Wrinkled surface-mediated antibacterial activity of graphene oxide nanosheets

ACS Applied Materials and Interfaces

Volumn 9, Issue 2, 2017, Pages 1343-1351

  Zou, Fengming ^a,b   Zhou, Hongjian ^a,b   Jeong, Do Young ^c   Kwon, Junyoung ^a   Eom, Seong Un ^a   Park, Tae Jung ^d   Hong, Suck Won ^a   Lee, Jaebeom ^a  

^a Pusan National University   (South Korea)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c Samsung Electro Mechanics   (South Korea)

^d Chung Ang University   (South Korea)

Author keywords

Antibacterial activity; Graphene oxide; Molecular dynamics; Nanosheet; Surface roughness

Indexed keywords

CYTOLOGY; ESCHERICHIA COLI; FILTRATION; GRAPHENE; GRAPHENE OXIDE; MOLECULAR DYNAMICS; NANOSHEETS; OXIDE FILMS; THIN FILMS;

ANTI-BACTERIAL ACTIVITY; ANTI-MICROBIAL ACTIVITY; ANTIBACTERIAL PROPERTIES; ANTIBACTERIAL TREATMENT; GRAPHENE OXIDE NANOSHEETS; MYCOBACTERIUM SMEGMATIS; ROOT MEAN SQUARE VALUES; TWO-DIMENSIONAL MATERIALS;

SURFACE ROUGHNESS;

ANTIINFECTIVE AGENT; GRAPHITE; NANOMATERIAL; OXIDE;

ESCHERICHIA COLI; STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; ESCHERICHIA COLI; GRAPHITE; NANOSTRUCTURES; OXIDES; STAPHYLOCOCCUS AUREUS;

EID: 85027058246     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.6b15085     Document Type: Article

References (53)

