University of Groningen

Multidrug resistance in Lactococcus lactisBolhuis, Hendrik

IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite fromit. Please check the document version below.

Document VersionPublisher's PDF, also known as Version of record

Publication date:1996

Link to publication in University of Groningen/UMCG research database

Citation for published version (APA):Bolhuis, H. (1996). Multidrug resistance in Lactococcus lactis. [s.n.].

CopyrightOther than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of theauthor(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).

Take-down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.

Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons thenumber of authors shown on this cover page is limited to 10 maximum.

Download date: 10-11-2020

133

REFERENCES

A1. Ahmed,M., Borsch,C.M., Neyfakh,A.A. and Schuldiner,S. (1993) Mutants of the

Bacil lus subtilis multidrug transporter Bmr with altered sensitivity to theantihypertensive alkaloid reserpine. J. Biol. Chem., 268, 11086-11089.

2. Ahmed,M., Borsch,C.M., Taylor,S.S., Vazquez-Laslop,N. and Neyfakh,A.A. (1994)A protein that activates expression of a multidrug efflux transporter upon binding thetransporter substrates. J. Biol. Chem., 269, 28506-28513.

3. Ahmed,M., Lyass,L., Markham,P.N., Taylor,S.S., Vazquez-Laslop,N. andNeyfakh,A.A. (1995). Two highly similar multidrug transporters of Bacillus subtiliswhose expression is differentially regulated. J. Bacteriol., 177, 3904-3910.

4. Aldema,M.L., McMurry,L.M., Walmsley,A.R. and Levy,S.B. (1996) Purification of theTn10-specified tetracycline efflux antiporter TetA in a native state as a polyhistidinefusion protein. Mol. Microbiol., 19, 187-195.

5. Allen,C.N., Harpur,E.S., Gray,T.J.B., Simmons,N.L. and Hirst,B.H. (1990) Efflux ofBCECF by a novel ATP-dependent transport mechanism in epithelial cells.Biochem. Biophys. Res. Commun., 172, 262-267.

6. Allikmets,R., Gerrard,B., Court,D. and Dean,M. (1993) Cloning and organization ofthe abc and mdl genes of Escherichia coli: relationship to eukaryotic multidrugresistance. Gene, 136, 231-236.

7. Altenberg,G.A., Young,G., Horton,J.K., Glass,D., Belli,J.A. and Reuss,L. (1993)Changes in intra- or extracellular pH do not mediate P-glycoprotein-dependentmultidrug resistance. Proc. Natl. Acad. Sci. USA, 90, 9735-9738.

8. Altenberg,G.A., Vanoye,C.G., Horton,J.K. and Reuss,L. (1994) Unidirectional fluxesof rhodamine 123 in multidrug resistant cells: Evidence against direct extrusion fromthe plasma membrane. Proc. Natl. Acad. Sci. USA, 91, 4654-4657.

9. Alton,N.K. and Vapnek,D. (1979) Nucleotide sequence analysis of thechloramphenicol resistance transposon Tn9. Nature, 282, 864-869.

10. Ambudkar,S.V., Zlotnick,G.W. and Rosen,B.P. (1984) Calcium efflux fromEscherichia coli: Evidence for two systems. J. Biol. Chem., 259, 6142-6146.

11. Ambudkar,S.V., Lelong,I.H., Zhang,J., Cardarelli,C.O., Gottesman,M.M. andPastan,I. (1992) Partial purification and reconstitution of the human multidrug-resistance pump: characterization of the drug-stimulated ATP hydrolysis. Proc. Natl.Acad. Sci. USA, 89, 8472-8476.

12. Ames,G.F-L., Mimura,C.S. and Shyamala,V. (1990) Bacterial periplasmicpermeases belong to a family of transport proteins operating from E. coli to human:traffic ATPases. FEMS Microbiol. Rev., 75, 429-446.

References

134

13. Ames,G.F-L. and Joshi,A.K. (1990) Energy coupling in bacterial periplasmicpermeases. J. Bacteriol., 172, 4133-4137.

14. Andersen,O.S. (1978) Permeability properties of unmodified lipid bilayermembranes. In Tosteson,D.C. (ed.), Membrane transport in biology, vol. 1.Springer verlag, Berlin. pp. 369-446.

15. Ariza,R.R., Cohen,S.P., Bachhawat,N., Levy,S.B. and Demple,B. (1994) Repressormutations in the marRAB operon that activate oxidative stress genes and multipleantibiotic resistance in Escherichia coli. J. Bacteriol., 176, 143-148.

16. Auland,M.E., Roufogalis,B.D., Devaux,P.F. and Zachowski,A. (1994) Recon-stitution of ATP-dependent aminophospholipid translocation in proteoliposomes.Proc. Natl. Acad. Sci. USA, 91, 10938-10942.

17. Austin,E.A., Graves,J.F., Hite,L.A., Parker,C.T. and Schnaitman,C.A. (1990)Genetic analysis of lipopolysaccharide core biosynthesis by Escherichia coli K-12:insertion mutagenesis of the rfa locus. J. Bacteriol., 172, 5312-5325.

B18. Balzi,E., Wang,M., Leterme,S., Van Dijck,L. and Goffeau,A. (1994) PDR5, a novel

yeast multidrug resistance conferring transporter controlled by the transcriptionregulator PDR1. J. Biol. Chem., 269, 2206-2214.

19. Barabas,K., Sizensky,J.A. and Faulk,W.P. (1992) Transferrin conjugates ofadriamycin are cytotoxic without intercalating nuclear DNA. J. Biol. Chem., 267,9437-9442.

20. Barrasa,M.I., Tercero,j.a., Lacalle,R.A. and Jimenez,A. (1995) The ard1 gene fromStreptomyces capreolus encodes a polypeptide of the ABC-transporterssuperfamily which confers resistance to the aminonucleoside antibiotic A201A. Eur.J. Biochem., 228, 562-569.

21. Beaudet,L. and Gros,P. (1995) Functional dissection of P-glycoprotein nucleotide-binding domains in chimeric and mutant proteins. J. Biol. Chem., 270, 17159-17170.

22. Beck,W.T. and Qian,X-D. (1992) Photoaffinity substrates for P-glycoprotein.Biochem. Pharmacol., 43, 89-93.

23. Bêja,O. and Bibi,E. (1995) Multidrug resistance protein (Mdr)-alkaline phosphatasehybrids in Escherichia coli suggest a major revision in the topology of theC-terminal half of Mdr. J. Biol. Chem., 270, 12351-12354.

24. Bentley,J., Hyatt,L.S., Ainley,K., Parish,J.H., Herbert,R.B. and White,G.R. (1993)Cloning and sequence analysis of an Escherichia coli gene conferring bicyclomycinresistance. Gene, 127, 117-120.

25. Berkower,C. and Michaelis,S. (1991) Mutational analysis of the yeast a-factortransporter STE6, a member of the ATP binding cassette (ABC) proteinsuperfamily. EMBO J., 10, 3777-3785.

26. Bibi,E., Gros,P. and Kaback,H.R. (1993) Functional expression of mouse mdr1 in

References

135

Escherichia coli. Proc. Natl. Acad. Sci. USA, 90, 9209-9213.27. Bibi,E. and Béjà,O. (1994) Membrane topology of multidrug resistance protein

expressed in Escherichia coli; N-terminal domain. J. Biol. Chem., 269, 19910-19915.

28. Bielicki,J.K., Johnson,W.J., Glick,J.M. and Rothblat,G.H. (1991) Efflux ofphospholipid from fibroblast with normal and elevated levels of cholesterol.Biochim. Biophys. Acta, 1084, 7-14.

29. Bishop,L., Agbayani,R., Ambudkar,S.V., Maloney,P.C. and Ames,G.F-L. (1989)Reconstitution of a bacterial periplasmic permease in proteoliposomes anddemonstration of ATP hydrolysis concomitant with transport. Proc. Natl. Acad. Sci.USA, 86, 6953-6957.

30. Bissinger,P.H. and Kuchler,K. (1994) Molecular cloning and expression of theSaccharomyces cerevisiae STS1 gene product. A yeast ABC transporterconferring mycotoxin resistance. J. Biol. Chem., 269, 4180-4186.

31. Bissonnette,L., Champetier,S., Buisson,J.-P. and Roy,P.H. (1991) Characterizationof the non-enzymatic chloramphenicol resistance (cmlA) gene of the In4 integron ofTn1696: similarity of the product to transmembrane transport proteins. J. Bacteriol.,173, 4493-4502.

32. Blight,M.A. and Holland,I.B. (1990) Structure and function of haemolysin B, P-glycoprotein and other members of a novel family of ATP-dependent membranetranslocators. Mol. Microbiol., 4, 873-880.

