Role of a Zn-independent DksA in Zn homeostasis and stringent response

Molecular Microbiology

Volumn 79, Issue 3, 2011, Pages 700-715

  Blaby Haas, Crysten E ^a   Furman, Ran ^b   Rodionov, Dmitry A ^c,d   Artsimovitch, Irina ^b   De Crécy Lagard, Valérie ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c BURNHAM INSTITUTE   (United States)

^d INSTITUTE FOR INFORMATION TRANSMISSION PROBLEMS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DKSA; TRANSCRIPTION FACTOR DKSA2; TRANSCRIPTION FACTOR ZUR; UNCLASSIFIED DRUG; ZINC;

ARTICLE; BACTERIAL GROWTH; BINDING SITE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; HOMEOSTASIS; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROMOTER REGION; PSEUDOMONAS AERUGINOSA; TRANSCRIPTION REGULATION; UPREGULATION;

AMINO ACIDS; CHELATING AGENTS; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; HOMEOSTASIS; NUCLEIC ACID CONFORMATION; PHYLOGENY; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STABILITY; PSEUDOMONAS AERUGINOSA; RNA, MESSENGER; SPECTROPHOTOMETRY, ATOMIC; TRANSCRIPTION, GENETIC; ZINC;

ESCHERICHIA COLI; PSEUDOMONAS AERUGINOSA;

EID: 78751693014     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07475.x     Document Type: Article

References (81)

