Abstract
Search for new antimicrobial agents is of great significance due to the issue of antimicrobial resistance, which nowadays has become more important than many diseases. The aim of this study was to evaluate the toxicity and biological effects of a dextran-graft-polyacrylamide (D-PAA) polymer-nanocarrier with/without silver or gold nanoparticles (AgNPs/D-PAA and AuNPs/D-PAA, respectively) to analyze their potential to replace or supplement conventional antibiotic therapy. The toxicity of nanocomplexes against eukaryotic cells was assessed on primary dermal fibroblasts using scratch, micronucleus and proliferation assays. DPPH (2,2-diphenyl-1-picrylhydrazylradical) assay was used to evaluate the antioxidant capacity of D-PAA, AgNPs/D-PAA and AuNPs/D-PAA. DNA cleavage, antimicrobial and biofilm inhibition effects of nanocomplexes were investigated. Nanocomplexes were found to be of moderate toxicity against fibroblasts with no genotoxicity observed. AgNPs/D-PAA reduced motility and proliferation at lower concentrations compared with the other studied nanomaterials. AgNPs/D-PAA and AuNPs/D-PAA showed radical scavenging capacities in a dose-dependent manner. The antimicrobial activity of AgNPs/D-PAA against various bacteria was found to be much higher compared to D-PAA and AuNPs/D-PAA, especially against E. hirae, E. faecalis and S. aureus, respectively. D-PAA, AgNPs/D-PAA and AuNPs/D-PAA showed DNA-cleaving and biofilm inhibitory activity, while AgNPs/D-PAA displayed the highest anti-biofilm activity. AgNPs/D-PAA and AuNPs/D-PAA were characterized by good antimicrobial activity. According to the findings of the study, AgNPs/D-PAA and AuNPs/D-PAA can be evaluated as alternatives for the preparation of new antimicrobial agents, the fight against biofilms, sterilization and disinfection processes. Our findings confirm the versatility of nanosystems based on dextran–polyacrylamide polymers and indicate that AgNPs/D-PAA and AuNPs/D-PAA can be evaluated as alternatives for the preparation of novel antimicrobial agents.
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Data are available from the corresponding authors on reasonable request.
References
Abdellatif AAH, Alturki HNH, Tawfeek HM (2021) Different cellulosic polymers for synthesizing silver nanoparticles with antioxidant and antibacterial activities. Sci Rep 11(1):84. https://doi.org/10.1038/s41598-020-79834-6
Abushaheen MA, Muzaheed, Fatani AJ, Alosaimi M, Mansy W, George M et al (2020) Antimicrobial resistance, mechanisms and its clinical significance. Disease-a-Month 66(6):100971. https://doi.org/10.1016/j.disamonth.2020.100971
Alkhulaifi MM, Alshehri JH, Alwehaibi MA, Awad MA, Al-Enazi NM, Aldosari NS et al (2020) Green synthesis of silver nanoparticles using citrus limon peels and evaluation of their antibacterial and cytotoxic properties. Saudi J Biol Sci 27(12):3434–3441. https://doi.org/10.1016/j.sjbs.2020.09.031
Ansar S, Tabassum H, Aladwan NSM, Naiman Ali M, Almaarik B, AlMahrouqi S et al (2020) Eco friendly silver nanoparticles synthesis by Brassica oleracea and its antibacterial, anticancer and antioxidant properties. Sci Rep 10(1):18564. https://doi.org/10.1038/s41598-020-74371-8
Aygün A, Özdemir S, Gülcan M, Cellat K, Şen F (2020) Synthesis and characterization of reishi mushroom-mediated green synthesis of silver nanoparticles for the biochemical applications. J Pharm Biomed Anal 178:112970. https://doi.org/10.1016/j.jpba.2019.112970
