The SMR family: A novel family of multidrug efflux proteins involved with the efflux of lipophilic drugs

Molecular Microbiology

Volumn 19, Issue 6, 1996, Pages 1167-1175

  Paulsen, Ian T ^a,b   Skurray, Ronald A ^a   Tam, Roland ^b   Saier Jr , Milton H ^b   Turner, Raymond J ^c   Weiner, Joel H ^c   Goldberg, Edward B ^d   Grinius, Leonas L ^e  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e PROCTER AND GAMBLE PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLYCOPROTEIN P;

ANTIBIOTIC RESISTANCE; LIPOPHILICITY; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVIEW;

AMINO ACID SEQUENCE; ANTIPORTERS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT, ACTIVE; CARRIER PROTEINS; CONSERVED SEQUENCE; DRUG RESISTANCE, MULTIPLE; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PHYLOGENY; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS);

EID: 0029925159     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.1996.tb02462.x     Document Type: Review

References (64)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Aquilla, H., Link, T., and Klingenberg, M. (1987) Solute carriers involved in energy transfer of mitochondria from a homologous protein family. FEBS Lett 212: 1-9.
3. Arceci, R.J., Croop, J.M., Horwitz, S.B., and Housman, D. (1988) The gene encoding multidrug resistance is induced and expressed at high levels during pregnancy in the secretory epithelium of the uterus. Proc Natl Acad Sci USA 85: 4350-4354.
4. Bairoch, A. (1992) PROSITE: a dictionary of sites and patterns in proteins. Nucl Acids Res 20 (Suppl): S2013-2018.
5. Burton, P.S., Conradi, R.A., Hilgers, A.R., and Ho, N.F.H. (1993) Evidence for a polarized efflux system for peptides in the apical membrane of Caco-2 cells. Biochem Biophys Res Commun 190: 760-766.
6. Cole, S.T. (1987) Nucleotide sequence and comparative analysis of the frd operon encoding the fumarate reductase of Proteus vulgaris: extensive sequence divergence of the membrane anchors and absence of an frd-linked ampC cephalosporinase gene. Eur J Biochem 167: 481-488.
7. Devereux, J., Hasberli, P., and Smithies, O. (1984) A comprehensive set of sequence analysis programmes for the VAX. Nucl Acids Res 12: 387-395.
8. Dinh, T., Paulsen, I.T., and Saier, Jr, M.H. (1994) A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of Gram-negative bacteria. J Bacteriol 176: 3825-3831.
9. Espanol, M.J., and Saier, Jr, M.H. (1995) Topological and segmental phylogenetic analyses of the anion exchanger (band 3) family of transporters. Molec Mem Biol 12: 193-200.
10. Feng, D.-F., and Doolittle, R.F. (1990) Progressive alignment and phylogenetic tree construction of protein sequences. Meth Enzymol 183: 375-387.
11. Flocco, M.M., and Mowbray, S.L. (1994) Planar interactions of arginine and aromatic side-chains in proteins. J Mol Biol 235: 709-717.
12. Fojo, A.T., Ueda, K., Slamon, D.J., Poplac, D.G., Gottesman, M.M., and Pastan, I. (1987) Expression of a multidrug-resistance gene in human tumors and tissues. Proc Natl Acad Sci USA 84: 265-269.
13. Gottesman, M.M., and Pastan, I. (1993) Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 62: 385-427.
14. Greener, T., Govezensky, D., and Zamir, A. (1993) A novel multicopy suppressor of groEL mutation includes two nested open reading frames transcribed from different promoters. EMBO J 12: 889-896.
15. Griffith, J.K., Baker, M.E., Rouch, D.A., Page, M.G.P., Skurray, R.A., Paulsen, I.T., Chater, K.F., Baldwin, S.A., and Henderson, P.J.F. (1992) Membrane transport proteins: implications of sequence comparisons. Curr Opin Cell Biol 4: 684-695.
16. Grinius, L., Dreguniene, G., Goldberg, E.B., Liao, C.H., and Projan, S.J. (1992) A staphylococcal multidrug resistance gene product is a member of a new protein family. Plasmid 27: 119-129.
17. Grinius, L.L., and Goldberg, E.B. (1994) Bacterial multidrug resistance is due to a single membrane protein which functions as a drug pump. J Biol Chem 269: 29998-30004.
