1887

Microbiology Society logo

Volume 160, Issue 3

Editor's Choice Invasion of endothelial cells and arthritogenic potential of endocarditis-associated Free

Abstract

Although infection by is a model of extracellular mucosal pathogenesis, different clones have been also associated with invasive infections such as sepsis, endocarditis, septic arthritis and osteomyelitis. The mechanisms that promote infection and haematogenic dissemination need further investigation. In this study we evaluated the association and invasion mechanisms with human umbilical vein endothelial cells (HUVECs) and experimental arthritis in mice of endocarditis-associated strains and control non-invasive strains. strains were able to adhere to and invade HUVECs at different levels. The endocarditis-associated strains displayed an aggregative adherence pattern and a higher number of internalized viable cells in HUVECs. Transmission electron microscopy (TEM) analysis revealed intracellular bacteria free in the cytoplasm and/or contained in a host-membrane-confined compartment as single micro-organisms. Data showed bacterial internalization dependent on microfilament and microtubule stability and involvement of protein phosphorylation in the HUVEC signalling pathway. A high number of affected joints and high arthritis index in addition to the histopathological features indicated a strain-dependent ability of to cause severe polyarthritis. A correlation between the arthritis index and increased systemic levels of IL-6 and TNF-α was observed for endocarditis-associated strains. In conclusion, higher incidence of potential mechanisms by which may access the bloodstream through the endothelial barrier and stimulate the production of pro-inflammatory cytokines such as IL-6 and TNF-α, in addition to the ability to affect the joints and induce arthritis through haematogenic spread are thought to be related to the pathogenesis of endocarditis-associated strains.

  • Received:
  • Accepted:
  • Published Online:
Funding
This study was supported by the:
  • CAPES
  • FAPERJ
  • CNPq
  • SR-2/UERJ
  • the ProgramaNacional de Pós-Doutorado
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.069948-0
2014-03-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/3/537.html?itemId=/content/journal/micro/10.1099/mic.0.069948-0&mimeType=html&fmt=ahah

