Rose bengal-encapsulated chitosan nanoparticles for the photodynamic treatment of Trichophyton species.

Trichophyton interdigitale Trichophyton mentagrophytes Trichophyton rubrum functionalized nanoparticles photodynamic therapy rose bengal

Journal

Photochemistry and photobiology
ISSN: 1751-1097
Titre abrégé: Photochem Photobiol
Pays: United States
ID NLM: 0376425

Informations de publication

Date de publication:
21 Jul 2023
Historique:
revised: 29 05 2023
received: 30 03 2023
accepted: 04 07 2023
medline: 21 7 2023
pubmed: 21 7 2023
entrez: 21 7 2023
Statut: aheadofprint

Résumé

Rose bengal (RB) solutions coupled with a green laser have proven to be efficient in clearing resilient nail infections caused by Trichophyton rubrum in a human pilot study and in extensive in vitro experiments. Nonetheless, the RB solution can become diluted or dispersed over the tissue and prevented from penetrating the nail plate to reach the subungual area where fungal infection proliferates. Nanoparticles carrying RB can mitigate the problem of dilution and are reported to effectively penetrate through the nail. For this reason, we have synthesized RB-encapsulated chitosan nanoparticles with a peak distribution size of ~200 nm and high reactive oxygen species (ROS) production. The RB-encapsulated chitosan nanoparticles aPDT were shown to kill more than 99% of T. rubrum, T. mentagrophytes, and T. interdigitale spores, which are the common clinically relevant pathogens in onychomycosis. These nanoparticles are not cytotoxic against human fibroblasts, which promotes their safe application in clinical translation.

Identifiants

pubmed: 37477110
doi: 10.1111/php.13839
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023 The Authors. Photochemistry and Photobiology published by Wiley Periodicals LLC on behalf of American Society for Photobiology.

