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Surface-Adaptive, Antimicrobially Loaded, Micellar Nanocarriers with Enhanced Penetration and Killing Efficiency in Staphylococcal Biofilms
Abstract
Biofilms cause persistent bacterial infections and are extremely recalcitrant to antimicrobials, due in part to reduced penetration of antimicrobials into biofilms that allows bacteria residing in the depth of a biofilm to survive antimicrobial treatment. Here, we describe the preparation of surface-adaptive, Triclosan-loaded micellar nanocarriers showing (1) enhanced biofilm penetration and accumulation, (2) electrostatic targeting at acidic pH toward negatively charged bacterial cell surfaces in a biofilm, and (3) antimicrobial release due to degradation of the micelle core by bacterial lipases. First, it was established that mixed-shell-polymeric-micelles (MSPM) consisting of a hydrophilic poly(ethylene glycol) (PEG)-shell and pH-responsive poly(β-amino ester) become positively charged at pH 5.0, while being negatively charged at physiological pH. This is opposite to single-shell-polymeric-micelles (SSPM) possessing only a PEG-shell and remaining negatively charged at pH 5.0. The stealth properties of the PEG-shell combined with its surface-adaptive charge allow MSPMs to penetrate and accumulate in staphylococcal biofilms, as demonstrated for fluorescent Nile red loaded micelles using confocal-laser-scanning-microscopy. SSPMs, not adapting a positive charge at pH 5.0, could not be demonstrated to penetrate and accumulate in a biofilm. Once micellar nanocarriers are bound to a staphylococcal cell surface, bacterial enzymes degrade the MSPM core to release its antimicrobial content and kill bacteria over the depth of a biofilm. This constitutes a highly effective pathway to control blood-accessible staphylococcal biofilms using antimicrobials, bypassing biofilm recalcitrance to antimicrobial penetration.
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Citations
Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890
Bacterial Biofilms: A Common Cause of Persistent Infections
Costerton, J. W., Stewart, P. S., & Greenberg, E. P. (1999) · Science · doi:10.1126/science.284.5418.1318 · Cited by 12,167
Flemming, H.-C., & Wingender, J. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2415 · Cited by 10,137
Bacterial biofilms: from the Natural environment to infectious diseases
Hall-Stoodley, L., Costerton, J. W., & Stoodley, P. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro821 · Cited by 7,143
Stimuli-responsive nanocarriers for drug delivery
Mura, S., Nicolas, J., & Couvreur, P. (2013) · Nature Materials · doi:10.1038/nmat3776 · Cited by 6,289
Effect of pegylation on pharmaceuticals
Harris, J. M., & Chess, R. B. (2003) · Nature Reviews Drug Discovery · doi:10.1038/nrd1033 · Cited by 3,431
Impact of Nanotechnology on Drug Delivery
Farokhzad, O. C., & Langer, R. (2009) · ACS Nano · doi:10.1021/nn900002m · Cited by 3,348
Liu, S., Zeng, T. H., Hofmann, M., Burcombe, E., Wei, J., Jiang, R., Kong, J., & Chen, Y. (2011) · ACS Nano · doi:10.1021/nn202451x · Cited by 2,929
Understanding biofilm resistance to antibacterial agents
Davies, D. (2003) · Nature Reviews Drug Discovery · doi:10.1038/nrd1008 · Cited by 2,781
Polymeric systems for controlled drug release
Uhrich, K. E., Cannizzaro, S. M., Langer, R. S., & Shakesheff, K. M. (1999) · Chemical Reviews · doi:10.1021/cr940351u · Cited by 2,633
Toxicity of Graphene and Graphene Oxide Nanowalls Against Bacteria
Akhavan, O., & Ghaderi, E. (2010) · ACS Nano · doi:10.1021/nn101390x · Cited by 2,606
Silver as Antibacterial Agent: Ion, Nanoparticle, and Metal
Chernousova, S., & Epple, M. (2013) · Angewandte Chemie International Edition · doi:10.1002/anie.201205923 · Cited by 2,264
Multifunctional Magnetic Nanoparticles: Design, Synthesis, and Biomedical Applications
Gao, J., Gu, H., & Xu, B. (2009) · Accounts of Chemical Research · doi:10.1021/ar9000026 · Cited by 1,907
Huh, A. J., & Kwon, Y. J. (2011) · Journal of Controlled Release · doi:10.1016/j.jconrel.2011.07.002 · Cited by 1,864
Survival strategies of infectious biofilms
