Skip to main content
SpringerLink
Log in

The photodynamic effect of methylene blue and toluidine blue on Candida albicans is dependent on medium conditions

  • Published:
The Journal of Microbiology Aims and scope Submit manuscript

Abstract

Due to the increased number of immunocompromised patients, the infections associated with the pathogen of the genus Candida and other fungi have increased dramatically. Photodynamic antimicrobial chemotherapy (PACT) has been presented as a potential antimicrobial therapy, in a process that combines light and a photosensitizing drug, which promotes a phototoxic response by the treated cells. In this work, we studied the effects of the different medium conditions during PACT, using either methylene blue (MB) or toluidine blue (TB) on Candida albicans. The inhibition of the growth produced by PACT was decreased for different pH values (6.0, 7.0, and 8.0) in a buffered medium. The phototoxic effects were observed only in the presence of saline (not buffered medium). PACT was modulated by calcium in a different manner using either MB or TB. Also when using MB both verapamil or sodium azide were able to decrease the phototoxic effects on the C. albicans. These results show that PACT is presented as a new and promising antifungal therapy, however, new studies are necessary to understand the mechanism by which this event occurs.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Almeida, R.D., B.J. Manadas, A.P. Carvalho, and C.B. Duarte. 2004. Intracellular signaling mechanisms in photodynamic therapy. Biochim. Biophys. Acta. 1704, 59–86.

    PubMed  CAS  Google Scholar 

  • Barchiesi, F., A.L. Colombo, D.A. McGough, A.W. Fothergill, and M.G. Rinaldi. 1994. In vitro activity of itraconazole aginst fluconazole-susceptible and -resistant Candida albicans isolates from oral cavities from patients infected with the human immunodeficiency virus. Antimicrob. Agents Chemother. 38, 1530–1533.

    PubMed  CAS  Google Scholar 

  • Bennett, J.E., K. Izumikawa, and K.A. Marr. 2004. Mechanism of increased fluconazole resistance in Candida glabrata during prophylaxis. Antimicrob. Agents Chemother. 48, 1773–1777.

    Article  PubMed  CAS  Google Scholar 

  • Bhatti, M., A. MacRobert, S. Meghji, B. Henderson, and M. Wilson. 1998. A study of the uptake of toluidine blue O by Porphyromonas gingivalis and the mechanism of lethal photosensitization. Photochem. Photobiol. 68, 370–376.

    Article  PubMed  CAS  Google Scholar 

  • Bliss, J.M., C.E. Bigelow, T.H. Foster, and C.G. Haidaris. 2004. Susceptibility of Candida species to photodynamic effects of photofrin. Antimicrob. Agents Chemother. 48, 2000–2006.

    Article  PubMed  CAS  Google Scholar 

  • Böhmer, R.M. and G. Morstyn. 1985. Uptake of hematoporphyrin derivative by normal and malignant cells: Effect of serum, pH, temperature, and cell size. Cancer Res. 45, 5328–5334.

    PubMed  Google Scholar 

  • Calderone, R.A. 2002. Candida and Candidiasis. Washington D.C. ASM Press, USA.

    Google Scholar 

  • Cannon, R.D., E. Lamping, A.R. Holmes, K. Niimi, K. Tanabe, M. Niimi, and B.C. Monk. 2007. Candida albicans drug resistance — another way to cope with stress. Microbiology 153, 3211–3217.

    Article  PubMed  CAS  Google Scholar 

  • Chabrier-Roselló, Y., T.H. Foster, N. Pérez-Nazario, S. Mitra, and C.G. Haidaris. 2005. Sensitivity of Candida albicans germ tubes and biofilms to photofrin-mediated phototoxicity. Antimicrob. Agents Chemother. 49, 4288–4295.

    Article  PubMed  CAS  Google Scholar 

  • Cormick, M.P., M.G. Alvarez, M. Rovera, and E.N. Durantini. 2009. Photodynamic inactivation of Candida albicans sensitized by tri- and tetra-cationic porphyrin derivatives. Eur. J. Med. Chem. 44, 1592–1599.

    Article  PubMed  CAS  Google Scholar 

  • Demidova, T.N. and M.R. Hamblin. 2005. Effect of cell-photo-sensitizer binding and cell density on microbial photoinactivation. Antimicrob. Agents Chemother. 49, 2329–2335.

