Unexpected coregulator range for the global regulator Lrp of Escherichia coli and Proteus mirabilis

Journal of Bacteriology

Volumn 193, Issue 5, 2011, Pages 1054-1064

  Hart, Benjamin R ^a   Blumenthal, Robert M ^a,b  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b UNIVERSITY OF TOLEDO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BACTERIAL PROTEIN; GLYCINE; HELIX LOOP HELIX PROTEIN; HISTIDINE; ISOLEUCINE; LEUCINE; LRP PROTEIN; LYSINE; METHIONINE; PROLINE; SERINE; THREONINE; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ACTINOBACILLUS PLEUROPNEUMONIAE; AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; ENTEROBACTERIACEAE; ESCHERICHIA COLI; GENE EXPRESSION; GENE SEQUENCE; KLEBSIELLA AEROGENES; MYCOBACTERIUM TUBERCULOSIS; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEUS MIRABILIS; PSEUDOMONAS AERUGINOSA; REGULATORY MECHANISM; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SENSITIVITY ANALYSIS; SEQUENCE HOMOLOGY; VIBRIO CHOLERAE;

BASE SEQUENCE; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; LEUCINE-RESPONSIVE REGULATORY PROTEIN; MOLECULAR SEQUENCE DATA; PLASMIDS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEUS MIRABILIS;

ENTEROBACTERIACEAE; ESCHERICHIA COLI; PROTEUS MIRABILIS;

EID: 79951639212     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01183-10     Document Type: Article

References (80)

