Plugging into proteins: Poisoning protein function by a hydrophobic nanoparticle

ACS Nano

Volumn 4, Issue 12, 2010, Pages 7508-7514

  Zuo, Guanghong ^a,b   Huang, Qing ^b   Wei, Guanghong ^a   Zhou, Ruhong ^c,d   Fang, Haiping ^a,b  

^a FUDAN UNIVERSITY   (China)

^b SHANGHAI INSTITUTE OF APPLIED PHYSICS   (China)

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

^d Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

hydrophobic interaction; molecular dynamics; nanoparticle toxicity; protein function poisoning; protein nanoparticle interaction

Indexed keywords

ACTIVE SITE; CANCER THERAPEUTICS; HUMAN HEALTH; HYDROPHOBIC CORE; HYDROPHOBIC INTERACTIONS; HYDROPHOBIC NANOPARTICLES; HYDROPHOBIC RESIDUES; LARGE-SCALE MOLECULAR DYNAMICS; MOLECULAR LEVELS; NANOPARTICLE TOXICITY; NANOSCALE PARTICLES; NOVEL ROUTE; ONE-FORM; PROMISING MATERIALS; PROTEIN FUNCTION POISONING; PROTEIN FUNCTIONS; STABLE COMPLEXES; WW DOMAIN;

AMINO ACIDS; BINDING SITES; BIOSENSORS; CARBON NANOTUBES; COMPLEXATION; DRUG DELIVERY; HEALTH RISKS; HYDROPHOBICITY; MOLECULAR DYNAMICS; PROTEINS; TOXICITY;

NANOPARTICLES;

CARBON NANOTUBE; PROTEIN;

ARTICLE; CHEMICAL PHENOMENA; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR DYNAMICS; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS;

HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR DYNAMICS SIMULATION; NANOTUBES, CARBON; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEINS; THERMODYNAMICS;

EID: 78650754795     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn101762b     Document Type: Article

References (63)

