Skip to main content

Advertisement

Log in

Photoinactivation of Candida albicans and Escherichia coli using aluminium phthalocyanine on gold nanoparticles

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

Abstract

The conjugates of aluminium phthalocyanine (complex 1) with gold nanorods (complex 1–AuNRs) and bipyramids (complex 1–AuBPs) showed improved singlet oxygen quantum yields of 0.23 and 0.24, respectively, compared to that of complex 1 alone at 0.12. Complex 1 and its conjugates were used for the photoinactivation of fungi (C. albicans) and bacteria cells (E. coli). The Q band absorbances were the same for the Pc alone and when conjugated to AuNPs. The efficiency of these conjugates was evaluated by measuring the log reduction of the microorganisms (C. albicans and E. coli) after irradiation with visible light in the presence of photosensitizers. Aluminium phthalocyanine alone showed log 1.78 and log 2.51 reductions for C. albicans and E. coli respectively. However, the conjugates showed higher photosensitization with log 2.08 and log 3.34 for C. albicans and E. coli, respectively using 1–AuBPs. For complex 1–AuNRs log 2.53 and log 3.71 were achieved for C. albicans and E. coli respectively. The statistical analysis of the results showed that the enhanced photoinactivation observed in both microorganisms was irrespective of the shape of the nanoparticles conjugated. Photoinactivation of C. albicans was less than that of E. coli even though a higher concentration of complex 1 or its conjugates was used in C. albicans.

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

Notes and references

  1. K. McKenzie, M. Maclean, I. V. Timoshkin, E. Endarko, S. J. MacGregor, J. G. Anderson, Photoinactivation of Bacteria Attached to Glass and Acrylic Surfaces by 405 nm Light: Potential Application for Biofilm Decontamination, Photochem. Photobiol., 2013, 89, 927–935.

    Article  CAS  PubMed  Google Scholar 

  2. J. Almeida, J. P. C. Tome, M. G. P. M. S. Neves, A. C. Tome, J. A. S. Caveleiro, A. Cunha, L. Costa, M. A. F. Faustino, A. Almeida, Photodynamic inactivation of multidrug-resistant bacteria in hospital wastewaters: influence of residual antibiotics, Photochem. Photobiol. Sci., 2014, 13, 626–633.

    Article  CAS  PubMed  Google Scholar 

  3. P. Eggimann, J. Garbino, D. Pittet, Epidemiology of Candida species infections in critically ill non-immunosuppressed patients, Lancet Infect. Dis., 2003, 3, 685–702.

    Article  PubMed  Google Scholar 

  4. L. Ryskova, V. Buchta, R. Slezak, Photodynamic Antimicrobial Therapy, Cent. Eur. J. Biol., 2010, 5, 400–406.

    CAS  Google Scholar 

  5. P. Calzavara-Pinton, M. Rossi, R. Sala, M. Venturini, Photodynamic Antifungal Chemotherapy, Photochem. Photobiol., 2012, 88, 512–522.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. M. B. Spesia, M. Rovera, E. N. Durantini, Photodynamic inactivation of Escherichia coli and Streptococcus mitis by cationic zinc(II) phthalocyanines in media with blood derivatives, Eur. J. Med. Chem., 2010, 45, 2198–2205.

    Article  CAS  PubMed  Google Scholar 

  9. A. Segalla, C. D. Borsarelli, S. E. Braslavsky, J. D. Spikes, G. G. Roncucci, D. Dei, G. Chiti, G. Jori, E. Reddi, Photophysical, photochemical and antibacterial photosensitizing properties of a novel octacationic Zn(II)-phthalocyanine, Photochem. Photobiol. Sci., 2002, 1, 641–648.

    Article  CAS  PubMed  Google Scholar 

  10. V. Kussovski, V. Mantareva, I. Angelou, P. Orozova, D. Wöhrle, G. Schnurpfeil, E. Borisova, L. Auramov, Photodynamic inactivation of Aeromonas hydrophila by cationic phthalocyanines with different hydrophobicity, FEMS Microbiol. Lett., 2009, 294, 133–140.

