Rutin-coated zinc oxide nanoparticles: a promising antivirulence formulation against pathogenic bacteria.

Fatemeh Azizi Alidoust, Behnam Rasti, Hojjatolah Zamani, Mirsasan Mirpour, Amir Mirzaie
Author Information
  1. Fatemeh Azizi Alidoust: Department of Microbiology, Faculty of Basic Sciences, Lahijan Branch, Islamic Azad University (IAU), Lahijan, Guilan, Iran.
  2. Behnam Rasti: Department of Microbiology, Faculty of Basic Sciences, Lahijan Branch, Islamic Azad University (IAU), Lahijan, Guilan, Iran. behnam.rasti@iau.ac.ir.
  3. Hojjatolah Zamani: Department of Biology, University of Guilan, Rasht, Iran. h_zamani@guilan.ac.ir.
  4. Mirsasan Mirpour: Department of Microbiology, Faculty of Basic Sciences, Lahijan Branch, Islamic Azad University (IAU), Lahijan, Guilan, Iran.
  5. Amir Mirzaie: Department of Biology, Parand Branch, Islamic Azad University, Parand, Iran.

Abstract

The use of engineered nanoparticles against pathogenic bacteria has gained attention. In this study, zinc oxide nanoparticles conjugated with rutin were synthesized and their antivirulence properties against Pseudomonas aeruginosa and Staphylococcus aureus. The physicochemical characteristics of ZnO-Rutin NPs were investigated using SEM, FT-IR, XRD, DLS, EDS, and zeta potential analyses. Antimicrobial properties were evaluated by well diffusion, microdilution, growth curve, and hemolytic activity assays. The expression of quorum sensing (QS) genes including the lasI and rhlI in P. aeruginosa and agrA in S. aureus was assessed using real-time PCR. Swimming, swarming, twitching, and pyocyanin production by P. aeruginosa were evaluated. The NPs were amorphous, 14-100 nm in diameter, surface charge of -34.3 mV, and an average hydrodynamic size of 161.7 nm. Regarding the antibacterial activity, ZnO-Rutin NPs were more potent than ZnO NPs and rutin, and stronger inhibitory effects were observed on S. aureus than on P. aeruginosa. ZnO-Rutin NPs inhibited the hemolytic activity of P. aeruginosa and S. aureus by 93.4 and 92.2%, respectively, which was more efficient than bare ZnO NPs and rutin. ZnO-Rutin NPs reduced the expression of the lasI and rhlI in P. aeruginosa by 0.17-0.43 and 0.37-0.70 folds, respectively while the expression of the agrA gene in S. aureus was decreased by 0.46-0.56 folds. Furthermore, ZnO-Rutin NPs significantly reduced the swimming and twitching motility and pyocyanin production of P. aeruginosa. This study demonstrates the antivirulence features of ZnO-Rutin NPs against pathogenic bacteria which can be associated with their QS inhibitory effects.

