1887

Abstract

Systemic release of norepinephrine (NE) is a component of the acute host response to infection, and studies in the field of microbial endocrinology indicate generally that NE increases the bacterial growth rate and promotes invasive disease. However, NE attenuates experimental invasive pneumococcal disease. We determined that NE promoted pneumococcal growth but paradoxically decreased pneumococcal adhesion to host cells. This effect was independent of the classical adhesin CbpA. Microarray analysis indicated that the effect of NE involved two two-component regulatory systems that both regulate expression of the Piu iron uptake ABC transport operon. We propose that NE, a known siderophore, enhances iron availability to the bacteria, resulting in greater bacterial replication and decreased expression of Piu operon products. Downregulation of the operon includes decreased expression of the Piu-associated adhesin PiuD. Our results suggested that the iron-dependent inhibitory effect of NE on pneumococcal adherence is a mechanism underlying the amelioration of pneumococcal disease by NE.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.065607-0
2013-11-01
2021-03-06
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/11/2333.html?itemId=/content/journal/micro/10.1099/mic.0.065607-0&mimeType=html&fmt=ahah

References

  1. Bansal T., Englert D., Lee J., Hegde M., Wood T. K., Jayaraman A..( 2007;). Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157 : H7 chemotaxis, colonization, and gene expression. Infect Immun75:4597–4607 [CrossRef][PubMed]
    [Google Scholar]
  2. Barnes P. J..( 1990;). Neural control of airway function: new perspectives. Mol Aspects Med11:351–423 [CrossRef][PubMed]
    [Google Scholar]
  3. Bearson B. L., Bearson S. M. D., Uthe J. J., Dowd S. E., Houghton J. O., Lee I., Toscano M. J., Lay D. C. Jr.( 2008;). Iron regulated genes of Salmonella enterica serovar Typhimurium in response to norepinephrine and the requirement of FepDGC for norepinephrine-enhanced growth. Microbes Infect10:807–816 [CrossRef][PubMed]
    [Google Scholar]
  4. Burton C. L., Chhabra S. R., Swift S., Baldwin T. J., Withers H., Hill S. J., Williams P..( 2002;). The growth response of Escherichia coli to neurotransmitters and related catecholamine drugs requires a functional enterobactin biosynthesis and uptake system. Infect Immun70:5913–5923 [CrossRef][PubMed]
    [Google Scholar]
  5. Cakan G., Turkoz M., Turan T., Ahmed K., Nagatake T..( 2003;). S-carboxymethylcysteine inhibits the attachment of Streptococcus pneumoniae to human pharyngeal epithelial cells. Microb Pathog34:261–265 [CrossRef][PubMed]
    [Google Scholar]
  6. Chen C., Brown D. R., Xie Y., Green B. T., Lyte M..( 2003;). Catecholamines modulate Escherichia coli O157 : H7 adherence to murine cecal mucosa. Shock20:183–188 [CrossRef][PubMed]
    [Google Scholar]
  7. Clarke M. B., Hughes D. T., Zhu C., Boedeker E. C., Sperandio V..( 2006;). The QseC sensor kinase: a bacterial adrenergic receptor. Proc Natl Acad Sci U S A103:10420–10425 [CrossRef][PubMed]
    [Google Scholar]
  8. Cogan T. A., Thomas A. O., Rees L. E., Taylor A. H., Jepson M. A., Williams P. H., Ketley J., Humphrey T. J..( 2007;). Norepinephrine increases the pathogenic potential of Campylobacter jejuni.. Gut56:1060–1065 [CrossRef][PubMed]
    [Google Scholar]
  9. De Backer D., Biston P., Devriendt J., Madl C., Chochrad D., Aldecoa C., Brasseur A., Defrance P., Gottignies P., Vincent J.-L..SOAP II Investigators( 2010;). Comparison of dopamine and norepinephrine in the treatment of shock. N Engl J Med362:779–789 [CrossRef][PubMed]
    [Google Scholar]
  10. Esler M., Jennings G., Korner P., Blombery P., Sacharias N., Leonard P..( 1984;). Measurement of total and organ-specific norepinephrine kinetics in humans. Am J Physiol247:E21–E28[PubMed]
    [Google Scholar]
  11. Freestone P. P., Lyte M..( 2008;). Microbial endocrinology: experimental design issues in the study of interkingdom signalling in infectious disease. Adv Appl Microbiol64:75–105 [CrossRef][PubMed]
    [Google Scholar]
  12. Freestone P. P., Lyte M., Neal C. P., Maggs A. F., Haigh R. D., Williams P. H..( 2000;). The mammalian neuroendocrine hormone norepinephrine supplies iron for bacterial growth in the presence of transferrin or lactoferrin. J Bacteriol182:6091–6098 [CrossRef][PubMed]
    [Google Scholar]
