Bactericidal Effect of Gold-Chitosan Nanocomposites in Coculture Models of Pathogenic Bacteria and Human Macrophages

ACS Applied Materials and Interfaces

Volumn 9, Issue 21, 2017, Pages 17693-17701

  Mendoza, Gracia ^a,c   Regiel Futyra, Anna ^d   Andreu, Vanesa ^a,c   Sebastián, Víctor ^a,b,c   Kyzioł, Agnieszka ^d   Stochel, Grazyna ^d   Arruebo, Manuel ^a,b,c  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^c INSTITUTO ARAGONÉS DE CIENCIAS DE LA SALUD   (Spain)

^d JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

bactericidal nanomaterials; chitosan; gold nanoparticles; infection; nanocomposites

Indexed keywords

CELLS; CHITIN; CHITOSAN; CYTOLOGY; ESCHERICHIA COLI; GOLD; MACROPHAGES; MAMMALS; MICROORGANISMS; NANOCOMPOSITES; NANOSTRUCTURED MATERIALS; SCANNING ELECTRON MICROSCOPY; SELF ASSEMBLY;

ANTIMICROBIAL MATERIALS; BACTERICIDAL ABILITY; BACTERICIDAL EFFECTS; GOLD NANOPARTICLES; INFECTION; PATHOGENIC BACTERIUM; RESISTANCE MECHANISMS; STAPHYLOCOCCUS AUREUS;

BACTERIA;

ANTIINFECTIVE AGENT; CHITOSAN; GOLD; METAL NANOPARTICLE; NANOCOMPOSITE;

BACTERIUM; COCULTURE; HUMAN; MACROPHAGE;

ANTI-BACTERIAL AGENTS; BACTERIA; CHITOSAN; COCULTURE TECHNIQUES; GOLD; HUMANS; MACROPHAGES; METAL NANOPARTICLES; NANOCOMPOSITES;

EID: 85020037462     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.6b15123     Document Type: Article

References (54)