33. Bolhuis,H., Molenaar,D., Poelarends,G., van Veen,H.W., Poolman,B.,Driessen,A.J.M. and Konings,W.N. (1994) Proton motive force-driven and ATP-dependent drug extrusion systems in multidrug resistant Lactococcus lactis. J.Bacteriol., 176, 6957-6964.

34. Bolhuis,H., Poelarends,G., van Veen,H.W., Poolman,B., Driessen,A.J.M. andKonings,W.N. (1995) The lactococcal lmrP gene encodes a proton motive force-dependent drug transporter. J. Biol. Chem., 270, 26092-26098.

35. Bolhuis,H., Molenaar,D., van Veen,H.W., Poolman,B., Driessen,A.J.M. andKonings,W.N. (1996a) Multidrug resistance in Lactococcus lactis: evidence forATP-dependent drug extrusion from the inner leaflet of the cytoplasmic membrane.EMBO J., In Press.

36. Bolhuis,H., van Veen,H.W., Brands,J.R., Putman,M., Poolman,B., Driessen,A.J.M.and Konings,W.N. (1996b) Energetics and mechanism of drug transport mediatedby the lactococcal MDR transporter LmrP. J. Biol. Chem., In Press.

37. Borst,P. and Ouellette,M. (1995) New mechanisms of drug resistance in parasiticprotozoa. Annu. Rev. Microbiol., 49, 427-460.

38. Bradley,G., Juranka,P.F. and Ling,V. (1988) Mechanism of multidrug resistance.Biochim. Biophys. Acta, 948, 87-128.

39. Bray,P.G. and Ward,S.A. (1993) Malaria chemotherapy: Resistance to quinolinecontaining drugs in Plasmodium falciparum. FEMS Microbiol. Lett., 113, 1-8.

40. Breeuwer,P., Drocourt,J-L., Rombouts,F.M. and Abee,T. (1994) Energy-dependent,carrier-mediated extrusion of carboxyfluorescein from Saccharomyces cerevisiaeallows rapid assessment of cell viability by flow cytometry. Appl. Environ.

References

136

Microbiol., 60, 1467-1472.41. Bruggemann,E.P., Currier,S.J., Gottesman,M.M. and Pastan,I. (1992)

Characterization of the azidopine and vinblastine binding site of P-glycoprotein. J.Biol. Chem., 267, 21020-21026.

C42. Chen,C-J., Chin,J.E., Ueda,K., Clark,D.P., Pastan,I., Gottesman,M.M. and

Roninson,I.B. (1986) Internal duplication and homology with bacterial transportproteins in the mdr1 (P-glycoprotein) gene from multidrug resistant human cells.Cell, 47, 381-389.

43. Chevereau,M., Daniels,P.J., Davies,J. and LeGoffic,F. (1974) Aminoglycosideresistance in bacteria mediated by gentamicin acetyltransferase II, an enzymemodifying the 2'-amino group of aminoglycoside antibiotics. Biochemistry, 13,598-603.

44. Cohen,S.P., Hächler,H. and Levy,S.B. (1993a) Genetic and functional analysis ofthe multiple antibiotic resistance (mar) locus in Escherichia coli. J. Bacteriol., 175,1484-1492.

45. Cohen,S.P., Levy,S.B., Foulds,J. and Rosner,J.L. (1993b) Salicylate induction ofantibiotic resistance in Escherichia coli; activation of the mar operon and a mar-independent pathway. J. Bacteriol., 175, 7856-7862.

46. Collington,G.K., Allen,C.N., Simmons,N.L. and Hirst,B.H. (1991) Pharmacologicalprofile of inhibition of BCECF efflux in human HCT-8 intestinal epithelial cells.Biochem. Pharmacol., 42, 33-38.

47. Cowman,A.F., Galatis,D. and Thompson,J.K. (1994) Selection for mefloquineresistance in Plasmodium falciparum is linked to amplification of the pfmdr1 geneand cross-resistance to halofantrine and quinine. Proc. Natl. Acad. Sci. USA, 91,1143-1147.

48. Cranney,M.N., Cundall,R.B., Jones,G.R., Richards,J.T. and Thomas,E.W. (1983)Fluorescence lifetime and quenching studies on some interesting diphenyl-hexatriene membrane probes. Biochim. Biophys. Acta, 735, 418-425.

49. Cullinton,B.J. (1992) Drug-resistant TB may bring epidemic. Nature, 356, 473.50. Currier,S.J., Kane,S.E., Willingham,M.C., Cardarelli,C.O., Pastan,I. and

Gottesman,M.M. (1992) Identification of residues in the first cytoplasmic loop of P-glycoprotein involved in the function of chimeric Human MDR1-MDR2 transporters.J. Biol. Chem., 267, 25153-25159.

D51. Danø, K. (1973) Active outward transport of daunomycin in resistant Ehrlich ascites

tumor cells. Biochem. Biophys. Acta, 323, 466-483.52. Dean,D.A., Davidson,A.L. and Nikaido,H. (1989) Maltose transport in membrane

vesicels of Escherichia coli is linked to ATP hydrolysis. Proc. Natl. Acad. Sci. USA,86, 9134-9138.

References

137

53. Decottignies,A., Kolaczkowski, M., Balzi,E. and Goffeau,A. (1994) Solubilizationand characterization of the overexpressed PDR5 multidrug resistance nucleotidetriphosphatase of yeast. J. Biol. Chem., 269, 12797-12803.

54. Decottignies,A., Lambert,L., Catty,P., Degand,H., Epping,E.A., Moye-Rowley, W.S.,Balzi,E. and Goffeau,A. (1995) Identification and characterization of SNQ2, a newmultidrug ATP binding cassette transporter of the yeast plasma membrane. J. Biol.Chem., 270, 18150-18157.

55. Devaux,P.F. (1992) Protein involvement in transmembrane lipid assymetry. Annu.Rev. Biophys. Biomol. Struct., 21, 417-439.

56. Devaux,P.F. and Zachowski,A. (1994) Maintenance and consequences ofmembrane phospholipid asymmetry. Chem. Phys. Lipids., 73, 107-120.

57. Devine,S.E., Ling,V. and Melera,P.W. (1992) Amino acid substitutions in the sixthtransmembrane domain of P-glycoprotein alter multidrug resistance. Proc. Natl.Acad. Sci. USA, 89, 4564-4568.

58. De Wolf,F.A., Maliepaard,M., Van Dorsten,F., Berghuis,I., Nicolay,K. and deKruijff,B. (1991) Comparable interaction of doxorubicin with various acidicphospholipids results in changes of lipid order and dynamics. Biochim. Biophys.Acta, 1096, 67-80.

59. Dong,Y.J., Chen,G., Duran,G.E., Kouyama,K., Chao,A.C., Sikic,B.I., Gollapudi,S.V.,Gupta,S. and Gardner,P. (1994) Volume-activated chloride current is not related toP- glycoprotein overexpression. Cancer Res., 54, 5029-5032.

60. Driessen,A.J.M., van den Hooven,H.W., Kuiper,W., van de kamp,M., Sahl,H.G.,Konings,R.N.H. and Konings,W.N. (1995) Mechanistic studies of lantibiotic-inducedpermeabilization of phospholipid vesicles. Biochemistry, 34, 1606-1614.

61. Dougherty,D.A. (1996) Cation-B interactions in chemistry and biology: A new viewof benzene, Phe, Tyr, and Trp. Science, 271, 163-168.

E62. Endicott,J.A. and Ling, V. (1989) The biochemistry of P-glycoprotein-mediated

multidrug resistance. Annu. Rev. Biochem., 58, 137-171.63. Eytan,G.D., Borgnia,M.J., Regev,R. and Assaraf,Y.G. (1994) Transport of

polypeptide ionophores into proteoliposomes reconstituted with rat liverP-glycoprotein. J. Biol. Chem., 269, 26058-26065.

F64. Fahey,R.C., Brown,W.C., Adams,W.B. and Worsham,M.B. (1978) Occurrence of

glutathione in bacteria. J. Bacteriol., 133, 1126-1129.65. Fath,M.J. and Kolter,R. (1993) ABC transporters: Bacterial exporters. Microbiol.

Rev., 57, 995-1017.66. Feller,N. Broxterman,H.J., Wahrer,D.C. and Pinedo,H.M. (1995) ATP-dependent

efflux of calcein by the multidrug resistance protein (MRP): no inhibition byintracellular glutathione depletion. FEBS Lett., 368, 385-388.

References

138

67. Felmlee,T., Pellet,S. and Welch,R.A. (1985) Nucleotide sequence of an Escherichiacoli chromosomal hemolysin. J. Bacteriol., 163, 94-105.