1. Adams, M. D., et al. 1990. Nucleotide sequence and genetic characterization reveal six essential genes for the LIV-I and LS transport systems of Escherichia coli. J. Biol. Chem. 265:11436-11443.
2. Ambartsoumian, G., R. D'Ari, R. T. Lin, and E. B. Newman. 1994. Altered amino acid metabolism in lrp mutants of Escherichia coli K12 and their derivatives. Microbiology 140(Pt. 7):1737-1744.
3. Aviv, M., H. Giladi, G. Schreiber, A. B. Oppenheim, and G. Glaser. 1994. Expression of the genes coding for the Escherichia coli integration host factor are controlled by growth phase, rpoS, ppGpp and by autoregulation. Mol. Microbiol. 14:1021-1031.
4. Baek, C. H., S. Wang, K. L. Roland, and R. Curtiss III. 2009. Leucine-responsive regulatory protein (Lrp) acts as a virulence repressor in Salmonella enterica serovar Typhimurium. J. Bacteriol. 191:1278-1292.
5. Baumbach, J., S. Rahmann, and A. Tauch. 2009. Reliable transfer of transcriptional gene regulatory networks between taxonomically related organisms. BMC Syst. Biol. 3:8.
6. Berthiaume, F., et al. 2004. Influence of L-leucine and L-alanine on Lrp regulation of foo, coding for F1651, a Pap homologue. J. Bacteriol. 186:8537-8541. (Pubitemid 39603247)
7. Bhagwat, S. P., M. R. Rice, R. G. Matthews, and R. M. Blumenthal. 1997. Use of an inducible regulatory protein to identify members of a regulon: application to the regulon controlled by the leucine-responsive regulatory protein (Lrp) in Escherichia coli. J. Bacteriol. 179:6254-6263.
8. Blomfield, I. C., P. J. Calie, K. J. Eberhardt, M. S. McClain, and B. I. Eisenstein. 1993. Lrp stimulates phase variation of type 1 fimbriation in Escherichia coli K-12. J. Bacteriol. 175:27-36.
9. Borst, D. W., R. M. Blumenthal, and R. G. Matthews. 1996. Use of an in vivo titration method to study a global regulator: effect of varying Lrp levels on expression of gltBDF in Escherichia coli. J. Bacteriol. 178:6904-6912.
10. Boulette, M. L., et al. 2009. Characterization of alanine catabolism in Pseudomonas aeruginosa and its importance for proliferation in vivo. J. Bacteriol. 191:6329-6334.
11. Calvo, J. M., and R. G. Matthews. 1994. The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli. Microbiol. Rev. 58:466-490.
12. Charlier, D., M. Roovers, T. L. Thia-Toong, V. Durbecq, and N. Glansdorff. 1997. Cloning and identification of the Sulfolobus solfataricus lrp gene encoding an archaeal homologue of the eubacterial leucine-responsive global transcriptional regulator Lrp. Gene 201:63-68. (Pubitemid 27504079)
13. Chen, C. F., et al. 1997. Metabolic regulation of lrp gene expression in Escherichia coli K-12. Microbiology 143(Pt. 6):2079-2084. (Pubitemid 27290301)
14. Chen, S., and J. M. Calvo. 2002. Leucine-induced dissociation of Escherichia coli Lrp hexadecamers to octamers. J. Mol. Biol. 318:1031-1042.
15. Chen, S., Z. Hao, E. Bieniek, and J. M. Calvo. 2001. Modulation of Lrp action in Escherichia coli by leucine: effects on non-specific binding of Lrp to DNA. J. Mol. Biol. 314:1067-1075.
16. Chen, S., M. H. Rosner, and J. M. Calvo. 2001. Leucine-regulated self-association of leucine-responsive regulatory protein (Lrp) from Escherichia coli. J. Mol. Biol. 312:625-635.
17. Cho, B. K., C. L. Barrett, E. M. Knight, Y. S. Park, and B. O. Palsson. 2008. Genome-scale reconstruction of the Lrp regulatory network in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 105:19462-19467.
18. Crost, C., et al. 2004. Influence of environmental cues on transcriptional regulation of foo and clp coding for F165(1) and CS31A adhesins in Escherichia coli. Res. Microbiol. 155:475-482.
19. Daniel, J., and A. Danchin. 1979. Involvement of cyclic AMP and its receptor protein in the sensitivity of Escherichia coli K 12 toward serine: excretion of 2-ketobutyrate, a precursor of isoleucine. Mol. Gen. Genet. 176:343-350.
20. De Felice, M., et al. 1977. Growth inhibition of Escherichia coli K-12 by L-valine: a consequence of a regulatory pattern. Mol. Gen. Genet. 156:1-7.
21. de los Rios, S., and J. J. Perona. 2007. Structure of the Escherichia coli leucine-responsive regulatory protein Lrp reveals a novel octameric assembly. J. Mol. Biol. 366:1589-1602.
22. Dennis, P. P., and H. Bremer. 1974. Macromolecular composition during steady-state growth of Escherichia coli B/r. J. Bacteriol. 119:270-281.
23. Dirla, S., J. Y. Chien, and R. Schleif. 2009. Constitutive mutations in the Escherichia coli AraC protein. J. Bacteriol. 191:2668-2674.
24. Ernsting, B. R., J. W. Denninger, R. M. Blumenthal, and R. G. Matthews. 1993. Regulation of the gltBDF operon of Escherichia coli: how is a leucinein-sensitive operon regulated by the leucine-responsive regulatory protein? J. Bacteriol. 175:7160-7169.
25. Ettema, T. J., A. B. Brinkman, T. H. Tani, J. B. Rafferty, and J. Van Der Oost. 2002. A novel ligand-binding domain involved in regulation of amino acid metabolism in prokaryotes. J. Biol. Chem. 277:37464-37468.
