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Treponema denticola TroR is a manganese- and iron-dependent transcriptional repressor
dc.contributor.authorBrett, Paul J.en_US
dc.contributor.authorBurtnick, Mary N.en_US
dc.contributor.authorFenno, J. Christopheren_US
dc.contributor.authorGherardini, Frank C.en_US
dc.date.accessioned2010-06-01T19:04:38Z
dc.date.available2010-06-01T19:04:38Z
dc.date.issued2008-10en_US
dc.identifier.citationBrett, Paul J.; Burtnick, Mary N.; Fenno, J. Christopher; Gherardini, Frank C. (2008). " Treponema denticola TroR is a manganese- and iron-dependent transcriptional repressor." Molecular Microbiology 70(2): 396-409. <http://hdl.handle.net/2027.42/72265>en_US
dc.identifier.issn0950-382Xen_US
dc.identifier.issn1365-2958en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/72265
dc.identifier.urihttp://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=18761626&dopt=citationen_US
dc.description.abstractTreponema denticola harbours a genetic locus with significant homology to most of the previously characterized Treponema pallidum tro operon. Within this locus are five genes ( troABCDR ) encoding for the components of an ATP-binding cassette cation-transport system ( troABCD ) and a DtxR-like transcriptional regulator ( troR ). In addition, a σ 70 -like promoter and an 18 bp region of dyad symmetry were identified upstream of the troA start codon. This putative operator sequence demonstrated similarity to the T. pallidum TroR (TroR Tp ) binding sequence; however, the position of this motif with respect to the predicted tro promoters differed. Interestingly, unlike the T. pallidum orthologue, T. denticola TroR (TroR Td ) possesses a C-terminal Src homology 3-like domain commonly associated with DtxR family members. In the present study, we show that TroR Td is a manganese- and iron-dependent transcriptional repressor using Escherichia coli reporter constructs and in T. denticola . In addition, we demonstrate that although TroR Td possessing various C-terminal deletions maintain metal-sensing capacities, these truncated proteins exhibit reduced repressor activities in comparison with full-length TroR Td . Based upon these findings, we propose that TroR Td represents a novel member of the DtxR family of transcriptional regulators and is likely to play an important role in regulating both manganese and iron homeostases in this spirochaete.en_US
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dc.publisherBlackwell Publishing Ltden_US
dc.rightsJournal compilation © 2008 Blackwell Publishingen_US
dc.titleTreponema denticola TroR is a manganese- and iron-dependent transcriptional repressoren_US
dc.typeArticleen_US
dc.subject.hlbsecondlevelMicrobiology and Immunologyen_US
dc.subject.hlbtoplevelScienceen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumBiologic and Materials Sciences, School of Dentistry, University of Michigan, Ann Arbor, MI 48109, USAen_US
dc.contributor.affiliationotherLaboratory of Zoonotic Pathogens, Rocky Mountain Laboratories, NIAID, NIH, Hamilton, MT 59840, USA.en_US
dc.identifier.pmid18761626en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/72265/1/j.1365-2958.2008.06418.x.pdf
dc.identifier.doi10.1111/j.1365-2958.2008.06418.xen_US
dc.identifier.sourceMolecular Microbiologyen_US
dc.identifier.citedreferenceBates, C.S., Toukoki, C., Neely, M.N., and Eichenbaum, Z. ( 2005 ) Characterization of MtsR, a new metal regulator in group A streptococcus, involved in iron acquisition and virulence. Infect Immun 73: 5743 – 5753.en_US