    Article  PubMed  CAS  Google Scholar 

  • Gad, F., T. Zahra, T. Hasan, and M.R. Hamblin. 2004. Effects of growth phase and extracellular slime on photodynamic inactivation of Gram-positive pathogenic bacteria. Antimicrob. Agents Chemother. 48, 2173–2178.

    Article  PubMed  CAS  Google Scholar 

  • Gudlaugsson, O., S. Gillespie, K. Lee, J. Vande Berg, J. Hu, S. Messer, L. Herwaldt, M. Pfaller, and D. Diekema. 2003. Attributable mortality of nosocomial candidemia, revisited. Clin. Infect. Dis. 37, 1172–1177.

    Article  PubMed  Google Scholar 

  • Hamblin, M.R., D.A. O’Donnell, N. Murthy, C.H. Contag, and T. Hasan. 2002. Rapid control of wound infections by targeted photodynamic therapy monitored by in vivo bioluminescence imaging. Photochem. Photobiol. 75, 51–57.

    Article  PubMed  CAS  Google Scholar 

  • Hamblin, M.R., J.L. Miller, I. Rizvi, H.G. Loew, and T. Hasan. 2001. Pegylation of a chlorine6 polymer conjugate increases tumor targeting of photosensitizer. Cancer Res. 61, 7155–7162.

    PubMed  CAS  Google Scholar 

  • Horsburgh, C.R. and C.H. Kirkpatrick. 1983. Long-term therapy of chronic mucocutaneous candidiasis with ketoconazole: experience with twenty-one patients. Am. J. Med. 74, 23–29.

    Article  PubMed  Google Scholar 

  • Jori, G. 2006. Photodynamic therapy of microbial infections: state of the art and perspectives. J. Environ. Pathol. Toxicol. Oncol. 25, 505–519.

    PubMed  Google Scholar 

  • Komerik, N., H. Nakanishi, A.J. MacRobert, B. Henderson, and P. Speight. 2003. In vivo killing of Porphyromonas gingivalis by toluidine blue-mediated photosensitization in an animal model. Antimicrob. Agents Chemother. 47, 932–940.

    Article  PubMed  CAS  Google Scholar 

  • Lambrechts, S.A.G., M.G. Aalders, and J. Van Marle. 2005. Mechanistic study of the photodynamic inactivation of Candida albicans by a cationic porphyrin. Antimicrob. Agents Chemother. 49, 2026–2034.

    Article  PubMed  CAS  Google Scholar 

  • Lambrechts, S.A., T.N. Demidova, M.C. Aalders, T. Hasan, and M.R. Hamblin. 2005. Photodynamic therapy for Staphylococcus aureus infected burn wounds in mice. Photochem. Photobiol. Sci. 4, 503–509.

    Article  PubMed  CAS  Google Scholar 

  • MacDonald, I. and T.J. Dougherty. 2001. Basic principles of photodynamic therapy. J. Porphyrins Phthalocyanines 5, 105–129.

    Article  CAS  Google Scholar 

  • Morgan, J., M.I. Meltzer, B.D. Plikaytis, A.N. Sofair, S. Huie-White, S. Wilcox, L.H. Harrison, E.C. Seaberg, R.A. Hajjeh, and S.M. Teutsch. 2005. Excess mortality, hospital stay, and cost due to candidemia: a case-control study using data from population-based candidemia surveillance. Infect. Control Hosp. Epidemiol. 26, 540–547.

    Article  PubMed  Google Scholar 

  • Munin, E., L.M. Giroldo, L.P. Alves, and M.S. Costa. 2007. Study of germ tube formation by Candida albicans after photodynamic antimicrobial chemotherapy (PACT). J. Photochem. Photobiol. 88, 16–20.

    Article  CAS  Google Scholar 

  • Peloi, L.S., R.R. Soares, C.E. Biondo, V.R. Souza, N. Hioka, and E. Kimura. 2008. Photodynamic effect of light-emitting diode light on cell growth inhibition induced by methylene blue. J. Biosci. 33, 231–237.

    Article  PubMed  CAS  Google Scholar 

  • Pfaller, M.A., S.A. Messer, R.J. Hollis, R.N. Jones, and D.J. Diekema. 2002. In vitro activities of ravuconazole and voriconazole compared with those of four approved systemic antifungal agents against 6,970 clinical isolates of Candida spp. Antimicrob. Agents Chemother. 46, 1723–1727.