Bharathi D, Vasantharaj S, Bhuvaneshwari V (2018) Green synthesis of silver nanoparticles using Cordia dichotoma fruit extract and its enhanced antibacterial, anti-biofilm and photo catalytic activity. Mater Res Express 5(5):055404. https://doi.org/10.1088/2053-1591/aac2ef
Brito J, Hlushko H, Abbott A, Aliakseyeu A, Hlushko R, Sukhishvili SA (2021) Integrating antioxidant functionality into polymer materials: fundamentals, strategies, and applications. ACS Appl Mater Interfaces 13(35):41372–41395. https://doi.org/10.1021/acsami.1c08061
Bruna T, Maldonado-Bravo F, Jara P, Caro N (2021) Silver nanoparticles and their antibacterial applications. Int J Mol Sci. https://doi.org/10.3390/ijms22137202
Bulavin L, Kutsevol N, Chumachenko V, Soloviov D, Kuklin A, Marynin A (2016) SAXS combined with UV–Vis spectroscopy and QELS: accurate characterization of silver sols synthesized in polymer matrices. Nanoscale Res Lett 11(1):35. https://doi.org/10.1186/s11671-016-1230-2
Chumachenko V, Kutsevol N, Rawiso M, Schmutz M, Blanck C (2014) In situ formation of silver nanoparticles in linear and branched polyelectrolyte matrices using various reducing agents. Nanoscale Res Lett 9(1):164. https://doi.org/10.1186/1556-276x-9-164
Chumachenko VA, Shton IO, Shishko ED, Kutsevol NV, Marinin AI, Gamaleia NF (2016) Branched copolymers dextran-graft-polyacrylamide as nanocarriers for delivery of gold nanoparticles and photosensitizers to tumor cells. In: Fesenko O, Yatsenko L (eds) Nanophysics, nanophotonics, surface studies, and applications. Springer, Cham
Chumachenko V, Kutsevol N, Harahuts Y, Rawiso M, Marinin A, Bulavin L (2017) Star-like dextran-graft-pnipam copolymers. Effect of internal molecular structure on the phase transition. J Mol Liq 235:77–82. https://doi.org/10.1016/j.molliq.2017.02.098
Długosz O, Szostak K, Staroń A, Pulit-Prociak J, Banach M (2020) Methods for reducing the toxicity of metal and metal oxide NPs as biomedicine. Materials (Basel). https://doi.org/10.3390/ma13020279
Elbaz NM, Ziko L, Siam R, Mamdouh W (2016) Core-shell silver/polymeric nanoparticles-based combinatorial therapy against breast cancer in-vitro. Sci Rep 6(1):30729. https://doi.org/10.1038/srep30729
Fadel M, Kassab K, Abd El Fadeel DA, Nasr M, El Ghoubary NM (2018) Comparative enhancement of curcumin cytotoxic photodynamic activity by nanoliposomes and gold nanoparticles with pharmacological appraisal in HepG2 cancer cells and Erlich solid tumor model. Drug Dev Ind Pharm 44(11):1809–1816. https://doi.org/10.1080/03639045.2018.1496451
Feng G-n, Huang X-t, Jiang X-l, Deng T-w, Li Q-x, Li J-x et al (2021) The antibacterial effects of supermolecular nano-carriers by combination of silver and photodynamic therapy. Front Chem. https://doi.org/10.3389/fchem.2021.666408
Floris P, Garbujo S, Rolla G, Giustra M, Salvioni L, Catelani T et al (2021) The role of polymeric coatings for a safe-by-design development of biomedical gold nanoparticles assessed in zebrafish embryo. Nanomaterials. https://doi.org/10.3390/nano11041004
Frieri M, Kumar K, Boutin A (2017) Antibiotic resistance. J Infect Public Health 10(4):369–378. https://doi.org/10.1016/j.jiph.2016.08.007
Fulaz S, Vitale S, Quinn L, Casey E (2019) Nanoparticle-biofilm interactions: the role of the EPS matrix. Trends Microbiol 27(11):915–926. https://doi.org/10.1016/j.tim.2019.07.004
Gherasim O, Puiu RA, Bîrcă AC, Burdușel AC, Grumezescu AM (2020) An updated review on silver nanoparticles in biomedicine. Nanomaterials (Basel). https://doi.org/10.3390/nano10112318
Goswami SR, Sahareen T, Singh M, Kumar S (2015) Role of biogenic silver nanoparticles in disruption of cell–cell adhesion in Staphylococcus aureus and Escherichia coli biofilm. J Ind Eng Chem 26:73–80. https://doi.org/10.1016/j.jiec.2014.11.017