1. Levy, S. B.; Marshall, B. Antibacterial Resistance Worldwide: Causes, Challenges and Responses. Nat. Med. 2004, 10, S122−S129.
2. Upadhyayula, V. K.; Deng, S.; Mitchell, M. C.; Smith, G. B. Application of Carbon Nanotube Technology for Removal of Contaminants in Drinking Water: A Review. Sci. Total Environ. 2009, 408, 1−13.
3. Martinez, M. N.; Papich, M. G.; Drusano, G. L. Dosing Regimen Matters: The Importance of Early Intervention and Rapid Attainment of The Pharmacokinetic/Pharmacodynamic Target. Antimicrob. Agents Chemother. 2012, 56, 2795−2805.
4. Cozzone, A. J. An Insight into Future Antibacterial Therapy. Emerging Microbes Infect. 2012, 1, e38.
5. Azam, A.; Ahmed, A. S.; Oves, M.; Khan, M. S.; Habib, S. S.; Memic, A. Antimicrobial Activity of Metal Oxide Nanoparticles Against Gram-positive and Gram-negative Bacteria: A Comparative Study. Int. J. Nanomed. 2012, 7, 6003−6009.
6. Besinis, A.; De Peralta, T.; Handy, R. D. The Antibacterial Effects of Silver, Titanium Dioxide and Silica Dioxide Nanoparticles Compared to The Dental Disinfectant Chlorhexidine on Streptococcus Mutans Using A Suite of Bioassays. Nanotoxicology 2014, 8, 1−16.
7. Emami-Karvani, Z.; Chehrazi, P. Antibacterial Activity of ZnO Nanoparticle on Gram-positive and gram-negative Bacteria. Afr. J. Microbiol. Res. 2011, 5, 1368−1373.
8. Usman, M. S.; El Zowalaty, M. E.; Shameli, K.; Zainuddin, N.; Salama, M.; Ibrahim, N. A. Synthesis, Characterization, and Antimicrobial Properties of Copper Nanoparticles. Int. J. Nanomed. 2013, 8, 4467−4479.
9. 60 Water Suspension. Environ. Toxicol. Chem. 2005, 24, 2757−2762.
10. Kang, S.; Mauter, M. S.; Elimelech, M. Physicochemical Determinants of Multiwalled Carbon Nanotube Bacterial Cytotoxicity. Environ. Sci. Technol. 2008, 42, 7528−7534.
11. Zhu, Z.; Meng, H.; Liu, W.; Liu, X.; Gong, J.; Qiu, X.; Jiang, L.; Wang, D.; Tang, Z. Superstructures and SERS Properties of Gold Nanocrystals with Different Shapes. Angew. Chem. 2011, 123, 1631− 1634.
12. Li, Z.; Cheng, E.; Huang, W.; Zhang, T.; Yang, Z.; Liu, D.; Tang, Z. Improving The Yield of Mono-DNA-Functionalized Gold Nanoparticles Through Dual Steric Hindrance. J. Am. Chem. Soc. 2011, 133, 15284−15287.
13. Xia, Y.; Nguyen, T. D.; Yang, M.; Lee, B.; Santos, A.; Podsiadlo, P.; Tang, Z.; Glotzer, S. C.; Kotov, N. A. Self-Assembly of Self-Limiting Monodisperse Supraparticles from Polydisperse Nanoparticles. Nat. Nanotechnol. 2011, 6, 580−587.
14. Deryabin, D. G.; Efremova, L. V.; Vasilchenko, A. S.; Saidakova, E. V.; Sizova, E. A.; Troshin, P. A.; Zhilenkov, A. V.; Khakina, E. E. A Zeta Potential Value Determines the Aggregates Size of Pentasubstituted [60] Fullerene Derivatives in Aqueous Suspension Whereas Positive Charge is Required for Toxicity Against Bacterial Cells. J. Nanobiotechnol. 2015, 13, 50.
15. Kang, S.; Pinault, M.; Pfefferle, L. D.; Elimelech, M. Single-Walled Carbon Nanotubes Exhibit Strong Antimicrobial Activity. Langmuir 2007, 23, 8670−8673.
16. Yang, C.; Mamouni, J.; Tang, Y.; Yang, L. Antimicrobial Activity of Single-Walled Carbon Nanotubes: Length Effect. Langmuir 2010, 26, 16013−16019.
17. Arias, L. R.; Yang, L. Inactivation of Bacterial Pathogens by Carbon Nanotubes in Suspensions. Langmuir 2009, 25, 3003−3012.
18. Dong, L.; Henderson, A.; Field, C. Antimicrobial Activity of Single-Walled Carbon Nanotubes Suspended in Different Surfactants. J. Nanotechnol. 2012, 2012, 928924.
19. Vecitis, C. D.; Zodrow, K. R.; Kang, S.; Elimelech, M. Electronic-Structure-Dependent Bacterial Cytotoxicity of Single-Walled Carbon Nanotubes. ACS Nano 2010, 4, 5471−5479.
