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The Role of the QseC Quorum-Sensing Sensor Kinase in Epinephrine-Enhanced Motility and Biofilm Formation by Escherichia coli

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Abstract

Biofilms play a pivotal role in infections related to devices. Biofilm formation in Escherichia coli is mediated by the quorum-sensing E. coli regulator C (QseC), the histidine sensor kinase that can sense epinephrine (EPI)/norepinephrine (NE). In this study, we evaluate the role of the QseC quorum-sensing sensor kinase in epinephrine-enhanced motility and biofilm formation by E. coli. An E. coli MC1000 qseC mutant was constructed. We investigated the role of the QseC in the formation of biofilms on the surface of medical-grade polyvinyl chloride using the E. coli K-12 MC1000 strain as well as a corresponding qseC mutant. Addition of EPI/NE increased biofilm formation by wild-type K-12 MC1000 but not by the isogenic qseC mutant. Scanning confocal laser microscopy corroborated these results by showing that EPI/NE addition significantly increased biofilm’s thickness. As expected, the addition of EPI/NE to the qseC mutant, which lacks the ability to sense the hormones, failed to stimulate biofilm formation. Since EPI/NE addition increased bacterial motility, we proposed that their stimulatory effects on biofilm formation occur by enhancing bacterial motility and altering biofilm architecture. We also found that EPI/NE regulate motility and the biofilm phenotype via QseC, as motility was diminished and biofilm formation was significantly decreased in a qseC deletion mutant. These results indicate that EPI/NE induce E. coli biofilm formation on the surface of polyvinyl chloride through QseC. Cross-talk between E. coli (quorum sensing) and host hormones may explain the pathogen-caused opportunistic infections that occur in patients with prosthetic devices used during hormone level fluctuations in the host.

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References

  1. Karchmer, A. W. (2000). Infections of prosthetic heart valves. In F. Waldvogel & A. L. Bisno (Eds.), Infections associated with indwelling devices (pp. 145–172). Washington DC: American Society for Microbiology.

    Google Scholar 

  2. Karchmer, A. W., & Longworth, D. L. (2002). Infections of intracardiac devices. Infectious Disease Clinics of North America, 16, 477–505.

    Article  PubMed  Google Scholar 

  3. Steckelberg, J. M., & Osmon, D. R. (2000). Prosthetic joint infections. In F. Waldvogel & A. L. Bisno (Eds.), Infections associated with indwelling devices (pp. 173–209). Washington DC: American Society for Microbiology.

    Google Scholar 

  4. Kulkarni, A., Drake, J. M., & Lamberti-Pasculli, M. (2001). Cerebrospinal fluid shunt infection, a prospective study of risk factors. Journal of Neurosurgery, 94, 195–201.

    Article  CAS  PubMed  Google Scholar 

  5. Turgut, M., Alabaz, D., Erbey, F., Kocabas, E., Erman, T., Alhan, E., et al. (2005). Cerebrospinal fluid shunt infections in children. Pediatric Neurosurgery, 41, 131–136.

    Article  CAS  PubMed  Google Scholar 

  6. Hedrick, T. L., Adams, J. D., & Sawyer, R. G. (2006). Implant-associated infections. An overview. Journal of Long-Term Effects of Medical Implants, 16, 83–99.

    Article  CAS  PubMed  Google Scholar 

  7. Costerton, J. W., Stewart, P. S., & Greenberg, E. P. (1999). Bacterial biofilms: a common cause of persistent infections. Science, 284, 1318–1322.

    Article  CAS  PubMed  Google Scholar 

  8. Costerton, J. W. (2005). Biofilm theory can guide the treatment of device-related orthopaedic infections. Clinical Orthopaedics and Related Research, 437, 7–11.

    Article  PubMed  Google Scholar 

  9. Costerton, J. W., Montanaro, L., & Arciola, C. R. (2007). Bacterial communications in implant infections: a target for an intelligence war. International Journal of Artificial Organs, 30, 757–763.

