1887

Abstract

is a porcine respiratory pathogen, well known as the aetiological agent of Glässer’s disease. comprises strains of different virulence, but the virulence factors of this bacterium are not well defined. A neuraminidase activity has been previously detected in , but the role of sialylation in the virulence of this bacterium has not been studied. To explore the relationship between sialic acid (Neu5Ac) and virulence, we assessed the distribution of genes involved in sialic acid metabolism in 21 strains from different clinical origins (including nasal and systemic isolates). The neuraminidase gene , together with CMP-Neu5Ac synthetase and sialyltransferase genes , and , were included in the study. Neuraminidase activity was found to be common in isolates, and the gene from 12 isolates was expressed in and further characterized. Sequence analysis showed that the NanH predicted protein contained the motifs characteristic of the catalytic site of sialidases. While an association between the presence of and the different origins of the strains was not detected, the gene was predominantly present in the systemic isolates, and was not amplified from any of the nasal isolates tested. Analysis of the lipooligosaccharide (LOS) from reference strains Nagasaki (virulent, ) and SW114 (non-virulent, ) showed the presence of sialic acid in the LOS from the Nagasaki strain, supporting the role of sialylation in the virulence of this bacterial pathogen. Further studies are needed to clarify the role of sialic acid in the pathogenicity of .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.056994-0
2012-08-01
2019-08-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/8/2117.html?itemId=/content/journal/micro/10.1099/mic.0.056994-0&mimeType=html&fmt=ahah

