Lasers in Medical Science

, Volume 33, Issue 3, pp 647–653 | Cite as

Biofilm formation by Candida albicans is inhibited by photodynamic antimicrobial chemotherapy (PACT), using chlorin e6: increase in both ROS production and membrane permeability

  • Moisés Lopes Carvalho
  • Ana Paula Pinto
  • Leandro José Raniero
  • Maricilia Silva Costa
Original Article
  • 163 Downloads

Abstract

Candida albicans is an opportunistic fungal producing both superficial and systemic infections in immunocompromised patients. Furthermore, it has been described an increase in the frequency of infections which have become refractory to standard antifungal therapy. Photodynamic antimicrobial chemotherapy (PACT) is a potential antimicrobial therapy that combines visible light and a nontoxic dye, known as a photosensitizer, producing reactive oxygen species (ROS) that can kill the treated cells. The objective of this study was to investigate the effects of PACT, using chlorin e6, as a photosensitizer on C. albicans. In this work, we studied the effect of PACT on both cell growth and biofilm formation by C. albicans. In addition, both ROS production and cell permeability were determined after PACT. PACT inhibited both growth and biofilm formation by C. albicans. We have also observed that PACT increased both ROS production (six times) and cell membrane permeability (five times) in C. albicans. PACT decreased both cell growth and biofilm development. The effect of PACT using chlorin e6 on C. albicans could be associated with an increase in ROS production, which could increase cell permeability, producing permanent damage to the cell membranes, leading to the cell death.

Keywords

Photodynamic antimicrobial chemotherapy PACT Candida albicans Chlorin e6 

Notes

Acknowledgements

This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Role of funding source

The authors would like to thank FAPESP for the financial support.

Compliance with ethical standards

Conflict of interest

The authors have no financial, personal, or other conflicts of interest related to this work.

Ethical approval

In this study, all experiments were performed using cultures of Candida albicans (ATCC 10231), therefore, it is not necessarily approved by local authorities.

Informed consent

We have obtained permission from all the authors. We declare that the material has not been published in whole or in part elsewhere; the paper is not currently being considered for publication elsewhere.