    CAS  PubMed  Google Scholar 

  10. Hall-Stoodley, L., & Stoodley, P. (2009). Evolving concepts in biofilm infections. Cellular Microbiology, 11, 1034–1043.

    Article  CAS  PubMed  Google Scholar 

  11. Francolini, I., & Donelli, G. (2010). Prevention and control of biofilm-based medical-device- related infections. FEMS Immunology and Medical Microbiology, 59, 227–238.

    CAS  PubMed  Google Scholar 

  12. Aslam, S. (2008). Effect of antibacterials on biofilms. American Journal of Infection Control, 36(10), 9–11.

    Article  Google Scholar 

  13. Lewis, K. (2008). Multidrug tolerance of biofilms and persister cells. Current Topics in Microbiology and Immunology, 322, 107–131.

    CAS  PubMed  Google Scholar 

  14. Sperandio, V., Torres, A. G., & Kaper, J. B. (2002). 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. Molecular Microbiology, 43, 809–821.

    Article  CAS  PubMed  Google Scholar 

  15. Williams, P. (2007). Quorum sensing, communication and cross-kingdom signaling in the bacterial world. Microbiology, 153, 3923–3938.

    Article  CAS  PubMed  Google Scholar 

  16. Li, J., Attila, C., Wang, L., et al. (2007). Quorum sensing in Escherichia coli is signaled by AI-2/LsrR: Effects on small RNA and biofilm architecture. Journal of Bacteriology, 189, 6011–6020.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Walters, M., & Sperandio, V. (2006). Quorum sensing in Escherichia coli and Salmonella. International Journal of Medical Microbiology, 296, 125–131.

    Article  CAS  PubMed  Google Scholar 

  18. Hughes DT, Clarke MB, Yamamoto K, Rasko DA, Sperandio V. (2009) The QseC adrenergic signaling cascade in Enterohemorrhagic E. coli (EHEC). PLoS Pathog, doi: 10.1371/journal.ppat.1000553.

  19. Reading, N. C., Torres, A. G., Kendall, M. M., Hughes, D. T., Yamamoto, K., & Sperandio, V. (2007). A novel two-component signaling system that activates transcription of an enterohemorrhagic Escherichia coli effector involved in remodeling of host actin. Journal of Bacteriology, 189, 2468–2476.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Datsenko, K. A., & Wanner, B. L. (2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proceedings of the National Academy of Sciences of the United States of America, 97, 6640–6645.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Pratt, L. A., & Kolter, R. (1998). Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Molecular Microbiology, 30, 285–293.

    Article  CAS  PubMed  Google Scholar 

  22. Zhao, G. Q., Ye, L. H., Huang, Y. C., Yang, D. K., Li, L., Xu, G., et al. (2011). In vitro model of bacterial biofilm formation on polyvinyl chloride biomaterial. Cell Biochemistry and Biophysics, 61, 371–376.

    Article  CAS  PubMed  Google Scholar 

  23. Sperandio, V., Torres, A. G., Jarvis, B., Nataro, J. P., & Kaper, J. B. (2003). Bacteria-host communication: the language of hormones. Proceedings of the National Academy of Sciences of the United States of America, 100, 8951–8956.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Anderl, J. N., Franklin, M. J., & Stewart, P. S. (2000). Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrobial Agents and Chemotherapy, 44, 1818–1824.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Cunningham, C. D, I. I. I., Slattery, W. H, I. I. I., & Luxford, W. M. (2004). Postoperative infection in cochlear implant patients. Otolaryngology - Head and Neck Surgery, 131, 109–114.

    Article  PubMed  Google Scholar 

  26. Livni, G., Yuhas, Y., Ashkenazi, S., & Michowiz, S. (2004). In vitro bacterial adherence to ventriculoperitoneal shunts. Pediatric Neurosurgery, 40, 64–69.

    Article  CAS  PubMed  Google Scholar 

  27. Waters, C. M., & Bassler, B. L. (2005). Quorum sensing: cell-to-cell communication in bacteria. Annual Review of Cell and Developmental Biology, 21, 319–346.