Fux, C. A., Costerton, J. W., Stewart, P. S., & Stoodley, P. (2005) · Trends in Microbiology · doi:10.1016/j.tim.2004.11.010 · Cited by 1,812
Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets
Tu, Y., Lv, M., Xiu, P., Huynh, T., Zhang, M., Castelli, M., Liu, Z., Huang, Q., Fan, C., Fang, H., et al. (2013) · Nature Nanotechnology · doi:10.1038/nnano.2013.125 · Cited by 1,508
Nanotechnology as a therapeutic tool to combat microbial resistance
Pelgrift, R. Y., & Friedman, A. J. (2013) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2013.07.011 · Cited by 1,432
Triclosan targets lipid synthesis
McMurry, L. M., Oethinger, M., & Levy, S. B. (1998) · Nature · doi:10.1038/28970 · Cited by 1,019
Triclosan: environmental exposure, toxicity and mechanisms of action
Dann, A. B., & Hontela, A. (2011) · Journal of Applied Toxicology · doi:10.1002/jat.1660 · Cited by 868
Enzyme-responsive polymeric assemblies, nanoparticles and hydrogels
Hu, J., Zhang, G., & Liu, S. (2012) · Chemical Society Reviews · doi:10.1039/c2cs35103j · Cited by 722
Biodegradable nanostructures with selective lysis of microbial membranes
Nederberg, F., Zhang, Y., Tan, J. P. K., Xu, K., Wang, H., Yang, C., Gao, S., Guo, X. D., Fukushima, K., Li, L., et al. (2011) · Nature Chemistry · doi:10.1038/nchem.1012 · Cited by 614
Zhao, Y., Tian, Y., Cui, Y., Liu, W., Ma, W., & Jiang, X. (2010) · Journal of the American Chemical Society · doi:10.1021/ja1028843 · Cited by 592
Liu, S., Wei, L., Hao, L., Fang, N., Chang, M. W., Xu, R., Yang, Y., & Chen, Y. (2009) · ACS Nano · doi:10.1021/nn901252r · Cited by 567
Radovic-Moreno, A. F., Lu, T. K., Puscasu, V. A., Yoon, C. J., Langer, R., & Farokhzad, O. C. (2012) · ACS Nano · doi:10.1021/nn3008383 · Cited by 539
Modulating Antibacterial Immunity via Bacterial Membrane-Coated Nanoparticles
Gao, W., Fang, R. H., Thamphiwatana, S., Luk, B. T., Li, J., Angsantikul, P., Zhang, Q., Hu, C.-M. J., & Zhang, L. (2015) · Nano Letters · doi:10.1021/nl504798g · Cited by 509
Tseng, B. S., Zhang, W., Harrison, J. J., Quach, T. P., Song, J. L., Penterman, J., Singh, P. K., Chopp, D. L., Packman, A. I., & Parsek, M. R. (2013) · Environmental Microbiology · doi:10.1111/1462-2920.12155 · Cited by 466
More Effective Nanomedicines through Particle Design
Wang, J., Byrne, J. D., Napier, M. E., & DeSimone, J. M. (2011) · Small · doi:10.1002/smll.201100442 · Cited by 466
Lipid and polymer nanoparticles for drug delivery to bacterial biofilms
Forier, K., Raemdonck, K., De Smedt, S. C., Demeester, J., Coenye, T., & Braeckmans, K. (2014) · Journal of Controlled Release · doi:10.1016/j.jconrel.2014.03.055 · Cited by 464
Gogoi, S. K., Gopinath, P., Paul, A., Ramesh, A., Ghosh, S. S., & Chattopadhyay, A. (2006) · Langmuir · doi:10.1021/la060661v · Cited by 446
Lipase-Sensitive Polymeric Triple-Layered Nanogel for “On-Demand” Drug Delivery
Xiong, M.-H., Bao, Y., Yang, X.-Z., Wang, Y.-C., Sun, B., & Wang, J. (2012) · Journal of the American Chemical Society · doi:10.1021/ja211279u · Cited by 361
Horev, B., Klein, M. I., Hwang, G., Li, Y., Kim, D., Koo, H., & Benoit, D. S. W. (2015) · ACS Nano · doi:10.1021/nn507170s · Cited by 340
Self-citationRodricks, J. V., Swenberg, J. A., Borzelleca, J. F., Maronpot, R. R., & Shipp, A. M. (2010) · Critical Reviews in Toxicology · doi:10.3109/10408441003667514 · Cited by 292
Core–Shell Supramolecular Gelatin Nanoparticles for Adaptive and “On-Demand” Antibiotic Delivery
Li, L.-L., Xu, J.-H., Qi, G.-B., Zhao, X., Yu, F., & Wang, H. (2014) · ACS Nano · doi:10.1021/nn501040h · Cited by 291
van Oosten, M., Schäfer, T., Gazendam, J. A. C., Ohlsen, K., Tsompanidou, E., de Goffau, M. C., Harmsen, H. J. M., Crane, L. M. A., Lim, E., Francis, K. P., et al. (2013) · Nature Communications · doi:10.1038/ncomms3584 · Cited by 289
Hydrogel Containing Nanoparticle-Stabilized Liposomes for Topical Antimicrobial Delivery
Gao, W., Vecchio, D., Li, J., Zhu, J., Zhang, Q., Fu, V., Li, J., Thamphiwatana, S., Lu, D., & Zhang, L. (2014) · ACS Nano · doi:10.1021/nn500110a · Cited by 249
Russell, A. D. (2004) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkh171 · Cited by 223
Antimicrobial delivery systems for local infection prophylaxis in orthopedic- and trauma surgery
