Characterization and regulation of the Resistance-Nodulation-Cell Division-type multidrug efflux pumps MdtABC and MdtUVW from the fire blight pathogen Erwinia amylovora

BMC Microbiology

Volumn 14, Issue 1, 2014, Pages

  Pletzer, Daniel ^a   Weingart, Helge ^a  

^a JACOBS UNIVERSITY BREMEN   (Germany)

Author keywords

BaeR; CpxR; Erwinia amylovora; Fire blight; MdtABC; MdtUVW; Multidrug efflux; Plant pathogen; RND transporter

Indexed keywords

ANTI-BACTERIAL AGENTS; BIOLOGICAL TRANSPORT, ACTIVE; DRUG RESISTANCE, BACTERIAL; ERWINIA AMYLOVORA; GENE DELETION; GENE EXPRESSION PROFILING; GENES, MDR; MALUS; MEMBRANE TRANSPORT PROTEINS; PLANT ROOTS; SUBSTRATE SPECIFICITY; TANNINS; TUNGSTEN COMPOUNDS;

EID: 84904078740     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-14-185     Document Type: Article

References (58)

1. Vanneste J, Fire blight: The disease and its causative agent, Erwinia amylovora Oxon, UK: CABI Publishing 2000
2. Phenolic compounds and their role in disease resistance. Nicholson RL, Hammerschmidt R, Annu Rev Phytopathol 1992 30 369 389 (Pubitemid 24411041)
3. Mechanism of antibiotic efflux in Gram-negative bacteria. Zgurskaya HI, Krishnamoorthy G, Tikhonova EB, Lau SY, Stratton KL, Front Biosci 2003 8 862 873
4. Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Piddock LJ, Clin Microbiol Rev 2006 19 382 402
5. Multidrug efflux pumps of gram-negative bacteria. Nikaido H, J Bacteriol 1996 178 5853 5859 (Pubitemid 26337766)
6. Molecular mechanisms that confer antibacterial drug resistance. Walsh C, Nature 2000 406 775 781
7. The phytoalexin-inducible multidrug efflux pump AcrAB contributes to virulence in the fire blight pathogen, Erwinia amylovora. Burse A, Weingart H, Ullrich MS, Mol Plant-Microbe Interact 2004 17 43 54 (Pubitemid 38398226)
8. Crystal structure of bacterial multidrug efflux transporter AcrB. Murakami S, Nakashima R, Yamashita E, Yamaguchi A, Nature 2002 419 587 593
9. Bypassing the periplasm: reconstitution of the AcrAB multidrug efflux pump of Escherichia coli. Zgurskaya HI, Nikaido H, Proc Natl Acad Sci U S A 1999 96 7190 7195 (Pubitemid 29299637)
10. Engineered disulfide bonds support the functional rotation mechanism of multidrug efflux pump AcrB. Seeger MA, von Ballmoos C, Eicher T, Brandstatter L, Verrey F, Diederichs K, Pos KM, Nat Struct Mol Biol 2008 15 199 205 (Pubitemid 351207515)
11. 2C heterotrimer. Kim HS, Nagore D, Nikaido H, J Bacteriol 2010 192 1377 1386
12. 2C complex of Escherichia coli. Kim HS, Nikaido H, Biochemistry 2012 51 4188 4197
13. The putative response regulator BaeR stimulates multidrug resistance of Escherichia coli via a novel multidrug exporter system, MdtABC. Nagakubo S, Nishino K, Hirata T, Yamaguchi A, J Bacteriol 2002 184 4161 4167 (Pubitemid 34774296)
14. The baeSR two-component regulatory system activates transcription of the yegMNOB (mdtABCD) transporter gene cluster in Escherichia coli and increases its resistance to novobiocin and deoxycholate. Baranova N, Nikaido H, J Bacteriol 2002 184 4168 4176 (Pubitemid 34774297)
15. Regulation of multidrug efflux systems involved in multidrug and metal resistance of Salmonella enterica serovar Typhimurium. Nishino K, Nikaido E, Yamaguchi A, J Bacteriol 2007 189 9066 9075
16. The BaeSR regulon is involved in defense against zinc toxicity in E. coli. Wang D, Fierke CA, Metallomics 2013 5 372 383
