1887

Abstract

Few studies have examined virulence gene expression in . In this study, expression of key pneumococcal virulence genes , , , , , , and in the nasopharynx, lungs and bloodstream of mice was investigated, following intranasal challenge with the serotype 2 strain D39. Bacterial RNA was extracted, linearly amplified and assayed by real-time RT-PCR. At 72 h, mRNA was present at higher levels in the nasopharynx and lungs than in the blood. At this time-point, the mRNAs for PspA and PiaA were most abundant in the nasopharynx, whereas no significant difference in gene expression between niches was observed for , and . Both and mRNAs were present in higher amounts in the nasopharynx than in the lungs or blood. These findings illustrate the dynamic nature of pneumococcal virulence gene expression .

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2006-02-01
2019-10-17
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References

  1. Avery, O. T., MacLeod, C. M. & McCarty, M. ( 1944; ). Studies on the chemical nature of the substance inducing transformation of pneumococcal types. Induction of transformation by a deoxyribonucleic acid fraction isolated from pneumococcus type III. J Exp Med 79, 137–158.[CrossRef]
    [Google Scholar]
  2. Benton, K. A., Everson, M. P. & Briles, D. E. ( 1995; ). A pneumolysin-negative mutant of Streptococcus pneumoniae causes chronic bacteremia rather than acute sepsis in mice. Infect Immun 63, 448–455.
    [Google Scholar]
  3. Berry, A. M. & Paton, J. C. ( 1996; ). Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae. Infect Immun 64, 5255–5262.
    [Google Scholar]
  4. Berry, A. M., Ogunniyi, A. D., Miller, D. C. & Paton, J. C. ( 1999; ). Comparative virulence of Streptococcus pneumoniae strains with insertion-duplication, point, and deletion mutations in the pneumolysin gene. Infect Immun 67, 981–985.
    [Google Scholar]
  5. Boulnois, G. J., Paton, J. C., Mitchell, T. J. & Andrew, P. W. ( 1991; ). Structure and function of pneumolysin, the multifunctional, thiol-activated toxin of Streptococcus pneumoniae. Mol Microbiol 5, 2611–2616.[CrossRef]
    [Google Scholar]
  6. Briles, D. E., Hollingshead, S. K., King, J., Swift, A., Braun, P. A., Park, M. K., Ferguson, L. M., Nahm, M. H. & Nabors, G. S. ( 2000a; ). Immunization of humans with recombinant pneumococcal surface protein A (rPspA) elicits antibodies that passively protect mice from fatal infection with Streptococcus pneumoniae bearing heterologous PspA. J Infect Dis 182, 1694–1701.[CrossRef]
    [Google Scholar]
  7. Briles, D. E., Hollingshead, S. K., Nabors, G. S., Paton, J. C. & Brooks-Walter, A. ( 2000b; ). The potential for using protein vaccines to protect against otitis media caused by Streptococcus pneumoniae. Vaccine 8, S87–S95.
    [Google Scholar]
  8. Brown, J. S., Ogunniyi, A. D., Woodrow, M. C., Holden, D. W. & Paton, J. C. ( 2001; ). Immunization with components of two iron uptake ABC transporters protects mice against systemic Streptococcus pneumoniae infection. Infect Immun 69, 6702–6706.[CrossRef]
    [Google Scholar]
  9. Claverys, J. P., Granadel, C., Berry, A. M. & Paton, J. C. ( 1999; ). Penicillin tolerance in Streptococcus pneumoniae, autolysis and the Psa ATP-binding cassette (ABC) manganese permease. Mol Microbiol 32, 881–883.[CrossRef]
    [Google Scholar]
  10. Dave, S., Brooks-Walter, A., Pangburn, M. K. & McDaniel, L. S. ( 2001; ). PspC, a pneumococcal surface protein, binds human factor H. Infect Immun 69, 3435–3437.[CrossRef]
    [Google Scholar]
  11. Dintilhac, A., Alloing, G., Granadel, C. & Claverys, J. P. ( 1997; ). Competence and virulence of Streptococcus pneumoniae: Adc and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Mol Microbiol 25, 727–739.[CrossRef]
    [Google Scholar]
  12. Håkansson, A., Roche, H., Mirza, S., McDaniel, L. S., Brooks-Walter, A. & Briles, D. E. ( 2001; ). Characterization of binding of human lactoferrin to pneumococcal surface protein A. Infect Immun 69, 3372–3381.[CrossRef]
    [Google Scholar]
  13. Hammerschmidt, S., Bethe, G., Remane, P. H. & Chhatwal, G. S. ( 1999; ). Identification of pneumococcal surface protein A as a lactoferrin-binding protein of Streptococcus pneumoniae. Infect Immun 67, 1683–1687.
