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Abstract:

Among the biologically required first row, late d-block metals from MnII to ZnII, the catalytic and structural reach of ZnII ensures that this essential micronutrient touches nearly every major metabolic process or pathway in the cell. Zn is also toxic in excess, primarily because it is a highly competitive divalent metal and will displace more weakly bound transition metals in the active sites of metalloenzymes if left unregulated. The vertebrate innate immune system uses several strategies to exploit this "Achilles heel" of microbial physiology, but bacterial evolution has responded in kind. This review highlights recent insights into transcriptional, transport, and trafficking mechanisms that pathogens use to "win the fight" over zinc and thrive in an otherwise hostile environment. © 2016 by The American Society for Biochemistry and Molecular Biology, Inc.

Registro:

Documento: Artículo
Título:Bacterial strategies to maintain zinc metallostasis at the host-pathogen interface
Autor:Capdevila, D.A.; Wang, J.; Giedroc, D.P.
Filiación:Dept. of Chemistry, Indiana University, 800 E. Kirkwood Ave., Bloomington, IN 47405-7102, United States
Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, IN 47405-7102, United States
Departamento de Quimica Inorganica, Analitica y Quimica Fisica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, C1428EHA, Argentina
Palabras clave:Manganese; Pathogens; Structural metals; Transition metals; Zinc; Achilles heel; Bacterial evolution; Divalent metals; Hostile environments; Innate immune systems; Metabolic process; Metalloenzymes; Microbial physiology; Metals; bacillithiol; cyanocobalamin; glutathione; reactive oxygen metabolite; RNA polymerase; siderophore; thiol derivative; unclassified drug; zinc ion; zinc; Acinetobacter baumannii; allostasis; allosterism; Bacillus subtilis; bacterial outer membrane; bacterial strain; bioavailability; carboxy terminal sequence; cation transport; cytoplasm; DNA binding; Escherichia coli; host pathogen interaction; hydrolysis; in vivo study; molecular recognition; Mycobacterium tuberculosis; nonhuman; priority journal; Salmonella enterica; Shigella sonnei; Short Survey; Staphylococcus aureus; Streptococcus pneumoniae; Streptomyces coelicolor; transcription regulation; zinc efflux; zinc homeostasis; zinc metallostasis; zinc uptake; animal; bacterial phenomena and functions; bacterium; host pathogen interaction; human; metabolism; physiology; Animals; Bacteria; Bacterial Physiological Phenomena; Host-Pathogen Interactions; Humans; Zinc
Año:2016
Volumen:291
Número:40
Página de inicio:20858
Página de fin:20868
DOI: http://dx.doi.org/10.1074/jbc.R116.742023
Título revista:Journal of Biological Chemistry
Título revista abreviado:J. Biol. Chem.
ISSN:00219258
CODEN:JBCHA
CAS:cyanocobalamin, 53570-76-6, 68-19-9, 8064-09-3; glutathione, 70-18-8; RNA polymerase, 9014-24-8; thiol derivative, 13940-21-1; zinc ion, 23713-49-7; zinc, 7440-66-6, 14378-32-6; Zinc
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00219258_v291_n40_p20858_Capdevila

Referencias:

  • Andreini, C., Banci, L., Bertini, I., Rosato, A., Counting the zinc-proteins encoded in the human genome (2006) J. Proteome Res., 5, pp. 196-201
  • Outten, C.E., O'Halloran, T.V., Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis (2001) Science, 292, pp. 2488-2492
