1887

Abstract

, a component of the porcine respiratory disease complex, colonizes the respiratory tract of swine by binding to the cilia of the bronchial epithelial cells. Mechanisms of pathogenesis are poorly understood for , but previous work has indicated that it responds to the environmental stressors heat shock, iron deprivation and oxidative compounds. For successful infection, must effectively resist host responses to the colonization of the respiratory tract. Among these are changes in hormonal levels in the mucosal secretions. Recent work in the stress responses of other bacteria has included the response to the catecholamine norepinephrine. The idea that can respond to a host hormone, however, is novel and has not previously been demonstrated. To test this, organisms in the early exponential phase of growth were exposed to 100 μM norepinephrine for 4 h, and RNA samples from these cultures were collected and compared to RNA samples from control cultures using two-colour PCR-based microarrays. The response included slowed growth and changes in mRNA transcript levels of 84 genes, 53 of which were upregulated in response to norepinephrine. A larger proportion of the genes upregulated than those downregulated were involved with transcription and translation. The downregulated genes were mostly involved with metabolism, which correlated with the reduction in growth of the mycoplasma. Approximately 51 % of the genes were hypothetical with no known function. Thus, in response to norepinephrine, appears to upregulate protein expression while downregulating general metabolism.

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2008-09-01
2019-11-12
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References