20. Shen, H.; Zhang, L.; Liu, M.; Zhang, Z. Biomedical Applications of Graphene. Theranostics 2012, 2, 283−294.
21. Akhavan, O.; Ghaderi, E. Toxicity of Graphene and Graphene Oxide Nanowalls Against Bacteria. ACS Nano 2010, 4, 5731−5736.
22. Perreault, F.; de Faria, A. F.; Elimelech, M. Environmental Applications of Graphene-based Nanomaterials. Chem. Soc. Rev. 2015, 44, 5861−5896.
23. Hu, W.; Peng, C.; Luo, W.; Lv, M.; Li, X.; Li, D.; Huang, Q.; Fan, C. Graphene-Based Antibacterial Paper. ACS Nano 2010, 4, 4317−4323.
24. Li, Y.; Yuan, H.; Bussche, A.; Creighton, M.; Hurt, R. H.; Kane, A. B.; Gao, H. Graphene Microsheets Enter Cells Through Spontaneous Membrane Penetration at Edge Asperities and Corner Sites. Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 12295−12300.
25. Mao, J.; Guo, R.; Yan, L. T. Simulation and Analysis of Cellular Internalization Pathways and Membrane Perturbation for Graphene Nanosheets. Biomaterials 2014, 35, 6069−6077.
26. Yin, H.; Tang, H.; Wang, D.; Gao, Y.; Tang, Z. Facile Synthesis of Surfactant-Free Au Cluster/Graphene Hybrids for High-Performance Oxygen Reduction Reaction. ACS Nano 2012, 6, 8288−8297.
27. Zhao, S.; Li, Y.; Yin, H.; Liu, Z.; Luan, E.; Zhao, F.; Tang, Z.; Liu, S. Three-Dimensional Graphene/Pt Nanoparticle Composites as Freestanding Anode for Enhancing Performance of Microbial Fuel Cells. Sci. Adv. 2015, 1, e1500372.
28. Li, Y.; Tang, J.; He, L.; Liu, Y.; Liu, Y.; Chen, C.; Tang, Z. Core-Shell Upconversion Nanoparticle@Metal-Organic Framework Nanop-robes for Luminescent/Magnetic Dual-Mode Targeted Imaging. Adv. Mater. 2015, 27, 4075−4080.
29. Chen, J.; Peng, H.; Wang, X.; Shao, F.; Yuan, Z.; Han, H. Graphene Oxide Exhibits Broad-Spectrum Antimicrobial Activity Against Bacterial Phytopathogens and Fungal Conidia by Intertwining and Membrane Perturbation. Nanoscale 2014, 6, 1879−1889.
30. Liu, S.; Zeng, T. H.; Hofmann, M.; Burcombe, E.; Wei, J.; Jiang, R.; Kong, J.; Chen, Y. Antibacterial Activity of Graphite, Graphite Oxide, Graphene Oxide, and Reduced Graphene Oxide: Membrane and Oxidative Stress. ACS Nano 2011, 5, 6971−6980.
31. Gurunathan, S.; Han, J. W.; Dayem, A. A.; Eppakayala, V.; Kim, J. H. Oxidative Stress-Mediated Antibacterial Activity of Graphene Oxide and Reduced Graphene Oxide in Pseudomonas Aeruginosa. Int. J. Nanomed. 2012, 7, 5901−5914.
32. 2 Thin film for Photoinactivation of Bacteria in Solar Light Irradiation. J. Phys. Chem. C 2009, 113, 20214−20220.
33. Liu, S.; Hu, M.; Zeng, T. H.; Wu, R.; Jiang, R.; Wei, J.; Wang, L.; Kong, J.; Chen, Y. Lateral Dimension-dependent Antibacterial Activity of Graphene Oxide Sheets. Langmuir 2012, 28, 12364−12372.
34. Fasolino, A.; Los, J. H.; Katsnelson, M. I. Intrinsic Ripples in Graphene. Nat. Mater. 2007, 6, 858−861.
35. Zang, J.; Ryu, S.; Pugno, N.; Wang, Q.; Tu, Q.; Buehler, M. J.; Zhao, X. Multifunctionality and Control of the Crumpling and Unfolding of Large-area Graphene. Nat. Mater. 2013, 12, 321−325.
36. Zang, J.; Cao, C.; Feng, Y.; Liu, J.; Zhao, X. Stretchable and High-performance Supercapacitors with Crumpled Graphene Papers. Sci. Rep. 2014, 4, 6492.
37. Bowden, N.; Brittain, S.; Evans, A. G.; Hutchinson, J. W.; Whitesides, G. M. Spontaneous Formation of Ordered Structures in Thin Films of Metals Supported on An Elastomeric Polymer. Nature 1998, 393, 146−149.
38. Stafford, C. M.; Harrison, C.; Beers, K. L.; Karim, A.; Amis, E. J.; VanLandingham, M. R.; Kim, H. C.; Volksen, W.; Miller, R. D.; Simonyi, E. E. A buckling-based Metrology for Measuring the Elastic Moduli of Polymeric Thin Films. Nat. Mater. 2004, 3, 545−550.
