Sonochemically-Produced Metal-Containing Polydopamine Nanoparticles and Their Antibacterial and Antibiofilm Activity

Langmuir

Volumn 32, Issue 20, 2016, Pages 5201-5212

  Yeroslavsky, Gil ^a   Lavi, Ronit ^a   Alishaev, Abraham ^b   Rahimipour, Shai ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b University of Miami College of Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CHELATION; HEAVY IONS; LEACHING; METAL NANOPARTICLES; METALS; NANOPARTICLES; PHYSIOLOGY; REDOX REACTIONS; SHELLS (STRUCTURES); SONOCHEMISTRY; SYNTHESIS (CHEMICAL);

ANTI-MICROBIAL ACTIVITY; BACTERICIDAL MECHANISMS; CORE SHELL STRUCTURE; MOUSE EMBRYONIC FIBROBLASTS; PHYSIOLOGICAL CONDITION; REACTIVE OXYGEN SPECIES; SONOCHEMICAL IRRADIATION; SONOCHEMICAL SYNTHESIS;

SILVER;

ANTIINFECTIVE AGENT; COPPER; INDOLE DERIVATIVE; NANOPARTICLE; POLYDOPAMINE; POLYMER; SILVER;

ANIMAL; BIOFILM; CHEMISTRY; DRUG EFFECT; MOUSE; NANOTECHNOLOGY; NIH 3T3 CELL LINE; PHYSIOLOGY; STAPHYLOCOCCUS AUREUS; SURFACE PROPERTY; ULTRASOUND;

ANIMALS; ANTI-BACTERIAL AGENTS; BIOFILMS; COPPER; INDOLES; MICE; NANOPARTICLES; NANOTECHNOLOGY; NIH 3T3 CELLS; POLYMERS; SILVER; STAPHYLOCOCCUS AUREUS; SURFACE PROPERTIES; ULTRASONIC WAVES;

EID: 84971300457     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/acs.langmuir.6b00576     Document Type: Article

References (64)