1. Nikaido, H. Multidrug Resistance in Bacteria Annu. Rev. Biochem. 2009, 78, 119-146 10.1146/annurev.biochem.78.082907.145923
2. Jena, P.; Mohanty, S.; Mallick, R.; Jacob, B.; Sonawane, A. Toxicity and Antibacterial Assessment of Chitosan-Coated Silver Nanoparticles on Human Pathogens and Macrophage Cells Int. J. Nanomed. 2012, 7, 1805-1818 10.2147/IJN.S28077
3. He, M.; Miyajima, F.; Roberts, P.; Ellison, L.; Pickard, D. J.; Martin, M. J.; Connor, T. R.; Harris, S. R.; Fairley, D.; Bamford, K. B.; D'Arc, S.; Brazier, J.; Brown, D.; Coia, J. E.; Douce, G.; Gerding, D.; Kim, H. J.; Koh, T. H.; Kato, H.; Senoh, M.; Louie, T.; Michell, S.; Butt, E.; Peacock, S. J.; Brown, N. M.; Riley, T.; Songer, G.; Wilcox, M.; Pirmohamed, M.; Kuijper, E.; Hawkey, P.; Wren, B. W.; Dougan, G.; Parkhill, J.; Lawley, T. D. Emergence and Global Spread of Epidemic Healthcare-Associated Clostridium difficile Nat. Genet. 2013, 45 (1) 109-113 10.1038/ng.2478
4. Courtney, C. M.; Goodman, S. M.; McDaniel, J. A.; Madinger, N. E.; Chatterjee, A.; Nagpal, P. Photoexcited Quantum Dots for Killing Multidrug-Resistant Bacteria Nat. Mater. 2016, 15 (5) 529-534 10.1038/nmat4542
5. Blair, J. M. A.; Webber, M. A.; Baylay, A. J.; Ogbolu, D. O.; Piddock, L. J. V. Molecular Mechanisms of Antibiotic Resistance Nat. Rev. Microbiol. 2015, 13 (1) 42-51 10.1038/nrmicro3380
6. CDC. AntibioticResistance Threats in the US, (2013.
7. O'Neill, J. AMR Review, https://amr-review.org/.
8. Zhi-Wen, Y.; Yan-Li, Z.; Man, Y.; Wei-Jun, F. Clinical Treatment of Pandrug-Resistant Bacterial Infection Consulted by Clinical Pharmacist Saudi Pharm. J. 2015) 23 (4) 377-380 10.1016/j.jsps.2015.01.001
9. Falagas, M. E.; Bliziotis, I. A. Pandrug-Resistant Gram-Negative Bacteria: The Dawn of the Post-Antibiotic Era? Int. J. Antimicrob. Agents 2007, 29 (6) 630-636 10.1016/j.ijantimicag.2006.12.012
10. Cioffi, N.; Torsi, L.; Ditaranto, N.; Tantillo, G.; Ghibelli, L.; Sabbatini, L.; Bleve-Zacheo, T.; D'Alessio, M.; Zambonin, P. G.; Traversa, E. Copper Nanoparticle/polymer Composites with Antifungal and Bacteriostatic Properties Chem. Mater. 2005, 17 (21) 5255-5262 10.1021/cm0505244
11. Rai, M.; Yadav, A.; Gade, A. Silver Nanoparticles as a New Generation of Antimicrobials Biotechnol. Adv. 2009, 27 (1) 76-83 10.1016/j.biotechadv.2008.09.002
12. Regiel-Futyra, A.; Kus-Liśkiewicz, M.; Sebastian, V.; Irusta, S.; Arruebo, M.; Stochel, G.; Kyzioł, A. Development of Noncytotoxic Chitosan-Gold Nanocomposites as Efficient Antibacterial Materials ACS Appl. Mater. Interfaces 2015, 7 (2) 1087-1099 10.1021/am508094e
13. Shrivastava, S.; Bera, T.; Roy, A.; Singh, G.; Ramachandrarao, P.; Dash, D. Characterization of Enhanced Antibacterial Effects of Novel Silver Nanoparticles Nanotechnology 2007, 18 (22) 225103 10.1088/0957-4484/18/22/225103
14. Sondi, I.; Salopek-Sondi, B. Silver Nanoparticles as Antimicrobial Agent: A Case Study on E. coli as a Model for Gram-Negative Bacteria J. Colloid Interface Sci. 2004, 275 (1) 177-182 10.1016/j.jcis.2004.02.012
15. Prabhu, S.; Poulose, E. K. Silver Nanoparticles: Mechanism of Antimicrobial Action, Synthesis, Medical Applications, and Toxicity Effects Int. Nano Lett. 2012, 2 (1) 32 10.1186/2228-5326-2-32
16. Song, L.; Connolly, M.; Fernández-Cruz, M. L.; Vijver, M. G.; Fernández, M.; Conde, E.; de Snoo, G. R.; Peijnenburg, W. J. G. M.; Navas, J. M. Species-Specific Toxicity of Copper Nanoparticles among Mammalian and Piscine Cell Lines Nanotoxicology 2014, 8 (4) 383-393 10.3109/17435390.2013.790997
17. Suliman, Y. A. O.; Ali, D.; Alarifi, S.; Harrath, A. H.; Mansour, L.; Alwasel, S. H. Evaluation of Cytotoxic, Oxidative Stress, Proinflammatory and Genotoxic Effect of Silver Nanoparticles in Human Lung Epithelial Cells Environ. Toxicol. 2015, 30 (2) 149-160 10.1002/tox.21880
18. Zhang, Y.; Shareena Dasari, T. P.; Deng, H.; Yu, H. Antimicrobial Activity of Gold Nanoparticles and Ionic Gold J. Environ. Sci. Health. C. Environ. Carcinog. Ecotoxicol. Rev. 2015, 33 (3) 286-327 10.1080/10590501.2015.1055161