    Article  CAS  PubMed  Google Scholar 

  28. Keller, L., & Surette, M. G. (2006). Communication in bacteria: an ecological and evolutionary perspective. Nature Reviews Microbiology, 4, 249–258.

    Article  CAS  PubMed  Google Scholar 

  29. Walters, M., Sircili, M. P., & Sperandio, V. (2006). AI-3 synthesis is not dependent on luxS in Escherichia coli. Journal of Bacteriology, 188, 5668–5681.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Kaper, J. B., & Sperandio, V. (2005). Bacterial cell-to-cell signaling in the gastrointestinal tract. Infection and Immunity, 73, 3197–3209.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Pacheco, A. R., & Sperandio, V. (2009). Inter-kingdom signaling: chemical language between bacteria and host. Current Opinion in Microbiology, 12, 192–198.

    Article  CAS  PubMed  Google Scholar 

  32. Curtis, M. M., & Sperandio, V. (2011). A complex relationship: the interaction among symbiotic microbes, invading pathogens, and their mammalian host. Mucosal Immunology, 4, 133–138.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Clarke, M. B., Hughes, D. T., Zhu, C., Boedeker, E. C., & Sperandio, V. (2006). The QseC sensor kinase: a bacterial adrenergic receptor. Proceedings of the National Academy of Sciences of the United States of America, 103, 10420–10425.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Freestone, P. P., Williams, P. H., Haigh, R. D., Maqqs, A. F., Neal, C. P., & Lyte, M. (2002). Growth stimulation of intestinal commensal Escherichia coli by catecholamines: A possible contributory factor in trauma-induced sepsis. Shock, 18, 465–470.

    Article  PubMed  Google Scholar 

  35. Lyte, M., & Ernst, S. (1992). Catecholamine induced growth of gram negative bacteria. Life Sciences, 50, 203–212.

    Article  CAS  PubMed  Google Scholar 

  36. Kopin, I. J., Zukowska-Grojec, Z., Bayorh, M. A., & Goldstein, D. S. (1984). Estimation of intrasynaptic norepinephrine concentrations at vascular neuroeffector junctions in vivo. Naunyn Schmiedebergs Arch Pharmacol, 325, 298–305.

    Article  CAS  PubMed  Google Scholar 

  37. Leinhardt, D. J., Arnold, J., Shipley, K. A., Muqhal, M. M., Little, R. A., & Irving, M. H. (1993). Plasma NE concentrations do not accurately reflect sympathetic nervous system activity in human sepsis. American Journal of Physiology, 265, E284–E288.

    CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank the E. coli Genetic Stock Centre (Yale University) for sending plasmids pKD3, pKD46, pCP20, and E. coli strain MC1000. The authors thank Dr. Zhang HT from the Immunology and Biology Laboratory, Institute of Zoology, Chinese Academy of Science for E. coli isolates and for technical advice. This work was supported by Grants 30872555 and 81260228 from the National Natural Science Foundation of China.

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Authors and Affiliations

  1. Department of Cardiac and Thoracic Surgery, Third Affiliated Hospital of Kunming Medical University, No. 519, KunZhou Road, Kunming, 650118, Yunnan, China

    Kun Yang, Yun-chao Huang, Lian-hua Ye & Guang-jian Li

  2. Department of Anaesthesiology, First Affiliated Hospital of Kunming Medical University, Kunming, 650032, China

    Kun Yang, Jie Huang & Hua-mei Chen

  3. Department of Cardiac Surgery, First Affiliated Hospital of Kunming Medical University, Kunming, 650032, China

    Jun Meng

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  1. Kun Yang
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Correspondence to Yun-chao Huang.

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Kun Yang and Jun Meng have contributed equally to this work.

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Yang, K., Meng, J., Huang, Yc. et al. The Role of the QseC Quorum-Sensing Sensor Kinase in Epinephrine-Enhanced Motility and Biofilm Formation by Escherichia coli . Cell Biochem Biophys 70, 391–398 (2014). https://doi.org/10.1007/s12013-014-9924-5

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