  13. Freestone P. P. E., Haigh R. D., Williams P. H., Lyte M..( 2003;). Involvement of enterobactin in norepinephrine-mediated iron supply from transferrin to enterohaemorrhagic Escherichia coli.. FEMS Microbiol Lett222:39–43 [CrossRef][PubMed]
    [Google Scholar]
  14. Freestone P. P., Haigh R. D., Lyte M..( 2007;). Specificity of catecholamine-induced growth in Escherichia coli O157 : H7, Salmonella enterica and Yersinia enterocolitica.. FEMS Microbiol Lett269:221–228 [CrossRef][PubMed]
    [Google Scholar]
  15. Freestone P. P., Sandrini S. M., Haigh R. D., Lyte M..( 2008;). Microbial endocrinology: how stress influences susceptibility to infection. Trends Microbiol16:55–64 [CrossRef][PubMed]
    [Google Scholar]
  16. Gonzales X. F., Deshmukh A., Pulse M., Johnson K., Jones H. P..( 2008;). Stress-induced differences in primary and secondary resistance against bacterial sepsis correspond with diverse corticotropin releasing hormone receptor expression by pulmonary CD11c+ MHC II+ and CD11c MHC II+ APCs. Brain Behav Immun22:552–564 [CrossRef][PubMed]
    [Google Scholar]
  17. Hegde M., Wood T. K., Jayaraman A..( 2009;). The neuroendocrine hormone norepinephrine increases Pseudomonas aeruginosa PA14 virulence through the las quorum-sensing pathway. Appl Microbiol Biotechnol84:763–776 [CrossRef][PubMed]
    [Google Scholar]
  18. Hughes D. T., Clarke M. B., Yamamoto K., Rasko D. A., Sperandio V..( 2009;). The QseC adrenergic signaling cascade in enterohemorrhagic E. coli (EHEC). PLoS Pathog5:e1000553 [CrossRef][PubMed]
    [Google Scholar]
  19. Jomaa M., Yuste J., Paton J. C., Jones C., Dougan G., Brown J. S..( 2005;). Antibodies to the iron uptake ABC transporter lipoproteins PiaA and PiuA promote opsonophagocytosis of Streptococcus pneumoniae.. Infect Immun73:6852–6859 [CrossRef][PubMed]
    [Google Scholar]
  20. Jordan D..( 2001;). Central nervous pathways and control of the airways. Respir Physiol125:67–81 [CrossRef][PubMed]
    [Google Scholar]
  21. Kadioglu A., Weiser J. N., Paton J. C., Andrew P. W..( 2008;). The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol6:288–301 [CrossRef][PubMed]
    [Google Scholar]
  22. Kontiokari T., Uhari M., Koskela M..( 1998;). Antiadhesive effects of xylitol on otopathogenic bacteria. J Antimicrob Chemother41:563–565 [CrossRef][PubMed]
    [Google Scholar]
  23. Kurola P., Tapiainen T., Sevander J., Kaijalainen T., Leinonen M., Uhari M., Saukkoriipi A..( 2011;). Effect of xylitol and other carbon sources on Streptococcus pneumoniae biofilm formation and gene expression in vitro.. APMIS119:135–142 [CrossRef][PubMed]
    [Google Scholar]
  24. Kvetnansky R..( 2004;). Stressor specificity and effect of prior experience on catecholamine biosynthetic enzyme phenylethanolamine N-methyltransferase. Ann N Y Acad Sci1032:117–129 [CrossRef][PubMed]
    [Google Scholar]
  25. Lyte M., Erickson A. K., Arulanandam B. P., Frank C. D., Crawford M. A., Francis D. H..( 1997;). Norepinephrine-induced expression of the K99 pilus adhesin of enterotoxigenic Escherichia coli.. Biochem Biophys Res Commun232:682–686 [CrossRef][PubMed]
    [Google Scholar]
  26. Lyte M., Freestone P. P., Neal C. P., Olson B. A., Haigh R. D., Bayston R., Williams P. H..( 2003;). Stimulation of Staphylococcus epidermidis growth and biofilm formation by catecholamine inotropes. Lancet361:130–135 [CrossRef][PubMed]
    [Google Scholar]
  27. Mann B., Orihuela C., Antikainen J., Gao G., Sublett J., Korhonen T. K., Tuomanen E..( 2006;). Multifunctional role of choline binding protein G in pneumococcal pathogenesis. Infect Immun74:821–829 [CrossRef][PubMed]
    [Google Scholar]
  28. Methner U., Rabsch W., Reissbrodt R., Williams P. H..( 2008;). Effect of norepinephrine on colonisation and systemic spread of Salmonella enterica in infected animals: role of catecholate siderophore precursors and degradation products. Int J Med Microbiol298:429–439 [CrossRef][PubMed]
    [Google Scholar]
  29. Miethke M., Skerra A..( 2010;). Neutrophil gelatinase-associated lipocalin expresses antimicrobial activity by interfering with L-norepinephrine-mediated bacterial iron acquisition. Antimicrob Agents Chemother54:1580–1589 [CrossRef][PubMed]
    [Google Scholar]
  30. Moreira C. G., Weinshenker D., Sperandio V..( 2010;). QseC mediates Salmonella enterica serovar typhimurium virulence in vitro and in vivo.. Infect Immun78:914–926 [CrossRef][PubMed]
    [Google Scholar]
