Inducible expression of a resistance-nodulation-division-type efflux pump in Staphylococcus aureus provides resistance to linoleic and arachidonic acids

Journal of Bacteriology

Volumn 197, Issue 11, 2015, Pages 1893-1905

  Alnaseri, Heba ^a   Arsic, Benjamin ^a   Schneider, James E T ^a   Kaiser, Julienne C ^a   Scinocca, Zachariah C ^a,b   Heinrichs, David E ^a   McGavin, Martin J ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID DERIVATIVE; BACTERIAL PROTEIN; FATTY ACID; LINOLEIC ACID; RESISTANCE NODULATION DIVISION TYPE EFFLUX PUMP; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERICIDAL ACTIVITY; FARE GENE; FARR GENE; GENE EXPRESSION; GENE INACTIVATION; GENE SEQUENCE; GRAM POSITIVE BACTERIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; SINGLE NUCLEOTIDE POLYMORPHISM; STAPHYLOCOCCUS AUREUS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MICROBIOLOGY; STAPHYLOCOCCUS INFECTION; TRANSPORT AT THE CELLULAR LEVEL;

POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

ARACHIDONIC ACIDS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; LINOLEIC ACID; POLYMORPHISM, SINGLE NUCLEOTIDE; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84929429303     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02607-14     Document Type: Article

References (86)

1. Boucher H, Miller LG, Razonable RR. 2010. Serious infections caused by methicillin-resistant Staphylococcus aureus. Clin Infect Dis 51(Suppl 2): S183-S197. http://dx.doi.org/10.1086/653519.
2. Kochanek KD, Xu J, Murphy SL, Minino AM, Kung HC. 2012. Deaths: final data for 2009. Natl Vital Stat Rep 60:1-117.
3. van Hal SJ, Jensen SO, Vaska VL, Espedido BA, Paterson DL, Gosbell IB. 2012. Predictors of mortality in Staphylococcus aureus bacteremia. Clin Microbiol Rev 25:362-386. http://dx.doi.org/10.1128/CMR.05022-11.
4. DeLeo FR, Diep BA, Otto M. 2009. Host defense and pathogenesis in Staphylococcus aureus infections. Infect Dis Clin North Am 23:17-34. http://dx.doi.org/10.1016/j.idc.2008.10.003.
5. Archer GL. 1998. Staphylococcus aureus: a well-armed pathogen. Clin Infect Dis 26:1179-1181. http://dx.doi.org/10.1086/520289.
6. Lowy FD. 1998. Staphylococcus aureus infections. N Engl J Med 339:520-532. http://dx.doi.org/10.1056/NEJM199808203390806.
7. de Lencastre H, Oliveira D, Tomasz A. 2007. Antibiotic resistant Staphylococcus aureus: a paradigm of adaptive power. Curr Opin Microbiol 10:428-435. http://dx.doi.org/10.1016/j.mib.2007.08.003.
8. Pearson H. 2002. "Superbug" hurdles key drug barrier. Nature 418:469. http://dx.doi.org/10.1038/418469b.
9. Mediavilla JR, Chen L, Mathema B, Kreiswirth BN. 2012. Global epidemiology of community-associated methicillin resistant Staphylococcus aureus (CA-MRSA). Curr Opin Microbiol 15:588-595. http://dx.doi.org/10.1016/j.mib.2012.08.003.
10. Diekema DJ, Richter SS, Heilmann KP, Dohrn CL, Riahi F, Tendolkar S, McDanel JS, Doern GV. 2014. Continued emergence of USA300 methicillin-resistant Staphylococcus aureus in the United States: results from a nationwide surveillance study. Infect Control Hosp Epidemiol 35:285-292. http://dx.doi.org/10.1086/675283.
11. Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL. 2005. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5:751-762. http://dx.doi.org/10.1016/S1473-3099(05)70295-4.
12. Thurlow LR, Joshi GS, Clark JR, Spontak JS, Neely CJ, Maile R, Richardson AR. 2013. Functional modularity of the arginine catabolic mobile element contributes to the success of USA300 methicillin-resistant Staphylococcus aureus. Cell Host Microbe 13:100-107. http://dx.doi.org/10.1016/j.chom.2012.11.012.
