–7649.
Novick RP, Murphy E, Gryczan TJ, Baron E, Edelman I. Penicillinase plasmids of Staphylococcus aureus: Restriction-deletion maps. Plasmid 1979; 2:109–129.
Diels L, Faelen M, Mergeay M, Nies D. Mercury transposons from plasmids governing multiple resistance to heavy metals in Alcaligenes eutrophus CH34. Arch Int Physiol Biochim 1985; 93:B27–B28.
Mergeay M, Nies D, Schlegel HG, Gerits J, Charles P, Van Gijsegem F. Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J Bacteriol 1985; 162:328–343.
Nies D, Mergeay M, Friedrich B, Schlegel HG. Cloning of plasmid genes encoding resistance to cadmium, zinc, and cobalt in Alcaligenes eutrophus CH34. J Bacteriol 1987; 169:4865–4868.
Nies DH, Silver S. Plasmid-determined inducible efflux is responsible for resistance to cadmium, zinc, and cobalt in Alcaligenes eutrophus. J Bacteriol 1989; 171:896–900.
Nies DH, Nies A, Chu L, Silver S. Expression and nucleotide sequence of a plasmid-determined divalent cation efflux system from Alcaligenes eutrophus. Proc Natl Acad Sei USA 1989; 86:7351–7355.
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Lynn, A.R., Rosen, B.P. (1994). Transport Systems for Arsenic, Antimony, and Cadmium Ions Encoded by Bacterial Plasmids. In: Foà, P.P., Walsh, M.F. (eds) Ion Channels and Ion Pumps. Endocrinology and Metabolism, vol 6. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-2596-6_25
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DOI: https://doi.org/10.1007/978-1-4612-2596-6_25
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