dc.identifier.citedreferenceBlencowe, D.K., and Morby, A.P. ( 2003 ) Zn(II) metabolism in prokaryotes. FEMS Microbiol Rev 27: 291 – 311.en_US
dc.identifier.citedreferenceBraun, V. ( 2003 ) Iron uptake by Escherichia coli. Front Biosci 8: s1409 – s1421.en_US
dc.identifier.citedreferenceBrennan, R.G., and Matthews, B.W. ( 1989 ) The helix-turn-helix DNA binding motif. J Biol Chem 264: 1903 – 1906.en_US
dc.identifier.citedreferenceBrown, J.S., and Holden, D.W. ( 2002 ) Iron acquisition by Gram-positive bacterial pathogens. Microbes Infect 4: 1149 – 1156.en_US
dc.identifier.citedreferenceBurtnick, M.N., Downey, J.S., Brett, P.J., Boylan, J.A., Frye, J.G., Hoover, T.R., and Gherardini, F.C. ( 2007 ) Insights into the complex regulation of rpoS in Borrelia burgdorferi. Mol Microbiol 65: 277 – 293.en_US
dc.identifier.citedreferenceChan, E.C., Siboo, R., Keng, T., Psarra, N., Hurley, R., Cheng, S.L., and Iugovaz, I. ( 1993 ) Treponema denticola (ex Brumpt 1925) sp. nov., nom. rev., and identification of new spirochete isolates from periodontal pockets. Int J Syst Bacteriol 43: 196 – 203.en_US
dc.identifier.citedreferenceChou, C.J., Wisedchaisri, G., Monfeli, R.R., Oram, D.M., Holmes, R.K., Hol, W.G., and Beeson, C. ( 2004 ) Functional studies of the Mycobacterium tuberculosis iron-dependent regulator. J Biol Chem 279: 53554 – 53561.en_US
dc.identifier.citedreferenceChu, L., Kennell, W., and Holt, S.C. ( 1994 ) Characterization of hemolysis and hemoxidation activities by Treponema denticola. Microb Pathog 16: 183 – 195.en_US
dc.identifier.citedreferenceCornelissen, C.N. ( 2003 ) Transferrin-iron uptake by Gram-negative bacteria. Front Biosci 8: d836 – 847.en_US
dc.identifier.citedreferenceD'Aquino, J.A., and Ringe, D. ( 2003 ) Determinants of the SRC homology domain 3-like fold. J Bacteriol 185: 4081 – 4086.en_US
dc.identifier.citedreferenceD'Aquino, J.A., Lattimer, J.R., Denninger, A., D'Aquino, K.E., and Ringe, D. ( 2007 ) Role of the N-terminal helix in the metal ion-induced activation of the diphtheria toxin repressor DtxR. Biochemistry 46: 11761 – 11770.en_US
dc.identifier.citedreferenceDesrosiers, D.C., Sun, Y.C., Zaidi, A.A., Eggers, C.H., Cox, D.L., and Radolf, J.D. ( 2007 ) The general transition metal (Tro) and Zn2+ (Znu) transporters in Treponema pallidum: analysis of metal specificities and expression profiles. Mol Microbiol 65: 137 – 152.en_US
dc.identifier.citedreferenceDing, X., Zeng, H., Schiering, N., Ringe, D., and Murphy, J.R. ( 1996 ) Identification of the primary metal ion-activation sites of the diphtheria tox repressor by X-ray crystallography and site-directed mutational analysis. Nat Struct Biol 3: 382 – 387.en_US
dc.identifier.citedreferenceFaraldo-Gomez, J.D., and Sansom, M.S. ( 2003 ) Acquisition of siderophores in gram-negative bacteria. Nat Rev Mol Cell Biol 4: 105 – 116.en_US
dc.identifier.citedreferenceFerguson, A.D., and Deisenhofer, J. ( 2004 ) Metal import through microbial membranes. Cell 116: 15 – 24.en_US
dc.identifier.citedreferenceFrederick, J.F., Rogers, E.A., and Marconi, R.T. ( 2008 ) Analysis of a growth phase regulated-two component regulatory system in the periodontal pathogen, Treponema denticola. J Bacteriol doi:10.1128/JB.00046-08en_US
dc.identifier.citedreferenceGherardini, F.C., Boylan, J.A., and Brett, P.J. ( 2006 ) Metal utilization and oxidative stress. In Pathogenic Treponema: Molecular and Cellular Biology. Radolf, J.D., and Lukehart, S.A. (eds). Norwich: Caister Academic Press, pp. 101 – 126.en_US
dc.identifier.citedreferenceGlasfeld, A., Guedon, E., Helmann, J.D., and Brennan, R.G. ( 2003 ) Structure of the manganese-bound manganese transport regulator of Bacillus subtilis. Nat Struct Biol 10: 652 – 657.en_US
