The Epinephrine/Norepinephrine/Autoinducer-3 Interkingdom Signaling System in Escherichia coli O157:H7

  • Cristiano G. Moreira
  • Vanessa Sperandio


Epinephrine/norepinephrine/AI-3 signaling is used as an interkingdom chemical signaling system between microbes and their hosts. This system is also exploited by pathogens to regulate virulence traits. In enterohemorrhagic E. coli (EHEC) O157:H7, it is essential for pathogenesis and flagella motility. These three signals activate expression of a pathogenicity island named locus of enterocyte effacement (LEE), Shiga toxin, and the flagella regulon. These signals are sensed by the two-component system QseBC, whereas the bacterial membrane receptor QseC autophosphorylates and phosphorylates the QseB response regulator initiating a complex phosphorelay signaling cascade that activates the expression of a second two-component system, QseEF. The QseEF two-component system is also involved in the expression of the virulence genes, and it senses epinephrine, phosphate, and sulfate. This complex signaling cascade still needs to be completely elucidated.


Quorum Sensing Hemolytic Uremic Syndrome Pathogenicity Island Shiga Toxin Francisella Tularensis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Barba, J., V. H. Bustamante, M. A. Flores-Valdez, W. Deng, B. B. Finlay, and J. L. Puente. A Positive Regulatory Loop Controls Expression of the Locus of Enterocyte Effacement-Encoded Regulators Ler and Grla. J Bacteriol 187, no. 23 (2005): 7918–30.PubMedCrossRefGoogle Scholar
  2. Bearson, B. L., and S. M. Bearson. The Role of the Qsec Quorum-Sensing Sensor Kinase in Colonization and Norepinephrine-Enhanced Motility of Salmonella enterica Serovar Typhimurium. Microb Pathog 44, no. 4 (2008): 271–8.PubMedCrossRefGoogle Scholar
  3. Boerlin, P., S. A. McEwen, F. Boerlin-Petzold, J. B. Wilson, R. P. Johnson, and C. L. Gyles. Associations between Virulence Factors of Shiga Toxin-Producing Escherichia coli and Disease in Humans. J Clin Microbiol 37, no. 3 (1999): 497–503.PubMedGoogle Scholar
  4. Bustamante, V. H., F. J. Santana, E. Calva, and J. L. Puente. Transcriptional Regulation of Type Iii Secretion Genes in Enteropathogenic Escherichia coli: Ler Antagonizes H-Ns-Dependent Repression. Mol Microbiol 39, no. 3 (2001): 664–78.PubMedCrossRefGoogle Scholar
  5. Campellone, K. G., D. Robbins, and J. M. Leong. Espfu Is a Translocated Ehec Effector That Interacts with Tir and N-Wasp and Promotes Nck-Independent Actin Assembly. Dev Cell 7, no. 2 (2004): 217–28.PubMedCrossRefGoogle Scholar
  6. Charpentier, X., and E. Oswald. Identification of the Secretion and Translocation Domain of the Enteropathogenic and Enterohemorrhagic Escherichia coli Effector Cif, Using Tem-1 Beta-Lactamase as a New Fluorescence-Based Reporter. J Bacteriol 186, no. 16 (2004): 5486–95.PubMedCrossRefGoogle Scholar
  7. Chen, X., S. Schauder, N. Potier, A. Van Dorssealaer, I. Pelczer, B.L. Bassler, and F.M. Hughson. Structural Identification of a Bacterial Quorum-Sensing Signal Containing Boron. Nature 415 (2002): 545–49.PubMedCrossRefGoogle Scholar
