Cited by 902Bacterial biofilms and quorum sensingEscherichia coli research studiesBacterial Genetics and Biotechnology

Bacteria–host communication: the language of hormones

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Sperandio, Vanessa, Torres, Alfredo G., Jarvis, Bruce, Nataro, James P., Kaper, James B.·2003·Proceedings of the National Academy of Sciences

Abstract

The interbacterial communication system known as quorum sensing (QS) utilizes hormone-like compounds referred to as autoinducers to regulate bacterial gene expression. Enterohemorrhagic Escherichia coli (EHEC) serotype O157:H7 is the agent responsible for outbreaks of bloody diarrhea in several countries. We previously proposed that EHEC uses a QS regulatory system to "sense" that it is within the intestine and activate genes essential for intestinal colonization. The QS system used by EHEC is the LuxS/autoinducer 2 (AI-2) system extensively involved in interspecies communication. The autoinducer AI-2 is a furanosyl borate diester whose synthesis depends on the enzyme LuxS. Here we show that an EHEC luxS mutant, unable to produce the bacterial autoinducer, still responds to a eukaryotic cell signal to activate expression of its virulence genes. We have identified this signal as the hormone epinephrine and show that beta- and alpha-adrenergic antagonists can block the bacterial response to this hormone. Furthermore, using purified and in vitro synthesized AI-2 we showed that AI-2 is not the autoinducer involved in the bacterial signaling. EHEC produces another, previously undescribed autoinducer (AI-3) whose synthesis depends on the presence of LuxS. These results imply a potential cross-communication between the luxS/AI-3 bacterial QS system and the epinephrine host signaling system. Given that eukaryotic cell-to-cell signaling typically occurs through hormones, and that bacterial cell-to-cell signaling occurs through QS, we speculate that QS might be a "language" by which bacteria and host cells communicate.

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Crossref · 10.1073/pnas.1537100100

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  • Bacteria produce noradrenaline as a quorum sensing molecule, and noradrenaline and adrenaline can promote pathogenesis and growth.

    “bacteria produce noradrenaline as a quorum sensing molecule, and noradrenaline and adrenaline can promote pathogenesis and growth (229, 230)”
  • Enterohemorrhagic E. coli can sense luminal norepinephrine or adrenaline to express its virulence traits.

    “Enterohemorrhagic E. coli can sense luminal norepinephrine or adrenaline to express its virulence traits.45”
  • Exogenous epinephrine is an inducer of the O157:H7 virulence factor.

    “Sperandio et al. showed that exogenous epinephrine is an inducer of the 0157:H7 virulence factor.120”

    From The Gut Microbiome and the Brain (2014) · cites this paper as [120]

