The tib adherence locus of enterotoxigenic Escherichia coli is regulated by cyclic AMP receptor protein

Journal of Bacteriology

Volumn 193, Issue 6, 2011, Pages 1369-1376

  Espert, Shirley M ^a   Elsinghorst, Eric A ^b   Munson, George P ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; CYCLIC AMP BINDING PROTEIN; ESCHERICHIA COLI ENTEROTOXIN; GLYCOPROTEIN; RNA; TIBA GLYCOPROTEIN; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BINDING SITE; ENTEROTOXIGENIC ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GRAM NEGATIVE BACTERIUM; INTESTINE MUCOSA; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BANGLADESH; BINDING SITES; DNA FOOTPRINTING; DNA, BACTERIAL; DNA-BINDING PROTEINS; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; FECES; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; GENETIC LOCI; HUMANS; POINT MUTATION; PROTEIN BINDING; RECEPTORS, CYCLIC AMP; VIRULENCE FACTORS;

ESCHERICHIA COLI; NEGIBACTERIA;

EID: 79952397832     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00288-10     Document Type: Article

References (77)

1. Abramoff, M. D., P. J. Magalhaes, and S. J. Ram. 2004. Image processing with image. J. Biophotonics Int. 11:36-41.
2. Alderete, J. F., and D. C. Robertson. 1977. Nutrition and enterotoxin synthesis by enterotoxigenic strains of Escherichia coli: defined medium for production of heat-stable enterotoxin. Infect. Immun. 15:781-788.
3. Alderete, J. F., and D. C. Robertson. 1977. Repression of heat-stable enterotoxin synthesis in enterotoxigenic Escherichia coli. Infect. Immun. 17:629-633.
4. Allen, K., M. Randolph, and J. Fleckenstein. 2006. Importance of heat-labile enterotoxin in colonization of the adult mouse small intestine by human enterotoxigenic Escherichia coli strains. Infect. Immun. 74:869-875.
5. Baba, T., et al. 2006. Construction of Escherichia coli K-12 in-frame, singlegene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:1-11.
6. Barba, J., et al. 2005. A positive regulatory loop controls expression of the locus of enterocyte effacement-encoded regulators Ler and GrlA. J. Bacteriol. 187:7918-7930. (Pubitemid 41691685)
7. Bell, A., et al. 1990. Mutations that alter the ability of the Escherichia coli cyclic AMP receptor protein to activate transcription. Nucleic Acids Res. 18:7243-7250. (Pubitemid 120006024)
8. Berthiaume, F., M. F. Leblond, J. Harel, and M. Mourez. 2010. Growthphase-dependent expression of the operon coding for the glycosylated autotransporter adhesin AIDA-I of pathogenic Escherichia coli. FEMS Microbiol. Lett. 311:176-184.
9. Blattner, F. R., et al. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1462. (Pubitemid 27449228)
10. Bodero, M., and G. Munson. 2009. Cyclic AMP receptor protein-dependent repression of heat-labile enterotoxin. Infect. Immun. 77:791-798.
11. Bodero, M., M. Pilonieta, and G. Munson. 2007. Repression of the inner membrane lipoprotein NlpA by Rns in enterotoxigenic Escherichia coli. J. Bacteriol. 189:1627-1632. (Pubitemid 46446124)
12. Botsford, J., and J. Harman. 1992. Cyclic AMP in prokaryotes. Microbiol. Mol. Biol. Rev. 56:100-122.
13. Boyer, H. W., and D. Roulland-Dussoix. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472.
14. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
15. Browning, D., and S. Busby. 2004. The regulation of bacterial transcription initiation. Nat. Rev. Microbiol. 2:57-65.
16. Buchet, A., W. Nasser, K. Eichler, and M. Mandrand-Berthelot. 1999. Positive co-regulation of the Escherichia coli carnitine pathway cai and fix operons by CRP and the CaiF activator. Mol. Microbiol. 34:562-575.