1. 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
2. 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
3. Wang, X.; Yang, L. L.; Chen, Z.; Shin, D. M. Application of Nanotechnology in Cancer Therapy and Imaging CA Cancer J. Clin. 2008, 58, 97-110
4. Li, H. K.; Huang, J. H.; Lv, J. H.; An, H. J.; Zhang, X. D.; Zhang, Z. Z.; Fan, C. H.; Hu, J. Nanoparticle PCR: Nanogold-Assisted PCR with Enhanced Specificity Angew. Chem., Int. Ed. 2005, 44, 5100-5103
5. Service, R. F. Is Nanotechnology Dangerous? Science 2000, 290, 1526-1527
6. Donaldson, K.; Aitken, R.; Tran, L.; Stone, V.; Duffin, R.; Forrest, G.; Alexander, A. Carbon Nanotubes: A Review of Their Properties in Relation to Pulmonary Toxicology and Workplace Safety Toxicol. Sci. 2006, 92, 5-22
7. Gilbert, N. Nanoparticle Safety in Doubt Nature 2009, 460, 937-937
8. Nel, A.; Xia, T.; Madler, L.; Li, N. Toxic Potential of Materials at the Nanolevel Science 2006, 311, 622-627
9. Zhao, Y. L.; Xing, G. M.; Chai, Z. F. Nanotoxicology: Are Carbon Nanotubes Safe? Nat. Nanotechnol. 2008, 3, 191-192
10. Chen, Z.; Meng, H.; Xing, G. M.; Chen, C. Y.; Zhao, Y. L.; Jia, G.; Wang, T. C.; Yuan, H.; Ye, C.; Zhao, F. et al. Acute Toxicological Effects of Copper Nanoparticles In Vivo Toxical. Lett. 2006, 163, 109-120
11. Maynard, A. D.; Baron, P. A.; Foley, M.; Shvedova, A. A.; Kisin, E. R.; Castranova, V. Exposure to Carbon Nanotube Material: Aerosol Release During the Handling of Unrefined Single-Walled Carbon Nanotube Material J. Toxicol. Environ. Health A 2004, 67, 87-107
12. Ryman-Rasmussen, J. P.; Cesta, M. F.; Brody, A. R.; Shipley-Phillips, J. K.; Everitt, J. I.; Tewksbury, E. W.; Moss, O. R.; Wong, B. A.; Dodd, D. E.; Andersen, M. E. et al. Inhaled Carbon Nanotubes Reach the Subpleural Tissue in Mice Nat. Nanotechnol. 2009, 4, 747-751
13. Kolosnjaj, J.; Szwarc, H.; Moussa, F. Toxicity Studies of Carbon Nanotubes Adv. Exp. Med. Biol. 2007, 620, 181-204
14. Porter, A. E.; Gass, M.; Muller, K.; Skepper, J. N.; Midgley, P. A.; Welland, M. Direct Imaging of Single-Walled Carbon Nanotubes in Cells Nat. Nanotechnol. 2007, 2, 713-717
15. Ma-Hock, L.; Treumann, S.; Strauss, V.; Brill, S.; Luizi, F.; Mertler, M.; Wiench, K.; Gamer, A. O.; van Ravenzwaay, B.; Landsiedel, R. Inhalation Toxicity of Multiwall Carbon Nanotubes in Rats Exposed for 3 Months Toxicol. Sci. 2009, 112, 468-481
16. Poland, C. A.; Duffin, R.; Kinloch, I.; Maynard, A.; Wallace, W. A. H.; Seaton, A.; Stone, V.; Brown, S.; MacNee, W.; Donaldson, K. Carbon Nanotubes Introduced into the Abdominal Cavity of Mice Show Asbestos-like Pathogenicity in a Pilot Study Nat. Nanotechnol. 2008, 3, 423-428
17. Schipper, M. L.; Nakayama-Ratchford, N.; Davis, C. R.; Kam, N. W. S.; Chu, P.; Liu, Z.; Sun, X. M.; Dai, H. J.; Gambhir, S. S. A Pilot Toxicology Study of Single-Walled Carbon Nanotubes in a Small Sample of Mice Nat. Nanotechnol. 2008, 3, 216-221
18. Shvedova, A. A.; Kisin, E. R.; Mercer, R.; Murray, A. R.; Johnson, V. J.; Potapovich, A. I.; Tyurina, Y. Y.; Gorelik, O.; Arepalli, S.; Schwegler-Berry, D. et al. Unusual Inflammatory and Fibrogenic Pulmonary Responses to Single-Walled Carbon Nanotubes in Mice Am. J. Physiol. Lung Cell. Mol. Physiol. 2005, 289, L698-L708
19. Mitchell, L. A.; Lauer, F. T.; Burchiel, S. W.; McDonald, J. D. Mechanisms for How Inhaled Multiwalled Carbon Nanotubes Suppress Systemic Immune Function in Mice Nat. Nanotechnol. 2009, 4, 451-456
20. Li, Z.; Hulderman, T.; Salmen, R.; Chapman, R.; Leonard, S. S.; Young, S.-H.; Shvedova, A.; Luster, M. I.; Simeonova, P. P. Cardiovascular Effects of Pulmonary Exposure to Single-Wall Carbon Nanotubes Environ. Health Perspect. 2007, 115, 377-382
