Synthesis of Pincer type carbene and their Ag(I)-NHC complexes, and their Antimicrobial activities

Year 2022, , 53 - 61, 28.06.2022

Murat Turkyilmaz , Murat Dönmez , Murat Ates

https://doi.org/10.47481/jscmt.1117139

Cited By: 3

Abstract

In this study, theophylline (1) compounds were synthesized with addition of 2-bromoetha-nol, 2-bromoacetamide and methyl-2-bromoacetate to attain symmetric connections to NHCs (2a–c). New complexes containing the symmetric N-heterocyclic carbene (NHC) ligands were synthesized using azolium salts in dimethyl formamide (DMF). After the NHC predecessor compounds reacted with Ag₂O, Ag(I)-NHC complexes were synthesized in the following: 7,9-di-(2-hydroxyethyl)-8,9-dihydro-1,3-dimethyl-1H-purine-2,6(3H,7H)-dionedium silver(I)bromide (3a), 7,9-di(acetamide)-8,9-dihydro-1,3-dimethyl-1H-purine-2,6(3H,7H)-di-ondium silver(I)bromide (3b) and 7,9-di(methylacetate)-8,9-dihydro-1,3-dimethyl-1H-pu-rine-2,6(3H,7H)-diondiumsilver(I)bromide (3c). Both synthesized NHC predecessors (2a-c) and Ag(I)-NHC complexes (3a-c) were described by FTIR, 1H-NMR, 13C-NMR, liquid and solid-state conductivity values, TGA analysis, melting point analysis and XRD spectroscopy. In-vitro antibacterial activities of NHC-predecessors and Ag(I)-NHC complexes were tested against gram-positive bacteria (Staphylococcus Aureus and Bacillus Cereus), gram-negative bacteria (Escherichia Coli and Listeria Monocytogenes), and fungus (Candida Albicans) in Tryptic Soy Broth method. Ag(I)-NHC complexes showed higher antibacterial activity than pure NHC predecessors. The lowest microbial inhibition concentration (MIC) value of compound 3a was obtained as 11.56 μg/ml for Escherichia Coli and 11.52 μg/ml for Staphylococcus Aureus. All tested complexes displayed antimicrobial activity with different results.

Keywords

Antimicrobial activity, Candida Albicans, N-heterocyclic carbene (NHCs), SEM analysis., theophylline