Gulbagca F, Ozdemir S, Gulcan M, Sen F (2019) Synthesis and characterization of Rosa canina-mediated biogenic silver nanoparticles for anti-oxidant, antibacterial, antifungal, and DNA cleavage activities. Heliyon 5(12):e02980. https://doi.org/10.1016/j.heliyon.2019.e02980
Gümüşgöz Çelik G, Gonca S, Şahin B, Özdemir S, Atilla D, Gürek AG (2022) Novel axially symmetric and unsymmetric silicon(iv) phthalocyanines having anti-inflammatory groups: synthesis, characterization and their biological properties. Dalton Trans 51(19):7517–7529. https://doi.org/10.1039/D2DT00652A
Karabasz A, Bzowska M, Szczepanowicz K (2020) Biomedical applications of multifunctional polymeric nanocarriers: a review of current literature. Int J Nanomed 15:8673–8696. https://doi.org/10.2147/ijn.S231477
Karami A, Xie Z, Zhang J, Kabir MS, Munroe P, Kidd S et al (2020) Insights into the antimicrobial mechanism of Ag and I incorporated ZnO nanoparticle derivatives under visible light. Mater Sci Eng C 107:110220. https://doi.org/10.1016/j.msec.2019.110220
Keshari AK, Srivastava R, Singh P, Yadav VB, Nath G (2020) Antioxidant and antibacterial activity of silver nanoparticles synthesized by Cestrum nocturnum. J Ayurveda Integr Med 11(1):37–44. https://doi.org/10.1016/j.jaim.2017.11.003
Klębowski B, Depciuch J, Parlińska-Wojtan M, Baran J (2018) Applications of noble metal-based nanoparticles in medicine. Int J Mol Sci. https://doi.org/10.3390/ijms19124031
Kutsevol N, Bezugla T, Bezuglyi M, Rawiso M (2012) Branched dextran-graft-polyacrylamide copolymers as perspective materials for nanotechnology. Macromol Symposia 317(1):82–90. https://doi.org/10.1002/masy.201100087
Kutsevol N, Naumenko A, Chumachenko V, Yeshchenko O, Harahuts Y, Pavlenko V (2018) Aggregation processes in hybrid nanosystem polymer/nanosilver/cisplatin. Ukr J Phys 63(6):513. https://doi.org/10.15407/ujpe63.6.513
Kutsevol N, Kuziv Y, Bezugla T, Virych P, Marynin A, Borikun T et al (2022) Application of new multicomponent nanosystems for overcoming doxorubicin resistance in breast cancer therapy. Appl Nanosci 12(3):427–437. https://doi.org/10.1007/s13204-020-01653-y
Lee NY, Ko WC, Hsueh PR (2019) Nanoparticles in the treatment of infections caused by multidrug-resistant organisms. Front Pharmacol 10:1153. https://doi.org/10.3389/fphar.2019.01153
Madakka M, Jayaraju N, Rajesh N (2021) Evaluating the antimicrobial activity and antitumor screening of green synthesized silver nanoparticles compounds, using Syzygium jambolanum, towards MCF7 cell line (breast cancer cell line). J Photochem Photobiol 6:100028. https://doi.org/10.1016/j.jpap.2021.100028
Mahamuni-Badiger PP, Patil PM, Badiger MV, Patel PR, Thorat-Gadgil BS, Pandit A et al (2020) Biofilm formation to inhibition: role of zinc oxide-based nanoparticles. Mater Sci Eng C Mater Biol Appl 108:110319. https://doi.org/10.1016/j.msec.2019.110319
Maraveas C, Bayer IS, Bartzanas T (2021) Recent advances in antioxidant polymers: from sustainable and natural monomers to synthesis and applications. Polymers 13(15):2465
Milanezi FG, Meireles LM, de Christo Scherer MM, de Oliveira JP, da Silva AR, de Araujo ML et al (2019) Antioxidant, antimicrobial and cytotoxic activities of gold nanoparticles capped with quercetin. Saudi Pharm J 27(7):968–974. https://doi.org/10.1016/j.jsps.2019.07.005
Mohd-Zahid MH, Zulkifli SN, Che Abdullah CA, Lim J, Fakurazi S, Wong KK et al (2021) Gold nanoparticles conjugated with anti-CD133 monoclonal antibody and 5-fluorouracil chemotherapeutic agent as nanocarriers for cancer cell targeting. RSC Adv 11(26):16131–16141. https://doi.org/10.1039/D1RA01093J
