Antibacterial Activity of Linezolid against Gram-Negative Bacteria: Utilization of ε-Poly-l-Lysine Capped Silica Xerogel as an Activating Carrier
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials and Culture Media
2.2. Preparation of Silica Xerogel Using Volcanic Tuff (Solid S0)
2.3. Synthesis of Linezolid Loaded Silica Xerogel (Solid S1) and ε-Poly-l-Lysine Capped Linezolid Loaded Silica Xerogel (Solid S2)
2.4. Material Characterization
2.5. Antibacterial Activity
3. Results and Discussion
4. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Hammad, A.; Abutaleb, N.S.; Elsebaei, M.M.; Norvil, A.B.; Alswah, M.; Ali, A.O.; Abdel-Aleem, J.A.; Alattar, A.; Bayoumi, S.A.; Gowher, H.; et al. From Phenylthiazoles to Phenylpyrazoles: Broadening the Antibacterial Spectrum toward Carbapenem-Resistant Bacteria. J. Med. Chem. 2019, 62, 7998–8010. [Google Scholar] [CrossRef] [PubMed]
- Yarlagadda, V.; Manjunath, G.B.; Sarkar, P.; Akkapeddi, P.; Paramanandham, K.; Shome, B.R.; Ravikumar, R.; Haldar, J. Glycopeptide Antibiotic to Overcome the Intrinsic Resistance of Gram-Negative Bacteria. ACS Infect. Dis. 2016, 2, 132–139. [Google Scholar] [CrossRef] [PubMed]
- Serri, A.; Mahboubi, A.; Zarghi, A.; Moghimi, H.R. PAMAM-dendrimer Enhanced Antibacterial Effect of Vancomycin Hydrochloride Against Gram-Negative Bacteria. J. Pharm. Pharm. Sci. 2019, 22, 10–21. [Google Scholar] [CrossRef] [PubMed]
- Bernardos, A.; Piacenza, E.; Sancenon, F.; Hamidi, M.; Maleki, A.; Turner, R.J.; Martínez-Máñez, R. Mesoporous Silica-Based Materials with Bactericidal Properties. Small 2019, 15, e1900669. [Google Scholar] [CrossRef] [PubMed]
- Rai, M.; Ingle, A.P.; Pandit, R.; Paralikar, P.; Gupta, I.; Chaud, M.V.; Dos Santos, C.A. Broadening the spectrum of small-molecule antibacterials by metallic nanoparticles to overcome microbial resistance. Int. J. Pharm. 2017, 532, 139–148. [Google Scholar] [CrossRef] [PubMed]
- Nicolosi, D.; Scalia, M.; Nicolosi, V.M.; Pignatello, R. Encapsulation in fusogenic liposomes broadens the spectrum of action of vancomycin against Gram-negative bacteria. Int. J. Antimicrob. Agents 2010, 35, 553–558. [Google Scholar] [CrossRef] [Green Version]
- Cottarel, G.; Wierzbowski, J. Combination drugs, an emerging option for antibacterial therapy. Trends Biotechnol. 2007, 25, 547–555. [Google Scholar] [CrossRef]
- Ulubayram, K.; Calamak, S.; Shahbazi, R.; Eroglu, I. Nanofibers Based Antibacterial Drug Design, Delivery and Applications. Curr. Pharm. Des. 2015, 21, 1930–1943. [Google Scholar] [CrossRef]
- Chen, C.; Yang, K. Ebselen bearing polar functionality: Identification of potent antibacterial agents against multidrug-resistant Gram-negative bacteria. Bioorg. Chem. 2019, 93, 103286. [Google Scholar] [CrossRef]
- Mas, N.; Galiana, I.; Mondragon, L.; Aznar, E.; Climent, E.; Cabedo, N.; Sancenon, F.; Murguia, J.R.; Martínez-Máñez, R.; Marcos, M.D.; et al. Enhanced efficacy and broadening of antibacterial action of drugs via the use of capped mesoporous nanoparticles. Chemistry 2013, 19, 11167–11171. [Google Scholar] [CrossRef]