68. François, V., Louarn, J., Patte, J., and Louarn, J. M. (1987) A system for in vivoselection of genomic rearrangements with predetermined endpoints in Escherichiacoli using modified Tn10 transposons. Gene, 56, 99-108

69. Frezard,F. and Garnier-Suillerot,A. (1991). DNA-Containing liposomes as a modelfor the study of cell membrane permeation by anthracycline derivatives.Biochemistry, 30, 5038-5043.

70. Foote,S.J., Thompson,J.K., Cowman,A.F. and Kemp,D.J. (1989) Amplification ofthe multidrug resistance gene in some chloroquine-resistant isolates of P.falciparum. Cell, 57, 912-930.

71. Furukawa,H., Tsay,J.T., Jackowski,S., Takamura,Y. and Rock,C.O. (1993)Thiolactomycin Resistance in Escherichia coli Is Associated with the MultidrugResistance Efflux Pump Encoded by emrAB. J. Bacteriol., 175, 3723-3729.

G72. Gambino,L., Gracheck,S.J. and Miller,P.F. (1993) Overexpression of the MarA

positive regulator is sufficient to confer multiple antibiotic resistance in Escherichiacoli. J. Bacteriol., 175, 2888-2894.

73. Garrido,M.C., Herrero,M., Kolter,R. and Moreno,F. (1988) The export of the DNAreplication inhibitor microcin B17 provides immunity for the host cell. EMBO J., 7,1853-1862.

74. Gasser,F. (1994) Safety of lactic acid bacteria and their occurrence in humanclinical infections. Bull. Inst. Pasteur., 92, 45-67.

75. Gasson,M.J. (1983) J. Bacteriol. 154, 1-9.76. George,A.M., Hall,R.M. and Stokes,H.W. (1995) Multidrug resistance in Klebsiella

pneumoniae: a novel gene, ramA, confers a multidrug resistance phenotype inEscherichia coli. Microbiology, 141, 1909-1920.

77. Georges,E., Tsuruo,T. and Ling,V. (1993) Topology of P-glycoprotein asdetermined by epitope mapping of MRK-16 monoclonal antibody. J. Biol. Chem.,268, 1792-1798.

78. Germann,U.A., Willingham,M.C., Pastan,I. and Gottesman,M.M. (1990) Expressionof the human multidrug transporter in insect cells by a recombinant baculovirus.Biochemistry, 29, 2295-2303.

79. Germann,U.A., Chambers,T.C., Ambudkar,S.V., Pastan,I. and Gottesman,M.M.(1995) Effects of phosphorylation of P-glycoprotein on multidrug resistance. J.Bioenerg. Biomembr., 27, 53-61.

80. Glaasker,E., Konings,W.N. and Poolman,B. (1996) The application of pH sensitivefluorescent dyes in lactic acid bacteria reveals distinct extrusion systems forunmodified and conjugated dyes. Mol. membr. biol., In press.

81. Gottesman,M.M. and Pastan,I. (1988) The multidrug transporter, a double-edgedsword. J. Biol. Chem., 263, 12163-12166.

82. Gottesman,M.M. and Pastan,I. (1993) Biochemistry of multidrug resistance

References

139

mediated by the multidrug transporter. Annu. Rev. Biochem., 62, 385-427.83. Gottesman,M.M. (1993) How cancer cells evade chemotherapy. Cancer Res., 53,

747-754.84. Gottesman,M.M., Hrycyna,CA., Schoenlein,P.V., Germann,U.A. and Pastan,I. (1996)

Annu. Rev. Genet., 29, 607-649.85. Greenberger,L.M., Lisanti,C.J., Silva,J.T. and Horwitz,S.B. (1991) Domain mapping

of the photoaffinity drug-binding sites in P-glycoprotein encoded by mouse mdr1b.J. Biol. Chem., 266, 20744-20751.

86. Greenberger,L.M. (1993) Major photoaffinity drug labelling sites for Iodoarylazidoprazosin in P-glycoprotein are within, or immediately C-terminal to,transmembrane domains 6 and 12. J. Biol. Chem., 268, 11417-11425.

87. Grinius,L.L., Dregunienne,G. Goldberg,E.B., Liao,C-H. and Projan,S.J. (1992) Astaphylococcal multidrug resistance gene product is a member of a new proteinfamily. Plasmid, 27, 119-129.

88. Grinius,L.L. and Goldberg,E.B. (1994) Bacterial multidrug resistance is due to asingle membrane protein which functions as a drug pump. J. Biol. Chem., 269,29998-30004.

89. Gros,P., Croop,J. and Housman,D. (1986) Mammalian multidrug resistance gene:Complete cDNA sequence indicates strong homology to bacterial transportproteins. Cell, 47, 371-380.

90. Gros,P., Talbot,F., Tangwai,D., Bibi,E. and Kaback,H.R. (1992) Lipophilic cations- A group of model substrates for the multidrug-resistance transporter.Biochemistry, 31, 1992-1998.

91. Gründemann,D., Gorboulev,V., Gambaryan,S., Veyhl,M. and Koepsell,H. (1994)Drug extrusion mediated by a new prototype of polyspecific transporter. Nature,372, 549-552.

92. Guilfoile,P.G. and Hutchinson,C.R. (1991) A bacterial analog of the mdr gene ofmammalian tumour cells is present in Streptomyces peuceticus, the producer ofdaunorubicin and doxorubicin. Proc. Natl. Acad. Sci. USA., 88, 8553-8557.

93. Guilfoile,P.G. and Hutchinson,C.R. (1992). Sequence and transcriptional analysisof the Streptomyces glaucescens tcmAR tetracenomycin C resistance andrepressor gene loci. J. Bacteriol., 174, 3651-3658.

H94. Hächler,H., Cohen,S.P. and Levy,S.B. (1991) marA, a regulated locus which

controls expression of chromosomal multiple antibiotic resistance in Escherichiacoli. J. Bacteriol., 173, 5532-5538.

95. Hagman,K.E., Pan,W., Spratt,B.G., Balthazar,J.T., Judd,R.C. and Shafer,W.M.(1995) Microbiology, 141, 611-622.

96. Hagting,A., Kunji,E.R.S., Leenhouts,K.J., Poolman,B. and Konings,W.N. (1994) Thedi- and tripeptide transport protein of Lactococcus lactis; A new type of bacterial

References

140

peptide transporter. J. Biol. Chem., 269, 11391-11399.97. Haugland,R.P. (1992) Handbook of fluorescent probes and research chemicals.

Molecular Probes, Inc. Eugene USA.98. Hayes,J.D. and Wolf,C.R. (1990) Molecular mechanisms of drug resistance.

Biochem. J., 272, 281-295.99. Henderson,P.J.F. (1991) Studies of translocation catalysis. Biosci. Reports, 11,

477-538.100. Higgins,C.F., Hiles,I.D., Salmond,G.P.C., Gill,D.R., Downie,J.A., Evans,I.J.,

Holland,I.B., Gray,L., Buckel,S.D., Bell,A.W. and Hermodson,M.A. (1986) A familyof related ATP-binding subunits coupled to many distinct biological processes inbacteria. Nature, 323, 448-450.

101. Higgins,C.F. (1992) ABC transporters: from microorganisms to man. Annu. Rev.Cell Biol., 8, 67-113.

102. Higgins,C.F. and Gottesman,M.M. (1992) Is the multidrug transporter a flippase.Trends Biochem. Sci., 17, 18-21.

103. Higgins,C.F. (1994) Flip-Flop: The transmembrane translocation of lipids Cell, 79,393-395.

104. Hiles,I.D., Gallagher,M.P., Jamieson,D.J. and Higgins,C.F. (1987) Molecularcharacterization of the oligopeptide permease of Salmonella typhimurium. J. Mol.Biol., 195, 125-142.

105. Hillen,W., and Berens,C. (1994) Mechanisms underlying expression of Tn10encoded tetracycline resistance. Annu. Rev. Microbiol., 48, 345-369.

106. Hinrichs,W., Kisker,C., Düvel,M., Müller,A., Tovar,K., Hillen,W. and Saenger,W.(1994) Structure of the Tet repressor-tetracycline complex and regulation ofantibiotic resistance. Science, 264, 418-420.

107. Hollô,Z., Homolya,L., Davis,C.W. and Sarkadi,B. (1994) Calcein accumulation asa fluorometric functional assay of the multidrug transporter. Biochim. Biophys. Acta,1191, 384-388.

108. Homolya,L., Hollô,Z., Germann,U.A., Pastan,I., Gottesman,M.M. and Sarkadi,B.(1993) Fluorescent cellular indicators are extruded by the multidrug resistanceprotein. J. Biol. Chem., 268, 21493-21496.

109. Horio,M., Gottesman,M.M. and Pastan,I. (1988) ATP-dependent transport ofvinblastine in vesicles from human multidrug-resistant cells. Proc. Natl. Acad. Sci.USA., 85, 3580-3584.

