Characterization of the Escherichia coli O157:H7 Sakai GadE regulon

Journal of Bacteriology

Volumn 191, Issue 6, 2009, Pages 1868-1877

  Vanaja, Sivapriya Kailasan ^a   Bergholz, Teresa M ^a,b   Whittam, Thomas S ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLUTAMATE DECARBOXYLASE; PROTEIN GADE; UNCLASSIFIED DRUG; ACID; ESCHERICHIA COLI PROTEIN; GADE PROTEIN, E COLI; LEE PROTEIN, E COLI; PHOSPHOPROTEIN; TRANSCRIPTION FACTOR;

ACIDITY; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CONTROLLED STUDY; ESCHERICHIA COLI O157; EVOLUTION; GADA GENE; GADB GENE; GADC GENE; GADE GENE; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE LOCUS; GENE REPRESSION; GENETIC TRANSCRIPTION; HORIZONTAL GENE TRANSFER; INTESTINE CELL; LER GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REGULATORY MECHANISM; REGULON; BINDING SITE; ESCHERICHIA COLI INFECTION; GENE SILENCING; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PROTEIN BINDING; VIRULENCE;

ESCHERICHIA COLI; ESCHERICHIA COLI O157:H-;

ACIDS; BINDING SITES; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENE SILENCING; HUMANS; PHOSPHOPROTEINS; PROTEIN BINDING; REGULON; TRANSCRIPTION FACTORS; VIRULENCE;

EID: 63049110420     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01481-08     Document Type: Article

References (61)