  • Begg, S.L., Eijkelkamp, B.A., Luo, Z., Couñago, R.M., Morey, J.R., Maher, M.J., Ong, C.L., McDevitt, C.A., Dysregulation of transition metal ion homeostasis is the molecular basis for cadmium toxicity in Streptococcus pneumoniae (2015) Nat. Commun., 6, p. 6418
  • Jacobsen, F.E., Kazmierczak, K.M., Lisher, J.P., Winkler, M.E., Giedroc, D.P., Interplay between manganese and zinc homeostasis in the human pathogen Streptococcus pneumoniae (2011) Metallomics, 3, pp. 38-41
  • Weinberg, E.D., Nutritional immunity. Host's attempt to withold iron from microbial invaders (1975) JAMA, 231, pp. 39-41
  • Corbin, B.D., Seeley, E.H., Raab, A., Feldmann, J., Miller, M.R., Torres, V.J., Anderson, K.L., Skaar, E.P., Metal chelation and inhibition of bacterial growth in tissue abscesses (2008) Science, 319, pp. 962-965
  • Kehl-Fie, T.E., Skaar, E.P., Nutritional immunity beyond iron: A role for manganese and zinc (2010) Curr. Opin. Chem. Biol., 14, pp. 218-224
  • Ong, C.L., Gillen, C.M., Barnett, T.C., Walker, M.J., McEwan, A.G., An antimicrobial role for zinc in innate immune defense against group A streptococcus (2014) J. Infect. Dis., 209, pp. 1500-1508
  • Neyrolles, O., Mintz, E., Catty, P., Zinc and copper toxicity in host defense against pathogens: Mycobacterium tuberculosis as a model example of an emerging paradigm (2013) Front Cell Infect. Microbiol., 3, p. 89
  • Hood, M.I., Mortensen, B.L., Moore, J.L., Zhang, Y., Kehl-Fie, T.E., Sugitani, N., Chazin, W.J., Skaar, E.P., Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration (2012) PLoS Pathog, 8
  • Damo, S.M., Kehl-Fie, T.E., Sugitani, N., Holt, M.E., Rathi, S., Murphy, W.J., Zhang, Y., Chazin, W.J., Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens (2013) Proc. Natl. Acad. Sci. U.S.A., 110, pp. 3841-3846
  • Gagnon, D.M., Brophy, M.B., Bowman, S.E., Stich, T.A., Drennan, C.L., Britt, R.D., Nolan, E.M., Manganese binding properties of human calprotectin under conditions of high and low calcium: X-ray crystallographic and advanced electron paramagnetic resonance spectroscopic analysis (2015) J. Am. Chem. Soc., 137, pp. 3004-3016
  • Stephan, J.R., Nolan, E.M., Calcium-induced tetramerization and zinc chelation shield human calprotectin from degradation by host and bacterial extracellular proteases (2016) Chem. Sci., 7, pp. 1962-1975
  • Nakashige, T.G., Zhang, B., Krebs, C., Nolan, E.M., Human calprotectin is an iron-sequestering host-defense protein (2015) Nat. Chem. Biol., 11, pp. 765-771
  • Haley, K.P., Delgado, A.G., Piazuelo, M.B., Mortensen, B.L., Correa, P., Damo, S.M., Chazin, W.J., Gaddy, J.A., The human antimicrobial protein calgranulin C participates in control of Helicobacter pylori growth and regulation of virulence (2015) Infect. Immun., 83, pp. 2944-2956
  • Cunden, L.S., Gaillard, A., Nolan, E.M., Calcium ions tune the zinc-sequestering properties and antimicrobial activity of human S100A12 (2016) Chem. Sci., 7, pp. 1338-1348
  • Reyes-Caballero, H., Campanello, G.C., Giedroc, D.P., Metalloregulatory proteins: Metal selectivity and allosteric switching (2011) Biophys. Chem., 156, pp. 103-114
  • Foster, A.W., Patterson, C.J., Pernil, R., Hess, C.R., Robinson, N.J., Cytosolic Ni(II) sensor in cyanobacterium: Nickel detection follows nickel affinity across four families of metal sensors (2012) J. Biol. Chem., 287, pp. 12142-12151
  • Foster, A.W., Osman, D., Robinson, N.J., Metal preferences and metallation (2014) J. Biol. Chem., 289, pp. 28095-28103
  • Waldron, K.J., Rutherford, J.C., Ford, D., Robinson, N.J., Metalloproteins and metal sensing (2009) Nature, 460, pp. 823-830