Keywords

References

  1. Abbasi M, Gholizadeh R, Kasaee SR, Vaez A, Chelliapan S, Fadhil Al-Qaim F, Kamyab H et al (2023) An intriguing approach toward antibacterial activity of green synthesized rutin-templatedmesoporous silica nanoparticles decorated with nanosilver. Sci Rep 13(1):5987. https://doi.org/10.1038/s41598-023-33095-1 [DOI: 10.1038/s41598-023-33095-1]
  2. Abbas HA, Shaker GH, Mosallam FM, Gomaa SE (2022) Novel silver metformin nano-structure to impede virulence of staphylococcus aureus. AMB Express 12(1):84. https://doi.org/10.1186/s13568-022-01426-6 [DOI: 10.1186/s13568-022-01426-6]
  3. Abdelghafar A, Yousef N, Askoura M (2022) Zinc oxide nanoparticles reduce biofilm formation, synergize antibiotics action and attenuate staphylococcus aureus virulence in host; an important message to clinicians. BMC Microbiol 22(1):1���17. https://doi.org/10.1186/s12866-022-02658-z [DOI: 10.1186/s12866-022-02658-z]
  4. Akbar N, Aslam Z, Siddiqui R, Shah MR, Khan NA (2021) Zinc oxide nanoparticles conjugated with clinically-approved medicines as potential antibacterial molecules. AMB Express 11:1���16. https://doi.org/10.1186/s13568-021-01261-1 [DOI: 10.1186/s13568-021-01261-1]
  5. Al-Shabib NA, Husain FM, Ahmad I, Khan MS, Khan RA, Khan JM (2017) Rutin inhibits mono and multi-species biofilm formation by foodborne drug resistant escherichia coli and staphylococcus aureus. Food Control 79:325���332. https://doi.org/10.1016/j.foodcont.2017.03.004 [DOI: 10.1016/j.foodcont.2017.03.004]
  6. Alvarez MDLA, Debattista NB, Pappano NB (2006) Synergism of flavonoids with bacteriostatic action gainst saphylococcus aureus ATCC 25 923 and Escherichia coli ATCC 25 922. Biocell 30(1):39���42 [DOI: 10.32604/biocell.2006.30.039]
  7. Amin MU, Khurram M, Khattak B, Khan J (2015) Antibiotic additive and synergistic action of rutin, morin and quercetin against methicillin resistant staphylococcus aureus. BMC Complement Altern Med 15:1���12. https://doi.org/10.1186/s12906-015-0580-0 [DOI: 10.1186/s12906-015-0580-0]
  8. Arima H, Ashida H, Danno GI (2002) Rutin-enhanced antibacterial activities of flavonoids against bacillus cereus and salmonella enteritidis. Biosci Biotechnol Biochem 66(5):1009���1014 [DOI: 10.1271/bbb.66.1009]
  9. Brandelli A, Ritter AC, Veras FF (2017) Antimicrobial activities of metal nanoparticles. In: Rai M, Shegokar R (eds) Metal nanoparticles in pharma. Springer, Cham, pp 337���363 [DOI: 10.1007/978-3-319-63790-7_15]
  10. Cheung GY, Bae JS, Otto M (2021) Pathogenicity and virulence of staphylococcus aureus. Virulence 12(1):547���569. https://doi.org/10.1080/21505594.2021.1878688 [DOI: 10.1080/21505594.2021.1878688]
  11. CLSI (2021) Performance standards for antimicrobial susceptibility testing; CLSI supplement M100, 31st edition. Clinical and Laboratory Standards Institute, Wayne
  12. Foster TJ (2017) Antibiotic resistance in staphylococcus aureus. Current status and future prospects. FEMS Microbiol Rev 41(3):430���449. https://doi.org/10.1093/femsre/fux007 [DOI: 10.1093/femsre/fux007]
  13. Garc��a-Lara B, Saucedo-Mora M��, Rold��n-S��nchez JA, P��rez-Eretza B, Ramasamy M, Lee J, Garc��a-Contreras R et al (2015) Inhibition of quorum-sensing-dependent virulence factors and biofilm formation of clinical and environmental pseudomonas aeruginosa strains by ZnO nanoparticles. Lett Appl Microbiol 61(3):299���305 [DOI: 10.1111/lam.12456]
  14. Geisinger E, Adhikari RP, Jin R, Ross HF, Novick RP (2006) Inhibition of rot translation by RNAIII, a key feature of agr function. Mol Microbiol 61(4):1038���1048 [DOI: 10.1111/j.1365-2958.2006.05292.x]
  15. Gomaa SE, Shaker GH, Mosallam FM, Abbas HA (2022) Knocking down pseudomonas aeruginosa virulence by oral hypoglycemic metformin nano emulsion. World J Microbiol Biotechnol 38(7):119. https://doi.org/10.1007/s11274-022-03302-8 [DOI: 10.1007/s11274-022-03302-8]
  16. Goorabjavari SVM, Golmohamadi F, Haririmonfared S, Ahmadi H, Golisani S, Yari H, Falahati M et al (2021) Thermodynamic and anticancer properties of inorganic zinc oxide nanoparticles synthesized through co-precipitation method. J Mol Liq 330:115602. https://doi.org/10.1016/j.molliq.2021.115602 [DOI: 10.1016/j.molliq.2021.115602]
  17. Gupta A, Landis RF, Rotello VM (2016) Nanoparticle-based antimicrobials: surface functionality is critical. F1000Rese. https://doi.org/10.12688/f1000research.7595.1 [DOI: 10.12688/f1000research.7595.1]
  18. Ha DG, Kuchma SL, O���Toole GA (2014a) Plate-based assay for swarming motility in Pseudomonas aeruginosa. In: Filloux A, Ramos JL (eds) Pseudomonas methods and protocols. Methods in molecular biology, vol 1149. Humana, New York, NY. https://doi.org/10.1007/978-1-4939-0473-0_8 [DOI: 10.1007/978-1-4939-0473-0_8]
  19. Ha DG, Kuchma SL, O���Toole GA (2014b) Plate-based assay for swimming motility in pseudomonas aeruginosa. In: Filloux A, Ramos JL (eds) Pseudomonas methods and protocols. methods in molecular biology, vol 1149. Humana, New York, NY
  20. Janaki AC, Sailatha E, Gunasekaran S (2015) Synthesis, characteristics and antimicrobial activity of ZnO nanoparticles. SpectrochimicaActa Part a: Molecular and Biomolecular Spectroscopy 144:17���22. https://doi.org/10.1016/j.saa.2015.02.041 [DOI: 10.1016/j.saa.2015.02.041]
  21. Khodaparast S, Ghanbari F, Zamani H (2022) Evaluation of the effect of ibuprofen in combination with ciprofloxacin on the virulence-associated traits, and efflux pump genes of pseudomonas aeruginosa. World J Microbiol Biotechnol 38(7):125. https://doi.org/10.1007/s11274-022-03316-2 [DOI: 10.1007/s11274-022-03316-2]
