Abstract
Emerging β-lactam antibiotic resistance necessitates the development of new therapeutic approaches. One approach to counteract this issue is the use of nanoparticles (NPs) for antimicrobial agent delivery. In this work, superparamagnetic MnFe2O4 NPs were synthesized via a simple co-precipitation method followed by coating with a SiO2 shell using tetraethoxysilane (TEOS) to prevent agglomeration and also increase the density of hydroxyl groups on the surface of MnFe2O4 NPs. The resulting MnFe2O4@SiO2 nanostructures were further functionalized with 3-aminopropyltriethoxysilane (APTES) to introduce NH2 groups on the surface of NPs for covalent grafting of ampicillin (AMP), β-lactam antibiotic. The MnFe2O4@AMP NPs proved to be highly effective for the eradication of Escherichia coli bacteria with a minimum inhibitory concentration (MIC) equivalent to 4 µg/mL of immobilized AMP, lowered by 50% compared to free AMP. The intrinsic multivalence effect of the nanostructures as well as the protection of the COO− group of the antibiotic from the attack of β-lactamase enzyme is believed to be responsible for enhanced efficiency of the hybrid compared to free AMP.
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References
Ansari SAMK, Ficiara E, Ruffinatti FA, Stura I, Argenziano M, Abollino O, Cavalli R, Guiot C, Agata FD (2019) Magnetic iron oxide nanoparticles: synthesis, characterization and functionalization for biomedical applications in the central nervous system. Materials (Basel) 12:465. https://doi.org/10.3390/ma12030465
Bongu CS, Ragupathi J, Nallathamby K (2016) Exploration of MnFeO3/multiwalled carbon nanotubes composite as potential anode for lithium ion batteries. Inorg Chem 55:11644–11651. https://doi.org/10.1021/acs.inorgchem.6b00953
Ciro Y, Rojas J, Garzon JO, Salamanca CH (2019) Synthesis, characterisation and biological evaluation of ampicillin-chitosan-polyanion nanoparticles produced by ionic gelation and polyelectrolyte complexation assisted by high-intensity sonication. Polymers 11:1758. https://doi.org/10.3390/polym11111758
Das M, Mishra D, Dhak P, Gupta S, Maiti TK, Basak A, Pramanik P (2009) Biofunctionalized, phosphonate-grafted, ultrasmall iron oxide nanoparticles for combined targeted cancer therapy and multimodal imaging. Small 5:2883–2893. https://doi.org/10.1002/smll.200901219
Esmaeili A, Ghobadianpour S (2016) Vancomycin loaded superparamagnetic MnFe2O4 nanoparticles coated with PEGylated chitosan to enhance antibacterial activity. Int J Pharm 501:326–330. https://doi.org/10.1016/j.ijpharm.2016.02.013
Fan Y, Pauer AC, Gonzales AA, Fenniri H (2019) Enhanced antibiotic activity of ampicillin conjugated to gold nanoparticles on PEGylated rosette nanotubes. Int J Nanomed 14:7281–7289. https://doi.org/10.2147/IJN.S209756
Gao R, Mu X, Hao Y, Zhang L, Zhang J, Tang Y (2014) Combination of surface imprinting andimmobilized template techniques for preparation of core–shell molecularly imprinted polymers based on directly am ino-modified Fe3O4 nanoparticles for specific recognition of bovine hemoglobin. J Mater Chem B 2:1733–1741. https://doi.org/10.1039/C3TB21684E
Geng L, Yan F, Dong C, An C (2019) Design and Regulation of Novel MnFe2O4@C nanowires as high performance electrode for supercapacitor. Nanomaterials (Basel) 9:777. https://doi.org/10.3390/nano9050777
Ghutepati PR, Salunkhe AB, Khot VM, Pawar SH (2019) APTES (3-aminopropyltriethoxy silane) functionalized MnFe2O4 nanoparticles: a potential material for magnetic fluid hyperthermia. Chem Pap 73:2189–2197. https://doi.org/10.1007/s11696-11019-00768-z
Hernandez-Hernandez AA, Aguirre-Alvarez G, Carino-Cortes R, Mendoza-Huizar LH, Jimenez-Alvarado R (2020) Iron oxide nanoparticles: synthesis, functionalization, and applications in diagnosis and treatment of cancer. Pap Chem. https://doi.org/10.1007/s11696-020-01229-8