13. Planet PJ, Larussa SJ, Dana A, Smith H, Xu A, Ryan C, Uhlemann AC, Boundy S, Goldberg J, Narechania A, Kulkarni R, Ratner AJ, Geoghegan JA, Kolokotronis SO, Prince A. 2013. Emergence of the epidemic methicillin-resistant Staphylococcus aureus strain USA300 Coincides with horizontal transfer of the arginine catabolic mobile element and speGmediated adaptations for survival on skin. mBio 4(6):e00889-13. http://dx.doi.org/10.1128/mBio.00889-13.
14. Takigawa H, Nakagawa H, Kuzukawa M, Mori H, Imokawa G. 2005. Deficient production of hexadecenoic acid in the skin is associated in part with the vulnerability of atopic dermatitis patients to colonization by Staphylococcus aureus. Dermatology 211:240-248. http://dx.doi.org/10.1159/000087018.
15. Cork MJ, Robinson DA, Vasilopoulos Y, Ferguson A, Moustafa M, MacGowan A, Duff GW, Ward SJ, Tazi-Ahnini R. 2006. New perspectives on epidermal barrier dysfunction in atopic dermatitis: geneenvironment interactions. J Allergy Clin Immunol 118:3-23. http://dx.doi.org/10.1016/j.jaci.2006.04.042.
16. Do TQ, Moshkani S, Castillo P, Anunta S, Pogosyan A, Cheung A, Marbois B, Faull KF, Ernst W, Chiang SM, Fujii G, Clarke CF, Foster K, Porter E. 2008. Lipids including cholesteryl linoleate and cholesteryl arachidonate contribute to the inherent antibacterial activity of human nasal fluid. J Immunol 181:4177-4187. http://dx.doi.org/10.4049/jimmunol.181.6.4177.
17. Xiong Z, Ge S, Chamberlain NR, Kapral FA. 1993. Growth cycleinduced changes in sensitivity of Staphylococcus aureus to bactericidal lipids from abscesses. J Med Microbiol 39:58-63. http://dx.doi.org/10.1099/00222615-39-1-58.
18. Shryock TR, Kapral FA. 1992. The production of bactericidal fatty acids from glycerides in staphylococcal abscesses. J Med Microbiol 36:288-292. http://dx.doi.org/10.1099/00222615-36-4-288.
19. Parsons JB, Yao J, Frank MW, Jackson P, Rock CO. 2012. Membrane disruption by antimicrobial fatty acids releases low-molecular-weight proteins from Staphylococcus aureus. J Bacteriol 194:5294-5304. http://dx.doi.org/10.1128/JB.00743-12.
20. Clarke SR, Mohamed R, Bian L, Routh AF, Kokai-Kun JF, Mond JJ, Tarkowski A, Foster SJ. 2007. The Staphylococcus aureus surface protein IsdA mediates resistance to innate defenses of human skin. Cell Host Microbe 1:199-212. http://dx.doi.org/10.1016/j.chom.2007.04.005.
21. Truong-Bolduc QC, Villet RA, Estabrooks ZA, Hooper DC. 2014. Native efflux pumps contribute resistance to antimicrobials of skin and the ability of Staphylococcus aureus to colonize skin. J Infect Dis 209:1485-1493. http://dx.doi.org/10.1093/infdis/jit660.
22. Min Y, Blois A, Geppert J, Khalil F, Ghebremeskel K, Holmsen H. 2014. Dietary fat intake, circulating and membrane fatty acid composition of healthy Norwegian men and women. J Hum Nutr Diet 27:69-75. http://dx.doi.org/10.1111/jhn.12105.
23. Koehrer P, Saab S, Berdeaux O, Isaico R, Gregoire S, Cabaret S, Bron AM, Creuzot-Garcher CP, Bretillon L, Acar N. 2014. Erythrocyte phospholipid and polyunsaturated fatty acid composition in diabetic retinopathy. PLoS One 9:e106912. http://dx.doi.org/10.1371/journal.pone.0106912.
24. Arsic B, Zhu Y, Heinrichs DE, McGavin MJ. 2012. Induction of the staphylococcal proteolytic cascade by antimicrobial fatty acids in community acquired methicillin resistant Staphylococcus aureus. PLoS One 7:e45952. http://dx.doi.org/10.1371/journal.pone.0045952.
25. Cadieux B, Vijayakumaran V, Bernards MA, McGavin MJ, Heinrichs DE. 2014. Role of lipase from community-associated methicillin-resistant Staphylococcus aureus strain USA300 in hydrolyzing triglycerides into growth-inhibitory free fatty acids. J Bacteriol 196:4044-4056. http://dx.doi.org/10.1128/JB.02044-14.