  8. Cherezov, V., D. M. Rosenbaum, M. A. Hanson, S. G. Rasmussen, F. S. Thian, T. S. Kobilka, H. J. Choi, P. Kuhn, W. I. Weis, B. K. Kobilka, and R. C. Stevens. High-Resolution Crystal Structure of an Engineered Human Beta2-Adrenergic G Protein-Coupled Receptor. Science 318, no. 5854 (2007): 1258–65.PubMedCrossRefGoogle Scholar
  9. Clarke, M. B., D. T. Hughes, C. Zhu, E. C. Boedeker, and V. Sperandio. The Qsec Sensor Kinase: A Bacterial Adrenergic Receptor. Proc Natl Acad Sci U S A 103, no. 27 (2006): 10420–5.PubMedCrossRefGoogle Scholar
  10. Clarke, M. B., and V. Sperandio. Transcriptional Autoregulation by Quorum Sensing Escherichia coli Regulators B and C (Qsebc) in Enterohaemorrhagic E. coli (Ehec). Mol Microbiol 58, no. 2 (2005): 441–55.PubMedCrossRefGoogle Scholar
  11. Clarke, M. B., and V. Sperandio. Transcriptional Regulation of Flhdc by Qsebc and Sigma (Flia) in Enterohaemorrhagic Escherichia coli. Mol Microbiol 57, no. 6 (2005): 1734–49.PubMedCrossRefGoogle Scholar
  12. Deibel, C., S. Kramer, T. Chakraborty, and F. Ebel. Espe, a Novel Secreted Protein of Attaching and Effacing Bacteria, Is Directly Translocated into Infected Host Cells, Where It Appears as a Tyrosine-Phosphorylated 90 Kda Protein. Mol Microbiol 28, no. 3 (1998): 463–74.PubMedCrossRefGoogle Scholar
  13. Deng, W., J. L. Puente, S. Gruenheid, Y. Li, B. A. Vallance, A. Vazquez, J. Barba, J. A. Ibarra, P. O’Donnell, P. Metalnikov, K. Ashman, S. Lee, D. Goode, T. Pawson, and B. B. Finlay. Dissecting Virulence: Systematic and Functional Analyses of a Pathogenicity Island. Proc Natl Acad Sci U S A 101, no. 10 (2004): 3597–602.PubMedCrossRefGoogle Scholar
  14. DeVinney, R., A. Gauthier, A. Abe, and B. B. Finlay. Enteropathogenic Escherichia coli: A Pathogen That Inserts Its Own Receptor into Host Cells. Cell Mol Life Sci 55, no. 6–7 (1999): 961–76.PubMedGoogle Scholar
  15. Donohue-Rolfe, A., G. T. Keusch, C. Edson, D. Thorley-Lawson, and M. Jacewicz. Pathogenesis of Shigella Diarrhea. I×. Simplified High Yield Purification of Shigella Toxin and Characterization of Subunit Composition and Function by the Use of Subunit-Specific Monoclonal and Polyclonal Antibodies. J Exp Med 160, no. 6 (1984): 1767–81.PubMedCrossRefGoogle Scholar
  16. Elliott, S. J., V. Sperandio, J. A. Giron, S. Shin, J. L. Mellies, L. Wainwright, S. W. Hutcheson, T. K. McDaniel, and J. B. Kaper. The Locus of Enterocyte Effacement (Lee)-Encoded Regulator Controls Expression of Both Lee- and Non-Lee-Encoded Virulence Factors in Enteropathogenic and Enterohemorrhagic Escherichia coli. Infect Immun 68, no. 11 (2000): 6115–26.PubMedCrossRefGoogle Scholar
  17. Elliott, S. J., L. A. Wainwright, T. K. McDaniel, K. G. Jarvis, Y. K. Deng, L. C. Lai, B. P. McNamara, M. S. Donnenberg, and J. B. Kaper. The Complete Sequence of the Locus of Enterocyte Effacement (Lee) from Enteropathogenic Escherichia coli E2348/69. Mol Microbiol 28, no. 1 (1998): 1–4.PubMedCrossRefGoogle Scholar
  18. Elliott, S. J., J. Yu, and J. B. Kaper. The Cloned Locus of Enterocyte Effacement from Enterohemorrhagic Escherichia coli O157:H7 Is Unable to Confer the Attaching and Effacing Phenotype Upon E. coli K-12. Infect Immun 67, no. 8 (1999): 4260–3.PubMedGoogle Scholar