1. Aberg, A., Shingler, V., and Balsalobre, C. (2008) Regulation of the fimB promoter: a case of differential regulation by ppGpp and DksA in vivo. Mol Microbiol 67: 1223-1241.
2. Akanuma, G., Nanamiya, H., Natori, Y., Nomura, N., and Kawamura, F. (2006) Liberation of zinc-containing L31 (RpmE) from ribosomes by its paralogous gene product, YtiA, in Bacillus subtilis. J Bacteriol 188: 2715-2720.
3. 2+ uptake system ZnuABC is required for bacterial zinc homeostasis in intracellular environments and contributes to the virulence of Salmonella enterica. Infect Immun 75: 5867-5876.
4. Andreini, C., Banci, L., Bertini, I., and Rosato, A. (2006) Zinc through the three domains of life. J Proteome Res 5: 3173-3178.
5. Artsimovitch, I., Svetlov, V., Anthony, L., Burgess, R., and Landick, R. (2000) RNA polymerases from Bacillus subtilis and Escherichia coli differ in recognition of regulatory signals in vitro. J Bacteriol 182: 6027-6035.
6. Barker, M., and Gourse, R. (2001) Regulation of rRNA transcription correlates with nucleoside triphosphate sensing. J Bacteriol 183: 6315-6323.
7. Belogurov, G., Mooney, R., Svetlov, V., Landick, R., and Artsimovitch, I. (2009) Functional specialization of transcription elongation factors. EMBO J 28: 112-122.
8. Benson, D.A., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., and Sayers, E.W. (2009) GenBank. Nucleic Acids Res 37: D26-D31.
9. Blencowe, D., and Morby, A. (2003) Zn(II) metabolism in prokaryotes. FEMS Microbiol Rev 27: 291-311.
10. Branny, P., Pearson, J., Pesci, E., Köhler, T., Iglewski, B., and Van Delden, C. (2001) Inhibition of quorum sensing by a Pseudomonas aeruginosa dksA homologue. J Bacteriol 183: 1531-1539.
11. Bremer, H., and Dennis, P. (2008) Feedback control of ribosome function in Escherichia coli. Biochimie 90: 493-499.
12. Brown, L., Gentry, D., Elliott, T., and Cashel, M. (2002) DksA affects ppGpp induction of RpoS at a translational level. J Bacteriol 184: 4455-4465.
13. Burgess, R., and Anthony, L. (2001) How sigma docks to RNA polymerase and what sigma does. Curr Opin Microbiol 4: 126-131.
14. Caldwell, C., Chen, Y., Goetzmann, H., Hao, Y., Borchers, M., Hassett, D., etal. (2009) Pseudomonas aeruginosa exotoxin pyocyanin causes cystic fibrosis airway pathogenesis. Am J Pathol 175: 2473-2488.
15. Campoy, S., Jara, M., Busquets, N., Pérez De Rozas, A., Badiola, I., and Barbé, J. (2002) Role of the high-affinity zinc uptake ZnuABC system in Salmonella enterica serovar typhimurium virulence. Infect Immun 70: 4721-4725.
16. Choi, K., and Schweizer, H. (2005) An improved method for rapid generation of unmarked Pseudomonas aeruginosa deletion mutants. BMC Microbiol 5: 30.
17. Choi, K., Kumar, A., and Schweizer, H. (2006) A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods 64: 391-397.
18. Clohessy, P., and Golden, B. (1995) Calprotectin-mediated zinc chelation as a biostatic mechanism in host defence. Scand J Immunol 42: 551-556.
19. Dahiya, I., and Stevenson, R. (2010) The ZnuABC operon is important for Yersinia ruckeri infections of rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 33: 331-340.
20. Dalebroux, Z., Yagi, B., Sahr, T., Buchrieser, C., and Swanson, M. (2010) Distinct roles of ppGpp and DksA in Legionella pneumophila differentiation. Mol Microbiol 76: 200-219.
21. Davis, L., Kakuda, T., and DiRita, V. (2009) A Campylobacter jejuni znuA orthologue is essential for growth in low-zinc environments and chick colonization. J Bacteriol 191: 1631-1640.
22. Edgar, R. (2004) muscle: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
23. Farrell, H., Garvey, M., Cormican, M., Laffey, J., and Rowan, N. (2010) Investigation of critical inter-related factors affecting the efficacy of pulsed light for inactivating clinically relevant bacterial pathogens. J Appl Microbiol 108: 1494-1508.
24. Felsenstein, J. (1997) An alternating least squares approach to inferring phylogenies from pairwise distances. Syst Biol 46: 101-111.
25. Gaballa, A., and Helmann, J.D. (1998) Identification of a zinc-specific metalloregulatory protein, Zur, controlling zinc transport operons in Bacillus subtilis. J Bacteriol 180: 5815-5821.
26. Gabriel, S., and Helmann, J. (2009) Contributions of Zur-controlled ribosomal proteins to growth under zinc starvation conditions. J Bacteriol 191: 6116-6122.
27. Gabriel, S.E., Miyagi, F., Gaballa, A., and Helmann, J.D. (2008) Regulation of the Bacillus subtilis yciC gene and insights into the DNA-binding specificity of the zinc-sensing metalloregulator Zur. J Bacteriol 190: 3482-3488.
28. Graham, A., Hunt, S., Stokes, S., Bramall, N., Bunch, J., Cox, A., etal. (2009) Severe zinc depletion of Escherichia coli: roles for high affinity zinc binding by ZinT, zinc transport and zinc-independent proteins. J Biol Chem 284: 18377-18389.