Supporting Institution

Trakya University

Project Number

TUBAP-2014-106

References

• [1] Adagu, I. S., Nolder, D., Warhurst, D. C., & Rossignol J. F. (2002). In vitro activity of nitazoxanide and related compounds against isolates of Giardia intestinalis, Entamoeba histolytica and Trichomonas vaginalis. Journal of Antimicrobial Chemotherapy, 49(1), 103-111. https://doi.org/10.1093/jac/49.1.103.
• [2] Aktas, A., Taslimi, P., Gulcin, I. & Gok, Y. (2017). Novel NHC Precursors: Synthesis, Characterization, and Carbonic Anhydrase and Acetylcholinesterase Inhibitory Properties. Archiv der Pharmazie Chemistry in Life Sciences. 350(6), e201700045. https://doi.org/10.1002/ardp.201700045 .
• [3] Angoy, M., Jiménez, M. V., Lahoz, F. J., Vispe, E., & Pérez-Torrente, J. J. (2022). Polymerization of phenylacetylene catalyzed by rhodium(I) complexes with N-functionalized N-heterocyclic carbene ligands. Polymer Chemistry, 13, 1411-1421. https://doi.org/1.1039/D1PY650D.
• [4] Arce-Rodríguez, A., Pankratz, D., Preusse, M., Nikel, P. I., & Häussler, S. (2022). Dual Effect: High NADH Levels Contribute to Efflux-Mediated Antibiotic Resistance but Drive Lethality Mediated by Reactive Oxygen Species. mBio, 13(1). https://doi.org/10.1128/mbio.02434-21.
• [5] Augustine, R., Malik, H. N., Singhal, D. K., Mukherjee, A., Malakar, D., Kalarikkal, N., & Thomas, S. (2014). Electrospun polycaprolactone/ZnO nanocomposite membranes as biomaterials with antibacterial and cell adhesion properties. Journal Polymer Research, 21(3), 347. https://doi.org/10.1007/s10965-013-0347-6.
• [6] Awwad, N. S., Saleh, K., Abbas,. H. A. S., Alhanash, A. M., Alqadi, F. S., & Hamdy, M. S. (2019). Induction apoptosis in liver cancer cells by altering natural hydroxyapatite to scavenge excess sodium without deactivate sodium-potassium pump. Materials Research Express, 6(5), 055403. https://doi.org/10.1088/2053-1591/AB045C.
• [7] Balachandar, R., Navaneethan, R., Biruntha, M., Kumar, K. K. A., Govarthanan M., & Karmegam, N. (2022). Antibacterial activity of silver nanoparticles phytosynthesized from Glochidion candolleanum leaves. Materials Letters, 311, 131572. https://doi.org/10.1016/j.matlet.2021.131572.
• [8] Baixauli, F., Villa, M., & Pearce, E. L. (2019). Potassium shapes antitumor immunity. Metabolism Science, 363(6434), 1395-1396. https://doi.org/10.1126/science.aaw8800. [9] Barnes, P. J. (2013). Theophylline, national heart and lung institute, imperial college, London, UK American Journal of Respiratory and Critical Care Medicine, 188(8), 901-906. https://doi.org/10.1164/rccm.201302-0388PP.
• [10] Bera, S. S. & Szostak, M. 2022. Cobalt–N-Heterocyclic Carbene Complexes in Catalysis, Journal American Chemical Society, 12(5), 3111–3137. https://doi.org/10.1021/acscatal.1c05869.
• [11] Bertrand, B., Stefan L., Pirrotta, M., Monchaud, D., Bodio, E., Richard, P., Le Gendre P., Warmerdam, E., de Jager, M. H., Groothuis, G. M. M., Picquet, M., & Casini, A. (2014). Caffeine-Based Gold(I) N Heterocyclic Carbenes as Possible Anticancer Agents: Synthesis and Biological Properties. Inorganic Chemistry, 53(4), 2296-2303.https://doi.org/10.1021/ic403011h.
• [12] Bourissou, D., Guerret, O., Gabbai, P.F., & Betrand, G. (2000). Stable Carbenes. Chemical Reviews, 100(1), 39-92. https://doi.org/10.1021/cr940472u.
• [13] Campillo, D., Escudero, D., Baya, M., & Martín, A. (2022). Heteropolymetallic Architectures as Snapshots of Transmetallation Processes at Different Degrees of Transfer. Enviromental Research, 28(7), e202104538. https://doi.org/10.1002/chem.202104538.
• [14] Cara, A., Ferry, T., & Josse, J. (2022). Prophylactic Antibiofilm Activity of Antibiotic-Loaded Bone Cements against Gram-Negative Bacteria, Antibiotics, 11(2), 137. https://doi.org/10.3390/antibiotics11020137.