Mu W, Fang W, Yao Y (2021) Synthesis of Ag@Au core-shell NPs loaded with ciprofloxacin as enhanced antimicrobial properties for the treatment and nursing care of Escherichia coli infection. Microb Pathog 150:104619. https://doi.org/10.1016/j.micpath.2020.104619
Najahi-Missaoui W, Arnold RD, Cummings BS (2020) Safe nanoparticles: are we there yet? Int J Mol Sci. https://doi.org/10.3390/ijms22010385
Niño-Martínez N, Salas Orozco MF, Martínez-Castañón GA, Torres Méndez F, Ruiz F (2019) Molecular mechanisms of bacterial resistance to metal and metal oxide nanoparticles. Int J Mol Sci. https://doi.org/10.3390/ijms20112808
Okkeh M, Bloise N, Restivo E, De Vita L, Pallavicini P, Visai L (2021) Gold nanoparticles: can they be the next magic bullet for multidrug-resistant bacteria? Nanomaterials (Basel). https://doi.org/10.3390/nano11020312
Olfati A, Kahrizi D, Balaky STJ, Sharifi R, Tahir MB, Darvishi E (2021) Green synthesis of nanoparticles using Calendula officinalis extract from silver sulfate and their antibacterial effects on Pectobacterium caratovorum. Inorg Chem Commun 125:108439. https://doi.org/10.1016/j.inoche.2020.108439
Prakash J, Pivin JC, Swart HC (2015) Noble metal nanoparticles embedding into polymeric materials: from fundamentals to applications. Adv Colloid Interface Sci 226:187–202. https://doi.org/10.1016/j.cis.2015.10.010
Rai MK, Deshmukh SD, Ingle AP, Gade AK (2012) Silver nanoparticles: the powerful nanoweapon against multidrug-resistant bacteria. J Appl Microbiol 112(5):841–852. https://doi.org/10.1111/j.1365-2672.2012.05253.x
Ravichandran V, Vasanthi S, Shalini S, Ali Shah SA, Harish R (2016) Green synthesis of silver nanoparticles using Atrocarpus altilis leaf extract and the study of their antimicrobial and antioxidant activity. Mater Lett 180:264–267. https://doi.org/10.1016/j.matlet.2016.05.172
Reznickova A, Novotna Z, Kvitek O, Kolska Z, Svorcik V, Gold (2015) Silver and carbon nanoparticles grafted on activated polymers for biomedical applications. J Nanosci Nanotechnol 15(12):10053–10073. https://doi.org/10.1166/jnn.2015.11689
Salih Ağırtaş M, Karataş C, Özdemir S (2015) Synthesis of some metallophthalocyanines with dimethyl 5-(phenoxy)-isophthalate substituents and evaluation of their antioxidant-antibacterial activities. Spectrochim Acta A Mol Biomol Spectrosc 135:20–24. https://doi.org/10.1016/j.saa.2014.06.139
Sekar V, Al-Ansari MM, Narenkumar J, Al-Humaid L, Arunkumar P, Santhanam A (2022) Synthesis of gold nanoparticles (AuNPs) with improved anti-diabetic, antioxidant and anti-microbial activity from Physalis minima. J King Saud Univ Sci 34(6):102197. https://doi.org/10.1016/j.jksus.2022.102197
Sies H, Jones DP (2020) Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat Rev Mol Cell Biol 21(7):363–383. https://doi.org/10.1038/s41580-020-0230-3
Sinenko SA, Starkova TY, Kuzmin AA, Tomilin AN (2021) Physiological signaling functions of reactive oxygen species in stem cells: from flies to man. Front Cell Dev Biol. https://doi.org/10.3389/fcell.2021.714370
Singh P, Pandit S, Beshay M, Mokkapati V, Garnaes J, Olsson ME et al (2018) Anti-biofilm effects of gold and silver nanoparticles synthesized by the Rhodiola rosea rhizome extracts. Artif Cells Nanomed Biotechnol 46(sup3):S886-s99. https://doi.org/10.1080/21691401.2018.1518909
