Cell Biochemistry and Biophysics

, Volume 68, Issue 1, pp 49–54 | Cite as

Macromolecular Oxidation in Planktonic Population and Biofilms of Proteus mirabilis Exposed to Ciprofloxacin

Original Paper

Abstract

Diverse chemical and physical agents can alter cellular functions associated with the oxidative metabolism, thus stimulating the production of reactive oxygen species (ROS). Proteins and lipids may be important targets of oxidation, and this may alter their functions in planktonic bacterial physiology. However, more research is necessary to determine the precise role of cellular stress and macromolecular oxidation in biofilms. The present study was designed to evaluate whether ciprofloxacin (CIP) could oxidize the lipids to malondialdehyde (MDA) and the proteins to carbonyl residues and to advanced oxidation protein products (AOPP) in planktonic populations and biofilms of Proteus mirabilis. Incubation with CIP generated an increase of lipid and protein oxidation in planktonic cells, with a greater effect found in sensitive strains than resistant ones. Biofilms showed higher basal levels of oxidized macromolecules than planktonic bacteria, but there was no significant enhancement of MDA, carbonyl, or AOPP with antibiotic. The results described in this article show the high basal levels of MDA, carbonyls, and AOPP, with aging and loss of proliferation of biofilms cells. The low response to the oxidative stress generated by CIP in biofilms helps to clarify the resistance to antibiotics of P. mirabilis when adhered to surfaces.

Keywords

Proteus mirabilis Ciprofloxacin Planktonic population Biofilms Protein oxidation Lipid oxidation 