  • Osman, D., Piergentili, C., Chen, J., Chakrabarti, B., Foster, A.W., Lurie-Luke, E., Huggins, T.G., Robinson, N.J., Generating a metal-responsive transcriptional regulator to test what confers metal sensing in cells (2015) J. Biol. Chem., 290, pp. 19806-19822
  • Gilston, B.A., Wang, S., Marcus, M.D., Canalizo-Hernández, M.A., Swindell, E.P., Xue, Y., Mondragón, A., O'Halloran, T.V., Structural and mechanistic basis of zinc regulation across the E. coli Zur regulon (2014) PLoS Biol., 12
  • Philips, S.J., Canalizo-Hernandez, M., Yildirim, I., Schatz, G.C., Mondragón, A., O'Halloran, T.V., Allosteric transcriptional regulation via changes in the overall topology of the core promoter (2015) Science, 349, pp. 877-881
  • Ma, Z., Jacobsen, F.E., Giedroc, D.P., Coordination chemistry of bacterial metal transport and sensing (2009) Chem. Rev., 109, pp. 4644-4681
  • Kloosterman, T.G., Van Der Kooi-Pol, M.M., Bijlsma, J.J., Kuipers, O.P., The novel transcriptional regulator SczA mediates protection against Zn2+ stress by activation of the Zn2+-resistance gene czcD in Streptococcus pneumoniae (2007) Mol. Microbiol., 65, pp. 1049-1063
  • Giedroc, D.P., Arunkumar, A.I., Metal sensor proteins: Nature's metalloregulated allosteric switches (2007) Dalton Trans, 29, pp. 3107-3120
  • Waldron, K.J., Robinson, N.J., How do bacterial cells ensure that metalloproteins get the correct metal? (2009) Nat. Rev. Microbiol., 7, pp. 25-35
  • Pennella, M.A., Shokes, J.E., Cosper, N.J., Scott, R.A., Giedroc, D.P., Structural elements of metal selectivity in metal sensor proteins (2003) Proc. Natl. Acad. Sci. U.S.A., 100, pp. 3713-3718
  • Ma, Z., Gabriel, S.E., Helmann, J.D., Sequential binding and sensing of Zn(II) by Bacillus subtilis Zur (2011) Nucleic Acids Res., 39, pp. 9130-9138
  • Ma, Z., Faulkner, M.J., Helmann, J.D., Origins of specificity and cross-talk in metal ion sensing by Bacillus subtilis Fur (2012) Mol. Microbiol., 86, pp. 1144-1155
  • Eicken, C., Pennella, M.A., Chen, X., Koshlap, K.M., VanZile, M.L., Sacchettini, J.C., Giedroc, D.P., A metal-ligand-mediated intersubunit allosteric switch in related SmtB/ArsR zinc sensor proteins (2003) J. Mol. Biol., 333, pp. 683-695
  • Arunkumar, A.I., Campanello, G.C., Giedroc, D.P., Solution structure of a paradigm ArsR family zinc sensor in the DNA-bound state (2009) Proc. Natl. Acad. Sci. U.S.A., 106, pp. 18177-18182
  • Shin, J.-H., Jung, H.J., An, Y.J., Cho, Y.-B., Cha, S.-S., Roe, J.-H., Graded expression of zinc-responsive genes through two regulatory zinc-binding sites in Zur (2011) Proc. Natl. Acad. Sci. U.S.A., 108, pp. 5045-5050
  • Guerra, A.J., Dann, C.E., 3rd, Giedroc, D.P., Crystal structure of the zinc-dependent MarR family transcriptional regulator AdcR in the Zn(II)-bound state (2011) J. Am. Chem. Soc., 133, pp. 19614-19617
  • Sanson, M., Makthal, N., Flores, A.R., Olsen, R.J., Musser, J.M., Kumaraswami, M., Adhesin competence repressor (AdcR) from Streptococcus pyogenes controls adaptive responses to zinc limitation and contributes to virulence (2015) Nucleic Acids Res., 43, pp. 418-432
  • Reyes-Caballero, H., Guerra, A.J., Jacobsen, F.E., Kazmierczak, K.M., Cowart, D., Koppolu, U.M., Scott, R.A., Giedroc, D.P., The metalloregulatory zinc site in Streptococcus pneumoniae AdcR, a zinc-activated MarR family repressor (2010) J. Mol. Biol., 403, pp. 197-216
  • Wang, K., Sitsel, O., Meloni, G., Autzen, H.E., Andersson, M., Klymchuk, T., Nielsen, A.M., Gourdon, P., Structure and mechanism of Zn2+-transporting P-type ATPases (2014) Nature, 514, pp. 518-522