Sorokin A, Prokopiuk V, Grankina I, Borovoy I, Tkachenko A, Yefimova S (2022) Amphi-PIC J-aggregate-protein complexes: stability in blood and toxicity to cell cultures. IEEE 12th International Conference Nanomaterials: Applications & Properties (NAP). https://doi.org/10.1109/NAP55339.2022.9934581
Tkachenko A, Virych P, Myasoyedov V, Prokopiuk V, Onishchenko A, Butov D et al (2022) Cytotoxicity of hybrid noble metal-polymer composites. Biomed Res Int 2022:1487024. https://doi.org/10.1155/2022/1487024
Turunc E, Kahraman O, Binzet R (2021) Green synthesis of silver nanoparticles using pollen extract: characterization, assessment of their electrochemical and antioxidant activities. Anal Biochem 621:114123. https://doi.org/10.1016/j.ab.2021.114123
Yeshchenko OA, Naumenko AP, Kutsevol NV, Maskova DO, Harahuts II, Chumachenko VA et al (2018) Anomalous inverse hysteresis of phase transition in thermosensitive dextran-graft-PNIPAM copolymer/Au nanoparticles hybrid nanosystem. J Phys Chem C 122(14):8003–8010. https://doi.org/10.1021/acs.jpcc.8b01111
Yin Z, Burger N, Kula-Alwar D, Aksentijević D, Bridges HR, Prag HA et al (2021) Structural basis for a complex I mutation that blocks pathological ROS production. Nat Commun 12(1):707. https://doi.org/10.1038/s41467-021-20942-w
Zhang Y, Shareena Dasari TP, Deng H, Yu H (2015) Antimicrobial activity of gold nanoparticles and ionic gold. J Environ Sci Health Part C 33(3):286–327. https://doi.org/10.1080/10590501.2015.1055161
Zhao W, Lam JCF, Chiuman W, Brook MA, Li Y (2008) Enzymatic cleavage of nucleic acids on gold nanoparticles: a generic platform for facile colorimetric biosensors. Small 4(6):810–816. https://doi.org/10.1002/smll.200700757
Zulfiqar H, Amjad MS, Mehmood A, Mustafa G, Binish Z, Khan S et al (2022) Antibacterial, antioxidant, and phytotoxic potential of phytosynthesized silver nanoparticles using Elaeagnus umbellata fruit extract. Molecules 27(18):5847
Acknowledgements
The authors thank to University of Strasbourg Institut Charles Sadron, French PAUSE program for emergency welcome of Ukrainian scientist Dr. Nataliya Kutsevol (2022–2023), Catherine Foussat and Mélanie Legros from the characterization group of the Institut Charles Sadron (Strasbourg, France) for size exclusion chromatography characterization of the star-shaped polymer.
Funding
This study was supported in part by the funds provided by the Ministry of the Education and Science of Ukraine, Project no. 0122U00181 (Hybrid nanosystems based on “smart” polymers for biotechnology and medicine) and by National Research Foundation of Ukraine, Project 2020.02/0022 (Plasmon hybrid nanosystems “metal-polymer-fluorophore” with enhanced optical response for photonics and biomedical applications).
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Conceptualization: AT, ND, NK; Original draft writing: AT, N.K; Experimental data acquisition: SÖ, GT, AO, VP, VC, PV, VP; Interpretation of data: SÖ, GT, KO, VP, AO; Statistical analysis: KO, AO; Funding: NK.
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The study was approved by the Committee of Ethics and Bioethics at Kharkiv National Medical University, Kharkiv, Ukraine (minutes #3 dated 28 August 2020) and was performed in compliance with the EU Directive 2010/63/EU on the protection of animals used for scientific purposes.
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Tkachenko, A., Özdemir, S., Tollu, G. et al. Antibacterial and antioxidant activity of gold and silver nanoparticles in dextran–polyacrylamide copolymers. Biometals 37, 115–130 (2024). https://doi.org/10.1007/s10534-023-00532-7
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DOI: https://doi.org/10.1007/s10534-023-00532-7