Zinc oxide nanoparticles inhibit bacterial biofilm formation via altering cell membrane permeability

References

• Cortes, M. E.; Jessika, C. B.; Ruben, D. S. Biofilm Formation, Control and Novel Strategies for Eradication. In Science against microbial pathogens: communicating current research and technological advances. Méndez-Vilas, A., Ed.; Formatex Research Center: Badajoz, Spain, 2011; pp. 896–905.
   Google Scholar
• Srey, S.; Jahid, I. K.; Ha, S. D. Biofilm Formation in Food Industries: A Food Safety Concern. Food Control. 2013, 31, 572–585.
   Web of Science ®Google Scholar
• Qian, P. Y.; Lau, S. C.; Dahms, H. U.; Dobretsov, S.; Harder, T. Marine Biofilms as Mediators of Colonization by Marine Macroorganisms: Implications for Antifouling and Aquaculture. Mar. Biotechnol. 2007, 9, 399–410.
   PubMed Web of Science ®Google Scholar
• Bryers, J. D. Medical Biofilms. Biotechnol. Bioeng. 2008, 100, 1–18.
   PubMed Web of Science ®Google Scholar
• Bjarnsholt, T.; Ciofu, O.; Molin, S.; Givskov, M.; Hoiby, N. Applying Insights from Biofilm Biology to Drug Development—Can a New Approach Be Developed? Nat. Rev. Drug Discov. 2013, 12, 791–808.
   PubMed Web of Science ®Google Scholar
• Raihana, A. K. M. P.; Ranjitha, K.; Rishad, P.; Sabeela, P. P.; Prasobh, G. R.; Shrikumar, S. Importance of Nanotechnology in Pharmaceutical Formulations-A Review. IJRDO J. Health Sci. Nurs. 2017, 2, 1–13.
   Google Scholar
• Santhoshkumar, J.; Kumar, S. V.; Rajeshkumar, S. Synthesis of Zinc Oxide Nanoparticles Using Plant Leaf Extract against Urinary Tract Infection Pathogen. Resour. Effic. Technol. 2017, 3, 459–465.
   Google Scholar
• Agarwal, H.; Kumar, S. V.; Rajeshkumar, S. A Review on Green Synthesis of Zinc Oxide Nanoparticles–an Eco-Friendly Approach. Resour. Effic. Technol. 2017, 3, 406–413.
   Google Scholar
• Chandrasekaran, R.; Gnanasekar, S.; Seetharaman, P.; Keppanan, R.; Arockiaswamy, W.; Sivaperumal, S. Formulation of Carica Papaya Latex-Functionalized Silver Nanoparticles for Its Improved Antibacterial and Anticancer Applications. J. Mol. Liq. 2016, 219, 232–238.
   Web of Science ®Google Scholar
• Agarwal, A.; Mehra, A.; Karthik, L.; Kumar, G.; Rao, K. V. B. Antibiofouling Property of Marine Actinobacteria and Its Mediated Nanoparticle. IJNP. 2014, 7, 294–306.
   Google Scholar
• Kumar, D.; Karthik, L.; Kumar, G.; Rao, K. V. B. Biosynthesis of Silver Nanoparticles from Marine Yeast and Their Antimicrobial Activity against Multidrug Resistant Pathogens. Pharmacologyonline. 2011, 3, 1100–1111.
   Google Scholar
• Naveen, K. S. H.; Kumar, G.; Karthik, L.; Rao, K. V. B. Extracellular Biosynthesis of Silver Nanoparticles Using the Filamentous Fungus Penicillium sp. Arch. Appl. Sci. Res. 2010, 2, 161–167.
   Google Scholar
• Ravichandran, S.; Paluri, V.; Kumar, G.; Loganathan, K.; Rao, K. V. B. A Novel Approach for the Biosynthesis of Silver Oxide Nanoparticles Using Aqueous Leaf Extract of Callistemon Lanceolatus (Myrtaceae) and Their Therapeutic Potential. J. Exp. Nanosci. 2016, 11, 445–458.
   Web of Science ®Google Scholar
• Sanaeimehr, Z.; Javadi, I.; Namvar, F. Antiangiogenic and Antiapoptotic Effects of Green-Synthesized Zinc Oxide Nanoparticles Using Sargassum Muticum Algae Extraction. Cancer Nanotechnol. 2018, 9, 3.
