Adsorption of Villin Headpiece onto Graphene, Carbon Nanotube, and C60: Effect of Contacting Surface Curvatures on Binding Affinity

The adsorption of protein villin headpiece (HP35) onto a graphene has been investigated using large scale molecular dynamics simulations, and the results are compared with similar adsorptions onto a single-wall carbon nanotube and a fullerene, C60. It is found that HP35 loses most of its native secondary and tertiary structures after the adsorption onto graphene. The pi-pi stacking interactions between the graphene and HP35's aromatic residues play a key role in this adsorption. The graphene's softness also helps the binding by adapting its own shape to fit better with aromatic residues in forming stronger pi-pi stacking interactions. Interestingly, the mechanism of HP35 adsorption onto the other two graphitic nanomaterials is found to be somewhat different, in which the pi-pi stacking interactions play a lesser role than the dispersion interactions between the nanomaterial and HP35's aliphatic side chains. These findings indicate that in addition to the chemical composition, the shape of the nanoparticle is also an important factor in determining its interaction with proteins: the contacting surface curvature can lead to different adsorption mechanisms.

[1]  Carsten Kutzner,et al.  GROMACS 4:  Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation. , 2008, Journal of chemical theory and computation.

[2]  V. Pande,et al.  Absolute comparison of simulated and experimental protein-folding dynamics , 2002, Nature.

[3]  A. Geim,et al.  Two-dimensional gas of massless Dirac fermions in graphene , 2005, Nature.

[4]  Yuliang Zhao,et al.  Nanotoxicology: Are carbon nanotubes safe? , 2008, Nature nanotechnology.

[5]  Jianpeng Ma,et al.  Protein structural transitions and their functional role , 2005, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[6]  Chad A. Mirkin,et al.  Oligonucleotide-Modified Gold Nanoparticles for Intracellular Gene Regulation , 2006, Science.

[7]  Haiping Fang,et al.  Effect of the ordered water on protein folding: an off-lattice Gō-like model study. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[8]  S. Gambhir,et al.  Quantum Dots for Live Cells, in Vivo Imaging, and Diagnostics , 2005, Science.

[9]  John E. Straub,et al.  Structures of beta-amyloid peptide 1-40, 1-42, and 1-55-the 672-726 fragment of APP-in a membrane environment with implications for interactions with gamma-secretase. , 2009, Journal of the American Chemical Society.

[10]  R. Zhou,et al.  Binding of blood proteins to carbon nanotubes reduces cytotoxicity , 2011, Proceedings of the National Academy of Sciences.

[11]  T. Darden,et al.  Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems , 1993 .

[12]  Jingyuan Li,et al.  Controllable water channel gating of nanometer dimensions. , 2005, Journal of the American Chemical Society.

[13]  Hangjun Lu,et al.  Manipulating biomolecules with aqueous liquids confined within single-walled nanotubes. , 2009, Journal of the American Chemical Society.

[14]  Jun Hu,et al.  Nanoparticle PCR: nanogold-assisted PCR with enhanced specificity. , 2005, Angewandte Chemie.

[15]  H. Berendsen,et al.  Molecular dynamics with coupling to an external bath , 1984 .

[16]  B. Berne,et al.  Nanoscale dewetting transition in protein complex folding. , 2007, The journal of physical chemistry. B.

[17]  P. Kollman,et al.  Pathways to a protein folding intermediate observed in a 1-microsecond simulation in aqueous solution. , 1998, Science.

[18]  P. Kim,et al.  Experimental observation of the quantum Hall effect and Berry's phase in graphene , 2005, Nature.

[19]  Chunhai Fan,et al.  Graphene on Au(111): a highly conductive material with excellent adsorption properties for high-resolution bio/nanodetection and identification. , 2010, Chemphyschem : a European journal of chemical physics and physical chemistry.

[20]  R. Aitken,et al.  Carbon nanotubes: a review of their properties in relation to pulmonary toxicology and workplace safety. , 2006, Toxicological sciences : an official journal of the Society of Toxicology.

[21]  X. Gong,et al.  Electrostatic gating of a nanometer water channel , 2007, Proceedings of the National Academy of Sciences.

[22]  Jian Zhang,et al.  Metal-coupled folding of Cys2His2 zinc-finger. , 2008, Journal of the American Chemical Society.

[23]  Ruhong Zhou,et al.  Plugging into proteins: poisoning protein function by a hydrophobic nanoparticle. , 2010, ACS nano.

[24]  Andre K. Geim,et al.  Electric Field Effect in Atomically Thin Carbon Films , 2004, Science.

[25]  A. Garcia,et al.  Simulation of the pressure and temperature folding/unfolding equilibrium of a small RNA hairpin. , 2008, Journal of the American Chemical Society.