  31. Moscoso M., García E., López R..( 2006;). Biofilm formation by Streptococcus pneumoniae: role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion. J Bacteriol188:7785–7795 [CrossRef][PubMed]
    [Google Scholar]
  32. O’Brien K. L., Wolfson L. J., Watt J. P., Henkle E., Deloria-Knoll M., McCall N., Lee E., Mulholland K., Levine O. S., Cherian T..Hib and Pneumococcal Global Burden of Disease Study Team( 2009;). Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet374:893–902 [CrossRef][PubMed]
    [Google Scholar]
  33. O’Donnell P. M., Aviles H., Lyte M., Sonnenfeld G..( 2006;). Enhancement of in vitro growth of pathogenic bacteria by norepinephrine: importance of inoculum density and role of transferrin. Appl Environ Microbiol72:5097–5099 [CrossRef][PubMed]
    [Google Scholar]
  34. Orihuela C. J., Gao G., Francis K. P., Yu J., Tuomanen E. I..( 2004;). Tissue-specific contributions of pneumococcal virulence factors to pathogenesis. J Infect Dis190:1661–1669 [CrossRef][PubMed]
    [Google Scholar]
  35. Paris I., Martinez-Alvarado P., Perez-Pastene C., Vieira M. N., Olea-Azar C., Raisman-Vozari R., Cardenas S., Graumann R., Caviedes P., Segura-Aguilar J..( 2005;). Monoamine transporter inhibitors and norepinephrine reduce dopamine-dependent iron toxicity in cells derived from the substantia nigra. J Neurochem92:1021–1032 [CrossRef][PubMed]
    [Google Scholar]
  36. Rasko D. A., Moreira C. G., Li R., Reading N. C., Ritchie J. M., Waldor M. K., Williams N., Taussig R., Wei S..& other authors ( 2008;). Targeting QseC signaling and virulence for antibiotic development. Science321:1078–1080 [CrossRef][PubMed]
    [Google Scholar]
  37. Rosch J. W., Mann B., Thornton J., Sublett J., Tuomanen E..( 2008;). Convergence of regulatory networks on the pilus locus of Streptococcus pneumoniae.. Infect Immun76:3187–3196 [CrossRef][PubMed]
    [Google Scholar]
  38. Sandrini S. M., Shergill R., Woodward J., Muralikuttan R., Haigh R. D., Lyte M., Freestone P. P..( 2010;). Elucidation of the mechanism by which catecholamine stress hormones liberate iron from the innate immune defense proteins transferrin and lactoferrin. J Bacteriol192:587–594 [CrossRef][PubMed]
    [Google Scholar]
  39. Scheckelhoff M. R., Telford S. R., Wesley M., Hu L. T..( 2007;). Borrelia burgdorferi intercepts host hormonal signals to regulate expression of outer surface protein A. Proc Natl Acad Sci U S A104:7247–7252 [CrossRef][PubMed]
    [Google Scholar]
  40. Schreurs A. J., Nijkamp F. P..( 1982;). Haemophilus influenzae induced loss of lung beta-adrenoceptor binding sites and modulation by changes in peripheral catecholaminergic input. Eur J Pharmacol77:95–102 [CrossRef][PubMed]
    [Google Scholar]
  41. Schreurs A. J., Versteeg D. H., Nijkamp F. P..( 1982;). Involvement of catecholamines in Haemophilus influenzae induced decrease of beta-adrenoceptor function. Naunyn Schmiedebergs Arch Pharmacol320:235–239 [CrossRef][PubMed]
    [Google Scholar]
  42. Standish A. J., Stroeher U. H., Paton J. C..( 2007;). The pneumococcal two-component signal transduction system RR/HK06 regulates CbpA and PspA by two distinct mechanisms. J Bacteriol189:5591–5600 [CrossRef][PubMed]
    [Google Scholar]
  43. Suer E., Sayrac S., Sarinay E., Ozturk H. E., Turkoz M., Ichinose A., Nagatake T., Ahmed K..( 2008;). Variation in the attachment of Streptococcus pneumoniae to human pharyngeal epithelial cells after treatment with S-carboxymethylcysteine. J Infect Chemother14:333–336 [CrossRef][PubMed]
    [Google Scholar]
  44. Talbot U. M., Paton A. W., Paton J. C..( 1996;). Uptake of Streptococcus pneumoniae by respiratory epithelial cells. Infect Immun64:3772–3777[PubMed]
    [Google Scholar]
  45. Tapiainen T., Sormunen R., Kaijalainen T., Kontiokari T., Ikäheimo I., Uhari M..( 2004;). Ultrastructure of Streptococcus pneumoniae after exposure to xylitol. J Antimicrob Chemother54:225–228 [CrossRef][PubMed]
    [Google Scholar]
  46. Vlisidou I., Lyte M., van Diemen P. M., Hawes P., Monaghan P., Wallis T. S., Stevens M. P..( 2004;). The neuroendocrine stress hormone norepinephrine augments Escherichia coli O157 : H7-induced enteritis and adherence in a bovine ligated ileal loop model of infection. Infect Immun72:5446–5451 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.065607-0
Loading
/content/journal/micro/10.1099/mic.0.065607-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error