Reduced Cytotoxicity of Graphene Nanosheets Mediated by Blood-Protein Coating

ACS Nano

Volumn 9, Issue 6, 2015, Pages 5713-5724

  Chong, Yu ^a   Ge, Cuicui ^a   Yang, Zaixing ^a   Garate, Jose Antonio ^b   Gu, Zonglin ^a   Weber, Jeffrey K ^b   Liu, Jiajia ^a   Zhou, Ruhong ^a,b,c  

^a SOOCHOW UNIVERSITY   (China)

^b IBM T J WATSON RESEARCH CENTER   (United States)

^c Department of Chemistry Columbia University ^*  (United States)

Author keywords

blood proteins; cytotoxicity; graphene; interactions; safe design

Indexed keywords

ADSORPTION; BEAM PLASMA INTERACTIONS; BINS; BLOOD; BODY FLUIDS; CARBON; CARDIOVASCULAR SYSTEM; CYTOTOXICITY; GRAPHENE; HYDROPHOBICITY; MEDICAL APPLICATIONS; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; NANOPARTICLES; NANOSTRUCTURED MATERIALS; SINGLE-WALLED CARBON NANOTUBES (SWCN); YARN;

ADSORPTION CAPACITIES; BIOMEDICAL APPLICATIONS; BLOOD PROTEIN; FLORESCENCE SPECTROSCOPY; HYDROPHOBIC INTERACTIONS; INTERACTION MECHANISMS; SAFE DESIGNS; SINGLE-WALLED CARBON NANOTUBE (SWCNTS);

PROTEINS;

GRAPHITE; NANOPARTICLE; PLASMA PROTEIN;

ADSORPTION; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; HUMAN; MOLECULAR DYNAMICS; SURFACE PROPERTY; TUMOR CELL LINE;

ADSORPTION; BLOOD PROTEINS; CELL LINE, TUMOR; CELL SURVIVAL; GRAPHITE; HUMANS; MOLECULAR DYNAMICS SIMULATION; NANOPARTICLES; SURFACE PROPERTIES;

EID: 84935022317     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn5066606     Document Type: Article

References (80)