110. Hughes,A.L. (1994) Evolution of the ATP-binding-cassette transmembranetransporters of vertebrates. Mol. Biol. Evol., 11, 899-910.

111. Hughes,C., Stanley,P. and Koronakis,V. (1992) E. coli hemolysin interactions withprokaryotic and eukaryotic cell membranes. Bioessays, 14, 519-525.

112. Hyde,S.C., Emsley,P. Hartshorn,M.J. Mimmack,M.M. Gileadi,U. Pearce,S.R.Gallagher,M.P. Gill,D.R., Hubbard,R.E. and Higgins,C.F. (1990) Structural modelof the ATP-binding proteins associated with cystic fibrosis, multidrug resistance andbacterial transport. Nature, 346, 362-365.

References

141

I113. Ishida,H., Fuziwara,H., Kaibori,Y., Horiuchi,T., Sato,K. and Osada,Y. (1995) Cloning

of multidrug resistance gene pqrA from Proteus vulgaris. Antimicrob. AgentsChemother., 39, 453-457.

114. Ishikawa,T. (1992) The ATP-dependent glutathione S-conjugate export pump.Trends Biochem. Sci., 17, 463-468.

115. Iwata,S., Ostermeier,C., Ludwig,B. and Michel,H. (1995) Structure at 2.8 Åresolution of cytochrome c oxidase from Paracoccus denitrificans. Nature, 376,660-669.

J116. Jarlier,V. and Nikaido,H. (1994) Mycobacterial cell wall: Structure and role in natural

resistance to antibiotics. FEMS Microbiol. Lett., 123, 11-18.117. Jessen-marshall,A.E., Paul,N.J. and Brooker,R.J. (1995) The conserved motif,

GXXX(D/E)(R/K)XG[X](R/K)(R/K), in hydrophilic loop 2/3 of the lactose permease.J. Biol. Chem., 270, 16251-16257.

118. Johnston,L.H. and Dyke,K.G.H. (1969) Ethidium bromide resistance, a new markeron the staphylococcal penicillinase plasmid. J. Bacteriol. 100, 1413-1414.

119. Juliano,R.L. and Ling,V. (1976) A surface glycoprotein modulating drug permeabilityin Chinese hamster ovary cell mutants. Biochim. Biophys. Acta, 455, 152-162.

K120. Kaatz,G.W., Seo,S.M. and Ruble,C.A. (1993) Efflux-mediated fluoroquinolone

resistance in Staphylococcus aureus. Antimicrob. Agents Chemother., 37, 1086-1094.

121. Kaback,H.R. (1971) Transport in isolated bacterial membrane vesicles. Methods.Enzymol., 31, 698-709.

122. Kamimoto,Y., Gatmaitan,Z., Hsu,J. and Arias,I.M. (1989) The function of Gp170, themultidrug resistance gene product, in rat liver canalicular membrane vesicles. J.Biol. Chem., 264, 11693-11698.

123. Karow,M. and Georgopoulos,C. (1993) The essential Escherichia coli msbA gene,a multicopy suppressor of null mutations in the htrB gene, is related to the universallyconserved family of ATP-dependent translocators. Mol. Microbiol., 7, 69-79.

124. Kern,W.V., Andriof,E., Oethinger,M., Kern,P., Hacker,J. and Marre,R. (1994)Emergence of fluoroquinolone-resistant Escherichia coli at a cancer center.Antimicrob. Agents Chemother., 38, 681-687.

125. Klein,J.R., Henrich,B.H. and Plapp,R. (1991) Molecular analysis and nucleotidesequence of the envCD operon of Escherichia coli. Mol. Gen. Genet., 230, 230-240.

References

142

126. Kisker,C., Hinrichs,W., Tovar,K., Hillen,W. and Saenger,W. (1995) The complexformed between Tet repressor and tetracycline-Mg reveals mechanism of2+

antibiotic resistance. J. Mol. Biol., 247, 260-280.127. Kitagawa,S., Matsubayashi,M., Kotani,K., Usui,K. and Kametani,F. (1991)

Asymmetry of membrane fluidity in the lipid bilayer of blood platelets: Fluorescencestudy with diphenylhexatriene and analogs. J. Membrane Biol., 119, 221-227.

128. Kok,J., van der Vossen,J.M.B.M. and Venema,G. (1984) Construction of plasmidcloning vectors for lactic streptococci which also replicate in Bacillus subtilis andEscherichia coli. Appl. Environ. Microbiol., 48, 726-731.

129. Kornelisse,R.F., de Groot,R. and Neijens,H.J. (1995) Bacterial meningitis:Mechanisms of disease and therapy. Eur. J. Pediatr., 154, 85-96.

130. Koronakis,V., Stanley,P., Koronakis,E. and Hughes,C. (1992) The HlyB/HlyD-dependent secretion of toxins by Gram-negative bacteria. FEMS Microbiol.Immunol., 105, 45-54.

131. Koronakis,V., Stanley,P., Koronakis,E. and Hughes,C. (1993) The HlyB/HlyD-dependent secretion of toxins by Gram-negative bacteria. FEMS Microbiol.Immun., 105, 45-54.

132. Karow,M. and Georgopoulos,C. (1993) The essential Escherichia coli msbA gene,a multicopy suppressor of null mutations in the htrB gene, is related to the universallyconserved family of ATP-dependent translocators. Mol. Microbiol., 7, 69-79.

133. Kuhry,J.G., Duportal,G., Bronner,C. and Laustriat,G. (1985) Plasma membranefluidity measurements on whole living cells by fluorescence anisotropy oftrimethylammonium-diphenylhexatriene. Biochim. Biophys. Acta, 845, 60-67.

134. Kyte,J., and Doolittle,R.F. (1982) J. Mol. Biol., 157, 105-132.

L135. Laemmli,U.K. (1970) Cleavage of structural proteins during the assembly of the

head of bacteriophage T4. Nature, 227, 680-685.136. Lambert,B., and Le Pecq,J.-B. (1984) Effect of mutation, electric membrane

potential, and metabolic inhibitors on the accessibility of nucleic acids to ethidiumbromide in Escherichia coli cells. Biochemistry, 83, 166-176.

137. Läuger,P. and Neumcke,B. (1973). Theoretical analysis of ion conductance in lipid bilayermembranes. In Eisenman,G. (ed.), Membranes. Vol. 2. Lipid bilayers and antibiotics.Marcel Dekker, Inc., New York, pp. 1-59.

138. Leenhouts, K.J., Kok,J. and Venema,G. (1990) Stability of integrated plasmids inthe chromosome of Lactococcus lactis. Appl. Environ. Microbiol., 56, 2726- 2735.

139. Leenhouts,K.J., and Venema,G. Lactococcal plasmid vectors. (1993) In Plasmidsa practical approach. (Hardy,K.G. Ed) pp66-94, IRL Press, Oxford.

140. Leier,I., Jedlitschky,G., Buchholz,U., Cole,S.P.C., Deeley,R.G. and Keppler,D.(1994) The MRP gene encodes an ATP-dependent export pump for leukotriene C 4

and structurally related conjugates. J. Biol. Chem., 269, 27807-27810.141. Le Pecq,J.-B. and Paoletti,C. (1967). A fluorescent complex between ethidium

References

143

bromide and nucleic acids. J. Mol. Biol., 27, 87-106.142. Levy,S.B. (1992). Active efflux mechanisms for antimicrobial resistance.

Antimicrob. Agents Chemother., 36, 695-703.143. Lewis,K. (1994). Multidrug resistance pumps in bacteria: variations on a theme.

Trends Biochem. Sci., 17, 18-21.144. Linton,K.J. Cooper,H.N., Hunter,I.S. and Leadlay,P.F. (1994) An ABC-transporter

from streptomyces longisporoflavus confers resistance to the polyether-ionophoreantibiotic tetronasin. Mol. Microbiol., 11, 777-785.

145. Littlejohn,T.G., DiBerardino,D., Messerotti,L.J., Spiers,S.J. and Skurray,R.A. (1990)Structure and evolution of a family of genes encoding antiseptic and disinfectantresistance in Staphylococcus aureus. Gene, 101, 59-66.

146. 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 ofantiseptic and disinfectant resistance in Staphylococcus aureus. FEMS Microbiol.Lett., 95, 259-266.

147. Liu,Y., Peter,D., Roghani,A., Schuldiner,S., Privé,G.G., Eisenberg,D., Brecha,N.Edwards,R.H. (1992) A cDNA that suppresses MPP toxicity encodes a vesicular+

amine transporter. Cell, 70, 539-551.148. Loe,D.W., Almquist,K.C., Deeley,R.G. and Cole,S.P.C. (1996) Multidrug resistance

protein (MRP)-mediated transport of leukotriene C and chemo-therapeutic agents4

in membrane vesicles; Demonstration of glutathione-dependent vincristinetransport. J. Biol. Chem., 271, 9675-9682.

