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.
Similar content being viewed by others
References
P. W. Taylor, P. D. Stapleton, J. P. Luzio, New ways to treat bacterial infections, Drug Discovery Today, 2002, 7, 1086–1091.
M. R. Hamblin, T. Hasan, Photodynamic therapy: a new antimicrobial approach to infectious disease?, Photochem. Photobiol. Sci., 2004, 3, 436–450.
G. Jori, S. B. Brown, Photosensitized inactivation of microorganisms, Photochem. Photobiol. Sci., 2004, 5, 403–405.
E. N. Durantini, Photodynamic inactivation of bacteria, Curr. Bioact. Comp., 2006, 2, 127–142.
M. Ochsner, Photophysical and photobiological processes in photodynamic therapy of tumours, J. Photochem. Photobiol., B, 1997, 39, 1–18.
M. C. DeRosa, R. J. Crutchley, Photosensitized singlet oxygen and its applications, Coord. Chem. Rev., 2002, 233-234, 351–371.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
C. Sheu, C. S. Foote, Endoperoxide formation in a guanosine derivative, J. Am. Chem. Soc., 1993, 115, 10446–10447.
J. Cadet, T. Douki, D. Gasparutto, J.-L. Ravanat, Oxidative damage to DNA: formation, measurement and biochemical features, Mutat. Res., 2003, 531, 5–23.
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.
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.
U. Nir, H. Ladan, Z. Malik, Y. Nitzan, In vivo effects of porphyrins on bacterial DNA, J. Photochem. Photobiol., B, 1991, 11, 295–306.
G. Bertoloni, F. M. Lauro, G. Cortella, M. Merchat, Photosensitizing activity of hematoporphyrin on Staphylococcus aureus cells, Biochim. Biophys. Acta, 2000, 1475, 169–174.
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.
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.
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.
C. Z. Chen, S. L. Cooper, Interactions between dendrimer biocides and bacterial membranes, Biomaterials, 2002, 23, 3359–3368.
J. Jae-Young, K. Se-Kwon, Antimicrobial action of novel chitin derivative, Biochim. Biophys. Acta, 2006, 1760, 104–109.
M. W. Van Der Woude, A. J. Bäumler, Phase and antigenic variation in bacteria, Clin. Microbiol. Rev., 2004, 17, 581–611.
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.
T. Demidova, M. Hamblin, Effects of cell-photosensitizer binding and cell density on microbial photoinactivation, Antimicrob. Agents Chemother., 2005, 6, 49, 2329–2335.
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.
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.
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.
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.
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.
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.
Y. Nitzan, H. Ashkenazi, Photoinactivation of Deinococcus radiodurans: an unusual Gram-positive microorganism, Photochem. Photobiol., 1999, 69, 505–510.
Y. Nitzan, M. Gutterman, Z. Malik, B. Ehrenberg, Inactivation of gram-negative bacteria by photosensitized porphyrins, Photochem. Photobiol., 1992, 55, 89–96.
Author information
Authors and Affiliations
Corresponding author
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1039/b804965c