Surface-Adaptive Gold Nanoparticles with Effective Adherence and Enhanced Photothermal Ablation of Methicillin-Resistant Staphylococcus aureus Biofilm

ACS Nano

Volumn 11, Issue 9, 2017, Pages 9330-9339

  Hu, Dengfeng ^a   Li, Huan ^a   Wang, Bailiang ^b   Ye, Zi ^b   Lei, Wenxi ^a   Jia, Fan ^a   Jin, Qiao ^a   Ren, Ke Feng ^a   Ji, Jian ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

biofilm; gold nanoparticles; mixed charged zwitterion; pH responsive; photothermal therapy

Indexed keywords

ABLATION; BACTERIA; FIBER OPTIC SENSORS; GOLD; HEALTH RISKS; HISTOLOGY; INFRARED DEVICES; IRRADIATION; METAL NANOPARTICLES; NANOPARTICLES; SELF ASSEMBLED MONOLAYERS; SURFACE TREATMENT; TISSUE;

11-MERCAPTOUNDECANOIC ACID; ACIDIC MICROENVIRONMENT; GOLD NANOPARTICLES; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MIXED CHARGED ZWITTERION; PH-RESPONSIVE; PHOTOTHERMAL THERAPY; RESISTANCE TO ANTIBIOTICS;

BIOFILMS;

ANTIINFECTIVE AGENT; GOLD; METAL NANOPARTICLE;

ANIMAL; BIOFILM; CHEMISTRY; DELAYED RELEASE FORMULATION; DRUG EFFECT; HUMAN; INFRARED RADIATION; LEPORIDAE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; PH; PHYSIOLOGY; PROCEDURES; RADIATION RESPONSE; STAPHYLOCOCCUS INFECTION; THERMOTHERAPY;

ANIMALS; ANTI-BACTERIAL AGENTS; BIOFILMS; DELAYED-ACTION PREPARATIONS; GOLD; HUMANS; HYDROGEN-ION CONCENTRATION; HYPERTHERMIA, INDUCED; INFRARED RAYS; METAL NANOPARTICLES; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; RABBITS; STAPHYLOCOCCAL INFECTIONS;

EID: 85029925321     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.7b04731     Document Type: Article

References (57)