Hussain S, Joo J, Kang J, Kim B, Braun GB, She Z, Kim D, Mann AP, MölderT TT, Carnazza S, Guglielmino S, Sailor MJ, Ruoslahti E (2018) Antibiotic-loaded nanoparticles targeted to the site of infection enhance antibacterial efficacy. Nat Biomed Eng 2:95–103. https://doi.org/10.1038/s41551-017-0187-5
Jardim KV, Palomec-Garfias AF, Andrade BYG, Chaker JA, Báo SN, Marquez-Beltran C, Moya SE, Parize AL, Sousa MH (2018) Novel magneto-responsive nanoplatforms based on MnFe2O4 nanoparticles layerby- layer functionalized with chitosan and sodium alginate for magnetic controlled release of curcumin. Mater Sci Eng C 92:184–195. https://doi.org/10.1016/j.msec.2018.06.039
Jijie R, Barras A, Bouckaert J, Dumitrascu N, Szunerit S, Boukherroub R (2018) Enhanced antibacterial activity of carbon dots functionalized with ampicillin combined with visible light triggered photodynamic effects. Colloids Surf B Biointerfaces 170:347–354. https://doi.org/10.1016/j.colsurfb.2018.06.040
Jijie R, Barras A, Teodorescu F, Boukherroub R, Szunerit S (2017) Advancements on the molecular design of nanoantibiotics: current level of development and future challenges. Mol Syst Des Eng 2:349–369. https://doi.org/10.1039/C7ME00048K
Kalmer RR, Mohammadi M, Karimi A, Najafpour G, Haghighatnia Y (2019) Fabrication and evaluation of carboxymethylated diethylaminoethyl cellulose microcarriers as support for cellular applications. Carbohyd Polym 226:115284. https://doi.org/10.1016/j.carbpol.2019.115284
Khatoon N, Alam H, Khan A, Raza K, Sardar M (2019) Ampicillin Silver Nanoformulations against Multidrug resistant bacteria. Sci Rep 9:6848. https://doi.org/10.1038/s41598-019-43309-0
Kim J, Cho HR, Jeon H, Kim D, Song C, Lee N, Choi SH, Hyeon T (2017) Continuous O2-evolving MnFe2O4 nanoparticle-anchored mesoporous silica nanoparticles for efficient photodynamic therapy in hypoxic cancer. J Am Chem Soc 139:10992–10995. https://doi.org/10.1021/jacs.7b05559
Kumar M, Curtis A, Hoskins C (2018) Application of nanoparticle technologies in the combat against anti-microbial resistance. Pharmaceutics 10:1–17. https://doi.org/10.3390/pharmaceutics10010011
Langeroudi MP, Binaeian E (2018) Tannin-APTES modified Fe3O4 nanoparticles as a carrier of methotrexate drug:kinetic, isotherm and thermodynamic studies. Mater Chem Phys 218:210–217. https://doi.org/10.1016/j.matchemphys.2018.07.044
Liu Y, Li Y, Li XM, He T (2013) Kinetics of (3-Aminopropyl)triethoxylsilane (APTES) Silanization of Superparamagnetic Iron Oxide Nanoparticles. Langmuir 29:15275–15282. https://doi.org/10.1021/la403269u
Mazur M, Barras A, Kuncser V, Galatanu A, Zaitzev V, Turcheniuk KV, Woisel P, Lyskawa J, Laure W, Siriwardena A, Boukherroub R, Szunerits S (2013) Iron oxide magnetic nanoparticles with versatile surface functions based on dopamine anchors. Nanoscale 5:2692–2702. https://doi.org/10.1039/C3NR33506B
Mondal DK, Borgohain C, Paul N, Borah JP (2018) Improved heating efficiency of bifunctional MnFe2O4/ZnS nanocomposite for magnetic hyperthermia application. Physica B Condens Matter 567:122–128. https://doi.org/10.1016/j.physb.2018.11.068
Olariu CI, Yiu HHP, Bouffier L, Nedjadi T, Costello E, Williams SR, Halloran CM, Rosseinsky MJ (2011) Multifunctional Fe3O4 nanoparticles for targeted bi-modal imaging of pancreatic cancer. J Mater Chem 21:12650–12659. https://doi.org/10.1039/C1JM11370D
Oliveira JFA, Saito A, Bido AT, Kobarg J, Stassen HK, Cardoso MB (2017) Defeating bacterial resistance and preventing mammalian cells toxicity through rational design of antibiotic-functionalized nanoparticles. Sci Rep 7:1326. https://doi.org/10.1038/s41598-017-01209-1
Pal M, Rakshit R, Mandal K (2014) Surface modification of MnFe2O4 nanoparticles to impart intrinsic multiple fluorescence and novel photocatalytic properties. ACS Appl Mater Interfaces 6:4903–4910. https://doi.org/10.1021/am405950q