149. Lomovskaya,O. and Lewis,K. (1992) Emr, an Escherichia coli locus for multidrugresistance. Proc. Natl. Acad. Sci. USA, 89, 8938-8942.

150. Lomovskaya,O., Lewis,K. and Matin,A. (1995) EmrR is a negative regulator of theEscherichia coli multidrug resistance pump EmrAB. J. Bacteriol., 177, 2328-2334.

151. Loo,T.W. and Clarke,D.M. (1994) Mutations to amino acids located in predictedtransmembrane segment 6 (TM6) modulate the activity and substrate specificity ofhuman P-glycoprotein. Biochemistry, 33, 14049-14057.

152. Loo,T.W. and Clarke,D.M. (1995) Membrane topology of a cysteine-less mutant ofhuman P-glycoprotein J. Biol. Chem., 270, 843-848.

153. Luz,J.G., Wei,L-Y., Basu,S. and Roepe,P.D. (1994) Transfection of mouse MDR1inhibits Na -independent Cl /HCO exchange in chinese hamster ovary+ - -

3

cells. Biochemistry, 33, 7239-7249.

M154. 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.

155. Ma,D., Cook,D.N., Hearst,J.E. and Nikaido,H. (1994) Efflux pumps and drugresistance in Gram-negative bacteria. Trends Microbiol., 12, 489-493.

References

144

156. Ma,D., Cook,D.N., Alberti,M., Pon,N.G., Nikaido,H. and Hearst,J.E. (1995) GenesacrA and acrB encode a stress-induced efflux system of Escherichia coli. Mol.Microbiol., 16, 45-55.

157. Marger,M.D. and Saier,Jr,M.H. (1993) A major superfamily of transmembranefacilitators that catalyse uniport, symport and antiport. Trends Biochem. Sci., 18,13-20.

158. Markham,P.N., Ahmed,M. and Neyfakh,A.A. (1996) The drug-binding activity of themultidrug responding transcriptional regulator BmrR resides in its C-terminaldomain. J. Bacteriol., 178, 1473-1475.

159. Martin,R.G. and Rosner,J.L. (1995) Binding of purified multiple antibiotic-resistancerepressor protein (MarR) to mar operator sequences. Proc. Natl. Acad. Sci. USA,92, 5456-5460.

160. Mátyus,L. (1992) Fluorescence resonance energy transfer measurements on cellsurfaces. A spectroscopic tool for determining protein interactions. J. Photochem.Photobiol., 12, 323-337.

161. McGrath,J.P. and Varshavsky,A. (1989) The yeast STE6 gene encodes ahomologue of the mammalian multidrug resistance P-glycoprotein. Nature, 340,400-404.

162. McMurry,L., Petrucci,R.E. and Levy,S.B. (1980) Active efflux of tetracycline encodedby four genetically different tetracycline resistance determinants in Escherichia coli.Proc. Natl. Acad. Sci. USA, 77, 3974-3977.

163. Meister, A. (1988) Glutathione metabolism and its selective modification. J. Biol.Chem., 263, 17205-17208.

164. 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.

165. Midgley,M. (1987) An efflux system for cationic dyes and related compounds inEscherichia coli. Microbiol. Sci., 4, 125-127.

166. Midgley,M. (1994) Characteristics of an ethidium efflux system in Enterococcushirae. FEMS Microbiol. Lett., 120, 119-124.

167. Mimura,C.S., Holbrook,S.R. and Ames,G.F-L. (1991) Structural model of thenucleotide-binding conserved component of periplasmic permeases. Proc. Natl.Acad. Sci. USA, 88, 84-88.

168. Miyauchi,S., Komatsubara,M. and Kamo,N. (1992) In archaebacteria, there is adoxorubicin efflux pump similar to mammalian P-glycoprotein. Biochim. Biophys.Acta, 1110, 144-150.

169. Molenaar,D., Abee,T. and Konings,W.N. (1991) Continuous measurement of thecytoplasmic pH in Lactococcus lactis with a fluorescent pH indicator. Biochim.Biophys. Acta, 1115, 75-83.

170. Molenaar,D., Bolhuis,H., Abee,T., Poolman,B. and Konings,W.N. (1992) The effluxof a fluorescent probe is catalyzed by an ATP-driven extrusion system inLactococcus lactis. J. Bacteriol., 174, 3118-3124.

171. Mülder,H.S., van Grondelle,R., Westerhoff,H.V. and Lankelma,J. (1993) A plasmamembrane 'vacuum cleaner' for daunorubicin in non-P-glycoprotein multidrug

References

145

resistant SW-1573 human non-small cell lung carcinoma cells: a study usingfluorescence resonance energy transfer. Eur. J. Biochem., 218, 871-882.

172. Müller,M., Meijer,C., Zaman,G.J.R., Borst,P., Scheper,R.J., Mulder,N.H., deVries,E.G. and Jansen,P.L.M. (1994) Overexpression of the gene encoding themultidrug resistance associated protein results in increased ATP-dependentglutathione S-conjugate transport. Proc. Natl. Acad. Sci. USA, 91, 13033-13037.

N173. Neyfakh,A.A., Bidnenko,V.E. and Chen,L.B. (1991) Efflux-mediated multidrug

resistance in Bacillus subtilis: similarities and dissimilarities with the mammaliansystem. Proc. Natl. Acad. Sci. USA. 88, 4781-4785.

174. Neyfakh,A.A. (1992) The multidrug efflux transporter of Bacillus subtilis is astructural and functional homolog of the Staphylococcus NorA protein. Antimicrob.Agents Chemother., 36, 484-485.

175. Nikaido,H. and Thanassi,D.G. (1993) Penetration of lipophilic agents with multipleprotonation sites into bacterial cells tetracyclines and fluoroquinolones as examples.Antimicrob. Agents Chemother., 37, 1393-1399.

176. Nikaido,H. (1994) Prevention of drug access to bacterial targets: permeabilitybarriers and active efflux. Science, 264, 382-388.

177. Noda,Y., Yoda,K., Takatsuki,A. and Yamasaki,M. (1992) TmrB protein, responsiblefor tunicamycin resistance of Bacillus subtilis, is a novel ATP-binding membraneprotein. J. Bacteriol., 174, 4302-4307.

O178. Okusu,H., Ma,D. and Nikaido,H. (1996) AcrAB efflux pump plays a major role in the

antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance(Mar) mutants. J. Bacteriol., 178, 306-308.

179. Olano,C., Rodríguez,A.M., Méndez,C. and Salas,J.A. (1995) A second ABCtransporter is involved in oleandomycin resistance and its secretion byStreptomyces antibioticus. Mol. Microbiol., 16, 333-343.

180. Oude Elferink,R.P., Ottenhoff,R., Radominska,A., Hofmann,A.F., Kuipers.F. andJansen,P.L. (1991) Inhibition of glutathione-conjugate secretion from isolatedhepatocytes by dipolar bile acids and other organic anions. Biochem. J., 274, 281-286

P181. 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 andprokaryotes - an analysis. Gene, 124, 1-11.

182. Paulsen,I.T. Brown,M.H., Dunstan,S.J. and Skurray,R.A. (1995) Molecular

References

146

characterization of the staphylococcal multidrug resistance export protein QacC. J.Bacteriol., 177, 2827-2833.

183. Paulsen,I.T., Skurray,R.A., Tam,R., Sajer,Jr.,M.H., Turner,R.J., Weiner,J.H.,Goldberg,E.B. and Grinius,L.L. (1996) The SMR family: a novel family of multidrugefflux proteins involved with the efflux of lipophilic drugs. Mol. Microbiol., 19, 1167-1175.

184. Pawagi,A.B., Wang,J., Silverman,M., Reithmeier,R.A.F. and Deber,C.M. (1994)Transmembrane aromatic amino acid distribution in P-glycoprotein: A functionalrole in broad substrate specificity. J. Mol. Biol., 235, 554-564.

185. Pedersen,P.L. (1995) Multidrug resistance: A fascinating, clinically relevant problemin bioenergetics. J. Bioenerg. Biomembr., 27, 3-5.

186. Podlesek,Z., Comino,A., Herzog-Velikonja,B., ðgur-Bertok,D., Komel,R. andGrabnar,M. (1995) Bacillus licheniformis bacitracin-resistance ABC transporter:relationship to mammalian multidrug resistance. Mol. Microbiol., 16, 969-976.

187. Poole,K., Krebes,K., McNally,C. and Neshat,S. (1993) Multiple antibiotic resistancein Pseudomonas aeruginosa - evidence for involvement of an efflux operon. J.Bacteriol., 175, 7363-7372.

