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A search for enhanced photodynamic activity against Staphylococcus aureus planktonic cells and biofilms: the evaluation of phthalocyanine–detonation nanodiamond–Ag nanoconjugates

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Abstract

The present work reports on the synthesis and characterization of novel zinc (2) and indium (3) 2-amino-4-bromophenoxy substituted phthalocyanines (Pcs) along with the self-assembled nanoconjugates formed via π–π stacking interaction onto detonation nanodiamonds (DNDs) to form 2@DNDs and 3@DNDs. 2@DNDs and 3@DNDs were covalently linked to chitosan–silver mediated nanoparticles (CSAg) to form 2@DNDs-CSAg and 3@DNDs-CSAg nanoconjugates. High singlet oxygen quantum yields in DMSO of 0.69 and 0.72 for Pcs alone and 0.90 and 0.92 for 2@DNDs-CSAg and 3@DNDs-CSAg, respectively, were obtained. The photodynamic antimicrobial chemotherapy (PACT) activity of both phthalocyanines and nanoconjugates was tested against planktonic cells and biofilms of S. aureus. 2@DNDs-CSAg and 3@DNDs-CSAg caused effective killing with a log reduction of 9.74. In addition, PACT studies on single-species S. aureus biofilms were carried out with log reduction values of 5.12 and 5.27 at 200 μg mL−1 for 2@DNDs-CSAg and 3@DNDs-CSAg, respectively.

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References

  1. S. Szunerits, A. Barras and R. Boukherroublnt, Antibacterial applications of nanodiamonds, Int. J. Environ. Res. Public Health, 2016, 13(4), 413–427, DOI: 10.3390/ijerphl3040413.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. L. C. Gomes and F. J. Mergulhão, SEM analysis of surface impact on biofilm antibiotic treatment, Scanning, 2017, 2017, 2960194, DOI: 10.1155/2017/2960194.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Q. Deng, P. Sun, L. Zhang, Z. Liu, H. Wang, J. Ren and X. Qu, Porphyrin MOF dots–based, function-adaptive nanoplatform for enhanced penetration and photodynamic eradication of bacterial biofilms, Adv. Funct. Mater., 2019, 29(30), 1903018–1903027, DOI: 10.1002/adfm.201903018.

    Article  CAS  Google Scholar 

  4. R. Singh, S. Nadhe, S. Wadhwani, U. Shedbalkar and B. A. Chopade, Nanoparticles for control of biofilms of acinetobacter specie, Materials, 2016, 9(5), 383–399, DOI: 10.3390/ma9050383.

    Article  PubMed Central  CAS  Google Scholar 

  5. A. Taraszkiewicz, G. Fila, M. Grinholc and J. Nakonieczna, Innovative strategies to overcome bioflm resistance, BioMed Res. Int., 2013, 2013, 150653, DOI: 10.1155/2013/150653.

    Article  PubMed  CAS  Google Scholar 

  6. H. Mahmoudi, A. Bahador, M. Pourhajibagher and M. Y. Alikhani, Antimicrobial photodynamic therapy: an effective alternative approach to control bacterial infections, J. Lasers Med. Sci., 2018, 9(3), 154–160, DOI: 10.15171/jlms.2018.29.

    Article  PubMed  PubMed Central  Google Scholar 

  7. S. Rajesh, E. Koshi, K. Philip and A. Mohan, Antimicrobial photodynamic therapy: An overview, J. Indian Soc. Periodontal., 2011, 15(4), 323–327.

    Article  CAS  Google Scholar 

  8. A. Wozniak and M. Grinholc, Combined antimicrobial activity of photodynamic inactivation and antimicrobialsstate of the art, Front. Microbiol., 2018, 9(930), 1–19.

    Google Scholar 

  9. A. Galstyan and U. Dobrindt, Breaching the wall: morphological control of efficacy of phthalocyanine-based photoantimicrobials, J. Mater. Chem. B, 2018, 6, 4630–4637.

    Article  CAS  PubMed  Google Scholar 

  10. D. K. Muli, B. L. Carpenter, M. Mayukh, R. A. Ghiladi and D. V. McGrath, Dendritic near-IR absorbing zinc phthalocyanines for antimicrobial photodynamic therapy, Tetrahedron Lett., 2015, 56, 3541–3545.