29. Gray, R., MacGregor, G., Noble, D., Imrie, M., Dewar, M., Boyd, A., etal. (2008) Sputum proteomics in inflammatory and suppurative respiratory diseases. Am J Respir Crit Care Med 178: 444-452.
30. BAD promoter. J Bacteriol 177: 4121-4130.
31. Haas, C.E., Rodionov, D.A., Kropat, J., Malasarn, D., Merchant, S.S., and de Crécy-Lagard, V. (2009) A subset of the diverse COG0523 family of putative metal chaperones is linked to zinc homeostasis in all kingdoms of life. BMC Genomics 10: 470.
32. Hoang, T., Karkhoff-Schweizer, R., Kutchma, A., and Schweizer, H. (1998) 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. Gene 212: 77-86.
33. Jude, F., Köhler, T., Branny, P., Perron, K., Mayer, M., Comte, R., and van Delden, C. (2003) Posttranscriptional control of quorum-sensing-dependent virulence genes by DksA in Pseudomonas aeruginosa. J Bacteriol 185: 3558-3566.
34. Kang, P., and Craig, E. (1990) Identification and characterization of a new Escherichia coli gene that is a dosage-dependent suppressor of a dnaK deletion mutation. J Bacteriol 172: 2055-2064.
35. Kehl-Fie, T., and Skaar, E. (2010) Nutritional immunity beyond iron: a role for manganese and zinc. Curr Opin Chem Biol 14: 218-224.
36. Kim, S., Watanabe, K., Shirahata, T., and Watarai, M. (2004) Zinc uptake system (znuA locus) of Brucella abortus is essential for intracellular survival and virulence in mice. J Vet Med Sci 66: 1059-1063.
37. Kurachi, M. (1958) Studies on the biosynthesis of pyocyanine. Bull Inst Chem Res Kyoto Univ 36: 188-196.
38. Laptenko, O., Lee, J., Lomakin, I., and Borukhov, S. (2003) Transcript cleavage factors GreA and GreB act as transient catalytic components of RNA polymerase. EMBO J 22: 6322-6334.
39. Laptenko, O., Kim, S., Lee, J., Starodubtseva, M., Cava, F., Berenguer, J., etal. (2006) pH-dependent conformational switch activates the inhibitor of transcription elongation. EMBO J 25: 2131-2141.
40. Lee, J., and Helmann, J. (2007) Functional specialization within the Fur family of metalloregulators. Biometals 20: 485-499.
41. Łyzen, R., Kochanowska, M., Wegrzyn, G., and Szalewska-Palasz, A. (2009) Transcription from bacteriophage lambda pR promoter is regulated independently and antagonistically by DksA and ppGpp. Nucleic Acids Res 37: 6655-6664.
42. Magnusson, L., Farewell, A., and Nyström, T. (2005) ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13: 236-242.
43. Magnusson, L., Gummesson, B., Joksimović, P., Farewell, A., and Nyström, T. (2007) Identical, independent, and opposing roles of ppGpp and DksA in Escherichia coli. J Bacteriol 189: 5193-5202.
44. Makarova, K., Ponomarev, V., and Koonin, E. (2001) Two C or not two C: recurrent disruption of Zn-ribbons, gene duplication, lineage-specific gene loss, and horizontal gene transfer in evolution of bacterial ribosomal proteins. Genome Biol 2: RESEARCH 0033.
45. Marchler-Bauer, A., Anderson, J., Chitsaz, F., Derbyshire, M., DeWeese-Scott, C., Fong, J., etal. (2009) CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 37: D205-D210.
46. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
47. Natori, Y., Nanamiya, H., Akanuma, G., Kosono, S., Kudo, T., Ochi, K., and Kawamura, F. (2007) A fail-safe system for the ribosome under zinc-limiting conditions in Bacillus subtilis. Mol Microbiol 63: 294-307.
48. Novichkov, P., Laikova, O., Novichkova, E., Gelfand, M., Arkin, A., Dubchak, I., and Rodionov, D. (2010) RegPrecise: a database of curated genomic inferences of transcriptional regulatory interactions in prokaryotes. Nucleic Acids Res 38: D111-D118.
49. Outten, C., and O'Halloran, T. (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292: 2488-2492.
50. Overbeek, R., Begley, T., Butler, R.M., Choudhuri, J.V., Chuang, H.Y., Cohoon, M., etal. (2005) The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 33: 5691-5702.
51. Palmer, K., Mashburn, L., Singh, P., and Whiteley, M. (2005) Cystic fibrosis sputum supports growth and cues key aspects of Pseudomonas aeruginosa physiology. J Bacteriol 187: 5267-5277.
52. Panina, E.M., Mironov, A.A., and Gelfand, M.S. (2003) Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc Natl Acad Sci USA 100: 9912-9917.
53. Patzer, S., and Hantke, K. (1998) The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 28: 1199-1210.
54. Patzer, S., and Hantke, K. (2000) The zinc-responsive regulator Zur and its control of the znu gene cluster encoding the ZnuABC zinc uptake system in Escherichia coli. J Biol Chem 275: 24321-24332.
55. Paul, B., Barker, M., Ross, W., Schneider, D., Webb, C., Foster, J., and Gourse, R. (2004) DksA: a critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and the initiating NTP. Cell 118: 311-322.
56. Paul, B., Berkmen, M., and Gourse, R. (2005) DksA potentiates direct activation of amino acid promoters by ppGpp. Proc Natl Acad Sci USA 102: 7823-7828.