  19. Endo, Y., K. Tsurugi, T. Yutsudo, Y. Takeda, T. Ogasawara, and K. Igarashi. Site of Action of a Vero Toxin (Vt2) from Escherichia coli O157:H7 and of Shiga Toxin on Eukaryotic Ribosomes. Rna N-Glycosidase Activity of the Toxins. Eur J Biochem 171, no. 1–2 (1988): 45–50.PubMedCrossRefGoogle Scholar
  20. Freddolino, P. L., M. Y. Kalani, N. Vaidehi, W. B. Floriano, S. E. Hall, R. J. Trabanino, V. W. Kam, and W. A. Goddard, 3rd. Predicted 3d Structure for the Human Beta 2 Adrenergic Receptor and Its Binding Site for Agonists and Antagonists. Proc Natl Acad Sci U S A 101, no. 9 (2004): 2736–41.PubMedCrossRefGoogle Scholar
  21. Friedberg, D., T. Umanski, Y. Fang, and I. Rosenshine. Hierarchy in the Expression of the Locus of Enterocyte Effacement Genes of Enteropathogenic Escherichia coli. Mol Microbiol 34, no. 5 (1999): 941–52.PubMedCrossRefGoogle Scholar
  22. Furness, J. B. Types of Neurons in the Enteric Nervous System. J Auton Nerv Syst 81, no. 1–3 (2000): 87–96.PubMedCrossRefGoogle Scholar
  23. Goosney, D. L., R. DeVinney, and B. B. Finlay. Recruitment of Cytoskeletal and Signaling Proteins to Enteropathogenic and Enterohemorrhagic Escherichia coli Pedestals. Infect Immun 69, no. 5 (2001): 3315–22.PubMedCrossRefGoogle Scholar
  24. Gruenheid, S., I. Sekirov, N. A. Thomas, W. Deng, P. O’Donnell, D. Goode, Y. Li, E. A. Frey, N. F. Brown, P. Metalnikov, T. Pawson, K. Ashman, and B. B. Finlay. Identification and Characterization of Nlea, a Non-Lee-Encoded Type Iii Translocated Virulence Factor of Enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 51, no. 5 (2004): 1233–49.PubMedCrossRefGoogle Scholar
  25. Haack, K. R., C. L. Robinson, K. J. Miller, J. W. Fowlkes, and J. L. Mellies. Interaction of Ler at the Lee5 (Tir) Operon of Enteropathogenic Escherichia coli. Infection & Immunity 71, no. 1 (2003): 384–92.CrossRefGoogle Scholar
  26. Hughes, D. T., and V. Sperandio. Inter-Kingdom Signalling: Communication between Bacteria and Their Hosts. Nat Rev Microbiol 6, no. 2 (2008): 111–20.PubMedCrossRefGoogle Scholar
  27. Ide, T., S. Laarmann, L. Greune, H. Schillers, H. Oberleithner, and M. A. Schmidt. Characterization of Translocation Pores Inserted into Plasma Membranes by Type Iii-Secreted Esp Proteins of Enteropathogenic Escherichia coli. Cell Microbiol 3, no. 10 (2001): 669–79.PubMedCrossRefGoogle Scholar
  28. Iyoda, S., and H. Watanabe. Positive Effects of Multiple Pch Genes on Expression of the Locus of Enterocyte Effacement Genes and Adherence of Enterohaemorrhagic Escherichia coli O157 : H7 to Hep-2 Cells. Microbiology 150, no. Pt 7 (2004): 2357–571.PubMedCrossRefGoogle Scholar
  29. Jacewicz, M., H. Clausen, E. Nudelman, A. Donohue-Rolfe, and G. T. Keusch. Pathogenesis of Shigella Diarrhea. Xi. Isolation of a Shigella Toxin-Binding Glycolipid from Rabbit Jejunum and Hela Cells and Its Identification as Globotriaosylceramide. J Exp Med 163, no. 6 (1986): 1391–404.PubMedCrossRefGoogle Scholar