ter Boo, G.-J. A., Grijpma, D. W., Moriarty, T. F., Richards, R. G., & Eglin, D. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.02.020 · Cited by 209
Foulston, L., Elsholz, A. K. W., DeFrancesco, A. S., & Losick, R. (2014) · mBio · doi:10.1128/mbio.01667-14 · Cited by 207
Rothenburger, S., Spangler, D., Bhende, S., & Burkley, D. (2002) · Surgical Infections · doi:10.1089/sur.2002.3.s1-79 · Cited by 180
Formation and enhanced biocidal activity of water-dispersable organic nanoparticles
Zhang, H., Wang, D., Butler, R., Campbell, N. L., Long, J., Tan, B., Duncalf, D. J., Foster, A. J., Hopkinson, A., Taylor, D., et al. (2008) · Nature Nanotechnology · doi:10.1038/nnano.2008.188 · Cited by 158
Durmus, N. G., Taylor, E. N., Kummer, K. M., & Webster, T. J. (2013) · Advanced Materials · doi:10.1002/adma.201302627 · Cited by 156
Nanomaterials for the Treatment of Bacterial Biofilms
Wang, L., Gupta, A., & Rotello, V. M. (2015) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.5b00116 · Cited by 156
Ng, V. W. L., Ke, X., Lee, A. L. Z., Hedrick, J. L., & Yang, Y. Y. (2013) · Advanced Materials · doi:10.1002/adma.201302952 · Cited by 153
Molecular Imaging of Inflammation/Infection: Nuclear Medicine and Optical Imaging Agents and Methods
Signore, A., Mather, S. J., Piaggio, G., Malviya, G., & Dierckx, R. A. (2010) · Chemical Reviews · doi:10.1021/cr900351r · Cited by 134
Zhang, Z., Ma, R., & Shi, L. (2014) · Accounts of Chemical Research · doi:10.1021/ar5000264 · Cited by 115
Self-citationLeewenhoeck, A. (1684) · Philosophical Transactions of the Royal Society of London · doi:10.1098/rstl.1684.0030 · Cited by 114
Lim, Y. H., Tiemann, K. M., Heo, G. S., Wagers, P. O., Rezenom, Y. H., Zhang, S., Zhang, F., Youngs, W. J., Hunstad, D. A., & Wooley, K. L. (2015) · ACS Nano · doi:10.1021/nn507046h · Cited by 99
Triclosan, cytotoxicity, mode of action, and induction of apoptosis in human gingival cells in vitro
Zuckerbraun, H. L., Babich, H., May, R. J., & Sinensky, M. C. (1998) · European Journal Of Oral Sciences · doi:10.1046/j.0909-8836.1998.eos106204.x · Cited by 81
The potential for bio-optical imaging of biomaterial-associated infection in vivo
Sjollema, J., Sharma, P. K., Dijkstra, R. J. B., van Dam, G. M., van der Mei, H. C., Engelsman, A. F., & Busscher, H. J. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.11.068 · Cited by 60
Self-citationSelf-Regulated Multifunctional Collaboration of Targeted Nanocarriers for Enhanced Tumor Therapy
Gao, H., Cheng, T., Liu, J., Liu, J., Yang, C., Chu, L., Zhang, Y., Ma, R., & Shi, L. (2014) · Biomacromolecules · doi:10.1021/bm5009348 · Cited by 51
Self-citationvan der Mei, H. C., White, D. J., Atema‐Smit, J., Belt‐Gritter, E. V. D., & Busscher, H. J. (2005) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2005.00859.x · Cited by 48
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Lamont, R. J., Koo, H., & Hajishengallis, G. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0089-x · Cited by 2,217
Polymeric Nanoparticles for Drug Delivery
Beach, M. A., Nayanathara, U., Gao, Y., Zhang, C., Xiong, Y., Wang, Y., & Such, G. K. (2024) · Chemical Reviews · doi:10.1021/acs.chemrev.3c00705 · Cited by 1,155
Nanotechnology-based antimicrobials and delivery systems for biofilm-infection control
Liu, Y., Shi, L., Su, L., van der Mei, H. C., Jutte, P. C., Ren, Y., & Busscher, H. J. (2019) · Chemical Society Reviews · doi:10.1039/c7cs00807d · Cited by 737
Self-citationHu, D., Li, H., Wang, B., Ye, Z., Lei, W., Jia, F., Jin, Q., Ren, K.-F., & Ji, J. (2017) · ACS Nano · doi:10.1021/acsnano.7b04731 · Cited by 565
Hu, D., Deng, Y., Jia, F., Jin, Q., & Ji, J. (2020) · ACS Nano · doi:10.1021/acsnano.9b05493 · Cited by 489
Metadata
- Authors
- Liu, Y., Busscher, H. J., Zhao, B., Li, Y., Zhang, Z., van der Mei, H. C., Ren, Y., & Shi, L.
- Venue
- ACS Nano
- Publisher
- American Chemical Society (ACS)
- Published
- 2016-03-24
- Volume
- 10
- Issue
- 4
- Pages
- 4779-4789
- ISSN
- 1936-0851 (ISSN-L)
- 1936-086X
- OpenAlex
- W2309290067
- Cited by
- 379
- References
- 51
- FWCI
- 13.54
- Type
- journal article
- Language
- en
- Open access
- closed
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