Graphene Induces Formation of Pores That Kill Spherical and Rod-Shaped Bacteria

ACS Nano

Volumn 9, Issue 8, 2015, Pages 8458-8467

  Pham, Vy T H ^a   Truong, Vi Khanh ^a   Quinn, Matthew D J ^a   Notley, Shannon M ^a   Guo, Yachong ^b   Baulin, Vladimir A ^b   Al Kobaisi, Mohammad ^a   Crawford, Russell J ^a   Ivanova, Elena P ^a  

^a SWINBURNE UNIVERSITY OF TECHNOLOGY   (Australia)

^b UNIVERSITAT ROVIRA I VIRGILI   (Spain)

Author keywords

bactericidal effect; edge densities; graphene nanosheet films; pore formation; single mean field simulation

Indexed keywords

BACTERIA; CELL DEATH; CELL MEMBRANES; CELLS; CYTOLOGY; NANOSHEETS;

BACTERICIDAL EFFECTS; EDGE DENSITIES; GRAPHENE NANOSHEETS; MEAN FIELD; PORE FORMATION;

GRAPHENE;

ANTIINFECTIVE AGENT; GRAPHITE;

ATOMIC FORCE MICROSCOPY; BACTERIUM ADHERENCE; CELL MEMBRANE; COMPUTER SIMULATION; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; PSEUDOMONAS AERUGINOSA; RAMAN SPECTROMETRY; SCANNING ELECTRON MICROSCOPY; STAPHYLOCOCCUS AUREUS; SURFACE PROPERTY; ULTRASTRUCTURE;

ANTI-BACTERIAL AGENTS; BACTERIAL ADHESION; CELL MEMBRANE; COMPUTER SIMULATION; GRAPHITE; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, SCANNING; PSEUDOMONAS AERUGINOSA; SPECTRUM ANALYSIS, RAMAN; STAPHYLOCOCCUS AUREUS; SURFACE PROPERTIES;

EID: 84940092765     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.5b03368     Document Type: Article

References (49)

