journal article·2018-05

Synthesis of chitosan/poly (ethylene glycol)-modified magnetic nanoparticles for antibiotic delivery and their enhanced anti-biofilm activity in the presence of magnetic field

Xi Wang, Aipeng Deng, Weiwei Cao, Qiang Li, Lina Wang, Jie Zhou, Bingcheng Hu, Xiaodong Xing

Journal of Materials Science· Volume 53· Issue 9
Publisher page

Abstract

Biocompatible Fe3O4/chitosan (CS)/poly (ethylene glycol) (PEG)/gentamicin (Gent) magnetic nanoparticles, namely Fe3O4@PEG-Gent NPs, have been successfully developed for antibiotic delivery. In which, PEG dicarboxylic acid was used to modify Fe3O4 NPs for good dispersity as well as offer sufficient carboxyl groups as binding sites. And then the free Gent was facilely loaded onto Fe3O4 NPs so as to achieve powerful antibacterial activity via electrostatic interactions. Under acidic condition, the CS and PEG of Fe3O4@PEG-Gent were protonated to introduce the positive charge to NPs surface, thus facilitating the contact with negatively charged bacterial cell membrane. What is more, the stretches of CS chains triggered by acidic pH may prevent the antimicrobial efficiency of Gent from weakening. Compared with the free antibiotic, these nanocomposites presented better antimicrobial efficacy against gram-positive bacteria S. aureus under acidic condition. Intriguingly, the confocal laser scanning macroscopy imaging suggested that the anti-biofilm efficacy of nanocomposites was significantly enhanced in the presence of an external magnetic field. Due to the superparamagnetic performance of Fe3O4 NPs, these nanocomposites were allowed deeper penetration into a mature biofilm of S. aureus by magnetic field, leading to an effective Gent delivery for eradication of biofilm. The ingenious fabrication of the antibiotic delivery system not only efficiently improved the effectiveness and bioavailability of Gent at acidic media, but also provided an innovative platform to treat bacterial biofilms-associated infection by applying extra environmental factors such as magnetic field.
Source: openaire · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Bacterial biofilms and quorum sensing · Antimicrobial agents and applications · Oral microbiology and periodontitis research

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (56)