   PubMed Web of Science ®Google Scholar
• Yusof, H. M.; Mohamad, R.; Zaidan, U. H.; Rahman, N. A. A. Microbial Synthesis of Zinc Oxide Nanoparticles and Their Potential Application as an Antimicrobial Agent and a Feed Supplement in Animal Industry: A Review. J. Anim. Sci. Biotechnol. 2019, 10, 57.
   PubMed Web of Science ®Google Scholar
• Bhowmik, D.; Bhattacharjee, C.; Kumar, K. P. S. A Potential Medicinal Importance of Zinc in Human Health and Chronic Disease. Int. J. Pharm. Biomed. Sci. 2010, 1, 5–11.
   Google Scholar
• Swain, P. S.; Rao, S. B. N.; Rajendran, D.; Dominic, G.; Selvaraju, S. Nano Zinc, an Alternative to Conventional Zinc as Animal Feed Supplement: A Review. Anim. Nutr. 2016, 2, 134–141.
   PubMedGoogle Scholar
• Uikey, P.; Vishwakarma, K. Review of Zinc Oxide (ZnO) Nanoparticles Applications and Properties. Int. J. Emerg. Technol. Comput. Sci. Elect. 2016, 21, 239–242.
   Google Scholar
• Ozgur, U.; Hofstetter, D.; Morkoc, H. ZnO Devices and Applications: A Review of Current Status and Future Prospects. Proc. IEEE. 2010, 98, 1255–1268.
   Web of Science ®Google Scholar
• FDA (Food and Drug Administration). Select Committee on GRAS Substances (SCOGS) Opinion: Zinc Salts. Washington DC, USA, 2015. Available at: http://www.fda.gov/Food/IngredientsPackagingLabeling/GRAS/SCOGS/ucm261041.html.
   Google Scholar
• Pulit-Prociak, J.; Chwastowski, J.; Kucharski, A.; Banach, M. Applied Surface Science Functionalization of Textiles with Silver and Zinc Oxide Nanoparticles. Appl. Surf. Sci. 2016, 385, 543–553.
   Web of Science ®Google Scholar
• Kasraei, S.; Sami, L.; Hendi, S.; Alikhani, M. Y.; Rezaei-Soufi, L.; Khamverdi, Z. Antibacterial Properties of Composite Resins Incorporating Silver and Zinc Oxide Nanoparticles on Streptococcus mutans and Lactobacillus. Restor. Dent. Endod. 2014, 39, 109–114.
   PubMedGoogle Scholar
• Siddique, S.; Shah, Z. H.; Shahid, S.; Yasmin, F. Preparation, Characterization and Antibacterial Activity of ZnO Nanoparticles on Broad Spectrum of Microorganisms. Acta Chim. Slov. 2013, 60, 660–665.
   PubMed Web of Science ®Google Scholar
• Swain, P.; Nayak, S. K.; Sasmal, A.; Behera, T.; Barik, S. K.; Swain, S. K.; Mishra, S. S.; Sen, A. K.; Das, J. K.; Jayasankar, P. Antimicrobial Activity of Metal Based Nanoparticles against Microbes Associated with Diseases in Aquaculture. World J. Microbiol. Biotechnol. 2014, 30, 2491–2502.
   PubMed Web of Science ®Google Scholar
• Al-Fori, M.; Dobretsov, S.; Myint, M. T. Z.; Dutta, J. Antifouling Properties of Zinc Oxide Nanorod Coatings. Biofouling. 2014, 30, 871–882.
   PubMed Web of Science ®Google Scholar
• Hussain, A.; Oves, M.; Alajmi, M. F.; Hussain, I.; Amir, S.; Ahmed, J.; Rehman, M. T.; El-Seedi, H. R.; Ali, I. Biogenesis of ZnO Nanoparticles Using Pandanus Odorifer Leaf Extract: Anticancer and Antimicrobial Activities. RSC Adv. 2019, 9, 15357–15369.
   PubMed Web of Science ®Google Scholar
• Khan, S. T.; Ahamed, M.; Musarrat, J.; Al-Khedhairy, A. A. Anti-Biofilm and Antibacterial Activities of Zinc Oxide Nanoparticles against the Oral Opportunistic Pathogens Rothia dentocariosa and Rothia mucilaginosa. Eur. J. Oral Sci. 2014, 122, 397–403.