1. Costerton, J. W.; Stewart, P. S.; Greenberg, E. P. Bacterial Biofilms: A Common Cause of Persistent Infections Science 1999, 284, 1318-1322 10.1126/science.284.5418.1318
2. Ladd, A. P.; Levy, M. S.; Quilty, J. Minimally Invasive Technique in Treatment of Complex, Subcutaneous Abscesses in Children J. Pediatr. Surg. 2010, 45, 1562-1566 10.1016/j.jpedsurg.2010.03.025
3. Andersson, D. I.; Hughes, D. Antibiotic Resistance and Its Cost: Is It Possible to Reverse Resistance? Nat. Rev. Microbiol. 2010, 8, 260-271 10.1038/nrmicro2319
4. Aminov, R. I. The Role of Antibiotics and Antibiotic Resistance in Nature Environ. Microbiol. 2009, 11, 2970-2988 10.1111/j.1462-2920.2009.01972.x
5. Abee, T.; Kovacs, A. T.; Kuipers, O. P.; van der Veen, S. Biofilm Formation and Dispersal in Gram-Positive Bacteria Curr. Opin. Biotechnol. 2011, 22, 172-179 10.1016/j.copbio.2010.10.016
6. Chua, S. L.; Liu, Y.; Yam, J. K.; Chen, Y.; Vejborg, R. M.; Tan, B. G.; Kjelleberg, S.; Tolker-Nielsen, T.; Givskov, M.; Yang, L. Dispersed Cells Represent a Distinct Stage in the Transition from Bacterial Biofilm to Planktonic Lifestyles Nat. Commun. 2014, 5, 4462 10.1038/ncomms5462
7. Davies, D. Understanding Biofilm Resistance to Antibacterial Agents Nat. Rev. Drug Discovery 2003, 2, 114-122 10.1038/nrd1008
8. Hall-Stoodley, L.; Costerton, J. W.; Stoodley, P. Bacterial Biofilms: From the Natural Environment to Infectious Diseases Nat. Rev. Microbiol. 2004, 2, 95-108 10.1038/nrmicro821
9. Yang, L.; Liu, Y.; Wu, H.; Song, Z.; Hoiby, N.; Molin, S.; Givskov, M. Combating Biofilms FEMS Immunol. Med. Microbiol. 2012, 65, 146-157 10.1111/j.1574-695X.2011.00858.x
10. Davies, D. G.; Marques, C. N. A Fatty Acid Messenger Is Responsible for Inducing Dispersion in Microbial Biofilms J. Bacteriol. 2009, 191, 1393-1403 10.1128/JB.01214-08
11. Randal Bollinger, R.; Barbas, A. S.; Bush, E. L.; Lin, S. S.; Parker, W. Biofilms in the Large Bowel Suggest an Apparent Function of the Human Vermiform Appendix J. Theor. Biol. 2007, 249, 826-831 10.1016/j.jtbi.2007.08.032
12. Spoering, A. L.; Lewis, K. Biofilms and Planktonic Cells of Pseudomonas Aeruginosa Have Similar Resistance to Killing by Antimicrobials J. Bacteriol. 2001, 183, 6746-6751 10.1128/JB.183.23.6746-6751.2001
13. Stoodley, P.; Debeer, D.; Lewandowski, Z. Liquid Flow in Biofilm Systems Appl. Environ. Microbiol. 1994, 60, 2711-2716
14. Gu, H. W.; Ho, P. L.; Tong, E.; Wang, L.; Xu, B. Presenting Vancomycin on Nanoparticles to Enhance Antimicrobial Activities Nano Lett. 2003, 3, 1261-1263 10.1021/nl034396z
15. Zhao, Y. Y.; Tian, Y.; Cui, Y.; Liu, W. W.; Ma, W. S.; Jiang, X. Y. Small Molecule-Capped Gold Nanoparticles as Potent Antibacterial Agents That Target Gram-Negative Bacteria J. Am. Chem. Soc. 2010, 132, 12349-12356 10.1021/ja1028843
16. Qi, X.; Zhou, C.; Li, P.; Xu, W.; Cao, Y.; Ling, H.; Ning Chen, W.; Ming, L. C.; Xu, R.; Lamrani, M.; Mu, Y.; Leong, S. S.; Wook Chang, M.; Chan-Park, M. B. Novel Short Antibacterial and Antifungal Peptides with Low Cytotoxicity: Efficacy and Action Mechanisms Biochem. Biophys. Res. Commun. 2010, 398, 594-600 10.1016/j.bbrc.2010.06.131