1. Abe, H., A. Miyahara, T. Oshima, K, Tashiro, Y. Ogura, S. Kuhara, N. Ogasawara, T. Hayashi, and T. Tobe. 2008. Global regulation by horizontally transferred regulators establishes the pathogenicity of Escherichia coli. DNA Res. 15:25-387
2. Abe, H., I. Tatsuno, T. Tobe, A. Okutani, and C. Sasakawa. 2002. Bicarbonate ion stimulates the expression of locus of enterocyte effacement-encoded genes in enterohemorrhagic Escherichia coli 0157:H7. Infect. Immun. 70: 3500-3509.
3. Alignan, M., T. Hewezi, M. Petitprez, G. Dechamp-Guillaume, and L. Gen-tzbittel, 2006. A cDNA microarray approach to decipher sunflower (Helian-thus annuus) responses to the necrotrophic fungus Phoma macdonaldii. New Phytol. 170:523-536.
4. Bergholz, T. M., C. L. Tarr, L. M. Christensen, D. J. Betting, and T. S. Whittam. 2007. Recent gene conversions between duplicated glutamate decarboxylase genes (gadA and gadB) in pathogenic Escherichia coli. Mol. Biol. Evol. 24:2323-2333.
5. Bergholz, T. M., and T. S. Whittam. 2007. Variation in acid resistance among enterohaemorrhagic Escherichia coli in a simulated gastric environment. J. Appl. Microbiol. 102:352-362.
6. Bergholz, T. M., L. M. Wick, W. Qi, J. T. Riordan, L. M. Ouellette, and T. S. Whittam. 2007. Global transcriptional response of Escherichia coli O157:H7 to growth transitions in glucose minimal medium. BMC Microbiol. 7:97.
7. Bhagwat, A. A., R. P. Phadke, D. Wheeler, S. Kalantre, M. Gudipati, and M. Bhagwat. 2003. Computational methods and evaluation of RNA stabilization reagents for genome-wide expression studies. J. Microbiol. Methods 55:399-409.
8. Canales, R. D., Y. Luo, J. C. Willey, B. Austermiller, C. C. Barbacioru, C. Boysen, K. Hunkapiller, R. Y. Jensen, C. R. Knight, K. Y. Lee, Y. Ma, B. Maqsodi, A. Papallo, E. H. Peters, K. Poulter, P. L. Ruppel, R. R. Samaha, L. Shi, W. Yang, L. Zhang, and F. M. Goodsaid. 2006. Evaluation of DNA microarray results with quantitative gene expression platforms. Nat. Biotech-nol. 24:1115-1122.
9. Castanie-Cornet, M.-P., and J. W. Foster. 2001. Escherichia coli acid resistance: cAMP receptor protein and a 20 bp cis-acting sequence control pH and stationary phase expression of the gadA and gadBC glutamate decarboxylase genes. Microbiology 147:709-715.
10. Castanie-Cornet, M.-P., T. A. Penfound, D. Smith, J. F. Elliott, and J. W. Foster. 1999. Control of acid resistance in Escherichia coli. J. Bacteriol. 181:3525-3535.
11. Castanié-Cornet, M.-P., H. Treffandier, A. Francez-Charlot, C. Gutierrez, and K. Cam. 2007. The glutamate-dependent acid resistance system in Escherichia coli: essential and dual role of the His-Asp phosphorelay RcsCDB/ AF. Microbiology 153:238-246.
12. Chen, J., J. Lozach, E. W. Garcia, B. Barnes, S. Luo, L Mikoulitch, L. Zhou, G. Sehroth, and J.-B. Fan. 25 June 2008. Highly sensitive and specific microRNA expression profiling using BeadArray technology. Nucleic Acids Res. 36:e87. [Epub ahead of print.]
13. Choi, S. H-, D. J. Baumler, and C. W. Kaspar. 2000. Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157: H7. Appl. Environ. Microbiol. 66:3911-3916.
14. Cui, X., and G. A. Churchill. 2003. Statistical tests for differential expression in cDNA microarray experiments. Genome Biol. 4:210.
15. Cui, X., J. T. Hwang, J. Qiu, N. J. Blades, and G. A. Churchill. 2005. Improved statistical tests for differential gene expression by shrinking variance components estimates. Biostatistics 6:59-75.
16. 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.
17. Deng, W., J. L. Puente, S. Gruenheid, Y. Li, B. A. Yallance, A, Vazquez, J. Barba, J. A. Ibarra, P. O'Donnell, P. Metalnikov, K. Ashman, S. Lee, D. Goode, T. Pawson, and B. B. Finlay. 2004. Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc. Natl. Acad. Sci. USA 101:3597-3602.
18. Foster, J. W. 2004. Escherichia coli acid resistance: tales of an amateur acidophile. Nat. Rev. Microbiol. 2:898-907.
19. Garmendia, J., G. Frankel, and V. F. Crepin. 2005. Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect. Immun. 73:2573-2585.