26. Kato Y, Suzuki T, Ida T, Maebashi K. 2010. Genetic changes associated with glycopeptide resistance in Staphylococcus aureus: predominance of amino acid substitutions in YvqF/VraSR. J Antimicrob Chemother 65:37-45. http://dx.doi.org/10.1093/jac/dkp394.
27. Renzoni A, Andrey DO, Jousselin A, Barras C, Monod A, Vaudaux P, Lew D, Kelley WL. 2011. Whole genome sequencing and complete genetic analysis reveals novel pathways to glycopeptide resistance in Staphylococcus aureus. PLoS One 6:e21577. http://dx.doi.org/10.1371/journal.pone.0021577.
28. Nickerson NN, Joag V, McGavin MJ. 2008. Rapid autocatalytic activation of the M4 metalloprotease aureolysin is controlled by a conserved N-terminal fungalysin-thermolysin-propeptide domain. Mol Microbiol 69:1530-1543. http://dx.doi.org/10.1111/j.1365-2958.2008.06384.x.
29. Yeung M, Balma-Mena A, Shear N, Simor A, Pope E, Walsh S, McGavin MJ. 2011. Identification of major clonal complexes and toxin producing strains among Staphylococcus aureus associated with atopic dermatitis. Microbes Infect 13:189-197. http://dx.doi.org/10.1016/j.micinf.2010.10.023.
30. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, Davidson MG, Lin F, Lin J, Carleton HA, Mongodin EF, Sensabaugh GF, Perdreau-Remington F. 2006. Complete genome sequence of USA300, an epidemic clone of community-acquired methicillin-resistant Staphylococcus aureus. Lancet 367:731-739. http://dx.doi.org/10.1016/S0140-6736(06)68231-7.
31. Altshuler D, Pollara VJ, Cowles CR, Van Etten WJ, Baldwin J, Linton L, Lander ES. 2000. An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 407:513-516. http://dx.doi.org/10.1038/35035083.
32. Novick RP. 1991. Genetic systems in staphylococci. Methods Enzymol 204:587-636. http://dx.doi.org/10.1016/0076-6879(91)04029-N.
33. Nickerson N, Ip J, Passos DT, McGavin MJ. 2010. Comparison of staphopain A (ScpA) and B (SspB) precursor activation mechanisms reveals unique secretion kinetics of proSspB (staphopain B), and a different interaction with its cognate staphostatin, SspC. Mol Microbiol 75:161-177. http://dx.doi.org/10.1111/j.1365-2958.2009.06974.x.
34. Fey PD, Endres JL, Yajjala VK, Widhelm TJ, Boissy RJ, Bose JL, Bayles KW. 2013. A genetic resource for rapid and comprehensive phenotype screening of nonessential Staphylococcus aureus genes. mBio 4:e00537-12. http://dx.doi.org/10.1128/mBio.00537-12.
35. Lee CY, Iandolo JJ. 1986. Lysogenic conversion of staphylococcal lipase is caused by insertion of the bacteriophage L54a genome into the lipase structural gene. J Bacteriol 166:385-391.
36. Charpentier E, Anton AI, Barry P, Alfonso B, Fang Y, Novick RP. 2004. Novel cassette-based shuttle vector system for gram-positive bacteria. Appl Environ Microbiol 70:6076-6085. http://dx.doi.org/10.1128/AEM.70.10.6076-6085.2004.
37. Mesak LR, Yim G, Davies J. 2009. Improved lux reporters for use in Staphylococcus aureus. Plasmid 61:182-187. http://dx.doi.org/10.1016/j.plasmid.2009.01.003.
38. Bae T, Schneewind O. 2006. Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55:58-63. http://dx.doi.org/10.1016/j.plasmid.2005.05.005.
39. Greenway DL, Dyke KG. 1979. Mechanism of the inhibitory action of linoleic acid on the growth of Staphylococcus aureus. J Gen Microbiol 115: 233-245. http://dx.doi.org/10.1099/00221287-115-1-233.
40. Ma D, Cook DN, Alberti M, Pon NG, Nikaido H, Hearst JE. 1995. Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli. Mol Microbiol 16:45-55. http://dx.doi.org/10.1111/j.1365-2958.1995.tb02390.x.
41. Hagman KE, Shafer WM. 1995. Transcriptional control of the mtr efflux system of Neisseria gonorrhoeae. J Bacteriol 177:4162-4165.