Références

Houang J, Perrone G, Mawad D, Boughton PC, Ruys AJ, Lauto A. Light treatments of nail fungal infections. J Biophotonics. 2018;11:e201700350. doi:10.1002/jbio.201700350
Shen JJ, Jemec GBE, Arendrup MC, Saunte DML. Photodynamic therapy treatment of superficial fungal infections: a systematic review. Photodiagnosis Photodyn Ther. 2020;31:101774. doi:10.1016/j.pdpdt.2020.101774
Foote CS. Definition of type I and type II photosensitized oxidation. Photochem Photobiol. 1991;54:659. doi:10.1111/j.1751-1097.1991.tb02071.x
Valenzeno DP. Photomodification of biological membranes with emphasis on singlet oxygen mechanisms. Photochem Photobiol. 1987;46:147-160. doi:10.1111/j.1751-1097.1987.tb04749.x
Gannon MJ, Brown SB. Photodynamic therapy and its applications in gynaecology. Br J Obstet Gynaecol. 1999;106:1246-1254. doi:10.1111/j.1471-0528.1999.tb08177.x
Bacellar IOL, Tsubone TM, Pavani C, Baptista MS. Photodynamic efficiency: from molecular photochemistry to cell death. Int J Mol Sci. 2015;16:20523-20559. doi:10.3390/ijms160920523
Gandin E, Lion Y, van de Vorst A. Quantum yield of singlet oxygen production by xanthene derivatives. Photochem Photobiol. 1983;37:271-278. doi:10.1111/j.1751-1097.1983.tb04472.x
Houang J, Halliday C, Chen S, Ho C-H, Bekmukhametova A, Lauto A. Effective photodynamic treatment of trichophyton species with rose bengal. J Biophotonics. 2021;14:e202000340. doi:10.1002/jbio.202000340
Houang J, Perrone GG, Pedrinazzi C, et al. Genetic tolerance to rose bengal photodynamic therapy and antifungal clinical application for onychomycosis. Adv Ther. 2018;2:1800105. doi:10.1002/adtp.201800105
Chang C-C, Yang Y-T, Yang J-C, Wu H-D, Tsai T. Absorption and emission spectral shifts of rose bengal associated with DMPC liposomes. Dyes Pigm. 2008;79:170-175. doi:10.1016/j.dyepig.2008.02.003
Xu D, Neckers DC. Aggregation of rose bengal molecules in solution. J Photochem. 1987;40:361-370. doi:10.1016/1010-6030(87)85013-X
Mahtab A, Anwar M, Mallick N, Naz Z, Jain G, Ahmad FJ. Transungual delivery of ketoconazole nanoemulgel for the effective management of onychomycosis. AAPS PharmSciTech. 2016;17:1477-1490. doi:10.1208/s12249-016-0488-0
Flores FC, Rosso RS, Cruz L, Beck RCR, Silva CB. An innovative polysaccharide nanobased nail formulation for improvement of onychomycosis treatment. Eur J Pharm Sci. 2017;100:56-63. doi:10.1016/j.ejps.2016.12.043
Bekmukhametova A, Ruprai H, Hook JM, Mawad D, Houang J, Lauto A. Photodynamic therapy with nanoparticles to combat microbial infection and resistance. Nanoscale. 2020;12:21034-21059. doi:10.1039/D0NR04540C
Tada DB, Baptista MS. Photosensitizing nanoparticles and the modulation of ROS generation. Front Chem. 2015;3:1-14. doi:10.3389/fchem.2015.00033
Rawal T, Parmar R, Tyagi RK, Butani S. Rifampicin loaded chitosan nanoparticle dry powder presents an improved therapeutic approach for alveolar tuberculosis. Colloids Surf. 2017;154:321-330. doi:10.1016/j.colsurfb.2017.03.044
Songsurang K, Praphairaksit N, Siraleartmukul K, Muangsin N. Electrospray fabrication of doxorubicin-chitosan-tripolyphosphate nanoparticles for delivery of doxorubicin. Arch Pharm Res. 2011;34:583-592. doi:10.1007/s12272-011-0408-5
Kaskoos R. Investigation of moxifloxacin loaded chitosan-dextran nanoparticles for topical instillation into eye: in-vitro and ex-vivo evaluation. Int J Pharm Investig. 2014;4:164-173. doi:10.4103/2230-973X.143114
Ing LY, Zin NM, Sarwar A, Katas H. Antifungal activity of chitosan nanoparticles and correlation with their physical properties. Int J Biomater. 2012;2012:1-9. doi:10.1155/2012/632698
Ta Q, Ting J, Harwood S, et al. Chitosan nanoparticles for enhancing drugs and cosmetic components penetration through the skin. Eur J Pharm Sci. 2021;160:105765. doi:10.1016/j.ejps.2021.105765
Dhamoon RK, Popli H, Gupta M. Novel drug delivery strategies for the treatment of onychomycosis. Pharm Nanotechnol. 2019;7:24-38. doi:10.2174/2211738507666190228104031
Shrestha A, Hamblin MR, Kishen A. Photoactivated rose bengal functionalized chitosan nanoparticles produce antibacterial/biofilm activity and stabilize dentin-collagen. Nanomedicine. 2014;10:491-501. doi:10.1016/j.nano.2013.10.010
de Freitas L, Calixto G, Chorilli M, et al. Polymeric nanoparticle-based photodynamic therapy for chronic periodontitis in vivo. Int J Mol Sci. 2016;17:769. doi:10.3390/ijms17050769
Sakima VT, Barbugli PA, Cerri PS, et al. Antimicrobial photodynamic therapy mediated by curcumin-loaded polymeric nanoparticles in a murine model of oral candidiasis. Molecules. 2018;23:2075. doi:10.3390/molecules23082075
Hermanson G. Bioconjugate Techniques. Elsevier Academic Press; 2008. doi:10.1016/B978-0-12-370501-3.X0001-X
Betzer O, Shilo M, Opochinsky R, et al. The effect of nanoparticle size on the ability to cross the blood-brain barrier: an in vivo study. Nanomedicine. 2017;12:1533-1546. doi:10.2217/nnm-2017-0022
Mendelovits A, Prat T, Gonen Y, Rytwo G. Improved colorimetric determination of chitosan concentrations by dye binding. Appl Spectrosc. 2012;66:979-982. doi:10.1366/12-06591a
Calvo P, Remuñán-López C, Vila-Jato JL, Alonso MJ. Novel hydrophilic chitosan-polyethylene oxide nanoparticles as protein carriers. J Appl Polym Sci. 1997;63:125-132. doi:10.1002/(SICI)1097-4628(19970103)63:1<125::AID-APP13>3.0.CO;2-4