1. 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 10.1021/nn202451x
2. Mao, H. Y.; Laurent, S.; Chen, W.; Akhavan, O.; Imani, M.; Ashkarran, A. A.; Mahmoudi, M. Graphene: Promises, Facts, Opportunities, and Challenges in Nanomedicine Chem. Rev. 2013, 113, 3407-3424 10.1021/cr300335p
3. Novoselov, K. S.; Falko, V. I.; Colombo, L.; Gellert, P. R.; Schwab, M. G.; Kim, K. A Roadmap for Graphene Nature 2012, 490, 192-200 10.1038/nature11458
4. Xu, M.; Liang, T.; Shi, M.; Chen, H. Graphene-like Two-Dimensional Materials Chem. Rev. 2013, 113, 3766-3798 10.1021/cr300263a
5. 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 10.1021/nn101097v
6. 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, 10.1038/srep04359
7. Akhavan, O.; Ghaderi, E. Toxicity of Graphene and Graphene Oxide Nanowalls against Bacteria ACS Nano 2010, 4, 5731-5736 10.1021/nn101390x
8. 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 10.2147/IJN.S37397
9. Krishnamoorthy, K.; Veerapandian, M.; Zhang, L. H.; Yun, K.; Kim, S. J. Antibacterial Efficiency of Graphene Nanosheets against Pathogenic Bacteria via Lipid Peroxidation J. Phys. Chem. C 2012, 116, 17280-17287 10.1021/jp3047054
10. Tu, Y.; Lv, M.; Xiu, P.; Huynh, T.; Zhang, M.; Castelli, M.; Liu, Z.; Huang, Q.; Fan, C.; Fang, H. et al. Destructive Extraction of Phospholipids from Escherichia coli Membranes by Graphene Nanosheets Nat. Nanotechnol. 2013, 8, 594-601 10.1038/nnano.2013.125
11. Mangadlao, J. D.; Santos, C. M.; Felipe, M. J. L.; De Leon, A. C. C.; Rodrigues, D. F.; Advincula, R. C. On the Antibacterial Mechanism of Graphene Oxide (GO) Langmuir-Blodgett Films Chem. Commun. 2015, 51, 2886-2889 10.1039/C4CC07836E
12. Hui, L.; Piao, J. G.; Auletta, J.; Hu, K.; Zhu, Y.; Meyer, T.; Liu, H.; Yang, L. Availability of the Basal Planes of Graphene Oxide Determines Whether It Is Antibacterial ACS Appl. Mater. Interfaces 2014, 6, 13183-13190 10.1021/am503070z
13. 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 10.1021/la3023908
14. Yang, X.; Li, Z.; Ju, E.; Ren, J.; Qu, X. Reduced Graphene Oxide Functionalized with a Luminescent Rare-Earth Complex for The Tracking and Photothermal Killing of Drug-Resistant Bacteria Chem.-Eur. J. 2014, 20, 394-398 10.1002/chem.201303964
15. Akhavan, O.; Ghaderi, E. Photocatalytic Reduction of Graphene Oxide Nanosheets on TiO2 Thin Film for Photoinactivation of Bacteria in Solar Light Irradiation J. Phys. Chem. C 2009, 113, 20214-20220 10.1021/jp906325q
16. Sun, H.; Gao, N.; Dong, K.; Ren, J.; Qu, X. Graphene Quantum Dots-Band-aids Used for Wound Disinfection ACS Nano 2014, 8, 6202-6210 10.1021/nn501640q
17. Shen, J.; Li, T.; Shi, M.; Li, N.; Ye, M. Polyelectrolyte-assisted One-Step Hydrothermal Synthesis of Ag-Reduced Graphene Oxide Composite and Its Antibacterial Properties Mater. Sci. Eng., C 2012, 32, 2042-2047 10.1016/j.msec.2012.05.017
18. de Faria, A. F.; Martinez, D. S. T.; Meira, S. M. M.; de Moraes, A. C. M.; Brandelli, A.; Filho, A. G. S.; Alves, O. L. Anti-adhesion and Antibacterial Activity of Silver Nanoparticles Supported on Graphene Oxide Sheets Colloids Surf., B 2014, 113, 115-124 10.1016/j.colsurfb.2013.08.006
19. Santos, C. M.; Tria, M. C.; Vergara, R. A.; Ahmed, F.; Advincula, R. C.; Rodrigues, D. F. Antimicrobial Graphene Polymer (PVK-GO) Nanocomposite Films Chem. Commun. 2011, 47, 8892-4 10.1039/c1cc11877c