   PubMed Web of Science ®Google Scholar
• Lee, J. H.; Kim, Y. G.; Cho, M. H.; Lee, J. ZnO Nanoparticles Inhibit Pseudomonas aeruginosa Biofilm Formation and Virulence Factor Production. Microbiol. Res. 2014, 169, 888–896.
   PubMed Web of Science ®Google Scholar
• Dasaroju, S.; Gottumukkala, K. M. Current Trends in the Research of Emblica Officinalis (Amla): A Pharmacological Perspective. Int. J. Pharm. Sci. Rev. Res. 2014, 24, 150–159.
   Google Scholar
• Lanka, S. A Review on Pharmacological, Medicinal and Ethnobotanical Important Plant: Phyllanthus Emblica Linn. (Syn. Emblica Officinalis). World J. Pharm. Res. 2018, 7, 380–396.
   Google Scholar
• Senthilkumar, S. R.; Thirumal, S. Green Tea (Camellia Sinensis) Mediated Synthesis of Zinc Oxide (ZnO) Nanoparticles and Studies on Their Antimicrobial Activities. Int. J. Pharm. Pharm. Sci. 2014, 6, 461–465.
   Google Scholar
• CLSI, Performance Standards for Antimicrobial Susceptibility Testing, 30th Edition. Available at: https://clsi.org/standards/products/microbiology/documents/m100/.
   Google Scholar
• Tagg, J. R.; Dajani, A. S.; Wannamaker, L. W. Bacteriocins of Gram-Positive Bacteria. Bacteriol. Rev. 1976, 40, 722–756.
   PubMedGoogle Scholar
• Kumar, G.; Karthik, L.; Rao, K. V. B. Antibacterial Activity of Aqueous Extract of Calotropis Gigantea Leaves–an in Vitro Study. Int. J. Pharm. Sci. Rev. Res. 2010, 4, 141–144.
   Google Scholar
• Okunji, C. O.; Okeke, C. N.; Gugnani, H. C.; Iwu, M. M. An Antifungal Spirostanol Saponin from Fruit Pulp of Dracaena Mannii. Int. J. Crude Drug Res. 1990, 28, 193–199.
   Google Scholar
• Hsueh, Y.-H.; Lin, K.-S.; Ke, W.-J.; Hsieh, C.-T.; Chiang, C.-L.; Tzou, D.-Y.; Liu, S.-T. The Antimicrobial Properties of Silver Nanoparticles in Bacillus subtilis Are Mediated by Released Ag+ Ions. PLOS One. 2015, 10, e0144306.
   PubMed Web of Science ®Google Scholar
• Garg, G.; Sharma, S.; Dua, A.; Mahajan, R. Antibacterial Potential of Polyphenol Rich Methanol Extract of Cardamom (Amomum Subulatum). J. Innovat. Bio. 2016, 3, 271–275.
   Google Scholar
• Patil, R. C.; Talekar, D. A. Method of Precipitation of ZnO Nanoparticles by Co-Precipitation Method Using Black Tiger Prawns (Panaeus monodon) Extract. Indian Patent Pending No. 2422/MUM/2013, 2013.
   Google Scholar
• Ramesh, P.; Rajendran, A.; Meenakshisundaram, M. Green Synthesis of Zinc Oxide Nanoparticles Using Flower Extract Cassia Auriculata. J. Nanosci. Nanotechnol. 2014, 2, 41–45.
   Google Scholar
• Singh, R. P.; Shukla, V. K.; Yadav, R. S.; Sharma, P. K.; Singh, P. K.; Pandey, A. C. Biological Approach of Zinc Oxide Nanoparticles Formation and Its Characterization. AML. 2011, 2, 313–317.
   Google Scholar
• Zhang, D. H.; Xue, Z. Y.; Wang, Q. P. The Blue Photoluminescence Emitted from ZnO Films Deposited on Glass Substrate by RF Magnetron Sputtering. J. Phys. D: Appl. Phys. 2002, 35, 2837–2840.
   Web of Science ®Google Scholar
• Djaja, N. F.; Montja, D. A.; Saleh, R. The Effect of Co Incorporation into ZnO Nanoparticles. AMPC. 2013, 03, 33–41.