18. Hagman, K.E., Pan, W., Spratt, B.G., Balthazar, J.T., Judd, R.C., and Shafer, W.M. (1995) Resistance of Neisseria gonorrhoeae to antimicrobial hydrophobic agents is modulated by the mtrCDE efflux system. Microbiology 141: 611-622.
19. Harte, R.A., and Rupley, J.A. (1968) Three dimensional pictures of molecular models - lysozyme. J Biol Chem 243: 1663-1669.
20. von Heijne, G. (1992) Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225: 487-494.
21. Higgins, C.F. (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8: 67-113.
22. Kagan, B.L., Ganz, T., and Lehrer, R.I. (1994) Defensins: a family of antimicrobial and cytotoxic peptides. Toxicology 87: 131-149.
23. Kandror, O., Busconi, L., Sherman, M., and Goldberg, A. (1994) Rapid degradation of abnormal protein in Escherichia coli involves chaperones GroEL and GroES. J Biol Chem 269: 23575-23582.
24. Kuan, J., and Saier, Jr, M.H. (1994) Phylogenetic relationships among bacteriorhodopsins. Res Microbiol 145: 273-285.
25. Leelaporn, A., Paulsen, I.T., Tennent, J.M., Littlejohn, T.G., and Skurray, R.A. (1994) Multidrug resistance to antiseptics and disinfectants in coagulase-negative staphylococci. J Med Microbiol 40: 214-220.
26. Lewis, K. (1994) Multidrug resistance pumps in bacteria: variations on a theme. Trends Biochem Sci 19: 119-123.
27. Littlejohn, T.G., DiBerardino, D., Messerotti, L.J., Spiers, S.J., and Skurray, R.A. (1991) Structure and evolution of a family of genes encoding antiseptic and disinfectant resistance in Staphylococcus aureus. Gene 101: 59-66.
28. Littlejohn, T.G., Paulsen, I.T., Gillespie, M.T., Tennent, J.M., Midgley, M., Jones, I.G., Purewal, A.S., and Skurray, R.A. (1992) Substrate specificity and energetics of antiseptic and disinfectant resistance in Staphylococcus aureus. FEMS Microbiol Lett 95: 259-266.
29. Loe, D.W., and Sharom, F.J. (1994) Interaction of multidrug-resistant Chinese hamster ovary cells with the peptide ionophore gramicidin D. Biochim Biophys Acta 1190: 72-84.
30. Lomovskaya, O., and Lewis, K. (1992) emr, an Escherichia coli locus for multidrug resistance. Proc Natl Acad Sci USA 89: 8938-8942.
31. Lyon, B.R., and Skurray, R.A. (1987) Antimicrobial resistance of Staphylococcus aureus: genetic basis. Microbiol Rev 51: 88-134.
32. Ma, D., Cook, D.N., Alberti, M., Pon, N.G., Nikaido, H., and Hearst, J.E. (1993) Molecular cloning and characterization of acrA and acrE genes of Escherichia coli. J Bacteriol 175: 6299-6313.
33. Ma, D., Cook, D.N., Alberti, M., Pon, N.G., Nikaido, H., and Hearst, J.E. (1995) Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli. Mol Microbiol 16: 45-55.
34. Maloney, P.C. (1994) Bacterial transporters. Curr Opin Cell Biol 6: 571-582.
35. Marger, M.D., and Saier, Jr, M.H. (1993) A major superfamily of transmembrane facilitators catalyzing uniport, symport and antiport. Trends Biochem Sci 18: 13-20.
36. Midgley, M. (1986) The phosphonium ion efflux system of Escherichia coli: relationship to the ethidium efflux system and energetic studies. J Gen Microbiol 132: 3187-3193.
37. Morimyo, M., Hongo, E., Hama-Inaba, H., and Machida, I. (1992) Cloning and characterization of the mvrC gene of Escherichia coli K-12 which confers resistance against methyl viologen toxicity. Nucl Acids Res 20: 3159-3165.
38. Neyfakh, A.A., Bidnenko, V.E., and Chen, L.B. (1991) Efflux-mediated multidrug resistance in Bacillus subtilis: similarities and dissimilarities with mammalian system. Proc Natl Acad Sci USA 88: 4781-4785.
39. Nies, D.H. (1995) The cobalt, zinc and cadmium efflux system CzcABC from Alcaligenes eutrophus functions as a cation-proton antiporter in Escherichia coli. J Bacteriol 177: 2707-2712.
40. Nikaido, H. (1994) Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264: 382-388.
41. Paulsen, I.T., and Skurray, R.A. (1993) Topology, structure and evolution of two families of proteins involved in antibiotic and antiseptic resistance in eukaryotes and prokaryotes - an analysis. Gene 124: 1-11.
42. Paulsen, I.T., Littlejohn, T.G., Rådström, P., Sundström, L., Sköld, O., Swedberg, G., and Skurray, R.A. (1993) The 3′ conserved segment of integrons contains a gene associated with multidrug resistance to antiseptics and disinfectants. Antimicrob Ag Chemother 37: 761-768.