17. Saravanan, R.; Li, X.; Lim, K.; Mohanram, H.; Peng, L.; Mishra, B.; Basu, A.; Lee, J. M.; Bhattacharjya, S.; Leong, S. S. Design of Short Membrane Selective Antimicrobial Peptides Containing Tryptophan and Arginine Residues for Improved Activity, Salt-Resistance, and Biocompatibility Biotechnol. Bioeng. 2014, 111, 37-49 10.1002/bit.25003
18. Pu, Y.; Hou, Z.; Khin, M. M.; Zamudio-Vazquez, R.; Poon, K. L.; Duan, H.; Chan-Park, M. B. Synthesis and Antibacterial Study of Sulfobetaine/Quaternary Ammonium-Modified Star-Shaped Poly[2-(dimethylamino)ethyl methacrylate]-Based Copolymers with an Inorganic Core Biomacromolecules 2017, 18, 44-55 10.1021/acs.biomac.6b01279
19. Su, Y.; Tian, L.; Yu, M.; Gao, Q.; Wang, D.; Xi, Y.; Yang, P.; Lei, B.; Ma, P. X.; Li, P. Cationic Peptidopolysaccharides Synthesized by â€Click' Chemistry with Enhanced Broad-Spectrum Antimicrobial Activities Polym. Chem. 2017, 8, 3788-3800 10.1039/C7PY00528H
20. Li, P.; Poon, Y. F.; Li, W.; Zhu, H. Y.; Yeap, S. H.; Cao, Y.; Qi, X.; Zhou, C.; Lamrani, M.; Beuerman, R. W.; Kang, E. T.; Mu, Y.; Li, C. M.; Chang, M. W.; Leong, S. S.; Chan-Park, M. B. A Polycationic Antimicrobial and Biocompatible Hydrogel with Microbe Membrane Suctioning Ability Nat. Mater. 2011, 10, 149-156 10.1038/nmat2915
21. Gao, Q.; Yu, M.; Su, Y.; Xie, M.; Zhao, X.; Li, P.; Ma, P. X. Rationally Designed Dual Functional Block Copolymers for Bottlebrush-like Coatings: in vitro and in Vivo Antimicrobial, Antibiofilm, and Antifouling Properties Acta Biomater. 2017, 51, 112-124 10.1016/j.actbio.2017.01.061
22. Gu, J.; Su, Y.; Liu, P.; Li, P.; Yang, P. An Environmentally Benign Antimicrobial Coating Based on a Protein Supramolecular Assembly ACS Appl. Mater. Interfaces 2017, 9, 198-210 10.1021/acsami.6b13552
23. Su, Y.; Zhi, Z.; Gao, Q.; Xie, M.; Yu, M.; Lei, B.; Li, P.; Ma, P. X. Autoclaving-Derived Surface Coating with in Vitro and in Vivo Antimicrobial and Antibiofilm Efficacies Adv. Healthcare Mater. 2017, 6, 1601173 10.1002/adhm.201601173
24. Zhi, Z.; Su, Y.; Xi, Y.; Tian, L.; Xu, M.; Wang, Q.; Padidan, S.; Li, P.; Huang, W. Dual-Functional Polyethylene Glycol-b-Polyhexanide Surface Coating with in Vitro and in Vivo Antimicrobial and Antifouling Activities ACS Appl. Mater. Interfaces 2017, 9, 10383-10397 10.1021/acsami.6b12979
25. Bruenke, J.; Roschke, I.; Agarwal, S.; Riemann, T.; Greiner, A. Quantitative Comparison of the Antimicrobial Efficiency of Leaching versus Nonleaching Polymer Materials Macromol. Biosci. 2016, 16, 647-654 10.1002/mabi.201500266
26. Mattheis, C.; Wang, H.; Meister, C.; Agarwal, S. Effect of Guanidinylation on the Properties of Poly(2-aminoethylmethacrylate)-based Antibacterial Materials Macromol. Biosci. 2013, 13, 242-255 10.1002/mabi.201200217
27. Mattheis, C.; Zhang, Y.; Agarwal, S. Thermo-Switchable Antibacterial Activity Macromol. Biosci. 2012, 12, 1401-1412 10.1002/mabi.201200207
28. Tan, L.; Maji, S.; Mattheis, C.; Zheng, M.; Chen, Y.; Caballero-Diaz, E.; Gil, P. R.; Parak, W. J.; Greiner, A.; Agarwal, S. Antimicrobial Hydantoin-Containing Polyesters Macromol. Biosci. 2012, 12, 1068-1076 10.1002/mabi.201100520
