Skip to main content
Log in

Mechanisms of Escherichia coli photodynamic inactivation by an amphiphilic tricationic porphyrin and 5,10,15,20-tetra(4-N,N,N-trimethylammoniumphenyl) porphyrin

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

The mechanistic aspects of Escherichia coli photodynamic inactivation (PDI) have been investigated in bacteria treated with 5,10,15-tris[4-(3-N,N,N-trimethylammoniumpropoxy)phenyl]-20-(4-trifluoromethylphenyl)porphyrin iodide (A3B3+) and visible light. The photosensitization activity of A3B3+ porphyrin was compared with that of 5,10,15,20-tetra(4-N,N,N-trimethylammonium phenyl)porphyrin p-tosylate (TMAP4+), which is an active tetracationic sensitizer to eradicate bacteria. The PDI damages on plasmid and genomic DNA were analyzed by electrophoresis. DNA photocleavage was observed after a long period of irradiation, when the bacterial cells are largely photoinactivated. Transmission electron microscopy (TEM) revealed structural changes with appearance of low density areas into the cells and irregularities in cell barriers, which could affect the normal cell membrane functionality. Also, damages on the cell-wall were not detected by scanning electron microscopy (SEM) and release of intracellular biopolymers was not found after PDI. These results indicate that the photodynamic activity of these cationic porphyrins produces DNA photodamage after a long period of irradiation. Therefore, an interference with membrane functions could be the main cause of E. coli photoinactivation upon short PDI treatments.

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.

Similar content being viewed by others

References

  1. P. W. Taylor, P. D. Stapleton, J. P. Luzio, New ways to treat bacterial infections, Drug Discovery Today, 2002, 7, 1086–1091.

    Article  Google Scholar 

  2. M. R. Hamblin, T. Hasan, Photodynamic therapy: a new antimicrobial approach to infectious disease?, Photochem. Photobiol. Sci., 2004, 3, 436–450.

    Article  CAS  Google Scholar 

  3. G. Jori, S. B. Brown, Photosensitized inactivation of microorganisms, Photochem. Photobiol. Sci., 2004, 5, 403–405.

    Article  Google Scholar 

  4. E. N. Durantini, Photodynamic inactivation of bacteria, Curr. Bioact. Comp., 2006, 2, 127–142.

    Article  CAS  Google Scholar 

  5. M. Ochsner, Photophysical and photobiological processes in photodynamic therapy of tumours, J. Photochem. Photobiol., B, 1997, 39, 1–18.

    Article  CAS  Google Scholar 

  6. M. C. DeRosa, R. J. Crutchley, Photosensitized singlet oxygen and its applications, Coord. Chem. Rev., 2002, 233-234, 351–371.

    Article  CAS  Google Scholar 

  7. M. Merchat, G. Spikes, G. Bertoloni, G. Jori, Studies on the mechanism of bacteria photosensitization by meso-substituted cationic porphyrins, J. Photochem. Photobiol. B, 1996, 35, 149–157.

    Article  CAS  Google Scholar 

  8. A. Minnock, D. I. Vernon, J. Schofield, J. Griffiths, J. H. Parish, S. B. Brown, Mechanism of uptake of a cationic water-soluble pyridinium zinc phthalocyanine across the outer membrane of Escherichia coli, Antimicrob. Agents Chemother., 2000, 44, 522–527.

    Article  CAS  Google Scholar 

  9. M. Salmon-Divon, Y. Nitzan, Z. Malik, Mechanistic aspect of Escherichia coli photodynamic inactivation by cationic tetra-meso(N-methylpyridyl)porphine, Photochem. Photobiol. Sci., 2004, 3, 423–429.

    Article  CAS  Google Scholar 

  10. Y. Nitzan, H. Ashkenazi, Photoinactivation of Acinetobacter baumannii and Escherichia coli B by cationic hydrophilic porphyrin at various light wavelengths, Curr. Microbiol., 2001, 42, 408–414.

    Article  CAS  Google Scholar 

  11. M. Merchat, G. Bertoloni, P. Giacomini, A. Villanueva, G. Jori, Meso-substituted cationic porphyrins as efficient photosensitizers of Gram-positive and Gram-negative bacteria, J. Photochem. Photobiol., B, 1996, 32, 153–157.