    Article  CAS  PubMed  Google Scholar 

  11. A. Minnock, D. I. Vernon, J. Schofield, J. Griffiths, J. H. Parish, S. B. Brown, Photoinactivation of bacteria. Use of a cationic water-soluble zinc phthalocyanine to photoinactivate both gram-positive and gram-negative bacteria, J. Photochem. Photobiol., B, 1996, 32, 159–164.

    Article  CAS  Google Scholar 

  12. D. A. Caminos, M. B. Spesia, P. Pons, E. N. Durantini, Mechanisms of Escherichia coli photodynamic inactivation by an amphiphilic tricationic porphyrin and 5,10,15,20-tetra(4-N,N,Ntrimethylammoniumphenyl) porphyrin, J. Photochem. Photobiol., 2008, 7, 1071–1078.

    CAS  Google Scholar 

  13. M. A. Di Palma, M. G. Alvarez, A. L. Ochoa, M. E. Milanesio, E. N. Durantini, Optimization of cellular uptake of zinc(II) 2,9,16,23-tetrakis[4-(N-methylpyridyloxy)]phthalocyanine for maximal photoinactivation of Candida albicans, Fungal Biol., 2013, 117, 744–751.

    Article  PubMed  CAS  Google Scholar 

  14. T. P. Mthethwa, Y. Arslanoglu, E. Antunes, T. Nyokong, Photophysical behaviour of cationic 2-(dimethylamino) ethanethio tetrasubtituted phthalocyanine complexes in the presence of gold nanoparticles, Polyhedron, 2012, 38, 169–177.

    Article  CAS  Google Scholar 

  15. M. Managa, M. A. Idowu, E. Antunes, T. Nyokong, Photophysicochemical behavior and antimicrobial activity of dihydroxosilicontris(diaquaplatinum)octacarboxyphthalocyanine, Spectrochim. Acta, Part A, 2014, 125, 147–153.

    Article  CAS  Google Scholar 

  16. N. Masilela, E. Antunes, T. Nyokong, Axial coordination of zinc and silicon phthalocyanines to silver and gold nanoparticles: an investigation of their photophysicochemical and antimicrobial behavior, J. Porphyrins Phthalocyanines, 2013, 17, 417–430.

    Article  CAS  Google Scholar 

  17. B. Duncan, C. Kim, V. M. Rotello, The forthcoming applications of gold nanoparticles in drug and gene delivery systems, J. Controlled Release, 2011, 149, 65–71.

    Article  CAS  Google Scholar 

  18. L. He, M. D. Musick, S. R. Nicewarner, F. G. Salinas, S. J. Benkovic, M. J. Natan, C. D. Keating, Colloidal Au-Enhanced Surface Plasmon Resonance for Ultrasensitive Detection of DNA Hybridization, J. Am. Chem. Soc., 2000, 122, 9071–9077.

    Article  CAS  Google Scholar 

  19. N. J. Durr, T. Larson, D. K. Smith, B. A. Korgel, K. Sokolov, A. Ben-Yakar, Two-Photon Luminescence Imaging of Cancer Cells Using Molecularly Targeted Gold Nanorods, Nano Lett., 2007, 7, 941–945.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. R. Bhattacharya, C. R. Patra, R. Verma, S. Kumar, P. R. Greipp, P. Mukherjee, Gold Nanoparticles Inhibit the Proliferation of Multiple Myeloma Cells, Adv. Mater., 2007, 19, 711–716.

    Article  CAS  Google Scholar 

  21. T. A. EI-Brolossy, T. Abdallah, M. B. Mohamed, S. Abdallah, K. Easawi, S. Negm, H. Talaat, Shape and size dependence of the surface plasmon resonance of gold nanoparticles studied by Photoacoustic technique, Eur. Phys. J. Special Topics, 2008, 153, 361–364.

    Article  Google Scholar 

  22. G. Zhang, J. B. Jasinski, J. L. Howell, D. Patel, D. P. Stephens, A. M. Godin, Tunability and stability of gold nanoparticles obtained from chloroauric acid and sodium thiosulfate reaction, Nanoscale Res. Lett., 2012, 7, 339.