Show source-provided references
1. Costerton JW, Stewart PS, Greenburg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–132210.1126/science.284.5418.1318 ↗
2. Stoodley LH, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–10810.1038/nrmicro821 ↗
3. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–63310.1038/nrmicro2415 ↗
4. Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–20910.1146/annurev.micro.56.012302.160705 ↗
5. Guo QQ, Zhao Y, Dai XM, Zhang TQ, Yu YJ, Zhang XQ, Li CX (2017) Functional silver nanocomposites as broad-spectrum antimicrobial and biofilm-disrupting agents. ACS Appl Mater Interfaces 9:16834–1684710.1021/acsami.7b02775 ↗
6. Taubes G (2008) The bacteria fight back. Science 321:356–36110.1126/science.321.5887.356 ↗
7. Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358:135–13810.1016/S0140-6736(01)05321-1 ↗
8. Ridenhour BJ, Metzger GA, France M, Gliniewicz K, Millstein J, Forney LJ, Top EM (2017) Persistence of antibiotic resistance plasmids in bacterial biofilms. Evol Appl 10:640–64710.1111/eva.12480 ↗
9. Gamazo C, Prior S, Concepción LM et al (2007) Biodegradable gentamicin delivery systems for parenteral use for the treatment of intracellular bacterial infections. Expert Opin Drug Del 4:677–68810.1517/17425247.4.6.677 ↗
10. Zhou W, Jia ZJ, Xiong P et al (2017) Bioinspired and biomimetic AgNPs/gentamicin-embedded silk fibroin coatings for robust antibacterial and osteogenetic applications. ACS Appl Mater Interfaces 9:166–173
11. Tange RA, Dreschler WA, Prins JM, Buller HR, Kuijper EJ, Speelman P (1995) Ototoxicity and nephrotoxicity of gentamicin vs netilmicin in patients with serious infections. A randomized clinical trial. Clin Otolaryngol Allied Sci 20:118–12310.1111/j.1365-2273.1995.tb00026.x ↗
12. Pezzulo AA, Tang XX, Hoegger MJ et al (2012) Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 487:109–11310.1038/nature11130 ↗
13. Jiang YJ, Yang X, Zhu R, Hu K, Lan WW, Wu F, Yang LH (2013) Acid-activated antimicrobial random copolymers: a mechanism-guided design of antimicrobial peptide mimics. Macromolecules 46:3959–396410.1021/ma400484b ↗
14. Wang BL, Liu HH, Wang ZF et al (2017) A self-defensive antibacterial coating acting through the bacteria-triggered release of a hydrophobic antibiotic from layer-by-layer films. J Mater Chem B 5:1498–150610.1039/C6TB02614A ↗
15. Abed N, Couvreur P (2014) Nanocarriers for antibiotics: a promising solution to treat intracellular bacterial infections. Int J Antimicrob Agents 43:485–49610.1016/j.ijantimicag.2014.02.009 ↗
16. Lu E, Franzblau S, Onyuksela H, Popescua C (2009) Preparation of aminoglycoside loaded chitosan nanoparticles using dextran sulfate as a counterion. J Microencapsul 26:346–35410.1080/02652040802365182 ↗
17. Soliman GM, Szychowski J, Hanessian S, Winnik FM (2010) Robust polymeric nanoparticles for the delivery of aminoglycoside antibiotics using carboxymethyldextran-b-poly(ethyleneglycols) lightly grafted with n-dodecyl groups. Soft Matter 6:4504–451410.1039/c0sm00316f ↗
18. Alphandary HP, Andremont A, Couvreur P (2000) Targeted delivery of antibiotics using liposomes and nanoparticles: research and applications. Int J Antimicrob Agents 13:155–16810.1016/S0924-8579(99)00121-1 ↗
19. Wu YH, Long YB, Li QL, Han SY, Ma JB, Wang YW, Gao H (2015) Layer-by-layer (LBL) self-assembled biohybrid nanomaterials for efficient antibacterial applications. ACS Appl Mater Interfaces 7:17255–1726310.1021/acsami.5b04216 ↗
20. Abdelghany SM, Quinn DJ, Ingram RJ, Gilmore BF, Donnelly RF, Taggart CC, Scott CJ (2012) Gentamicin-loaded nanoparticles show improved antimicrobial effects towards Pseudomonas aeruginosa infection. Int J Nanomed 7:4053–4063
21. Zhang L, Pornpattananangku D, Hu CMJ, Huang CM (2010) Development of nanoparticles for antimicrobial drug delivery. Curr Med Chem 17:585–59410.2174/092986710790416290 ↗
