Cyclic AMP (cAMP) and cAMP receptor protein influence both synthesis and uptake of extracellular autoinducer 2 in Escherichia coli

Journal of Bacteriology

Volumn 187, Issue 6, 2005, Pages 2066-2076

  Wang, Liang ^a,b   Hashimoto, Yoshifumi ^a   Tsao, Chen Yu ^a,b   Valdes, James J ^c   Bentley, William E ^a,b  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c EDGEWOOD CHEMICAL BIOLOGICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; C REACTIVE PROTEIN; CYCLIC AMP; CYCLIC AMP BINDING PROTEIN; GLUCOSE; PROTEIN AUTOINDUCER 2; S RIBOSYLHOMOCYSTEINASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BINDING SITE; CATABOLITE REPRESSION; CELL INTERACTION; COMPLEX FORMATION; CONSENSUS SEQUENCE; CONTROLLED STUDY; ENZYME REPRESSION; ESCHERICHIA COLI; GENE CONTROL; GENE FUNCTION; GENE MUTATION; GENETIC TRANSCRIPTION; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; TRANSCRIPTION REGULATION;

BACTERIAL PROTEINS; CARBON-SULFUR LYASES; CYCLIC AMP; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FERMENTATION; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSE; HOMOSERINE; LACTONES; MUTAGENESIS; N-GLYCOSYL HYDROLASES; OPERON; PROMOTER REGIONS (GENETICS); RECEPTORS, CELL SURFACE; RECEPTORS, CYCLIC AMP; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; TYPHIMURIUM;

EID: 14644406798     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.6.2066-2076.2005     Document Type: Article

References (61)

