Skip to main content
Log in

Contribution of Catalase and Superoxide Dismutase to the Intracellular Survival of Clinical Isolates of Staphylococcus aureus in Murine Macrophages

  • Original Article
  • Published:
Indian Journal of Microbiology Aims and scope Submit manuscript

Abstract

The present study was performed in order to carefully investigate the interaction of Staphylococcus aureus with murine macrophages and the contribution of catalase and superoxide dismutase in intracellular persistence of Staphylococcus aureus within murine macrophages during in vitro infection. We have reported that Staphylococcus aureus internalized by murine macrophages did not appear to be rapidly killed. Data indicating the contribution of a single catalase and superoxide dismutase in intracellular survival of Staphylococcus aureus were provided using established biochemical assays. The results of the present experiment suggest that the survival of Staphylococcus aureus within phagocytic cells is facilitated by its ability to resist oxidative products. Organisms in the log phase of growth clearly demonstrate a resistance to oxidative products.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Pailard D, Grellet J, Dubois V, Saux CM, Quentin C (2002) Discrepancy between uptake and intracellular activity of moxifloxacin in a staphylococcus aureus-Human THP-1 monocytic cell model. Antimicrobiol Agents Chemother 46(2):288–293

    Article  Google Scholar 

  2. Lowy FD (1998) Staphylococcus aureus infection. N Eng J Med 339(8):520–532

    Article  CAS  Google Scholar 

  3. Silverstein SC, Steinbery TH (1990) Host defense against bacterial and fungal infections. In: Davis BD, Dulbecco R, Eisen HN, Ginsberg HS (eds) Microbiology. J.P Lippincott Company, Philadelphia, pp 485–505

    Google Scholar 

  4. Stor ZG, Tartaglia LA, Farr SB, Ames BN (1990) Bacterial defense against oxidative stress. Trends Genet 6:363–368

    Article  Google Scholar 

  5. Hampton MB, Kettle AJ, Winterbourn CC (1998) Inside the neutrophil phagosome: oxidants myeloperoxidase and bacterial killing. Blood 92:3013–3017

    Google Scholar 

  6. Day WA, Sajecki JL, Pitts TM, Joens LA (2002) Role of catalase in Campylobacter jejuni intracellular survival. Infect Immun 68:6337–6345

    Article  Google Scholar 

  7. Martin SE, Chaven S (1987) Synthesis of catalase in Staphylococcus aureus MF-31. Appl Environ Microbiol 53:1207–1209

    PubMed  CAS  Google Scholar 

  8. Harrington FowlerLP, Henson PM, Wilder MS (1981) Fate of Listeria monocytogenes in resident and activated macrophages. Infect Immun 33:11–20

    PubMed  CAS  Google Scholar 

  9. Bayles KW, Wesson CA, Liou LF, Fox LK, Bohach GA, Trumble WR (1998) Intracellular S. aureus escapes the endosome and reduces apoptosis in epithelial cells. Infect Immun 66:336–342

    PubMed  CAS  Google Scholar 

  10. Balwit JM, Langevelde PV, Vann JM, Proctor RA (1994) Gentamicin resistant menadione and hemin auxotrophic Staphylococcus aureus persist within cultured endothelial cells. J Infect Dis 170:1033–1037

    PubMed  CAS  Google Scholar 

  11. Proctor RA, Balwit JM, Vesga O (1994) Variant subpopulation of Staphylococcus aureus as cause of persistent and recurrent infections. Infect Agents Dis 3:302–312

    PubMed  CAS  Google Scholar 

  12. Yancey RJ, Sanchez MS, Ford CW (1991) Activity of antibiotics against Staphylococcus aureus within polymorphonuclear neutrophils. Eur J Clin Microbiol Infect Dis 10:107–113

    Article  PubMed  CAS  Google Scholar 

  13. Clement MO, Watson SP, Foster SJ (1999) Characterization of the major superoxide dismutase of S.aureus and its role in starvation, survival, stress resistance and pathogenicity. J Bacteriol 181:3898–3903

    Google Scholar 

  14. Hamton MB, Kettle AJ, Winterbourn CC (1996) Involvement of superoxide and myeloperoxidase in oxygen dependent killing of S. aureus by neutrophils. Infect Immun 64:3512–3517

    Google Scholar 

  15. Gresham HD, Lowrance JH, Caver TE, Wilson BS, Cheung AL, Lindberg FP (2000) Survival of Staphylococcus aureus inside neutrophils contribute to infection. J Immunol 164:3713–3722

    PubMed  CAS  Google Scholar 

  16. Beaman L, Beaman BL (1984) The role of oxygen and its derivatives in microbial pathogenesis and host defense. Ann Rev Micobiol 38:27–48

    Article  CAS  Google Scholar 

  17. Verdrengh M, Tarkowski A (2000) Role of macrophages in Staphylococcus aureus induced arthritis and sepsis. Arthritis Rheum 43:2276–2282

