Antibacterial effect of protease-responsive cationic eugenol liposomes modified by gamma-polyglutamic acid against Staphylococcus aureus

References

• Pesavento G, Calonico C, Bilia A, et al. Antibacterial activity of Oregano, Rosmarinus and Thymus essential oils against Staphylococcus aureus and Listeria monocytogenes in beef meatballs. Food Control. 2015;54:188–199. doi: 10.1016/j.foodcont.2015.01.045.
   Web of Science ®Google Scholar
• Shi Y-G, Zhang R-R, Zhu C-M, et al. Antimicrobial mechanism of alkyl gallates against Escherichia coli and Staphylococcus aureus and its combined effect with electrospun nanofibers on Chinese Taihu icefish preservation. Food Chem. 2021;346:128949. doi: 10.1016/j.foodchem.2020.128949.
   PubMed Web of Science ®Google Scholar
• Lues J, Van Tonder I. The occurrence of indicator bacteria on hands and aprons of food handlers in the delicatessen sections of a retail group. Food Control. 2007;18(4):326–332. doi: 10.1016/j.foodcont.2005.10.010.
   Web of Science ®Google Scholar
• Bakkeren E, Diard M, Hardt W-D. Evolutionary causes and consequences of bacterial antibiotic persistence. Nat Rev Microbiol. 2020;18(9):479–490. doi: 10.1038/s41579-020-0378-z.
   PubMed Web of Science ®Google Scholar
• Birania S, Attkan AK, Kumar S, et al. Cold plasma in food processing and preservation: a review. J Food Process Eng. 2022;45(9):e14110. doi: 10.1111/jfpe.14110.
   Web of Science ®Google Scholar
• Falguera V, Pagán J, Garza S, et al. Ultraviolet processing of liquid food: a review: Part 2: effects on microorganisms and on food components and properties. Food Res Int. 2011;44(6):1580–1588. doi: 10.1016/j.foodres.2011.03.025.
   Web of Science ®Google Scholar
• Soni A, Smith J, Thompson A, et al. Microwave-induced thermal sterilization- A review on history, technical progress, advantages and challenges as compared to the conventional methods. Trends Food Sci Technol. 2020;97:433–442. doi: 10.1016/j.tifs.2020.01.030.
   Web of Science ®Google Scholar
• Ju J, Chen X, Xie Y, et al. Application of essential oil as a sustained release preparation in food packaging. Trends Food Sci Technol. 2019;92:22–32. doi: 10.1016/j.tifs.2019.08.005.
   Web of Science ®Google Scholar
• Ni Z-J, Wang X, Shen Y, et al. Recent updates on the chemistry, bioactivities, mode of action, and industrial applications of plant essential oils. Trends Food Sci & Technol. 2021;110:78–89. doi: 10.1016/j.tifs.2021.01.070.
   Web of Science ®Google Scholar
• Yang H, Zhan XJ, Song LY, et al. Synergistic antibacterial and anti-biofilm mechanisms of ultrasound combined with citral nanoemulsion against Staphylococcus aureus 29213. Int J Food Microbiol. 2023;391-393:110150. doi: 10.1016/j.ijfoodmicro.2023.110150.
   PubMed Web of Science ®Google Scholar
• Nagababu E, Rifkind JM, Boindala S, et al. (2010). Assessment of antioxidant activity of eugenol in vitro and in vivo. In: Uppu R, Murthy S, Pryor W, Parinandi N, editors. Free radicals and antioxidant protocols. Methods in Molecular Biology. Vol. 610; Clifton city, New Jersey, USA: Humana Press; pp. 165–180. doi: 10.1007/978-1-60327-029-8_10
   Google Scholar
• Hadidi M, Pouramin S, Adinepour F, et al. Chitosan nanoparticles loaded with clove essential oil: Characterization, antioxidant and antibacterial activities. Carbohydr Polym. 2020;236:116075. doi: 10.1016/j.carbpol.2020.116075.
   PubMed Web of Science ®Google Scholar
• Yuan G, Chen X, Li D. Chitosan films and coatings containing essential oils: the antioxidant and antimicrobial activity, and application in food systems. Food Res Int. 2016;89(Pt 1):117–128. doi: 10.1016/j.foodres.2016.10.004.
   PubMed Web of Science ®Google Scholar
• Peinado I, Mason M, Romano A, et al. Stability of β-carotene in polyethylene oxide electrospun nanofibers. Appl Surf Sci. 2016;370:111–116. doi: 10.1016/j.apsusc.2016.02.150.
   Web of Science ®Google Scholar
• Qiu J, Feng H, Lu J, et al. Eugenol reduces the expression of Virulence-Related exoproteins in Staphylococcus aureus. Appl Environ Microbiol. 2010;76(17):5846–5851. doi: 10.1128/AEM.00704-10.
   PubMed Web of Science ®Google Scholar
• Yadav MK, Chae S-W, Im GJ, et al. Eugenol: a phyto-compound effective against methicillin-resistant and methicillin-sensitive Staphylococcus aureus clinical strain biofilms. PLOS One. 2015;10(3):e0119564. doi: 10.1371/journal.pone.0119564.