- Sperandio, F.F.; Huang, Y.-Y.; Hamblin, M.R. Antimicrobial Photodynamic Therapy to Kill Gram-negative Bacteria. Recent Pat. Anti-Infect. Drug Discov. 2013, 8, 108–120. [Google Scholar] [CrossRef] [Green Version]
- Velikova, N.; Mas, N.; Miguel-Romero, L.; Polo, L.; Stolte, E.; Zaccaria, E.; Cao, R.; Taverne, N.; Murguia, J.R.; Martínez-Máñez, R.; et al. Broadening the antibacterial spectrum of histidine kinase autophosphorylation inhibitors via the use of epsilon-poly-L-lysine capped mesoporous silica-based nanoparticles. Nanomedicine 2017, 13, 569–581. [Google Scholar] [CrossRef] [PubMed]
- Hernández Montoto, A.; Montes, R.; Samadi, A.; Gorbe, M.; Terrés, J.M.; Cao-Milán, R.; Aznar, E.; Ibañez, J.; Masot, R.; Marcos, M.D.; et al. Gold Nanostars Coated with Mesoporous Silica Are Effective and Nontoxic Photothermal Agents Capable of Gate Keeping and Laser-Induced Drug Release. ACS Appl. Mater. Interface 2018, 10, 27644–27656. [Google Scholar] [CrossRef] [PubMed]
- García-Fernández, A.; Aznar, E.; Martínez-Máñez, R.; Sancenón, F. New Advances in In Vivo Applications of Gated Mesoporous Silica as Drug Delivery Nanocarriers. Small 2020, 16, 1902242. [Google Scholar] [CrossRef] [PubMed]
- Giménez, C.; de la Torre, C.; Gorbe, M.; Aznar, E.; Sancenón, F.; Murguía, J.R.; Martínez-Máñez, R.; Marcos, M.D.; Amorós, P. Gated Mesoporous Silica Nanoparticles for the Controlled Delivery of Drugs in Cancer Cells. Langmuir 2015, 31, 3753–3762. [Google Scholar] [CrossRef] [PubMed]
- Moreno, V.M.; Álvarez, E.; Izquierdo-Barba, I.; Baeza, A.; Serrano-López, J.; Vallet-Regí, M. Bacteria as nanoparticles carrier for enhancing penetration in a tumoral matrix model. Adv. Mater. Interfaces 2020, 7, 1901942. [Google Scholar] [CrossRef] [PubMed]
- Shadjou, N.; Hasanzadeh, M. Bone tissue engineering using silica-based mesoporous nanobiomaterials: Recent progress. Mater. Sci. Eng. C Mater. Biol. Appl. 2015, 55, 401–409. [Google Scholar] [CrossRef] [PubMed]
- Mas, N.; Arcos, D.; Polo, L.; Aznar, E.; Sánchez-Salcedo, S.; Sancenón, F.; García, A.; Marcos, M.D.; Baeza, A.; Vallet-Regí, M.; et al. Towards the Development of Smart 3D “Gated Scaffolds” for On-Command Delivery. Small 2014, 10, 4859–4864. [Google Scholar] [CrossRef]
- Wang, Y.; Zhao, Q.; Han, N.; Bai, L.; Li, J.; Liu, J.; Che, E.; Hu, L.; Zhang, Q.; Jiang, T.; et al. Mesoporous silica nanoparticles in drug delivery and biomedical applications. Nanomedicine 2015, 11, 313–327. [Google Scholar] [CrossRef]
- Llopis-Lorente, A.; Diez, P.; Sanchez, A.; Marcos, M.D.; Sancenon, F.; Martinez-Ruiz, P.; Villalonga, R.; Martínez-Máñez, R. Interactive models of communication at the nanoscale using nanoparticles that talk to one another. Nat. Commun. 2017, 8, 15511. [Google Scholar] [CrossRef] [Green Version]
- Giménez, C.; Climent, E.; Aznar, E.; Martínez-Máñez, R.; Sancenón, F.; Marcos, M.D.; Amorós, P.; Rurack, K. Towards chemical communication between gated nanoparticles. Angew. Chem. Int. Ed. 2014, 53, 12629–12633. [Google Scholar] [CrossRef] [PubMed]