  30. Jarvis, K. G., J. A. Giron, A. E. Jerse, T. K. McDaniel, M. S. Donnenberg, and J. B. Kaper. Enteropathogenic Escherichia coli Contains a Putative Type Iii Secretion System Necessary for the Export of Proteins Involved in Attaching and Effacing Lesion Formation. Proc Natl Acad Sci U S A 92, no. 17 (1995): 7996–8000.PubMedCrossRefGoogle Scholar
  31. Jerse, A. E., J. Yu, B. D. Tall, and J. B. Kaper. A Genetic Locus of Enteropathogenic Escherichia coli Necessary for the Production of Attaching and Effacing Lesions on Tissue Culture Cells. Proc Natl Acad Sci U S A 87, no. 20 (1990): 7839–43.PubMedCrossRefGoogle Scholar
  32. Kaper, J. B., J. P. Nataro, and H. L. Mobley. Pathogenic Escherichia coli. Nat Rev Microbiol 2, no. 2 (2004): 123–40.PubMedCrossRefGoogle Scholar
  33. Kenny, B., A. Abe, M. Stein, and B. B. Finlay. Enteropathogenic Escherichia coli Protein Secretion Is Induced in Response to Conditions Similar to Those in the Gastrointestinal Tract. Infect Immun 65, no. 7 (1997): 2606–12.PubMedGoogle Scholar
  34. Kenny, B., R. DeVinney, M. Stein, D. J. Reinscheid, E. A. Frey, and B. B. Finlay. Enteropathogenic E. coli (Epec) Transfers Its Receptor for Intimate Adherence into Mammalian Cells. Cell 91, no. 4 (1997): 511–20.PubMedCrossRefGoogle Scholar
  35. Kenny, B., and B. B. Finlay. Protein Secretion by Enteropathogenic Escherichia coli Is Essential for Transducing Signals to Epithelial Cells. Proc Natl Acad Sci U S A 92, no. 17 (1995): 7991–5.PubMedCrossRefGoogle Scholar
  36. Kenny, B., and M. Jepson. Targeting of an Enteropathogenic Escherichia coli (Epec) Effector Protein to Host Mitochondria. Cell Microbiol 2, no. 6 (2000): 579–90.PubMedCrossRefGoogle Scholar
  37. Kimmitt, P. T., C. R. Harwood, and M. R. Barer. Induction of Type 2 Shiga Toxin Synthesis in Escherichia coli O157 by 4-Quinolones. Lancet 353, no. 9164 (1999): 1588–9.PubMedCrossRefGoogle Scholar
  38. Kimmitt, P. T., C. R. Harwood, and M. R. Barer. Toxin Gene Expression by Shiga Toxin-Producing Escherichia coli: The Role of Antibiotics and the Bacterial Sos Response. Emerg Infect Dis 6, no. 5 (2000): 458–65.PubMedCrossRefGoogle Scholar
  39. Lindberg, A. A., J. E. Brown, N. Stromberg, M. Westling-Ryd, J. E. Schultz, and K. A. Karlsson. Identification of the Carbohydrate Receptor for Shiga Toxin Produced by Shigella dysenteriae Type 1. J Biol Chem 262, no. 4 (1987): 1779–85.PubMedGoogle Scholar
  40. McDaniel, T. K., K. G. Jarvis, M. S. Donnenberg, and J. B. Kaper. A Genetic Locus of Enterocyte Effacement Conserved among Diverse Enterobacterial Pathogens. Proc Natl Acad Sci U S A 92, no. 5 (1995): 1664–8.PubMedCrossRefGoogle Scholar
  41. McNamara, B. P., and M. S. Donnenberg. A Novel Proline-Rich Protein, Espf, Is Secreted from Enteropathogenic Escherichia coli Via the Type Iii Export Pathway. FEMS Microbiol Lett 166, no. 1 (1998): 71–8.PubMedCrossRefGoogle Scholar
  42. McNamara, B. P., A. Koutsouris, C. B. O’Connell, J. P. Nougayrede, M. S. Donnenberg, and G. Hecht. Translocated Espf Protein from Enteropathogenic Escherichia coli Disrupts Host Intestinal Barrier Function. J Clin Invest 107, no. 5 (2001): 621–9.PubMedCrossRefGoogle Scholar