42. Blair JM, Smith HE, Ricci V, Lawler AJ, Thompson LJ, Piddock LJ. 2015. Expression of homologous RND efflux pump genes is dependent upon AcrB expression: implications for efflux and virulence inhibitor design. J Antimicrob Chemother 70:424-431. http://dx.doi.org/10.1093/jac/dku380.
43. Pacheco SA, Hsu FF, Powers KM, Purdy GE. 2013. MmpL11 protein transports mycolic acid-containing lipids to the mycobacterial cell wall and contributes to biofilm formation in Mycobacterium smegmatis. J Biol Chem 288:24213-24222. http://dx.doi.org/10.1074/jbc.M113.473371.
44. Soding J, Biegert A, Lupas AN. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244-W248. http://dx.doi.org/10.1093/nar/gki408.
45. Bennett-Lovsey RM, Herbert AD, Sternberg MJ, Kelley LA. 2008. Exploring the extremes of sequence/structure space with ensemble fold recognition in the program PHYRE. Proteins 70:611-625. http://dx.doi.org/10.1002/prot.21688.
46. Agari Y, Agari K, Sakamoto K, Kuramitsu S, Shinkai A. 2011. TetRfamily transcriptional repressor Thermus thermophilus FadR controls fatty acid degradation. Microbiology 157:1589-1601. http://dx.doi.org/10.1099/mic.0.048017-0.
47. Agari Y, Sakamoto K, Kuramitsu S, Shinkai A. 2012. Transcriptional repression mediated by a TetR family protein, PfmR, from Thermus thermophilus HB8. J Bacteriol 194:4630-4641. http://dx.doi.org/10.1128/JB.00668-12.
48. Hoffmann KM, Williams D, Shafer WM, Brennan RG. 2005. Characterization of the multiple transferable resistance repressor, MtrR, from Neisseria gonorrhoeae. J Bacteriol 187:5008-5012. http://dx.doi.org/10.1128/JB.187.14.5008-5012.2005.
49. Murakami S, Nakashima R, Yamashita E, Yamaguchi A. 2002. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419:587-593. http://dx.doi.org/10.1038/nature01050.
50. Horsburgh MJ, Aish JL, White IJ, Shaw L, Lithgow JK, Foster SJ. 2002. SigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol 184:5457-5467. http://dx.doi.org/10.1128/JB.184.19.5457-5467.2002.
51. Shryock TR, Dye ES, Kapral FA. 1992. The accumulation of bactericidal lipids in staphylococcal abscesses. J Med Microbiol 36:332-336. http://dx.doi.org/10.1099/00222615-36-5-332.
52. Wille JJ, Kydonieus A. 2003. Palmitoleic acid isomer (C16:1Δ6) in human skin sebum is effective against gram-positive bacteria. Skin Pharmacol Appl Skin Physiol 16:176-187. http://dx.doi.org/10.1159/000069757.
53. Kazakov AE, Rodionov DA, Alm E, Arkin AP, Dubchak I, Gelfand MS. 2009. Comparative genomics of regulation of fatty acid and branchedchain amino acid utilization in proteobacteria. J Bacteriol 191:52-64. http://dx.doi.org/10.1128/JB.01175-08.
54. Parsons JB, Frank MW, Jackson P, Subramanian C, Rock CO. 2014. Incorporation of extracellular fatty acids by a fatty acid kinase-dependent pathway in Staphylococcus aureus. Mol Microbiol 92:234-245. http://dx.doi.org/10.1111/mmi.12556.
55. Parsons JB, Broussard TC, Bose JL, Rosch JW, Jackson P, Subramanian C, Rock CO. 2014. Identification of a two-component fatty acid kinase responsible for host fatty acid incorporation by Staphylococcus aureus. Proc Natl Acad Sci U S A 111:10532-10537. http://dx.doi.org/10.1073/pnas.1408797111.
56. Nakamura H. 1968. Genetic determination of resistance to acriflavine, phenethyl alcohol, and sodium dodecyl sulfate in Escherichia coli. J Bacteriol 96:987-996.
57. Nakamura H. 1965. Gene-controlled resistance to acriflavine and other basic dyes in Escherichia coli. J Bacteriol 90:8-14.
58. Schneiders T, Amyes SG, Levy SB. 2003. Role of AcrR and ramA in fluoroquinolone resistance in clinical Klebsiella pneumoniae isolates from Singapore. Antimicrob Agents Chemother 47:2831-2837. http://dx.doi.org/10.1128/AAC.47.9.2831-2837.2003.