• [15] Chang, Y. L., Hsu, Y. J., Chen, Y., Wang, Y. W., & Huang S. M. (2017). Theophylline exhibits anticancer activity via suppressing SRSF3 in cervical and breast cancer cell lines. Oncotarget, 8(60), 101461-101474. https://doi.org/10.18632/oncotarget.21464.
• [16] Chen, X., Wei, Z., Huang, K.-H., Uehling, M., Wleklinski, M., Krska, S., Makarov, A, A., Nowak, T., & Cooks, G. (2022). Pd Reaction Intermediates in Suzuki-Miyaura Cross-Coupling Characterized by Mass Spectrometry. ChemPlusChem, 87(3), e202100545. https://doi.org/10.1002/cplu.202100545.
• [17]. Cherak, Z., Loucif L., Moussi, A., Bendjama E., Benbouza A., & Rolain, J.-M. (2022). Emergence of Metallo-β-Lactamases and OXA-48 Carbapenemase Producing Gram-Negative Bacteria in Hospital Wastewater in Algeria: A Potential Dissemination Pathway Into the Environment. Microbial Drug Resistance, 28(1), 23-30. https://doi.org/10.1089/mdr.2020.0617.
• [18] Claraz, A. (2022). Bicyclic 5-6 Systems with One Bridgehead (Ring Junction) Nitrogen Atom: Four Extra Heteroatoms 2:2, Comprehensive Heterocyclic Chemistry IV, 11. Elsevier, 802-858. https://doi.org/10.1016/B978-0-12-818655-8.00086-X.
• [19] Dagi, H. T., Findik, D., Senkeles, C., & Arslan, U. (2016). Identification and antifungal susceptibility of Candida species isolated from bloodstream infections in Konya, Turkey. Annals of Clinical Microbiology and Antimicrobials, 15(1), 36. https://doi.org/10.1186/s12941-016-0153-1.
• [20] Das, R., Hepp, A., Daniliuc, C. G., & Hahn, F. E. (2014). Synthesis of complexes with protic NH,NH-NHC ligands via oxidative addition of 2-Halogenoazoles to zero-valent transition metals. Organometallics, 33(23), 6975-6987. https://doi.org/10.1021/om501120u.
• [21] Edwards, P. G., & Hahn, F. E. (2011). Synthesis and coordination chemistry of macrocyclic ligands featuring NHC donor groups. Dalton Trans, 40(40), 10278-10288. https://doi.org/10.1039/C1DT10864F.
• [22] Espíndola, L. C. P., Picão, R. C., Mançano, S. M. C. N., do Souto, R. M., & Colombo, A. P. V. (2022). Prevalence and antimicrobial susceptibility of Gram-negative bacilli in subgingival biofilm associated with periodontal diseases, Journal of Periodontology, 93(1), 69-79. https://doi.org/10.1002/JPER.20-0829.
• [23] Flowers, S. E. Johnson, M. C. Pitre B. Z., & Cossairt, B. M. (2018). Synthetic routes to a coordinatively unsaturated ruthenium complex supported by a tripodal, protic bis(N-heterocyclic carbene) phosphine ligand. Dalton Transactions, 47(4), 1276-1283. https://doi.org/10.1039/C7DT04333C.
• [24] Fox, M. A., Mahon, M. F., Patmore, N. J., & Weller, A. S. (2002). Solution and solid-state structure of the anion [Ag2{closo-CB11H12}4]2-. Inorganic Chemistry, 41(17), 4567-4573. https://doi.org/10.1021/ic025730h.
• [25] Gaydon, Q., & Bohle, D. S. (2022). Coordination Chemistry of the Parent Dithiocarbamate H2NCS2–: Organometallic Chemistry and Tris-Chelates of Group 9 Metals. Inorganic Chemistry, 61(11), 4660–4672. https://doi.org/10.1021/acs.inorgchem.1c03789.
• [26] Gil-Sepulcre, M., & Llobet, A. (2022). Molecular water oxidation catalysts based on first-row transition metal complexes. Natural Catalysis, 5(1), 79–82. https://doi.org/10.1038/s41929-022-00750-1.
• [27] Gomaa, A., Elshenawy, M., Afifi N., Mohammed, E., Thabit R., & Pharmacol J. (2009). Enhancement of the anti-inflammatory and anti-arthritic effects of theophylline by a low dose of a nitric oxide donor or non-specific nitric oxide synthase inhibitor. British J Pharmacology of Pharmacological, 158(7), 1835-1847. https://doi.org/10.1111/j.1476-5381.2009.00468.x.
• [28] Hahn, F. E. & Jahnke, M. C. (2008). Heterocyclic carbenes: synthesis and coordination chemistry. Angewandte Chemie International Edition, 47, 3122-3172. https://doi.org/10.1002/anie.200703883.