    Article  PubMed  CAS  Google Scholar 

  18. Anderson JC (1986) Staphylococcus. In: Gyles CL, Thunen CD (eds) Pathogenesis of bacterial infections in animals. Iowa State Univ Press, Ames, p 14

    Google Scholar 

  19. Collins CH, Lyne PM (1976) Microbiological methods, 4th edn. Butterworths, Boston, p 170

    Google Scholar 

  20. Yao L, Berman JW, Stephen MF, Franklin DL (1997) Correlation of histopathologic and bacteriologic changes in experimental murine model of bacteremic Staphylococcus aureus infection. Infect Immun 65:3889–3895

    PubMed  CAS  Google Scholar 

  21. Meltzer MS (1981) In: Adams DO, Edelson PJ, Koren HS (eds) Methods for studying mononuclear phagocytes. Academic Press, New York, p 133

    Google Scholar 

  22. Kahl BC, Goulian M, Wamel W, Herrmann M, Simon SM, Kaplan G, Peters G, Cheung AL (2000) Staphylococcus aureus RN6390 replicates and induces apoptosis in pulmonary epithelial cell line. Infect Immun 68:5385–5392

    Article  PubMed  CAS  Google Scholar 

  23. Nielson SL, Black FT, Storgaard M, Obel N (1995) Evaluation of a method for measurement of intracellular killing of Staphylococcus aureus in human neutrophil granulocytes. APMIS 103:460–468

    Article  Google Scholar 

  24. Barnes AC, Balebona MC, Horne MT, Ellis AE (1999) Superoxide dismutase and catalase in Photobacterium damselae subsp. Piscicida and their roles in resistance to reactive oxygen species. Microbiology 145:483–494

    Article  PubMed  CAS  Google Scholar 

  25. Beauchamp C, Fridovich (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  PubMed  CAS  Google Scholar 

  26. Woodbury W, Spencer AK, Stahmann MA (1971) An improved procedure using ferricyanide for detecting catalase isozymes. Anal Biochem 44:301–305

    Article  PubMed  CAS  Google Scholar 

  27. Lee JS, Bok SH, Park YB, Lee MK, Choi MS (2003) 4-Hydroxycinnamate lowers plasma and hepatic lipids without changing antioxidant enzyme activities. Ann Nutr Metab 47:144–151

    Article  PubMed  CAS  Google Scholar 

  28. Soop M, Duxbury H, Agwunobi AO, Agwunobi AO, Gibson JM, Hopkins SJ et al (2002) Euglycemic hyperinsulinemia augments the cytokine and endocrine responses to endotoxins in humans. Am J Physiol Endocrinol Metab 282:E1276–E1285

    PubMed  CAS  Google Scholar 

  29. Macay MB, Seral C, Leclercq MP, Tulkens PM, Bambeke VF (2006) Pharmacodynamic evaluation of the intracellular activities of antibiotics against Staphylococcus aureus in a model of THP-1 macrophages. Antimicrob Agents Chemother 50:841–851

    Article  Google Scholar 

  30. Johnston RB Jr, Keele BB Jr, Misra HP, Lehmeyer JE, Webb LS, Bachner RL, Rajagopalan KV (1975) The role of superoxide anion generation in phagocytic bactericidal activity. Studies with normal and chronic granulomatous disease leukocytes. J Clin Invest 55:1357–1360

    Article  PubMed  CAS  Google Scholar 

  31. Sanchez MS, Ford CW, Yancey RJ (1994) Effect of tumor necrosis factor alpha, interleukin 1 beta and antibiotics on the killing of intracellular Staphylococcus aureus. J Dairy Sci 77:1251–1258

    Article  PubMed  CAS  Google Scholar 

  32. Bekker LG, Freeman S, Murray P, Ryffel B, Kaplan G (2001) Tumor necrosis factor alpha controls intracellular mycobacterial growth by both inducible nitric oxide synthase dependent and inducible nitric oxide synthase independent pathways. J Immunol 166:6728–6734

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was carried out with support of an unrestricted research grant from Indian Council of Medical Research (ICMR), New Delhi, Government of India, provided to Dr. Biswadev Bishayi, Senior Lecturer, Department of physiology, University of Calcutta, Kolkata. We are deeply indebted to Prof. (Mrs.) Manjusree Bal, Department of Physiology, University of Calcutta, for supplying us with S. aureus (CMC-524, ICH-629 and ICH-757). We remain thankful to Prof. Sanghamitra Raha, Saha Institute of Nuclear Physics, Kolkata, India, for their kind help and guidance in the in situ staining techniques.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Biswadev Bishayi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Das, D., Bishayi, B. Contribution of Catalase and Superoxide Dismutase to the Intracellular Survival of Clinical Isolates of Staphylococcus aureus in Murine Macrophages. Indian J Microbiol 50, 375–384 (2010). https://doi.org/10.1007/s12088-011-0063-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12088-011-0063-z

Keywords

Navigation