59. Olliver A, Valle M, Chaslus-Dancla E, Cloeckaert A. 2004. Role of an acrR mutation in multidrug resistance of in vitro-selected fluoroquinolone-resistant mutants of Salmonella enterica serovar Typhimurium. FEMS Microbiol Lett 238:267-272. http://dx.doi.org/10.1111/j.1574-6968.2004.tb09766.x.
60. Webber MA, Talukder A, Piddock LJ. 2005. Contribution of mutation at amino acid 45 of AcrR to acrB expression and ciprofloxacin resistance in clinical and veterinary Escherichia coli isolates. Antimicrob Agents Chemother 49:4390-4392. http://dx.doi.org/10.1128/AAC.49.10.4390-4392.2005.
61. Xiao Q, Vakulenko S, Chang M, Mobashery S. 2014. Mutations in mmpL and in cell wall stress stimulon contribute to resistance to oxadiazole antibiotics in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 58:5841-5847. http://dx.doi.org/10.1128/AAC.03501-14.
62. Liu JH, Pan YS, Yuan L, Wu H, Hu GZ, Chen YX. 2013. Genetic variations in the active efflux pump genes acrA/B and tolC in different drug-induced strains of Escherichia coli CVCC 1547. Genet Mol Res 12: 2829-2836. http://dx.doi.org/10.4238/2013.August.8.3.
63. Bina XR, Provenzano D, Nguyen N, Bina JE. 2008. Vibrio cholerae RND family efflux systems are required for antimicrobial resistance, optimal virulence factor production, and colonization of the infant mouse small intestine. Infect Immun 76:3595-3605. http://dx.doi.org/10.1128/IAI.01620-07.
64. Lindemann A, Koch M, Pessi G, Muller AJ, Balsiger S, Hennecke H, Fischer HM. 2010. Host-specific symbiotic requirement of BdeAB, a RegR-controlled RND-type efflux system in Bradyrhizobium japonicum. FEMS Microbiol Lett 312:184-191. http://dx.doi.org/10.1111/j.1574-6968.2010.02115.x.
65. Piddock LJ. 2006. Multidrug-resistance efflux pumps-not just for resistance. Nat Rev Microbiol 4:629-636. http://dx.doi.org/10.1038/nrmicro1464.
66. Buckley AM, Webber MA, Cooles S, Randall LP, La Ragione RM, Woodward MJ, Piddock LJ. 2006. The AcrAB-TolC efflux system of Salmonella enterica serovar Typhimurium plays a role in pathogenesis. Cell Microbiol 8:847-856. http://dx.doi.org/10.1111/j.1462-5822.2005.00671.x.
67. Jerse AE, Sharma ND, Simms AN, Crow ET, Snyder LA, Shafer WM. 2003. A gonococcal efflux pump system enhances bacterial survival in a female mouse model of genital tract infection. Infect Immun 71:5576-5582. http://dx.doi.org/10.1128/IAI.71.10.5576-5582.2003.
68. Lin J, Sahin O, Michel LO, Zhang Q. 2003. Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infect Immun 71:4250-4259. http://dx.doi.org/10.1128/IAI.71.8.4250-4259.2003.
69. Singh VK, Hattangady DS, Giotis ES, Singh AK, Chamberlain NR, Stuart MK, Wilkinson BJ. 2008. Insertional inactivation of branchedchain alpha-keto acid dehydrogenase in Staphylococcus aureus leads to decreased branched-chain membrane fatty acid content and increased susceptibility to certain stresses. Appl Environ Microbiol 74:5882-5890. http://dx.doi.org/10.1128/AEM.00882-08.
70. Anel A, Naval J, Gonzalez B, Torres JM, Mishal Z, Uriel J, Pineiro A. 1990. Fatty acid metabolism in human lymphocytes. I. Time-course changes in fatty acid composition and membrane fluidity during blastic transformation of peripheral blood lymphocytes. Biochim Biophys Acta 1044:323-331.
71. Yoshikai Y. 2001. Roles of prostaglandins and leukotrienes in acute inflammation caused by bacterial infection. Curr Opin Infect Dis 14:257-263. http://dx.doi.org/10.1097/00001432-200106000-00003.
72. Parsons JB, Frank MW, Subramanian C, Saenkham P, Rock CO. 2011. Metabolic basis for the differential susceptibility of Gram-positive pathogens to fatty acid synthesis inhibitors. Proc Natl Acad Sci U S A 108: 15378-15383. http://dx.doi.org/10.1073/pnas.1109208108.