20. Park, S.; Mohanty, N.; Suk, J. W.; Nagaraja, A.; An, J.; Piner, R. D.; Cai, W.; Dreyer, D. R.; Berry, V.; Ruoff, R. S. Biocompatible, Robust Free-Standing Paper Composed of a TWEEN/Graphene Composite Adv. Mater. 2010, 22, 1736-1740 10.1002/adma.200903611
21. Akhavan, O.; Choobtashani, M.; Ghaderi, E. Protein Degradation and RNA Efflux of Viruses Photocatalyzed by Graphene-Tungsten Oxide Composite under Visible Light Irradiation J. Phys. Chem. C 2012, 116, 9653-9659 10.1021/jp301707m
22. Kim, S.; Ryoo, S. R.; Na, H. K.; Kim, Y. K.; Choi, B. S.; Lee, Y.; Kim, D. E.; Min, D. H. Deoxyribozyme-loaded Nano-Graphene Oxide for Simultaneous Sensing and Silencing of the Hepatitis C Virus Gene in Liver Cells Chem. Commun. 2013, 49, 8241-8243 10.1039/c3cc43368d
23. Li, Y.; Yuan, H.; von dem 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 10.1073/pnas.1222276110
24. 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, 6279-88 10.1021/jp200686k
25. Yi, X.; Gao, H. Cell Interaction with Graphene Microsheets: Near-Orthogonal Cutting versus Parallel Attachment Nanoscale 2015, 7, 5457-5467 10.1039/C4NR06170E
26. Dallavalle, M.; Calvaresi, M.; Bottoni, A.; Melle-Franco, M.; Zerbetto, F. Graphene can Wreak Havoc with Cell Membranes ACS Appl. Mater. Interfaces 2015, 7, 4406-4414 10.1021/am508938u
27. Luan, B.; Huynh, T.; Zhao, L.; Zhou, R. Potential Toxicity of Graphene to Cell Functions via Disrupting Protein-Protein Interactions ACS Nano 2015, 9, 663-669 10.1021/nn506011j
28. Akhavan, O.; Ghaderi, E. Escherichia coli Bacteria Reduce Graphene Oxide to Bactericidal Graphene in a Self-limiting Manner Carbon 2012, 50, 1853-1860 10.1016/j.carbon.2011.12.035
29. Notley, S. M. Highly Concentrated Aqueous Suspensions of Graphene Through Ultrasonic Exfoliation with Continuous Surfactant Addition Langmuir 2012, 28, 14110-14113 10.1021/la302750e
30. Sham, A. Y. W.; Notley, S. M. A Review of Fundamental Properties and Applications of Polymer-Graphene Hybrid Materials Soft Matter 2013, 9, 6645-6653 10.1039/c3sm00092c
31. Tang, Y.; Huang, F.; Zhao, W.; Liu, Z.; Wan, D. Synthesis of Graphene-Supported Li4Ti5O12 Nanosheets for High Rate Battery Application J. Mater. Chem. 2012, 22, 11257-11260 10.1039/c2jm30624g
32. Lu, W.; Liu, S.; Qin, X.; Wang, L.; Tian, J.; Luo, Y.; Asiri, A. M.; Al-Youbi, A. O.; Sun, X. High-yield, Large-scale Production of Few-layer Graphene Flakes Within Seconds: Using Chlorosulfonic Acid and H2O2 as Exfoliating Agents J. Mater. Chem. 2012, 22, 8775-8777 10.1039/c2jm16741g
33. Hernandez, Y.; Nicolosi, V.; Lotya, M.; Blighe, F. M.; Sun, Z.; De, S.; McGovern, I. T.; Holland, B.; Byrne, M.; Gun'Ko, Y. K. et al. High-Yield Production of Graphene by Liquid-Phase Exfoliation of Graphite Nat. Nanotechnol. 2008, 3, 563-568 10.1038/nnano.2008.215
34. Lotya, M.; Hernandez, Y.; King, P. J.; Smith, R. J.; Nicolosi, V.; Karlsson, L. S.; Blighe, F. M.; De, S.; Wang, Z.; McGovern, I. T. et al. Liquid Phase Production of Graphene by Exfoliation of Graphite in Surfactant/Water Solutions J. Am. Chem. Soc. 2009, 131, 3611-3620 10.1021/ja807449u