  22. Lallo da Silva B, Abu��afy MP, BerbelManaia E, Oshiro Junior JA, Chiari-Andr��o BG, Pietro RCR, Chiavacci LA (2019) Relationship between structure and antimicrobial activity of zinc oxide nanoparticles: an overview. Int J Nanomed. https://doi.org/10.2147/IJN.S216204 [DOI: 10.2147/IJN.S216204]
  23. Li XZ, Pl��siat P, Nikaido H (2015) The challenge of efflux-mediated antibiotic resistance in gram-negative bacteria. Clin Microbiol Rev 28(2):337���418 [DOI: 10.1128/CMR.00117-14]
  24. Mehrabi M, Ghasemi MF, Rasti B, Falahati M, Mirzaie A, Hasan A (2021) Nanoporous iron oxide nanoparticle: hydrothermal fabrication, human serum albumin interaction and potential antibacterial effects. J Biomol Struct Dyn 39(7):2595���2606. https://doi.org/10.1080/07391102.2020.1751296 [DOI: 10.1080/07391102.2020.1751296]
  25. Memariani H, Memariani M, Ghasemian A (2019) An overview on anti-biofilm properties of quercetin against bacterial pathogens. World J Microbiol Biotechnol 35:1���16 [DOI: 10.1007/s11274-019-2719-5]
  26. Mendes CR, Dilarri G, Forsan CF, Sapata VDMR, Lopes PRM, de Moraes PB, Bidoia ED et al (2022) Antibacterial action and target mechanisms of zinc oxide nanoparticles against bacterial pathogens. Sci Rep 12(1):2658. https://doi.org/10.1038/s41598-022-06657-y [DOI: 10.1038/s41598-022-06657-y]
  27. Negahdari R, Bohlouli S, Sharifi S, Maleki Dizaj S, Rahbar Saadat Y, Khezri K, Raeesi S et al (2021) Therapeutic benefits of rutin and its nanoformulations. Phytother Res 35(4):1719���1738. https://doi.org/10.1002/ptr.6904 [DOI: 10.1002/ptr.6904]
  28. Palaniappan B, Solomon AP (2021) Targeting AgrA quorum sensing regulator by bumetanide attenuates virulence in staphylococcus aureus���a drug repurposing approach. Life Sci 273:119306 [DOI: 10.1016/j.lfs.2021.119306]
  29. Peng LY, Yuan M, Cui ZQ, Wu ZM, Yu ZJ, Song K, Fu BD et al (2018) Rutin inhibits quorum sensing, biofilm formation and virulence genes in avian pathogenic escherichia coli. Microb Pathog 119:54���59. https://doi.org/10.1016/j.micpath.2018.04.007 [DOI: 10.1016/j.micpath.2018.04.007]
  30. Perera WPTD, Dissanayake RK, Ranatunga UI, Hettiarachchi NM, Perera KDC, Unagolla JM, Pahalagedara LR et al (2020) Curcumin loaded zinc oxide nanoparticles for activity-enhanced antibacterial and anticancer applications. RSC Adv 10(51):30785���30795. https://doi.org/10.1039/D0RA05755J [DOI: 10.1039/D0RA05755J]
  31. Qin S, Xiao W, Zhou C, Pu Q, Deng X, Lan L, Wu M et al (2022) Pseudomonas aeruginosa: pathogenesis, virulence factors, antibiotic resistance, interaction with host, technology advances and emerging therapeutics. Signal Transduct Target Ther 7(1):199. https://doi.org/10.1038/s41392-022-01056-1 [DOI: 10.1038/s41392-022-01056-1]
  32. Reyes D, Andrey DO, Monod A, Kelley WL, Zhang G, Cheung AL (2011) Coordinated regulation by AgrA, SarA, and SarR to control agr expression in Staphylococcus aureus. J Bacteriol 193(21):6020���6031. https://doi.org/10.1128/jb.05436-11 [DOI: 10.1128/jb.05436-11]
  33. Saadati F, Shahryari S, Sani NM, Farajzadeh D, Zahiri HS, Vali H, Noghabi KA (2022) Effect of MA01 rhamnolipid on cell viability and expression of quorum-sensing (QS) genes involved in biofilm formation by methicillin-resistant staphylococcus aureus. Sci Rep 12(1):14833. https://doi.org/10.1038/s41598-022-19103-w [DOI: 10.1038/s41598-022-19103-w]
  34. Sri KV, Kondaiah A, Ratna JV, Annapurna A (2007) Preparation and characterization of quercetin and rutincyclodextrin inclusion complexes. Drug Dev Ind Pharm 33(3):245���253. https://doi.org/10.1080/03639040601150195 [DOI: 10.1080/03639040601150195]
  35. Strateva T, Mitov I (2011) Contribution of an arsenal of virulence factors to pathogenesis of pseudomonas aeruginosa infections. Annals of Microbiology 61(4):717���732. https://doi.org/10.1007/s13213-011-0273-y [DOI: 10.1007/s13213-011-0273-y]
  36. Sysak S, Czarczynska-Goslinska B, Szyk P, Koczorowski T, Mlynarczyk DT, Szczolko W, Goslinski T et al (2023) Metal nanoparticle-flavonoid connections: synthesis, physicochemical and biological properties, as well as potential applications in medicine. Nanomaterials 13(9):1531. https://doi.org/10.3390/nano13091531 [DOI: 10.3390/nano13091531]
  37. Thakur P, Chawla R, Narula A, Goel R, Arora R, Sharma RK (2016) Anti-hemolytic, hemagglutination inhibition and bacterial membrane disruptive properties of selected herbal extracts attenuate virulence of carbapenem resistant escherichia coli. Microb Pathog 95:133���141. https://doi.org/10.1016/j.micpath.2016.04.005 [DOI: 10.1016/j.micpath.2016.04.005]
  38. Therapeutic benefits of rutin and its nanoformulations . https://onlinelibrary.wiley.com/doi/abs/ https://doi.org/10.1002/ptr.6904
  39. Zahmatkesh H, Mirpour M, Zamani H, Rasti B, Asadi Rahmani F, Padasht N (2022) Effect of samarium oxide nanoparticles on virulence factors and motility of multi-drug resistant Pseudomonas aeruginosa. World J Microbiol Biotechnol 38(11):209. https://doi.org/10.1007/s11274-022-03384-4 [DOI: 10.1007/s11274-022-03384-4]
  40. Zahmatkesh H, Mirpour M, Zamani H, Rasti B (2023) Effect of samarium oxide nanoparticles fabricated by curcumin on efflux pump and virulence genes expression in MDR pseudomonas aeruginosa and staphylococcus aureus. J Cluster Sci 34(3):1227���1235 [DOI: 10.1007/s10876-022-02274-x]
  41. Zhou L, Cai L, Ruan H, Zhang L, Wang J, Jiang H, Chen J et al (2021) Electrospun chitosan oligosaccharide/polycaprolactonenanofibers loaded with wound-healing compounds of rutin and quercetin as antibacterial dressings. Int J Biol Macromol 183:1145���1154. https://doi.org/10.1016/j.ijbiomac.2021.05.031 [DOI: 10.1016/j.ijbiomac.2021.05.031]