17. Busby, S., and R. Ebright. 1999. Transcription activation by catabolite activator protein (CAP). J. Mol. Biol. 293:199-213. (Pubitemid 29516164)
18. Busque, P., A. Letellier, J. Harel, and J. D. Dubreuil. 1995. Production of Escherichia coli STb enterotoxin is subject to catabolite repression. Microbiology 141:1621-1627.
19. Choi, H. K., et al. 2002. Promoter analysis and regulatory characteristics of vvhBA encoding cytolytic hemolysin of Vibrio vulnificus. J. Biol. Chem. 277:47292-47299.
20. Combet, C., C. Blanchet, C. Geourjon, and G. Deléage. 2000. NPS@: network protein sequence analysis. Trends Biochem. Sci. 25:147-150.
21. Crossman, L. C., et al. 2010. A commensal gone bad: complete genome sequence of the prototypical enterotoxigenic Escherichia coli strain H10407. J. Bacteriol. 192:5822-5831.
22. Darling, A. C. E., B. Mau, F. R. Blattner, and N. T. Perna. 2004. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14:1394-1403.
23. Datsenko, K., and B. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
24. Devine, J. H., G. S. Shadel, and T. O. Baldwin. 1989. Identification of the operator of the lux regulon from the Vibrio fischeri strain ATCC 7744. Proc. Natl. Acad. Sci. U. S. A. 86:5688-5692.
25. Ebright, R. 1993. Transcription activation at class I CAP-dependent promoters. Mol. Microbiol. 8:797-802.
26. Edwards, R., and D. Schifferli. 1997. Differential regulation of fasA and fasH expression of Escherichia coli 987 P fimbriae by enviromental cues. Mol. Microbiol. 25:797-809.
27. Edwards, R. A., and J. L. Puente. 1998. Fimbrial expression in enteric bacteria: a critical step in intestinal pathogenesis. Trends Microbiol. 6:282-287.
28. Elliott, S. J., et al. 1999. Identification of CesT, a chaperone for the type III secretion of Tir in enteropathogenic Escherichia coli. Mol. Microbiol. 33:1176-1189.
29. Elsinghorst, E. A., and J. A. Weitz. 1994. Epithelial cell invasion and adherence directed by the enterotoxigenic Escherichia coli tib locus is associated with a 104-kilodalton outer membrane protein. Infect. Immun. 62:3463-3471.
30. Evans, D., D. Evans, T. Karjalainen, and C. Lee. 1991. Production of colonization factor antigen II of enterotoxigenic Escherichia coli is subject to catabolite repression. Curr. Microbiol. 23:71-74.
31. Evans, D., R. Silver, D. Evans, Jr., D. Chase, and S. Gorbach. 1975. Plasmid-controlled colonization factor associated with virulence in Esherichia coli enterotoxigenic for humans. Infect. Immun. 12:656.
32. Ferraris, R., S. Yasharpour, K. Lloyd, R. Mirzayan, and J. Diamond. 1990. Luminal glucose concentrations in the gut under normal conditions. Am. J. Physiol. 259:G822-837.
33. Finn, R. D., et al. 2010. The Pfam protein families database. Nucleic Acids Res. 38:D211-222.
34. Gama-Castro, S., et al. 2008. RegulonDB (version 6.0): gene regulation model of Escherichia coli K-12 beyond transcription, active (experimental) annotated promoters and Textpresso navigation. Nucleic Acids Res. 36: D120-D124. (Pubitemid 351149707)
35. Girard, V., et al. 2010. Conformation change in a self-recognizing autotransporter modulates bacterial cell-cell interaction. J. Biol. Chem. 285:10616-10626.
36. Gosset, G., Z. Zhang, S. Nayyar, W. A. Cuevas, and M. H. Saier. 2004. Transcriptome analysis of Crp-dependent catabolite control of gene expression in Escherichia coli. J. Bacteriol. 186:3516-3524.