43. Paulsen, I.T., Brown, M.H., Dunstan, S.J., and Skurray, R.A. (1995) Molecular characterisation of the staphylococcal multidrug resistance export protein QacC. J Bacteriol 177: 2827-2833.
44. Pawagi, A.B., Wang, J., Silverman, M., Reithmeier, R.A.F., and Deber, M.C. (1994) Transmembrane aromatic amino acid distribution in P-glycoprotein. A functional role in broad substrate specificity. J Mol Biol 235: 554-564.
45. Pearson, W.R., and Lipman, D.J. (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85: 2444-2448.
46. Poole, K., Krebes, K., McNally, C., and Neshat, S. (1993) Multiple antibiotic resistance in Pseudomonas aeruginosa: evidence for involvement of an efflux operon. J Bacteriol 175: 7363-7372.
47. Preston, G.M., Jung, J.S., Guggino, W.B., and Agre, P. (1994) Membrane topology of aquaporin CHIP. Analysis of functional epitope-scanning mutants by vectorial proteolysis. J Biol Chem 269: 1668-1673.
48. Purewal, A.S. (1991) Nucleotide sequence of the ethidium efflux gene from Escherichia coli. FEMS Microbiol Lett 82: 229-232.
49. Reizer, J., Reizer, A., and Saier, Jr, M.H. (1992) A new subfamily of bacterial ABC-type transport systems catalyzing export of drugs and carbohydrates. Prot Sci 1: 1326-1332.
50. Rouch, D.A., Cram, D.S., DiBernardino, D., Littlejohn, T.G., and Skurray, R.A. (1990) Efflux-mediated antiseptic resistance gene qacA from Staphylococcus aureus: common ancestry with tetracycline- and sugar-transport proteins. Mol Microbiol 4: 2051-2062.
51. Saier, Jr. M.H. (1994) Computer-aided analyses of transport protein sequences: gleaning evidence concerning function, structure, biogenesis, and evolution. Microbiol Rev 58: 71-93.
52. Saier, Jr. M.H., Tam, R., Reizer, A., and Reizer, J. (1994) Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Mol Microbiol 11: 841-847.
53. Sarkadi, B., Muller, M., Homolya, L., Hollo, Z., Seprodi, J., Germann, U.A., Gottesman, M.M., Price, E.M., and Boucher, R.C. (1994) Interaction of bioactive hydrophobic peptides with the human multidrug transporter. FASEB J 8: 766-770.
54. Sasatsu, M., Shima, K., Shibata, Y., and Kono, M. (1989) Nucleotide sequence of a gene that encodes resistance to ethidium bromide from a transferable plasmid in Staphylococcus aureus. Nucl Acids Res 17: 10103.
55. Sharma, R.C., Inoue, S., Roitelman, J., Schimke, R.T., and Simoni, R.D. (1992) Peptide transport by the multidrug resistance pump. J Biol Chem 267: 5731-5734.
56. Stokes, H.W., and Hall, R.M. (1989) A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: integrons. Mol Microbiol 3: 1669-1683.
57. Sundström, L., Rådström, P., Swedberg, G., and Sköld, O. (1988) Site-specific recombination promotes linkage between trimethoprim- and sulfonamide resistance genes. Sequence characterization of dhfrV and sull and a recombination active locus of Tn21. Mol Gen Genet 213: 191-201.
58. Tam, R., and Saier, Jr, M.H. (1993) Structural, functional and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 57: 320-346.
59. Taylor, D.E., Hou, Y., Turner, R.J., and Weiner, J.H. (1994) Location of a potassium tellurite resistance operon (tehA tehB) within the terminus of Escherichia coli K-12. J Bacteriol 176: 2740-2742.
60. Tennent, J.M., Lyon, B.R., Midgley, M., Jones, I.G., Purewal, A.S., and Skurray, R.A. (1989) Physical and biochemical characterization of the qacA gene encoding antiseptic and disinfectant resistance in Staphylococcus aureus. J Gen Microbiol 135: 1-10.
61. Toppmeyer, D.L., Slapak, C.A., Croop, J., and Kufe, D.W. (1994) Role of P-glycoprotein in dolastatin 10 resistance. Biochem Pharmacol 48: 609-612.
62. Traxler, B., Boyd, D., and Beckwith, J. (1993) The topological analysis of integral cytoplasmic membrane proteins. J Membr Biol 132: 1-11.
63. Walter, E.G., Weiner, J.H., and Taylor, D.E. (1991) Nucleotide sequence and overexpression of the tellurite-resistance determinant from the IncHII plasmid pHH1508a. Gene 101: 1-7.
64. + and is soluble in organic solvents. J Biol Chem 270: 6856-6863.