- de Luis, B.; Llopis-Lorente, A.; Rincón, P.; Gadea, J.; Sancenón, F.; Aznar, E.; Villalonga, R.; Murguía, J.R.; Martínez-Máñez, R. An interactive model of communication between abiotic nanodevices and microorganisms. Angew. Chem. Int. Ed. 2019, 58, 14986–14990. [Google Scholar] [CrossRef] [PubMed]
- Hasanzadeh, M.; Shadjou, N.; de la Guardia, M.; Eskandani, M.; Sheikhzadeh, P. Mesoporous silica-based materials for use in biosensors. TrAC Trends Anal. Chem. 2012, 33, 117–129. [Google Scholar] [CrossRef]
- El-Safty, S.A.; Shenashen, M.A. Nanoscale dynamic chemical, biological sensor material designs for control monitoring and early detection of advanced diseases. Mater. Today Bio 2020, 5, 100044. [Google Scholar] [CrossRef]
- Pla, L.; Santiago-Felipe, S.; Tormo-Mas, M.A.; Pemán, J.; Sancenón, F.; Aznar, E.; Martínez-Máñez, R. Aptamer-capped nanoporous anodic alumina for Staphylococcus aureus detection. Sens. Actuators B Chem. 2020, 320, 128281. [Google Scholar] [CrossRef]
- Ciriminna, R.; Fidalgo, A.; Pandarus, V.; Beland, F.; Ilharco, L.M.; Pagliaro, M. The sol-gel route to advanced silica-based materials and recent applications. Chem. Rev. 2013, 113, 6592–6620. [Google Scholar] [CrossRef]
- Ulker, Z.; Erkey, C. An emerging platform for drug delivery: Aerogel based systems. J. Control. Release 2014, 177, 51–63. [Google Scholar] [CrossRef]
- Guzel Kaya, G.; Yilmaz, E.; Deveci, H. Sustainable nanocomposites of epoxy and silica xerogel synthesized from corn stalk ash: Enhanced thermal and acoustic insulation performance. Compos. Part. B Eng. 2018, 150, 1–6. [Google Scholar] [CrossRef]
- Maleki, H.; Duraes, L.; Garcia-Gonzalez, C.A.; Del Gaudio, P.; Portugal, A.; Mahmoudi, M. Synthesis and biomedical applications of aerogels: Possibilities and challenges. Adv. Colloid Interface Sci. 2016, 236, 1–27. [Google Scholar] [CrossRef]
- Quintanar-Guerrero, D.; Ganem-Quintanar, A.; Nava-Arzaluz, M.G.; Pinon-Seundo, E. Silica xerogels as pharmaceutical drug carriers. Expert Opin. 2009, 6, 485–498. [Google Scholar] [CrossRef]
- Pérez, N.A.; Lima, E.; Bosch, P.; Méndez-Vivar, J. Consolidating materials for the volcanic tuff in western Mexico. J. Cult. Herit. 2014, 15, 352–358. [Google Scholar] [CrossRef]
- Lemougna, P.N.; Wang, K.-T.; Tang, Q.; Nzeukou, A.N.; Billong, N.; Melo, U.C.; Cui, X.-M. Review on the use of volcanic ashes for engineering applications. Resour. Conserv. Recycl. 2018, 137, 177–190. [Google Scholar] [CrossRef]
- Maranon, E.; Ulmanu, M.; Fernandez, Y.; Anger, I.; Castrillon, L. Removal of ammonium from aqueous solutions with volcanic tuff. J. Hazard. Mater. 2006, 137, 1402–1409. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brum, L.F.W.; dos Santos, C.; Gnoatto, J.A.; Moura, D.J.; Santos, J.H.Z.; Brandelli, A. Silica xerogels as novel streptomycin delivery platforms. J. Drug Deliv. Sci. Technol. 2019, 53, 101210. [Google Scholar] [CrossRef]
- Deon, M.; Morawski, F.M.; Passaia, C.; Dalmás, M.; Laranja, D.C.; Malheiros, P.S.; Nicolodi, S.; Arenas, L.T.; Costa, T.M.H.; de Menezes, E.W.; et al. Chitosan-stabilized gold nanoparticles supported on silica/titania magnetic xerogel applied as antibacterial system. J. Sol-Gel Sci. Technol. 2018, 89, 333–342. [Google Scholar] [CrossRef]