39. Yang, D.; Velamakanni, A.; Bozoklu, G.; Park, S.; Stoller, M.; Piner, R. D.; Stankovich, S.; Jung, I.; Field, D. A.; Ventrice, C. A. Chemical Analysis of Graphene Oxide Films after Heat and Chemical Treatments by X-ray Photoelectron and Micro-Raman Spectroscopy. Carbon 2009, 47, 145−152.
40. Wang, Z.; Zhu, W.; Qiu, Y.; Yi, X.; von dem Bussche, A.; Kane, A.; Gao, H.; Koski, K.; Hurt, R. Biological and Environmental Interactions of Emerging Two-dimensional Nanomaterials. Chem. Soc. Rev. 2016, 45, 1750−1780.
41. Akhavan, O.; Ghaderi, E.; Esfandiar, A. Wrapping Bacteria by Graphene Nanosheets for Isolation from Environment, Reactivation by Sonication, and Inactivation by Near-infrared Irradiation. J. Phys. Chem. B 2011, 115, 6279−6288.
42. Wang, Z.; Tonderys, D.; Leggett, S. E.; Williams, E. K.; Kiani, M. T.; Steinberg, R. S.; Qiu, Y.; Wong, I. Y.; Hurt, R. H. Wrinkled, Wavelength-tunable Graphene-based Surface Topographies for Directing Cell Alignment and Morphology. Carbon 2016, 97, 14−24.
43. Sasidharan, A.; Panchakarla, L. S.; Chandran, P.; Menon, D.; Nair, S.; Rao, C. N. R.; Koyakutty, M. Differential Nano-bio Interactions and Toxicity Effects of Pristine Versus Functionalized Graphene. Nanoscale 2011, 3, 2461−2464.
44. Kim, I. Y.; Park, S.; Kim, H.; Park, S.; Ruoff, R. S.; Hwang, S. J. Strongly-Coupled Freestanding Hybrid Films of Graphene and Layered Titanate Nanosheets: An Effective Way to Tailor the Physicochemical and Antibacterial Properties of Graphene Film. Adv. Funct. Mater. 2014, 24, 2288−2294.
45. Pham, V. T. H.; Truong, V. K.; Quinn, M. D. J.; Notley, S. M.; Guo, Y.; Baulin, V. A.; Al Kobaisi, M.; Crawford, R. J.; Ivanova, E. P. Graphene Induces Formation of Pores That Kill Spherical and Rod-Shaped Bacteria. ACS Nano 2015, 9, 8458−8467.
46. Tu, Y.; Lv, M.; Xiu, P.; Huynh, T.; Zhang, M.; Castelli, M.; Liu, Z.; Huang, Q.; Fan, C.; Fang, H. Destructive Extraction of Phospholipids from Escherichia Coli Membranes by Graphene Nanosheets. Nat. Nanotechnol. 2013, 8, 594−601.
47. Li, Y.; Liu, Y.; Fu, Y.; Wei, T.; Le Guyader, L.; Gao, G.; Liu, R. S.; Chang, Y. Z.; Chen, C. The Triggering of Apoptosis in Macrophages by Pristine Graphene through The MAPK and TGF-beta Signaling Pathways. Biomaterials 2012, 33, 402−411.
48. Liu, X.; Sen, S.; Liu, J.; Kulaots, I.; Geohegan, D.; Kane, A.; Puretzky, A. A.; Rouleau, C. M.; More, K. L.; Palmore, G. T. Antioxidant Deactivation on Graphenic Nanocarbon Surfaces. Small 2011, 7, 2775−2785.
49. Zou, X.; Zhang, L.; Wang, Z.; Luo, Y. Mechanisms of The Antimicrobial Activities of Graphene Materials. J. Am. Chem. Soc. 2016, 138, 2064−2077.
50. Murzyn, K.; Rog, T.; Pasenkiewicz-Gierula, M. Phosphatidyle-thanolamine-phosphatidylglycerol Bilayer as A Model of The Inner Bacterial Membrane. Biophys. J. 2005, 88, 1091−1103.
51. Li, J.; Wang, G.; Zhu, H.; Zhang, M.; Zheng, X.; Di, Z.; Liu, X.; Wang, X. Antibacterial Activity of Large-area Monolayer Graphene Film Manipulated by Charge Transfer. Sci. Rep. 2014, 4, 4359.
52. Perreault, F.; de Faria, A. F.; Nejati, S.; Elimelech, M. Antimicrobial Properties of Graphene Oxide Nanosheets: Why Size Matters. ACS Nano 2015, 9, 7226−7236.
53. Musico, Y. L.; Santos, C. M.; Dalida, M. L.; Rodrigues, D. F. Surface Modification of Membrane Filters Using Graphene and Graphene Oxide-Based Nanomaterials for Bacterial Inactivation and Removal. ACS Sustainable Chem. Eng. 2014, 2, 1559−1565.