    Article  CAS  Google Scholar 

  11. F. F. Sperandio, Y. Y. Huang and M. R. Hamblin, Antimicrobial photodynamic therapy to kill Gram-negative bacteria, Recent Pat. Antiinfect. Drug Discov., 2013, 8, 1–23.

    Article  CAS  Google Scholar 

  12. A. Sindelo, O. L. Osifeko and T. Nyokong, Synthesis, Photophysicochemical and photodynamic antimicrobial chemotherapy studies of indium pyridyl phthalocyanines: Charge versus bridging atom, Inorg. Chim. Acta, 2018, 476, 68–76.

    Article  CAS  Google Scholar 

  13. M. Wainwright, Photodynamic antimicrobial chemotherapy (PACT), J. Antimicrob. Chemother., 1998, 42, 13–28.

    Article  CAS  PubMed  Google Scholar 

  14. O. L. Osifeko, I. Uddin, P. N. Mashazi and T. Nyokong, Physicochemical and antimicrobial photodynamic chemotherapy of unsymmetrical indium phthalocyanines alone or in the presence of magnetic nanoparticles, New J. Chem., 2016, 40, 2710–2721.

    Article  CAS  Google Scholar 

  15. Z. Biyiklioglu, I. Ozturk, T. Arslan, A. Tunçel, K. Ocakoglu, M. H. Limoncu and F. Yurt, Synthesis and antimicrobial photodynamic activities of axially {4-[(1E)-3-oxo-3-(2-thienyl)prop-1-en-1-yl]phenoxy} groups substituted silicon phthalocyanine, subphthalocyanine on Gram-positive and Gram-negative bacteria, Dyes Pigm., 2019, 166, 149–158.

    Article  CAS  Google Scholar 

  16. F. Cieplik, L. Tabenski, W. Buchalla and T. Maisch, Antimicrobial photodynamic therapy for inactivation of biofilms formed by oral key pathogens, Front. Microbiol., 2014, 5(405), 1–17, DOI: 10.3389/fmicb.2014.00405.

    Google Scholar 

  17. Y. Gao, B. Mai, A. Wang, M. Li, X. Wang, K. Zhang, Q. Liu, S. Wei and P. Wang, Antimicrobial properties of a new type of photosensitizer derived from phthalocyanine against planktonic and biofilm forms of Staphylococcus aureus, Photodiagn. Photodyn. Ther., 2018, 21, 316–326, DOI: 10.1016/j.pdpdt.2018.01.003.

    Article  CAS  Google Scholar 

  18. V. Mantareva, V. Kussovski, I. Angelov, D. Wöhrle, R. Dimitrov, E. Popova and S. Dimitrov, Non-aggregated Ga(III)-phthaIocyanines in the photodynamic inactivation of planktonic and biofilm cultures of pathogenic microorganisms, Photochem. Photobiol. Sci., 2011, 10(1), 91–102, DOI: 10.1039/b9pp00154a.

    Article  CAS  PubMed  Google Scholar 

  19. A. Elbourne, V. K. Truong, S. Cheeseman, P. Rajapaksha, S. Gangadoo, J. Chapman and R. J. Crawford, The use of nanomaterials for the mitigation of pathogenic biofilm formation, Methods Microbiol., 2019, 46, 61–92.

    Article  CAS  Google Scholar 

  20. A. Y. Grün, C. B. App, A. Breidenbach, J. Meier, G. Metreveli, G. E. Schaumann and W. Manz, Effects of low dose silver nanoparticle treatment on the structure and community composition of bacterial freshwater biofilms, PLoS One, 2018, 13, e0199132, DOI: 10.1371/journal.pone.0199132.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. H. Palza, Antimicrobial polymers with metal nanoparticles, Int. J. Mol. Sci., 2015, 16, 2099–2116, DOI: 10.3390/ijmsl6012099.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. K. Naim, S. T. Nair, P. Yadav, A. Shanavas and P. P. Neelakandan, Supramolecular confinement within chitosan nanocomposites enhances singlet oxygen generation, ChemPlusChem, 2018, 83, 418–422.

    Article  CAS  PubMed  Google Scholar 

  23. R. K. Farag and R. R. Mohamed, Synthesis and characterization of carboxymethyl chitosan nanogels for swelling studies and antimicrobial activity, Molecules, 2013, 18, 190–203, DOI: 10.3390/moleculesl8010190.