    Article  CAS  Google Scholar 

  23. D. C. Hone, P. I. Walker, R. Evans-Gowing, S. Fitzgerald, A. Beeby, I. Chamber, M. J. Cook, D. A. Russel, Generation of Cytotoxic Singlet Oxygen via Phthalocyanine-Stabilized Gold Nanoparticles: A Potential Delivery Vehicle for Photodynamic Therapy, Langmuir, 2002, 18, 2985–2987.

    Article  CAS  Google Scholar 

  24. S. Tombe, E. Antunes, T. Nyokong, The photophysical and photochemical behaviour of coumarin-derivatized zinc phthalocyanine when conjugated with gold nanoparticles and electrospun into polymer fibers, New J. Chem., 2013, 37, 679–689.

    Article  CAS  Google Scholar 

  25. X. Huang, M. A. EI-Sayed, Plasmonic photo-thermal therapy (PPTT), Alexandria J. Med., 2011, 47, 1–9.

    Article  CAS  Google Scholar 

  26. S. Perni, P. Prokopovich, J. Pratten, I. P. Parkin, M. Wilson, Nanoparticles: their potential use in antibacterial photodynamic therapy, Photochem. Photobiol. Sci., 2011, 10, 712–720.

    Article  CAS  PubMed  Google Scholar 

  27. M. Chen, R. Liu, D. P. Tsai, A Versatile Route to the Controlled Synthesis of Gold Nanostructures, Cryst. Growth, 2009, 9, 2079–2087.

    Article  CAS  Google Scholar 

  28. N. Kuznetsova, E. A. Makarova, S. N. Dashkevich, N. S. Gretsova, E. A. Kalmykova, V. M. Negrimovsky, O. L. Kaliya, E. A. Lukyanets, Relationship between the photochemical properties and structure of porphyrins and related compounds, Russ. J. Gen. Chem., 2000, 70, 133–140.

    CAS  Google Scholar 

  29. I. Scalise, N. E. Durantini, Synthesis, properties, and photodynamic inactivation of Escherichia coli using a cationic and a noncharged Zn(II) pyridyloxyphthalocyanine derivative, Bioorg. Med. Chem., 2005, 13, 3037–3045.

    Article  CAS  PubMed  Google Scholar 

  30. E. A. Dupoy, D. Lazzeri, E. N. Durantini, Photodynamic activity of cationic and non-charged Zn(II) tetrapyridinoporphyrazine derivatives: biological consequences in human erythrocytes and Escherichia coli, Photochem. Photobiol. Sci., 2004, 3, 992–998.

    Article  CAS  Google Scholar 

  31. V. Mantareva, V. Kussovski, I. Angelov and S. Dimitrov, Advance photodynamic inactivation of dental pathogenic microorganisms with water-soluble and cationic phthalocyanines, in Science against microbial pathogens: Communicating Current Research and Technological Advances, ed. A. Mendez-Vilas, Formatex, 2011, vol. 1, pp. 650–661.

    Google Scholar 

  32. L. Ryskova, V. Buchta, M. Karaskova, J. Rakusan, J. Cerny, R. Siezak, In vitro antimicrobial activity of light-activated Phthalocyanines, Cent. Eur. J. Biol., 2013, 8, 168–177.

    CAS  Google Scholar 

  33. M. Durmus, S. Yesilot, V. Ahsen, Separation and mesogenic properties of tetraalkoxy-substituted phthalocyanine isomers, New J. Chem., 2006, 30, 675–678.

    Article  CAS  Google Scholar 

  34. A. Kotiaho, R. Lahtinen, A. Efimov, H. K. Metsberg, E. Sariola, H. Lehtivuori, N. V. Tkachenko, H. Lemmetyinen, Photoinduced Charge and Energy Transfer in Phthalocyanine-Functionalized Gold Nanoparticles, J. Phys. Chem. C, 2010, 114, 162–168.

    Article  CAS  Google Scholar 

  35. M. Liu, P. Guyot-Sionnest, Mechanism of Silver(I)-Assisted Growth of Gold Nanorods and Bipyramids, J. Phys. Chem. B., 2005, 109, 22192–22200.