Shu XZ, Zhu KJ. The influence of multivalent phosphate structure on the properties of ionically cross-linked chitosan films for controlled drug release. Eur J Pharm Biopharm. 2002;54:235-243. doi:10.1016/s0939-6411(02)00052-8
Mazancová P, Némethová V, Treľová D, Kleščíková L, Lacík I, Rázga F. Dissociation of chitosan/tripolyphosphate complexes into separate components upon pH elevation. Carbohydr Polym. 2018;192:104-110. doi:10.1016/j.carbpol.2018.03.030
Bekmukhametova A, Uddin MMN, Houang J, et al. Fabrication and characterization of chitosan nanoparticles using the coffee-ring effect for photodynamic therapy. Lasers Surg Med. 2022;54:758-766. doi:10.1002/lsm.23530
Shrestha A, Hamblin MR, Kishen A. Characterization of a conjugate between rose bengal and chitosan for targeted antibiofilm and tissue stabilization effects as a potential treatment of infected dentin. Antimicrob Agents Chemother. 2012;56:4876-4884. doi:10.1128/AAC.00810-12
Fan X, Zheng W, Singh DJ. Light scattering and surface plasmons on small spherical particles. Light Sci Appl. 2014;3:e179. doi:10.1038/lsa.2014.60
Vrignaud S, Benoit J-P, Saulnier P. Strategies for the nanoencapsulation of hydrophilic molecules in polymer-based nanoparticles. Biomaterials. 2011;32:8593-8604. doi:10.1016/j.biomaterials.2011.07.057
Li Q, Li X, Zhao C. Strategies to obtain encapsulation and controlled release of small hydrophilic molecules. Front Bioeng Biotechnol. 2020;8:437. doi:10.3389/fbioe.2020.00437
Bax DV, Davidenko N, Gullberg D, et al. Fundamental insight into the effect of carbodiimide crosslinking on cellular recognition of collagen-based scaffolds. Acta Biomater. 2017;49:218-234. doi:10.1016/j.actbio.2016.11.059
Elsabahy M, Wooley KL. Design of polymeric nanoparticles for biomedical delivery applications. Chem Soc Rev. 2012;41:2545-2561. doi:10.1039/c2cs15327k
Danaei M, Dehghankhold M, Ataei S, et al. Impact of particle size and polydispersity index on the clinical applications of lipidic nanocarrier systems. Pharmaceutics. 2018;10:1-17. doi:10.3390/pharmaceutics10020057
Murdan S, Milcovich G, Goriparthi GS. The pH of the human nail plate. In: Humbert P, Fanian F, Maibach HI, Agache P, eds. Agache's Measuring the Skin. Springer International Publishing; 2017:883-889. doi:10.1007/978-3-319-32383-1_122
Smith KA, Hao J, Li SK. Influence of pH on transungual passive and iontophoretic transport. J Pharm Sci. 2010;99:1955-1967. doi:10.1002/jps.21984
McAuley WJ, Jones SA, Traynor MJ, Guesné S, Murdan S, Brown MB. An investigation of how fungal infection influences drug penetration through onychomycosis patient's nail plates. Eur J Pharm Biopharm. 2016;102:178-184. doi:10.1016/j.ejpb.2016.03.008
Paramanantham P, Antony AP, Sruthil Lal SB, et al. Antimicrobial photodynamic inactivation of fungal biofilm using amino functionalized mesoporus silica-rose bengal nanoconjugate against Candida albicans. Sci Afr. 2018;1:e00007. doi:10.1016/j.sciaf.2018.e00007
Mei Y, Dai X, Yang W, Xu X, Liang Y. Antifungal activity of chitooligosaccharides against the dermatophyte Trichophyton rubrum. Int J Biol Macromol. 2015;77:330-335. doi:10.1016/j.ijbiomac.2015.03.042
Guo Y, Rogelj S, Zhang P. Rose bengal-decorated silica nanoparticles as photosensitizers for inactivation of gram-positive bacteria. Nanotechnology. 2010;21:65102. doi:10.1088/0957-4484/21/6/065102
Vt A, Paramanantham P, Sb SL, et al. Antimicrobial photodynamic activity of rose bengal conjugated multi walled carbon nanotubes against planktonic cells and biofilm of Escherichia coli. Photodiagnosis Photodyn Ther. 2018;24:300-310. doi:10.1016/j.pdpdt.2018.10.013
Chen J, Wu L, Lu M, Lu S, Li Z, Ding W. Comparative study on the fungicidal activity of metallic MgO nanoparticles and macroscale MgO against soilborne fungal phytopathogens. Front Microbiol. 2020;11:1-19. doi:10.3389/fmicb.2020.00365
Kong M, Chen XG, Xing K, Park HJ. Antimicrobial properties of chitosan and mode of action: a state of the art review. Int J Food Microbiol. 2010;144:51-63. doi:10.1016/j.ijfoodmicro.2010.09.012
Gondim BLC, Castellano LRC, de Castro RD, et al. Effect of chitosan nanoparticles on the inhibition of Candida spp. biofilm on denture base surface. Arch Oral Biol. 2018;94:99-107. doi:10.1016/j.archoralbio.2018.07.004
Dananjaya SHS, Erandani WKCU, Kim C-H, Nikapitiya C, Lee J, Zoysa M. Comparative study on antifungal activities of chitosan nanoparticles and chitosan silver nano composites against Fusarium oxysporum species complex. Int J Biol Macromol. 2017;105:478-488. doi:10.1016/j.ijbiomac.2017.07.056
Shilo M, Sharon A, Baranes K, Motiei M, Lellouche J-PM, Popovtzer R. The effect of nanoparticle size on the probability to cross the blood-brain barrier: an in-vitro endothelial cell model. J Nanobiotechnol. 2015;13:1-7. doi:10.1186/s12951-015-0075-7
Bseiso EA, Nasr M, Sammour OA, Abd El Gawad NA. Novel nail penetration enhancer containing vesicles ‘nPEVs’ for treatment of onychomycosis. Drug Deliv. 2016;23:2813-2819. doi:10.3109/10717544.2015.1099059
Sivandzade F, Bhalerao A, Cucullo L. Analysis of the mitochondrial membrane potential using the cationic JC-1 dye as a sensitive fluorescent probe. Bio Protoc. 2019;9:e3128. doi:10.21769/BioProtoc.3128