• [29] Haque, R. A., Asekunowo, P. O., Razali, M. R., & Mohammad, F. (2019). NHC–Silver(I) Complexes as Chemical Nucleases; Synthesis, Crystal Structures, and Antibacterial Studies. Heteroatom Chemistry, 253, 94-204. https://doi.org/10.1002/hc.21160.
• [30] Hamdani, H. E., Amane, M. & Duhayon, E. C. (2017). Crystal structure of tetraaquabis(1,3-dimethyl-2,6-dioxo-7H-purin-7-ido-kN7)cobalt(II). Acta Crystallographica Section E: Crystallographic Communications, 73(9), 1302-1304. https://doi.org/10.1107/S2056989017011379.
• [31] He, Z., Huang, K., Xiong, F., Zhang, S. F., Xue, J. R., Liang, Y., Jing, L. H. & Qin D. B. (2015). Self-assembly of imidazoliums salts based on acridine with silver oxide as coordination polymers: Synthesis, fluorescence and antibacterial activity. Journal of Organometalic Chemistry, 797, 67–75. https://doi.org/10.1016/j.jorganchem.2015.07.030.
• [32] Herrmann, W. A. (2002). N-Heterocyclic carbenes: A New concept in organometallic catalysis. Angewandte Chemie International Edition, 41(8), 1290-1309. https://doi.org/10.1002/1521-3773(20020415)41:8<1290::AID-ANIE1290>3.0.CO;2-Y.
• [33] Hu, A., & Wilson, J. J. (2022). Advancing Chelation Strategies for Large Metal Ions for Nuclear Medicine Applications, Accounts Chemical Research, 55(6), 904–915. https://doi.org/10.1021/acs.accounts.2c00003. [34] Hu, J., Li, M., Wan J., Sun J.,Gao, H., Zhang, F., & Zhang, Z. (2022). Metal-free oxidative synthesis of benzimidazole compounds by dehydrogenative coupling of diamines and alcohols. Organic & Biomolecular Chemistry, 20, 2852-2856. https://doi.org/10.1039/D2OB00165A.
• [35] Hu, X. L., Castro-Rodriguez, I., Olsen, K., & Meyer, K. (2004). Group 11 Metal complexes of N Heterocyclic carbene ligands: Nature of the Metal-Carbene Bond. Organometallics, 23(4), 755-764. https://doi.org/10.1021/om0341855.
• [36] Hussaini, S. Y., Haque, R. A., & Razali, M. R. (2019). Recent progress in silver(I)-, gold(I)/(III)- and palladium(II)-N-heterocyclic carbene complexes: A review towards biological perspectives. Journal of Organometalic Chemistry, 882, 96-111. https://doi.org/10.1016/j.jorganchem.2019.01.003.
• [37] Iqbal, M. A., Umar, M. I., Haque, R. A., Ahamed, M. B. K., Asmawi, M. Z. B. & Majid, A. M. S. A. (2015). Macrophage and Colon Tumor Cells as Targets for a Binuclear Silver(I) Nheterocyclic Carbene Complex, an Anti-inflammatory and Apoptosis Mediator. Inorganic Biochemistry, 146, 1-13. https://doi.org/10.1016/j.jinorgbio.2015.02.001.
• [38] Jiang, X., Wang, Y., & Jiang, S. (2010). The effects of substitution of Cr for Mo on the mechanical properties of nanocrystalline Mo5Si3 films. Nanoscale, 2(3), 394-398. https://doi.org/10.1039/b9nr00225a.
• [39] Karimi-Maleh, H., Khataee, A., Karimi, F., Baghayeri, M. F. L., Rouhi, J., Karaman, C., Karaman, O., & Boukherroubk, R. 2022. A green and sensitive guanine-based DNA biosensor for idarubicin anticancer monitoring in biological samples: A simple and fast strategy for control of health quality in chemotherapy procedure confirmed by docking investigation. Chemosphere, 291(3), 132928. https://doi.org/10.1016/j.chemosphere.2021.132928.
• [40] Karmakar, S., & Datta, A. (2014). Tunneling assists the 1, 2-Hydrogen shift in N-heterocyclic carbenes. Angewandte Chemie International Edition, 53, 9587-9591. https://doi.org/10.1002/anie.201404368.
• [41] Kampert, F., Brackemeyer, D., Tan, T. T. Y., & Hahn F. E. (2018). Selective C8-metalation of purine nucleosides via oxidative addition. Organometallics, 37, 4181-4185. https://doi.org/10.1021/acs.organomet.8b00685.