References

  1. 1.
    Elahi, M. M., Kong, Y. X., & Matata, B. M. (2009). Oxidative stress as a mediator of cardiovascular disease. Oxidative Medicine and Cellular Longevity, 2, 259–269.PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    Aiassa, V., Barnes, A. I., & Albesa, I. (2010). Resistance to ciprofloxacin by enhancement of antioxidant defences in biofilm and planktonic Proteus mirabilis. Biochemical and Biophysical Research Communications, 26, 84–88.CrossRefGoogle Scholar
  3. 3.
    Páez, P. L., Becerra, M. C., & Albesa, I. (2010). Effect of the association of reduced glutathione and ciprofloxacin on the antimicrobial activity in Staphylococcus aureus. FEMS Microbiology Letters, 303, 101–105.PubMedCrossRefGoogle Scholar
  4. 4.
    Fredriksson, A., Ballesteros, M., Dukan, S., & Nyström, T. (2005). Defense against protein carbonylation by DnaK/DnaJ and proteases of the heat shock regulon. Journal of Bacteriology, 187, 4207–4213.PubMedCentralPubMedCrossRefGoogle Scholar
  5. 5.
    Halliwell, B., & Whiteman, M. (2004). Measuring reactive species and oxidative damage in vivo and in cell culture: How should you do it and what do the results mean? British Journal of Pharmacology, 142, 231–255.PubMedCrossRefGoogle Scholar
  6. 6.
    Capeillère-Blandin, C., Gausson, V., Descamps-Latscha, B., & Witko-Sarsat, V. (2004). Biochemical and spectrophotometric significance of advanced oxidized protein products. Biochimica et Biophysica Acta, 1689, 91–102.PubMedCrossRefGoogle Scholar
  7. 7.
    Fink, S. P., Reddy, G. R., & Marnett, L. (1997). Mutagenicity in Escherichia coli of the major DNA adduct derived from the endogenous mutagen malondialdehyde. Proceedings of the National Academy of Sciences of the United States of America, 94, 8652–8657.PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Cabiscol, E., Piulats, E., Echave, P., Herrero, E., & Ros, J. (2000). Oxidative stress promotes specific protein damage in S. cerevisiae. Journal of Biological Chemistry, 275, 27393–27398.PubMedGoogle Scholar
  9. 9.
    Stewart, P. S., & Costerton, J. W. (2001). Antibiotic resistance of bacteria in biofilms. Lancet, 358, 135–138.PubMedCrossRefGoogle Scholar
  10. 10.
    Jacobsen, S. M., & Shirtliff, M. E. (2011). Proteus mirabilis biofilms and catheter-associated urinary tract infections. Virulence, 2, 460–465.PubMedCrossRefGoogle Scholar
  11. 11.
    Kadurugamuwa, J. L., Modi, K., Yu, J., Francis, K. P., Purchio, T., & Contag, P. R. (2005). Noninvasive biophotonic imaging for monitoring of catheter associated urinary tract infections and therapy in mice. Infection and Immunity, 73, 3878–3887.PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Clinical and Laboratory Standards Institute (CLSI) (formerly NCCLS). (2006). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard (7th ed.). CSLI Document M7-A7. Wayne: Clinical and Laboratory Standards Institute.Google Scholar
  13. 13.
    O’Toole, G. A., & Kolter, R. (1998). Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signaling pathways: A genetic analysis. Molecular Microbiology, 28, 449–461.PubMedCrossRefGoogle Scholar
  14. 14.
    Deighton, M. A., Capstick, J., Domalewski, E., & Van Nguyen, T. (2001). Methods for studying biofilms produced by Staphylococcus epidermidis. Methods in Enzymology, 336, 177–195.PubMedGoogle Scholar
  15. 15.
    Resch, A., Rosenstein, R., Nerz, C., & Götz, F. (2005). Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Applied and Environment Microbiology, 71, 2663–2676.CrossRefGoogle Scholar
  16. 16.
    Becerra, M. C., Páez, P. L., Laróvere, L. E., & Albesa, I. (2006). Lipids and DNA oxidation in Staphylococcus aureus as a consequence of oxidative stress generated by ciprofloxacin. Molecular and Cellular Biochemistry, 285, 29–34.PubMedCrossRefGoogle Scholar
  17. 17.
    Witko-Sarsat, V., Friedlander, M., Nguyen Khoa, T., Capeillère-Blandin, C., Nguyen, A. T., Canteloup, S., et al. (1998). Advanced oxidation protein products as novel mediators of inflammation and monocyte activation in chronic renal failure. Journal of Immunology, 161, 2524–2532.Google Scholar
  18. 18.
    Stauffer, C. E. (1975). A linear standard curve for the Folin–Lowry determination of protein. Analytical Biochemistry, 69, 646–648.PubMedCrossRefGoogle Scholar
  19. 19.
    Wagai, N., & Tawara, K. (1992). Possible reasons for difference in phototoxic potential of 5-quinolone antibacterial agents: Generation of toxic oxygen. Free Radical Research Communications, 17, 387–398.PubMedCrossRefGoogle Scholar
  20. 20.
    Páez, P. L., Becerra, M. C., & Albesa, I. (2011). Comparison of macromolecular oxidation by reactive oxygen species in three bacterial genera exposed to different antibiotics. Cell Biochemistry and Biophysics, 61, 467–472.PubMedCrossRefGoogle Scholar
  21. 21.
    Cooper, S. (1988). Rate and topography of cell wall synthesis during the division cycle of Salmonella typhimurium. Journal of Bacteriology, 170, 422–430.PubMedCentralPubMedGoogle Scholar
  22. 22.
    Nyström, T. (1998). To be or not to be: The ultimate decision of the growth-arrested bacterial cell. FEMS Microbiology Reviews, 21, 283–290.CrossRefGoogle Scholar
  23. 23.
    Marquis, R. E., Sim, J., & Shin, S. I. (1994). Molecular mechanisms of resistance to heat and oxidative damage. Journal of Applied Bacteriology, 76, 40S–48S.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Departamento de Farmacia, Facultad de Ciencias QuímicasUniversidad Nacional de CórdobaCórdobaArgentina

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