57. Perederina, A., Svetlov, V., Vassylyeva, M., Tahirov, T., Yokoyama, S., Artsimovitch, I., and Vassylyev, D. (2004) Regulation through the secondary channel - structural framework for ppGpp-DksA synergism during transcription. Cell 118: 297-309.
58. Perron, K., Comte, R., and van Delden, C. (2005) DksA represses ribosomal gene transcription in Pseudomonas aeruginosa by interacting with RNA polymerase on ribosomal promoters. Mol Microbiol 56: 1087-1102.
59. Petrarca, P., Ammendola, S., Pasquali, P., and Battistoni, A. (2010) The Zur-regulated ZinT protein is an auxiliary component of the high-affinity ZnuABC zinc transporter that facilitates metal recruitment during severe zinc shortage. J Bacteriol 192: 1553-1564.
60. Potrykus, K., and Cashel, M. (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62: 35-51.
61. Potrykus, K., Vinella, D., Murphy, H., Szalewska-Palasz, A., D'Ari, R., and Cashel, M. (2006) Antagonistic regulation of Escherichia coli ribosomal RNA rrnB P1 promoter activity by GreA and DksA. J Biol Chem 281: 15238-15248.
62. Qiu, D., Damron, F., Mima, T., Schweizer, H., and Yu, H. (2008) PBAD-based shuttle vectors for functional analysis of toxic and highly regulated genes in Pseudomonas and Burkholderia spp. and other bacteria. Appl Environ Microbiol 74: 7422-7426.
63. Rutherford, S., Villers, C., Lee, J., Ross, W., and Gourse, R. (2009) Allosteric control of Escherichia coli rRNA promoter complexes by DksA. Genes Dev 23: 236-248.
64. Sambrook, J., and Russell, D. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
65. Sankaran, B., Bonnett, S.A., Shah, K., Gabriel, S., Reddy, R., Schimmel, P., etal. (2009) Zinc-independent folate biosynthesis: genetic, biochemical, and structural investigations reveal new metal dependence for GTP cyclohydrolase IB. J Bacteriol 191: 6936-6949.
66. Schneider, D., Gaal, T., and Gourse, R. (2002) NTP-sensing by rRNA promoters in Escherichia coli is direct. Proc Natl Acad Sci USA 99: 8602-8607.
67. Schröder, J., Jochmann, N., Rodionov, D., and Tauch, A. (2010) The Zur regulon of Corynebacterium glutamicum ATCC 13032. BMC Genomics 11: 12.
68. Schweizer, H., and Hoang, T. (1995) An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 158: 15-22.
69. Srivatsan, A., and Wang, J. (2008) Control of bacterial transcription, translation and replication by (p)ppGpp. Curr Opin Microbiol 11: 100-105.
70. Stebbins, C., Borukhov, S., Orlova, M., Polyakov, A., Goldfarb, A., and Darst, S. (1995) Crystal structure of the GreA transcript cleavage factor from Escherichia coli. Nature 373: 636-640.
71. Stover, C., Pham, X., Erwin, A., Mizoguchi, S., Warrener, P., Hickey, M., etal. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
72. Symersky, J., Perederina, A., Vassylyeva, M., Svetlov, V., Artsimovitch, I., and Vassylyev, D. (2006) Regulation through the RNA polymerase secondary channel. Structural and functional variability of the coiled-coil transcription factors. J Biol Chem 281: 1309-1312.
73. Tehranchi, A., Blankschien, M., Zhang, Y., Halliday, J., Srivatsan, A., Peng, J., etal. (2010) The transcription factor DksA prevents conflicts between DNA replication and transcription machinery. Cell 141: 595-605.
74. Trautinger, B., Jaktaji, R., Rusakova, E., and Lloyd, R. (2005) RNA polymerase modulators and DNA repair activities resolve conflicts between DNA replication and transcription. Mol Cell 19: 247-258.
75. Vassylyeva, M., Perederina, A., Svetlov, V., Yokoyama, S., Artsimovitch, I., and Vassylyev, D. (2004) Cloning, expression, purification, crystallization and initial crystallographic analysis of transcription factor DksA from Escherichia coli. Acta Crystallogr D Biol Crystallogr 60: 1611-1613.
76. Vassylyeva, M., Svetlov, V., Dearborn, A., Klyuyev, S., Artsimovitch, I., and Vassylyev, D. (2007) The carboxy-terminal coiled-coil of the RNA polymerase beta'-subunit is the main binding site for Gre factors. EMBO Rep 8: 1038-1043.
77. Viducic, D., Ono, T., Murakami, K., Susilowati, H., Kayama, S., Hirota, K., and Miyake, Y. (2006) Functional analysis of spoT, relA and dksA genes on quinolone tolerance in Pseudomonas aeruginosa under nongrowing condition. Microbiol Immunol 50: 349-357.
78. Winsor, G., Van Rossum, T., Lo, R., Khaira, B., Whiteside, M., Hancock, R., and Brinkman, F. (2009) Pseudomonas Genome Database: facilitating user-friendly, comprehensive comparisons of microbial genomes. Nucleic Acids Res 37: D483-D488.
79. Yang, X., Becker, T., Walters, N., and Pascual, D. (2006) Deletion of znuA virulence factor attenuates Brucella abortus and confers protection against wild-type challenge. Infect Immun 74: 3874-3879.
80. Zenkin, N., Yuzenkova, Y., and Severinov, K. (2006) Transcript-assisted transcriptional proofreading. Science 313: 518-520.
81. Zhou, Y., and Jin, D. (1998) The rpoB mutants destabilizing initiation complexes at stringently controlled promoters behave like 'stringent' RNA polymerases in Escherichia coli. Proc Natl Acad Sci USA 95: 2908-2913.