Post P, Wulitzer L, Friedrichs WM, Weber AP (2018) Characterization and applications of nanoparticles modified in-flight with silica or silica-organic coatings. Nanomaterials 8:530. https://doi.org/10.3390/nano8070530
Rashid Z, Soleimani M, Ghahremanzadeh R, Vossoughi M, Esmaeili E (2017) Effective surface modification of MnFe2O4@SiO2@PMIDA magnetic nanoparticles for rapid and high-density antibody immobilization. Appl Surf Sci 426:1023–1029. https://doi.org/10.1016/j.apsusc.2017.07.246
Reddy DHK, Wei W, Shuo L, Song MH, Yun YS (2017) Fabrication of stable and regenerable amine functionalized magnetic nanoparticles (MnFe2O4@SiO2-NH2) as a potential material for Pt(IV) recovery from acidic solutions. ACS Appl Mater Interfaces 9:18650–18659. https://doi.org/10.1021/acsami.6b16813
Sen S, Konar S, Pathak A, Dasgupta S, Gupta SD (2014) Effect of functionalized magnetic MnFe2O4 nanoparticles on fibrillation of human serum albumin. J Phys Chem B 118:11667–11676. https://doi.org/10.1021/jp507902y
Shah SA, Asdi MH, Hashmi MU, Umar MF, Awan SU (2012) Thermo-responsive copolymer coated MnFe2O4 magnetic nanoparticles for hyperthermia therapy and controlled drug delivery. Mater Chem Phys 137:365–371. https://doi.org/10.1016/j.matchemphys.2012.09.035
Swaidan A, Borthakur P, Boruah PK, Das MR, Barras A, Hamieh S, Toufaily J, Hamieh T, Szunerits S, Boukherroub R (2019) A facile preparation of CuS-BSA nanocomposite as enzyme mimics: Application for selective and sensitive sensing of Cr(VI) ions. Sens Actuators B Chem 294:253–262. https://doi.org/10.1016/j.snb.2019.05.052
Taavoni-Gilan A (2019) Chemical synthesis of MnFe2O4/chitosan nanocomposites for controlled release of ofloxacin drug. J Chin Chem Soc 66:600–607. https://doi.org/10.1002/jccs.201800402
Wang G, Zhao D, Ma Y, Zhang Z, Che H, Mu J, Zhang X, Zhang Z (2018) Synthesis and characterization of polymer-coated manganese ferrite nanoparticles as controlled drug delivery. Appl Surf Sci 428:258–263. https://doi.org/10.1016/j.apsusc.2017.09.096
Wang H, Yao Q, Wang C, Ma Z, Sun Q, Fan B, Jin C, Chen Y (2017) Hydrothermal synthesis of nanooctahedra MnFe2O4onto thewood surface with soft magnetism, fire resistance and electromagneticwave absorption. Nanomaterials (Basel) 7:118. https://doi.org/10.3390/nano7060118
Wu W, He Q, Jiang C (2008) Magnetic iron oxide nanoparticles: synthesis and surfacefunctionalization strategies. Nanoscale Res Lett 3:397–415. https://doi.org/10.1007/s11671-008-9174-9
Zhan S, Zhu D, Ma S, Yu W, Jia Y, Li Y, Yu H, Shen Z (2015) Highly efficient removal of pathogenic bacteria with magnetic graphene composite. Appl Mater Interfaces 7:4290–4298. https://doi.org/10.1021/am508682s
Zhu N, Ji H, Yu P, Niu J, Farooq MU, Akram MW, Udego IO, Li H, Niu X (2018) Surface modification of magnetic iron oxide nanoparticles. Nanomaterials (Basel) 8:810. https://doi.org/10.3390/nano8100810
Acknowledgements
Authors are sincerely acknowledged the financial support provided by the Centre National de la Recherche Scientifique (CNRS), the University of Lille, the Hauts-de-France region. Authors are also gratefully acknowledged Babol Noshirvani University of Technology throughout Ph.D. Research Grant No.: BNUT/ 945150001/98. This study was part of Ph.D. thesis of Neda Akhlaghi, proposed and approved by Faculty of Chemical Engineering, Noshirvani University of Technology, Babol, Iran. Authors are also gratefully acknowledged Biotechnology Research Institute of Chemical Engineering in Babol Noshirvani University of Technology and Centre National de la Recherche Scientifique in University of Lille for facilitating the present research.
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Akhlaghi, N., Najafpour-Darzi, G., Barras, A. et al. Magnetic MnFe2O4 Core–shell nanoparticles coated with antibiotics for the ablation of pathogens. Chem. Pap. 75, 377–387 (2021). https://doi.org/10.1007/s11696-020-01306-y
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DOI: https://doi.org/10.1007/s11696-020-01306-y