1. Shannon, K. P.; French, G. L. Increasing Resistance to Antimicrobial Agents of Gram-Negative Organisms Isolated at a London Teaching Hospital, 1995-2000 J. Antimicrob. Chemoth. 2004, 53, 818-825 10.1093/jac/dkh135
2. Lewis, K.; Klibanov, A. M. Surpassing Nature: Rational Design of Sterile-Surface Materials Trends Biotechnol. 2005, 23, 343-348 10.1016/j.tibtech.2005.05.004
3. Dueholm, M. S.; Sondergaard, M. T.; Nilsson, M.; Christiansen, G.; Stensballe, A.; Overgaard, M. T.; Givskov, M.; Tolker-Nielsen, T.; Otzen, D. E.; Nielsen, P. H. Expression of Fap Amyloids in Pseudomonas Aeruginosa, P. Fluorescens, and P. Putida Results in Aggregation and Increased Biofilm Formation MicrobiologyOpen 2013, 2, 365-382 10.1002/mbo3.81
4. Chopra, I. The Increasing Use of Silver-Based Products as Antimicrobial Agents: A Useful Development or a Cause for Concern? J. Antimicrob. Chemother. 2007, 59, 587-590 10.1093/jac/dkm006
5. Grass, G.; Rensing, C.; Solioz, M. Metallic Copper as an Antimicrobial Surface Appl. Environ. Microbiol. 2011, 77, 1541-1547 10.1128/AEM.02766-10
6. Feng, Q. L.; Wu, J.; Chen, G. Q.; Cui, F. Z.; Kim, T. N.; Kim, J. O. A Mechanistic Study of the Antibacterial Effect of Silver Ions on Escherichia Coli and Staphylococcus Aureus J. Biomed. Mater. Res. 2000, 52, 662-668 10.1002/1097-4636(20001215)52:4<662::AID-JBM10>3.0.CO;2-3
7. Le Ouay, B.; Stellacci, F. Antibacterial Activity of Silver Nanoparticles: A Surface Science Insight Nano Today 2015, 10, 339-354 10.1016/j.nantod.2015.04.002
8. Yoshida, Y.; Furuta, S.; Niki, E. Effects of Metal Chelating-Agents on the Oxidation of Lipids Induced by Copper and Iron Biochim. Biophys. Acta, Lipids Lipid Metab. 1993, 1210, 81-88 10.1016/0005-2760(93)90052-B
9. Dwyer, D. J.; Kohanski, M. A.; Collins, J. J. Role of Reactive Oxygen Species in Antibiotic Action and Resistance Curr. Opin. Microbiol. 2009, 12, 482-489 10.1016/j.mib.2009.06.018
10. Jaiswal, S.; McHale, P.; Duffy, B. Preparation and Rapid Analysis of Antibacterial Silver, Copper and Zinc Doped Sol-Gel Surfaces Colloids Surf., B 2012, 94, 170-176 10.1016/j.colsurfb.2012.01.035
11. Sureshkumar, M.; Siswanto, D. Y.; Lee, C. K. Magnetic Antimicrobial Nanocomposite Based on Bacterial Cellulose and Silver Nanoparticles J. Mater. Chem. 2010, 20, 6948-6955 10.1039/c0jm00565g
12. Liao, Y.; Wang, Y.; Feng, X.; Wang, W.; Xu, F.; Zhang, L. Antibacterial Surfaces through Dopamine Functionalization and Silver Nanoparticle Immobilization Mater. Chem. Phys. 2010, 121, 534-540 10.1016/j.matchemphys.2010.02.019
13. Lee, H.; Dellatore, S. M.; Miller, W. M.; Messersmith, P. B. Mussel-Inspired Surface Chemistry for Multifunctional Coatings Science 2007, 318, 426-430 10.1126/science.1147241
14. Dreyer, D. R.; Miller, D. J.; Freeman, B. D.; Paul, D. R.; Bielawski, C. W. Elucidating the Structure of Poly(Dopamine) Langmuir 2012, 28, 6428-6435 10.1021/la204831b
15. Hong, S.; Na, Y. S.; Choi, S.; Song, I. T.; Kim, W. Y.; Lee, H. Non-Covalent Self-Assembly and Covalent Polymerization Co-Contribute to Polydopamine Formation Adv. Funct. Mater. 2012, 22, 4711-4717 10.1002/adfm.201201156
16. Liebscher, J.; Mrowczynski, R.; Scheidt, H. A.; Filip, C.; Hadade, N. D.; Turcu, R.; Bende, A.; Beck, S. Structure of Polydopamine: A Never-Ending Story? Langmuir 2013, 29, 10539-10548 10.1021/la4020288
17. Bothner-By, A. A. Quinone-Hydroquinone Exchange Reactions. Ii. Duroquinone and Durohydroquinone Exchange in Buffered Methanol Solution J. Am. Chem. Soc. 1953, 75, 728-730 10.1021/ja01099a065