    [Google Scholar]
  14. Hoskins, J., Alborn, W. E., Jr, Arnold, J. & 39 other authors ( 2001; ). Genome of the bacterium Streptococcus pneumoniae strain R6. J Bacteriol 183, 5709–5717.[CrossRef]
    [Google Scholar]
  15. Iannelli, F., Chiavolini, D., Ricci, S., Oggioni, M. R. & Pozzi, G. ( 2004; ). Pneumococcal surface protein C contributes to sepsis caused by Streptococcus pneumoniae in mice. Infect Immun 72, 3077–3080.[CrossRef]
    [Google Scholar]
  16. Janulczyk, R., Iannelli, F., Sjoholm, A. G., Pozzi, G. & Bjorck, L. ( 2000; ). Hic, a novel surface protein of Streptococcus pneumoniae that interferes with complement function. J Biol Chem 275, 37257–37263.[CrossRef]
    [Google Scholar]
  17. Kim, J. O., Romero-Steiner, S., Sorensen, U. B., Blom, J., Carvalho, M., Barnard, S., Carlone, G. & Weiser, J. N. ( 1999; ). Relationship between cell surface carbohydrates and intrastrain variation on opsonophagocytosis of Streptococcus pneumoniae. Infect Immun 67, 2327–2333.
    [Google Scholar]
  18. King, S. J., Hippe, K. R., Gould, J. M., Bae, D., Peterson, S., Cline, R. T., Fasching, C., Janoff, E. N. & Weiser, J. N. ( 2004; ). Phase variable desialylation of host proteins that bind to Streptococcus pneumoniae in vivo and protect the airway. Mol Microbiol 54, 159–171.[CrossRef]
    [Google Scholar]
  19. Kwon, H. Y., Kim, S. W., Choi, M. H., Ogunniyi, A. D., Paton, J. C., Park, S. H., Pyo, S. N. & Rhee, D. K. ( 2003; ). Effect of heat shock and mutations in ClpL and ClpP on virulence gene expression in Streptococcus pneumoniae. Infect Immun 71, 3757–3765.[CrossRef]
    [Google Scholar]
  20. Lawrence, M. C., Pilling, P. A., Epa, V. C., Berry, A. M., Ogunniyi, A. D. & Paton, J. C. ( 1998; ). The crystal structure of pneumococcal surface antigen PsaA reveals a metal-binding site and a novel structure for a putative ABC-type binding protein. Structure 6, 1553–1561.[CrossRef]
    [Google Scholar]
  21. Livak, K. J. & Schmittgen, T. D. ( 2001; ). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.[CrossRef]
    [Google Scholar]
  22. McAllister, L. J., Tseng, H. J., Ogunniyi, A. D., Jennings, M. P., McEwan, A. G. & Paton, J. C. ( 2004; ). Molecular analysis of the psa permease complex of Streptococcus pneumoniae. Mol Microbiol 53, 889–901.[CrossRef]
    [Google Scholar]
  23. McCool, T. L., Cate, T. R., Moy, G. & Weiser, J. N. ( 2002; ). The immune response to pneumococcal proteins during experimental human carriage. J Exp Med 195, 359–365.[CrossRef]
    [Google Scholar]
  24. Morona, J. K., Paton, J. C., Miller, D. C. & Morona, R. ( 2000; ). Tyrosine phosphorylation of CpsD negatively regulates capsular polysaccharide biosynthesis in Streptococcus pneumoniae. Mol Microbiol 35, 1431–1442.
    [Google Scholar]
  25. Novak, R., Braun, J. S., Charpentier, E. & Tuomanen, E. ( 1998; ). Penicillin tolerance genes of Streptococcus pneumoniae: the ABC-type manganese permease complex Psa. Mol Microbiol 29, 1285–1296.[CrossRef]
    [Google Scholar]
  26. Ogunniyi, A. D., Giammarinaro, P. & Paton, J. C. ( 2002; ). The genes encoding virulence-associated proteins and the capsule of Streptococcus pneumoniae are upregulated and differentially expressed in vivo. Microbiology 148, 2045–2053.