MeSH Term

Zinc Oxide
Rutin
Pseudomonas aeruginosa
Staphylococcus aureus
Anti-Bacterial Agents
Quorum Sensing
Microbial Sensitivity Tests
Nanoparticles
Bacterial Proteins
Metal Nanoparticles
Hemolysis
Virulence
Particle Size
Pyocyanine

Chemicals

Zinc Oxide
Rutin
Anti-Bacterial Agents
Bacterial Proteins
Pyocyanine

Word Cloud

Created with Highcharts 10.0.0NPsaeruginosaZnO-RutinPaureusSnanoparticlespathogenicbacteriaoxiderutinantivirulenceactivityexpression0studyzincpropertiesusingevaluatedhemolyticsensingQSlasIrhlIagrAtwitchingpyocyaninproductionZnOinhibitoryeffectsrespectivelyreducedfoldsuseengineeredgainedattentionconjugatedsynthesizedPseudomonasStaphylococcusphysicochemicalcharacteristicsinvestigatedSEMFT-IRXRDDLSEDSzetapotentialanalysesAntimicrobialwelldiffusionmicrodilutiongrowthcurveassaysquorumgenesincludingassessedreal-timePCRSwimmingswarmingamorphous14-100 nmdiametersurfacecharge-343 mVaveragehydrodynamicsize1617 nmRegardingantibacterialpotentstrongerobservedinhibited934922%efficientbare17-04337-070genedecreased46-056FurthermoresignificantlyswimmingmotilitydemonstratesfeaturescanassociatedRutin-coatednanoparticles:promisingformulationAntibacterialQuorumRutinZinc

Similar Articles

Cited By