  • Lu, M., Fu, D., Structure of the zinc transporter YiiP (2007) Science, 317, pp. 1746-1748
  • Gupta, S., Chai, J., Cheng, J., D'Mello, R., Chance, M.R., Fu, D., Visualizing the kinetic power stroke that drives proton-coupled zinc(II) transport (2014) Nature, 512, pp. 101-104
  • Cerasi, M., Liu, J.Z., Ammendola, S., Poe, A.J., Petrarca, P., Pesciaroli, M., Pasquali, P., Battistoni, A., The ZupT transporter plays an important role in zinc homeostasis and contributes to Salmonella enterica virulence (2014) Metallomics, 6, pp. 845-853
  • Sheng, Y., Fan, F., Jensen, O., Zhong, Z., Kan, B., Wang, H., Zhu, J., Dual zinc transporter systems in Vibrio cholerae promote competitive advantages over gut microbiome (2015) Infect. Immun., 83, pp. 3902-3908
  • Botella, H., Peyron, P., Levillain, F., Poincloux, R., Poquet, Y., Brandli, I., Wang, C., Maridonneau-Parini, I., Mycobacterial P1-type ATPases mediate resistance to zinc poisoning in human macrophages (2011) Cell Host Microbe, 10, pp. 248-259
  • Nairn, B.L., Lonergan, Z.R., Wang, J., Braymer, J.J., Zhang, Y., Calcutt, M.W., Lisher, J.P., Skaar, E.P., The response of Acinetobacter baumannii to zinc starvation (2016) Cell Host Microbe, 19, pp. 826-836
  • Grass, G., Fan, B., Rosen, B.P., Franke, S., Nies, D.H., Rensing, C., ZitB (YbgR), a member of the cation diffusion facilitator family, is an additional zinc transporter in Escherichia coli (2001) J. Bacteriol., 183, pp. 4664-4667
  • Blindauer, C.A., Advances in the molecular understanding of biological zinc transport (2015) Chem. Comm., 51, pp. 4544-4563
  • Kolaj-Robin, O., Russell, D., Hayes, K.A., Pembroke, J.T., Soulimane, T., Cation diffusion facilitator family: Structure and function (2015) FEBS Lett., 589, pp. 1283-1295
  • Grass, G., Otto, M., Fricke, B., Haney, C.J., Rensing, C., Nies, D.H., Munkelt, D., FieF (YiiP) from Escherichia coli mediates decreased cellular accumulation of iron and relieves iron stress (2005) Arch. Microbiol., 183, pp. 9-18
  • Coudray, N., Valvo, S., Hu, M., Lasala, R., Kim, C., Vink, M., Zhou, M., Stokes, D.L., Inward-facing conformation of the zinc transporter YiiP revealed by cryoelectron microscopy (2013) Proc. Natl. Acad. Sci. U.S.A., 110, pp. 2140-2145
  • Zogzas, C.E., Aschner, M., Mukhopadhyay, S., Structural elements in the transmembrane and cytoplasmic domains of the metal transporter SLC30A10 are required for its manganese efflux activity (2016) J. Biol. Chem., 291, pp. 15940-15957
  • Martin, J.E., Giedroc, D.P., Functional determinants of metal ion transport and selectivity in paralogous cation diffusion facilitator transporters CzcD and MntE in Streptococcus pneumoniae (2016) J. Bacteriol., 198, pp. 1066-1076
  • Nishito, Y., Tsuji, N., Fujishiro, H., Takeda, T.A., Yamazaki, T., Teranishi, F., Okazaki, F., Kambe, T., Direct comparison of manganese detoxification/efflux proteins and molecular characterization of ZnT10 as a manganese transporter (2016) J. Biol. Chem., 291, pp. 14773-14787
  • Quadri, M., Federico, A., Zhao, T., Breedveld, G.J., Battisti, C., Delnooz, C., Severijnen, L.A., Willemsen, R., Mutations in SLC30A10 cause parkinsonism and dystonia with hypermanganesemia, polycythemia, and chronic liver disease (2012) Am. J. Hum. Genet., 90, pp. 467-477
  • Strausak, D., Solioz, M., CopY is a copper-inducible repressor of the Enterococcus hirae copper ATPases (1997) J. Biol. Chem., 272, pp. 8932-8936