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  1. [2]McDaniel, T. K., Jarvis, K. G., Donnenberg, M. S. & Kaper, J. B. (1995) Proc. Natl. Acad. Sci. USA 92, 1664–1668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. [3]Elliott, S. J., Wainwright, L. A., McDaniel, T. K., Jarvis, K. G., Deng, Y. K., Lai, L. C., McNamara, B. P., Donnenberg, M. S. & Kaper, J. B. (1998) Mol. Microbiol. 28, 1–4. [DOI] [PubMed] [Google Scholar]
  3. [4]Mellies, J. L., Elliott, S. J., Sperandio, V., Donnenberg, M. S. & Kaper, J. B. (1999) Mol. Microbiol. 33, 296–306. [DOI] [PubMed] [Google Scholar]
  4. [5]Sperandio, V., Mellies, J. L., Delahay, R. M., Frankel, G., Crawford, J. A., Nguyen, W. & Kaper, J. B. (2000) Mol. Microbiol. 38, 781–793. [DOI] [PubMed] [Google Scholar]
  5. [6]Sperandio, V., Mellies, J. L., Nguyen, W., Shin, S. & Kaper, J. B. (1999) Proc. Natl. Acad. Sci. USA 96, 15196–15201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. [7]Sperandio, V., Torres, A. G., Giron, J. A. & Kaper, J. B. (2001) J. Bacteriol. 183, 5187–5197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. [8]Chen, X., Schauder, S., Potier, N., Van Dorssealaer, A., Pelczer, I., Bassler, B. L. & Hughson, F. M. (2002) Nature 415, 545–549. [DOI] [PubMed] [Google Scholar]
  8. [9]Surette, M. G., Miller, M. B. & Bassler, B. L. (1999) Proc. Natl. Acad. Sci. USA 96, 1639–1644. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. [10]Schauder, S., Shokat, K., Surette, M. G. & Bassler, B. L. (2001) Mol. Microbiol. 41, 463–476. [DOI] [PubMed] [Google Scholar]
  10. [11]de Kievit, T. R. & Iglewski, B. H. (2000) Infect. Immun. 68, 4839–4849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. [12]Schauder, S. & Bassler, B. L. (2001) Genes Dev. 15, 1468–1480. [DOI] [PubMed] [Google Scholar]
  12. [13]Sperandio, V., Li, C. C. & Kaper, J. B. (2002) Infect. Immun. 70, 3085–3093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. [14]Sperandio, V., Torres, A. G. & Kaper, J. B. (2002) Mol. Microbiol. 43, 809–821. [DOI] [PubMed] [Google Scholar]
  14. [15]Griffin, P. M., Ostroff, S. M., Tauxe, R. V., Greene, K. D., Wells, J. G., Lewis, J. H. & Blake, P. A. (1988) Ann. Intern. Med. 109, 705–712. [DOI] [PubMed] [Google Scholar]
  15. [17]Surette, M. G. & Bassler, B. L. (1998) Proc. Natl. Acad. Sci. USA 95, 7046–7050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. [18]Jarvis, K. G., Giron, J. A., Jerse, A. E., McDaniel, T. K., Donnenberg, M. S. & Kaper, J. B. (1995) Proc. Natl. Acad. Sci. USA 92, 7996–8000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. [19]Knutton, S., Baldwin, T., Williams, P. H. & McNeish, A. S. (1989) Infect. Immun. 57, 1290–1298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. [20]Behrens, M., Sheikh, J. & Nataro, J. P. (2002) Infect. Immun. 70, 2915–2925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. [21]Elliott, S. J., Hutcheson, S. W., Dubois, M. S., Mellies, J. L., Wainwright, L. A., Batchelor, M., Frankel, G., Knutton, S. & Kaper, J. B. (1999) Mol. Microbiol. 33, 1176–1189. [DOI] [PubMed] [Google Scholar]
  20. [23]Lyte, M., Frank, C. D. & Green, B. T. (1996) FEMS Microbiol. Lett. 139, 155–159. [DOI] [PubMed] [Google Scholar]
  21. [24]Kinney, K. S., Austin, C. E., Morton, D. S. & Sonnenfeld, G. (2000) Life Sci. 67, 3075–3085. [DOI] [PubMed] [Google Scholar]
  22. [25]Elwan, M. A. & Sakuragawa, N. (1997) NeuroReport 8, 3435–3438. [DOI] [PubMed] [Google Scholar]
  23. [26]Eisenhofer, G., Aneman, A., Friberg, P., Hooper, D., Fandriks, L., Lonroth, H., Hunyady, B. & Mezey, E. (1997) J. Clin. Endocrinol. Metab. 82, 3864–3871. [DOI] [PubMed] [Google Scholar]
  24. [27]Horger, S., Schultheiss, G. & Diener, M. (1998) Am. J. Physiol. 275, G1367–G1376. [DOI] [PubMed] [Google Scholar]
  25. [28]Visick, K. L., Foster, J., Doino, J., McFall-Ngai, M. & Ruby, E. G. (2000) J. Bacteriol. 182, 4578–4586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. [29]Hooper, L. V. & Gordon, J. I. (2001) Science 292, 1115–1118. [DOI] [PubMed] [Google Scholar]
  27. [30]Neish, A. S., Gewirtz, A. T., Zeng, H., Young, A. N., Hobert, M. E., Karmali, V., Rao, A. S. & Madara, J. L. (2000) Science 289, 1560–1563. [DOI] [PubMed] [Google Scholar]
  28. [31]Telford, G., Wheeler, D., Williams, P., Tomkins, P. T., Appleby, P., Sewell, H., Stewart, G. S., Bycroft, B. W. & Pritchard, D. I. (1998) Infect. Immun. 66, 36–42. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. [32]Smith, R. S., Fedyk, E. R., Springer, T. A., Mukaida, N., Iglewski, B. H. & Phipps, R. P. (2001) J. Immunol. 167, 366–374. [DOI] [PubMed] [Google Scholar]
  30. [33]Palfreyman, R. W., Watson, M. L., Eden, C. & Smith, A. W. (1997) Infect. Immun. 65, 617–622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. [34]Gallio, M., Sturgill, G., Rather, P. & Kylsten, P. (2002) Proc. Natl. Acad. Sci. USA 99, 12208–12213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. [35]Bender, D. A. (1985) Amino Acid Metabolism (Wiley, New York).
  33. [36]Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., et al. (2001) Nature 409, 860–921. [DOI] [PubMed] [Google Scholar]
  34. [37]Freestone, P. P., Haigh, R. D., Williams, P. H. & Lyte, M. (1999) FEMS Microbiol. Lett. 172, 53–60. [DOI] [PubMed] [Google Scholar]
  35. [38]Freestone, P. P., Lyte, M., Neal, C. P., Maggs, A. F., Haigh, R. D. & Williams, P. H. (2000) J. Bacteriol. 182, 6091–6098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. [39]Burton, C. L., Chhabra, S. R., Swift, S., Baldwin, T. J., Withers, H., Hill, S. J. & Williams, P. (2002) Infect. Immun. 70, 5913–5923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. [40]Lyte, M., Arulanandam, B. P. & Frank, C. D. (1996) J. Lab. Clin. Med. 128, 392–398. [DOI] [PubMed] [Google Scholar]
  38. [41]Lyte, M., Erickson, A. K., Arulanandam, B. P., Frank, C. D., Crawford, M. A. & Francis, D. H. (1997) Biochem. Biophys. Res. Commun. 232, 682–686. [DOI] [PubMed] [Google Scholar]
  39. [42]Lamont, I. L., Beare, P. A., Ochsner, U., Vasil, A. I. & Vasil, M. L. (2002) Proc. Natl. Acad. Sci. USA 99, 7072–7077. [DOI] [PMC free article] [PubMed] [Google Scholar]