  43. Mellies, J. L., S. J. Elliott, V. Sperandio, M. S. Donnenberg, and J. B. Kaper. The Per Regulon of Enteropathogenic Escherichia coli: Identification of a Regulatory Cascade and a Novel Transcriptional Activator, the Locus of Enterocyte Effacement (Lee)-Encoded Regulator (Ler). Mol Microbiol 33, no. 2 (1999): 296–306.PubMedCrossRefGoogle Scholar
  44. Merighi, M., A. Carroll-Portillo, A. N. Septer, A. Bhatiya, and J. S. Gunn. Role of Salmonella Enterica Serovar Typhimurium Two-Component System Prea/Preb in Modulating Pmra-Regulated Gene Transcription. J Bacteriol 188, no. 1 (2006): 141–9.PubMedCrossRefGoogle Scholar
  45. Merighi, M., A. N. Septer, A. Carroll-Portillo, A. Bhatiya, S. Porwollik, M. McClelland, and J. S. Gunn. Genome-Wide Analysis of the Prea/Preb (Qseb/Qsec) Regulon of Salmonella enterica Serovar Typhimurium. BMC Microbiol 9, no. 1 (2009): 42.PubMedCrossRefGoogle Scholar
  46. Miller, S. T., K. B. Xavier, S. R. Campagna, M. E. Taga, M. F. Semmelhack, B. L. Bassler, and F. M. Hughson. Salmonella typhimurium Recognizes a Chemically Distinct Form of the Bacterial Quorum-Sensing Signal Ai-2. Mol Cell 15, no. 5 (2004): 677–87.PubMedCrossRefGoogle Scholar
  47. Neely, M. N., and D. I. Friedman. Functional and Genetic Analysis of Regulatory Regions of Coliphage H-19b: Location of Shiga-Like Toxin and Lysis Genes Suggest a Role for Phage Functions in Toxin Release. Mol Microbiol 28, no. 6 (1998): 1255–67.PubMedCrossRefGoogle Scholar
  48. Perera, L. P., L. R. Marques, and A. D. O’Brien. Isolation and Characterization of Monoclonal Antibodies to Shiga-Like Toxin Ii of Enterohemorrhagic Escherichia coli and Use of the Monoclonal Antibodies in a Colony Enzyme-Linked Immunosorbent Assay. J Clin Microbiol 26, no. 10 (1988): 2127–31.PubMedGoogle Scholar
  49. Rasko, D. A., C. G. Moreira, R. Li de, N. C. Reading, J. M. Ritchie, M. K. Waldor, N. Williams, R. Taussig, S. Wei, M. Roth, D. T. Hughes, J. F. Huntley, M. W. Fina, J. R. Falck, and V. Sperandio. Targeting Qsec Signaling and Virulence for Antibiotic Development. Science 321, no. 5892 (2008): 1078–80.PubMedCrossRefGoogle Scholar
  50. Reading, N. C., A. G. Torres, M. M. Kendall, D. T. Hughes, K. Yamamoto, and V. Sperandio. A Novel Two-Component Signaling System That Activates Transcription of an Enterohemorrhagic Escherichia coli Effector Involved in Remodeling of Host Actin. J Bacteriol 189, no. 6 (2007): 2468–76.PubMedCrossRefGoogle Scholar
  51. Ritter, A., D. L. Gally, P. B. Olsen, U. Dobrindt, A. Friedrich, P. Klemm, and J. Hacker. The Pai-Associated Leux Specific Trna5(Leu) Affects Type 1 Fimbriation in Pathogenic Escherichia coli by Control of Fimb Recombinase Expression. Mol Microbiol 25, no. 5 (1997): 871–82.PubMedCrossRefGoogle Scholar
  52. Roe, A. J., D. E. Hoey, and D. L. Gally. Regulation, Secretion and Activity of Type Iii-Secreted Proteins of Enterohaemorrhagic Escherichia coli O157. Biochem Soc Trans 31, no. Pt 1 (2003): 98–103.PubMedGoogle Scholar