• [42] Kosuru, S. R., Chang, Y.-L., Chen, P.-Y., Lee,W. Lai, Y.-C. Ding, S. Chen, H.-Y., Chen, H.-Y., & Chang, Y.-C., (2022). Ring-Opening Polymerization of ε-Caprolactone by Using Aluminum Complexes Bearing Aryl Thioether Phenolates: Labile Thioether Chelation. Inorganic. Chemistry, 61(9), 3997–4008. https://doi.org/10.1021/acs.inorgchem.1c03683.
• [43] Kösterke, T., Kösters, J., Würthwein, E. U., Mück-Lichtenfeld, C., Schulte Brinke, C. F., Lahoz, F., & Hahn, F. E. (2012). Synthesis of Complexes Containing an Anionic NHC Ligand with an Unsubstituted Ring-Nitrogen Atom. Chemistry-A European Journal, 18(46), 14594-14598. https://doi.org/10.1002/chem.201202973.
• [44] Kösterke, T., Pape, T., & Hahn, F. E. (2011). Synthesis of NHC complexes by oxidative addition of 2-Chloro-N-methylbenzimidazole. Journal American Chemical Society, 133(7), 2112-2115. https://doi.org/10.1021/ja110634h.
• [45] Kuwata, S., & Hahn, F. E. (2018). Complexes bearing protic N-heterocyclic carbene ligands. Chemical Reviews, 118(119), 9642-9677. https://doi.org/10.1021/acs.chemrev.8b00176.
• [46] Li, Y., Wang, W.-X., & Liu, H. (2022). Gut-microbial adaptation and transformation of silver nanoparticles mediated the detoxification of Daphnia manga and their offspring, Environtal Science:Nano, 9, 361-374. https://doi.org/10.1039/D1EN00765C.
• [47] Lv, G., Guo, L., Qiu, L., Yang, H., Wang, T., Liu, H., & Lin, J. (2015). Lipophilicity-dependent ruthenium N-heterocyclic carbene complexes as potential anticancer agents. Dalton Transactions, 44(16), 7324–7331. https://doi.org/10.1039/C5DT00169B.
• [48]. Marelius, D. C., Darrow E. H., Moore C. E., Golen, J. A., Rheingold, A. L., & Grotjahn, D. B. (2015). Hydrogen-bonding pincer complexes with two protic N-Heterocyclic carbenes from direct metalation of a 1,8-Bis(imidazol-1-yl)carbazole by Platinum, Palladium, and Nickel. Chemistry A European Journal, 21(31), 10988-10992. https://doi.org/10.1002/chem.201501945.
• [49] Meier, N., Hahn F. E., Pape, T., Siering C. S. R., & Waldvogel, S. (2007). Molecular recognition utilizing complexes with NH, NR-stabilized carbene ligands. European Journal Inorganic Chemistry, 9(66), 1210-1214. https://doi.org/10.1002/ejic.200601258.
• [50] Medici, S., Peana M., Crisponi, G., Nurchi, V. M., Lachowicz, J. I., Remelli M., & Zoroddu, M. A. (2016). Silver coordination compounds: a new horizon in medicine. Coordination Chemical Reviews, 327-328, 349-359. https://doi.org/10.1016/j.ccr.2016.05.015.
• [51] Mohamed, H. A. Lake, B. R. M. Laing, T. Phillips R. M., & Willans, C. E. (2015). Synthesis and anticancer activity of silver(I)–N-heterocyclic carbene complexes derived from the natural xanthine products caffeine, theophylline and theobromine. Dalton Transactions, 44(16), 7563-7569. https://doi.org/10.1039/C4DT03679D.
• [52] Nikolić, M. V., Mijajlović, M. Ž., Jevtić, V. V., Ratković, Z. R., Radojević, I. D., Čomić, Lj. R., Novaković, S. B., Bogdanović, G. A., Trifunović, S. R., & Radić, G. P. (2014). Synthesis, characterization and antimicrobial activity of copper(II) complexes with some S-alkyl derivatives of thiosalicylic acid. Crystal structure of the binuclear copper(II) complex with S-methyl derivative of thiosalicylic acid. Polyhedron, 79, 80-87. https://doi.org/10.1016/j.poly.2014.04.053.
• [53]Nunnari, G., Argyris E., Fang, J., Mehlman, K. E., Pomerantz, R. J., & Daniel, R. (2005). Inhibition of HIV-1 replication by caffeine and caffeine-related methylxanthines. Virology, 335(2), 177-184. https://doi.org/10.1016/j.virol.2005.02.015.
• [54] Oñatibia-Astibia, A., Franco, R. & Martínez-Pinilla E. 2017. Health benefits of methylxanthines in neurodegenerative diseases, Molecılar Nutritoon & Food Research. 61(6), 1600670. https://doi.org/10.1002/mnfr.201600670.