Cited by

Sorted by citations

Authors
Sperandio, V., Torres, A. G., Jarvis, B., Nataro, J. P., & Kaper, J. B.
Affiliations
University of Maryland, Baltimore (US)
Venue
Proceedings of the National Academy of Sciences
Published
2003-07-07
Volume
100
Issue
15
Pages
8951-8956
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
OpenAlex
W2040641257
Cited by
902
References
42
Citations by year
2026: 19 · 2025: 16 · 2024: 31 · 2023: 35 · 2022: 37 · 2021: 36 · 2020: 26 · 2019: 44 · 2018: 38 · 2017: 29 · 2016: 39 · 2015: 37 · 2014: 44 · 2013: 34 · 2012: 60
FWCI
14.16
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (5r01ai041325-05)
  • National Institute of Allergy and Infectious Diseases (R01AI021657, AI 41325, AI21657, R37AI021657)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
quorum sensing, autoinducer-2, LuxS, Escherichia coli O157:H7, epinephrine, virulence gene expression, adrenergic antagonists, intestinal colonization
MeSH terms
Bacterial Proteins, Epinephrine, Escherichia coli Infections, Genes, Bacterial, HeLa Cells, Homoserine, Humans, Lactones, Mutation, Phosphoproteins, Carbon-Sulfur Lyases, Virulence, Signal Transduction, Gene Expression Regulation, Bacterial, Escherichia coli O157, Escherichia coli Proteins, In Vitro Techniques

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