  53. Rosenshine, I., S. Ruschkowski, and B. B. Finlay. Expression of Attaching/Effacing Activity by Enteropathogenic Escherichia coli Depends on Growth Phase, Temperature, and Protein Synthesis Upon Contact with Epithelial Cells. Infect Immun 64, no. 3 (1996): 966–73.PubMedGoogle Scholar
  54. Russell, R. M., F. C. Sharp, D. A. Rasko, and V. Sperandio. Qsea and Grlr/Grla Regulation of the Locus of Enterocyte Effacement Genes in Enterohemorrhagic Escherichia coli. J Bacteriol 189, no. 14 (2007): 5387–92.PubMedCrossRefGoogle Scholar
  55. Schauder, S., K. Shokat, M. G. Surette, and B. L. Bassler. The Luxs Family of Bacterial Autoinducers: Biosynthesis of a Novel Quorum-Sensing Signal Molecule. Mol Microbiol 41, no. 2 (2001): 463–76.PubMedCrossRefGoogle Scholar
  56. Schmitt, C. K., M. L. McKee, and A. D. O’Brien. Two Copies of Shiga-Like Toxin Ii-Related Genes Common in Enterohemorrhagic Escherichia coli Strains Are Responsible for the Antigenic Heterogeneity of the O157:H- Strain E32511. Infect Immun 59, no. 3 (1991): 1065–73.PubMedGoogle Scholar
  57. Sharma, V. K., and R. L. Zuerner. Role of Hha and Ler in Transcriptional Regulation of the Esp Operon of Enterohemorrhagic Escherichia coli O157:H7. J Bacteriol 186, no. 21 (2004): 7290–301.PubMedCrossRefGoogle Scholar
  58. Sharp, F. C., and V. Sperandio. Qsea Directly Activates Transcription of Lee1 in Enterohemorrhagic Escherichia coli. Infect Immun 75, no. 5 (2007): 2432–40.PubMedCrossRefGoogle Scholar
  59. Sperandio, V., C. C. Li, and J. B. Kaper. Quorum-Sensing Escherichia coli Regulator A: A Regulator of the Lysr Family Involved in the Regulation of the Locus of Enterocyte Effacement Pathogenicity Island in Enterohemorrhagic E. coli. Infect Immun 70, no. 6 (2002): 3085–93.PubMedCrossRefGoogle Scholar
  60. Sperandio, V., J. L. Mellies, W. Nguyen, S. Shin, and J. B. Kaper. Quorum Sensing Controls Expression of the Type Iii Secretion Gene Transcription and Protein Secretion in Enterohemorrhagic and Enteropathogenic Escherichia coli. Proc Natl Acad Sci U S A 96, no. 26 (1999): 15196–201.PubMedCrossRefGoogle Scholar
  61. Sperandio, V., A. G. Torres, J. A. Giron, and J. B. Kaper. Quorum Sensing Is a Global Regulatory Mechanism in Enterohemorrhagic Escherichia coli O157:H7. J Bacteriol 183, no. 17 (2001): 5187–97.PubMedCrossRefGoogle Scholar
  62. Sperandio, V., A. G. Torres, B. Jarvis, J. P. Nataro, and J. B. Kaper. Bacteria-Host Communication: The Language of Hormones. Proc Natl Acad Sci U S A 100, no. 15 (2003): 8951–6.PubMedCrossRefGoogle Scholar
  63. Sperandio, V., A. G. Torres, and J. B. Kaper. Quorum Sensing Escherichia coli Regulators B and C (Qsebc): A Novel Two-Component Regulatory System Involved in the Regulation of Flagella and Motility by Quorum Sensing in E. coli. Mol Microbiol 43, no. 3 (2002): 809–21.PubMedCrossRefGoogle Scholar
  64. Surette, M. G., and B. L. Bassler. Quorum Sensing in Escherichia coli and Salmonella typhimurium. Proc Natl Acad Sci U S A 95, no. 12 (1998): 7046–50.PubMedCrossRefGoogle Scholar
  65. Surette, M. G., M. B. Miller, and B. L. Bassler. Quorum Sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: A New Family of Genes Responsible for Autoinducer Production. Proc Natl Acad Sci U S A 96, no. 4 (1999): 1639–44.PubMedCrossRefGoogle Scholar
