Synergistic Inhibitory Effect of Biosynthesized ZnO-CuO Nanocomposite on Biofilm Formation of Proteus mirabilis
Main Article Content
Abstract
Proteus mirabilis is considered the third most common cause of catheter-associated urinary tract infections. With urease production, the potency of the catheter’s blockage due to the formation of biofilm is significantly enhanced. This study was aimed at exploring whether green synthesized ZnO-CuO nanoparticles (ZnO-CuO NPs) can function as an anti-biofilm agent produced by P.Mirabilis. The characterization of biosynthesized nanoparticles was carried out to determine the chemical and physical properties of the product using AFM, TEM, FESEM, XRD, and UV visible spectrometry. The hexagonal structure was confirmed by XRD, the size range was marked at 96.00nm by TEM, and FESEM was used to confirm the surface morphology. AFM analysis is used to reveal the roughness and distribution of nanoparticles. UV-visible spectra of the synthesized nanoparticles recorded a maximum peak at 287nm and 232nm. Zinc and Copper nanoparticles showed remarkable biofilm inhibitory effects on wild-type strains of multidrug-resistant Proteus mirabilis.
Downregulation changes in LuxS expression using real-time PCR technology were detected after treatment with the ZnO-CuO nanocomposite of these strains. A cytotoxicity test of CuO-ZnO NPs-based nanocomposite showed that this nanocomposite is safe for use, where the IC50 was 161.6 µg/mL. Anti-cancer activity against urethral bladder cancer cell lines was recorded in vitro, where the IC50 was 107.4 µg/mL.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
licenseTermsHow to Cite
Publication Dates
References
Spirescu, V.A.; Șuhan, R.; Niculescu, A.-G.; Grumezescu, V.; Negut, I.; Holban, A.M.; Oprea, O.-C.; Bîrcă, A.C.; Vasile, B. Ștefan; Grumezescu, A.M. Biofilm-Resistant Nanocoatings Based on ZnO Nanoparticles and Linalool. Nanomaterials (Basel) 2021, 11, 2564. https://doi.org/10.3390/nano11102564.
Balaure, P.C.; Grumezescu, A.M. Recent Advances in Surface Nanoengineering for Biofilm Prevention and Control. Part II: Active, Combined Active and Passive, and Smart Bacteria-Responsive Antibiofilm Nanocoatings. Nanomaterials (Basel) 2020, 10, 1527, doi:10.339/nano10081527.
Kazemzadeh-Narbat, M.; Cheng, H.; Chabok, R.; Alvarez, M.M.; de la Fuente-Nunez, C.; Phillips, K.S.; Khademhosseini, A. Strategies for Antimicrobial Peptide Coatings on Medical Devices: A Review and Regulatory Science Perspective. Crit. Rev. Biotechnol. 2021, 41, 94–120, doi:10.1080/07388551/2020.1828810.
Alwash, A. The Green Synthesize of Zinc Oxide Catalyst Using Pomegranate Peels Extract for the Photocatalytic Degradation of Methylene Blue Dye. Baghdad Sci. J. 2020, 17, 0787, doi:10.21123/bsj.2020.17.3.0787.
Mohammed, L.S.; Ahmed, M.E. Effects of ZnO NPS on Streptococcus pyogenes in Vivo. Annals of Tropical Medicine and Public Health 2020, 23, 214–223, DOI:10.36295/ASRO.2020.23228.
Jiang, Q.; Chen, J.; Yang, C.; Yin, Y.; Yao, K. Quorum Sensing: A Prospective Therapeutic Target for Bacterial Diseases. Biomed Res. Int. 2019, 2019, 2015978, doi: 10.1155/2019/2015978.
Khalil, A.T.; Ovais, M.; Iqbal, J.; Ali, A.; Ayaz, M.; Abbas, M.; Ahmad, I.; Devkota, H.P. Microbes-Mediated Synthesis Strategies of Metal Nanoparticles and Their Potential Role in Cancer Therapeutics. Semin. Cancer Biol. 2022, 86, 693–705. DOI: 10.1016/j.semcancer.2021.06.006.
Noor, S.; Shah, Z.; Javed, A.; Ali, A.; Hussain, S.B.; Zafar, S.; Ali, H.; Muhammad, S.A. A Fungal Based Synthesis Method for Copper Nanoparticles with the Determination of Anticancer, Antidiabetic and Antibacterial Activities. J. Microbiol. Methods 2020, 174, 105966. DOI: 10.1016/j.mimet.2020.105966.