1. Michalet, X.; Pinaud, F. F.; Bentolila, L. A.; Tsay, J. M.; Doose, S.; Li, J. J.; Sundaresan, G.; Wu, A. M.; Gambhir, S. S.; Weiss, S. Quantum Dots for Live Cells, in Vivo Imaging, and Diagnostics Science 2005, 307, 538-544
2. Rosi, N. L.; Giljohann, D. A.; Thaxton, C. S.; Lytton-Jean, A. K. R.; Han, M. S.; Mirkin, C. A. Oligonucleotide-Modified Gold Nanoparticles for Intracellular Gene Regulation Science 2006, 312, 1027-1030
3. Grossman, J. H.; McNeil, S. E. Nanotechnology in Cancer Medicine Phys. Today 2012, 65, 38-42
4. Mundra, R. V.; Wu, X.; Sauer, J.; Dordick, J. S.; Kane, R. S. Nanotubes in Biological Applications Curr. Opin. Biotechnol. 2014, 28, 25-32
5. Iijima, S. Helical Microtubules of Graphitic Carbon Nature 1991, 354, 56-58
6. Snow, E. S.; Perkins, F. K.; Houser, E. J.; Badescu, S. C.; Reinecke, T. L. Chemical Detection with a Single-Walled Carbon Nanotube Capacitor Science 2005, 307, 1942-1945
7. Hinds, B. J.; Chopra, N.; Rantell, T.; Andrews, R.; Gavalas, V.; Bachas, L. G. Aligned Multiwalled Carbon Nanotube Membranes Science 2004, 303, 62-65
8. Singh, R.; Pantarotto, D.; Lacerda, L.; Pastorin, G.; Klumpp, C.; Prato, M.; Bianco, A.; Kostarelos, K. Tissue Biodistribution and Blood Clearance Rates of Intravenously Administered Carbon Nanotube Radiotracers Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 3357-3362
9. Liu, Z.; Sun, X.; Nakayama-Ratchford, N.; Dai, H. Supramolecular Chemistry on Water-Soluble Carbon Nanotubes for Drug Loading and Delivery ACS Nano 2007, 1, 50-56
10. Heister, E.; Neves, V.; Lamprecht, C.; Silva, S. R. P.; Coley, H. M.; McFadden, J. Drug Loading, Dispersion Stability, and Therapeutic Efficacy in Targeted Drug Delivery with Carbon Nanotubes Carbon 2012, 50, 622-632
11. Liu, Z.; Chen, K.; Davis, C.; Sherlock, S.; Cao, Q.; Chen, X.; Dai, H. Drug Delivery with Carbon Nanotubes for in Vivo Cancer Treatment Cancer Res. 2008, 68, 6652-6660
12. Moon, H. K.; Lee, S. H.; Choi, H. C. In vivo near-Infrared Mediated Tumor Destruction by Photothermal Effect of Carbon Nanotubes ACS Nano 2009, 3, 3707-3713
13. Robinson, J. T.; Welsher, K.; Tabakman, S. M.; Sherlock, S. P.; Wang, H.; Luong, R.; Dai, H. High Performance in Vivo near-IR (>1 Mm) Imaging and Photothermal Cancer Therapy with Carbon Nanotubes Nano Res. 2010, 3, 779-793
14. Bardhan, N. M.; Ghosh, D.; Belcher, A. M. Carbon Nanotubes as in Vivo Bacterial Probes Nat. Commun. 2014, 5, 4918-4928
15. Geim, A. K. Graphene: Status and Prospects Science 2009, 324, 1530-1534
16. Schwierz, F. Graphene Transistors Nat. Nanotechnol. 2010, 5, 487-496
17. Sreekanth, K. V.; Zeng, S.; Shang, J.; Yong, K.-T.; Yu, T. Excitation of Surface Electromagnetic Waves in a Graphene-Based Bragg Grating Sci. Rep. 2012, 2, 737-743
18. Kürüm, U.; Ekiz, O. Ö.; Yaglioglu, H. G.; Elmali, A.; Ürel, M.; Güner, H.; Mizrak, A. K.; Ortą, B.; Dâna, A. Electrochemically Tunable Ultrafast Optical Response of Graphene Oxide Appl. Phys. Lett. 2011, 98, 141103
19. Feng, L.; Liu, Z. Graphene in Biomedicine: Opportunities and Challenges Nanomedicine 2011, 6, 317-324
20. Sanchez, V. C.; Jachak, A.; Hurt, R. H.; Kane, A. B. Biological Interactions of Graphene-Family Nanomaterials: An Interdisciplinary Review Chem. Res. Toxicol. 2012, 25, 15-34
21. Yang, K.; Zhang, S.; Zhang, G.; Sun, X.; Lee, S. T.; Liu, Z. Graphene in Mice: Ultrahigh in Vivo Tumor Uptake and Efficient Photothermal Therapy Nano Lett. 2010, 10, 3318-3323