  66. 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. An Extensive Repertoire of Type Iii Secretion Effectors in Escherichia coli O157 and the Role of Lambdoid Phages in Their Dissemination. Proc Natl Acad Sci U S A 103, no. 40 (2006): 14941–6.PubMedCrossRefGoogle Scholar
  67. Tomson, F. L., V. K. Viswanathan, K. J. Kanack, R. P. Kanteti, K. V. Straub, M. Menet, J. B. Kaper, and G. Hecht. Enteropathogenic Escherichia coli Espg Disrupts Microtubules and in Conjunction with Orf3 Enhances Perturbation of the Tight Junction Barrier. Mol Microbiol 56, no. 2 (2005): 447–64.PubMedCrossRefGoogle Scholar
  68. Tu, X., I. Nisan, C. Yona, E. Hanski, and I. Rosenshine. Esph, a New Cytoskeleton-Modulating Effector of Enterohaemorrhagic and Enteropathogenic Escherichia coli. Mol Microbiol 47, no. 3 (2003): 595–606.PubMedCrossRefGoogle Scholar
  69. Waddell, T., S. Head, M. Petric, A. Cohen, and C. Lingwood. Globotriosyl Ceramide Is Specifically Recognized by the Escherichia coli Verocytotoxin 2. Biochem Biophys Res Commun 152, no. 2 (1988): 674–9.PubMedCrossRefGoogle Scholar
  70. Walters, M., and V. Sperandio. Autoinducer 3 and Epinephrine Signaling in the Kinetics of Locus of Enterocyte Effacement Gene Expression in Enterohemorrhagic Escherichia coli. Infect Immun 74, no. 10 (2006): 5445–55.PubMedCrossRefGoogle Scholar
  71. Weiss, D. S., A. Brotcke, T. Henry, J. J. Margolis, K. Chan, and D. M. Monack. In Vivo Negative Selection Screen Identifies Genes Required for Francisella Virulence. Proc Natl Acad Sci U S A 104, no. 14 (2007): 6037–42.PubMedCrossRefGoogle Scholar
  72. Wilson, R. K., R. K. Shaw, S. Daniell, S. Knutton, and G. Frankel. Role of Escf, a Putative Needle Complex Protein, in the Type Iii Protein Translocation System of Enteropathogenic Escherichia coli. Cellular Microbiology 3, no. 11 (2001): 753–62.PubMedCrossRefGoogle Scholar
  73. Yamashima, T. Jokichi Takamine (1854-1922), the Samurai Chemist, and His Work on Adrenalin. J Med Biogr 11, no. 2 (2003): 95–102.PubMedGoogle Scholar
  74. Zhang, L., R. R. Chaudhuri, C. Constantinidou, J. L. Hobman, M. D. Patel, A. C. Jones, D. Sarti, A. J. Roe, I. Vlisidou, R. K. Shaw, F. Falciani, M. P. Stevens, D. L. Gally, S. Knutton, G. Frankel, C. W. Penn, and M. J. Pallen. “Regulators Encoded in the Escherichia coli Type Iii Secretion System 2 Gene Cluster Influence Expression of Genes within the Locus for Enterocyte Effacement in Enterohemorrhagic E. coli O157:H7.” Infect Immun 72, no. 12 (2004): 7282-93.PubMedCrossRefGoogle Scholar
  75. Zhang, W., M. Bielaszewska, T. Kuczius, and H. Karch. Identification, Characterization, and Distribution of a Shiga Toxin 1 Gene Variant (Stx(1c)) in Escherichia coli Strains Isolated from Humans. J Clin Microbiol 40, no. 4 (2002): 1441-6.PubMedCrossRefGoogle Scholar

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© Springer-Verlag New York 2010

Authors and Affiliations

  1. 1.Molecular Microbiology DepartmentUniversity of Texas Southwestern Medical CenterDallasUSA

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