Evolutionary origins of multidrug and drug-specific efflux pumps in bacteria

FASEB Journal

Volumn 12, Issue 3, 1998, Pages 265-274

  Saier Jr , Milton H ^a   Paulsen, Ian T ^a   Sliwinski, Marek K ^a   Pao, Stephanie S ^a   Skurray, Ronald A ^b   Nikaido, Hiroshi ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antibiotics; Antimicrobial agents; Drugs; Evolution; Phylogenetic trees; Resistance; Transport

Indexed keywords

BACTERIAL GENETICS; DRUG TRANSPORT; ESCHERICHIA COLI; EVOLUTION; METHANOBACTERIUM; MULTIDRUG RESISTANCE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; REVIEW;

ANIMALIA; ARCHAEA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; METHANOBACTERIUM; METHANOCALDOCOCCUS JANNASCHII; METHANOCOCCUS; PROKARYOTA;

EID: 2642672835     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.12.03.265     Document Type: Review

References (57)

1. Nikaido, H., and Saier, M. H., Jr. (1992). Transport proteins in bacteria: Common themes in their design. Science 258, 936-942
2. Saier, M. H., Jr. (1994) Computer-aided analyses of transport protein sequences: Gleaning evidence concerning function, structure, biogenesis, and evolution. Microbiol. Rev. 58, 71-93
3. Tam, R., and Saier, M. H., Jr. (1993) Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol. Rev. 57, 320-346
4. Saier, M. H., Jr. (1996) Phylogenetic approaches to the identification and characterization of protein families and superfamilies. Microb. Comp. Genomics 1, 129-150
5. Paulsen, I. T., Sliwinski, M. K., and Saier, M. H., Jr. (1998) Microbial genome analyses: Global comparisons of transport capabilities based on phylogenies, bioenergetics and substrate specificities. J. Mol. Biol. In press
6. Lewis, K. (1994) Multidrug resistance pumps in bacteria: Variations on a theme. Trends Biochem. Sci. 19, 119-123
7. Nikaido, H. (1994) Prevention of drug access to bacterial targets: Permeability barriers and active efflux. Science 264, 382-388
8. Davies, J. (1992) Another look at antibiotic resistance. 1991 Fred Griffith Review Lecture. J. Gen. Microbiol. 138, 1553-1559
9. Parr, T. R., Jr., and Saier, M. H., Jr. (1992) The bacterial phosphotransferase system as a potential vehicle for the entry of novel antibiotics. Res. Microbiol. 143, 443-447
10. Fleischmann, R. D., Adams, M. D., White, O., Clayton, R. A., Kirkness, E. F., Kerlavage, A. R., Bult, C. J., Tomb, J.-F., Dougherty, B. A., Merrick, J. M., McKenney, K., Sutton, G., FitzHugh, W., Fields, C., Gocayne, J. D., Scott, J., Shirley, R., Liu, L.-I., Glodek, A., Kelley, J. M., Weidman, J. F., Phillips, C. A., Spriggs, T., Hedblom, E., Cotton, M. D., Utterback, T. R., Hanna, M. C., Nguyen, D. T., Saudek, D. M., Brandon, R. C., Fine, L. D., Fritchman, J. L., Fuhrmann, J. L., Geoghagen, N. S. M., Gnehm, C. L., McDonald, L. A., Small, K. V., Fraser, C. M., Smith, H. O., and Venter, J. C. (1995) Whole-genome random sequencing and as- sembly of Haemophilus influenzae Rd. Science 269, 496-512
11. Fraser, C. M., Gocayne, J. D., White, O., Adams, M. D., Clayton, R. A., Fleischmann, R. D., Bult, C. J., Kerlavage, A. R., Sutton, G., Kelley, J. M., Fritchman, J. L., Weidman, J. F., Small, K. V., Sandusky, M., Fuhrmann, J., Nguyen, D., Utterback, T. R., Saudek, D. M., Phillips, C. A., Merrick, J. M., Tomb, J.-F., Dougherty, B. A., Bott, K. F., Hu, P.-C., Lucier, T. S., Peterson, S. N., Smith, H. O., Hutchison, C. A., III, and Venter, J. C. (1995) The minimal gene complement of Mycoplasma genitalium. Science 270, 397-403
12. Blattner, F. R., Plunkett, G., III., Bloch, C. A., Perna, N. T., Burland, V., Riley, M., Collado-Vides, J., Glasner, J. D., Rode, C. K., Mayhew, G. F., Gregor, J., Davis, N. W., Kirkpatrick, H. A., Goeden, M. A., Rose, D. J., Mau, B., and Shao, Y. (1997) The complete genome sequence of Escherichia coli K-12. Science 277, 1453-1474
13. Biaudet, V., Samson, F., Anagnostopoulos, C., Ehrlich, S. D., and Bessières, P. (1996) Computerized genetic map of Bacillus subtilis. Microbiology 142, 2669-2729