19. Cui, Y.; Zhao, Y.; Tian, Y.; Zhang, W.; Lü, X.; Jiang, X. The Molecular Mechanism of Action of Bactericidal Gold Nanoparticles on Escherichia coli Biomaterials 2012, 33 (7) 2327-2333 10.1016/j.biomaterials.2011.11.057
20. Zhang, W.; Li, Y.; Niu, J.; Chen, Y. Photogeneration of Reactive Oxygen Species on Uncoated Silver, Gold, Nickel, and Silicon Nanoparticles and Their Antibacterial Effects Langmuir 2013, 29 (15) 4647-4651 10.1021/la400500t
21. Jokerst, J. V.; Lobovkina, T.; Zare, R. N.; Gambhir, S. S. Nanoparticle PEGylation for Imaging and Therapy Nanomedicine (London, U. K.) 2011, 6 (4) 715-728 10.2217/nnm.11.19
22. Niidome, T.; Yamagata, M.; Okamoto, Y.; Akiyama, Y.; Takahashi, H.; Kawano, T.; Katayama, Y.; Niidome, Y. PEG-Modified Gold Nanorods with a Stealth Character for in Vivo Applications J. Controlled Release 2006, 114 (3) 343-347 10.1016/j.jconrel.2006.06.017
23. Rhim, J.-W.; Hong, S.-I.; Park, H.-M.; Ng, P. K. W. Preparation and Characterization of Chitosan-Based Nanocomposite Films with Antimicrobial Activity J. Agric. Food Chem. 2006, 54 (16) 5814-5822 10.1021/jf060658h
24. Vijayakumar, S.; Ganesan, S.; Vijayakumar, S.; Ganesan, S. In Vitro Cytotoxicity Assay on Gold Nanoparticles with Different Stabilizing Agents J. Nanomater. 2012, 2012, 1-9 10.1155/2012/734398
25. Dash, M.; Chiellini, F.; Ottenbrite, R. M.; Chiellini, E. Chitosan-A Versatile Semi-Synthetic Polymer in Biomedical Applications Prog. Polym. Sci. 2011, 36 (8) 981-1014 10.1016/j.progpolymsci.2011.02.001
26. Mu, H.; Guo, F.; Niu, H.; Liu, Q.; Wang, S.; Duan, J. Chitosan Improves Anti-Biofilm Efficacy of Gentamicin through Facilitating Antibiotic Penetration Int. J. Mol. Sci. 2014, 15 (12) 22296-22308 10.3390/ijms151222296
27. No, H. K.; Young Park, N.; Ho Lee, S.; Meyers, S. P. Antibacterial Activity of Chitosans and Chitosan Oligomers with Different Molecular Weights Int. J. Food Microbiol. 2002, 74 (1) 65-72 10.1016/S0168-1605(01)00717-6
28. Schiffman, J. D.; Schauer, C. L. Cross-Linking Chitosan Nanofibers Biomacromolecules 2007, 8 (2) 594-601 10.1021/bm060804s
29. Costa-Pinto, A. R.; Martins, A. M.; Castelhano-Carlos, M. J.; Correlo, V. M.; Sol, P. C.; Longatto-Filho, A.; Battacharya, M.; Reis, R. L.; Neves, N. M. In Vitro Degradation and in Vivo Biocompatibility of Chitosan-Poly(butylene succinate) Fiber Mesh Scaffolds J. Bioact. Compat. Polym. 2014, 29 (2) 137-151 10.1177/0883911514521919
30. Bumgardner, J. D.; Wiser, R.; Gerard, P. D.; Bergin, P.; Chestnutt, B.; Marin, M.; Ramsey, V.; Elder, S. H.; Gilbert, J. A. Chitosan: Potential Use as a Bioactive Coating for Orthopaedic and Craniofacial/Dental Implants J. Biomater. Sci., Polym. Ed. 2003, 14 (5) 423-438 10.1163/156856203766652048
31. Croisier, F.; Jérôme, C. Chitosan-Based Biomaterials for Tissue Engineering Eur. Polym. J. 2013, 49 (4) 780-792 10.1016/j.eurpolymj.2012.12.009
32. Machul, A.; Mikołajczyk, D.; Regiel-Futyra, A.; Heczko, P. B.; Strus, M.; Arruebo, M.; Stochel, G.; Kyzioł, A. Study on Inhibitory Activity of Chitosan-Based Materials against Biofilm Producing Pseudomonas aeruginosa Strains J. Biomater. Appl. 2015, 30 (3) 269-278 10.1177/0885328215578781
33. Shalumon, K. T.; Anulekha, K. H.; Nair, S. V.; Nair, S. V.; Chennazhi, K. P.; Jayakumar, R. Sodium Alginate/poly(vinyl alcohol)/nano ZnO Composite Nanofibers for Antibacterial Wound Dressings Int. J. Biol. Macromol. 2011, 49 (3) 247-254 10.1016/j.ijbiomac.2011.04.005
34. Raafat, D.; von Bargen, K.; Haas, A.; Sahl, H.-G. Insights into the Mode of Action of Chitosan as an Antibacterial Compound Appl. Environ. Microbiol. 2008, 74 (12) 3764-3773 10.1128/AEM.00453-08
35. Goy, R. C.; Britto, D. de; Assis, O. B. G. A Review of the Antimicrobial Activity of Chitosan Polim.: Cienc. Tecnol. 2009, 19 (3) 241-247 10.1590/S0104-14282009000300013