    Article  CAS  Google Scholar 

  24. P. Sahariah and M. Másson, Antimicrobial chitosan and chitosan derivatives: a review of the structure-activity relationship, Biomacromolecules, 2017, 18, 3846–3868.

    Article  CAS  PubMed  Google Scholar 

  25. D. Raafat and H. G. Sahl, Chitosan and its antimicrobial potential-a critical literature survey, Microb. Biotechnol., 2009, 2(2), 186–201.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Z. Nate, M. J. Moloto, P. K. Mubiayi and P. N. Sibiya, Green synthesis of chitosan capped silver nanoparticles and their antimicrobial activity, Mater. Res. Soc., 2018, 3(42–43), 2505–2517, DOI: 10.1557/adv.2018.368.

    CAS  Google Scholar 

  27. A. R. Futyra, M. Kus-Liśkiewicz, V. Sebastian, S. Irusta, M. Arruebo, A. Kyziol and G. Stochel, Development of noncytotoxic silver-chitosan nanocomposites for efficient control of biofilm forming microbes, RSC Adv., 2017, 7(83), 52398–52413.

    Article  Google Scholar 

  28. M. Pérez-Díaz, E. Alvarado-Gomez, M. Magaña-Aquino, R. Sánchez-Sánchez, C. Velasquillo, C. Gonzalez, A. Ganem-Rondero, G. Martínez-Castañon, N. Zavala-Alonso and F. Martinez-Gutierrez, Anti-biofilm activity of chitosan gels formulated with silver nanoparticles and their cytotoxic effect on human fibroblasts, Mater. Sci. Eng., C, 2016, 60, 317–323.

    Article  CAS  Google Scholar 

  29. Y. H. Hsieh, W. C. Chuang, K. H. Yu, C. P. Jheng and C. I. Lee, Sequential photodynamic therapy with phthalocyanine encapsulated chitosan-tripolyphosphate nanoparticles and flucytosine treatment against Candida tropicalis, Pharmaceutics, 2019, 11(1), 16–26.

    Article  CAS  PubMed Central  Google Scholar 

  30. R. Matshitse, S. Khene and T. Nyokong, Photophysical and nonlinear optical characteristics of pyridyl substituted phthalocyanine - detonation nanodiamond conjugated systems in solution, Diamond Relat. Mater., 2019, 94, 218–232.

    Article  CAS  Google Scholar 

  31. R. Matshitse, B. P. Ngoy, M. Managa, J. Mack and T. Nyokong, Photophysical properties and photodynamic therapy activities detonated-nanodiamonds-BODIPY-phthalocyanines nanoassemblies, Photodiagn. Photodyn. Ther., 2019, 26, 101–110.

    Article  CAS  Google Scholar 

  32. E. Kirbaç and A. Erdogmus, New non-peripherally substituted zinc phthalocyanines; synthesis, and comparative photophysicochemical properties, J. Mol. Struct., 2020, 1202, 1273922, DOI: 10.1016/j.molstruc.2019.127392.

    Article  CAS  Google Scholar 

  33. A. Ogunsipe, J. Y. Chen and T. Nyokong, Photophysical studies of zinc(II) phthalocyanine-effects of substituents and solvents, New J. Chem., 2004, 28, 822–827.

    Article  CAS  Google Scholar 

  34. T. Nyokong and E. Antunes, Photochemical and photophysical properties of metallophthalocyanines, in The Handbook of porphyrin science, ed. K. M. Kadish, K. M. Smith and R. Guilard, World Scientific, Singapore, 2010, pp. 247–349.

  35. Y. I. Openda, P. Sen, M. Managa and T. Nyokong, Acetophenone substituted phthalocyanines and their graphene quantum dots conjugates as photosensitizers for photodynamic antimicrobial chemotherapy against Staphylococcus aureus, Photodiagn. Photodyn. Ther., 2020, 29, 101607–101617.

    Article  CAS  Google Scholar 

  36. A. Magadla, D. O. Olowole, M. Managa and T. Nyokong, Physicochemical and antimicrobial photodynamic chemotherapy (against E. coli) by indium phthalocyanines in the presence of silver-iron bimetallic nanoparticles, Polyhedron, 2019, 162, 30–36.