14. Bult, C. J., White, O., Olsen, G. J., Zhou, L., Fleischmann, R. D., Sutton, G. G., Blake, J. A., FitzGerald, L. M., Clayton, R. A., Go- cayne, J. D., Kerlavage, A. R., Dougherty, B. A., Tomb, J.-F., Adams, M. D., Reich, C. I., Overbeek, R., Kirkness, E. F., Weinstock, K. G., Merrick, J. M., Glodek, A., Scott, J. L., Geoghagen, N. S. M., Weidman, J. F., Fuhrmann, J. L., Nguyen, D., Utterback, T. R., Kelley, J. M., Peterson, J. D., Sadow, P. W., Hanna, M. C., Cotton, M. D., Roberts, K. M., Hurst, M. A., Kaine, B. P., Borodovsky, M., Klenk, H.-P., Fraser, C. M., Smith, H. O., Woese, C. R., and Venter, J. C. (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273, 1058-1073
15. Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y., Miyajima, N., Hirosawa, M., Sugiura, M., Sasamoto, S., Kimura, T., Hosouchi, T., Matsuno, A., Muraki, A., Nakazaki, N., Naruo, K., Okumura, S., Shimpo, S., Takeuchi, C., Wada, T., Watanabe, A., Yamada, M., Yasuda, M., and Tabata, S. (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3, 109-136
16. Higgins, C. F. (1992) ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8, 67-113
17. Griffith, J. K., Baker, M. E., Rouch, D. A., Page, M. G., Skurray, R. A., Paulsen, I. T., Chater, K. F., Baldwin, S. A., and Henderson, P. J. (1992) Membrane transport proteins: Implications of sequence comparisons. Curr. Opin. Cell Biol. 4, 684-695
18. Marger, M. D., and Saier, M. H., Jr. (1993) A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem. Sci. 18, 13-20
19. Paulsen, I. T., Skurray, R. A., Tarn, R., Saier, M. H., Jr., Turner, R. J., Weiner, J. H., Goldberg, E. B., and Grinius, L. L. (1996) The SMR family: A novel family of multidrug efflux proteins involved with the efflux of lipophilic drugs. Mol. Microbiol. 19, 1167-1175
20. Saier, M. H., Jr., Tarn, 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
21. Paulsen, I. T., Brown, M. H., and Skurray, R. A. (1996) Proton-dependent multidrug efflux systems. Microbiol. Rev. 60, 575-608
22. George, A. M. (1996) Multidrug resistance in enteric and other gram-negative bacteria. FEMS Microbiol. Lett. 139, 1-10
23. Dinh, T., Paulsen, I. T., and Saier, M. H., Jr. (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
24. Paulsen, I. T., Park, J. H., Choi, P. S., and Saier, M. H., Jr. (1997) A family of Gram-negative bacterial outer membrane factors that function in the export of proteins, carbohydrates, drugs and heavy metals from Gram-negative bacteria. FEMS Microbiol. Lett. 156, 1-8.
25. Nikaido, H. (1996) Multidrug efflux pumps of gram-negative bacteria. J. Bacterial. 178, 5853-5859
26. Holland, I. B., and Blight, M. A. (1996) Structure and function of HlyB, the ABC-transporter essential for haemolysin secretion from Escherichia coli. In Handbook of Biological Physics (W. N. Konings, H. R. Kaback and J. S. Lolkema, eds) Vol. 2, pp. 111-135, Elsevier, Amsterdam
27. Path, M. J., and Kolter, R. (1993) ABC-transporters: The bacterial exporters. Microbiol. Rev. 57, 995-1017
28. Pigeon, R. P., and Silver, R. P. (1994) Topological and mutational analysis of KpsM, the hydrophobic component of the ABC-transporter involved in the export of polysialic acid in Escherichia coli K1. Mol Microbiol. 14, 871-881
29. Feng, D.-F., and Doolittle, R. F. (1990) Progressive alignment and phylogenetic tree construction of protein sequences. Methods Enzymol. 183, 375-387
30. Paulsen, I. T., Beness, A. M., and Saier, M. H., Jr. (1997) Computer-based analyses of the protein constituents of transport systems catalyzing export of complex carbohydrates in bacteria. Microbiology 143, 2685-2699
31. Saurin, W., and Dassa, E. (1994) Sequence relationships between integral inner membrane proteins of binding protein-dependent transport systems: Evolution by recurrent gene duplications. Prot. Sci. 3, 325-344
32. Reizer, J., Reizer, A., and Saier, M. H., Jr. (1992) A new subfamily of bacterial ABC-type transport systems catalyzing export of drugs and carbohydrates. Prot. Sci. 1, 1326-1332
33. Bolhuis, H., van Veen, H. W., Molenaar, D., Poolman, B., Driessen, A. J. M., and Konings, W. N. (1996) Multidrug resistance in Lactococcus lactis: Evidence for ATP-dependent drug extrusion from the inner leaflet of the cytoplasmic membrane. EMBO J. 15, 4239-4245
34. Gros, P., and Hanna, M. (1996) The P-glycoprotein family and multidrug resistance: An overview. In Handbook of Biological Physics (W. N. Konings, H. R. Kaback, and J. S. Lolkema, eds) Vol. 2, pp. 137-163, Elsevier, Amsterdam