188. Poole,K. (1994) Bacterial multidrug resistance - Emphasis on efflux mechanismsand Pseudomonas aeruginosa. J. Antimicrob. Chemother., 34, 453-456.

189. Poolman,B., Driessen,A.J.M. and Konings,W.N. (1987) Regulation of solutetransport in streptococci by external and internal pH values. Microbiol. Rev., 51,498-508.

190. Poolman,B. and Konings,W.N. (1993) Secondary solute transport in bacteria.Biochim. Biophys. Acta, 1183, 5-39.

191. Poolman,B., Knol,J,M., van der Does,C., Henderson,P.J.F., Liang,W-J., Leblanc,G.,Pourcher,T. and Mus-Veteau,I. (1996) Cation and sugar selectivity determinants ina novel family of transport proteins. Mol. Microbiol., 19, 911-922.

192. Prendergast,F.G., Haugland,R.P. and Callahan,P.J. (1981) 1-[4-(trimethylamino)-phenyl]-6-phenylhexa-1,3,5-triene: Synthesis, fluorescence properties, and use ofthe fluorescence probe of lipid bilayers. Biochemistry, 20, 7333-7338.

193. Purewal,A.S. (1991) Nucleotide sequence of the ethidium efflux gene fromEscherichia coli. FEMS Microbiol. Lett., 82, 229-232.

R194. Raviv,Y., Pollard,H.B., Bruggemann,E.P., Pastan,I. and Gottesman,M.M. (1990)

Photosensitized labeling of a functional multidrug transporter in living drug resistanttumor cells. J. Biol. Chem., 265, 3975-3980.

195. Raymond,M., Gros,P., Whiteway,M. and Thomas,D.Y. (1992) Functional comple-mentation of yeast ste6 by a mammalian multidrug resistance mdr gene. Science,256, 232-234.

196. Reizer,J., Reizer,A. and Saier,Jr.,M.H. (1994) A functional superfamily ofsodium/solute symporters. Biochim. Biophys. Acta, 1197, 133-166.

197. Rodriguez,A.M., Olano,C., Vilches,C., Mendez,C. and Salas,J.A. (1993)

References

147

Streptomyces antibioticus contains at least three oleandomycin-resistancedeterminants, one of which shows similarity with proteins of the ABC-transportersuperfamily. Mol. Microbiol., 8, 571-582.

198. Roepe,P.D. (1992) Analysis of the steady-state and initial rate of doxorubicin effluxfrom a series of multidrug-resistant cells expressing different levels of P-glycoprotein. Biochemistry, 31, 12555-12564.

199. Roepe,P.D., Weisburg,J.H., Luz,J.G., Hoffman,M.M. and Wei,L-Y. (1994) Novel Cl --

dependent intracellular pH regulation in murine MDR1 transfectants and potentialimplications. Biochemistry, 33, 11008-11015.

200. Rosner,J.L. and Slonczewski,J.L. (1994) Dual regulation of inaA by the multipleantibiotic resistance (Mar) and superoxide (SoxRS) stress response systems ofEscherichia coli. J. Bacteriol., 176, 6262-6269.

201. Ross,J.I., Eady,E.A., Cove,J.H., Cunliffe,W.J., Baumberg,S. and Wootton,J.C.(1990) Inducible erythromycin resistance in Staphylococci is encoded by a memberof the ATP-binding transport super-gene family. Mol. Microbiol., 4, 1207-1214.

202. Ross,J.I., Eady,E.A., Cove,J.H. and Baumberg,S. (1995) Identification of achromosomally encoded ABC-transport system with which the staphylococcalerythromycin exporter MsrA may interact. Gene, 153, 93-98.

203. Rosteck,P.R., Reynolds,P.A. and Hershberger,C.L. (1991) Homology betweenproteins controlling Streptomyces fradiae tylosin resistance and ATP-bindingtransport. Gene, 102, 27-32.

204. Rouch,D.A., Cram,D.S., DiBerardino,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.

205. Ruetz,S. and Gros,P. (1994a) Phosphatidylcholine translocase: a physiological rolefor the mdr2 gene. Cell, 77, 1071-1081.

206. Ruetz,S. and Gros,P. (1994b) Functional expression of P-glycoproteins in secretoryvesicles. J. Biol. Chem., 269, 12277-12284.

S207. 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.

208. Sambrook,J., Fritsch,E.F. and Maniatis,T. (1989) Molecular cloning: A laboratorymanual, 2nd ed., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.

209. Sanders.J.W., Leenhouts,K.J., Haandrikman,A.J., Venema,G. and Kok,J. (1995)Stress response in Lactococcus lactis: cloning, expression analysis, and mutationof the lactococcal superoxide dismutase gene. J. Bacteriol., 177, 5254-5260.

210. Sanger,F., Nicklen,S. and Coulson,A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA, 74, 5463-5467.

211. Sarkadi,B., Price,E.M., Boucher,R.C., Germann,U.A. and Scarborough,G.A. (1992)Expression of the human multidrug resistance cDNA in insect cells generates a high

References

148

activity drug-stimulated membrane ATPase. J. Biol. Chem., 267, 4854-4858. 212. Scarborough,G.A. (1995) Drug-stimulated ATPase activity of the human

P-glycoprotein. J. Bioenerg. Biomembr., 27, 37-41.213. Schachter,D., Cogan,U. and Abbott,R.E. (1982) Asymmetry of lipid dynamics in

Human erythrocyte membranes studied with permeant fluorophores. Biochemistry,21, 2146-2150.

214. Schinkel,A.H. and Borst,P. (1991) Multidrug resistance mediated by P-glycoprotein.Cancer Biol., 2, 213-226.

215. Schinkel,A.H., Kemp,S., Dollé,M., Rudenko,G. and Wagenaar,E. (1993) N-glycosylation and deletion mutants of the human MDR1 P-glycoprotein. J. Biol.Chem., 268,7474-7481.

216. Schinkel, A.H., Smit,J.J.M., Van Tellingen,O., Beijnen,J.H., Wagenaar,E., VanDeemter,L., Mol,C.A.A.M., Van Der Valk,M.A., Robanus-Maandag,E.C., TeRiele,H.P.J., Berns,A.J.M. and Borst,P. (1994) Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increasedsensitivity to drugs. Cell, 77, 491-502.

217. Schlemmer,S.R. and Sirotnak,F.M. (1994) Functional studies of P-glycoprotein ininside-out plasma membrane vesicles derived from murine erythroleukemia cellsoverexpressing MDR3: Properties and kinetics of the interaction of vinblastine withP-glycoprotein and evidence for its active mediated transport. J. Biol. Chem., 269,31059-31066.

218. Schoner,B., Geistlich,M., Rosteck,Jr,P. Rao,R.N., Reynolds,P., Cox,K., Burgett,S.and Hershberger,C. (1992) Sequence similarity between macrolide-resistancedeterminants and ATP-binding transport proteins. Gene, 115, 93-96.

219. Schuldiner,S., Shirvan,A. and Linial,M. (1995). Vesicular Neurotransmittertransporters: from bacteria to humans. Physiol. Rev., 75, 369-392.

220. Schwartz,R.M. and Dayhoff,M.O. (1987) In Atlas of protein sequence and structure,(Dayhoff,M.O. Ed.), vol 5 suppl. 3. pp. 353-358, Nat. Biomed. Res.Found.,Washington, DC.

221. Senior,A.E., Al-Shawi,M.K. and Urbatsch,I.L. (1995) ATP hydrolysis by multidrug-resistance protein from chines hamster ovary cells. J. Bioenerg. Biomembr., 27,31-36.

222. Seoane,A.S. and Levy,S.B. (1995a) Identification of new genes regulated by themarRAB operon in Escherichia coli. J. Bacteriol., 177, 530-535.

223. Seoane,A.S. and Levy,S.B. (1995b) Characterization of MarR, the repressor of themultiple antibiotic resistance (mar) operon in Escherichia coli. J. Bacteriol., 177,3414-3419.

224. Shapiro,A.B. and Ling,V. (1995a) Using purified P-glycoprotein to understandmultidrug resistance. J. Bioenerg. Biomembr., 27, 7-13.

225. Shapiro,A.B. and Ling,V. (1995b) Reconstitution of drug transport by purified P-glycoprotein. J. Biol. Chem., 270, 16167-16175.

226. Sharma,R.C., Inoue,S., Roitelman,J., Schimke,R.T. and Simoni,R.D. (1992) Peptidetransport by the multidrug resistance pump. J. Biol. Chem., 267, 5731-5734.

227. Sharom,F.J. (1995) Characterization and functional reconstitution of the multidrug

References

149

transporter. J. Bioenerg. Biomembr., 27, 15-22. 228. Sheps,J.A., Cheung,I. and Ling,V. (1995) Hemolysin transport in Escherichia coli:

Point mutants in HlyB compensate for a deletion in the predicted amphiphilic helixregion of the HlyA signal. J. Biol. Chem., 270, 14829-14834.