  1. Adams, C., Pitzer, J. E. & Minion, F. C. ( 2005; ). In vivo expression analysis of the P97 and P102 paralog families of Mycoplasma hyopneumoniae. Infect Immun 73, 7784–7787.[CrossRef]
    [Google Scholar]
  2. Anderson, M. T. & Armstrong, S. K. ( 2006; ). The Bordetella bfe system: growth and transcriptional response to siderophores, catechols, and neuroendocrine catecholamines. J Bacteriol 188, 5731–5740.[CrossRef]
    [Google Scholar]
  3. 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 Immun 75, 4597–4607.[CrossRef]
    [Google Scholar]
  4. Benjamini, Y. & Hochberg, Y. ( 2000; ). On the adaptive control of the false discovery rate in multiple testing with independent statistics. J Educ Behav Stat 25, 60–83.[CrossRef]
    [Google Scholar]
  5. Chang, L.-J., Chen, W.-H., Minion, F. C. & Shiuan, D. ( 2008; ). Mycoplasmas regulate the expression of heat shock proteins through CIRCE-HrcA interaction. Biochem Biophys Res Commun 367, 213–218.[CrossRef]
    [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. Shock 20, 183–188.[CrossRef]
    [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 A 103, 10420–10425.[CrossRef]
    [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. ( 2006; ). Norepinephrine increases the pathogenic potential of Campylobacter jejuni. Gut 56, 1060–1065.
    [Google Scholar]
  9. DeBey, M. C. & Ross, R. F. ( 1994; ). Ciliostasis and loss of cilia induced by Mycoplasma hyopneumoniae in porcine tracheal organ cultures. Infect Immun 62, 5312–5318.
    [Google Scholar]
  10. Djordjevic, S. P., Cordwell, S. J., Djordjevic, M. A., Wilton, J. & Minion, F. C. ( 2004; ). Proteolytic processing of the Mycoplasma hyopneumoniae cilium adhesin. Infect Immun 72, 2791–2802.[CrossRef]
    [Google Scholar]
  11. Dowd, S. E. ( 2007; ). Escherichia coli O157 : H7 gene expression in the presence of catecholamine norepinephrine. FEMS Microbiol Lett 273, 214–223.[CrossRef]
    [Google Scholar]
  12. 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 Lett 269, 221–228.[CrossRef]
    [Google Scholar]
  13. Gallup, J. M. & Ackermann, M. R. ( 2006; ). Addressing fluorogenic real-time qPCR inhibition using the novel custom Excel file system ‘Focusfield2-6GallupqPCRSet-upTool-001’ to attain consistently high fidelity qPCR reactions. Biol Proced Online 8, 87–152.[CrossRef]
    [Google Scholar]
  14. Hsu, T., Artiushin, S. & Minion, F. C. ( 1997; ). Cloning and functional analysis of the P97 swine cilium adhesin gene of Mycoplasma hyopneumoniae. J Bacteriol 179, 1317–1323.
    [Google Scholar]
  15. Ivanova, N., Pavlov, M. Y., Bouakaz, E., Ehrenberg, M. & Schiavone, L. H. ( 2005; ). Mapping the interaction of SmpB with ribosomes by footprinting of ribosomal RNA. Nucleic Acids Res 33, 3529–3539.[CrossRef]
    [Google Scholar]
  16. Jenkins, C., Wilton, J. L., Minion, F. C., Falconer, L., Walker, M. J. & Djordjevic, S. P. ( 2006; ). Two domains within the Mycoplasma hyopneumoniae cilium adhesin bind heparin. Infect Immun 74, 481–487.[CrossRef]
    [Google Scholar]
  17. Madsen, M. L., Nettleton, D., Thacker, E. L., Edwards, R. & Minion, F. C. ( 2006a; ). Transcriptional profiling of Mycoplasma hyopneumoniae during heat shock using microarrays. Infect Immun 74, 160–166.[CrossRef]
    [Google Scholar]
  18. Madsen, M. L., Nettleton, D., Thacker, E. L. & Minion, F. C. ( 2006b; ). Transcriptional profiling of Mycoplasma hyopneumoniae during iron depletion using microarrays. Microbiology 152, 937–944.[CrossRef]
    [Google Scholar]
  19. Madsen, M. L., Puttamreddy, S., Thacker, E. L., Carruthers, M. D. & Minion, F. C. ( 2008; ). Transcriptome changes in Mycoplasma hyopneumoniae during infection. Infect Immun 76, 658–663.[CrossRef]
    [Google Scholar]
  20. Minion, F. C., Lefkowitz, E. L., Madsen, M. L., Cleary, B. J., Swartzell, S. M. & Mahairas, G. G. ( 2004; ). The genome sequence of Mycoplasma hyopneumoniae strain 232, the agent of swine mycoplasmosis. J Bacteriol 186, 7123–7133.[CrossRef]
    [Google Scholar]
  21. Nakano, M., Takahashi, A., Sakai, Y. & Nakaya, Y. ( 2007; ). Modulation of pathogenicity with norepinephrine related to the type III secretion system of Vibrio parahaemolyticus. J Infect Dis 195, 1353–1360.[CrossRef]
    [Google Scholar]
  22. 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 Microbiol 72, 5097–5099.[CrossRef]
    [Google Scholar]
  23. Opriessnig, T., Thacker, E. L., Yu, S., Fenaux, M., Meng, X. J. & Halbur, P. G. ( 2004; ). Experimental reproduction of postweaning multisystemic wasting syndrome in pigs by dual infection with Mycoplasma hyopneumoniae and porcine circovirus type 2. Vet Pathol 41, 624–640.[CrossRef]
    [Google Scholar]
  24. 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. J Bacteriol 189, 2468–2476.[CrossRef]