    Article  CAS  PubMed  Google Scholar 

  36. C. J. Orendorff, C. J. Murphy, Quantitation of metal content in the silver-assisted growth of gold nanorods, J. Phys. Chem. B., 2006, 110, 3990–3994.

    Article  CAS  PubMed  Google Scholar 

  37. D. J. Lewis, T. M. Day, J. V. MacPherson, Z. Pikramenou, Luminescent nanobeads: attachment of surface reactive Eu (III) complexes to gold nanoparticles, Chem. Commun., 2006, 1433–1435.

    Google Scholar 

  38. T. Hauck, in A Statistical Model for the Estimation of Gold Nanorod Extinction Coefficients, Term report, University of Toronto, 2005.

    Google Scholar 

  39. H. D. Hill, J. E. Millstone, M. J. Banholzer, C. A. Mirkin, The role radius of curvature plays in thiolated oligonucleotide loading on gold nanoparticles, ACS Nano, 2009, 3, 418–424.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. R. Schmidt, E. McNellis, W. Freyer, D. Brete, T. Grebel, C. Gahl, K. Reuter, M. Weinelt, Azobenzene-functionalized alkanethiols in self-assembled monolayers on gold, Appl. Phys. A, 2008, 93, 267–275.

    Article  CAS  Google Scholar 

  41. K. Heister, M. Zharnikov, M. Grunze, L. S. O. Johansson, Adsorption of Alkanethiols and Biphenylthiols on Au and Ag Substrates: A High-Resolution X-ray Photoelectron Spectroscopy Study, J. Phys. Chem. B, 2001, 105, 4058–4061.

    Article  CAS  Google Scholar 

  42. M. Zharnikov, S. Frey, K. Heister, M. Grunze, Modification of Alkanethiolate Monolayers by Low Energy Electron Irradiation: Dependence on the Substrate Material and on the Length and Isotopic Composition of the Alkyl Chains, Langmuir, 2000, 16, 2697–2705.

    Article  CAS  Google Scholar 

  43. D. G. Castner, K. Hinds, D. W. Grainger, X-ray photoelectron spectroscopy sulfur 2p study of organic thiol and disulfide binding interactions with gold surfaces, Langmuir, 1996, 12, 5083–5086.

    Article  CAS  Google Scholar 

  44. D. Nilsson, S. Watcharinyanon, M. Eng, L. Li, E. Moons, L. S. O. Johansson, M. Zharnikov, A. Shaporenko, B. Albinson, J. Martensson, Characterization of Self-Assembled Monolayers of Oligo(phenyleneethynylene) Derivatives of Varying Shapes on Gold: Effect of Laterally Extended p-Systems, Langmuir, 2007, 23, 6170–6181.

    Article  CAS  PubMed  Google Scholar 

  45. K. Artyushlcova, B. Kiefer, B. Halevl, A. Knop-Gericke, R. Schlogl, P. Atanassov, Density functional theory calculations of XPS binding energy shift for nitrogen-containing graphene-like structures, Chem. Commun., 2013, 49, 2539–2541.

    Article  CAS  Google Scholar 

  46. Y. Zhong, M. Jaidann, Y. Zhang, G. Zhang, H. Liu, M. I. Ionescu, R. Li, X. Sun, H. Abou-Rachid, L. Lussier, Synthesis of high nitrogen doping of carbon nanotubes and modeling the stabilization of filled DAATO@CNTs (10,10) for nanoenergetic materials, J. Phys. Chem. Solids, 2010, 71, 134–139.

    Article  CAS  Google Scholar 

  47. L. Chen, P. Peng, L. Lin, T. C. K. Yang, C. Huang, Facile Preparation of Nitrogen-Doped Activated Carbon for Carbon Dioxide Adsorption, Aerosol Air Qual. Res., 2014, 14, 916–927.

    Article  CAS  Google Scholar 

  48. Z. Zhou, Y. Huang, Synthesis of LiFePO4/C cathode materials by carbothermal reduction method using two kinds of Fe3+ precursors, J. Phys. Conf. Ser., 2009, 188, 012012.

    Article  Google Scholar 

  49. Y. Luo, Preparation of silver nanoparticles by heating a quaternary ammonium polyelectrolyte-AgNO3 aqueous solution in basic conditions, Indian J. Chem., 2007, 46A, 1266–1269.