229. Shinbo,T., Kama,N., Kurihara,K. and Kobataka,Y. (1978) PVC-based electrodesensitive to DDA as a device to monitor the membrane potential in biological+

systems. Arch. Biochem. Biophys., 187, 414-422.230. Sikkema,J., de Bont,J.A.M. and Poolman,B. (1995) Mechanism of membrane

toxicity of hydrocarbons. Microbiol. Rev., 59, 201-222.231. Silver,S. and Walderhaug,M. (1992) Gene regulation of plasmid- and chromosome-

determined inorganic ion transport in bacteria. Microbiol. Rev., 56, 195-228.232. Simon,S.M., Roy,D. and Schindler,M. (1994) Intracellular pH and the control of

multidrug resistance. Proc. Natl. Acad. Sci. USA, 91, 1128-1132.233. Simon,S.M. and Schindler,M. (1994) Cell biological mechanisms of multidrug

resistance in tumors. Proc. Natl. Acad. Sci. USA, 91, 3497-3504.

234. Skach,W.R., Calayag,M.C. and Lingappa,V.R. (1993) Evidence for an alternatemodel of human P-glycoprotein structure and biogenesis. J. Biol. Chem., 268,6903-6908.

235. Smit,J.J.M., Schinkel,A.H., Oude Elferink,R.P.J., Groen,A.K., Wagenaar,E., vanDeemter,L., Mol,C.A.A.M., Ottenhoff,R., van der Lugt,N.M.T., van Roon,M.A., van derValk,M.A., Offerhaus,G.J.A., Berns,A.J.M. and Borst,P. (1993) Homozygousdisruption of the murine mdr2 P-glycoprotein gene leads to a complete absence ofphospholipid from bile and to liver disease. Cell, 75, 451-462.

236. Speelmans,G., Staffhorst,R.W.H.M., de Kruijff,B. and de Wolf,F.A. (1994) Transportstudies of doxorubicin in model membranes indicate a difference in passive diffusionacross and binding at the outer and inner leaflets of the plasma membrane.Biochemistry, 33, 13761-13768.

237. Speelmans,G., Staffhorst,R.W.H.M., de Wolf,F.A. and de Kruijff,B. (1995)Verapamil competes with doxorubicin for binding to anionic phospholipids resultingin increased internal concentrations and rates of passive transport of doxorubicin.Biochim. Biophys. Acta, 1238, 137-146.

238. Speer,B.S., Shoemaker,N.B. and Salyers,A.A. (1992) Bacterial resistance totetracycline: Mechanism, transfer, and clinical significance. Clin. Microbiol. Rev.,5, 387-399.

239. Spoelstra,E.C., Westerhoff,H.V., Dekker,H. and Lankelma.J. (1992) Kinetics ofdaunorubicin transport by P-glycoprotein of intact cancer cells. Eur. J. Biochem.,207, 567-579.

240. Spratt,B.G. (1994) Resistance to antibiotics mediated by target alterations.Science, 264, 388-393.

241. Stein,W.D., Cardarelli,C., Pastan,I. and Gottesman,M.M. (1994) Kinetic evidencesuggesting that the multidrug transporter differentially handles influx and efflux of itssubstrates. Mol. Pharmacol., 45, 763-772.

References

150

T242. Takata,R., Osawa,S., Tanaka,K., Teraoka,H. and Tamaki,M. (1970) Genetic studies

of the ribosomal proteins in Escherichia coli; Mapping of erythromycin resistancemutations which lead to alteration of a 50s ribosomal protein component. Mol. Gen.Genet., 109, 123-130.

243. Tankovic,J., Desplaces,N., Duval,J. and Courvalin,P. (1994) In vivo selection duringpefloxacin therapy of a mutant of Staphylococcus aureus with two mechanisms offluoroquinolone resistance. Antimicrob. Agents Chemother., 38, 1149-1151.

244. 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 encodingantiseptic and disinfectant resistance in Staphylococcus aureus. J. Gen.Microbiol., 135, 1-10.

245. Travis,J. (1994) Reviving the antibiotic miracle? Science, 264, 360-362.

U246. Ueda,K., Cardarelli,C., Gottesman,M.M. and Pastan,I. (1987) Expression of a full-

length cDNA for the human "MDR1" gene confers resistance to colchicine,doxorubicin, and vinblastine. Proc. Natl. Acad. Sci. USA, 84, 3004-3008.

247. Urbatsch,I.L. and Senior,A.E. (1995) Effects of lipids on ATPase activity of purifiedchinese hamster P-glycoprotein. Arch. Biochem. Biophys., 316, 135-140.

248. Urbatsch,I.L., Sankaran,B., Weber,J. and Senior,A.E. (1995a) P-glycoprotein isstably inhibited by vanadate-induced trapping of nucleotide at a single catalytic site.J. Biol. Chem., 270, 19383-19390.

249. Urbatsch,I.L., Sankaran,B., Bhagat,S. and Senior,A.E. (1995b) Both P-glycoproteinnucleotide-binding sites are catalytically active. J. Biol. Chem., 270, 26956-26961.

V250. Vaara,M. (1992) Agents that increase the permeability of the outer membrane.

Microbiol. Rev., 56, 395-411.251. Valverde,M.A., Diaz,M., Sepulveda,F., Gill,D.R., Hyde,S.C. and Higgins,C.F. (1992)

Volume-regulated chloride channels associated with the human multidrug-resistance P-glycoprotein. Nature, 355, 830-833.

252. Van Veen,H.W., Bolhuis,H., Putman,M. and Konings,W.N. (1996a) Multidrugresistance in prokaryotes: molecular mechanisms of drug efflux. In ‘Handbook ofBiological Physics’, Vol. II Transport Processes in Eukaryotic and prokaryoticmembranes. Eds, H.R. Kaback, W.N. Konings, J.S. Lolkema. Chapter XI pElseviers, Amsterdam.

253. Van Veen,H.W., Venema,K., Bolhuis,H., Oussenko,I., Kok,J., Poolman,B.,Driessen,A.J.M. and Konings,W.N. (1996b) Multidrug resistance mediated by abacterial homolog of the human drug transporter MDR1. Proc. Natl. Acad. Sci.USA, In press.

254. van Schie,B.J., Hellingwerf,K.J., van Dijken,J.P., Elferink,M.G.L., van Dijl,J.M.,

References

151

Kuenen,J.G. and Konings,W.N. (1985) Energy transduction by electron transfer viaa pyrrolo-quinoline quinone dependent glucose dehydrogenase in Escherichia coli,Pseudomonas aeruginosa and Acinetobacter calcoaceticus (var. lwoffi). J.Bacteriol., 163, 493-499.

255. Versantvoort,C.H.M., Broxterman,H.J., Feller,N., Dekker,H., Kuiper,C.M. andLankelma,J. (1992) Probing daunorubicin accumulation defects in non-P-glycoprotein expressing multidrug resistant cell lines using digitonin. Int. J. Cancer,50, 906-911.

256. Volkman,S.K., Cowman,A.F. and Wirth,D.F. (1995) Functional complementation ofthe ste6 gene of Saccharomyces cerevisiae with the pfmdr1 gene of Plasmodiumfalciparum. Proc. Natl. Acad. Sci. USA, 92, 8921-8925.

257. von Heijne, G. (1986) The distribution of positively charged residues in bacterialinner membrane proteins correlates with the transmembrane topology. EMBO J. 5,3021-3027.

W258. Wadkins,R.M. and Houghton,P.J. (1993) The role of drug-lipid interactions in the

biological activity of modulators of multi-drug resistance. Biochim. Biophys. Acta,1153, 225-236.

259. Wadler,S. and Yang,C-P.H. (1991) Reversal of doxorubicin resistance byhydrophobic but not hydrophilic, forskolins. Mol. Pharmacol., 40, 960-964.

260. Wandersman,C. and Delepelaire,P. (1990) TolC, an Escherichia coli outermembrane protein required for hemolysin secretion. Proc. Natl. Acad. Sci. USA,87, 4776-4780.

261. Waring,M.J. (1965) Complex formation between ethidium bromide and nucleicacids. J. Mol. Biol., 13, 269-282.

262. Wei,L-Y. and Roepe,P.D. (1994) Low external pH and osmotic shock increase theexpression of Human MDR protein. Biochemistry, 33, 7229-7238.

263. West,I.C. (1990) What determines the substrate specificity of the multidrugresistance pump. Trends Biochem. Sci., 15, 42-46.