- Storm, W.L.; Youn, J.; Reighard, K.P.; Worley, B.V.; Lodaya, H.M.; Shin, J.H.; Schoenfisch, M.H. Superhydrophobic nitric oxide-releasing xerogels. Acta Biomater. 2014, 10, 3442–3448. [Google Scholar] [CrossRef]
- Guzel Kaya, G.; Yilmaz, E.; Deveci, H. A novel silica xerogel synthesized from volcanic tuff as an adsorbent for high-efficient removal of methylene blue: Parameter optimization using Taguchi experimental design. J. Chem. Technol. Biotechnol. 2019, 94, 2729–2737. [Google Scholar] [CrossRef]
- Mohammadian, M.; Jafarzadeh Kashi, T.S.; Erfan, M.; Soorbaghi, F.P. Synthesis and characterization of silica aerogel as a promising drug carrier system. J. Drug Deliv. Sci. Technol. 2018, 44, 205–212. [Google Scholar] [CrossRef]
- Hu, W.; Li, M.; Chen, W.; Zhang, N.; Li, B.; Wang, M.; Zhao, Z. Preparation of hydrophobic silica aerogel with kaolin dried at ambient pressure. Colloid Surf. A Physicochem. Eng. Asp. 2016, 501, 83–91. [Google Scholar] [CrossRef]
- Zhu, H.; Jia, S.; Yang, H.; Tang, W.; Jia, Y.; Tan, Z. Characterization of bacteriostatic sausage casing: A composite of bacterial cellulose embedded with ɛ-polylysine. Food Sci. Biotechnol. 2010, 19, 1479–1484. [Google Scholar] [CrossRef]
- Lei, Y.; Hu, Z.; Cao, B.; Chen, X.; Song, H. Enhancements of thermal insulation and mechanical property of silica aerogel monoliths by mixing graphene oxide. Mater. Chem. Phys. 2017, 187, 183–190. [Google Scholar] [CrossRef]
- Huang, D.; Guo, C.; Zhang, M.; Shi, L. Characteristics of nanoporous silica aerogel under high temperature from 950 °C to 1200 °C. Mater. Des. 2017, 129, 82–90. [Google Scholar] [CrossRef]
- Kashyap Khatri, S.; Bathnanand, M.; Nikhila, R. Formulation and Evaluation of Wound Healing Activity of Linezolid Topical Preparations on Diabetic Rats. Int. J. Appl. Pharm. 2016, 8, 30–36. [Google Scholar]
- Shi, K.; Liu, Y.; Ke, L.; Fang, Y.; Yang, R.; Cui, F. Epsilon-poly-L-lysine guided improving pulmonary delivery of supramolecular self-assembled insulin nanospheres. Int. J. Biol. Macromol. 2015, 72, 1441–1450. [Google Scholar] [CrossRef]
- Lin, L.; Xue, L.; Duraiarasan, S.; Haiying, C. Preparation of ε-polylysine/chitosan nanofibers for food packaging against Salmonella on chicken. Food Pack Shelf Life 2018, 17, 134–141. [Google Scholar] [CrossRef]
- Lv, J.M.; Meng, Y.C.; Shi, Y.G.; Li, Y.H.; Chen, J.; Sheng, F. Properties of epsilon-polylysine·HCl/high-methoxyl pectin polyelectrolyte complexes and their commercial application. J. Food Process. Preserv. 2020, 44, e14320. [Google Scholar] [CrossRef]
- Huber, L.; Zhao, S.; Malfait, W.J.; Vares, S.; Koebel, M.M. Fast and Minimal-Solvent Production of Superinsulating Silica Aerogel Granulate. Angew. Chem. Int. Ed. 2017, 56, 4753–4756. [Google Scholar] [CrossRef]
- Shi, F.; Liu, J.-X.; Song, K.; Wang, Z.-Y. Cost-effective synthesis of silica aerogels from fly ash via ambient pressure drying. J. Non-Cryst. Solids 2010, 356, 2241–2246. [Google Scholar] [CrossRef]