    Article  CAS  Google Scholar 

  37. L. J. Tavaresa, E. D. de Avila, M. I. Kleina, B. H. D. Panariello, D. M. P. Spolidório and A. C. Pavarina, Antimicrobial photodynamic therapy alone or in combination with antibiotic local administration against biofilms of Fusobacterium nucleatum and Porphyromonas gingivalis, J. Photochem. Photobiol., B, 2018, 188, 135–145.

    Article  CAS  Google Scholar 

  38. J. Tan, Z. Liu, Y. Sun, L. Yang and L. Gao, Inhibitory effects of photodynamic inactivation on planktonic cells and biofilms of Candida auris, Mycopathologia, 2019, 9184, 525–531, DOI: 10.1007/S11046-019-00352-9.

    Article  CAS  Google Scholar 

  39. L. Özdemir, Y. Yilmaz, M. Sönmez, M. Akkurt and M. N. Tahir, Synthesis and crystal structure of a new phthalonitrile and its phthalocyanines bearing diamagnetic metals, synthesis and reactivity in inorganic, metalorganic, Synth. React. Inorg. Metal-Org. Nano-Metal Chem., 2016, 46, 110–117.

    Article  CAS  Google Scholar 

  40. Z. Kanat and H. Dincer., The synthesis and characterization of nonperipherally tetraterminal alkynyl substituted phthalocyanines and glycoconjugation via the click reaction, Dalton Trans., 2014, 43, 8654–8663.

    Article  CAS  PubMed  Google Scholar 

  41. Y. Rio, M. S. Rodriguez-Morgade and T. Torres, Modulating the electronic properties of porphyrinoids: a voyage from the violet to the infrared regions of the electromagnetic spectrum, Org. Biomol. Chem., 2008, 6, 1877–1894.

    Article  CAS  PubMed  Google Scholar 

  42. E. Gürel, M. Pişkin, S. Altun, Z. Odabaş and M. Durmuş, Synthesis, characterization and investigation of the photophysical and photochemical properties of highly soluble novel metal-free, zinc(II), and indium(III) phthalocyanines substituted with 2,3,6-trimethylphenoxy moieties, Dalton Trans., 2015, 44, 6202–6211.

    Article  PubMed  CAS  Google Scholar 

  43. W. Shi, H. Fan, S. Ai and L. Zhu, Preparation of fluorescent graphene quantum dots from humic acid for bioimaging application, New J. Chem., 2015, 39, 7054–7059.

    Article  CAS  Google Scholar 

  44. J. Wu, P. Wang, F. Wang and Y. Fang, Investigation of the microstructures of graphene quantum dots (GQDs) by surface-enhanced raman spectroscopy, Nanomaterials, 2018, 8, 864–874.

    Article  PubMed Central  CAS  Google Scholar 

  45. Z. Li, C. He, Z. Wang, Y. Gao, Y. Dong, C. Zhao, Z. Chen, Y. Wu and W. Song, An ethylenediamine-modified graphene oxide covalently functionalized with tetracarboxylic Zn(II) phthalocyanine hybrid for enhanced nonlinear optical properties, Photochem. Photobiol. Sci., 2016, 15, 910–919.

    Article  CAS  PubMed  Google Scholar 

  46. M. Miletin, P. Zimcik and V. Novakova, Photodynamic properties of aza-analogues of phthalocyanines, Photochem. Photobiol. Sci., 2018, 17, 1749–1766.

    Article  CAS  PubMed  Google Scholar 

  47. T. Nyokong, Effects of substituents on the photochemical and photophysical properties of main group metal phthalocyanines, Coord. Chem. Rev., 2007, 251(13), 1707–1722.

    Article  CAS  Google Scholar 

  48. B. T. Bomanda, W. Waudo, B. P. Ngoy, J. T. Muya, M. Mbala, J. Mack and T. Nyokong, Macroheterocycles, 2018, 11, 501–508.

    Article  CAS  Google Scholar 

  49. N. Rapulenyane, E. Antunes and T. Nyokong, A study of the photophysicochemical and antimicrobial properties of two zinc phthalocyanine-silver nanoparticle conjugates, New J. Chem., 2013, 37, 1216–1223.