References

  1. Appelbaum P. C., Dossett J. H. ( 1982). Arthritis caused by unidentified gram-positive rods in a child with acute lymphocytic leukemia. J Clin Microbiol 15:525–527[PubMed]
     [Google Scholar]
  2. Barakett V., Morel G., Lesage D., Petit J. C. ( 1993). Septic arthritis due to a nontoxigenic strain of Corynebacterium diphtheriae subspecies mitis . Clin Infect Dis 17:520–521 [View Article][PubMed]
     [Google Scholar]
  3. Belko J., Wessel D. L., Malley R. ( 2000). Endocarditis caused by Corynebacterium diphtheriae: case report and review of the literature. Pediatr Infect Dis J 19:159–163 [View Article][PubMed]
     [Google Scholar]
  4. Bertuccini L., Baldassarri L., von Hunolstein C. ( 2004). Internalization of non-toxigenic Corynebacterium diphtheriae by cultured human respiratory epithelial cells. Microb Pathog 37:111–118 [View Article][PubMed]
     [Google Scholar]
  5. Bremell T., Lange S., Yacoub A., Rydén C., Tarkowski A. ( 1991). Experimental Staphylococcus aureus arthritis in mice. Infect Immun 59:2615–2623[PubMed]
     [Google Scholar]
  6. Cossart P., Sansonetti P. J. ( 2004). Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304:242–248 [View Article][PubMed]
     [Google Scholar]
  7. Damade R., Pouchot J., Delacroix I., Boussougant Y., Vinceneux P. ( 1993). Septic arthritis due to Corynebacterium diphtheriae . Clin Infect Dis 16:446–447 [View Article][PubMed]
     [Google Scholar]
  8. Dias A. A., Silva F. C. Jr, Santos L. S., Ribeiro-Carvalho M. M., Sabbadini P. S., Santos C. S., Filardy A. A., Myioshi A., Azevedo V. A. & other authors ( 2011). Strain-dependent arthritogenic potential of the zoonotic pathogen Corynebacterium ulcerans . Vet Microbiol 153:323–331 [View Article][PubMed]
     [Google Scholar]
  9. dos Santos C. S., dos Santos L. S., de Souza M. C., dos Santos Dourado F., de Souza de Oliveira Dias A. A., Sabbadini P. S., Pereira G. A., Cabral M. C., Hirata R. Jr, de Mattos-Guaraldi A. L. ( 2010). Non-opsonic phagocytosis of homologous non-toxigenic and toxigenic Corynebacterium diphtheriae strains by human U-937 macrophages. Microbiol Immunol 54:1–10 [View Article][PubMed]
     [Google Scholar]
  10. Drevets D. A. ( 1998). Listeria monocytogenes virulence factors that stimulate endothelial cells. Infect Immun 66:232–238[PubMed]
     [Google Scholar]
  11. Feldmann M., Brennan F. M., Maini R. N. ( 1996). Role of cytokines in rheumatoid arthritis. Annu Rev Immunol 14:397–440 [View Article][PubMed]
     [Google Scholar]
  12. Finlay B. B., Falkow S. ( 1997). Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61:136–169[PubMed]
     [Google Scholar]
  13. Gibson R. L., Lee M. K., Soderland C., Chi E. Y., Rubens C. E. ( 1993). Group B streptococci invade endothelial cells: type III capsular polysaccharide attenuates invasion. Infect Immun 61:478–485[PubMed]
     [Google Scholar]
  14. Goldenberg D. L., Reed J. I. ( 1985). Bacterial arthritis. N Engl J Med 312:764–771 [View Article][PubMed]
     [Google Scholar]
  15. Guran P., Mollaret H. H., Chatelain R., Gropman M., Prigent F., Béal G. ( 1979). [Septic arthritis due to a nontoxigenic diphtheria bacillus]. Arch Fr Pediatr 36:926–929[PubMed]
     [Google Scholar]
  16. Hirata R. Jr, Napoleão F., Monteiro-Leal L. H., Andrade A. F. B., Nagao P. E., Formiga L. C. D., Fonseca L. S., Mattos-Guaraldi A. L. ( 2002). Intracellular viability of toxigenic Corynebacterium diphtheriae strains in HEp-2 cells. FEMS Microbiol Lett 215:115–119 [View Article][PubMed]
     [Google Scholar]
  17. Hirata R. Jr, Souza S. M. S., Rocha-de-Souza C. M., Andrade A. F. B., Monteiro-Leal L. H., Formiga L. C. D., Mattos-Guaraldi A. L. ( 2004). Patterns of adherence to HEp-2 cells and actin polymerisation by toxigenic Corynebacterium diphtheriae strains. Microb Pathog 36:125–130 [View Article][PubMed]
     [Google Scholar]
  18. Hirata R. Jr, Pereira G. A., Filardy A. A., Gomes D. L., Damasco P. V., Rosa A. C., Nagao P. E., Pimenta F. P., Mattos-Guaraldi A. L. ( 2008). Potential pathogenic role of aggregative-adhering Corynebacterium diphtheriae of different clonal groups in endocarditis. Braz J Med Biol Res 41:986–991 [View Article][PubMed]
     [Google Scholar]
  19. Mattos-Guaraldi A. L., Formiga L. C. D. ( 1998). Bacteriological properties of a sucrose-fermenting Corynebacterium diphtheriae strain isolated from a case of endocarditis. Curr Microbiol 37:156–158 [View Article][PubMed]
     [Google Scholar]
  20. Mattos-Guaraldi A. L., Duarte Formiga L. C., Pereira G. A. ( 2000). Cell surface components and adhesion in Corynebacterium diphtheriae . Microbes Infect 2:1507–1512 [View Article][PubMed]