- Sarawade, P.B.; Kim, J.-K.; Hilonga, A.; Kim, H.T. Production of low-density sodium silicate-based hydrophobic silica aerogel beads by a novel fast gelation process and ambient pressure drying process. Solid State Sci. 2010, 12, 911–918. [Google Scholar] [CrossRef]
- Liu, G.; Yang, R.; Li, M. Liquid adsorption of basic dye using silica aerogels with different textural properties. J. Non-Cryst. Solids 2010, 356, 250–257. [Google Scholar] [CrossRef]
- Guzel Kaya, G.; Deveci, H. Effect of Aging Solvents on Physicochemical and Thermal Properties of Silica Xerogels Derived from Steel Slag. ChemistrySelect 2020, 5, 1586–1591. [Google Scholar] [CrossRef]
- Rao, A.P.; Rao, A.V.; Gurav, J.L. Effect of protic solvents on the physical properties of the ambient pressure dried hydrophobic silica aerogels using sodium silicate precursor. J. Porous Mater. 2007, 15, 507–512. [Google Scholar] [CrossRef]
- Sperling, R.A.; Parak, W.J. Surface modification, functionalization and bioconjugation of colloidal inorganic nanoparticles. Philos. Trans. A Math. Phys. Eng. Sci. 2010, 368, 1333–1383. [Google Scholar] [CrossRef] [PubMed]
- Ma, X.-k.; Lee, N.-H.; Oh, H.-J.; Kim, J.-W.; Rhee, C.-K.; Park, K.-S.; Kim, S.-J. Surface modification and characterization of highly dispersed silica nanoparticles by a cationic surfactant. Colloid Surf. A Physicochem. Eng. Asp. 2010, 358, 172–176. [Google Scholar] [CrossRef]
- Tan, L.; Tan, X.; Fang, M.; Yu, Z.; Wang, X. Effects of humic acid and Mg2+ on morphology and aggregation behavior of silica aerogels. J. Mol. Liq. 2018, 264, 261–268. [Google Scholar] [CrossRef]
- Wang, L.; Hu, C.; Shao, L. The antimicrobial activity of nanoparticles: Present situation and prospects for the future. Int. J. Nanomed. 2017, 12, 1227–1249. [Google Scholar] [CrossRef] [Green Version]
- Hasan, J.; Crawford, R.J.; Ivanova, E.P. Antibacterial surfaces: The quest for a new generation of biomaterials. Trends Biotechnol. 2013, 31, 295–304. [Google Scholar] [CrossRef]
- Katsikogianni, M.; Missirlis, Y.F. Concise Review of Mechanisms of Bacterial Adhesion to Biomaterials and of Techniques Used in Estimating Bacteria-Material Interactions. Eur. Cell Mater. 2004, 8, 37–57. [Google Scholar] [CrossRef]
- Ruiz-Rico, M.; Fuentes, C.; Pérez-Esteve, É.; Jiménez-Belenguer, A.I.; Quiles, A.; Marcos, M.D.; Martínez-Máñez, R.; Barat, J.M. Bactericidal activity of caprylic acid entrapped in mesoporous silica nanoparticles. Food Control 2015, 56, 77–85. [Google Scholar] [CrossRef]
- Zahedi Bialvaei, A.; Rahbar, M.; Yousefi, M.; Asgharzadeh, M.; Samadi Kafil, H. Linezolid: A promising option in the treatment of Gram-positives. J. Antimicrob. Chemother. 2017, 72, 354–364. [Google Scholar] [CrossRef] [Green Version]
- Chang, Y.; McLandsborough, L.; McClements, D.J. Cationic Antimicrobial (ε-Polylysine)–Anionic Polysaccharide (Pectin) Interactions: Influence of Polymer Charge on Physical Stability and Antimicrobial Efficacy. J. Agric. Food Chem. 2012, 60, 1837–1844. [Google Scholar] [CrossRef] [PubMed]