    Article  PubMed  CAS  Google Scholar 

  • Posteraro, B., M. Tumbarello, M. La Sorda, T. Spanu, E.M. Trecarichi, F. De Bernardis, G. Scoppettuolo, M. Sanguinetti, and G. Fadda. 2006. Azole resistance of Candida glabrata in a case of recurrent fungemia. J. Clin. Microbiol. 44, 3046–3047.

    Article  PubMed  CAS  Google Scholar 

  • Ruhnke, M., A. Schmidt-Westhausen, and J. Morschhäuser. 2000. Development of simultaneous resistance to fluconazole in Candida albicans and Candida dubliniensis in a patient with AIDS. J. Antimicrob. Chemother. 46, 291–295.

    Article  PubMed  CAS  Google Scholar 

  • Sanguinetti, M., B. Posteraro, B. Fiori, S. Ranno, R. Torelli, and G. Fadda. 2005. Mechanisms of azole resistance in clinical isolates of Candida glabrata collected during a hospital survey of antifungal resistance. Antimicrob. Agents Chemother. 49, 668–679.

    Article  PubMed  CAS  Google Scholar 

  • Sharma, M., A. Dube, H. Bansal, and P.K. Gupta. 2004. Effect of pH on uptake and photodynamic action of chlorin p6 on human colon and breast adenocarcinoma cell lines. Photochem. Photobiol. Sci. 3, 231–235.

    Article  PubMed  CAS  Google Scholar 

  • Sharma, M., K. Sahu, A. Dube, and P.K. Gupta. 2005. Extracellular pH influences the mode of cell death in human colon adenocarcinoma cells subjected to photodynamic treatment with chlorin p6. J. Photochem. Photobiol. B 81, 107–113.

    Article  PubMed  CAS  Google Scholar 

  • Smijs, T.G.M., J.A. Bouwstra, M. Talebi, and S. Pavel. 2007. Investigation of conditions involved in the susceptibility of the dermatophyte Trichophyton rubrum to photodynamic treatment. J. Antimicrob. Chemother. 60, 750–759.

    Article  PubMed  CAS  Google Scholar 

  • So, C.W., P.W. Tsang, P.C. Lo, C.J. Seneviratne, L.P. Samaranayake, and W.P. Fong. 2009. Photodynamic inactivation of Candida albicans by BAM-SiPc. Mycoses. Feb 26. [in press].

  • Souza, S.C., J.C. Junqueira, I. Balducci, C.Y. Koga-Ito, E. Munin, and A.O.C. Jorge. 2006. Photosensitization of different Candida species by low power laser light. J. Photochem. Photibiol. 83, 34–38.

    Article  CAS  Google Scholar 

  • Tegos, G.P. and M.R. Hamblin. 2006. Phenothiazinium antimicrobial photosensitizers are substrates of bacterial multidrug resistance pumps. Antimicrob. Agents Chemother. 50, 196–203.

    Article  PubMed  CAS  Google Scholar 

  • Uzdensky, A., A. Lobanov, M. Bibov, and Y. Petin. 2007. Involvement of Ca2+- and cyclic adenosine monophosphate-mediated signaling pathways in photodynamic injury of isolated crayfish neuron and satellite glial cells. J. Neurosci. Res. 85, 860–870.

    Article  PubMed  CAS  Google Scholar 

  • Zheng, J.H., D. Shi, Y. Zhao, and Z.L. Chen. 2006. Role of calcium signal in apoptosis and protective mechanism of colon cancer cell line SW480 in response to 5-aminolevulinic acid-photodynamic therapy. Ai Zheng. 25, 683–688.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Instituto de Pesquisa e Desenvolvimento-IP&D, Universidade do Vale do Paraíba-UNIVAP, Av. Shishima Hifumi, 2911, CEP: 12244-000, São José dos Campos, SP, Brazil

    Gabriela Guimarães Carvalho, Monalisa Poliana Felipe & Maricilia Silva Costa

Authors
  1. Gabriela Guimarães Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monalisa Poliana Felipe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maricilia Silva Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maricilia Silva Costa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carvalho, G.G., Felipe, M.P. & Costa, M.S. The photodynamic effect of methylene blue and toluidine blue on Candida albicans is dependent on medium conditions. J Microbiol. 47, 619–623 (2009). https://doi.org/10.1007/s12275-009-0059-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-009-0059-0

Keywords

Search

Navigation