   PubMed Web of Science ®Google Scholar
• Choi M-J, Soottitantawat A, Nuchuchua O, et al. Physical and light oxidative properties of eugenol encapsulated by molecular inclusion and emulsion–diffusion method. Food Res Int. 2009;42(1):148–156. doi: 10.1016/j.foodres.2008.09.011.
   Web of Science ®Google Scholar
• Chen K, Zhang M, Mujumdar AS, et al. Quinoa protein-gum Arabic complex coacervates as a novel carrier for eugenol: Preparation, characterization and application for minced pork preservation. Food Hydrocolloids. 2021;120:106915. doi: 10.1016/j.foodhyd.2021.106915.
   Web of Science ®Google Scholar
• Talón E, Lampi A-M, Vargas M, et al. Encapsulation of eugenol by spray-drying using whey protein isolate or lecithin: Release kinetics, antioxidant and antimicrobial properties. Food Chem. 2019;295:588–598. doi: 10.1016/j.foodchem.2019.05.115.
   PubMed Web of Science ®Google Scholar
• Torchilin VP. Recent advances with liposomes as pharmaceutical carriers. Nat Rev Drug Discov. 2005;4(2):145–160. doi: 10.1038/nrd1632.
   PubMed Web of Science ®Google Scholar
• da Silva Barbosa RF, Yudice EDC, Mitra SK, et al. Characterization of rosewood and cinnamon cassia essential oil polymeric capsules: stability, loading efficiency, release rate and antimicrobial properties. Food Control. 2021;121:107605. doi: 10.1016/j.foodcont.2020.107605.
   Web of Science ®Google Scholar
• Prakash B, Kujur A, Yadav A, et al. Nanoencapsulation: an efficient technology to boost the antimicrobial potential of plant essential oils in food system. Food Control. 2018;89:1–11. doi: 10.1016/j.foodcont.2018.01.018.
   Web of Science ®Google Scholar
• Lin L, Gu Y, Sun Y, et al. Characterization of chrysanthemum essential oil triple-layer liposomes and its application against Campylobacter jejuni on chicken. LWT. 2019;107:16–24. doi: 10.1016/j.lwt.2019.02.079.
   Web of Science ®Google Scholar
• Risaliti L, Kehagia A, Daoultzi E, et al. Liposomes loaded with Salvia triloba and Rosmarinus officinalis essential oils: in vitro assessment of antioxidant, antiinflammatory and antibacterial activities. J Drug Delivery Sci Technol. 2019;51:493–498. doi: 10.1016/j.jddst.2019.03.034.
   Web of Science ®Google Scholar
• Sebaaly C, Jraij A, Fessi H, et al. Preparation and characterization of clove essential oil-loaded liposomes. Food Chem. 2015;178:52–62. doi: 10.1016/j.foodchem.2015.01.067.
   PubMed Web of Science ®Google Scholar
• Lee Y, Thompson DH. Stimuli-responsive liposomes for drug delivery. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2017;9(5):e1450. doi: 10.1002/wnan.1450.
   Web of Science ®Google Scholar
• Yuba E. Development of functional liposomes by modification of stimuli-responsive materials and their biomedical applications. J Mater Chem B. 2020;8(6):1093–1107. doi: 10.1039/c9tb02470k.
   PubMed Web of Science ®Google Scholar
• Ge Y, Tang J, Fu H, et al. Characteristics, controlled-release and antimicrobial properties of tea tree oil liposomes-incorporated chitosan-based electrospun nanofiber mats. Fibers Polym. 2019;20(4):698–708. doi: 10.1007/s12221-019-1092-1.
   Web of Science ®Google Scholar
• Wu Z, Zhou W, Pang C, et al. Multifunctional chitosan-based coating with liposomes containing laurel essential oils and nanosilver for pork preservation. Food Chem. 2019;295:16–25. doi: 10.1016/j.foodchem.2019.05.114.
   PubMed Web of Science ®Google Scholar
• Lee N-R, Go T-H, Lee S-M, et al. In vitro evaluation of new functional properties of poly-γ-glutamic acid produced by Bacillus subtilis D7. Saudi J Biol Sci. 2014;21(2):153–158. doi: 10.1016/j.sjbs.2013.09.004.
   PubMed Web of Science ®Google Scholar
• Richert L, Lavalle P, Vautier D, et al. Cell interactions with polyelectrolyte multilayer films. Biomacromolecules. 2002;3(6):1170–1178. doi: 10.1021/bm0255490.
   PubMed Web of Science ®Google Scholar
• Schultz P, Vautier D, Richert L, et al. Polyelectrolyte multilayers functionalized by a synthetic analogue of an anti-inflammatory peptide, α-MSH, for coating a tracheal prosthesis. Biomaterials. 2005;26(15):2621–2630. doi: 10.1016/j.biomaterials.2004.06.049.