17. Novel inducers of the envelope stress response BaeSR in Salmonella Typhimurium: BaeR is critically required for tungstate waste disposal. Appia-Ayme C, Patrick E, Sullivan MJ, Alston MJ, Field SJ, AbuOun M, Anjum MF, Rowley G, PLoS One 2011 6 23713
18. A third envelope stress signal transduction pathway in Escherichia coli. Raffa RG, Raivio TL, Mol Microbiol 2002 45 1599 1611 (Pubitemid 35231977)
19. Characterization of the induction and cellular role of the BaeSR two-component envelope stress response of Escherichia coli. Leblanc SK, Oates CW, Raivio TL, J Bacteriol 2011 193 3367 3375
20. The BaeSR two-component regulatory system mediates resistance to condensed tannins in Escherichia coli. Zoetendal EG, Smith AH, Sundset MA, Mackie RI, Appl Environ Microbiol 2008 74 535 539
21. Characterization of the Cpx regulon in Escherichia coli strain MC4100. Price NL, Raivio TL, J Bacteriol 2009 191 1798 1815
22. Periplasmic stress and ECF sigma factors. Raivio TL, Silhavy TJ, Annu Rev Microbiol 2001 55 591 624 (Pubitemid 32978117)
23. Just scratching the surface: an expanding view of the Cpx envelope stress response. Vogt SL, Raivio TL, FEMS Microbiol Lett 2012 326 2 11
24. The Cpx envelope stress response is controlled by amplification and feedback inhibition. Raivio TL, Popkin DL, Silhavy TJ, J Bacteriol 1999 181 5263 5272 (Pubitemid 29416345)
25. Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Otto K, Silhavy TJ, Proc Natl Acad Sci U S A 2002 99 2287 2292 (Pubitemid 34169053)
26. Comprehensive studies of drug resistance mediated by overexpression of response regulators of two-component signal transduction systems in Escherichia coli. Hirakawa H, Nishino K, Hirata T, Yamaguchi A, J Bacteriol 2003 185 1851 1856 (Pubitemid 36297885)
27. Indole induces the expression of multidrug exporter genes in Escherichia coli. Hirakawa H, Inazumi Y, Masaki T, Hirata T, Yamaguchi A, Mol Microbiol 2005 55 1113 1126 (Pubitemid 40299181)
28. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG, Mol Syst Biol 2011 7 539
29. Darwin v. 2.0: an interpreted computer language for the biosciences. Gonnet GH, Hallett MT, Korostensky C, Bernardin L, Bioinformatics 2000 16 101 103 (Pubitemid 30248584)
30. Iron and citrate export by a major facilitator superfamily pump regulates metabolism and stress resistance in Salmonella Typhimurium. Frawley ER, Crouch ML, Bingham-Ramos LK, Robbins HF, Wang W, Wright GD, Fang FC, Proc Natl Acad Sci U S A 2013 110 12054 12059
31. TOPCONS: consensus prediction of membrane protein topology. Bernsel A, Viklund H, Hennerdal A, Elofsson A, Nucleic Acids Res 2009 37 465 468
32. Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Saier MH Jr, Tam R, Reizer A, Reizer J, Mol Microbiol 1994 11 841 847 (Pubitemid 24199651)
33. Proton-dependent multidrug efflux systems. Paulsen IT, Brown MH, Skurray RA, Microbiol Rev 1996 60 575 608 (Pubitemid 26415669)
34. Characterization of AcrD, a resistance-nodulation-cell division-type multidrug efflux pump from the fire blight pathogen Erwinia amylovora. Pletzer D, Weingart H, BMC Microbiol 2014 14 13
35. Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Murakami S, Nakashima R, Yamashita E, Matsumoto T, Yamaguchi A, Nature 2006 443 173 179 (Pubitemid 44387601)
36. Virulence and drug resistance roles of multidrug efflux systems of Salmonella enterica serovar Typhimurium. Nishino K, Latifi T, Groisman EA, Mol Microbiol 2006 59 126 141
37. Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Treutter D, Plant Biol 2005 7 581 591 (Pubitemid 43004025)
38. Antimicrobial properties of tannins. Scalbert A, Phytochemistry 1991 30 3875 3883
39. Induction of antimicrobial 3-deoxyflavonoids in pome fruit trees controls fire blight. Halbwirth H, Fischer TC, Roemmelt S, Spinelli F, Schlangen K, Peterek S, Sabatini E, Messina C, Speakman JB, Andreotti C, Rademacher W, Bazzi C, Costa G, Treutter D, Forkmann G, Stich K, Z Naturforsch C 2003 58 765 770 (Pubitemid 38069701)
40. Analysis of condensed tannins: a review. Schofield P, Mbugua DM, Pell AN, Anim Feed Sci Technol 2001 91 21 40 (Pubitemid 32515977)
41. β-lactam resistance modulated by the overexpression of response regulators of two-component signal transduction systems in Escherichia coli. Hirakawa H, Nishino K, Yamada J, Hirata T, Yamaguchi A, J Antimicrob Chemother 2003 52 576 582 (Pubitemid 37258416)
42. Activity of plant flavonoids against antibiotic-resistant bacteria. Xu HX, Lee SF, Phytother Res 2001 15 39 43 (Pubitemid 32155108)
43. Antimicrobial activity of flavonoids. Cushnie TP, Lamb AJ, Int J Antimicrob Agents 2005 26 343 356 (Pubitemid 41483464)
44. Recent advances in understanding the antibacterial properties of flavonoids. Cushnie TP, Lamb AJ, Int J Antimicrob Agents 2011 38 99 107
45. Sambrook J, Russell DW, Molecular cloning: a laboratory manual Cold Spring Harbor: Cold Spring Harbor Press 2001
46. Analysis of the role of the type III effector inventory of Pseudomonas syringae pv. phaseolicola 1448a in interaction with the plant. Zumaquero A, Macho AP, Rufián JS, Beuzón CR, J Bacteriol 2010 192 4474 4488
47. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP, Gene 1998 212 77 86 (Pubitemid 28269135)
48. R cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Cherepanov PP, Wackernagel W, Gene 1995 158 9 14
49. Clinical and Laboratory Standards Institute, Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard Wayne, PA: CLSI document M7-A7 9 2012
50. PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Hobert O, Biotechniques 2002 32 728 730 (Pubitemid 34298696)
51. Hornik K, R: A language and environment for statistical computing Vienna, Austria: R Foundation for Statistical Computing 2013
52. Antagonistic activities of epiphytic bacteria from soybean leaves against Pseudomonas syringae pv. glycinea in vitro and in planta. May R, Völksch B, Kampmann G, Microb Ecol 1997 34 118 124 (Pubitemid 27335848)
53. Extraction of high-quality bacterial RNA from infected leaf tissue for bacterial in planta gene expression analysis by multiplexed fluorescent Northern hybridization. Schenk A, Weingart H, Ullrich MS, Mol Plant Pathol 2008 9 227 235 (Pubitemid 351280996)
54. Complete nucleotide sequence of ubiquitous plasmid pEA29 from Erwinia amylovora strain Ea88: gene organization and intraspecies variation. McGhee GC, Jones AL, Appl Environ Microbiol 2000 66 4897 4907
55. Evaluation of reference genes for real-time RT-PCR expression studies in the plant pathogen Pectobacterium atrosepticum. Takle GW, Toth IK, Brurberg MB, BMC Plant Biol 2007 7 50
56. Artemis: sequence visualization and annotation. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B, Bioinformatics 2000 16 944 945
57. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ, Bioinformatics 2009 25 1189 1191
58. The Pfam protein families database. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD, Nucleic Acids Res 2012 40 290 301