35. Zhu, L.; Zhao, X.; Li, Y.; Yu, X.; Li, C.; Zhang, Q. High-Quality Production of Graphene by Liquid-Phase Exfoliation of Expanded Graphite Mater. Chem. Phys. 2013, 137, 984-990 10.1016/j.matchemphys.2012.11.012
36. Ni, Z. H.; Wang, H. M.; Ma, Y.; Kasim, J.; Wu, Y. H.; Shen, Z. X. Tunable Stress and Controlled Thickness Modification in Graphene by Annealing ACS Nano 2008, 2, 1033-1039 10.1021/nn800031m
37. Ferrari, A. C.; Meyer, J. C.; Scardaci, V.; Casiraghi, C.; Lazzeri, M.; Mauri, F.; Piscanec, S.; Jiang, D.; Novoselov, K. S.; Roth, S. et al. Raman Spectrum of Graphene and Graphene Layers Phys. Rev. Lett. 2006, 97, 97 10.1103/PhysRevLett.97.187401
38. Shinbrot, T.; Muzzio, F. J. Reverse Buoyancy in Shaken Granular Beds Phys. Rev. Lett. 1998, 81, 4365-4368 10.1103/PhysRevLett.81.4365
39. Hong, D. C.; Quinn, P. V.; Luding, S. Reverse Brazil Nut Problem: Competition between Percolation and Condensation Phys. Rev. Lett. 2001, 86, 3423-3426 10.1103/PhysRevLett.86.3423
40. Ivanova, E. P.; Mitik-Dineva, N.; Wang, J.; Pham, D. K.; Wright, J. P.; Nicolau, D. V.; Mocanasu, R. C.; Crawford, R. J. Staleya guttiformis Attachment on Poly(tert-butylmethacrylate) Polymeric Surfaces Micron 2008, 39, 1197-1204 10.1016/j.micron.2008.04.009
41. Mitik-Dineva, N.; Wang, J.; Truong, V. K.; Stoddart, P.; Malherbe, F.; Crawford, R. J.; Ivanova, E. P. Escherichia coli, Pseudomonas aeruginosa and Staphylococcus aureus Attachment Patterns on Glass Surfaces with Nanoscale Roughness Curr. Microbiol. 2009, 58, 268-273 10.1007/s00284-008-9320-8
42. Truong, V. K.; Rundell, S.; Lapovok, R.; Estrin, Y.; Wang, J. Y.; Berndt, C. C.; Barnes, D. G.; Fluke, C. J.; Crawford, R. J.; Ivanova, E. P. Effect of Ultrafine-Grained Titanium Surfaces on Adhesion of Bacteria Appl. Microbiol. Biotechnol. 2009, 83, 925-937 10.1007/s00253-009-1944-5
43. Webb, H. K.; Boshkovikj, V.; Fluke, C. J.; Truong, V. K.; Hasan, J.; Baulin, V. A.; Lapovok, R.; Estrin, Y.; Crawford, R. J.; Ivanova, E. P. Bacterial Attachment on Sub-Nanometrically Smooth Titanium Substrata Biofouling 2013, 29, 163-170 10.1080/08927014.2012.757697
44. Ivanova, E. P.; Truong, V. K.; Webb, H. K.; Baulin, V. A.; Wang, J. Y.; Mohammodi, N.; Wang, F.; Fluke, C.; Crawford, R. J. Differential Attraction and Repulsion of Staphylococcus aureus and Pseudomonas aeruginosa on Molecularly Smooth Titanium Films Sci. Rep. 2011, 1, 165 10.1038/srep00165
45. Akhavan, O.; Ghaderi, E.; Akhavan, A. Size-dependent Genotoxicity of Graphene Nanoplatelets in Human Stem Cells Biomaterials 2012, 33, 8017-8025 10.1016/j.biomaterials.2012.07.040
46. Akhavan, O.; Ghaderi, E.; Emamy, H.; Akhavan, F. Genotoxicity of Graphene Nanoribbons in Human Mesenchymal Stem Cells Carbon 2013, 54, 419-431 10.1016/j.carbon.2012.11.058
47. Gao, H. Probing Mechanical Principles of Cell-Nanomaterial Interactions J. Mech. Phys. Solids 2014, 62, 312-339 10.1016/j.jmps.2013.08.018
48. Flemming, H. C.; Wingender, J. The Biofilm Matrix Nat. Rev. Microbiol. 2010, 8, 623-633 10.1038/nrmicro2415
49. Senneville, E.; Joulie, D.; Legout, L.; Valette, M.; Dezèque, H.; Beltrand, E.; Roselé, B.; D'Escrivan, T.; Loïez, C.; Caillaux, M. et al. Outcome and Predictors of Treatment Failure in Total Hip/Knee Prosthetic Joint Infections due to Staphylococcus aureus Clin. Infect. Dis. 2011, 53, 334-340 10.1093/cid/cir402