   Google Scholar
• Bindu, P.; Thomas, S. Estimation of Lattice Strain in ZnO Nanoparticles: X-Ray Peak Profile Analysis. J. Theor. Appl. Phys. 2014, 8, 123–134.
   Google Scholar
• Al Abdullah, K.; Awad, S.; Zaraket, J.; Salame, C. Synthesis of ZnO Nanopowders by Using Sol-Gel and Studying Their Structural and Electrical Properties at Different Temperature. Energy Procedia. 2017, 119, 557–565.
   Google Scholar
• Muhammad, W.; Naimat Ullah, S.; Haroon, M.; Abbasi, B. H. Optical, Morphological and Biological Analysis of Zinc Oxide Nanoparticles (ZnO NPs) Using Papaver Somniferum L. RSC Adv. 2019, 9, 29541–29548.
   PubMed Web of Science ®Google Scholar
• Devi, R. S.; Gayathri, R. Green Synthesis of Zinc Oxide Nanoparticles by Using Hibiscus Rosa-Sinensis. Int. J. Curr. Eng. Technol. 2014, 4, 2444–2446.
   Google Scholar
• Gnanasangeetha, D.; Thambavani, D. S. One Pot Synthesis of Zinc Oxide Nanoparticles via Chemical and Green Method. Res. J. Mater. Sci. 2013, 1, 1–8.
   Google Scholar
• Hiremath, S.; Chandraprabha, M. N.; Antonyraj, M. A. L.; Gopal, I. V.; Jain, A.; Bansal, K. Green Synthesis of ZnO Nanoparticles by Calotropis Gigantea. International Journal of Current Engineering and Technology 2013, 1, 118–120.
   Google Scholar
• Franklin, N. M.; Rogers, N. J.; Apte, S. C.; Batley, G. E.; Gadd, G. E.; Casey, P. S. Comparative Toxicity of Nanoparticulate ZnO, Bulk ZnO, and ZnCl2 to a Freshwater Microalga (Pseudokirchneriella subcapitata): the Importance of Particle Solubility. Environ. Sci. Technol. 2007, 41, 8484–8490.
   PubMed Web of Science ®Google Scholar
• Xia, W. J.; Onyuksel, H. Mechanistic Studies on Surfactant Induced Membrane Permeability Enhancement. Pharm. Res 2000, 17, 612–618.
   PubMed Web of Science ®Google Scholar
• Sayed, S. R. M.; Bahkali, A. H.; Bakri, M. M.; Hirad, A. H.; Elgorban, A. M.; El-Metwally, M. A. Antibacterial Activity of Biogenic Silver Nanoparticles Produced by Aspergillus terreus. Int. J. Pharmacol. 2015, 11, 858–863.
   Web of Science ®Google Scholar
• Wu, Y.; Yang, Y.; Zhang, Z.; Wang, Z.; Zhao, Y.; Sun, L. A Facile Method to Prepare Size-Tunable Silver Nanoparticles and Its Antibacterial Mechanism. Adv. Powder Technol. 2018, 29, 407–415.
   Web of Science ®Google Scholar
• Ni, Z.; Gu, X.; He, Y.; Wang, Z.; Zou, X.; Zhao, Y.; Sun, L. Synthesis of Silver Nanoparticle-Decorated Hydroxyapatite (HA@Ag) Poriferous Nanocomposites and the Study of Their Antibacterial Activities. RSC Adv. 2018, 8, 41722–41730.
   PubMed Web of Science ®Google Scholar
• Senthilkumar, S.; Kashinath, L.; Ashok, M.; Rajendran, A. Antibacterial Properties and Mechanism of Gold Nanoparticles Obtained from Pergularia Daemia Leaf Extract. JNMR. 2017, 6, 5.
   Google Scholar
• Dobrucka, R.; Długaszewska, J. Biosynthesis and Antibacterial Activity of ZnO Nanoparticles Using Trifolium pratense Flower Extract. Saudi J. Biol. Sci. 2016, 23, 517–523.
   PubMed Web of Science ®Google Scholar
• Anbukkarasi, V.; Srinivasan, R.; Elangovan, N. Antimicrobial Activity of Green Synthesized Zinc Oxide Nanoparticles from Emblica Officinalis. Int. J. Pharm. Sci. Rev. Res 2015, 33, 110–115.