29. Liu, R.; Chen, X.; Chakraborty, S.; Lemke, J. J.; Hayouka, Z.; Chow, C.; Welch, R. A.; Weisblum, B.; Masters, K. S.; Gellman, S. H. Tuning the Biological Activity Profile of Antibacterial Polymers via Subunit Substitution Pattern J. Am. Chem. Soc. 2014, 136, 4410-4418 10.1021/ja500367u
30. Liu, R.; Chen, X.; Falk, S. P.; Masters, K. S.; Weisblum, B.; Gellman, S. H. Nylon-3 Polymers Active Against Drug-Resistant Candida Albicans Biofilms J. Am. Chem. Soc. 2015, 137, 2183-2186 10.1021/ja512567y
31. Liu, C.; Liu, B.; Chan-Park, M. B. Synthesis of Polycaprolactone-Polyimide-Polycaprolactone Triblock Copolymers via a 2-Step Sequential Copolymerization and Their Application as Carbon Nanotube Dispersants Polym. Chem. 2017, 8, 674-681 10.1039/C6PY01933A
32. Liu, R.; Chen, X.; Falk, S. P.; Mowery, B. P.; Karlsson, A. J.; Weisblum, B.; Palecek, S. P.; Masters, K. S.; Gellman, S. H. Structure-Activity Relationships among Antifungal Nylon-3 Polymers: Identification of Materials Active Against Drug-Resistant Strains of Candida Albicans J. Am. Chem. Soc. 2014, 136, 4333-4342 10.1021/ja500036r
33. Bakhshi, H.; Agarwal, S. Dendrons as Active Clicking Tool for Generating Non-Leaching Antibacterial Materials Polym. Chem. 2016, 7, 5322-5330 10.1039/C6PY01105E
34. Hauenstein, O.; Agarwal, S.; Greiner, A. Bio-Based Polycarbonate as Synthetic Toolbox Nat. Commun. 2016, 7, 11862 10.1038/ncomms11862
35. Landis, R. F.; Gupta, A.; Lee, Y. W.; Wang, L. S.; Golba, B.; Couillaud, B.; Ridolfo, R.; Das, R.; Rotello, V. M. Cross-Linked Polymer-Stabilized Nanocomposites for the Treatment of Bacterial Biofilms ACS Nano 2017, 11, 946-952 10.1021/acsnano.6b07537
36. Wang, J.; Nguyen, T. D.; Cao, Q.; Wang, Y.; Tan, M. Y.; Chan-Park, M. B. Selective Surface Charge Sign Reversal on Metallic Carbon Nanotubes for Facile Ultrahigh Purity Nanotube Sorting ACS Nano 2016, 10, 3222-3232 10.1021/acsnano.5b05795
37. Xing, C.; Yang, G.; Liu, L.; Yang, Q.; Lv, F.; Wang, S. Conjugated Polymers for Light-Activated Antifungal Activity Small 2012, 8, 524-529 10.1002/smll.201290023
38. Yuan, H.; Chong, H.; Wang, B.; Zhu, C.; Liu, L.; Yang, Q.; Lv, F.; Wang, S. Chemical Molecule-Induced Light-Activated System for Anticancer and Antifungal Activities J. Am. Chem. Soc. 2012, 134, 13184-13187 10.1021/ja304986t
39. Hsiao, C. W.; Chen, H. L.; Liao, Z. X.; Sureshbabu, R.; Hsiao, H. C.; Lin, S. J.; Chang, Y.; Sung, H. W. Effective Photothermal Killing of Pathogenic Bacteria by Using Spatially Tunable Colloidal Gels with Nano-Localized Heating Sources Adv. Funct. Mater. 2015, 25, 721-728 10.1002/adfm.201403478
40. Zharov, V. P.; Mercer, K. E.; Galitovskaya, E. N.; Smeltzer, M. S. Photothermal Nanotherapeutics and Nanodiagnostics for Selective Killing of Bacteria Targeted with Gold Nanoparticles Biophys. J. 2006, 90, 619-627 10.1529/biophysj.105.061895
41. Park, S. J.; Kang, E. B.; Sharker, S. M.; Lee, G.; In, I.; Park, S. Y. NIR-Mediated Antibacterial Clay Nanocomposites: Exfoliation of Montmorillonite Nanolayers by IR825 Intercalation Macromol. Mater. Eng. 2016, 301, 141-148 10.1002/mame.201500272
42. Wu, M. C.; Deokar, A. R.; Liao, J. H.; Shih, P. Y.; Ling, Y. C. Graphene-Based Photothermal Agent for Rapid and Effective Killing of Bacteria ACS Nano 2013, 7, 1281-1290 10.1021/nn304782d