22. Gao P, Nie X, Zou M, Shi YJ, Cheng G (2011) Recent advances in materials for extended-release antibiotic delivery system. J Antibiot 64:625–63410.1038/ja.2011.58 ↗
23. Fabrega J, Renshaw JC, Lead JR (2009) Interactions of silver nanoparticles with Pseudomonas putida biofilms. Environ Sci Technol 43:9004–900910.1021/es901706j ↗
24. Wu W, Wu ZH, Yu TY, Jiang CZ, Kim WS (2015) Recent progress on magnetic iron oxide nanoparticles: synthesis, surface functional strategies and biomedical applications. Sci Technol Adv Mater 16:23501–2354310.1088/1468-6996/16/2/023501 ↗
25. Mushtaq MW, Kanwal F, Batool A et al (2017) Polymer-coated CoFe2O4 nanoassemblies as biocompatible magnetic nanocarriers for anticancer drug delivery. J Mater Sci 52:9282–9293. https://doi.org/10.1007/s10853-017-1141-310.1007/s10853-017-1141-3 ↗
26. Mahmoudi M, Sant S, Wang B, Laurent S, Sen T (2011) Superparamagnetic iron oxide nanoparticles (SPIONs): development, surface modification and applications in chemotherapy. Adv Drug Deliv Rev 63:24–4610.1016/j.addr.2010.05.006 ↗
27. Mosaia T, Jeong CJ, Shin GJ et al (2013) Recyclable and stable silver deposited magnetic nanoparticles with poly (vinyl pyrrolidone)-catechol coated iron oxide for antimicrobial activity. Mat Sci Eng C Mater 33:3786–379410.1016/j.msec.2013.05.009 ↗
28. Wang CW, Xu SP, Zhang KH, Li M, Li QJ, Xiao R, Wang SQ (2017) Streptomycin-modified Fe3O4–Au@Ag core–satellite magnetic nanoparticles as an effective antibacterial agent. J Mater Sci 52:1357–1368. https://doi.org/10.1007/s10853-016-0430-610.1007/s10853-016-0430-6 ↗
29. Wang X, Cao WW, Xiang Q et al (2017) Silver nanoparticle and lysozyme/tannic acid layer-by-layer assembly antimicrobial multilayer on magnetic nanoparticle by an eco-friendly route. Mater Sci Eng C Mater 76:886–89610.1016/j.msec.2017.03.192 ↗
30. Yao QF, Gao YY, Gao TY et al (2016) Surface arming magnetic nanoparticles with amine N-halamines as recyclable antibacterial agents: construction and evaluation. Colloids Surf B 144:319–32610.1016/j.colsurfb.2016.04.024 ↗
31. Dong A, Sun Y, Lan S et al (2013) Barbituric acid-based magnetic N-halamine nanoparticles as recyclable antibacterial agents. ACS Appl Mater Interfaces 5:8125–813310.1021/am402191j ↗
32. Bromberg L, Chang EP, Lorenzo CA, Magariños B, Concheiro A, Hatton TA (2010) Binding of functionalized paramagnetic nanoparticles to bacterial lipopolysaccharides and DNA. Langmuir 26:8829–883510.1021/la904589p ↗
33. Bromberg L, Chang EP, Hatton TA, Concheiro A, Magarinos B, Lorenzo CA (2011) Bactericidal core-shell paramagnetic nanoparticles functionalized with poly(hexamethylene biguanide). Langmuir 27:420–42910.1021/la1039909 ↗
34. Dong HC, Huang JY, Koepsel RR, Ye PL, Russell AJ, Matyjaszewski K (2011) Recyclable antibacterial magnetic nanoparticles grafted with quaternized poly(2-(dimethylamino)ethyl methacrylate) brushes. Biomacromolecules 12:1305–131110.1021/bm200031v ↗
35. Wang X, Xiang Q, Cao WW, Jin F, Peng XF, Hu BC, Xing XD (2016) Fabrication of magnetic nanoparticles armed with quaternarized N-halamine polymers as recyclable antibacterial agents. J Biomater Sci Polym Ed 27:1909–192510.1080/09205063.2016.1239954 ↗
36. Durmus NG, Taylor EN, Kummer KM, Webster TJ (2013) Enhanced efficacy of superparamagnetic iron oxide nanoparticles against antibiotic-resistant biofilms in the presence of metabolites. Adv Mater 25:5706–571310.1002/adma.201302627 ↗
37. Durmus NG, Webster TJ (2013) Eradicating antibiotic-resistant biofilms with silver-conjugated superparamagnetic iron oxide nanoparticles. Adv Healthc Mater 2:165–17110.1002/adhm.201200215 ↗
38. Taylor EN, Kummer KM, Durmus NG, Leuba K, Tarquinio KM, Webster TJ (2012) Superparamagnetic iron oxide nanoparticles (SPION) for the treatment of antibiotic-resistant biofilms. Small 8:3016–302710.1002/smll.201200575 ↗