    [Google Scholar]
  27. Orihuela, C. J., Janssen, R., Robb, C. W., Watson, D. A. & Niesel, D. W. ( 2000; ). Peritoneal culture alters Streptococcus pneumoniae protein profiles and virulence properties. Infect Immun 68, 6082–6086.[CrossRef]
    [Google Scholar]
  28. Orihuela, C. J., Gao, G., Francis, K. P., Yu, J. & Tuomanen, E. I. ( 2004a; ). Tissue-specific contributions of pneumococcal virulence factors to pathogenesis. J Infect Dis 190, 1661–1669.[CrossRef]
    [Google Scholar]
  29. Orihuela, C. J., Radin, J. N., Sublett, J. E., Gao, G., Kaushal, D. & Tuomanen, E. I. ( 2004b; ). Microarray analysis of pneumococcal gene expression during invasive disease. Infect Immun 72, 5582–5596.[CrossRef]
    [Google Scholar]
  30. Palaniappan, R., Singh, S., Singh, U. P. & 7 other authors ( 2005; ). Differential PsaA-, PspA-, PspC-, and PdB-specific immune responses in a mouse model of pneumococcal carriage. Infect Immun 73, 1006–1013.[CrossRef]
    [Google Scholar]
  31. Paton, J. C. ( 1998; ). Novel pneumococcal surface proteins: role in virulence and vaccine potential. Trends Microbiol 6, 85–87.[CrossRef]
    [Google Scholar]
  32. Pericone, C. D., Overweg, K., Hermans, P. W. & Weiser, J. N. ( 2000; ). Inhibitory and bactericidal effects of hydrogen peroxide production by Streptococcus pneumoniae on other inhabitants of the upper respiratory tract. Infect Immun 68, 3990–3997.[CrossRef]
    [Google Scholar]
  33. Ram, S., Sharma, A. K., Simpson, S. D., Gulati, S., McQuillen, D. P., Pangburn, M. K. & Rice, P. A. ( 1998; ). A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J Exp Med 187, 743–752.[CrossRef]
    [Google Scholar]
  34. Ren, B., Szalai, A. J., Thomas, O., Hollingshead, S. K. & Briles, D. E. ( 2003; ). Both family 1 and family 2 PspA proteins can inhibit complement deposition and confer virulence to a capsular serotype 3 strain of Streptococcus pneumoniae. Infect Immun 71, 75–85.[CrossRef]
    [Google Scholar]
  35. Rosenow, C., Ryan, P., Weiser, J. N., Johnson, S., Fontan, P., Ortqvist, A. & Masure, H. R. ( 1997; ). Contribution of novel choline-binding proteins to adherence, colonization and immunogenicity of Streptococcus pneumoniae. Mol Microbiol 25, 819–829.[CrossRef]
    [Google Scholar]
  36. Shakhnovich, E. A., King, S. J. & Weiser, J. N. ( 2002; ). Neuraminidase expressed by Streptococcus pneumoniae desialylates the lipopolysaccharide of Neisseria meningitidis and Haemophilus influenzae: a paradigm for interbacterial competition among pathogens of the human respiratory tract. Infect Immun 70, 7161–7164.[CrossRef]
    [Google Scholar]
  37. Shaper, M., Hollingshead, S. K., Benjamin, W. H. J. & Briles, D. E. ( 2004; ). PspA protects Streptococcus pneumoniae from killing by apolactoferrin, and antibody to PspA enhances killing of pneumococci by apolactoferrin. Infect Immun 72, 5031–5040.[CrossRef]
    [Google Scholar]
  38. Steinfort, C., Wilson, R. & Mitchell, T. ( 1989; ). Effects of Streptococcus pneumoniae on human respiratory epithelium in vitro. Infect Immun 57, 2006–2013.
    [Google Scholar]
  39. Tseng, H. J., McEwan, A. G., Paton, J. C. & Jennings, M. P. ( 2002; ). Virulence of Streptococcus pneumoniae: PsaA mutants are hypersensitive to oxidative stress. Infect Immun 70, 1635–1639.[CrossRef]
    [Google Scholar]
  40. Tu, A. H., Fulgham, R. L., McCrory, M. A., Briles, D. E. & Szalai, A. J. ( 1999; ). Pneumococcal surface protein A inhibits complement activation by Streptococcus pneumoniae. Infect Immun 67, 4720–4724.
    [Google Scholar]
  41. Wu, H.-Y., Virolainen, A., Mathews, B., King, J., Russell, M. W. & Briles, D. E. ( 1997; ). Establishment of a Streptococcus pneumoniae nasopharyngeal colonization model in adult mice. Microb Pathog 23, 127–137.[CrossRef]
    [Google Scholar]
  42. Zhang, J.-R., Mostov, K. E., Lamm, M. E., Nanno, M., Shimida, S., Ohwaki, M. & Tuomanen, E. I. ( 2000; ). The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell 102, 827–837.[CrossRef]
    [Google Scholar]
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