22. Okada, F. Beyond Foreign-Body-Induced Carcinogenesis: Impact of Reactive Oxygen Species Derived from Inflammatory Cells in Tumorigenic Conversion and Tumor Progression Int. J. Cancer. 2007, 121, 2364-2372
23. Soldano, C.; Mahmood, A.; Dujardin, E. Production, Properties and Potential of Graphene Carbon 2010, 48, 2127-2150
24. Chang, Y.; Yang, S.-T.; Liu, J.-H.; Dong, E.; Wang, Y.; Cao, A.; Liu, Y.; Wang, H. In Vitro Toxicity Evaluation of Graphene Oxide on A549 Cells Toxicol. Lett. 2011, 200, 201-210
25. Zhang, Y.; Ali, S. F.; Dervishi, E.; Xu, Y.; Li, Z.; Casciano, D.; Biris, A. S. Cytotoxicity Effects of Graphene and Single-Wall Carbon Nanotubes in Neural Phaeochromocytoma-Derived pc12 Cells ACS Nano 2010, 4, 3181-3186
26. Yang, K.; Wan, J.; Zhang, S.; Zhang, Y.; Lee, S. T.; Liu, Z. In Vivo Pharmacokinetics, Long-Term Biodistribution, and Toxicology of Pegylated Graphene in Mice ACS Nano 2011, 5, 516-522
27. 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
28. Zhang, W.; Wang, C.; Li, Z.; Lu, Z.; Li, Y.; Yin, J. J.; Zhou, Y. T.; Gao, X.; Fang, Y.; Nie, G. Unraveling Stress-Induced Toxicity Properties of Graphene Oxide and the Underlying Mechanism Adv. Mater. 2012, 24, 5391-5397
29. Zhao, Y.; Xing, G.; Chai, Z. Nanotoxicology: Are Carbon Nanotubes Safe? Nat. Nanotechnol. 2008, 3, 191-192
30. Nel, A.; Xia, T.; Mädler, L.; Li, N. Toxic Potential of Materials at the Nanolevel Science 2006, 311, 622-627
31. Nel, A. E.; Mädler, L.; Velegol, D.; Xia, T.; Hoek, E. M. V; Somasundaran, P.; Klaessig, F.; Castranova, V.; Thompson, M. Understanding Biophysicochemical Interactions at the Nano-Bio Interface Nat. Mater. 2009, 8, 543-557
32. Yang, K.; Ma, Y.-Q. Computer Simulation of the Translocation of Nanoparticles with Different Shapes across a Lipid Bilayer Nat. Nanotechnol. 2010, 5, 579-583
33. Shi, X.; von dem Bussche, A.; Hurt, R. H.; Kane, A. B.; Gao, H. Cell Entry of One-Dimensional Nanomaterials Occurs by Tip Recognition and Rotation Nat. Nanotechnol. 2011, 6, 714-719
34. Vácha, R.; Martinez-Veracoechea, F. J.; Frenkel, D. Receptor-Mediated Endocytosis of Nanoparticles of Various Shapes Nano Lett. 2011, 11, 5391-5395
35. Salvador-Morales, C.; Townsend, P.; Flahaut, E.; Vénien-Bryan, C.; Vlandas, A.; Green, M. L. H.; Sim, R. B. Binding of Pulmonary Surfactant Proteins to Carbon Nanotubes; Potential for Damage to Lung Immune Defense Mechanisms Carbon 2007, 45, 607-617
36. Linse, S.; Cabaleiro-Lago, C.; Xue, W.-F.; Lynch, I.; Lindman, S.; Thulin, E.; Radford, S. E.; Dawson, K. A. Nucleation of Protein Fibrillation by Nanoparticles Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 8691-8696
37. Lundqvist, M.; Stigler, J.; Elia, G.; Lynch, I.; Cedervall, T.; Dawson, K. A. Nanoparticle Size and Surface Properties Determine the Protein Corona with Possible Implications for Biological Impacts Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 14265-14270
38. 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
39. Akhavan, O.; Ghaderi, E. Toxicity of Graphene and Graphene Oxide Nanowalls against Bacteria ACS Nano 2010, 4, 5731-5736
40. 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
41. 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
42. 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