37. Grainger, D. C., D. Hurd, M. Harrison, J. Holdstock, and S. J. W. 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.
38. Haldimann, A., and B. Wanner. 2001. Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria. J. Bacteriol. 183:6384-6393. (Pubitemid 34059412)
39. Henderson, I., and J. Nataro. 2001. Virulence functions of autotransporter proteins. Infect. Immun. 69:1231-1243.
40. Holcroft, C. C., and S. M. Egan. 2000. Roles of cyclic AMP receptor protein and the carboxyl-terminal domain of the alpha subunit in transcription activation of the Escherichia coli rhaBAD operon. J. Bacteriol. 182:3529-3535.
41. Iyoda, S., et al. 2006. The GrlR-GrlA regulatory system coordinately controls the expression of flagellar and LEE-encoded type III protein secretion systems in enterohemorrhagic Escherichia coli. J. Bacteriol. 188:5682-5692. (Pubitemid 44384076)
42. Kalivoda, E. J., N. A. Stella, D. M. O'Dee, G. J. Nau, and R. M. Q. Shanks. 2008. The cyclic AMP-dependent catabolite repression system of Serratia marcescens mediates biofilm formation through regulation of type 1 fimbriae. Appl. Environ. Microbiol. 74:3461-3470.
43. Kanack, K. J., L. J. Runyen-Janecky, E. P. Ferrell, S.-J. Suh, and S. E. H. West. 2006. Characterization of DNA-binding specificity and analysis of binding sites of the Pseudomonas aeruginosa global regulator, Vfr, a homologue of the Escherichia coli cAMP receptor protein. Microbiology 152:3485-3496.
44. Karjalainen, T., D. Evans, and D. Evans. 1991. Catabolite repression of the colonization factor antigen I (CFA/I) operon of Escherichia coli. Curr. Microbiol. 23:307-313.
45. Kazakov, A. E., et al. 2007. RegTransBase - a database of regulatory sequences and interactions in a wide range of prokaryotic genomes. Nucleic Acids Res. 35:D407-412.
46. Khankal, R., J. W. Chin, D. Ghosh, and P. C. Cirino. 2009. Transcriptional effects of CRP* expression in Escherichia coli. J. Biol. Eng. 3:13.
47. Kim, T.-J., et al. 2007. Direct transcriptional control of the plasminogen activator gene of Yersinia pestis by the cyclic AMP receptor protein. J. Bacteriol. 189:8890-8900.
48. Kovacikova, G., and K. Skorupski. 2001. Overlapping binding sites for the virulence gene regulators AphA, AphB and cAMP-CRP at the Vibrio cholerae tcpPH promoter. Mol. Microbiol. 41:393-407.
49. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
50. Lathem, W. W., P. A. Price, V. L. Miller, and W. E. Goldman. 2007. A plasminogen-activating protease specifically controls the development of primary pneumonic plague. Science 315:509-513.
51. Lawson, C. L., et al. 2004. Catabolite activator protein: DNA binding and transcription activation. Curr. Opin. Struct. Biol. 14:10-20.
52. Lim, S., et al. 2003. Molecular analysis of Salmonella enterotoxin gene expression. J. Microbiol. Biotechnol. 13:598-606.
53. Lindenthal, C., and E. A. Elsinghorst. 2001. Enterotoxigenic Escherichia coli TibA glycoprotein adheres to human intestine epithelial cells. Infect. Immun. 69:52-57.
54. Lindenthal, C., and E. A. Elsinghorst. 1999. Identification of a glycoprotein produced by enterotoxigenic Escherichia coli. Infect. Immun. 67:4084-4091.
55. Lo-Tseng, T., J. Lee, and R. E. Isaacson. 1997. Regulators of Escherichia coli K99 region 1 genes. Adv. Exp. Med. Biol. 412:303-310.
56. Maris, A. E., et al. 2002. Dimerization allows DNA target site recognition by the NarL response regulator. Nat. Struct. Biol. 9:771-778.
57. Martinez-Cadena, M., L. Guzman-Verduzco, H. Stieglitz, and Y. Kupersztoch-Portnoy. 1981. Catabolite repression of Escherichia coli heat-stable enterotoxin activity. J. Bacteriol. 145:722-728. (Pubitemid 11140396)