References

  1. 1.
    Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB (2004) Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39:309–317CrossRefPubMedGoogle Scholar
  2. 2.
    Pfaller MA, Diekema DJ (2010) Epidemiology of invasive mycoses in North America. Crit Rev Microbiol 36:1–53CrossRefPubMedGoogle Scholar
  3. 3.
    Lockhart SR, Iqbal N, Cleveland AA, Farley MM, Harrison LH, Bolden CB, Baughman W, Stein B, Hollick R, Park BJ, Chiller T (2012) Species identification and antifungal susceptibility testing of Candida bloodstream isolates from population-based surveillance studies in two U.S. cities from 2008 to 2011. J Clin Microbiol 50:3435–3442CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Groll AH, Lumb J (2012) New developments in invasive fungal disease. Future Microbiol 7:179–184CrossRefPubMedGoogle Scholar
  5. 5.
    Wisplinghoff H, Ebbers J, Geurtz L, Stefanik D, Major Y, Edmond MB, Wenzel RP, Seifert H (2014) Nosocomial bloodstream infections due to Candida spp. in the USA: species distribution, clinical features and antifungal susceptibilities. Int J Antimicrob Agents 43:78–81CrossRefPubMedGoogle Scholar
  6. 6.
    Tsui C, Kong EF, Jabra-Rizk MA (2016) Pathogenesis of Candida albicans biofilm. Pathog Dis 74:ftw018CrossRefPubMedGoogle Scholar
  7. 7.
    Ganguly S, Mitchell AP (2011) Mucosal biofilms of Candida albicans. Curr Opin Microbiol 14:380–385CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Nobile CJ, Johnson AD (2015) Candida albicans biofilms and human disease. Annu Rev Microbiol 69:71–92CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Seneviratne CJ, Jin L, Samaranayake LP (2008) Biofilm lifestyle of Candida: a mini review. Oral Dis 14:582–590CrossRefPubMedGoogle Scholar
  10. 10.
    Sardi JC, Almeida AM, Mendes Giannini MJ (2011) New antimicrobial therapies used against fungi present in subgingival sites—a brief review. Arch Oral Biol 56:951–959CrossRefPubMedGoogle Scholar
  11. 11.
    Lewis RE, Viale P, Kontoyiannis DP (2012) The potential impact of antifungal drug resistance mechanisms on the host immune response to Candida. Virulence 3:368–376CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Tobudic S, Kratzer C, Lassnigg A, Presterl E (2012) Antifungal susceptibility of Candida albicans in biofilms. Mycoses 55:199–204CrossRefPubMedGoogle Scholar
  13. 13.
    Gonçalves SS, Souza AC, Chowdhary A, Meis JF, Colombo AL (2016) Epidemiology and molecular mechanisms of antifungal resistance in Candida and Aspergillus. Mycoses 59:198–219CrossRefPubMedGoogle Scholar
  14. 14.
    Dai T, Fuchs BB, Coleman JJ, Prates RA, Astrakas C, St Denis TG, Ribeiro MS, Mylonakis E, Hamblin MR, Tegos GP (2012) Concepts and principles of photodynamic therapy as an alternative antifungal discovery platform. Front Microbiol 3:1–16CrossRefGoogle Scholar
  15. 15.
    Allison RR, Moghissi K (2013) Photodynamic therapy (PDT): PDT mechanisms. Clin Endosc 46:24–29CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Alves E, Faustino MA, Neves MG, Cunha A, Tome J, Almeida A (2014) An insight on bacterial cellular targets of photodynamic inactivation. Future Med Chem 6:141–164CrossRefPubMedGoogle Scholar
  17. 17.
    Taraszkiewicz A, Szewczyk G, Sarna T, Bielawski KP, Nakonieczna J (2015) Photodynamic inactivation of Candida albicans with imidazoacridinones: influence of irradiance, photosensitizer uptake and reactive oxygen species generation. PLoS One 10:e0129301CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Calzavara-Pinton P, Rossi MT, Sala R, Venturini M (2012) Photodynamic antifungal chemotherapy. Photochem Photobiol 88:512–522CrossRefPubMedGoogle Scholar
  19. 19.
    Yang YT, Chien HF, Chang PH, Chen YC, Jay M, Tsai T, Chen CT (2013) Photodynamic inactivation of chlorin e6-loaded CTAB-liposomes against Candida albicans. Lasers Surg Med 45:175–185CrossRefPubMedGoogle Scholar
  20. 20.
    Prates RA, Fuchs BB, Mizuno K, Naqvi Q, Kato IT, Ribeiro MS, Mylonakis E, Tegos GP, Hamblin MR (2013) Effect of virulence factors on the photodynamic inactivation of Cryptococcus neoformans. PLoS One 8:e54387CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Rosseti IB, Chagas LR, Costa MS (2014) Photodynamic antimicrobial chemotherapy (PACT) inhibits biofilm formation by Candida albicans, increasing both ROS production and membrane permeability. Lasers Med Sci 29:1059–1064CrossRefPubMedGoogle Scholar
  22. 22.
    Rosseti IB, Costa MS (2014) The viability of biofilm produced by Candida albicans is decreased by photodynamic antimicrobial chemotherapy (PACT) with toluidine blue. Trends in Photochemistry & Photobiology 6:19–24Google Scholar
  23. 23.
    Dovigo LN, Carmello JC, Carvalho MT, Mima EG, Vergani CE, Bagnato VS, Pavarina AC (2013) Photodynamic inactivation of clinical isolates of Candida using Photodithazine®. Biofouling 29:1057–1067CrossRefPubMedGoogle Scholar