43. Li, Y.; Feng, L.; Shi, X.; Wang, X.; Yang, Y.; Yang, K.; Liu, T.; Yang, G.; Liu, Z. Surface Coating-Dependent Cytotoxicity and Degradation of Graphene Derivatives: Towards the Design of Non-Toxic, Degradable Nano-Graphene Small 2014, 10, 1544-1554
44. Zhang, Y.; Wu, C.; Guo, S.; Zhang, J. Interactions of Graphene and Graphene Oxide with Proteins and Peptides Nanotechnol. Rev. 2013, 2, 27-45
45. Mu, Q.; Su, G.; Li, L.; Gilbertson, B. O.; Yu, L. H.; Zhang, Q.; Sun, Y. P.; Yan, B. Size-Dependent Cell Uptake of Protein-Coated Graphene Oxide Nanosheets ACS Appl. Mater. Interfaces 2012, 4, 2259-2266
46. Hu, W.; Peng, C.; Lv, M.; Li, X.; Zhang, Y.; Chen, N.; Fan, C.; Huang, Q. Protein Corona-Mediated Mitigation of Cytotoxicity of Graphene Oxide ACS Nano 2011, 5, 3693-3700
47. Lesniak, A.; Fenaroli, F.; Monopoli, M. P.; Åberg, C.; Dawson, K. A.; Salvati, A. Effects of the Presence or Absence of a Protein Corona on Silica Nanoparticle Uptake and Impact on Cells ACS Nano 2012, 6, 5845-5857
48. Lesniak, A.; Salvati, A.; Santos-Martinez, M. J.; Radomski, M. W.; Dawson, K. A.; Åberg, C. Nanoparticle Adhesion to the Cell Membrane and Its Effect on Nanoparticle Uptake Efficiency J. Am. Chem. Soc. 2013, 135, 1438-1444
49. Zhang, Y.; Wu, C.; Guo, S.; Zhang, J. Interactions of graphene and graphene oxide with proteins and peptides Nanotechnol Rev. 2013, 2, 27-45
50. Ding, Z.; Ma, H.; Chen, Y. Interaction of Graphene Oxide with Human Serum Albumin and Its Mechanism RSC Adv. 2014, 4, 55290-55295
51. Kim, J. A.; Salvati, A.; Aberg, C.; Dawson, K. A. Suppression of Nanoparticle Cytotoxicity Approaching in Vivo Serum Concentrations: Limitations of in Vitro Testing for Nanosafety Nanoscale 2014, 6, 14180-14184
52. Ge, C.; Du, J.; Zhao, L.; Wang, L.; Liu, Y.; Li, D.; Yang, Y.; Zhou, R.; Zhao, Y.; Chai, Z. Binding of Blood Proteins to Carbon Nanotubes Reduces Cytotoxicity Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 16968-16973
53. Zhou, R.; Huang, X.; Margulis, C. J.; Berne, B. J. Hydrophobic Collapse in Multidomain Protein Folding Science 2004, 305, 1605-1609
54. Liu, P.; Huang, X.; Zhou, R.; Berne, B. J. Observation of a Dewetting Transition in the Collapse of the Melittin Tetramer Nature 2005, 437, 159-162
55. Lerf, A.; He, H.; Forster, M.; Klinowski, J. Structure of Graphite Oxide Revisited J. Phys. Chem. B 1998, 102, 4477-4482
56. Shih, C. J.; Lin, S.; Sharma, R.; Strano, M. S.; Blankschtein, D. Understanding the pH-Dependent Behavior of Graphene Oxide Aqueous Solutions: A Comparative Experimental and Molecular Dynamics Simulation Study Langmuir 2012, 28, 235-241
57. Medhekar, N. V.; Ramasubramaniam, A.; Ruoff, R. S.; Shenoy, V. B. Hydrogen Bond Networks in Graphene Oxide Composite Paper: Structure and Mechanical Properties ACS Nano 2010, 4, 2300-2306
58. Gómez-Navarro, C.; Meyer, J. C.; Sundaram, R. S.; Chuvilin, A.; Kurasch, S.; Burghard, M.; Kern, K.; Kaiser, U. Atomic Structure of Reduced Graphene Oxide Nano Lett. 2010, 10, 1144-1148
59. Ganguly, A.; Sharma, S.; Papakonstantinou, P.; Hamilton, J. Probing the Thermal Deoxygenation of Graphene Oxide Using High-Resolution in Situ X-Ray-Based Spectroscopies J. Phys. Chem. C 2011, 115, 17009-17019
60. O'Brien, E. P.; Stan, G.; Thirumalai, D.; Brooks, B. R. Factors Governing Helix Formation in Peptides Confined to Carbon Nanotubes Nano Lett. 2008, 8, 3702-3708