26. Grainger, D. C., D. Hurd, M. D. Goldberg, and S. J. Busby. 2006. Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res. 34:4642-4652.
27. Grainger, D. C., D. Hurd, M. Harrison, J. Holdstock, and S. J. Busby. 2005. Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc. Natl. Acad. Sci. U. S. A. 102:17693-17698.
28. Haney, S. A., J. V. Platko, D. L. Oxender, and J. M. Calvo. 1992. Lrp, a leucine-responsive protein, regulates branched-chain amino acid transport genes in Escherichia coli. J. Bacteriol. 174:108-115.
29. Harris, C. L. 1981. Cysteine and growth inhibition of Escherichia coli: threonine deaminase as the target enzyme. J. Bacteriol. 145:1031-1035. (Pubitemid 11139043)
30. Hecht, K., S. Zhang, T. Klopotowski, and G. F. Ames. 1996. D-histidine utilization in Salmonella typhimurium is controlled by the leucine-responsive regulatory protein (Lrp). J. Bacteriol. 178:327-331.
31. Hershberg, R., and H. Margalit. 2006. Co-evolution of transcription factors and their targets depends on mode of regulation. Genome Biol. 7:R62.
32. Hung, S. P., P. Baldi, and G. W. Hatfield. 2002. Global gene expression profiling in Escherichia coli K12. The effects of leucine-responsive regulatory protein. J. Biol. Chem. 277:40309-40323.
33. Janes, B. K., and R. A. Bender. 1999. Two roles for the leucine-responsive regulatory protein in expression of the alanine catabolic operon (dadAB) in Klebsiella aerogenes. J. Bacteriol. 181:1054-1058.
34. Janga, S. C., and E. Perez-Rueda. 2009. Plasticity of transcriptional machinery in bacteria is increased by the repertoire of regulatory families. Comput. Biol. Chem. 33:261-268.
35. Kim, S. H., B. L. Schneider, and L. Reitzer. 2010. Genetics and regulation of the major enzymes of alanine synthesis in Escherichia coli. J. Bacteriol. 192:5304-5311.
36. Klumpp, S., Z. Zhang, and T. Hwa. 2009. Growth rate-dependent global effects on gene expression in bacteria. Cell 139:1366-1375.
37. Landgraf, J. R., J. Wu, and J. M. Calvo. 1996. Effects of nutrition and growth rate on Lrp levels in Escherichia coli. J. Bacteriol. 178:6930-6936.
38. Lintner, R. E., et al. 2008. Limited functional conservation of a global regulator among related bacterial genera: Lrp in Escherichia, Proteus and Vibrio. BMC Microbiol. 8:60.
39. Lozada-Chavez, I., S. C. Janga, and J. Collado-Vides. 2006. Bacterial regulatory networks are extremely flexible in evolution. Nucleic Acids Res. 34: 3434-3445.
40. Madan Babu, M., S. A. Teichmann, and L. Aravind. 2006. Evolutionary dynamics of prokaryotic transcriptional regulatory networks. J. Mol. Biol. 358:614-633.
41. Marasco, R., et al. 1994. In vivo footprinting analysis of Lrp binding to the ilvIH promoter region of Escherichia coli. J. Bacteriol. 176:5197-5201.
42. Marshall, D. G., B. J. Sheehan, and C. J. Dorman. 1999. A role for the leucine-responsive regulatory protein and integration host factor in the regulation of the Salmonella plasmid virulence (spv) locus in Salmonella typhimurium. Mol. Microbiol. 34:134-145.
43. Martin, C. 1996. The clp (CS31A) operon is negatively controlled by Lrp, ClpB, and L-alanine at the transcriptional level. Mol. Microbiol. 21:281-292.
44. Martinez-Antonio, A., and J. Collado-Vides. 2003. Identifying global regulators in transcriptional regulatory networks in bacteria. Curr. Opin. Microbiol. 6:482-489.
45. Mathew, E., J. Zhi, and M. Freundlich. 1996. Lrp is a direct repressor of the dad operon in Escherichia coli. J. Bacteriol. 178:7234-7240. (Pubitemid 26424639)
46. Matthews, R. G., Y. Cui, D. Friedberg, and J. M. Calvo. 2000. Wild-type and hexahistidine-tagged derivatives of leucine-responsive regulatory protein from Escherichia coli. Methods Enzymol. 324:322-329.
47. McFarland, K. A., and C. J. Dorman. 2008. Autoregulated expression of the gene coding for the leucine-responsive protein, Lrp, a global regulator in Salmonella enterica serovar Typhimurium. Microbiology 154:2008-2016.
48. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Press, Cold Spring Harbor, NY.
49. Nakanishi, N., et al. 2009. Regulation of virulence by butyrate sensing in enterohaemorrhagic Escherichia coli. Microbiology 155:521-530.
50. Neidhardt, F. C., P. L. Bloch, and D. F. Smith. 1974. Culture medium for enterobacteria. J. Bacteriol. 119:736-747.
51. Newman, E. B., et al. 1998. Lack of S-adenosylmethionine results in a cell division defect in Escherichia coli. J. Bacteriol. 180:3614-3619. (Pubitemid 29115091)
52. Newman, E. B., R. D'Ari, and R. T. Lin. 1992. The leucine-Lrp regulon in E. coli: a global response in search of a raison d'etre. Cell 68:617-619.
53. Oliver, G., et al. 1987. Determination of the nucleotide sequence for the glutamate synthase structural genes of Escherichia coli K-12. Gene 60:1-11. (Pubitemid 18026823)