  • Raimunda, D., Long, J.E., Padilla-Benavides, T., Sassetti, C.M., Argüello, J.M., Differential roles for the Co2+/Ni2+ transporting ATPases, CtpD and CtpJ, in Mycobacterium tuberculosis virulence (2014) Mol. Microbiol., 91, pp. 185-197
  • Guan, G., Pinochet-Barros, A., Gaballa, A., Patel, S.J., Argüello, J.M., Helmann, J.D., PfeT, a P-type ATPase, effluxes ferrous iron and protects Bacillus subtilis against iron intoxication (2015) Mol. Microbiol., 98, pp. 787-803
  • Padilla-Benavides, T., Long, J.E., Raimunda, D., Sassetti, C.M., Argüello, J.M., A novel P1B-type Mn2+-transporting ATPase is required for secreted protein metallation in mycobacteria (2013) J. Biol. Chem., 288, pp. 11334-11347
  • Sharma, R., Rensing, C., Rosen, B.P., Mitra, B., The ATP hydrolytic activity of purified ZntA, a Pb(II)/Cd(II)/Zn(II)-translocating AT-Pase from. Escherichia coli (2000) J. Biol. Chem., 275, pp. 3873-3878
  • Rensing, C., Fan, B., Sharma, R., Mitra, B., Rosen, B.P., CopA: An Escherichia coli Cu(I)-translocating P-type ATPase (2000) Proc. Natl. Acad. Sci. U.S.A., 97, pp. 652-656
  • Hou, Z., Mitra, B., The metal specificity and selectivity of ZntA from Escherichia coli using the acylphosphate intermediate (2003) J. Biol. Chem., 278, pp. 28455-28461
  • Raimunda, D., Subramanian, P., Stemmler, T., Argüello, J.M., A tetrahedral coordination of zinc during transmembrane transport by P-type Zn2+-ATPases (2012) Biochim. Biophys. Acta, 1818, pp. 1374-1377
  • González-Guerrero, M., Eren, E., Rawat, S., Stemmler, T.L., Argüello, J.M., Structure of the two transmembrane Cu+ transport sites of the Cu+-ATPases (2008) J. Biol. Chem., 283, pp. 29753-29759
  • Gourdon, P., Liu, X.Y., Skjørringe, T., Morth, J.P., Møller, L.B., Pedersen, B.P., Nissen, P., Crystal structure of a copper-transporting PIB-type ATPase (2011) Nature, 475, pp. 59-64
  • Mattle, D., Zhang, L., Sitsel, O., Pedersen, L.T., Moncelli, M.R., Tadini-Buoninsegni, F., Gourdon, P., Meloni, G., A sulfur-based transport pathway in Cu+-ATPases (2015) EMBO Rep., 16, pp. 728-740
  • Couñago, R.M., Ween, M.P., Begg, S.L., Bajaj, M., Zuegg, J., O'Mara, M.L., Cooper, M.A., McDevitt, C.A., Imperfect coordination chemistry facilitates metal ion release in the Psa permease (2014) Nat. Chem. Biol., 10, pp. 35-41
  • Pederick, V.G., Eijkelkamp, B.A., Begg, S.L., Ween, M.P., McAllister, L.J., Paton, J.C., McDevitt, C.A., ZnuA and zinc homeostasis in Pseudomonas aeruginosa (2015) Sci. Rep., 5, p. 13139
  • Hollenstein, K., Frei, D.C., Locher, K.P., Structure of an ABC transporter in complex with its binding protein (2007) Nature, 446, pp. 213-216
  • Pinkett, H.W., Lee, A.T., Lum, P., Locher, K.P., Rees, D.C., An inward-facing conformation of a putative metal-chelate-type ABC transporter (2007) Science, 315, pp. 373-377
  • Ilari, A., Pescatori, L., Di Santo, R., Battistoni, A., Ammendola, S., Falconi, M., Berlutti, F., Chiancone, E., Salmonella enterica serovar Typhimurium growth is inhibited by the concomitant binding of Zn(II) and a pyrrolyl-hydroxamate to ZnuA, the soluble component of the ZnuABC transporter (1860) Biochim. Biophys. Acta, 2016, pp. 534-541
  • Petrarca, P., Ammendola, S., Pasquali, P., Battistoni, A., The Zur-regulated ZinT protein is an auxiliary component of the high-affinity ZnuABC zinc transporter that facilitates metal recruitment during severe zinc shortage (2010) J. Bacteriol., 192, pp. 1553-1564
  • Bersch, B., Bougault, C., Roux, L., Favier, A., Vernet, T., Durmort, C., New insights into histidine triad proteins: Solution structure of a Streptococcus pneumoniae PhtD domain and zinc transfer to AdcAII (2013) PLoS ONE, 8