43. 4@Au Nanoeggs as Photothermal Agents for Selective Killing of Nosocomial and Antibiotic-Resistant Bacteria Small 2009, 5, 51-56 10.1002/smll.200801042
44. Dong, K.; Ju, E.; Gao, N.; Wang, Z.; Ren, J.; Qu, X. Synergistic Eradication of Antibiotic-Resistant Bacteria Based Biofilms in Vivo Using a NIR-Sensitive Nanoplatform Chem. Commun. 2016, 52, 5312-5315 10.1039/C6CC00774K
45. Zou, X.; Zhang, L.; Wang, Z.; Luo, Y. Mechanisms of the Antimicrobial Activities of Graphene Materials J. Am. Chem. Soc. 2016, 138, 2064-2077 10.1021/jacs.5b11411
46. Kim, S. H.; Kang, E. B.; Jeong, C. J.; Sharker, S. M.; In, I.; Park, S. Y. Light Controllable Surface Coating for Effective Photothermal Killing of Bacteria ACS Appl. Mater. Interfaces 2015, 7, 15600-15606 10.1021/acsami.5b04321
47. Bokern, S.; Gries, K.; Görtz, H.-H.; Warzelhan, V.; Agarwal, S.; Greiner, A. Precisely Designed Gold Nanoparticles by Surface Polymerization-Artificial Molecules as Building Blocks for Novel Materials Adv. Funct. Mater. 2011, 21, 3753-3759 10.1002/adfm.201100590
48. Mitschang, F.; Schmalz, H.; Agarwal, S.; Greiner, A. Tea-Bag-like Polymer Nanoreactors Filled with Gold Nanoparticles Angew. Chem., Int. Ed. 2014, 53, 4972-4975 10.1002/anie.201402212
49. Ramasamy, M.; Lee, S. S.; Yi, D. K.; Kim, K. Magnetic, Optical Gold Nanorods for Recyclable Photothermal Ablation of Bacteria J. Mater. Chem. B 2014, 2, 981-988 10.1039/c3tb21310b
50. Ray, P. C.; Khan, S. A.; Singh, A. K.; Senapati, D.; Fan, Z. Nanomaterials for Targeted Detection and Photothermal Killing of Bacteria Chem. Soc. Rev. 2012, 41, 3193-3209 10.1039/c2cs15340h
51. Yang, H.; Heng, X.; Hu, J. Salt- and pH-Resistant Gold Nanoparticles Decorated with Mixed-Charge Zwitterionic Ligands, and Their pH-induced Concentration Behavior RSC Adv. 2012, 2, 12648-12651 10.1039/c2ra22165a
52. Liu, X. S.; Chen, Y. J.; Li, H.; Huang, N.; Jin, Q.; Ren, K. F.; Ji, J. Enhanced Retention and Cellular Uptake of Nanoparticles in Tumors by Controlling Their Aggregation Behavior ACS Nano 2013, 7, 6244-6257 10.1021/nn402201w
53. Liu, Y.; Busscher, H. J.; Zhao, B.; Li, Y.; Zhang, Z.; van der Mei, H. C.; Ren, Y.; Shi, L. Surface-Adaptive, Antimicrobially Loaded, Micellar Nanocarriers with Enhanced Penetration and Killing Efficiency in Staphylococcal Biofilms ACS Nano 2016, 10, 4779-4789 10.1021/acsnano.6b01370
54. Zharov, V. P.; Galitovskaya, E. N.; Johnson, C.; Kelly, T. Synergistic Enhancement of Selective Nanophotothermolysis with Gold Nanoclusters: Potential for Cancer Therapy Lasers Surg. Med. 2005, 37, 219-226 10.1002/lsm.20223
55. Zharov, V. P.; Letfullin, R. R.; Galitovskaya, E. N. Microbubbles-Overlapping Mode for Laser Killing of Cancer Cells with Absorbing Nanoparticle Clusters J. Phys. D: Appl. Phys. 2005, 38, 2571-2581 10.1088/0022-3727/38/15/007
56. Liu, X.; Huang, H.; Jin, Q.; Ji, J. Mixed Charged Zwitterionic Self-Assembled Monolayers as A Facile Way to Stabilize Large Gold Nanoparticles Langmuir 2011, 27, 5242-5251 10.1021/la2002223
57. Zhang, P.; Li, S.; Chen, H.; Wang, X.; Liu, L.; Lv, F.; Wang, S. Biofilm Inhibition and Elimination Regulated by Cationic Conjugated Polymers ACS Appl. Mater. Interfaces 2017, 9, 16933-16938 10.1021/acsami.7b05227