dc.identifier.citedreferenceGolynskiy, M.V., Davis, T.C., Helmann, J.D., and Cohen, S.M. ( 2005 ) Metal-induced structural organization and stabilization of the metalloregulatory protein MntR. Biochemistry 44: 3380 – 3389.en_US
dc.identifier.citedreferenceGuedon, E., and Helmann, J.D. ( 2003 ) Origins of metal ion selectivity in the DtxR/MntR family of metalloregulators. Mol Microbiol 48: 495 – 506.en_US
dc.identifier.citedreferenceHardham, J.M., Stamm, L.V., Porcella, S.F., Frye, J.G., Barnes, N.Y., Howell, J.K., et al. ( 1997 ) Identification and transcriptional analysis of a Treponema pallidum operon encoding a putative ABC transport system, an iron-activated repressor protein homolog, and a glycolytic pathway enzyme homolog. Gene 197: 47 – 64.en_US
dc.identifier.citedreferenceHazlett, K.R., Rusnak, F., Kehres, D.G., Bearden, S.W., La Vake, C.J., La Vake, M.E., et al. ( 2003 ) The Treponema pallidum tro operon encodes a multiple metal transporter, a zinc-dependent transcriptional repressor, and a semi-autonomously expressed phosphoglycerate mutase. J Biol Chem 278: 20687 – 20694.en_US
dc.identifier.citedreferenceHill, P.J., Cockayne, A., Landers, P., Morrissey, J.A., Sims, C.M., and Williams, P. ( 1998 ) SirR, a novel iron-dependent repressor in Staphylococcus epidermidis. Infect Immun 66: 4123 – 4129.en_US
dc.identifier.citedreferenceIkeda, J.S., Janakiraman, A., Kehres, D.G., Maguire, M.E., and Slauch, J.M. ( 2005 ) Transcriptional regulation of sitABCD of Salmonella enterica serovar Typhimurium by MntR and Fur. J Bacteriol 187: 912 – 922.en_US
dc.identifier.citedreferenceJakubovics, N.S., and Jenkinson, H.F. ( 2001 ) Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria. Microbiology 147: 1709 – 1718.en_US
dc.identifier.citedreferenceKaplan, J. ( 2002 ) Mechanisms of cellular iron acquisition: another iron in the fire. Cell 111: 603 – 606.en_US
dc.identifier.citedreferenceKehres, D.G., and Maguire, M.E. ( 2003 ) Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria. FEMS Microbiol Rev 27: 263 – 290.en_US
dc.identifier.citedreferenceLoesche, W.J., and Grossman, N.S. ( 2001 ) Periodontal disease as a specific, albeit chronic, infection: diagnosis and treatment. Clin Microbiol Rev 14: 727 – 752. Table of contents.en_US
dc.identifier.citedreferenceLove, J.F., VanderSpek, J.C., and Murphy, J.R. ( 2003 ) The src homology 3-like domain of the diphtheria toxin repressor (DtxR) modulates repressor activation through interaction with the ancillary metal ion-binding site. J Bacteriol 185: 2251 – 2258.en_US
dc.identifier.citedreferenceMiller, J.H. ( 1972 ) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.en_US
dc.identifier.citedreferenceMulrooney, S.B., and Hausinger, R.P. ( 2003 ) Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev 27: 239 – 261.en_US
dc.identifier.citedreferenceNikaido, H., and Saier, M.H., Jr ( 1992 ) Transport proteins in bacteria: common themes in their design. Science 258: 936 – 942.en_US
dc.identifier.citedreferenceOutten, C.E., and O'Halloran, T.V. ( 2001 ) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292: 2488 – 2492.en_US
dc.identifier.citedreferencePaster, B.J., Boches, S.K., Galvin, J.L., Ericson, R.E., Lau, C.N., Levanos, V.A., et al. ( 2001 ) Bacterial diversity in human subgingival plaque. J Bacteriol 183: 3770 – 3783.en_US
dc.identifier.citedreferencePatzer, S.I., and Hantke, K. ( 2001 ) Dual repression by Fe(2+)-Fur and Mn(2+)-MntR of the mntH gene, encoding an NRAMP-like Mn(2+) transporter in Escherichia coli. J Bacteriol 183: 4806 – 4813.en_US