54. Paul, L., R. M. Blumenthal, and R. G. Matthews. 2001. Activation from a distance: roles of Lrp and integration host factor in transcriptional activation of gltBDF. J. Bacteriol. 183:3910-3918.
55. Paul, L., P. K. Mishra, R. M. Blumenthal, and R. G. Matthews. 2007. Integration of regulatory signals through involvement of multiple global regulators: control of the Escherichia coli gltBDF operon by Lrp, IHF, Crp, and ArgR. BMC Microbiol. 7:2.
56. Platko, J. V., and J. M. Calvo. 1993. Mutations affecting the ability of Escherichia coli Lrp to bind DNA, activate transcription, or respond to leucine. J. Bacteriol. 175:1110-1117.
57. Platko, J. V., D. A. Willins, and J. M. Calvo. 1990. The ilvIH operon of Escherichia coli is positively regulated. J. Bacteriol. 172:4563-4570.
58. Potrykus, K., H. Murphy, N. Philippe, and M. Cashel. 2010. ppGpp is the major source of growth rate control in E. coli. Environ. Microbiol. [Epub ahead of print.] doi:10.1111/j.1462-2920.2010.02357.x.
59. Price, M. N., P. S. Dehal, and A. P. Arkin. 2007. Orthologous transcription factors in bacteria have different functions and regulate different genes. PLoS Comput. Biol. 3:1739-1750.
60. Primakoff, P. 1981. In vivo role of the relA+ gene in regulation of the lac operon. J. Bacteriol. 145:410-416.
61. Primakoff, P., and S. W. Artz. 1979. Positive control of lac operon expression in vitro by guanosine 5′-diphosphate 3′-diphosphate. Proc. Natl. Acad. Sci. U. S. A. 76:1726-1730.
62. Rasband, W. 2010. ImageJ. Documentation. http://rsb.info.nih.gov/ij/docs/ index.html.
63. Ren, J., et al. 2007. The structure and transcriptional analysis of a global regulator from Neisseria meningitidis. J. Biol. Chem. 282:14655-14664.
64. Rodgers, M. E., N. D. Holder, S. Dirla, and R. Schleif. 2009. Functional modes of the regulatory arm of AraC. Proteins 74:81-91.
65. Roesch, P. L., and I. C. Blomfield. 1998. Leucine alters the interaction of the leucine-responsive regulatory protein (Lrp) with the fim switch to stimulate site-specific recombination in Escherichia coli. Mol. Microbiol. 27:751-761.
66. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
67. Shrivastava, T., and R. Ramachandran. 2007. Mechanistic insights from the crystal structures of a feast/famine regulatory protein from Mycobacterium tuberculosis H37Rv. Nucleic Acids Res. 35:7324-7335.
68. Tagami, H., and H. Aiba. 1995. Role of CRP in transcription activation at Escherichia coli lac promoter: CRP is dispensable after the formation of open complex. Nucleic Acids Res. 23:599-605.
69. Tagami, H., T. Inada, T. Kunimura, and H. Aiba. 1995. Glucose lowers CRP* levels resulting in repression of the lac operon in cells lacking cAMP. Mol. Microbiol. 17:251-258.
70. Takahashi, H., T. Inada, P. Postma, and H. Aiba. 1998. CRP down-regulates adenylate cyclase activity by reducing the level of phosphorylated IIA(Glc), the glucose-specific phosphotransferase protein, in Escherichia coli. Mol. Gen. Genet. 259:317-326.
71. Tani, T. H., A. Khodursky, R. M. Blumenthal, P. O. Brown, and R. G. Matthews. 2002. Adaptation to famine: a family of stationary-phase genes revealed by microarray analysis. Proc. Natl. Acad. Sci. U. S. A. 99:13471-13476.
72. Wang, Q., J. Wu, D. Friedberg, J. Plakto, and J. M. Calvo. 1994. Regulation of the Escherichia coli lrp gene. J. Bacteriol. 176:1831-1839.
73. Weglenska, A., B. Jacob, and A. Sirko. 1996. Transcriptional pattern of Escherichia coli ihfB (himD) gene expression. Gene 181:85-88. (Pubitemid 26418251)
74. Wiese, D. E., II, B. R. Ernsting, R. M. Blumenthal, and R. G. Matthews. 1997. A nucleoprotein activation complex between the leucine-responsive regulatory protein and DNA upstream of the gltBDF operon in Escherichia coli. J. Mol. Biol. 270:152-168.
75. Wild, J., and W. Szybalski. 2004. Copy-control pBAC/oriV vectors for genomic cloning. Methods Mol. Biol. 267:145-154.
76. Willins, D. A., C. W. Ryan, J. V. Platko, and J. M. Calvo. 1991. Characterization of Lrp, an Escherichia coli regulatory protein that mediates a global response to leucine. J. Biol. Chem. 266:10768-10774.
77. Yan, K. K., G. Fang, N. Bhardwaj, R. P. Alexander, and M. Gerstein. 2010. Comparing genomes to computer operating systems in terms of the topology and evolution of their regulatory control networks. Proc. Natl. Acad. Sci. U. S. A. 107:9186-9191.
78. Yang, L., R. T. Lin, and E. B. Newman. 2002. Structure of the Lrp-regulated serA promoter of Escherichia coli K-12. Mol. Microbiol. 43:323-333.
79. Zhi, J., E. Mathew, and M. Freundlich. 1998. In vitro and in vivo characterization of three major dadAX promoters in Escherichia coli that are regulated by cyclic AMP-CRP and Lrp. Mol. Gen. Genet. 258:442-447.
80. Zhi, J., E. Mathew, and M. Freundlich. 1999. Lrp binds to two regions in the dadAX promoter region of Escherichia coli to repress and activate transcription directly. Mol. Microbiol. 32:29-40.