• [55] Pfaller, M. A, & Diekema, D. J., 2012. Progress in Antifungal Susceptibility Testing of Candida spp. by Use of Clinical and Laboratory Standards Institute Broth Microdilution Methods, 2010 to 2012. Journal of Clinical Microbiology, 50(9), 2846-2856. https://doi.org/10.1128/JCM.00937-12.
• [56] Pacholak, A., Burlaga, N., Frankowski, R., Zgoła-Grześkowiak, A., & Kaczorek, E. 2022. Azole fungicides: (Bio)degradation, transformation products and toxicity elucidation, Science of The Total Environment, 802, 149917. https://doi.org/10.1016/j.scitotenv.2021.149917.
• [57] Peng, H., Su Q., Lin, Z. C., Zhu, X. H., Peng, M. S., & Lv, Z. B. (2018). Potential suppressive effects of theophylline on human rectal cancer SW480 cells in vitro by inhibiting YKL-40 expression. Oncology Letters, 15(5), 7403-7408. https://doi.org/10.3892/ol.2018.8220.
• [58] Peris, E. (2018). Smart N-Heterocyclic carbene ligands in catalysis. Chemical Reviews, 118(19), 9988-10031. https://doi.org/10.1021/acs.chemrev.6b00695.
• [59] Ranjbar, Z. R., Khatamifar, M., & Fatemi S. J. (2018). Chelation therapy: Assessing the impact of deferasirox size on Lead (II) release from biological systems. Main Group Chemistry, 17(2), 181-189. https://doi.org/10.3233/MGC-180260.
• [60] Sarı, Y., Aktas, A., Celepci, D. B., Gok, Y. & Aygun, M. 2017. Synthesis, Characterization and Crystal Structure of New 2-Morpholinoethyl-Substituted Bis-(NHC)Pd(II) Complexes and the Catalytic Activity in the Direct Arylation Reaction. Catalysis Letters, 147(9), 2340-2351. https://doi.org/10.1007/s10562-017-2132-3.
• [61] Shah, S.R., Shah, Z., Khan, A., Ahmed, A., Sohani Hussain J., Csuk R., Anwar M. U., & Al-Harrasi A. (2019). Sodium, Potassium, and Lithium complexes of phenanthroline and diclofenac: First report on anticancer studies. ACS Omega, 4(25), 21559-21566. https://doi.org/10.1021/acsomega.9b03314.
• [62] Shan, N., & Zaworotko, M. J. (2008). The role of cocrystals in pharmaceutical science. Drug Discovery Today, 13(9-10), 440-446. https://doi.org/10.1016/j.drudis.2008.03.004.
• [63] Shahini, C. R., Achar G., Budagumpi, S., Tacke, M., & Patil, S. A. (2017). Synthesis, structural investigation and antibacterial studies of non–symmetrically p–nitrobenzyl substituted benzimidazole N–heterocyclic carbene–silver(I) complexes. Inorganic Chimica Acta, 466, 432-441. https://doi.org/10.1016/j.ica.2017.06.072.
• [64] Schmer, A., Alcaraz, A. G., Kyri, A. W., Schnakenburg G., Ferao A. E., & Streube, R. (2022). Synthesis of azadiphosphiridine complexes. Theoretical studies on ring formation, the P-to-P′ metal shift and the resulting nitrogen geometry. Dalton Transactions, (8):51, 3275-3279. https://doi.org/10.1039/D1DT04252A.
• [65] Soltani, S., Akhbari, K., & White, J. 2020. Synthesis, crystal structure and antibacterial activity of a homonuclear nickel(II) metal-organic nano supramolecular architecture. Polyhedron, 176, 114301. https://doi.org/10.1016/j.poly.2019.114301.
• [66] Szmukler-Moncler, S., Testori T., & Bernard, J. P. (2004). Etched implants: a comparative surface analysis of four implant systems. Journal of Biomedical Materials Research Part B Applied Biomaterial, 69B(1), 46-57. https://doi.org/10.1002/jbm.b.20021.
• [67] Thakar, M. A., Jha, S. S., Phasinam, K., Manne, R., Qureshi, Y., & Babu, V. V. H. (2022). X ray diffraction (XRD) analysis and evaluation of antioxidant activity of copper oxide nanoparticles synthesized from leaf extract of Cissus vitiginea, Materialstoday:Proceedings, 51(1), 319-324. https://doi.org/10.1016/j.matpr.2021.05.410.
• [68] Tiri, R. N. E., Gulbagca, F., Aygun, A., Cherif, A., & Sen, F., 2022. Biosynthesis of Ag–Pt bimetallic nanoparticles using propolis extract: Antibacterial effects and catalytic activity on NaBH4 hydrolysis, 206, 15-112622. Environmental Research, https://doi.org/10.1016/j.envres.2021.112622.