  24. 24.
    Ryu AR, Han CS, Oh HK, Lee MY (2015) Chlorin e6-mediated photodynamic inactivation with halogen light against microbes and fungus. Toxicol Environ Health Sci 7:231–238CrossRefGoogle Scholar
  25. 25.
    Quishida CC, Carmello JC, Mima EG, Bagnato VS, Machado AL, Pavarina AC (2015) Susceptibility of multispecies biofilm to photodynamic therapy using Photodithazine®. Lasers Med Sci 30:685–694CrossRefPubMedGoogle Scholar
  26. 26.
    Park JH, Moon YH, Bang IS, Kim YC, Kim SA, Ahn SG, Yoon JH (2010) Antimicrobial effect of photodynamic therapy using a highly pure chlorin e6. Lasers Med Sci 25:705–710CrossRefPubMedGoogle Scholar
  27. 27.
    Park JH, Ahn MY, Kim YC, Kim SA, Moon YH, Ahn SG, Yoon JH (2012) In vitro and in vivo antimicrobial effect of photodynamic therapy using a highly pure chlorin e6 against Staphylococcus aureus Xen29. Biol Pharm Bull 35:509–514CrossRefPubMedGoogle Scholar
  28. 28.
    Winkler K, Simon C, Finke M, Bleses K, Birke M, Szentmáry N, Hüttenberger D, Eppig T, Stachon T, Langenbucher A, Foth HJ, Herrmann M, Seitz B, Bischoff M (2016) Photodynamic inactivation of multidrug-resistant Staphylococcus aureus by chlorin e6 and red light (λ=670nm). J Photochem Photobiol B 162:340–347CrossRefPubMedGoogle Scholar
  29. 29.
    Uliana MP, Pires L, Pratavieira S, Brocksom TJ, de Oliveira KT, Bagnato VS, Kurachi C (2014) Photobiological characteristics of chlorophyll a derivatives as microbial PDT agents. Photochem Photobiol Sci 13:1137–1145CrossRefPubMedGoogle Scholar
  30. 30.
    Donnelly RF, McCarron PA, Tunney MM (2008) Antifungal photodynamic therapy. Microbiol Res 163:1–12CrossRefPubMedGoogle Scholar
  31. 31.
    Wainwright M (1998) Photodynamic antimicrobial chemotherapy (PACT). J Antimicrob Chemother 42:13–28CrossRefPubMedGoogle Scholar
  32. 32.
    Harris F, Chatfield LK, Phoenix DA (2005) Phenothiazinium based photosensitisers—photodynamic agents with a multiplicity of cellular targets and clinical applications. Curr Drug Targets 6:615–627CrossRefPubMedGoogle Scholar
  33. 33.
    Fuchs BB, Tegos GP, Hamblin MR, Mylonakis E (2007) Susceptibility of Cryptococcus neoformans to photodynamic inactivation is associated with cell wall integrity. Agents and Chemotherapy 51:2929–2936CrossRefGoogle Scholar
  34. 34.
    Giroldo LM, Felipe MP, Oliveira MA, Munin E, Alves LP, Costa MS (2009) Photodynamic antimicrobial chemotherapy (PACT) with methylene blue increases membrane permeability in Candida albicans. Lasers Med Sci 24:109–112CrossRefPubMedGoogle Scholar
  35. 35.
    Huang L, Dai T, Hamblin MR (2010) Antimicrobial photodynamic inactivation and photodynamic therapy for infections. Methods Mol Biol 635:155–173CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Cullen PJ, Sprague GF Jr (2012) The regulation of filamentous growth in yeast. Genetics 190:23–49CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Mathé L, Van Dijck P (2013) Recent insights into Candida albicans biofilm resistance mechanisms. Curr Genet 59:251–264CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Sardi JC, Pitangui Nde S, Rodríguez-Arellanes G, Taylor ML, Fusco-Almeida AM, Mendes-Giannini MJ (2014) Highlights in pathogenic fungal biofilms. Rev Iberoam Micol 31:22–29CrossRefGoogle Scholar
  39. 39.
    Miceli MH, Díaz JA, Lee AS (2011) Emerging opportunistic yeast infections. Lancet Infect Dis 11:142–151CrossRefPubMedGoogle Scholar
  40. 40.
    Finkel JS, Mitchell AP (2011) Genetic control of Candida albicans biofilm development. Nat Rev Microbiol 9:109–118CrossRefPubMedGoogle Scholar
  41. 41.
    DiDone L, Oga D, Krysan DJ (2011) A novel assay of biofilm antifungal activity reveals that amphotericin B and caspofungin lyse Candida albicans cells in biofilms. Yeast 28:561–568CrossRefPubMedGoogle Scholar
  42. 42.
    Sardi JC, Scorzoni L, Bernardi T, Fusco-Almeida AM, Mendes Giannini MJ (2013) Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. J Med Microbiol 62:10–24CrossRefPubMedGoogle Scholar
  43. 43.
    Hamblin MR, Hasan T (2004) Photodynamic therapy: a new antimicrobial approach to infectious disease? Photochem Photobiol Sci 3:436–450CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Bacellar IO, Tsubone TM, Pavani C, Baptista MS (2015) Photodynamic efficiency: from molecular photochemistry to cell death. Int J Mol Sci 16:20523–20559CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag London Ltd. 2017

Authors and Affiliations

  • Moisés Lopes Carvalho
    • 1
  • Ana Paula Pinto
    • 1
  • Leandro José Raniero
    • 1
  • Maricilia Silva Costa
    • 1
  1. 1.Instituto de Pesquisa e Desenvolvimento—IP&D. Universidade do Vale do Paraíba—UNIVAPSão José dos CamposBrazil

Personalised recommendations