39. Taylor EN, Webster TJ (2011) Multifunctional magnetic nanoparticles for orthopedic and biofilm infections. Int J Nanotechnol 8:21–3510.1504/IJNT.2011.037168 ↗
40. Subbiahdoss G, Sharifi S, Grijpma DW, Laurent S, van der Mei HC, Mahmoudi M, Busscher HJ (2012) Magnetic targeting of surface-modified superparamagnetic iron oxide nanoparticles yields antibacterial efficacy against biofilms of gentamicin-resistant staphylococci. Acta Biomater 8:2047–205510.1016/j.actbio.2012.03.002 ↗
41. Geilich BM, Gelfat I, Sridhar S, van de Van AL, Webster TJ (2017) Superparamagnetic iron oxide-encapsulating polymersome nanocarriers for biofilm eradication. Biomaterials 119:78–8510.1016/j.biomaterials.2016.12.011 ↗
42. Zhuk I, Jariwala F, Attygalle AB, Wu Y, Libera MR, Sukhishvili SA (2014) Self-defensive layer-by-layer films with bacteria-triggered antibiotic release. ACS Nano 8:7733–774510.1021/nn500674g ↗
43. Occhipinti E, Verderio P, Natalello A et al (2011) Investigating the structural biofunctionality of antibodies conjugated to magnetic nanoparticles. Nanoscale 3:387–39010.1039/C0NR00436G ↗
44. Tamanna T, Bulitta JB, Yu A (2015) Controlling antibiotic release from mesoporous silica nano drug carriers via self-assembled polyelectrolyte coating. J Mater Sci Mater Med 26:117–124. https://doi.org/10.1007/s10856-015-5444-010.1007/s10856-015-5444-0 ↗
45. Dong A, Lan S, Huang JF et al (2011) Preparation of magnetically separable N-halamine nanocomposites for the improved antibacterial application. J Colloid Interface Sci 364:333–34010.1016/j.jcis.2011.08.036 ↗
46. Zhang S, Zhou YF, Nie WY, Song LY (2012) Preparation of Fe3O4/chitosan/poly (acrylic acid) composite particles and its application in adsorbing copper ion (II). Cellulose 19:2081–209110.1007/s10570-012-9783-4 ↗
47. Wang Y, Cui Y, Huang JH et al (2015) Redox and pH dual-responsive mesoporous silica nanoparticles for site-specific drug delivery. Appl Surf Sci 356:1282–128810.1016/j.apsusc.2015.07.151 ↗
48. Wu J, Wang YJ, Jiang W, Xu SS, Tian RB (2014) Synthesis and characterization of recyclable clusters of magnetic nanoparticles as doxorubicin carriers for cancer therapy. Appl Surf Sci 321:43–4910.1016/j.apsusc.2014.09.184 ↗
49. Jian J, Xian L, Sha Z, Liu J, Di DH, Zhang Y, Zhao QF, Wang SL (2016) Redox and pH dual-responsive PEG and chitosan-conjugated hollow mesoporous silica for controlled drug release. Mater Sci Eng C Mater 67:26–3310.1016/j.msec.2016.04.091 ↗
50. Wu J, Jiang W, Shen YW, Jiang W, Tian RB (2017) Synthesis and characterization of mesoporous magnetic nanocomposites wrapped with chitosan gatekeepers for pH-sensitive controlled release of doxorubicin. Mater Sci Eng C Mater 70:132–14010.1016/j.msec.2016.08.054 ↗
51. Lee HS, Dastgheyb SS, Hickok NJ, Eckmann DM, Composto RJ (2015) Targeted release of tobramycin from a pH-responsive grafted bilayer challenged with S. aureus. Biomacromolecules 16:650–65910.1021/bm501751v ↗
52. Siepmann J, Peppas NA (2012) Modeling of drug release from delivery systems based on hydroxypropyl methylcellulose (HPMC). Adv Drug Deliv Rev 64:163–17410.1016/j.addr.2012.09.028 ↗
53. Čolović B, Pašalić S, Jokanović V (2012) Influence of hydroxyapatite pore geometry on tigecycline release kinetics. Ceram Int 38:6181–618910.1016/j.ceramint.2012.04.069 ↗
54. Shoaib MH, Tazeen J, Merchant HA, Yousuf RI (2006) Evaluation of drug release kinetics from ibuprofen matrix tablets using HPMC. Pak J Pharm Sci 19:119–124
55. Liu XM, Sheng GP, Luo HW et al (2010) Contribution of extracellular polymeric substances (EPS) to the sludge aggregation. Environ Sci Technol 44:4355–436010.1021/es9016766 ↗
56. Aksungur P, Demirbilek M, Denkbas EB, Vandervoort J, Ludwig A, Unlu N (2011) Development and characterization of Cyclosporine A loaded nanoparticles for ocular drug delivery: cellular toxicity, uptake, and kinetic studies. J Control Release 151:286–29410.1016/j.jconrel.2011.01.010 ↗