    Article  CAS  Google Scholar 

  12. E. Reddi, M. Ceccon, G. Valduga, G. Jori, J. C. Bommer, F. Elisei, L. Latterini, U. Mazzucato, Photophysical properties and antibacterial activity of meso-substituted cationic porphyrin, Photochem. Photobiol., 2002, 75, 462–470.

    Article  CAS  Google Scholar 

  13. D. Lazzeri, M. Rovera, L. Pascual, E. N. Durantini, Photodynamic studies and photoinactivation of Escherichia coli using meso-substituted cationic derivatives with asymmetric charge distribution, Photochem. Photobiol., 2004, 80, 286–293.

    Article  CAS  Google Scholar 

  14. S. Banfi, E. Caruso, L. Buccafurni, V. Battini, S. Zazzaron, P. Barbieri, V. Orlandi, Antibacterial activity of tetraaryl-porphyrin photosensitizers: An in vitro study on Gram negative and Gram positive bacteria, J. Photochem. Photobiol., B, 2006, 85, 28–38.

    Article  CAS  Google Scholar 

  15. P. Kubát, K. Lang, P. Anzenbacher, Jr., K. Jursíková, V. Král, B. Ehrenberg, Interaction of novel cationic meso-tetraphenylporphyrins in the ground and excited states with DNA and nucleotides, J. Chem. Soc., Perkin Trans., 2000, 1, 933–941.

    Article  Google Scholar 

  16. S. Mettath, B. R. Munson and R. K. Pandey, DNA interaction and photocleavage properties of porphyrins containing cationic substituents at the peripheral position, Bioconjug. Chem., 1999, 10, 94–102.

    Article  CAS  Google Scholar 

  17. H. Li, O. S. Fedorova, A. N. Grachev, W. R. Trumble, G. A. Bohach, L. Czuchajowski, A series of meso-tris(N-methyl-pyridiniumyl)-(4-alkylamidophenyl) porphyrins: synthesis, interaction with DNA and antibacterial activity, Biochim. Biophys. Acta, 1997, 1354, 252–260.

    Article  CAS  Google Scholar 

  18. J.-L. Ravanat, M. Berger, F. Benard, R. Langlois, R. Oullet, J. E. van Lier, J. Cadet, Phthalocyanine and naphthalocyanine photosensitized oxidation of 2’-deoxyguanosine: distint type I and type II products, Photochem. Photobiol., 1992, 55, 809–814.

    Article  CAS  Google Scholar 

  19. C. Sheu, C. S. Foote, Endoperoxide formation in a guanosine derivative, J. Am. Chem. Soc., 1993, 115, 10446–10447.

    Article  CAS  Google Scholar 

  20. J. Cadet, T. Douki, D. Gasparutto, J.-L. Ravanat, Oxidative damage to DNA: formation, measurement and biochemical features, Mutat. Res., 2003, 531, 5–23.

    Article  CAS  Google Scholar 

  21. J. Cadet, J.-L. Ravanat, G. R. Martinez, M. H. G. Medeiros, P. Di Mascio, Singlet oxygen oxidation of isolated and cellular DNA: product formation and mechanistic insights, Photochem. Photobiol., 2006, 82, 1219–1225.

    Article  CAS  Google Scholar 

  22. F. P. Imray, D. G. MacPhee, The role of DNA polymerase I and the rec system in survival of bacteria and bacteriophages damaged by the photodynamic action of acridine orange, Mol. Gen. Genet., 1973, 123, 289–298.

    Article  CAS  Google Scholar 

  23. U. Nir, H. Ladan, Z. Malik, Y. Nitzan, In vivo effects of porphyrins on bacterial DNA, J. Photochem. Photobiol., B, 1991, 11, 295–306.

    Article  CAS  Google Scholar 

  24. G. Bertoloni, F. M. Lauro, G. Cortella, M. Merchat, Photosensitizing activity of hematoporphyrin on Staphylococcus aureus cells, Biochim. Biophys. Acta, 2000, 1475, 169–174.

    Article  CAS  Google Scholar 

  25. D. A. Caminos, M. B. Spesia, E. N. Durantini, Photodynamic inactivation of Escherichia coli by novel meso-substituted porphyrins by 4-(3-N,N,N-trimethylammoniumpropoxy)phenyl and 4-(trifluoromethyl)phenyl groups, Photochem. Photobiol. Sci., 2006, 5, 56–65.