- Shukla, S.C.; Singh, A.; Pandey, A.K.; Mishra, A. Review on production and medical applications of ε-polylysine. Biochem. Eng. J. 2012, 65, 70–81. [Google Scholar] [CrossRef]
- Liu, J.-N.; Chang, S.-L.; Xu, P.-W.; Tan, M.-H.; Zhao, B.; Wang, X.-D.; Zhao, Q.-S. Structural Changes and Antibacterial Activity of Epsilon-poly-L-lysine in Response to pH and Phase Transition and Their Mechanisms. J. Agric. Food Chem. 2020, 68, 1101–1109. [Google Scholar] [CrossRef] [PubMed]
Material | Composition |
---|---|
Solid S0 | Silica xerogel |
Solid S1 | Silica xerogel loaded with linezolid |
Solid S2 | Silica xerogel loaded with linezolid and capped with ε-poly-l-lysine |
Material | SBET a (m2 g−1) | Pore Size (nm) | Pore Volume (cm3 g−1) | Bulk Density (g cm−3) |
---|---|---|---|---|
solid S0 | 195 | 10 | 0.50 | 0.037 |
Material | Zeta Potential (mV) | Electrophoretic Mobility (μm cm V−1 S−1) | Conductivity (mS cm−1) |
---|---|---|---|
solid S0 | −46.1 ± 0.1 | −3.62 ± 0.01 | 0.0327 |
solid S1 | −42.0 ± 1.1 | −3.29 ± 0.09 | 0.0314 |
solid S2 | 16.9 ± 0.6 | 1.33 ± 0.05 | 0.0271 |
Material | Linezolid (mmol g−1) | ε-poly-l-lysine (mmol g−1) |
---|---|---|
solid S1 | 0.188 | - |
solid S2 | 0.187 | 0.022 |
Active Compound | Escherichia coli | Pseudomonas aeruginosa | Staphylococcus aureus |
---|---|---|---|
linezolid | --- | --- | 1.00 |
ε-poly-l-lysine | 0.13 | 0.21 | 0.08 |
Material | Escherichia coli | Pseudomonas aeruginosa | Staphylococcus aureus |
---|---|---|---|
solid S1 | --- | --- | 1.37 |
solid S2 | 0.04 | 0.02 | 0.07 |
solid S3 | 0.29 | 0.21 | 0.51 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Guzel Kaya, G.; Medaglia, S.; Candela-Noguera, V.; Tormo-Mas, M.Á.; Marcos, M.D.; Aznar, E.; Deveci, H.; Martínez-Máñez, R. Antibacterial Activity of Linezolid against Gram-Negative Bacteria: Utilization of ε-Poly-l-Lysine Capped Silica Xerogel as an Activating Carrier. Pharmaceutics 2020, 12, 1126. https://doi.org/10.3390/pharmaceutics12111126
Guzel Kaya G, Medaglia S, Candela-Noguera V, Tormo-Mas MÁ, Marcos MD, Aznar E, Deveci H, Martínez-Máñez R. Antibacterial Activity of Linezolid against Gram-Negative Bacteria: Utilization of ε-Poly-l-Lysine Capped Silica Xerogel as an Activating Carrier. Pharmaceutics. 2020; 12(11):1126. https://doi.org/10.3390/pharmaceutics12111126
Chicago/Turabian StyleGuzel Kaya, Gulcihan, Serena Medaglia, Vicente Candela-Noguera, María Ángeles Tormo-Mas, María Dolores Marcos, Elena Aznar, Huseyin Deveci, and Ramón Martínez-Máñez. 2020. "Antibacterial Activity of Linezolid against Gram-Negative Bacteria: Utilization of ε-Poly-l-Lysine Capped Silica Xerogel as an Activating Carrier" Pharmaceutics 12, no. 11: 1126. https://doi.org/10.3390/pharmaceutics12111126
APA StyleGuzel Kaya, G., Medaglia, S., Candela-Noguera, V., Tormo-Mas, M. Á., Marcos, M. D., Aznar, E., Deveci, H., & Martínez-Máñez, R. (2020). Antibacterial Activity of Linezolid against Gram-Negative Bacteria: Utilization of ε-Poly-l-Lysine Capped Silica Xerogel as an Activating Carrier. Pharmaceutics, 12(11), 1126. https://doi.org/10.3390/pharmaceutics12111126