Ali, M.A.; Ahmed, T.; Wu, W.; Hossain, A.; Hafeez, R.; Islam Masum, M.M.; Wang, Y.; An, Q.; Sun, G.; Li, B. Advancements in Plant and Microbe-Based Synthesis of Metallic Nanoparticles and Their Antimicrobial Activity against Plant Pathogens. Nanomaterials (Basel) 2020, 10, 1146. DOI: 10.3390/nano10061146.
Gajdács, M.; Urbán, E. Comparative Epidemiology and Resistance Trends of Proteae in Urinary Tract Infections of Inpatients and Outpatients: A 10-Year Retrospective Study. Antibiotics (Basel) 2019, 8, 91. DOI: 10.3390/antibiotics8030091.
Jaffar, N.; Miyazaki, T.; Maeda, T. Biofilm Formation of Periodontal Pathogens on Hydroxyapatite Surfaces: Implications for Periodontium Damage: Biofilm Formation of Periodontal Pathogens on Hydroxyapatite Surfaces. J. Biomed. Mater. Res. A 2016, 104, 2873–2880. DOI: 10.1002/jbm.a.35827.
Punniyakotti, P.; Panneerselvam, P.; Perumal, D.; Aruliah, R.; Angaiah, S. Anti-Bacterial and Anti-Biofilm Properties of Green Synthesized Copper Nanoparticles from Cardiospermum Halicacabum Leaf Extract. Bioprocess Biosyst. Eng. 2020, 43, 1649–1657.DOI: 10.1007/s00449-020-02357-x.
Turakhia, B.; Divakara, M.B.; Santosh, M.S.; Shah, S. Green Synthesis of Copper Oxide Nanoparticles: A Promising Approach in the Development of Antibacterial Textiles. J Coat Technol Res 2020, 17, 531–540, https://doi.org/10.1007/s11998-019-00303-5.
Al-Assaf, A.I.S.; Ali, H.M.; Ad’hiah, A.H. Gene Expression of NLRP3 Inflammasome in Celiac Disease of Iraqi Children. Ibn AL- Haitham J. Pure Appl. Sci. 2021, 2021, 15–22, https://doi.org/10.30526/2021.IHICPAS.2645.
Emad, M.; Salama, K. A Comparison of the Effects of Lemon Peel -Silver Nanoparticles versus Brand Toothpastes and Mouthwashes on Staphylococcus Spp. Isolated from Teeth Caries. Iraqi J. Sci. 2020, 1894–1901. DOI: https://doi.org/10.24996/ijs.2020.61.8.6.
Kouhkan, M.; Ahangar, P.; Babaganjeh, L.A.; Allahyari-Devin, M. Biosynthesis of Copper Oxide Nanoparticles Using Lactobacillus Casei Subsp. Casei and Its Anticancer and Antibacterial Activities. Curr. Nanosci. 2020, 16, 101–111, DOI: 10.2174/1573413715666190318155801.
Janani, B.; Syed, A.; Raju, L.L.; Al-Harthi, H.F.; Thomas, A.M.; Das, A.; Khan, S.S. Synthesis of Carbon Stabilized Zinc Oxide Nanoparticles and Evaluation of Its Photocatalytic, Antibacterial and Anti-Biofilm Activities. J. Inorg. Organomet. Polym. Mater. 2020, 30, 2279–2288. https://doi.org/10.1007/s10904-019-01404-9.
Al-Jubouri, A.K.; Al-Saadi, N.H.; Kadhim, M.A. Anti-Inflammatory and Anti- Bacterial Activity of Copper Nanoparticles Synthesized from Myrtus communis Leaves Extract. Iraqi J. Agric. Sci. 2022, 53, 698–711, https://doi.org/10.36103/ijas.v53i3.1580.
Kang, Q.; Wang, X.; Zhao, J.; Liu, Z.; Ji, F.; Chang, H.; Yang, J.; Hu, S.; Jia, T.; Wang, X. Multidrug-Resistant Proteus Mirabilis Isolates Carrying Bla OXA-1 and Bla NDM-1 from Wildlife in China: Increasing Public Health Risk. Integr. Zool 2021, 16, 798–809. DOI: 10.1111/1749-4877.12510.