    Article  CAS  Google Scholar 

  26. D. A. Caminos, E. N. Durantini, Photodynamic inactivation of Escherichia coli immobilized on agar surfaces by a tricationic porphyrin, Bioorg. Med. Chem., 2006, 14, 4253–4259.

    Article  CAS  Google Scholar 

  27. D. A. Caminos, E. N. Durantini, Synthesis of asymmetrically meso-substituted porphyrins bearing amino groups as potential cationic photodynamic agents, J. Porphyrin Phthalocyanine, 2005, 9, 334–342.

    Article  CAS  Google Scholar 

  28. C. Z. Chen, S. L. Cooper, Interactions between dendrimer biocides and bacterial membranes, Biomaterials, 2002, 23, 3359–3368.

    Article  CAS  Google Scholar 

  29. J. Jae-Young, K. Se-Kwon, Antimicrobial action of novel chitin derivative, Biochim. Biophys. Acta, 2006, 1760, 104–109.

    Article  Google Scholar 

  30. M. W. Van Der Woude, A. J. Bäumler, Phase and antigenic variation in bacteria, Clin. Microbiol. Rev., 2004, 17, 581–611.

    Article  Google Scholar 

  31. D. A. Caminos, E. N. Durantini, Interaction and photodynamic activity of cationic porphyrin derivatives bearing different pattern of charge distribution with GMP and DNA, J. Photochem. Photobiol., A, 2008, 198, 274–281.

    Article  CAS  Google Scholar 

  32. T. Demidova, M. Hamblin, Effects of cell-photosensitizer binding and cell density on microbial photoinactivation, Antimicrob. Agents Chemother., 2005, 6, 49, 2329–2335.

    Article  Google Scholar 

  33. N. E. Mukundan, G. Petho, D. W. Dixon, M. S. Kim, L. G. Marzilli, Interactions of an electron-rich tetracationic tentacle porphyrin with calf thymus DNA, Inorg. Chem., 1994, 33, 4676–4687.

    Article  CAS  Google Scholar 

  34. S. Wu, Z. Li, L. Ren, B. Chen, F. Liang, X. Zhou, T. Jia, X. Cao, Dicationic pyridium porphyrins appending different peripheral substituents: synthesis and studies for their interactions with DNA, Bioorg. Med. Chem., 2006, 14, 2956–2965.

    Article  CAS  Google Scholar 

  35. T. Jia, Z.-X. Jiang, K. Wang, Z.-Y. Li, Binding and photocleavage of cationic porphyrin-phenylpiperazine hybrids to DNA, Biophys. Chem., 2006, 119, 295–302.

    Article  CAS  Google Scholar 

  36. H. Ashkenazi, Y. Nitzan, D. Gál, Photodynamic effects of antioxidant substituted porphyrin photosensitizers on Gram-positive and -negative bacteria, Photochem. Photobiol., 2003, 77, 186–191.

    Article  CAS  Google Scholar 

  37. G. Bertoloni, F. Rossi, G. Valduga, G. Jori, J. van Lier, Photosensitizing activity of water- and lipid-soluble phthalocyanines on Escherichia coli, FEMS Microbiol. Lett., 1990, 71, 149–156.

    Article  CAS  Google Scholar 

  38. G. Valduga, B. Breda, G. M. Giacometti, G. Jori, E. Reddi, Photosensitization of wild and mutant strains of Escherichia coli by meso-tetra(N-methyl-4-pyridyl)porphine, Biochem. Biophys. Res. Commun., 1999, 256, 84–88.

    Article  CAS  Google Scholar 

  39. Y. Nitzan, H. Ashkenazi, Photoinactivation of Deinococcus radiodurans: an unusual Gram-positive microorganism, Photochem. Photobiol., 1999, 69, 505–510.

    Article  CAS  Google Scholar 

  40. Y. Nitzan, M. Gutterman, Z. Malik, B. Ehrenberg, Inactivation of gram-negative bacteria by photosensitized porphyrins, Photochem. Photobiol., 1992, 55, 89–96.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Edgardo N. Durantini.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Caminos, D.A., Spesia, M.B., Pons, P. et al. Mechanisms of Escherichia coli photodynamic inactivation by an amphiphilic tricationic porphyrin and 5,10,15,20-tetra(4-N,N,N-trimethylammoniumphenyl) porphyrin. Photochem Photobiol Sci 7, 1071–1078 (2008). https://doi.org/10.1039/b804965c

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/b804965c

Navigation