1. Ahmer, B. M. 2004. Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol. Microbiol. 52:933-945.
2. Bainton, N. J., B. W. Bycroft, S. R. Chhabra, P. Stead, L. Gledhill, P. J. Hill, C. E. Rees, M. K. Winson, G. P. Salmond, G. S. Stewart, et al. 1992. A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic biosynthesis in Erwinia. Gene 116:87-91.
3. Barber, A. M., and V. B. Zhurkin. 1990. CAP binding sites reveal pyrimidine-purine pattern characteristic of DNA bending. J. Biomol. Struct. Dyn. 8:213-232.
4. Barber, A. M., V. B. Zhurkin, and S. Adhya. 1993. CRP-binding sites: evidence for two structural classes with 6-bp and 8-bp spacers. Gene 130:1-8.
5. Bassler, B. L., M. Wright, R. E. Showalter, and M. R. Silverman. 1993. Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol. Microbiol. 9:773-786.
6. Bassler, B. L., M. Wright, and M. R. Silverman. 1994. Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol. Microbiol. 13:273-286.
7. Beeston, A. L., and M. G. Surette. 2002. pfs-dependent regulation of autoinducer 2 production in Salmonella enterica serovar Typhimurium. J. Bacteriol. 184:3450-3456.
8. Bohannon, D. E., N. Connell, J. Keener, A. Tormo, M. Espinosa-Urgel, M. M. Zambrano, and R. Kolter. 1991. Stationary-phase-inducible "gearbox" promoters: differential effects of katF mutations and role of sigma 70. J. Bacteriol. 173:4482-4492.
9. Chapon, C, and A. Kolb. 1983. Action of CAP on the malT promoter in vitro. J. Bacteriol. 156:1135-1143.
10. Chen, X., S. Schauder, N. Potier, A. Van Dorsselaer, I. Pelczer, B. L. Bassler, and F. M. Hughson, 2002. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545-549.
11. Connell, N., Z. Han, F. Moreno, and R. Kolter. 1987. An E. coli promoter induced by the cessation of growth. Mol. Microbiol. 1:195-201.
12. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
13. Davies, D. G., M. R. Parsek, J. P. Pearson, B. H. Iglewski, J. W. Costerton, and E. P. Greenberg. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295-298.
14. DeLisa, M. P., J. J. Valdes, and W. E. Bentley. 2001. Mapping stress-induced changes in autoinducer AI-2 production in chemostat-cultivated Escherichia coli K-12. J. Bacteriol. 183:2918-2928.
15. DeLisa, M. P., J. J. Valdes, and W. E. Bentley. 2001. Quorum signaling via AI-2 communicates the "metabolic burden" associated with heterologous protein production in Escherichia coli. Biotechnol. Bioeng. 75:439-450.
16. DeLisa, M. P., C. F. Wu, L. Wang, J. J. Valdes, and W. E. Bentley. 2001. DNA microarray-based identification of genes controlled by autoinducer 2-stimulated quorum sensing in Escherichia coli. J. Bacteriol. 183:5239-5247.
17. Derzelle, S., E. Duchaud, F. Kunst, A. Danchin, and P. Bertin. 2002. Identification, characterization, and regulation of a cluster of genes involved in carbapenem biosynthesis in Photorhabdus luminescens. Appl. Environ. Microbiol. 68:3780-3789.
18. Elvers, K. T., and S. F. Park. 2002. Quorum sensing in Campylobacter jejuni: detection of a luxS encoded signalling molecule. Microbiology 148:1475-1481.
19. Engebrecht, J., K. Nealson, and M. Silverman. 1983. Bacterial bioluminescence; isolation and genetic analysis of functions from Vibrio fischeri. Cell 32:773-781.
20. Fuqua, W. C., and S. C. Winans. 1994. A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite. J. Bacteriol. 176:2796-2806.
21. Giebel, L. B., and R. A. Spritz. 1990. Site-directed mutagenesis using a double-stranded DNA fragment as a PCR primer. Nucleic Acids Res. 18: 4947.
22. Giron, J. A., A. G. Torres, E. Freer, and J. B. Kaper. 2002. The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol. Microbiol. 44:361-379.
23. Greenberg, E. P., J. W. Hastings, and S, Ulitzur. 1979. Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch. Microbiol. 120:87-91.
24. Greene, R. C. 1996. Biosynthesis of methionine, p. 542-560. In F. C. Neidhardt (ed.), Escherichia coli and Salmonella: cellular and molecular biology, vol. 1. American Society for Microbiology, Washington, D.C.
25. Hardie, K. R., C. Cooksley, A. D. Green, and K Winzer. 2003. Autoinducer 2 activity in Escherichia coli culture supernatants can be actively reduced despite maintenance of an active synthase, LuxS. Microbiology 149:715-728.
26. Ishizuka, H., A. Hanamura, T. Kunimura, and H. Aiba. 1993. A lowered concentration of cAMP receptor protein caused by glucose is an important determinant for catabolite repression in Escherichia coli. Mol. Microbiol. 10:341-350.
27. Joung, J. K., E. H. Chung, G. King, C. Yu, A. S. Hirsh, and A. Hochschild. 1995. Genetic strategy for analyzing specificity of dimer formation: Escherichia coli cyclic AMP receptor protein mutant altered in its dimerization specificity. Genes Dev. 9:2986-2996.
28. Kammann, M., J. Laufs, J. Schell, and B. Gronenborn. 1989. Rapid insertional mutagenesis of DNA by polymerase chain reaction (PCR). Nucleic Acids Res. 17:5404.