58. Maxam, A. M., and W. Gilbert. 1977. A new method for sequencing DNA. Proc. Natl. Acad. Sci. U. S. A. 74:560-564.
59. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
60. Müller, C., A. Åberg, and J. Straseviçiene. 2009. Type 1 fimbriae, a colonization factor of uropathogenic Escherichia coli, are controlled by the metabolic sensor CRP-cAMP. PLoS Pathog. 5:1-14.
61. Munson, G., and J. Scott. 1999. Binding site recognition by Rns, a virulence regulator in the AraC family. J. Bacteriol. 181:2110-2117. (Pubitemid 29164964)
62. Oh, M. H., S. M. Lee, D. H. Lee, and S. H. Choi. 2009. Regulation of the Vibrio vulnificus hupA gene by temperature alteration and cyclic AMP receptor protein and evaluation of its role in virulence. Infect. Immun. 77:1208-1215.
63. O'Neill, M. C. 1998. A general procedure for locating and analyzing protein-binding sequence motifs in nucleic acids. Proc. Natl. Acad. Sci. U. S. A. 95:10710-10715.
64. Puente, J. L., D. Bieber, S. W. Ramer, W. Murray, and G. K. Schoolnik. 1996. The bundle-forming pili of enteropathogenic Escherichia coli: transcriptional regulation by environmental signals. Mol. Microbiol. 20:87-100.
65. Russell, R., F. Sharp, and D. Rasko. 2007. QseA and GrlR/GrlA regulation of the locus of enterocyte effacement genes in enterohemorrhagic Escherichia coli. J. Bacteriol. 189:5387-5392. (Pubitemid 47076085)
66. Saitoh, T., et al. 2008. Transcription of the ehx enterohemolysin gene is positively regulated by GrlA, a global regulator encoded within the locus of enterocyte effacement in enterohemorrhagic Escherichia coli. J. Bacteriol. 190:4822-4830. (Pubitemid 351991050)
67. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U. S. A. 74:5463-5467.
68. Schnaitman, C. A. 1970. Protein composition of the cell wall and cytoplasmic membrane of Escherichia coli. J. Bacteriol. 104:890-901.
69. Schultz, S. C., G. C. Shields, and T. A. Steitz. 1991. Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees. Science 253:1001-1007.
70. Sherlock, O., R. Vejborg, and P. Klemm. 2005. The TibA adhesin/invasin from enterotoxigenic Escherichia coli is self recognizing and induces bacterial aggregation and biofilm formation. Infect. Immun. 73:1954-1963.
71. Skorupski, K., and R. K. Taylor. 1997. Cyclic AMP and its receptor protein negatively regulate the coordinate expression of cholera toxin and toxinco-regulated pilus in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 94:265-270.
72. Stewart, G. S., S. Lubinsky-Mink, C. G. Jackson, A. Cassel, and J. Kuhn. 1986. pHG165: a pBR322 copy number derivative of pUC8 for cloning and expression. Plasmid 15:172-181.
73. Suck, D. 1997. DNA recognition by structure-selective nucleases. Biopolymers 44:405-421.
74. White, C. E., and S. C. Winans. 2007. The quorum-sensing transcription factor TraR decodes its DNA binding site by direct contacts with DNA bases and by detection of DNA flexibility. Mol. Microbiol. 64:245-256.
75. Wickstrum, J., and S. Egan. 2002. Ni+-affinity purification of untagged cAMP receptor protein. Biotechniques 33:728-730. (Pubitemid 35168051)
76. Zhan, L., et al. 2008. The cyclic AMP receptor protein, CRP, is required for both virulence and expression of the minimal CRP regulon in Yersinia pestis biovar microtus. Infect. Immun. 76:5028-5037.
77. Zheng, D., C. Constantinidou, and J. Hobman. 2004. Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. Nucleic Acids Res. 32:5874-5893. (Pubitemid 39619170)