20. Hayashi, T., K. Makino, M. Ohnishi, K. Kurokawa, K. Ishii, K. Yokoyama, C.-G. Han, E. Ohtsubo, K. Nakayama, T. Murata, M. Tanaka, T. Tobe, T. Iida, H. Takami, T. Honda, C. Sasakawa, N. Ogasawara, T. Yasunaga, S. Kuhara, T. Shiba, M. Hattori, and H. Shinagawa. 2001. Complete genome sequence of enterohemorrhagic Escherichia coli 0157:H7 and genomic comparison with a laboratory strain K-12. DNA Res. 8:11-22.
21. Hommais, F., E. Krin, J.-Y. Coppee, C. Lacroix, E. Yeramian, A. Danchin, and P. Bertin. 2004. GadE (YhiE): a novel activator involved in the response to acid environment in Escherichia coli. Microbiology 150:61-72.
22. Hommais, F., E. Krin, C. Laurent-Winter, O. Soutourina, A. Malpertuy, J.-P. Le Caer, A. Danchin, and P. Bertin. 2001. Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol. Microbiol. 40:20-36.
23. Iyoda, S., and H. Watanabe. 2004. Positive effects of multiple pch genes on expression of the locus of enterocyte effacement genes and adherence of enterohaemorrhagic Escherichia coli 0157:H7 to HEp-2 cells. Microbiology 150:2357-2571.
24. Jin, W., R. M. Riley, R. D. Wolfinger, K. P. White, G. Passador-Gurgel, and G. Gibson. 2001. The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster. Nat. Genet. 29:389-395.
25. Just, J. R., and M. A. Daesehel. 2003. Antimicrobial effects of wine on Escherichia coli 0157:H7 and Salmonella typhimurium in a model stomach system. J. Food Sci. 68:285-290.
26. Karch, H., P. I. Tarr, and M. Bielaszewska. 2005. Enterohaemorrhagic Escherichia coli in human medicine. Int. J. Med. Microbiol. 295:405-118.
27. Large, T, M,, S. T. Walk, and T, S. Whittam. 2005. Variation in acid resistance among Shiga toxin-producing clones of pathogenic Escherichia coli. Appl. Environ. Microbiol. 71:2493-2500.
28. Law, D. 2000. Virulence factors of Escherichia coli 0157 and other Shiga toxin-producing E. coli. J. Appl. Microbiol. 88:729-745.
29. Li, H., C. Wood, T. Getchell, M. Getchell, and A. Stromberg. 2004. Analysis of oligonucleotide array experiments with repeated measures using mixed models. BMC Bioinformatics 5:209.
30. Lin, J., M. Smith, K. Chapin, H. Baik, G. Bennett, and J. Foster. 1996. Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl. Environ. Microbiol. 62:3094-3100.
31. Ma, Z., S. Gong, H. Richard, D. L. Tucker, T. Conway, and J. W. Foster. 2003. GadE (YhiE) activates glutamate decarboxylase-dependent acid resistance in Escherichia coli K-12. Mol. Microbiol. 49:1309-1320.
32. Ma, Z., N. Masuda, and J. W. Foster. 2004. Characterization of EvgAS-YdeO-GadE branched regulatory circuit governing glutamate-dependent acid resistance in Escherichia coli. J. Bacteriol. 186:7378-7389.
33. Mates, A. K., A. K. Sayed, and J, W. Foster. 2007. Products of the Escherichia coli acid fitness island attenuate metabolite stress at extremely low pH and mediate a cell density-dependent acid resistance. J. Bacteriol. 189:2759-2768.
34. McDaniel, T., K. Jarvis, M. Donnenberg, and J. Kaper. 1995. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. USA 92:1664-1668.
35. Mellies, J. L., A. M. S. Barron, and A. M. Carmona. 2007. Enteropathogenic and enterohemorrhagic Escherichia coli virulence gene regulation. Infect. Immun. 75:4199-4210.
36. Michino, H., K. Araki, S. Minami, S. Takaya, N. Sakai, M. Miyazaki, A. Ono, and H. Yanagawa. 1999. Massive outbreak of Escherichia coli 0157:H7 infection in schoolchildren in Sakai City. Japan, associated with consumption of white radish sprouts. Am. J. Epidemiol. 150:787-796.
37. Murphy, K., and K. Campellone, 2003. Lambda Red-mediated recombino-genic engineering of enterohemorrhagic and enteropathogenic E. coli. BMC Mol. Biol. 4:11.
38. Nadler, C, Y. Shifrin, S. Nov, S. Kobi, and I, Rosenshine. 2006. Characterization of enteropathogenic Escherichia coli mutants that fail to disrupt host cell spreading and attachment to substratum. Infect. Immun. 74:839-849.
39. Nakanishi, N., H. Abe, Y. Ogura, T. Hayashi, K. Tashiro, S. Kuhara, N. Sugimoto, and T. Tobe. 2006. ppGpp with DksA controls gene expression in the locus of enterocyte effacement (LEE) pathogenicity island of entero-haemorrhagic Escherichia coli through activation of two virulence regulatory genes. Mol. Microbiol. 61:194-205.
40. Peterson, W. L., P. A. Mackowiak, C. C. Barnett, M. Marling-Cason, and M. L. Haley. 1989. The human gastric bactericidal barrier: mechanisms of action, relative antibacterial activity, and dietary influences. J. Infect. Dis. 159:979-983.