  • Handali, M., Roychowdhury, H., Neupane, D.P., Yukl, E.T., AztD, a periplasmic zinc metallochaperone to an ATP-binding cassette (ABC) transporter system in Paracoccus denitrificans (2015) J. Biol. Chem., 290, pp. 29984-29992
  • Calmettes, C., Ing, C., Buckwalter, C.M., El Bakkouri, M., Chieh-Lin Lai, C., Pogoutse, A., Gray-Owen, S.D., Moraes, T.F., The molecular mechanism of zinc acquisition by the neisserial outer-membrane transporter ZnuD (2015) Nat. Commun., 6, p. 7996
  • Stork, M., Grijpstra, J., Bos, M.P., Mañas Torres, C., Devos, N., Poolman, J.T., Chazin, W.J., Tommassen, J., Zinc piracy as a mechanism of Neisseria meningitidis for evasion of nutritional immunity (2013) PLoS Pathog., 9
  • Noinaj, N., Easley, N.C., Oke, M., Mizuno, N., Gumbart, J., Boura, E., Steere, A.N., Buchanan, S.K., Structural basis for iron piracy by pathogenic Neisseria (2012) Nature, 483, pp. 53-58
  • Johnstone, T.C., Nolan, E.M., Beyond iron: Non-classical biological functions of bacterial siderophores (2015) Dalton Trans., 44, pp. 6320-6339
  • Chaturvedi, K.S., Hung, C.S., Crowley, J.R., Stapleton, A.E., Henderson, J.P., The siderophore yersiniabactin binds copper to protect pathogens during infection (2012) Nat. Chem. Biol., 8, pp. 731-736
  • Ghssein, G., Brutesco, C., Ouerdane, L., Fojcik, C., Izaute, A., Wang, S., Hajjar, C., Arnoux, P., Biosynthesis of a broad-spectrum nicotianamine-like metallophore in Staphylococcus aureus (2016) Science, 352, pp. 1105-1109
  • Nanamiya, H., Akanuma, G., Natori, Y., Murayama, R., Kosono, S., Kudo, T., Kobayashi, K., Kawamura, F., Zinc is a key factor in controlling alternation of two types of L31 protein in the Bacillus subtilis ribosome (2004) Mol. Microbiol., 52, pp. 273-283
  • Gabriel, S.E., Helmann, J.D., Contributions of Zur-controlled ribosomal proteins to growth under zinc starvation conditions (2009) J. Bacteriol., 191, pp. 6116-6122
  • Panina, E.M., Mironov, A.A., Gelfand, M.S., Comparative genomics of bacterial zinc regulons: Enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins (2003) Proc. Natl. Acad. Sci. U.S.A., 100, pp. 9912-9917
  • Napolitano, M., Rubio, M.Á., Santamaría-Gómez, J., Olmedo-Verd, E., Robinson, N.J., Luque, I., Characterization of the response to zinc deficiency in the cyanobacterium Anabaena sp. strain PCC 7120 (2012) J. Bacteriol., 194, pp. 2426-2436
  • Sankaran, B., Bonnett, S.A., Shah, K., Gabriel, S., Reddy, R., Schimmel, P., Rodionov, D.A., Swairjo, M.A., Zinc-independent folate biosynthesis: Genetic, biochemical, and structural investigations reveal new metal dependence for GTP cyclohydrolase IB (2009) J. Bacteriol., 191, pp. 6936-6949
  • Jaffe, E.K., An unusual phylogenetic variation in the metal ion binding sites of porphobilinogen synthase (2003) Chem. Biol., 10, pp. 25-34
  • Blaby-Haas, C.E., Furman, R., Rodionov, D.A., Artsimovitch, I., De Crécy-Lagard, V., Role of a Zn-independent DksA in Zn homeostasis and stringent response (2011) Mol. Microbiol., 79, pp. 700-715
  • Rae, T.D., Schmidt, P.J., Pufahl, R.A., Culotta, V.C., O'Halloran, T.V., Undetectable intracellular free copper: The requirement of a copper chaperone for superoxide dismutase (1999) Science, 284, pp. 805-808
  • Gabriel, S.E., Miyagi, F., Gaballa, A., Helmann, J.D., Regulation of the Bacillus subtilis yciC gene and insights into the DNA-binding specificity of the zinc-sensing metalloregulator Zur (2008) J. Bacteriol., 190, pp. 3482-3488