dc.identifier.citedreferencePennella, M.A., and Giedroc, D.P. ( 2005 ) Structural determinants of metal selectivity in prokaryotic metal-responsive transcriptional regulators. Biometals 18: 413 – 428.en_US
dc.identifier.citedreferencePosey, J.E., and Gherardini, F.C. ( 2000 ) Lack of a role for iron in the Lyme disease pathogen. Science 288: 1651 – 1653.en_US
dc.identifier.citedreferencePosey, J.E., Hardham, J.M., Norris, S.J., and Gherardini, F.C. ( 1999 ) Characterization of a manganese-dependent regulatory protein, TroR, from Treponema pallidum. Proc Natl Acad Sci USA 96: 10887 – 10892.en_US
dc.identifier.citedreferenceQiu, X., Verlinde, C.L., Zhang, S., Schmitt, M.P., Holmes, R.K., and Hol, W.G. ( 1995 ) Three-dimensional structure of the diphtheria toxin repressor in complex with divalent cation co-repressors. Structure 3: 87 – 100.en_US
dc.identifier.citedreferenceRatledge, C., and Dover, L.G. ( 2000 ) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54: 881 – 941.en_US
dc.identifier.citedreferenceRensing, C., and Grass, G. ( 2003 ) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27: 197 – 213.en_US
dc.identifier.citedreferenceSatcher, D.S. ( 2000 ) Surgeon General's report on oral health. Public Health Rep 115: 489 – 490.en_US
dc.identifier.citedreferenceSchiering, N., Tao, X., Zeng, H., Murphy, J.R., Petsko, G.A., and Ringe, D. ( 1995 ) Structures of the apo- and the metal ion-activated forms of the diphtheria tox repressor from Corynebacterium diphtheriae. Proc Natl Acad Sci USA 92: 9843 – 9850.en_US
dc.identifier.citedreferenceSchmitt, M.P. ( 1999 ) Identification of a two-component signal transduction system from Corynebacterium diphtheriae that activates gene expression in response to the presence of heme and hemoglobin. J Bacteriol 181: 5330 – 5340.en_US
dc.identifier.citedreferenceScott, D., Siboo, I.R., Chan, E.C., Klitorinos, A., and Siboo, R. ( 1993 ) Binding of hemin and congo red by oral hemolytic spirochetes. Oral Microbiol Immunol 8: 245 – 250.en_US
dc.identifier.citedreferenceSela, M.N. ( 2001 ) Role of Treponema denticola in periodontal diseases. Crit Rev Oral Biol Med 12: 399 – 413.en_US
dc.identifier.citedreferenceSeshadri, R., Myers, G.S., Tettelin, H., Eisen, J.A., Heidelberg, J.F., Dodson, R.J., et al. ( 2004 ) Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc Natl Acad Sci USA 101: 5646 – 5651.en_US
dc.identifier.citedreferenceSocransky, S.S., Haffajee, A.D., Cugini, M.A., Smith, C., and Kent, R.L., Jr ( 1998 ) Microbial complexes in subgingival plaque. J Clin Periodontol 25: 134 – 144.en_US
dc.identifier.citedreferenceTao, X., Schiering, N., Zeng, H.Y., Ringe, D., and Murphy, J.R. ( 1994 ) Iron, DtxR, and the regulation of diphtheria toxin expression. Mol Microbiol 14: 191 – 197.en_US
dc.identifier.citedreferenceTao, X., Zeng, H.Y., and Murphy, J.R. ( 1995 ) Transition metal ion activation of DNA binding by the diphtheria tox repressor requires the formation of stable homodimers. Proc Natl Acad Sci USA 92: 6803 – 6807.en_US
dc.identifier.citedreferenceXu, X., and Kolodrubetz, D. ( 2002 ) Construction and analysis of hemin binding protein mutants in the oral pathogen Treponema denticola. Res Microbiol 153: 569 – 577.en_US
dc.identifier.citedreferenceXu, X., Holt, S.C., and Kolodrubetz, D. ( 2001 ) Cloning and expression of two novel hemin binding protein genes from Treponema denticola. Infect Immun 69: 4465 – 4472.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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