   PubMed Web of Science ®Google Scholar
• Kurosaki T, Kitahara T, Kawakami S, et al. γ-Polyglutamic acid-coated vectors for effective and safe gene therapy. J Control Release. 2010;142(3):404–410. doi: 10.1016/j.jconrel.2009.11.010.
   PubMed Web of Science ®Google Scholar
• Sasai M, Sakura K, Matsuda T, et al. A novel formulation of cisplatin with γ-polyglutamic acid and chitosan reduces its adverse renal effects: an in vitro and in vivo animal study. Polymers . 2021;13(11):1803. doi: 10.3390/polym13111803.
   PubMed Web of Science ®Google Scholar
• Bantel H, Sinha B, Domschke W, et al. α-Toxin is a mediator of Staphylococcus aureus–induced cell death and activates caspases via the intrinsic death pathway independently of death receptor signaling. J Cell Biol. 2001;155(4):637–648. doi: 10.1083/jcb.200105081.
   PubMed Web of Science ®Google Scholar
• Pornpattananangkul D, Zhang L, Olson S, et al. Bacterial toxin-triggered drug release from gold nanoparticle-stabilized liposomes for the treatment of bacterial infection. J Am Chem Soc. 2011;133(11):4132–4139. doi: 10.1021/ja111110e.
   PubMed Web of Science ®Google Scholar
• Yao J, Jing J, Xu H, et al. Investigation on enzymatic degradation of γ-polyglutamic acid from Bacillus subtilis NX-2. J Mol Catal B: Enzym. 2009;56(2–3):158–164. doi: 10.1016/j.molcatb.2007.12.027.
   Google Scholar
• Cui H, Li W, Li C, et al. Liposome containing cinnamon oil with antibacterial activity against methicillin-resistant Staphylococcus aureus biofilm. Biofouling. 2016;32(2):215–225. doi: 10.1080/08927014.2015.1134516.
   PubMed Web of Science ®Google Scholar
• Ciobanu M, Heurtault B, Schultz P, et al. Layersome: development and optimization of stable liposomes as drug delivery system. Int J Pharm. 2007;344(1–2):154–157. doi: 10.1016/j.ijpharm.2007.05.037.
   PubMedGoogle Scholar
• Michel M, Izquierdo A, Decher G, et al. Layer by layer self-assembled polyelectrolyte multilayers with embedded phospholipid vesicles. Langmuir. 2005;21(17):7854–7859. doi: 10.1021/la049736q.
   PubMed Web of Science ®Google Scholar
• Migoń D, Wasilewski T, Suchy D. Application of QCM in peptide and protein-based drug product development. Molecules. 2020;25(17):3950. doi: 10.3390/molecules25173950.
   PubMed Web of Science ®Google Scholar
• Wang Q, Xie Y-F, Zhao W-J, et al. Rapid microchip-based FAIMS determination of trimethylamine, an indicator of pork deterioration. Anal Methods. 2014;6(9):2965–2972. doi: 10.1039/C3AY41941J.
   Web of Science ®Google Scholar
• Wang H, Zhao P, Liang X, et al. Folate-PEG coated cationic modified chitosan–cholesterol liposomes for tumor-targeted drug delivery. Biomaterials. 2010;31(14):4129–4138. doi: 10.1016/j.biomaterials.2010.01.089.
   PubMed Web of Science ®Google Scholar
• Siyal FJ, Memon Z, Siddiqui RA, et al. Eugenol and liposome-based nanocarriers loaded with eugenol protect against anxiolytic disorder via down regulation of neurokinin-1 receptors in mice. Pak J Pharm Sci. 2020;33(5(Supplementary):2275–2284.
   PubMed Web of Science ®Google Scholar
• Silvianti F, Siswanta D, Aprilita NH, et al. Adsorption characteristic of iron onto poly [eugenol-co-(divinyl benzene)] from aqueous solution. J Nat. 2017;17(2):108–117. doi: 10.24815/jn.v17i2.8076.
   Google Scholar
• Hu Q, Gerhard H, Upadhyaya I, et al. Antimicrobial eugenol nanoemulsion prepared by gum arabic and lecithin and evaluation of drying technologies. Int J Biol Macromol. 2016;87:130–140. doi: 10.1016/j.ijbiomac.2016.02.051.
   PubMed Web of Science ®Google Scholar
• De Leo V, Milano F, Agostiano A, et al. Recent advancements in polymer/liposome assembly for drug delivery: from surface modifications to hybrid vesicles. Polymers. 2021;13(7):1027. doi: 10.3390/polym13071027.
   PubMed Web of Science ®Google Scholar
• Huang W, Xu H, Xue Y, et al. Layer-by-layer immobilization of lysozyme–chitosan–organic rectorite composites on electrospun nanofibrous mats for pork preservation. Food Res Int. 2012;48(2):784–791. doi: 10.1016/j.foodres.2012.06.026.
   Web of Science ®Google Scholar
• Guo T, Huang M, Zhu Q, et al. Hyperspectral image-based multi-feature integration for TVB-N measurement in pork. J Food Eng. 2018;218:61–68. doi: 10.1016/j.jfoodeng.2017.09.003.
   Web of Science ®Google Scholar