61. Liu, J.; Yang, Z.; Li, H.; Gu, Z.; Garate, J. A.; Zhou, R. Dewetting Transition Assisted Clearance of (NFGAILS) Amyloid Fibrils from Cell Membranes by Graphene J. Chem. Phys. 2014, 141, 22D520
62. Hua, L.; Huang, X.; Liu, P.; Zhou, R.; Berne, B. J. Nanoscale Dewetting Transition in Protein Complex Folding J. Phys. Chem. B 2007, 111, 9069-9077
63. Krone, M. G.; Hua, L.; Soto, P.; Zhou, R.; Berne, B. J.; Shea, J.-E. Role of Water in Mediating the Assembly of Alzheimer Amyloid-Beta Abeta16-22 Protofilaments J. Am. Chem. Soc. 2008, 130, 11066-11072
64. Zhou, R. Trp-Cage: Folding Free Energy Landscape in Explicit Water Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 13280-13285
65. Jimenez-Cruz, C. A.; Kang, S.; Zhou, R. Large Scale Molecular Simulations of Nanotoxicity Wiley Interdiscip. Rev.: Syst. Biol. Med. 2014, 6, 329-343
66. Bernstein, F. C.; Koetzle, T. F.; Williams, G. J. B.; Meyer, E. F.; Brice, M. D.; Rodgers, J. R.; Kennard, O.; Shimanouchi, T.; Tasumi, M. The Protein Data Bank Eur. J. Biochem. 1977, 80, 319-324
67. Brown, J. H.; Volkmann, N.; Jun, G.; Henschen-Edman, A. H.; Cohen, C. The Crystal Structure of Modified Bovine Fibrinogen Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 85-90
68. Brightbill, H. D.; Jeet, S.; Lin, Z.; Yan, D.; Zhou, M.; Tan, M.; Nguyen, A.; Yeh, S.; Delarosa, D.; Leong, S. R. Antibodies Specific for a Segment of Human Membrane IgE Deplete IgE-Producing B Cells in Humanized Mice J. Clin. Invest. 2010, 120, 2218-2229
69. Wally, J.; Halbrooks, P. J.; Vonrhein, C.; Rould, M. A.; Everse, S. J.; Mason, A. B.; Buchanan, S. K. The Crystal Structure of Iron-Free Human Serum Transferrin Provides Insight into Inter-Lobe Communication and Receptor Binding J. Biol. Chem. 2006, 281, 24934-24944
70. Guex, N.; Peitsch, M. C. SWISS-MODEL and the Swiss-PdbViewer: An Environment for Comparative Protein Modeling Electrophoresis 1997, 18, 2714-2723
71. MacKerell, A. D.; Bashford, D.; Bellott; Dunbrack, R. L.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins J. Phys. Chem. B 1998, 102, 3586-3616
72. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38
73. Jorgensen, W.; Chandrasekhar, J.; Madura, J.; Impey, R.; Klein, M. Comparison of Simple Potential Functions for Simulating Liquid Water J. Chem. Phys. 1983, 79, 926-935
74. Lindahl, E.; Hess, B.; van der Spoel, D. GROMACS 3.0: A Package for Molecular Simulation and Trajectory Analysis J. Mol. Model. 2001, 7, 306-317
75. Bussi, G.; Donadio, D.; Parrinello, M. Canonical Sampling through Velocity Rescaling J. Chem. Phys. 2007, 126, 014101
76. Parrinello, M.; Rahman, A. Polymorphic Transitions in Single-Crystals-A New Molecular-Dynamics Method J. Appl. Phys. 1981, 52, 7182-7190
77. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: An N·log(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089-10092
78. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. G. E. M. LINCS: A Linear Constraint Solver for Molecular Simulations J. Comput. Chem. 1997, 18, 1463-1472
79. Miyamoto, S.; Kollman, P. A. SETTLE: An Analytical Version of the SHAKE and RATTLE Algorithm for Rigid Water Models J. Comput. Chem. 1992, 13, 952-962
80. Zuo, G.; Zhou, X.; Huang, Q.; Fang, H.; Zhou, R. Adsorption of Villin Headpiece onto Graphene, Carbon Nanotube, and C60: Effect of Contacting Surface Curvatures on Binding Affinity J. Phys. Chem. C 2011, 115, 23323-23328