36. Albee, L.; Perlman, H. E. Coli Infection Induces Caspase Dependent Degradation of NF-kappaB and Reduces the Inflammatory Response in Macrophages Inflammation Res. 2006, 55 (1) 2-9 10.1007/s00011-005-0001-9
37. Zhang, L.; Wang, C.-C. Inflammatory Response of Macrophages in Infection Hepatobiliary Pancreatic Dis. Int. 2014, 13 (2) 138-152 10.1016/S1499-3872(14)60024-2
38. Hoebe, K.; Janssen, E.; Beutler, B. The Interface between Innate and Adaptive Immunity Nat. Immunol. 2004, 5 (10) 971-974 10.1038/ni1004-971
39. Taylor, P. R.; Martinez-Pomares, L.; Stacey, M.; Lin, H.-H.; Brown, G. D.; Gordon, S. Macrophage Receptors and Immune Recognition Annu. Rev. Immunol. 2005, 23, 901-944 10.1146/annurev.immunol.23.021704.115816
40. Lawrence, T.; Natoli, G. Transcriptional Regulation of Macrophage Polarization: Enabling Diversity with Identity Nat. Rev. Immunol. 2011, 11 (11) 750-761 10.1038/nri3088
41. Weiss, G.; Schaible, U. E. Macrophage Defense Mechanisms against Intracellular Bacteria Immunol. Rev. 2015, 264 (1) 182-203 10.1111/imr.12266
42. Regiel, A.; Irusta, S.; Kyzioł, A.; Arruebo, M.; Santamaria, J. Preparation and Characterization of Chitosan-Silver Nanocomposite Films and Their Antibacterial Activity against Staphylococcus aureus Nanotechnology 2013, 24 (1) 15101 10.1088/0957-4484/24/1/015101
43. Gant, V. A.; Warnes, G.; Phillips, I.; Savidge, G. F. The Application of Flow Cytometry to the Study of Bacterial Responses to Antibiotics J. Med. Microbiol. 1993, 39 (2) 147-154 10.1099/00222615-39-2-147
44. Haiss, W.; Thanh, N. T. K.; Aveyard, J.; Fernig, D. G. Determination of Size and Concentration of Gold Nanoparticles from UV-Vis Spectra Anal. Chem. 2007, 79 (11) 4215-4221 10.1021/ac0702084
45. Stravodimos, K. G.; Singhal, P. C.; Sharma, S.; Reddy, K.; Smith, A. D. Escherichia coli Promotes Macrophage Apoptosis J. Endourol. 1999, 13 (4) 273-277 10.1089/end.1999.13.273
46. Kong, M.; Chen, X. G.; Xing, K.; Park, H. J. Antimicrobial Properties of Chitosan and Mode of Action: A State of the Art Review Int. J. Food Microbiol. 2010, 144 (1) 51-63 10.1016/j.ijfoodmicro.2010.09.012
47. Prema, P.; Thangapandiyan, S. In-Vitro Antibacterial Activity of Gold Nanoparticles Capped with Polysaccharide Stabilizing Agents Int. J. Pharm. Pharm. Sci. 2013, 5, 310-314
48. Pan, Y.; Neuss, S.; Leifert, A.; Fischler, M.; Wen, F.; Simon, U.; Schmid, G.; Brandau, W.; Jahnen-Dechent, W. Size-Dependent Cytotoxicity of Gold Nanoparticles Small 2007, 3 (11) 1941-1949 10.1002/smll.200700378
49. Jung, E. J.; Youn, D. K.; Lee, S. H.; No, H. K.; Ha, J. G.; Prinyawiwatkul, W. Antibacterial Activity of Chitosans with Different Degrees of Deacetylation and Viscosities Int. J. Food Sci. Technol. 2010, 45 (4) 676-682 10.1111/j.1365-2621.2010.02186.x
50. Ignatova, M.; Manolova, N.; Rashkov, I. Novel Antibacterial Fibers of Quaternized Chitosan and Poly(vinyl pyrrolidone) Prepared by Electrospinning Eur. Polym. J. 2007, 43 (4) 1112-1122 10.1016/j.eurpolymj.2007.01.012
51. Coma, V.; Deschamps, A.; Martial-Gros, A. Bioactive Packaging Materials from Edible Chitosan Polymer-Antimicrobial Activity Assessment on Dairy-Related Contaminants J. Food Sci. 2003, 68 (9) 2788-2792 10.1111/j.1365-2621.2003.tb05806.x
52. Chung, Y.; Su, Y.; Chen, C.; Jia, G.; Wang, H.; Wu, J. C. G.; Lin, J. Relationship between Antibacterial Activity of Chitosan and Surface Characteristics of Cell Wall Acta Pharmacol. Sin. 2004, 25 (7) 932-936
53. Sancilio, S.; di Giacomo, V.; Di Giulio, M.; Gallorini, M.; Marsich, E.; Travan, A.; Tarusha, L.; Cellini, L.; Cataldi, A. Biological Responses of Human Gingival Fibroblasts (HGFs) in an Innovative Co-culture Model with Streptococcus mitis to Thermosets Coated with a Silver Polysaccharide Antimicrobial System PLoS One 2014, 9 (5) e96520 10.1371/journal.pone.0096520
54. Marsich, E.; Travan, A.; Donati, I.; Turco, G.; Kulkova, J.; Moritz, N.; Aro, H. T.; Crosera, M.; Paoletti, S. Biological Responses of Silver-Coated Thermosets: An in Vitro and in Vivo Study Acta Biomater. 2013, 9 (2) 5088-5099 10.1016/j.actbio.2012.10.002