18. Mrowczynski, R.; Coy, L. E.; Scheibe, B.; Czechowski, T.; Augustyniak-Jablokow, M.; Jurga, S.; Tadyszak, K. Electron Paramagnetic Resonance Imaging and Spectroscopy of Polydopamine Radicals J. Phys. Chem. B 2015, 119, 10341-10347 10.1021/acs.jpcb.5b01524
19. Auten, R. L.; Davis, J. M. Oxygen Toxicity and Reactive Oxygen Species: The Devil Is in the Details Pediatr. Res. 2009, 66, 121-127 10.1203/PDR.0b013e3181a9eafb
20. Waite, J. H. Natures under Water Adhesive Specialist Int. J. Adhes. Adhes. 1987, 7, 9-14 10.1016/0143-7496(87)90048-0
21. Ye, Q.; Zhou, F.; Liu, W. M. Bioinspired Catecholic Chemistry for Surface Modification Chem. Soc. Rev. 2011, 40, 4244-4258 10.1039/c1cs15026j
22. Sun, K.; Xie, Y.; Ye, D.; Zhao, Y.; Cui, Y.; Long, F.; Zhang, W.; Jiang, X. Mussel-Inspired Anchoring for Patterning Cells Using Polydopamine Langmuir 2012, 28, 2131-2136 10.1021/la2041967
23. Nir, S.; Reches, M. Bio-Inspired Antifouling Approaches: The Quest Towards Non-Toxic and Non-Biocidal Materials Curr. Opin. Biotechnol. 2016, 39, 48-55 10.1016/j.copbio.2015.12.012
24. Ball, V. Activity of Alkaline Phosphatase Adsorbed and Grafted on Polydopamine Films J. Colloid Interface Sci. 2014, 429, 1-7 10.1016/j.jcis.2014.05.002
25. Ren, Y. H.; Rivera, J. G.; He, L. H.; Kulkarni, H.; Lee, D. K.; Messersmith, P. B. Facile, High Efficiency Immobilization of Lipase Enzyme on Magnetic Iron Oxide Nanoparticles Via a Biomimetic Coating BMC Biotechnol. 2011, 11, 63 10.1186/1472-6750-11-63
26. Zhang, R.-l.; Xu, S.; Luo, J.; Shi, D.-j.; Liu, C.; Liu, X.-y. One-Pot Green Synthesis of Nanohybrid Structures: Gold Nanoparticles in Poly(Gamma-Glutamic Acid) Copolymer Nanoparticles RSC Adv. 2014, 4, 25106-25113 10.1039/c4ra01094a
27. Shalev, T.; Gopin, A.; Bauer, M.; Stark, R. W.; Rahimipour, S. Non-Leaching Antimicrobial Surfaces through Polydopamine Bio-Inspired Coating of Quaternary Ammonium Salts or an Ultrashort Antimicrobial Lipopeptide J. Mater. Chem. 2012, 22, 2026-2032 10.1039/C1JM13994K
28. Yeroslavsky, G.; Girshevitz, O.; Foster-Frey, J.; Donovan, D. M.; Rahimipour, S. Antibacterial and Antibiofilm Surfaces through Polydopamine-Assisted Immobilization of Lysostaphin as an Antibacterial Enzyme Langmuir 2015, 31, 1064-1073 10.1021/la503911m
29. Yu, B.; Wang, D. A.; Ye, Q.; Zhou, F.; Liu, W. Robust Polydopamine Nano/Microcapsules and Their Loading and Release Behavior Chem. Commun. 2009, 6789-6791 10.1039/b910679k
30. Postma, A.; Yan, Y.; Wang, Y.; Zelikin, A. N.; Tjipto, E.; Caruso, F. Self-Polymerization of Dopamine as a Versatile and Robust Technique to Prepare Polymer Capsules Chem. Mater. 2009, 21, 3042-3044 10.1021/cm901293e
31. Zhang, Y.; Teo, B. M.; Goldie, K. N.; Stadler, B. Poly(N-Isopropylacrylamide)/Poly(Dopamine) Capsules Langmuir 2014, 30, 5592-5598 10.1021/la5005227
32. Zhang, L.; Wu, J.; Wang, Y.; Long, Y.; Zhao, N.; Xu, J. Combination of Bioinspiration: A General Route to Superhydrophobic Particles J. Am. Chem. Soc. 2012, 134, 9879-9881 10.1021/ja303037j
33. Yeroslavsky, G.; Richman, M.; Dawidowicz, L. O.; Rahimipour, S. Sonochemically Produced Polydopamine Nanocapsules with Selective Antimicrobial Activity Chem. Commun. 2013, 49, 5721-5723 10.1039/c3cc37762h
34. Skirtenko, N.; Richman, M.; Nitzan, Y.; Gedanken, A.; Rahimipour, S. A Facile One-Pot Sonochemical Synthesis of Surface-Coated Mannosyl Protein Microspheres for Detection and Killing of Bacteria Chem. Commun. 2011, 47, 12277-12279 10.1039/c1cc13518j