73. Miller DJ, Zhang YM, Subramanian C, Rock CO, White SW. 2010. Structural basis for the transcriptional regulation of membrane lipid homeostasis. Nat Struct Mol Biol 17:971-975. http://dx.doi.org/10.1038/nsmb.1847.
74. Adebusuyi AA, Foght JM. 2011. An alternative physiological role for the EmhABC efflux pump in Pseudomonas fluorescens cLP6a. BMC Microbiol 11:252. http://dx.doi.org/10.1186/1471-2180-11-252.
75. Cuthbertson L, Nodwell JR. 2013. The TetR family of regulators. Microbiol Mol Biol Rev 77:440-475. http://dx.doi.org/10.1128/MMBR.00018-13.
76. Orth P, Schnappinger D, Hillen W, Saenger W, Hinrichs W. 2000. Structural basis of gene regulation by the tetracycline inducible Tet repressor-operator system. Nat Struct Biol 7:215-219. http://dx.doi.org/10.1038/73324.
77. Fujihashi M, Nakatani T, Hirooka K, Matsuoka H, Fujita Y, Miki K. 2014. Structural characterization of a ligand-bound form of Bacillus subtilis FadR involved in the regulation of fatty acid degradation. Proteins 82:1301-1310. http://dx.doi.org/10.1002/prot.24496.
78. Ramos JL, Martinez-Bueno M, Molina-Henares AJ, Teran W, Watanabe K, Zhang X, Gallegos MT, Brennan R, Tobes R. 2005. The TetR family of transcriptional repressors. Microbiol Mol Biol Rev 69:326-356. http://dx.doi.org/10.1128/MMBR.69.2.326-356.2005.
79. Croxatto A, Chalker VJ, Lauritz J, Jass J, Hardman A, Williams P, Camara M, Milton DL. 2002. VanT, a homologue of Vibrio harveyi LuxR, regulates serine, metalloprotease, pigment, and biofilm production in Vibrio anguillarum. J Bacteriol 184:1617-1629. http://dx.doi.org/10.1128/JB.184.6.1617-1629.2002.
80. Novakova R, Homerova D, Feckova L, Kormanec J. 2005. Characterization of a regulatory gene essential for the production of the angucycline-like polyketide antibiotic auricin in Streptomyces aureofaciens CCM 3239. Microbiology 151:2693-2706. http://dx.doi.org/10.1099/mic.0.28019-0.
81. Lin YH, Miyamoto C, Meighen EA. 2000. Purification and characterization of a luxO promoter binding protein LuxT from Vibrio harveyi. Protein Expr Purif 20:87-94. http://dx.doi.org/10.1006/prep.2000.1285.
82. Kloosterman TG, van der Kooi-Pol MM, Bijlsma JJ, Kuipers OP. 2007. The novel transcriptional regulator SczA mediates protection against Zn2+ stress by activation of the Zn2+-resistance gene czcD in Streptococcus pneumoniae. Mol Microbiol 65:1049-1063. http://dx.doi.org/10.1111/j.1365-2958.2007.05849.x.
83. Christen S, Srinivas A, Bahler P, Zeller A, Pridmore D, Bieniossek C, Baumann U, Erni B. 2006. Regulation of the Dha operon of Lactococcus lactis: a deviation from the rule followed by the TetR family of transcription regulators. J Biol Chem 281:23129-23137. http://dx.doi.org/10.1074/jbc.M603486200.
84. Bratu S, Landman D, George A, Salvani J, Quale J. 2009. Correlation of the expression of acrB and the regulatory genes marA, soxS and ramA with antimicrobial resistance in clinical isolates of Klebsiella pneumoniae endemic to New York City. J Antimicrob Chemother 64:278-283. http://dx.doi.org/10.1093/jac/dkp186.
85. Ruiz C, Levy SB. 2014. Regulation of acrAB expression by cellular metabolites in Escherichia coli. J Antimicrob Chemother 69:390-399. http://dx.doi.org/10.1093/jac/dkt352.
86. Bailey AM, Paulsen IT, Piddock LJ. 2008. RamA confers multidrug resistance in Salmonella enterica via increased expression of acrB, which is inhibited by chlorpromazine. Antimicrob Agents Chemother 52:3604-3611. http://dx.doi.org/10.1128/AAC.00661-08.