References

  1. Almagro-Moreno S., Boyd E. F.. ( 2009;). Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine. . Infect Immun 77:, 3807–3816. [CrossRef][PubMed]
    [Google Scholar]
  2. Aragon V., Cerdà-Cuéllar M., Fraile L., Mombarg M., Nofrarías M., Olvera A., Sibila M., Solanes D., Segalés J.. ( 2010;). Correlation between clinico-pathological outcome and typing of Haemophilus parasuis field strains. . Vet Microbiol 142:, 387–393. [CrossRef][PubMed]
    [Google Scholar]
  3. Cerdà-Cuéllar M., Aragon V.. ( 2008;). Serum-resistance in Haemophilus parasuis is associated with systemic disease in swine. . Vet J 175:, 384–389. [CrossRef][PubMed]
    [Google Scholar]
  4. Dubray G., Limet J.. ( 1987;). Evidence of heterogeneity of lipopolysaccharides among Brucella biovars in relation to A and M specificities. . Ann Inst Pasteur Microbiol 138:, 27–37. [CrossRef][PubMed]
    [Google Scholar]
  5. Fox K. L., Cox A. D., Gilbert M., Wakarchuk W. W., Li J., Makepeace K., Richards J. C., Moxon E. R., Hood D. W.. ( 2006;). Identification of a bifunctional lipopolysaccharide sialyltransferase in Haemophilus influenzae: incorporation of disialic acid. . J Biol Chem 281:, 40024–40032. [CrossRef][PubMed]
    [Google Scholar]
  6. Garin-Bastuji B., Bowden R. A., Dubray G., Limet J. N.. ( 1990;). Sodium dodecyl sulfate-polyacrylamide gel electrophoresis and immunoblotting analysis of smooth-lipopolysaccharide heterogeneity among Brucella biovars related to A and M specificities. . J Clin Microbiol 28:, 2169–2174.[PubMed]
    [Google Scholar]
  7. Hood D. W., Makepeace K., Deadman M. E., Rest R. F., Thibault P., Martin A., Richards J. C., Moxon E. R.. ( 1999;). Sialic acid in the lipopolysaccharide of Haemophilus influenzae: strain distribution, influence on serum resistance and structural characterization. . Mol Microbiol 33:, 679–692. [CrossRef][PubMed]
    [Google Scholar]
  8. Hood D. W., Cox A. D., Gilbert M., Makepeace K., Walsh S., Deadman M. E., Cody A., Martin A., Månsson M.. & other authors ( 2001;). Identification of a lipopolysaccharide α-2,3-sialyltransferase from Haemophilus influenzae. . Mol Microbiol 39:, 341–351. [CrossRef][PubMed]
    [Google Scholar]
  9. Inzana T. J., Glindemann G., Cox A. D., Wakarchuk W., Howard M. D.. ( 2002;). Incorporation of N-acetylneuraminic acid into Haemophilus somnus lipooligosaccharide (LOS): enhancement of resistance to serum and reduction of LOS antibody binding. . Infect Immun 70:, 4870–4879. [CrossRef][PubMed]
    [Google Scholar]
  10. Jenkins G. A., Figueira M., Kumar G. A., Sweetman W. A., Makepeace K., Pelton S. I., Moxon R., Hood D. W.. ( 2010;). Sialic acid mediated transcriptional modulation of a highly conserved sialometabolism gene cluster in Haemophilus influenzae and its effect on virulence. . BMC Microbiol 10:, 48. [CrossRef][PubMed]
    [Google Scholar]
  11. Jin H., Wan Y., Zhou R., Li L., Luo R., Zhang S., Hu J., Langford P. R., Chen H.. ( 2008;). Identification of genes transcribed by Haemophilus parasuis in necrotic porcine lung through the selective capture of transcribed sequences (SCOTS). . Environ Microbiol 10:, 3326–3336. [CrossRef][PubMed]
    [Google Scholar]
  12. Jones P. A., Samuels N. M., Phillips N. J., Munson R. S. Jr, Bozue J. A., Arseneau J. A., Nichols W. A., Zaleski A., Gibson B. W., Apicella M. A.. ( 2002;). Haemophilus influenzae type b strain A2 has multiple sialyltransferases involved in lipooligosaccharide sialylation. . J Biol Chem 277:, 14598–14611. [CrossRef][PubMed]
    [Google Scholar]
  13. Laemmli U. K.. ( 1970;). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. . Nature 227:, 680–685. [CrossRef][PubMed]
    [Google Scholar]
  14. Lichtensteiger C. A., Vimr E. R.. ( 1997;). Neuraminidase (sialidase) activity of Haemophilus parasuis. . FEMS Microbiol Lett 152:, 269–274. [CrossRef][PubMed]
    [Google Scholar]
  15. Lichtensteiger C. A., Vimr E. R.. ( 2003;). Purification and renaturation of membrane neuraminidase from Haemophilus parasuis. . Vet Microbiol 93:, 79–87. [CrossRef][PubMed]
    [Google Scholar]
  16. Marion C., Burnaugh A. M., Woodiga S. A., King S. J.. ( 2011;). Sialic acid transport contributes to pneumococcal colonization. . Infect Immun 79:, 1262–1269. [CrossRef][PubMed]
    [Google Scholar]
  17. Martí-Lliteras P., López-Gómez A., Mauro S., Hood D. W., Viadas C., Calatayud L., Morey P., Servin A., Liñares J.. & other authors ( 2011;). Nontypable Haemophilus influenzae displays a prevalent surface structure molecular pattern in clinical isolates. . PLoS ONE 6:, e21133. [CrossRef][PubMed]
    [Google Scholar]
  18. Nakamura S., Shchepetov M., Dalia A. B., Clark S. E., Murphy T. F., Sethi S., Gilsdorf J. R., Smith A. L., Weiser J. N.. ( 2011;). Molecular basis of increased serum resistance among pulmonary isolates of non-typeable Haemophilus influenzae. . PLoS Pathog 7:, e1001247. [CrossRef][PubMed]
    [Google Scholar]
  19. Olvera A., Cerdà-Cuéllar M., Aragon V.. ( 2006;). Study of the population structure of Haemophilus parasuis by multilocus sequence typing. . Microbiology 152:, 3683–3690. [CrossRef][PubMed]
    [Google Scholar]
  20. Olvera A., Ballester M., Nofrarías M., Sibila M., Aragon V.. ( 2009;). Differences in phagocytosis susceptibility in Haemophilus parasuis strains. . Vet Res 40:, 24. [CrossRef][PubMed]
    [Google Scholar]
  21. Potier M., Mameli L., Bélisle M., Dallaire L., Melançon S. B.. ( 1979;). Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-α-d-N-acetylneuraminate) substrate. . Anal Biochem 94:, 287–296. [CrossRef][PubMed]
    [Google Scholar]
  22. Rapp-Gabrielson V., Oliveira S., Pijoan C.. ( 2006;). Haemophilus parasuis. . In Diseases of Swine, pp. 681–690. Edited by Straw B. E., Zimmerman J. J., D’Allaire S., Taylor D. J... Ames, IA:: Iowa State University Press;.
    [Google Scholar]
  23. Steenbergen S. M., Lichtensteiger C. A., Caughlan R., Garfinkle J., Fuller T. E., Vimr E. R.. ( 2005;). Sialic acid metabolism and systemic pasteurellosis. . Infect Immun 73:, 1284–1294. [CrossRef][PubMed]
    [Google Scholar]
  24. Takao A., Nagamune H., Maeda N.. ( 2010;). Sialidase of Streptococcus intermedius: a putative virulence factor modifying sugar chains. . Microbiol Immunol 54:, 584–595.[PubMed]
    [Google Scholar]
  25. Tsai C. M., Frasch C. E.. ( 1982;). A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. . Anal Biochem 119:, 115–119. [CrossRef][PubMed]
    [Google Scholar]
  26. Xu Z., Yue M., Zhou R., Jin Q., Fan Y., Bei W., Chen H.. ( 2011;). Genomic characterization of Haemophilus parasuis SH0165, a highly virulent strain of serovar 5 prevalent in China. . PLoS ONE 6:, e19631. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.056994-0
Loading
/content/journal/micro/10.1099/mic.0.056994-0
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