35. Avivi, S.; Felner, I.; Novik, I.; Gedanken, A. The Preparation of Magnetic Proteinaceous Microspheres Using the Sonochemical Method Biochim. Biophys. Acta, Gen. Subj. 2001, 1527, 123-129 10.1016/S0304-4165(01)00154-4
36. Shimanovich, U.; Eliaz, D.; Zigdon, S.; Volkov, V.; Aizer, A.; Cavaco-Paulo, A.; Michaeli, S.; Shav-Tal, Y.; Gedanken, A. Proteinaceous Microspheres for Targeted Rna Delivery Prepared by an Ultrasonic Emulsification Method J. Mater. Chem. B 2013, 1, 82-90 10.1039/C2TB00012A
37. Stepanovic, S.; Vukovic, D.; Dakic, I.; Savic, B.; Svabic-Vlahovic, M. A Modified Microtiter-Plate Test for Quantification of Staphylococcal Biofilm Formation J. Microbiol. Methods 2000, 40, 175-179 10.1016/S0167-7012(00)00122-6
38. de Avila, E. D.; Lima, B. P.; Sekiya, T.; Torii, Y.; Ogawa, T.; Shi, W.; Lux, R. Effect of Uv-Photofunctionalization on Oral Bacterial Attachment and Biofilm Formation to Titanium Implant Material Biomaterials 2015, 67, 84-92 10.1016/j.biomaterials.2015.07.030
39. Keston, A. S.; Brandt, R. The Fluorometric Analysis of Ultramicro Quantities of Hydrogen Peroxide Anal. Biochem. 1965, 11, 1-5 10.1016/0003-2697(65)90034-5
40. Hong, L.; Simon, J. D. Current Understanding of the Binding Sites, Capacity, Affinity, and Biological Significance of Metals in Melanin J. Phys. Chem. B 2007, 111, 7938-7947 10.1021/jp071439h
41. Ball, V.; Gracio, J.; Vila, M.; Singh, M. K.; Metz-Boutigue, M. H.; Michel, M.; Bour, J.; Toniazzo, V.; Ruch, D.; Buehler, M. J. Comparison of Synthetic Dopamine-Eumelanin Formed in the Presence of Oxygen and Cu2+ Cations as Oxidants Langmuir 2013, 29, 12754-12761 10.1021/la4029782
42. Bernsmann, F.; Ball, V.; Addiego, F.; Ponche, A.; Michel, M.; Gracio, J. J.; Toniazzo, V.; Ruch, D. Dopamine-Melanin Film Deposition Depends on the Used Oxidant and Buffer Solution Langmuir 2011, 27, 2819-2825 10.1021/la104981s
43. Leopold, N.; Lendl, B. A New Method for Fast Preparation of Highly Surface-Enhanced Raman Scattering (Sers) Active Silver Colloids at Room Temperature by Reduction of Silver Nitrate with Hydroxylamine Hydrochloride J. Phys. Chem. B 2003, 107, 5723-5727 10.1021/jp027460u
44. Aslan, K.; Leonenko, Z.; Lakowicz, J. R.; Geddes, C. D. Annealed Silver-Island Films for Applications in Metal-Enhanced Fluorescence: Interpretation in Terms of Radiating Plasmons J. Fluoresc. 2005, 15, 643-654 10.1007/s10895-005-2970-z
45. Rice, K. C.; Mann, E. E.; Endres, J. L.; Weiss, E. C.; Cassat, J. E.; Smeltzer, M. S.; Bayles, K. W. The Cida Murein Hydrolase Regulator Contributes to DNA Release and Biofilm Development in Staphylococcus Aureus Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 8113-8118 10.1073/pnas.0610226104
46. Donlan, R. M.; Costerton, J. W. Biofilms: Survival Mechanisms of Clinically Relevant Microorganisms Clin. Microbiol. Rev. 2002, 15, 167-193 10.1128/CMR.15.2.167-193.2002
47. Bjarnsholt, T.; Jensen, P. O.; Burmolle, M.; Hentzer, M.; Haagensen, J. A.; Hougen, H. P.; Calum, H.; Madsen, K. G.; Moser, C.; Molin, S.; Hoiby, N.; Givskov, M. Pseudomonas Aeruginosa Tolerance to Tobramycin, Hydrogen Peroxide and Polymorphonuclear Leukocytes Is Quorum-Sensing Dependent Microbiology 2005, 151, 373-383
48. Baker, J.; Sitthisak, S.; Sengupta, M.; Johnson, M.; Jayaswal, R. K.; Morrissey, J. A. Copper Stress Induces a Global Stress Response in Staphylococcus Aureus and Represses Sae and Agr Expression and Biofilm Formation Appl. Environ. Microbiol. 2010, 76, 150-160 10.1128/AEM.02268-09