Khan, M.F.; Husain, F.M.; Zia, Q.; Ahmad, E.; Jamal, A.; Alaidarous, M.; Banawas, S.; Alam, M.M.; Alshehri, B.A.; Jameel, M. Anti-Quorum Sensing and Anti-Biofilm Activity of Zinc Oxide Nanospikes. ACS Omega 2020, 5, 32203–32215, doi: 10.1021/acsomega.0c03634.
Siddiqi, K.S.; ur Rahman, A.; Tajuddin; Husen, A. Properties of Zinc Oxide Nanoparticles and Their Activity against Microbes. Nanoscale Res. Lett. 2018, 13, 141. https://doi.org/10.1186/s11671-018-2532-3.
Hasson, S.O.; Salman, S.A.K.; Hassan, S.F.; Abbas, S.M. Antimicrobial Effect of Eco- Friendly Silver Nanoparticles Synthesis by Iraqi Date Palm (Phoenix dactylifera) on Gram-Negative Biofilm-Forming Bacteria. Baghdad Sci. J. 2021, 18, 1149, DOI: https://doi.org/10.21123/bsj.2021.18.4.1149.
Ahmed, M.E.; Al-Shimmary, S.M. Comparative Study between Pure Bacterocin and Vancomycin on Biofilms of MRSA Isolated from Medical Implants. Journal of Pharmaceutical Sciences and Research, 2018, 10, 1476–1480.
Bondarenko, O.M.; Sihtmäe, M.; Kuzmičiova, J.; Ragelienė, L.; Kahru, A.; Daugelavičius, R. Plasma Membrane Is the Target of Rapid Antibacterial Action of Silver Nanoparticles in Escherichia coli and Pseudomonas aeruginosa. Int. J. Nanomedicine, 2018, 13, 6779–6790. DOI: 10.2147/IJN.S177163.
Hussein, E.I.; Al-Batayneh, K.; Masadeh, M.M.; Dahadhah, F.W.; Al Zoubi, M.S.; Aljabali, A.A.; Alzoubi, K.H. Assessment of Pathogenic Potential, Virulent Genes Profile, and Antibiotic Susceptibility of Proteus mirabilis from Urinary Tract Infection. Int. J. Microbiol. 2020, 2020, 1231807. https://doi.org/10.1155/2020/1231807.
Rajalakshmi, R.; Sangeetha, D.; Udhaya, V. Effect of Antifungal Drugs against Candida Isolates from Diabetic Women with Vaginitis. J. Infect. Dis. Ther 2017; 5, 331. doi: 10.4172/2332-0877.1000331.
Mishu, J.; Sm, N.; Hm, S.; Nabonee, K.; Zannat Dola, M.A.; Haque, N. Association between Biofilm Formation and Virulence Genes Expression and Antibiotic Resistance Pattern in Proteus Mirabilis, Isolated from Patients of Dhaka Medical College Hospital. Arch. Clin. Biomed. Res. 2022; 6, 3, 418-434. DOI: 10.26502/acbr.50170257.
Badawy, M.S.E.M.; Riad, O.K.M.; Taher, F.A.; Zaki, S.A. Chitosan and Chitosan-Zinc Oxide Nanocomposite Inhibit Expression of LasI and RhlI Genes and Quorum Sensing Dependent Virulence Factors of Pseudomonas aeruginosa. Int. J. Biol. Macromol. 2020, 149, 1109–1117, DOI: 10.1016/j.ijbiomac.2020.02.019.
Abdul-Hamza, H.K.; Mohammed, G.J. Anti-Quorum Sensing Effect of Streptococcus Agalatiaceae by Zinc Oxide, Copper Oxide, and Titanium Oxide Nanoparticles. J. Phys. Conf. Ser. 2021, 1999, 012031, https://iopscience.iop.org/article/10.1088/1742-6596/1999/1/012031.
Cai, X.; Liu, X.; Jiang, J.; Gao, M.; Wang, W.; Zheng, H.; Xu, S.; Li, R. Molecular Mechanisms, Characterization Methods, and Utilities of Nanoparticle Biotransformation in Nanosafety Assessments. Small, 2020; 16, e1907663, https://doi.org/10.1002/smll.201907663.
Ram, V.P.; Rao, L.V.; Rao, T.S.; Subramanyam, K.V.; Suresh, Y.; Srinivas, K. A Study on Antibiogram and Beta-Lactam Resistance of Proteus Mirabilis Isolated from Animals and Humans in Andhra Pradesh, India. Indian J. Anim. Res. 2021, doi: 10.18805/IJAR.B-4184.