    CAS  Google Scholar 

  50. D. Dorjnamjin, M. Ariunaa, Y. K. Shim, Synthesis of Silver Nanoparticles Using Hydroxyl Functionalized Ionic Liquids and Their Antimicrobial Activity, Int. J. Mol. Sci., 2008, 9, 807–820.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. W. Huang, S. Chen, Y. Liu, H. Fu, G. Wu, The controlled synthesis of stable gold nanoparticles in quaternary ammonium ionic liquids by simple heating, Nanotechnology, 2011, 22, 025602, (7 pages).

    Article  PubMed  CAS  Google Scholar 

  52. W. A. Gole, C. J. Murphy, Seed-Mediated Synthesis of Gold Nanorods: Role of the Size and Nature of the Seed, Chem. Mater., 2004, 16, 3633–3640.

    Article  CAS  Google Scholar 

  53. K. Heister, M. Zharnikov, M. Grunze, L. S. O. Johansson, A. Ulman, Characterization of X-ray Induced Damage in Alkanethiolate Monolayers by High-Resolution Photoelectron Spectroscopy, Langmuir, 2001, 17, 8–11.

    Article  CAS  Google Scholar 

  54. Y. W. Yang, L. J. Fan, High-Resolution XPS Study of Decanethiol on Au(111): Single Sulfur–Gold Bonding Interaction, Langmuir, 2002, 18, 1157–1164.

    Article  CAS  Google Scholar 

  55. N. R. Tiwari, A. Rathore, A. Prabhune, S. K. Kulkarni, Gold Nanoparticles for Colorimetric detection of hydrolysis of antibiotics by penicillin G acylase, Adv. Biosci. Biotechnol., 2010, 1, 322–329.

    Article  CAS  Google Scholar 

  56. S. Vukovic, S. Corni, B. Mennucci, Fluorescence Enhancement of Chromophores Close to Metal Nanoparticles. Optimal Setup Revealed by the Polarizable Continuum Model, J. Phys. Chem. C, 2009, 113, 121–133.

    Article  CAS  Google Scholar 

  57. A. R. Monahan, J. A. Brado, F. A. DeLuca, Dimerization of a copper(II)-phthalocyanine dye in carbon tetrachloride and benzene, J. Phys. Chem., 1972, 76, 446–449.

    Article  CAS  Google Scholar 

  58. S. Perni, C. Piccirillo, A. Kafizas, M. Uppal, J. Pratten, M. Wilson, I. P. Parkin, Antibacterial Activity of Light-Activated Silicone Containing Methylene Blue and Gold Nanoparticles of Different Sizes, J. Cluster Sci., 2010, 21, 427–438.

    Article  CAS  Google Scholar 

  59. E. S. Tuchina, V. V. Tuchin, B. N. Khlebtsov, N. G. Khlebtsov, Phototoxic effect of conjugates of plasmon-resonance nanoparticles with indocyanine green dye on Staphylococcus aureus induced by IR laser radiation, Quantum Electron., 2011, 41, 354–359.

    Article  CAS  Google Scholar 

  60. I. Maliszewska, A. Lesniewska, J. Olesiak-Banska, K. Matczyszyn, M. Samoc, Biogenic gold nanoparticles enhance methylene blue-induced phototoxic effect on Staphylococcus epidermidis, J. Nanopart. Res., 2014, 16, 1–16.

    Article  CAS  Google Scholar 

  61. S. George, A. Kishen, Influence of Photosensitizer Solvent on the Mechanisms of Photoactivated Killing of Enterococcus faecalis, Photochem. Photobiol., 2008, 84, 734–740.

    Article  CAS  PubMed  Google Scholar 

  62. M. Osumi, The ultrastructure of yeast: Cell wall structure and formation, Micron, 1998, 29, 207–233.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tebello Nyokong.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mthethwa, T., Nyokong, T. Photoinactivation of Candida albicans and Escherichia coli using aluminium phthalocyanine on gold nanoparticles. Photochem Photobiol Sci 14, 1346–1356 (2015). https://doi.org/10.1039/c4pp00315b

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c4pp00315b

Navigation