21. Cedervall, T.; Lynch, I.; Lindman, S.; Berggård, T.; Thulin, E.; Nilsson, H.; Dawson, K. A.; Linse, S. Understanding the Nanoparticle-Protein Corona Using Methods to Quantify Exchange Rates and Affinities of Proteins for Nanoparticles Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 2050-2055
22. Klein, J. Probing the Interactions of Proteins and Nanoparticles Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 2029-2030
23. Rocker, C.; Potzl, M.; Zhang, F.; Parak, W. J.; Nienhaus, G. U. A Quantitative Fluorescence Study of Protein Monolayer Formation on Colloidal Nanoparticles Nat. Nanotechnol. 2009, 4, 577-580
24. Shen, J. W.; Wu, T.; Wang, Q.; Kang, Y. Induced Stepwise Conformational Change of Human Serum Albumin on Carbon Nanotube Surfaces Biomaterials 2008, 29, 3847-3855
25. Xiao, Y.; Patolsky, F.; Katz, E.; Hainfeld, J. F.; Willner, I. "Plugging into Enzymes": Nanowiring of Redox Enzymes by a Gold Nanoparticle Science 2003, 299, 1877-1881
26. Saven, J. G. Computational Protein Design: Advances in the Design and Redesign of Biomolecular Nanostructures Curr. Opin. Colloid Interface Sci. 2010, 15, 13-17
27. Kang, Y.; Wang, Q.; Liu, Y. C.; Wu, T.; Chen, Q.; Guan, W. J. Dynamic Mechanism of Collagen-like Peptide Encapsulated into Carbon Nanotubes J. Phys. Chem. B 2008, 112, 4801-4807
28. Park, K. H.; Chhowalla, M.; Iqbal, Z.; Sesti, F. Single-Walled Carbon Nanotubes Are a New Class of Ion Channel Blockers J. Biol. Chem. 2003, 278, 50212-50216
29. Calvaresi, M.; Zerbetto, F. Baiting Proteins with C-60 ACS Nano 2010, 4, 2283-2299
30. Macias, M. J.; Hyvonen, M.; Baraldi, E.; Schultz, J.; Sudol, M.; Saraste, M.; Oschkinat, H. Structure of the WW Domain of a Kinase-Associated Protein Complexed with a Proline-Rich Peptide Nature 1996, 382, 646-649
31. Iijima, S. Helical Microtubules of Graphitic Carbon Nature 1991, 354, 56-58
32. Li, W. Z.; Xie, S. S.; Qian, L. X.; Chang, B. H.; Zou, B. S.; Zhou, W. Y.; Zhao, R. A.; Wang, G. Large-Scale Synthesis of Aligned Carbon Nanotubes Science 1996, 274, 1701-1703
33. Duan, Y.; Kollman, P. A. Pathways to a Protein Folding Intermediate Observed in a 1-Microsecond Simulation in Aqueous Solution Science 1998, 282, 740-744
34. Levy, Y.; Wolynes, P. G.; Onuchic, J. N. Protein Topology Determines Binding Mechanism Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 511-516
35. Snow, C. D.; Nguyen, H.; Pande, V. S.; Gruebele, M. Absolute Comparison of Simulated and Experimental Protein-Folding Dynamics Nature 2002, 420, 102-106
36. Zhou, R. H.; Huang, X. H.; Margulis, C. J.; Berne, B. J. Hydrophobic Collapse in Multidomain Protein Folding Science 2004, 305, 1605-1609
37. Liu, P.; Huang, X. H.; Zhou, R. H.; Berne, B. J. Observation of a Dewetting Transition in the Collapse of the Melittin Tetramer Nature 2005, 437, 159-162
38. Zuo, G. H.; Hu, J.; Fang, H. P. Effect of the Ordered Water on Protein Folding: An Off-Lattice Gō-Like Model Study Phys. Rev. E 2009, 79 031925
39. Mayor, U.; Guydosh, N. R.; Johnson, C. M.; Grossmann, J. G.; Sato, S.; Jas, G. S.; Freund, S. M. V.; Alonso, D. O. V.; Daggett, V.; Fersht, A. R. The Complete Folding Pathway of a Protein from Nanoseconds to Microseconds Nature 2003, 421, 863-867
40. Mirny, L.; Shakhnovich, E. Protein Folding Theory: From Lattice to All-Atom Models Annu. Rev. Biophys. Biomol. Struct. 2001, 30, 361-396
41. Garcia, A. E.; Paschek, D. Simulation of the Pressure and Temperature Folding/Unfolding Equilibrium of a Small RNA Hairpin J. Am. Chem. Soc. 2008, 130, 815-816
42. Miyashita, N.; Straub, J. E.; Thirumalai, D. Structures of β-Amyloid Peptide 1-40, 1-42, and 1-55-the 672-726 Fragment of App in a Membrane Environment with Implications for Interactions with γ-Secretase J. Am. Chem. Soc. 2009, 131, 17843-17852