Alavi, M.; Li, L.; Nokhodchi, A. Metal, Metal Oxide and Polymeric Nanoformulations for the Inhibition of Bacterial Quorum Sensing. Drug Discov. Today 2023, 28, 103392. DOI: 10.1016/j.drudis.2022.103392.
Yao, Y.; Zhou, Y.; Liu, L.; Xu, Y.; Chen, Q.; Wang, Y.; Wu, S.; Deng, Y.; Zhang, J.; Shao, A. Nanoparticle-Based Drug Delivery in Cancer Therapy and Its Role in Overcoming Drug Resistance. Front. Mol. Biosci. 2020, 7, DOI: 10.3389/fmolb.2020.00193.
Reddy, K.M.; Feris, K.; Bell, J.; Wingett, D.G.; Hanley, C.; Punnoose, A. Selective Toxicity of Zinc Oxide Nanoparticles to Prokaryotic and Eukaryotic Systems. Appl. Phys. Lett. 2007, 90, 2139021–2139023. doi: 10.1063/1.2742324.
Kang, Q.; Wang, X.; Zhao, J.; Liu, Z.; Ji, F.; Chang, H.; Yang, J.; Hu, S.; Jia, T.; Wang, X. Multidrug-Resistant Proteus Mirabilis Isolates Carrying blaOXA-1 and blaNDM-1 from Wildlife in China: Increasing Public Health Risk. Integr. Zool. 2021, 16, 798–809. DOI: 10.1111/1749-4877.12510.
Ameh, T.; Sayes, C.M. The Potential Exposure and Hazards of Copper Nanoparticles: A Review. Environ. Toxicol. Pharmacol. 2019, 71, 103220. DOI: 10.1016/j.etap.2019.103220.
Abbasi, A.; Ghorban, K.; Nojoomi, F.; Dadmanesh, M. Smaller Copper Oxide Nanoparticles Have More Biological Effects versus Breast Cancer and Nosocomial Infections Bacteria. Asian Pac. J. Cancer Prev, 2021, 22, 893–902. DOI: 10.31557/APJCP.2021.22.3.893.
Haupenthal, D.P.D.S.; Possato, J.C.; Zaccaron, R.P.; Mendes, C.; Rodrigues, M.S.; Nesi, R.T.; Pinho, R.A.; Feuser, P.E.; Machado-de-Ávila, R.A.; Comim, C.M. Effects of Chronic Treatment with Gold Nanoparticles on Inflammatory Responses and Oxidative Stress in Mdx Mice. J. Drug Target. 2020, 28, 46–54. DOI: 10.1080/1061186X.2019.1613408.
Ali, K.H.; Ibraheem, S.A.; Jabir, M.S.; Ali, K.A.; Taqi, Z.J.; Dan, F.D. Zinc Oxide Nanoparticles Induces Apoptosis in Human Breast Cancer Cells via Caspase-8 and P53 Pathway. Nano Biomed. Eng. 2019, 11, 35-43. https://doi.org/10.5101/nbe.v11i1.p35-43.
Rashid, A.E.; Ahmed, M.E.; Hamid, M.K. Evaluation of Antibacterial and Cytotoxicity Properties of Zinc Oxide Nanoparticles Synthesized by Precipitation Method against Methicillin-Resistant Staphylococcus aureus. Int. J. Drug Deliv. Technol. 2022, 12, 985–989. DOI:10.25258/ijddt.12.3.11.
Hassan, Z.J.S.; Hamid, M.K.; Ahmed, M.E. Synthesized Zinc Oxide Nanoparticles by the Precipitation Method on Streptococcus spp. from Dental Carries and Cytotoxicity Assay. Int. J. Drug Deliv. Technol. 2022, 12, 1327–1330. DOI: 10.25258/ijddt.12.3.65.
Mani, V.M.; Kalaivani, S.; Sabarathinam, S.; Vasuki, M.; Soundari, A.J.P.G.; Ayyappa Das, M.P.; Elfasakhany, A.; Pugazhendhi, A. Copper Oxide Nanoparticles Synthesized from an Endophytic Fungus Aspergillus terreus: Bioactivity and Anti-Cancer Evaluations. Environ. Res. 2021, 201, 111502. DOI: 10.1016/j.envres.2021.111502.