35. van Veen, H. W., Bolhuis, H., Putman, M., and Konings, W. N. (1996) Multidrug resistance in prokaryotes: Molecular mechanism of drug efflux. In Handbook of Biological Physics (W. N. Konings, H. R. Kaback, and J. S. Lolkema, eds) Vol. 2, pp. 165-187, Elsevier, Amsterdam
36. van Veen, H. W., Venema, K., Bolhuis, H., Oussenko, T., Kok, J., Poolman, B., Driessen, A. J. M., and Konings, W. N. (1996) Multidrug resistance mediated by a bacterial homolog of the human multidrug transporter MDR1. Proc. Natl. Acad. Sci. USA 93, 10668-10672
37. Pao, S. S., Paulsen, I. T., and Saier, M. H., Jr. (1998) Major facilitator superfamily. Microbiol. Mol. Biol. Rev. In press
38. Allard, J. D., and Bertrand, K. P. (1992) Membrane topology of the pBR322 tetracycline resistance protein. TetA-PhoA gene fusions and implications for the mechanism of TetA membrane insertion. J. Biol Chem. 267, 17809-17819
39. 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
40. Paulsen, I. T., Brown, M. H., Littlejohn, T. G., Mitchell, B. A., and Skurray, R. A. (1996) Molecular characterization of the mul- tidrug resistance proteins QacA and QacB: Membrane topology and identification of residues involved in specificity for divalent cations. Proc. Natl Acad. Sci. USA 93, 3630-3635
41. Grundemann, D., Gorboulev, V., Gambaryan, S., Veyhl, M., and Koepsell, H. (1994) Drug excretion mediated by a new prototype of polyspecific transporter. Nature (London) 372, 549-552
42. Goffeau, A., Park, J., Paulsen, I. T., Jonniaux, J.-L., Dinh, T., Mordant, P., and Saier, M. H., Jr. (1997) Multidrug-resistant transport proteins in yeast: Complete inventory and phylogenetic characterization of yeast open reading frames within the major facilitator superfamily. Yeast 13, 43-54
43. Schuldiner, S., Lebendiker, M., and Yerushalmi, H. (1997) EmrE, the smallest ion-coupled transporter, provides a unique paradigm for structure-function studies. J. Exp. Biol. 200, 335-341
44. Paulsen, I. T., Brown, M. H., Dunstan, S. J., and Skurray, R. A. (1995) Molecular characterization of the staphylococcal multidrug resistance export protein QacC. J. Bacterial. 177, 2827-2833
45. Arkin, I. T., Russ, W. P., Lebendiker, M., and Schuldiner, S. (1996) Determining the secondary structure and orientation of EmrE, a multi-drug transporter, indicates a transmembrane four-helix bundle. Biochemistry 35, 7233-7238
46. + and is soluble in organic solvents. J. Biol. Chem. 270, 6856-6863
47. Yerushalmi, H., Lebendiker, M., and Schuldiner, S. (1996) Negative dominance studies demonstrate the oligomeric structure of EmrE, a multidrug antiporter from Escherichia coli. J. Biol. Chem. 271, 31044-31048
48. Kuan, G., Dassa, E., Saurin, W., Hofnung, M., and Saier, M. H., Jr. (1995) Phylogenetic analyses of the ATP-binding constituents of bacterial extracytoplasmic receptor-dependent ABC-type nutrient uptake permaeases. Res. Microbiol. 146, 271-278
49. Higgins, C. F., and Gottesman, M. M. (1992) Is the multidrug transporter a flippase? Trends Biochem. Sci. 17, 18-21
50. Ruetz, S., and Gros, P. (1994) Phosphatidylcholine translocase: A physiological role for the mdr2 gene. Cell 77, 841-847
51. van Helvoort, A., Smith, A. J., Sprong, H., Fritzsche, I., Schinkel, A. H., Borst, P., and van Meer, G. (1996) MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine. Cell 87, 507-517
52. Sali, A., Overington, J. P., Johnson, M. S., and Blundell, T. L. (1990) From comparisons of protein sequences and structures to protein modelling and design. Trends Biochem. Sci. 15, 235-240
53. Singer, S. J. (1990) The structure and insertion of integral proteins in membranes. Annu. Rev. Cell Biol. 6, 247-296
54. Singer, S. J., and Yaffe, M. P. (1990) Embedded or not? Hydrophobic sequences and membranes. Trends Biochem. Sci. 15, 369-373
55. Rapoport, T. A., Jungnickel, B., and Kutay, U. (1996) Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. Annu. Rev. Biochem. 65, 271-303
56. Martoglio, B., Hofmann, M. W., Brunner, J., and Dobberstein, B. (1995) The protein-conducting channel in the membrane of the endoplasmic reticulum is open laterally toward the lipid bilayer. Cell 81, 207-214
57. Olsen, G. J., Woese, C. R., and Overbeek, R. (1994) The winds of (evolutionary) change: Breathing new life into microbiology. J. Bacteriol. 176, 1-6