43. Hua, L.; Huang, X.; Zhou, R.; Berne, B. J. Dynamics of Water Confined in the Interdomain Region of a Multidomain Protein J. Phys. Chem. B 2006, 110, 3704-3711
44. Liu, P.; Huang, X.; Zhou, R.; Berne, B. J. Hydrophobic Aided Replica Exchange: An Efficient Algorithm for Protein Folding in Explicit Solvent J. Phys. Chem. B 2006, 110, 19018-19022
45. Zhou, R. Exploring the Protein Folding Free Energy Landscape: Coupling Replica Exchange Method with P3me/Respa Algorithm J. Mol. Graphics Modell. 2004, 22, 451-463
46. Zhou, R.; Eleftheriou, M.; Royyuru, A. K.; Berne, B. J. Destruction of Long-Range Interactions by a Single Mutation in Lysozyme Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 5824-5829
47. Gao, Y. Q.; Yang, W.; Karplus, M. A Structure-Based Model for the Synthesis and Hydrolysis of ATP by F1-Atpase Cell 2005, 123, 195-205
48. Karplus, M.; Gao, Y. Q.; Ma, J.; van der Vaart, A.; Yang, W. Protein Structural Transitions and Their Functional Role Philos. Trans. R. Soc., A 2005, 363, 331-355; discussion 355-356
49. Roitberg, A. E.; Okur, A.; Simmerling, C. Coupling of Replica Exchange Simulations to a Non-Boltzmann Structure Reservoir J. Phys. Chem. B 2007, 111, 2415-2418
50. Gong, X. J.; Li, J. Y.; Lu, H. J.; Wan, R. Z.; Li, J. C.; Hu, J.; Fang, H. P. A Charge-Driven Molecular Water Pump Nat. Nanotechnol. 2007, 2, 709-712
51. Hummer, G.; Rasaiah, J. C.; Noworyta, J. P. Water Conduction through the Hydrophobic Channel of a Carbon Nanotube Nature 2001, 414, 188-190
52. Tu, Y. S.; Xiu, P.; Wan, R. Z.; Hu, J.; Zhou, R. H.; Fang, H. P. Water-Mediated Signal Multiplication with Y-Shaped Carbon Nanotubes Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 18120-18124
53. Li, J. Y.; Gong, X. J.; Lu, H. J.; Li, D.; Fang, H. P.; Zhou, R. H. Electrostatic Gating of a Nanometer Water Channel Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 3687-3692
54. Giovambattista, N.; Lopez, C. F.; Rossky, P. J.; Debenedetti, P. G. Hydrophobicity of Protein Surfaces: Separating Geometry from Chemistry Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 2274-2279
55. Dill, K. Dominant Forces in Protein Folding Biochemistry 1990, 29, 7133-7155
56. Wang, S.; Humphreys, E. S.; Chung, S. Y.; Delduco, D. F.; Lustig, S. R.; Wang, H.; Parker, K. N.; Rizzo, N. W.; Subramoney, S.; Chiang, Y. M.; Jagota, A. Peptides with Selective Affinity for Carbon Nanotubes Nat. Mater. 2003, 2, 196-200
57. Zheng, L. F.; Jain, D.; Burke, P. Nanotube-Peptide Interactions on a Silicon Chip J. Phys. Chem. C 2009, 113, 3978-3985
58. Kabsch, W.; Sander, C. Dictionary of Protein Secondary Structure: Pattern Recognition of Hydrogen-Bonded and Geometrical Features Biopolymers 1983, 22, 2577-2637
59. Braden, B. C.; Goldbaum, F. A.; Chen, B. X.; Kirschner, A. N.; Wilson, S. R.; Erlanger, B. F. X-ray Crystal Structure of an Anti-Buckminsterfullerene Antibody Fab Fragment: Biomolecular Recognition of C(60) Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 12193-12197
60. Noon, W. H.; Kong, Y.; Ma, J. Molecular Dynamics Analysis of a Buckyball-Antibody Complex Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 6466-6470
61. Allen, B. L.; Kichambare, P. D.; Gou, P.; Vlasova, I. I.; Kapralov, A. A.; Konduru, N.; Kagan, V. E.; Star, A. Biodegradation of Single-Walled Carbon Nanotubes through Enzymatic Catalysis Nano Lett. 2008, 8, 3899-2903
62. Duan, Y.; Wu, C.; Chowdhury, S.; Lee, M. C.; Xiong, G. M.; Zhang, W.; Yang, R.; Cieplak, P.; Luo, R.; Lee, T. S. et al. A Point-Charge Force Field for Molecular Mechanics Simulations of Proteins Based on Condensed-Phase Quantum Mechanical Calculations J. Comput. Chem. 2003, 24, 1999-2012
63. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. Gromacs 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation J. Chem. Theory Comp. 2008, 4, 435-447