    Article  CAS  Google Scholar 

  50. T. G. B. De Souza, M. G. Vivas, C. R. Mendonça, S. Plunkett, M. A. Filatov, M. O. Senge and L. J. De Boni, Studying the intersystem crossing rate and triplet quantum yield of meso substituted porphyrins by means of pulse train fluorescence technique, J. Porphyrins Phthalocyanines, 2016, 20, 282–291.

    Article  CAS  Google Scholar 

  51. M. Y. Berezin and S. Achilefu, Fluorescence lifetime measurements and biological imaging, Chem. Rev., 2010, 110(5), 2641–2684, DOI: 10.1021/cr900343z.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. J. R. Darwent, P. Douglas, A. Harriman, G. Porter and M. C. Richoux, Metal phthalocyanines and porphyrins as photosensitizers for reduction of water to hydrogen, Coord. Chem. Rev., 1982, 44, 83–126.

    Article  CAS  Google Scholar 

  53. A. Kelarakis, From highly graphitic to amorphous carbon dots: a critical review, MRS Energy Sustain., 2014, 1, 1–15, DOI: 10.1557/mre.2014.7.

    Article  Google Scholar 

  54. T. Dai, B. B. Fuchs, J. J. Coleman, R. A. Prates, C. Astrakas, T. G. St Denis, et al, Concepts and principles of photodynamic therapy as an alternative antifungal discovery platform, Front. Microbiol., 2012, 3(120), 1–16, DOI: 10.3389/fmicb.2012.00120.

    Google Scholar 

  55. L. M. Tokubo, P. L. Rosalen, J. D. C. O. Sardi, I. A. Freires, M. Fujimaki, J. E. Umeda, P. M. Barbosa, G. O. Tecchio, N. Hioka, C. F. de Freitas and R. S. S. Terada, Antimicrobial effect of photodynamic therapy using erythrosine/methylene blue combination on Streptococcus mutans biofilm, Photodiagn. Photodyn. Ther., 2018, 23, 94–98.

    Article  CAS  Google Scholar 

  56. P. S. Zolfaghari, S. Packer, M. Singer, S. P. Nair, J. Bennett, C. Street and M. Wilson, In vivo, killing of Staphylococcus aureus using a light-activated antimicrobial agent, BMC Microbiol., 2009, 9, 27.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. R. F. Donnelly, P. A. McCarron, M. M. Tunney and A. D. Woolfson, Potential of photodynamic therapy in treatment of fungal infections of the mouth. Design and characterisation of a mucoadhesive patch containing toluidine blue O., J. Photochem. Photobiol., B, 2007, 86, 59–69, DOI: 10.1016/j.jphotobiol.2006. 07.011.

    Article  CAS  Google Scholar 

  58. A. P. Ribeiro, M. C. Andrade, F. da Silva Jde, J. H. Jorge, F. L. Primo, A. C. Tedesco, et al., Photodynamic inactivation of planktonic cultures and biofilms of Candida albicans mediated by aluminum-chloride-phthalocyanine entrapped in nanoemulsions, Photochem. Photobiol., 2013, 89, 111–119, DOI: 10.HH/j.1751-1097.2012.01198.x.

    Article  CAS  PubMed  Google Scholar 

  59. I. B. Rosseti, L. R. Chagas and M. S. Costa, Photodynamic antimicrobial chemotherapy (PACT) inhibits biofilm formation by Candida albicans, increasing both ROS production and membrane permeability, Lasers Med. Sci., 2014, 29, 1059–1064, DOI: 10.1007/sl0103-013-1473-4.

    Article  PubMed  Google Scholar 

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  1. Institute for Nanotechnology Innovation, Department of Chemistry, Rhodes University, Makhanda, 6140, South Africa

    Yolande Ikala Openda, Refilwe Matshitse & Tebello Nyokong

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  2. Refilwe Matshitse
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Correspondence to Tebello Nyokong.

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Openda, Y.I., Matshitse, R. & Nyokong, T. A search for enhanced photodynamic activity against Staphylococcus aureus planktonic cells and biofilms: the evaluation of phthalocyanine–detonation nanodiamond–Ag nanoconjugates. Photochem Photobiol Sci 19, 1442–1454 (2020). https://doi.org/10.1039/d0pp00075b

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