Auteurs

Alina Bekmukhametova (A)

School of Science, Western Sydney University, Penrith, New South Wales, Australia.

Anu Antony (A)

School of Medicine, Western Sydney University, Penrith, New South Wales, Australia.

Catriona Halliday (C)

Centre for Infectious Diseases and Microbiology Laboratory Services, ICPMR, Westmead Hospital, Westmead, New South Wales, Australia.

Sharon Chen (S)

Centre for Infectious Diseases and Microbiology Laboratory Services, ICPMR, Westmead Hospital, Westmead, New South Wales, Australia.
Sydney Medical School, University of Sydney, Westmead, New South Wales, Australia.

Chun-Hoong Ho (CH)

School of Science, Western Sydney University, Penrith, New South Wales, Australia.
School of Biomedical Sciences, The University of Queensland, Brisbane, Queensland, Australia.

Mir Muhammad Nasir Uddin (MMN)

School of Science, Western Sydney University, Penrith, New South Wales, Australia.
Department of Pharmacy, Faculty of Biological Science, University of Chittagong, Chittagong, Bangladesh.

Leonardo Longo (L)

School of Medicine, University of Siena, Siena, Italy.

Christian Pedrinazzi (C)

School of Medicine, University of Pavia, Pavia, Italy.

Laurel George (L)

Advanced Materials Characterisation Facility (AMCF), Western Sydney University, Penrith, New South Wales, Australia.

Richard Wuhrer (R)

Advanced Materials Characterisation Facility (AMCF), Western Sydney University, Penrith, New South Wales, Australia.

Simon Myers (S)

School of Medicine, Western Sydney University, Penrith, New South Wales, Australia.

Damia Mawad (D)

School of Materials Science and Engineering, University of New South Wales, Kensington, New South Wales, Australia.
Australian Centre for NanoMedicine, UNSW Australia, Sydney, New South Wales, Australia.

Jessica Houang (J)

School of Science, Western Sydney University, Penrith, New South Wales, Australia.

Antonio Lauto (A)

School of Science, Western Sydney University, Penrith, New South Wales, Australia.
Biomedical Engineering & Neuroscience Research Group, The MARCS Institute, Western Sydney University, Penrith, New South Wales, Australia.

Classifications MeSH