  • Haas, C.E., Rodionov, D.A., Kropat, J., Malasarn, D., Merchant, S.S., De Crécy-Lagard, V., A subset of the diverse COG0523 family of putative metal chaperones is linked to zinc homeostasis in all kingdoms of life (2009) BMC Genomics, 10, p. 470
  • Farrugia, M.A., Macomber, L., Hausinger, R.P., Biosynthesis of the urease metallocenter (2013) J. Biol. Chem., 288, pp. 13178-13185
  • Lacasse, M.J., Zamble, D.B., [NiFe]-Hydrogenase maturation (2016) Biochemistry, 55, pp. 1689-1701
  • Padovani, D., Banerjee, R., AG-protein editor gates coenzyme B12 loading and is corrupted in methylmalonic aciduria (2009) Proc. Natl. Acad. Sci. U.S.A., 106, pp. 21567-21572
  • Blaby-Haas, C.E., Flood, J.A., De Crécy-Lagard, V., Zamble, D.B., YeiR: A metal-binding GTPase from Escherichia coli involved in metal homeostasis (2012) Metallomics, 4, pp. 488-497
  • Osman, D., Cavet, J.S., Metal sensing in Salmonella: Implications for pathogenesis (2011) Adv. Microb. Physiol., 58, pp. 175-232
  • Helbig, K., Bleuel, C., Krauss, G.J., Nies, D.H., Glutathione and transition-metal homeostasis in Escherichia coli (2008) J. Bacteriol., 190, pp. 5431-5438
  • Ma, Z., Chandrangsu, P., Helmann, T.C., Romsang, A., Gaballa, A., Helmann, J.D., Bacillithiol is a major buffer of the labile zinc pool in Bacillus subtilis (2014) Mol. Microbiol., 94, pp. 756-770
  • Newton, G.L., Rawat, M., La Clair, J.J., Jothivasan, V.K., Budiarto, T., Hamilton, C.J., Claiborne, A., Fahey, R.C., Bacillithiol is an antioxidant thiol produced in Bacilli (2009) Nat. Chem. Biol., 5, pp. 625-627
  • Murphy, J.T., Bruinsma, J.J., Schneider, D.L., Collier, S., Guthrie, J., Chinwalla, A., Robertson, J.D., Kornfeld, K., Histidine protects against zinc and nickel toxicity in Caenorhabditis elegans (2011) PLoS Genet., 7
  • Blindauer, C.A., Harrison, M.D., Robinson, A.K., Parkinson, J.A., Bowness, P.W., Sadler, P.J., Robinson, N.J., Multiple bacteria encode metallothioneins and SmtA-like zinc fingers (2002) Mol. Microbiol., 45, pp. 1421-1432
  • Maret, W., Krezel, A., Cellular zinc and redox buffering capacity of metallothionein/thionein in health and disease (2007) Mol. Med., 13, pp. 371-375
  • Gaballa, A., Newton, G.L., Antelmann, H., Parsonage, D., Upton, H., Rawat, M., Claiborne, A., Helmann, J.D., Biosynthesis and functions of bacillithiol, a major low-molecular-weight thiol in Bacilli (2010) Proc. Natl. Acad. Sci. U.S.A., 107, pp. 6482-6486

Citas:

---------- APA ----------
Capdevila, D.A., Wang, J. & Giedroc, D.P. (2016) . Bacterial strategies to maintain zinc metallostasis at the host-pathogen interface. Journal of Biological Chemistry, 291(40), 20858-20868.
http://dx.doi.org/10.1074/jbc.R116.742023
---------- CHICAGO ----------
Capdevila, D.A., Wang, J., Giedroc, D.P. "Bacterial strategies to maintain zinc metallostasis at the host-pathogen interface" . Journal of Biological Chemistry 291, no. 40 (2016) : 20858-20868.
http://dx.doi.org/10.1074/jbc.R116.742023
---------- MLA ----------
Capdevila, D.A., Wang, J., Giedroc, D.P. "Bacterial strategies to maintain zinc metallostasis at the host-pathogen interface" . Journal of Biological Chemistry, vol. 291, no. 40, 2016, pp. 20858-20868.
http://dx.doi.org/10.1074/jbc.R116.742023
---------- VANCOUVER ----------
Capdevila, D.A., Wang, J., Giedroc, D.P. Bacterial strategies to maintain zinc metallostasis at the host-pathogen interface. J. Biol. Chem. 2016;291(40):20858-20868.
http://dx.doi.org/10.1074/jbc.R116.742023