49. Hwang, E. T.; Lee, J. H.; Chae, Y. J.; Kim, Y. S.; Kim, B. C.; Sang, B. I.; Gu, M. B. Analysis of the Toxic Mode of Action of Silver Nanoparticles Using Stress-Specific Bioluminescent Bacteria Small 2008, 4, 746-750 10.1002/smll.200700954
50. Korytowski, W.; Sarna, T. Bleaching of Melanin Pigments. Role of Copper Ions and Hydrogen Peroxide in Autooxidation and Photooxidation of Synthetic Dopa-Melanin J. Biol. Chem. 1990, 265, 12410-12416
51. Sarna, T.; Hyde, J. S.; Swartz, H. M. Ion-Exchange in Melanin: An Electron Spin Resonance Study with Lanthanide Probes Science 1976, 192, 1132-1134 10.1126/science.179142
52. Zhao, H.; Joseph, J.; Zhang, H.; Karoui, H.; Kalyanaraman, B. Synthesis and Biochemical Applications of a Solid Cyclic Nitrone Spin Trap: A Relatively Superior Trap for Detecting Superoxide Anions and Glutathiyl Radicals Free Radical Biol. Med. 2001, 31, 599-606 10.1016/S0891-5849(01)00619-0
53. Buettner, G. R.; Mason, R. P. Spin-Trapping Methods for Detecting Superoxide and Hydroxyl Free Radicals in Vitro and in Vivo Methods Enzymol. 1990, 186, 127-133 10.1016/0076-6879(90)86101-Z
54. Finkelstein, E.; Rosen, G. M.; Rauckman, E. J. Production of Hydroxyl Radical by Decomposition of Superoxide Spin-Trapped Adducts Mol. Pharmacol. 1982, 21, 262-265
55. Applerot, G.; Lellouche, J.; Lipovsky, A.; Nitzan, Y.; Lubart, R.; Gedanken, A.; Banin, E. Understanding the Antibacterial Mechanism of Cuo Nanoparticles: Revealing the Route of Induced Oxidative Stress Small 2012, 8, 3326-3337 10.1002/smll.201200772
56. Khachatryan, L.; Vejerano, E.; Lomnicki, S.; Dellinger, B. Environmentally Persistent Free Radicals (Epfrs). 1. Generation of Reactive Oxygen Species in Aqueous Solutions Environ. Sci. Technol. 2011, 45, 8559-8566 10.1021/es201309c
57. Lomnicki, S.; Truong, H.; Vejerano, E.; Dellinger, B. Copper Oxide-Based Model of Persistent Free Radical Formation on Combustion-Derived Particulate Matter Environ. Sci. Technol. 2008, 42, 4982-4988 10.1021/es071708h
58. Colvin, V. L. The Potential Environmental Impact of Engineered Nanomaterials Nat. Biotechnol. 2003, 21, 1166-1170 10.1038/nbt875
59. Kim, S.; Choi, J. E.; Choi, J.; Chung, K. H.; Park, K.; Yi, J.; Ryu, D. Y. Oxidative Stress-Dependent Toxicity of Silver Nanoparticles in Human Hepatoma Cells Toxicol. In Vitro 2009, 23, 1076-1084 10.1016/j.tiv.2009.06.001
60. Hussain, S. M.; Hess, K. L.; Gearhart, J. M.; Geiss, K. T.; Schlager, J. J. In Vitro Toxicity of Nanoparticles in Brl 3a Rat Liver Cells Toxicol. In Vitro 2005, 19, 975-983 10.1016/j.tiv.2005.06.034
61. Chung, Y. C.; Chen, I. H.; Chen, C. J. The Surface Modification of Silver Nanoparticles by Phosphoryl Disulfides for Improved Biocompatibility and Intracellular Uptake Biomaterials 2008, 29, 1807-1816 10.1016/j.biomaterials.2007.12.032
62. Travan, A.; Pelillo, C.; Donati, I.; Marsich, E.; Benincasa, M.; Scarpa, T.; Semeraro, S.; Turco, G.; Gennaro, R.; Paoletti, S. Non-Cytotoxic Silver Nanoparticle-Polysaccharide Nanocomposites with Antimicrobial Activity Biomacromolecules 2009, 10, 1429-1435 10.1021/bm900039x
63. Nymark, P.; Catalan, J.; Suhonen, S.; Jarventaus, H.; Birkedal, R.; Clausen, P. A.; Jensen, K. A.; Vippola, M.; Savolainen, K.; Norppa, H. Genotoxicity of Polyvinylpyrrolidone-Coated Silver Nanoparticles in Beas 2b Cells Toxicology 2013, 313, 38-48 10.1016/j.tox.2012.09.014
64. Lee, Y. H.; Cheng, F. Y.; Chiu, H. W.; Tsai, J. C.; Fang, C. Y.; Chen, C. W.; Wang, Y. J. Cytotoxicity, Oxidative Stress, Apoptosis and the Autophagic Effects of Silver Nanoparticles in Mouse Embryonic Fibroblasts Biomaterials 2014, 35, 4706-4715 10.1016/j.biomaterials.2014.02.021