    [Google Scholar]
  25. Schafer, E. R., Oneal, M. J., Madsen, M. L. & Minion, F. C. ( 2007; ). Global transcriptional analysis of Mycoplasma hyopneumoniae following exposure to hydrogen peroxide. Microbiology 153, 3785–3790.[CrossRef]
    [Google Scholar]
  26. 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 A 104, 7247–7252.[CrossRef]
    [Google Scholar]
  27. Scholz, C., Stoller, G., Zarnt, T., Fischer, G. & Schmid, F. X. ( 1997; ). Cooperation of enzymatic and chaperone functions of trigger factor in the catalysis of protein folding. EMBO J 16, 54–58.[CrossRef]
    [Google Scholar]
  28. Storey, J. D. & Tibshirani, R. ( 2003; ). Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100, 9440–9445.[CrossRef]
    [Google Scholar]
  29. Sutton, M. D. ( 2004; ). The Escherichia coli dnaN159 mutant displays altered DNA polymerase usage and chronic SOS induction. J Bacteriol 186, 6738–6748.[CrossRef]
    [Google Scholar]
  30. Thacker, E. L., Halbur, P. G., Ross, R. F., Thanawongnuwech, R. & Thacker, B. J. ( 1999a; ). Mycoplasma hyopneumoniae potentiation of porcine reproductive and respiratory syndrome virus-induced pneumonia. J Clin Microbiol 37, 620–627.
    [Google Scholar]
  31. Thacker, E. L., Halbur, P. G., Ross, R. F., Thanawongnuwech, R. & Thacker, B. J. ( 1999b; ). Mycoplasma hyopneumoniae potentiation of porcine reproductive and respiratory syndrome virus-induced pneumonia. J Clin Microbiol 37, 620–627.
    [Google Scholar]
  32. Thacker, E. L., Thacker, B. J. & Janke, B. H. ( 2001; ). Interaction between Mycoplasma hyopneumoniae and swine influenza virus. J Clin Microbiol 39, 2525–2530.[CrossRef]
    [Google Scholar]
  33. Vasconcelos, A. T., Ferreira, H. B., Bizarro, C. V., Bonatto, S. L., Carvalho, M. O., Pinto, P. M., Almeida, D. F., Almeida, L. G., Almeida, R. & other authors ( 2005; ). Swine and poultry pathogens: the complete genome sequence of two strains of Mycoplasma hyopneumoniae and a strain of Mycoplasma synoviae. J Bacteriol 187, 5568–5577.[CrossRef]
    [Google Scholar]
  34. Voigt, W., Fruth, A., Tschape, H., Reissbrodt, R. & Williams, P. H. ( 2006; ). Enterobacterial autoinducer of growth enhances shiga toxin production by enterohemorrhagic Escherichia coli. J Clin Microbiol 44, 2247–2249.[CrossRef]
    [Google Scholar]
  35. Waldor, M. K. & Sperandio, V. ( 2007; ). Adrenergic regulation of bacterial virulence. J Infect Dis 195, 1248–1249.[CrossRef]
    [Google Scholar]
  36. Wang, A. & Crowley, D. E. ( 2005; ). Global gene expression responses to cadmium toxicity in Escherichia coli. J Bacteriol 187, 3259–3266.[CrossRef]
    [Google Scholar]
  37. Weinstein-Fischer, D. & Altuvia, S. ( 2007; ). Differential regulation of Escherichia coli topoisomerase I by Fis. Mol Microbiol 63, 1131–1144.[CrossRef]
    [Google Scholar]
  38. Wolfinger, R. D., Gibson, G., Wolfinger, E. D., Bennett, L., Hamadeh, H., Bushel, P., Afshari, C. & Paules, R. S. ( 2001; ). Assessing gene significance from cDNA microarray expression data via mixed models. J Comput Biol 8, 625–637.[CrossRef]
    [Google Scholar]
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These genes were differentially expressed during exposure to 100 μM norepinephrine compared to control non-exposed organisms. In the table we include genes in this list that were also differentially expressed in other studies and indicate whether they were up- or downregulated in those studies. We also include their putative COG role or function. Other information about these genes such membrane domains, etc., can be found at http://mycoplasma.genome.uab.eduin the database maintained by Elliott Lefkowitz. [ Excel file] (129 kb) The locations of significantly regulated genes are shown on a circular representation of the chromosome. The outer layer of small closed circles represent upregulated genes; the inside layer of open circles represent downregulated genes. [ PDF] (256 kb)

EXCEL

These genes were differentially expressed during exposure to 100 μM norepinephrine compared to control non-exposed organisms. In the table we include genes in this list that were also differentially expressed in other studies and indicate whether they were up- or downregulated in those studies. We also include their putative COG role or function. Other information about these genes such membrane domains, etc., can be found at http://mycoplasma.genome.uab.eduin the database maintained by Elliott Lefkowitz. [ Excel file] (129 kb) The locations of significantly regulated genes are shown on a circular representation of the chromosome. The outer layer of small closed circles represent upregulated genes; the inside layer of open circles represent downregulated genes. [ PDF] (256 kb)

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