     [Google Scholar]
  21. Matussek A., Strindhall J., Stark L., Rohde M., Geffers R., Buer J., Kihlström E., Lindgren P. E., Löfgren S. ( 2005). Infection of human endothelial cells with Staphylococcus aureus induces transcription of genes encoding an innate immunity response. Scand J Immunol 61:536–544 [View Article][PubMed]
     [Google Scholar]
  22. Menzies B. E., Kourteva I. ( 2000). Staphylococcus aureus alpha-toxin induces apoptosis in endothelial cells. FEMS Immunol Med Microbiol 29:39–45[PubMed]
     [Google Scholar]
  23. Mishra B., Dignan R. J., Hughes C. F., Hendel N. ( 2005). Corynebacterium diphtheriae endocarditis–surgery for some but not all. Asian Cardiovasc Thorac Ann 13:119–126 [View Article][PubMed]
     [Google Scholar]
  24. Ogawa S. K., Yurberg E. R., Hatcher V. B., Levitt M. A., Lowy F. D. ( 1985). Bacterial adherence to human endothelial cells in vitro . Infect Immun 50:218–224[PubMed]
     [Google Scholar]
  25. Ott L., Höller M., Rheinlaender J., Schäffer T. E., Hensel M., Burkovski A. ( 2010). Strain-specific differences in pili formation and the interaction of Corynebacterium diphtheriae with host cells. BMC Microbiol 10:257 [View Article][PubMed]
     [Google Scholar]
  26. Patey O., Bimet F., Riegel P., Halioua B., Emond J. P., Estrangin E., Dellion S., Alonso J. M., Kiredjian M. & other authors ( 1997). Clinical and molecular study of Corynebacterium diphtheriae systemic infections in France. J Clin Microbiol 35:441–445[PubMed]
     [Google Scholar]
  27. Pimenta F. P., Hirata R. Jr, Rosa A. C. , Milagres L. G., Mattos‐Guaraldi A. L. ( 2008). A multiplex PCR assay for simultaneous detection of Corynebacterium diphtheriae and differentiation between non-toxigenic and toxigenic isolates. J Med Microbiol 57:1438–1439[PubMed] [CrossRef]
     [Google Scholar]
  28. Plotkowski M. C., Saliba A. M., Pereira S. H. M., Cervante M. P., Bajolet-Laudinat O. ( 1994). Pseudomonas aeruginosa selective adherence to and entry into human endothelial cells. Infect Immun 62:5456–5463[PubMed]
     [Google Scholar]
  29. Puliti M., Nizet V., von Hunolstein C., Bistoni F., Mosci P., Orefici G., Tissi L. ( 2000). Severity of group B streptococcal arthritis is correlated with β-hemolysin expression. J Infect Dis 182:824–832 [View Article][PubMed]
     [Google Scholar]
  30. Puliti M., von Hunolstein C., Marangi M., Bistoni F., Tissi L. ( 2006). Experimental model of infection with non-toxigenic strains of Corynebacterium diphtheriae and development of septic arthritis. J Med Microbiol 55:229–235 [View Article][PubMed]
     [Google Scholar]
  31. Santos G. S., Lione V. O. F., Costa E Silva Filho F., Nagao P. E. ( 2005). Signal transduction in human endothelial cells induced by their interaction with group B Streptococci. Int J Mol Med 15:859–863[PubMed]
     [Google Scholar]
  32. Tiley S. M., Kociuba K. R., Heron L. G., Munro R. ( 1993). Infective endocarditis due to nontoxigenic Corynebacterium diphtheriae: report of seven cases and review. Clin Infect Dis 16:271–275 [View Article][PubMed]
     [Google Scholar]
  33. Tissi L., Marconi P., Mosci P., Merletti L., Cornacchione P., Rosati E., Recchia S., von Hunolstein C., Orefici G. ( 1990). Experimental model of type IV Streptococcus agalactiae (group B streptococcus) infection in mice with early development of septic arthritis. Infect Immun 58:3093–3100[PubMed]
     [Google Scholar]
  34. Vercellotti G. M., Lussenhop D., Peterson P. K., Furcht L. T., McCarthy J. B., Jacob H. S., Moldow C. F. ( 1984). Bacterial adherence to fibronectin and endothelial cells: a possible mechanism for bacterial tissue tropism. J Lab Clin Med 103:34–43[PubMed]
     [Google Scholar]
  35. von Hunolstein C., Alfarone G., Scopetti F., Pataracchia M., La Valle R., Franchi F., Pacciani L., Manera A., Giammanco A. & other authors ( 2003). Molecular epidemiology and characteristics of Corynebacterium diphtheriae and Corynebacterium ulcerans strains isolated in Italy during the 1990s. J Med Microbiol 52:181–188 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.069948-0
Loading
Invasion of endothelial cells and arthritogenic potential of endocarditis-associated Corynebacterium diphtheriae
Microbiology 160, 537 (2014); https://doi.org/10.1099/mic.0.069948-0
/content/journal/micro/10.1099/mic.0.069948-0
/content/journal/micro/10.1099/mic.0.069948-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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