Y264. Yamaguchi,A., Udagawa,T. and Sawai,T. (1990) Transport of divalent cations with

tetracycline as mediated by the transposon Tn10-encoded tetracycline resistanceprotein. J. Biol. Chem., 265, 4809-4813.

265. Yamaguchi,A., Someya,Y. and Sawai,T. (1992) Metal-Tetracycline/H antiporter of+

Escherichia coli encoded by transposon Tn10; The role of a conserved sequencemotif, GXXXXRXGRR, in a putative cytoplasmic loop between helices 2 and 3. J.Biol. Chem., 267, 19155-19162.

266. Yamaguchi,A., Kimura,T., Someya,Y. and Sawai,T. (1993) Metal-Tetracycline/H+

antiporter of Escherichia coli encoded by transposon Tn10; The structural

References

152

resemblance and functional difference in the role of the duplicated sequence motifbetween hydrophobic segments 2 and 3 and segments 8 and 9. J. Biol. Chem.,268, 6496-6504.

267. Yerushalmi,H., Lebendiker,M., and Schuldiner,S. (1995) EmrE, an Escherichia coli12-kDa multidrug transporter, exchanges toxic cations and H and is soluble in+

organic solvents. J. Biol. Chem., 270, 6856- 6863.268. Yoshida,H., Bogaki,M., Nakamura,S., Ubukata,K. and Konno,M. (1990) Nucleotide

sequence and characterization of the Staphylococcus aureus norA gene, whichconfers resistance to quinolones. J. Bacteriol., 172, 6942-6949.

Z269. Zaman,G.J.R., Versantvoort,C.H.M., Smit,J.J.M., Eijdems,E.W.H.M., de Haas,M.,

Smith,A.J., Broxterman,H.J., Mulder,N.H., de Vries,E.G.E., Baas,F. and Borst,P.(1993) Analysis of the expression of MRP, the gene for a new putativetransmembrane drug transporter, in human multidrug resistant lung cancer cell lines.Cancer Res., 53, 1747-1750.

270. Zaman,G.J.R., Flens,M.J., van Leusden,M.R., de Haas,M., Mulder,H.S.,Lankelma,J., Pinedo,H.M., Scheper,R.J., Baas,F., Broxterman,H.J. and Borst,P.(1994) The human multidrug resistance-associated protein MRP is a plasmamembrane drug-efflux pump. Proc. Natl. Acad. Sci. USA, 91, 8822-8826.

271. Zeuthen,T. and Stein,W.D. (1994) Cotransport of salt and water in membraneproteins: proteins as osmotic engines. J. Membrane Biol., 137, 179-195.

272. Zhanel,G.G., Karlowsky,J.A., Saunders,M.H., Davidson,R.J., Hoban,D.J.,Hancock,R.E.W., Mclean,I. and Nicolle,L.E. (1995) Development ofmultiple-antibiotic-resistant (Mar) mutants of Pseudomonas aeruginosa after serialexposure to fluoroquinolones. Antimicrob. Agents Chemother., 39, 489-495.

273. Zhang,J-T. and Ling,V. (1991) Study of membrane orientation and glycosylatedextracellular loops of mouse P-glycoprotein by in vitro translation. J. Biol. Chem.,266, 18224-18232.

274. Zhang,J-T. and Ling,V. (1995) Involvement of cytoplasmic factors regulating themembrane orientation of P-glycoprotein sequences. Biochemistry, 34, 9159-9165.

275. Zhang,J-T., Lee,C.H., Duthie,M. and Ling,V. (1995a) Topological determinants ofinternal transmembrane segments in P-glycoprotein sequences. J. Biol. Chem.,270, 1742-1746.

276. Zhang,X.P., Collins,K.I. and Greenberger,L.M. (1995b) Functional evidence thattransmembrane 12 and the loop between transmembrane 11 and 12 form part ofthe drug-binding domain in P-glycoprotein encoded by MDR1. J. Biol. Chem., 270,5441-5448.

277. Zhang,F., Yin,Y., Arrowsmith,C.H. and Ling,V. (1995) Secretion and circulardichroism analysis of the C-terminal signal peptides of HlyA and LktA.Biochemistry, 34, 4193-4201.

278. Zwietering,M.H., Jongenburger,I., Rombouts,F.M. and van 't Riet,K. (1990)Modelling of the bacterial growth curve. Appl. Environ. Microbiol., 56, 1875-1881.

155

LIST OF ABBREVIATIONS

)R Membrane potential)pH proton gradient)p, pmf proton motive force BCECF 2',7'-bis-(2-carboxyethyl)-5-(and-6)-carboxyfluoresceinBCECF-AM BCECF-acetoxymethyl ester TMA-DPH 1-[4-(trimethylamino) phenyl]-6-phenylhexa-1,3,5-trieneTMAP-DPH N-p-(6-phenyl-(1,3,5 hexatrienyl(phenyl-(propyl))))trimethyl-ammoniumDMA-DPH 1-[4-(dimethylamino)phenyl]-6-phenylhexa-1,3,5-triene) or the anionic DPH-CA 1,6-diphenylhexa-1,3,5-triene carboxylic acidNBD-PE N-(7-nitrobenz-2-oxa-1,3-diazol-4-yl)-1,2-dihexadecanoyl-sn-glycero-3-

phosphoethanolamineDPX P-xylene-bis-pyridinium bromide

IPTG isopropyl-$-D-thiogalactopyranosideDiSC(5) 3,3'-dipropylthiadicarbocyanine iodide3

TPP+ tetraphenyl phosphonium ionPQQ pyrrolo-quinoline quinoneNi-NTA Ni -nitrilo-tri-acetic acid2+

HEPES 4-(2-hydroxyethyl)-1-piperazinethane-sulfonate

MDR MultiDrug ResistanceSDR Specific Drug ResistanceTMS TransMembrane spannng SegmentTEXAN Toxin EXtruding AntiportersSMR Small Multidrug ResistanceMFS Major Facilitator SuperfamilyRND Resistance Nodulation Devision

157

LIST OF PUBLICATIONS

1. Bolhuis,H., van Veen,H.W. Poolman,B., Driessen,A.J.M. and Konings,W.N. (1996)Mechanism of multidrug transporters FEMS Microbiol. Rev., Submitted.

2. Bolhuis,H., van Veen,H.W. Brands,J.R., Putman,M., Poolman,B., Driessen,A.J.M.and Konings,W.N. (1996) Energetics and Mechanism of drug transport mediatedby the lactococcal multidrug transporter LmrP. J. Biol. Chem., In press.

3. Bolhuis,H., van Veen,H.W., Molenaar,D., Poolman,B., Driessen,A.J.M. andKonings,W.N. (1996) Multidrug resistance in Lactococcus lactis: Evidence forATP-dependent drug extrusion from the inner leaflet of the cytoplasmic membrane.the EMBO journal., 15, 4239-4245.

4. Bolhuis,H., Poelarends,G., van Veen,H.W., Poolman,B. Driessen,A.J.M. and Konings,W.N. (1995) The Lactococcal lmrP gene encodes a proton motive force-dependent drug transporter. J. Biol. Chem., 270, 26092-26098.

5. Bolhuis,H., Molenaar,D., Poelarends,G., van Veen,H.W., Poolman,B.,Driessen,A.J.M. and Konings,W.N. (1994) Proton motive force-driven and ATP-dependent drug extrusion systems in multidrug resistant Lactococcus lactis. J.Bacteriol., 176, 6957-6964.

6. Konings,W.N., Lolkema,J., Bolhuis,H., van Veen,H.W., Poolman,B. andDriessen,A.J.M. (1996) The role of transport processes in the survival of lacticacid bacteria. Ant. Leeuwenhoek., In press.

7. Laan,H., Bolhuis,H., Poolman,B., Abee,T. and Konings,W.N. (1993). Regulation ofproteinase synthesis in Lactococcus lactis. Acta Biotechnol., 13, 95-101

8. Molenaar,D., Bolhuis,H., Abee,T., Poolman,B. and Konings,W.N. (1992) The effluxof a fluorescent probe is catalyzed by an ATP-driven extrusion system inLactococcus lactis. J. Bacteriol., 174, 3118-3124.

9. van Veen,H.W., Bolhuis,H., Putman,M. and Konings,W.N. (1996) Multidrugresistance in prokaryotes: Molecular mechanisms of drug efflux. In Handbook ofBiological Physics, Vol II (Ed. Konings,W.N., Kaback,R.H., and Lolkema,J.) pp165-187. Elsevier Amsterdam.

10. van Veen,H.W., Venema,K., Bolhuis,H., Oussenko,I., Kok,J., Poolman,B.,Driessen, A.J.M. and Konings,W.N. (1996) Drug transport mediated by a novelprokaryotic homologue of the human multidrug resistance P-glycoprotein. Proc.Natl. Acad. Sci. USA, 93, 10668-10672.