   Web of Science ®Google Scholar
• Joel, C.; Badhusha, M. S. M. Green Synthesis of ZnO Nanoparticles Using Phyllanthus Embilica Stem Extract and Their Antibacterial Activity. Der. Pharmacia. Lettre. 2016, 8, 218–223.
   Google Scholar
• Pinto, G. M.; Nazareth, R. Green Synthesis and Characterization of Zinc Oxide Nanoparticles. J. Chem. Pharm. Res. 2016, 8, 427–432.
   Google Scholar
• Rangeela, M.; Rajeshkumar, S.; Lakshmi, T.; Roy, A. Anti-Inflammatory Activity of Zinc Oxide Nanoparticles Prepared Using Amla Fruits. Drug Invent. Today. 2019, 11, 2358–2361.
   Google Scholar
• Srinisha, M.; Rajeshkumar, S.; Lakshmi, T.; Roy, A. Antibacterial Activity of Zinc Oxide Nanoparticles Synthesized Using Amla Fruit against Oral Pathogens. Drug Invent. Today. 2019, 11, 1995–1997.
   Google Scholar
• Tasneem, U.; Yasin, N.; Nisa, I.; Shah, F.; Rasheed, U.; Momin, F.; Zaman, S.; Qasim, M. Biofilm Producing Bacteria: A Serious Threat to Public Health in Developing Countries. Food-Science. 2018, 01, 25–31.
   Google Scholar
• Mu, H.; Tang, J.; Liu, Q.; Sun, C.; Wang, T.; Duan, J. Potent Antibacterial Nanoparticles against Biofilm and Intracellular Bacteria. J. Sci. Rep. 2016, 6, 18877.
   PubMed Web of Science ®Google Scholar
• Rajput, N. S.; Bankar, A. Bio-Inspired Gold Nanoparticles Synthesis and Their Anti-Biofilm Efficacy. J. Pharm. Investig. 2017, 47, 521–530.
   Google Scholar
• Namasivayam, S. K. R.; Christo, B. B.; Arasu, S. M. K.; Kumar, K. A. M.; Deepak, K. Anti Biofilm Effect of Biogenic Silver Nanoparticles Coated Medical Devices against Biofilm of Clinical Isolate of Staphylococcus aureus. Global J. Med. Res, Pharma. Drug Discov. Toxicol. Med. 2013, 13, 25–30.
   Google Scholar
• Bhattacharyya, P.; Agarwal, B.; Goswami, M.; Maiti, D.; Baruah, S.; Tribedi, P. Zinc Oxide Nanoparticle Inhibits the Biofilm Formation of Streptococcus pneumoniae. Antonie Van Leeuwenhoek. 2018, 111, 89–99.
   PubMed Web of Science ®Google Scholar
• Sangani, M. H.; Moghaddam, M. N.; Forghanifard, M. M. Inhibitory Effect of Zinc Oxide Nanoparticles on Pseudomonas aeruginosa Biofilm Formation. Nanomed. J. 2015, 2, 121–128.
   Google Scholar
• Chaudhari, P. R.; Masurkar, S. A.; Shidore, V. B.; Kamble, S. P. Effect of Biosynthesized Silver Nanoparticles on Staphylococcus aureus Biofilm Quenching and Prevention of Biofilm Formation. Nano-Micro Lett. 2012, 4, 34–39.
   Web of Science ®Google Scholar
• Li, X.; Robinson, S. M.; Gupta, A.; Saha, K.; Jiang, Z.; Moyano, D. F.; Sahar, A.; Riley, M. A.; Rotello, V. M. Functional Gold Nanoparticles as Potent Antimicrobial Agents against Multi-Drug-Resistant Bacteria. ACS Nano. 2014, 8, 10682–10686.
   PubMed Web of Science ®Google Scholar
• Sadiq, I. M.; Chandrasekaran, N.; Mukherjee, A.; Studies on Effect of TiO2 Nanoparticles on Growth and Membrane Permeability of Escherichia coli, Pseudomonas aeruginosa, and Bacillus subtilis. Cnano. 2010, 6, 381–387.
   Google Scholar