29. Kimata, K., H. Takahashi, T. Inada, P. Postma, and H. Aiba. 1997. cAMP receptor protein-cAMP plays a crucial role in glucose-lactose diauxie by activating the major glucose transporter gene in Escherichia coli. Proc. Natl. Acad. Sci. USA 94:12914-12919.
30. Kleerebezem, M., L. E. Quadri, O. P. Kuipers, and W. M. de Vos. 1997. Quorum sensing by peptide pheromones and two-component signal-trans-duction systems in gram-positive bacteria. Mol. Microbiol. 24:895-904.
31. Kolb, A., S. Busby, H. Buc, S. Garges, and S. Adhya. 1993. Transcriptional regulation by cAMP and its receptor protein. Annu. Rev. Biochem. 62:749-795.
32. Koop, A. H., M. E. Hartley, and S. Bourgeois. 1987. A low-copy-number vector utilizing beta-galactosidase for the analysis of gene control elements. Gene 52:245-256.
33. Li, S., B. U. Lee, and L. J. Shimkets. 1992. csgA expression entrains Myxococcus xanthus development. Genes Dev. 6:401-410.
34. Lilley, B. N., and B. L. Bassler. 2000. Regulation of quorum sensing in Vibrio harveyi by LuxO and sigma-54. Mol. Microbiol. 36:940-954.
35. Magnuson, R., J. Solomon, and A. D. Grossman. 1994. Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell 77:207-216.
36. Makman, R. S., and E. W. Sutherland. 1965. Adenosine 3′,5′- phosphate in Escherichia coli. J. Biol. Chem. 240:1309-1314.
37. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
38. Miller, M. B., K. Skorupski, D. H. Lenz, R. K. Taylor, and B. L. Bassler. 2002. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110:303-314.
39. Miller, S. T., K. B. Xavier, S. R. Campagna, M. E. Taga, M. F. Semmelhack, B. L. Bassler, and F. M. Hughson. 2004. Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2. Mol. Cell 15:677-687.
40. More, M. I., L. D. Finger, J. L. Stryker, C. Fuqua, A. Eberhard, and S. C. Winans. 1996. Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates. Science 272:1655-1658.
41. Notley-McRobb, L., T. King, and T. Ferenci. 2002. rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J. Bacteriol. 184:806-811.
42. Novick, R. P., and T. W. Muir. 1999. Virulence gene regulation by peptides in staphylococci and other gram-positive bacteria. Curr. Opin. Microbiol. 2:40-45.
43. Parsek, M. R., D. L. Val, B. L. Hanzelka, J. E. Cronan, Jr., and E. P. Greenberg. 1999. Acyl homoserine-lactone quorum-sensing signal generation. Proc. Natl. Acad. Sci. USA 96:4360-4365.
44. Passador, L., J. M. Cook, M. J. Gambello, L. Rust, and B. H. Iglewski. 1993. Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260:1127-1130.
45. Prouty, A. M., W. H. Schwesinger, and J. S. Gunn. 2002. Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect. Immun. 70:2640-2649.
46. Pyles, E. A., and J. C. Lee. 1996. Mode of selectivity in cyclic AMP receptor protein-dependent promoters in Escherichia coli. Biochemistry 35:1162-1172.
47. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
48. Schauder, S., K. Shokat, M. G. Surette, and B. L. Bassler. 2001. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 41:463-476.
49. Shirabe, K., Y. Ebina, T. Miki, T. Nakazawa, and A. Nakazawa. 1985. Positive regulation of the colicin E1 gene by cyclic AMP and cyclic AMP receptor protein. Nucleic Acids Res. 13:4687-4698.
50. Sperandio, V., J. L. Mellies, W. Nguyen, S. Shin, and J. B. Kaper, 1999. Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA 96:15196-15201.
51. Sperandio, V., A. G. Torres, J. A. Giron, and J. B. Kaper. 2001. Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 183:5187-5197.
52. Surette, M. G., and B. L. Bassler. 1998. Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 95:7046-7050.
53. Surette, M. G., and B. L. Bassler. 1999. Regulation of autoinducer production in Salmonella typhimurium. Mol. Microbiol. 31:585-595.
54. Taga, M. E., S. T. Miller, and B. L. Bassler. 2003. Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium. Mol. Microbiol. 50:1411-1427.
55. Taga, M. E., J. L. Semmelhack, and B. L. Bassler. 2001. The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium. Mol. Microbiol. 42:777-793.
56. Val, D. L., and J. E. Cronan, Jr. 1998. In vivo evidence that S-adenosylmethionine and fatty acid synthesis intermediates are the substrates for the LuxI family of autoinducer synthases. J. Bacteriol. 180:2644-2651.
57. Wehmeier, U. F., and J. W. Lengeler. 1994. Sequence of the sor-operon for L-sorbose utilization from Klebsiella pneumoniae KAY2026. Biochim. Biophys. Acta 1208:348-351.
58. Winzer, K., K. R. Hardie, N. Burgess, N. Doherty, D. Kirke, M. T. Holden, R. Linforth, K. A. Cornell, A. J. Taylor, P. J. Hill, and P. Williams. 2002. LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone. Microbiology 148:909-922.
59. Winzer, K., K. R. Hardie, and P. Williams. 2002. Bacterial cell-to-cell communication: sorry, can't talk now-gone to lunch! Curr. Opin. Microbiol. 5:216-222.
60. Withers, H, S. Swift, and P. Williams. 2001. Quorum sensing as an integral component of gene regulatory networks in gram-negative bacteria. Curr. Opin. Microbiol. 4:186-193.
61. Xavier, K. B., and B. L. Bassler. 2003. LuxS quorum sensing: more than just a numbers game. Curr. Opin. Microbiol. 6:191-197.