41. Pfaffl, M. W. 1 May 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45. [Epub ahead of print.]
42. Price, S. B., J. C. Wright, F. J. DeGraves, M.-P. Castanie-Cornet, and J. W. Foster. 2004. Acid resistance systems required for survival of Escherichia coli 0157:H7 in the bovine gastrointestinal tract and in apple cider are different. Appl. Environ. Microbiol. 70:4792-4799.
43. Reid, S. D., C. J. Herbelin, A. C. Bumbaugh, R. K. Selander, and T. S. Whittam. 2000. Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406:64-67.
44. Rozen, S., and H. Skaletsky. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132:365-386.
45. Ruiz, C, L. M. McMurry, and S. B. Levy. 2008. Role of the multidrug resistance regulator MarA in global regulation of the hdeAB acid resistance operon in Escherichia coli. J. Bacteriol. 190:1290- 1297.
46. Sayed, A. K., C. Odom, and J. W. Foster. 2007. The Escherichia coli AraC-family regulators GadX and GadW activate gadE, the central activator of glutamate-dependent acid resistance. Microbiology 153:2584-2592.
47. Shin, S., M.-P. Castanie-Cornet, J. W. Foster, J. A. Crawford, C. Brinkley, and J. B. Kaper. 2001. An activator of glutamate decarboxylase genes regulates the expression of enteropathogenic Escherichia coli virulence genes through control of the plasmid-encoded regulator, Per. Mol. Microbiol. 41:1133-1150.
48. Smith, D. K., T. Kassam, B. Singh, and J. F. Elliott. 1992. Escherichia coli has two homologous glutamate decarboxylase genes that map to distinct loci. J. Bacteriol. 174:5820-5826.
49. Storey, J. D., and R. Tibshirani. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 100:9440-9445.
50. Subramanian, A., P. Tamayo, V. K. Mootha, S. Mukherjee, B. L. Ebert, M. A. Gillette, A. Paulovich, S. L. Pomeroy, T. R. Golub, E. S. Lander, and J. P. Mesirov. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102:15545-15550.
51. Tarr, P. I., C. A. Gordon, and W. L. Chandler. 2005. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365:1073-1086.
52. Tatsuno, I., K. Nagano, K. Taguchi, L. Rong, H. Mori, and C. Sasakawa. 2003. Increased adherence to Caco-2 cells caused by disruption of the yhiE and yhiE genes in enterohemorrhagic Escherichia coli 0157:H7. Infect. Immun. 71:2598-2606.
53. Tobe, T., H. Ando, H. Ishikawa, H. Abe, K. Tashiro, T. Hayashi, S. Kuhara, and N. Sugimoto. 2005. Dual regulatory pathways integrating the RcsC-RcsD-RcsB signalling system control enterohaemorrhagic Escherichia coli pathogenicity. Mol. Microbiol. 58:320-333.
54. Tobe, T., S. A. Beatson, H. Taniguchi, H. Abe, C. M. Bailey, A. Fivian, R. Younis, S. Matthews, O. Marches, G. Frankel, T. Hayashi, and M. J. Pallen. 2006. An extensive repertoire of type III secretion effectors in Escherichia coli OL57 and the role of lambdoid phages in their dissemination. Proc. Natl. Acad. Sci. USA 103:14941-14946.
55. Tramonti, A., M. De Canio, I. Delany, V. Scarlato, and D. De Biase. 2006. Mechanisms of transcription activation exerted by GadX and GadW at the gadA and gadBC gene promoters of the glutamate-based acid resistance system in Escherichia coli. J. Bacteriol. 188:8118- 8127.
56. Tucker, D. L., N. Tucker, and T. Conway. 2002. Gene expression profiling of the pH response in Escherichia coli. J. Bacteriol. 184:6551-6558.
57. Tucker, D. L., N. Tucker, Z. Ma, J. W. Foster, R. L. Miranda, P. S. Cohen, and T. Conway. 2003. Genes of the GadX-GadW regulon in Escherichia coli. J. Bacteriol. 185:3190-3201.
58. Umanski, T., I. Rosenshine, and D. Friedberg. 2002. Thermoregulated expression of virulence genes in enteropathogenic Escherichia coli. Microbiology 148:2735-2744.
59. s-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187:1591-1603.
60. Wick, L. M., W. Qi, D. W. Lacher, and T. S. Whittam. 2005. Evolution of genomic content in the stepwise emergence of Escherichia coli O157:H7. J. Bacteriol. 187:1783-1791.
61. Yuen, T., E. Wurmbach, R. L. Pfeffer, B. J. Ebersole, and S. C. Sealfon. 15 May 2002. Accuracy and calibration of commercial oligonucleotide and custom cDNA microarrays. Nucleic Acids Res. 30:e48. [Epub ahead of print.]