[26]  Fabio Ganazzoli,et al.  Surface Ordering of Proteins Adsorbed on Graphite , 2004 .

[27]  X. Gong,et al.  A charge-driven molecular water pump. , 2007, Nature nanotechnology.

[28]  Ruhong Zhou,et al.  Hydrophobic Collapse in Multidomain Protein Folding , 2004, Science.

[29]  Haiping Fang,et al.  Carbon Nanotube Wins the Competitive Binding over Proline-Rich Motif Ligand on SH3 Domain , 2011 .

[30]  Ruhong Zhou,et al.  Thermal denaturing of mutant lysozyme with both the OPLSAA and the CHARMM force fields. , 2006, Journal of the American Chemical Society.

[31]  N. Mohanty,et al.  Graphene-based single-bacterium resolution biodevice and DNA transistor: interfacing graphene derivatives with nanoscale and microscale biocomponents. , 2008, Nano letters.

[32]  W. Kabsch,et al.  Dictionary of protein secondary structure: Pattern recognition of hydrogen‐bonded and geometrical features , 1983, Biopolymers.

[33]  Effect of Curvature on the α-Helix Breaking Tendency of Carbon Based Nanomaterials , 2011 .

[34]  V. Subramanian,et al.  Exploring the changes in the structure of α-helical peptides adsorbed onto a single walled carbon nanotube using classical molecular dynamics simulation. , 2010, The journal of physical chemistry. B.

[35]  Guanghong Wei,et al.  Atomic-level study of adsorption, conformational change, and dimerization of an α-helical peptide at graphene surface. , 2011, The journal of physical chemistry. B.

[36]  Chunhai Fan,et al.  Graphene-based antibacterial paper. , 2010, ACS nano.

[37]  Ravi S Kane,et al.  Structure and function of enzymes adsorbed onto single-walled carbon nanotubes. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[38]  Valerie Daggett,et al.  The complete folding pathway of a protein from nanoseconds to microseconds , 2003, Nature.

[39]  Regine Herbst-Irmer,et al.  High-resolution x-ray crystal structures of the villin headpiece subdomain, an ultrafast folding protein. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Ruhong Zhou,et al.  Observation of a dewetting transition in the collapse of the melittin tetramer , 2005, Nature.

[41]  Hydration and dewetting near fluorinated superhydrophobic plates. , 2006, Journal of the American Chemical Society.

[42]  Carlos F. Lopez,et al.  Hydrophobicity of protein surfaces: Separating geometry from chemistry , 2008, Proceedings of the National Academy of Sciences.

[43]  A. Roitberg,et al.  Coupling of replica exchange simulations to a non-Boltzmann structure reservoir. , 2007, The journal of physical chemistry. B.

[44]  Rongzheng Wan,et al.  Stable liquid water droplet on a water monolayer formed at room temperature on ionic model substrates. , 2009, Physical review letters.

[45]  Daisuke Fujita,et al.  Perspectives and challenges of emerging single-molecule DNA sequencing technologies. , 2009, Small.

[46]  Y. Chiang,et al.  Peptides with selective affinity for carbon nanotubes , 2003, Nature materials.

[47]  Ruhong Zhou,et al.  Destruction of long-range interactions by a single mutation in lysozyme , 2007, Proceedings of the National Academy of Sciences.

[48]  Feng Zhao,et al.  Acute toxicological effects of copper nanoparticles in vivo. , 2006, Toxicology letters.

[49]  G. Hummer,et al.  Water conduction through the hydrophobic channel of a carbon nanotube , 2001, Nature.

[50]  Yang Xu,et al.  Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytoma-derived PC12 cells. , 2010, ACS nano.

[51]  Peter G Wolynes,et al.  Protein topology determines binding mechanism. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Xu Wang,et al.  Application of Nanotechnology in Cancer Therapy and Imaging , 2008, CA: a cancer journal for clinicians.

[53]  T. Xia,et al.  Toxic Potential of Materials at the Nanolevel , 2006, Science.

[54]  Rongzheng Wan,et al.  Water-mediated signal multiplication with Y-shaped carbon nanotubes , 2009, Proceedings of the National Academy of Sciences.

[55]  Wei Zhang,et al.  A point‐charge force field for molecular mechanics simulations of proteins based on condensed‐phase quantum mechanical calculations , 2003, J. Comput. Chem..

[56]  Tiffany R. Walsh,et al.  Modeling the Binding Affinity of Peptides for Graphitic Surfaces. Influences of Aromatic Content and Interfacial Shape , 2009 .

[57]  Ruhong Zhou,et al.  Replica exchange with solute tempering: efficiency in large scale systems. , 2007, The journal of physical chemistry. B.

[58]  Hui Xie,et al.  Importance of aromatic content for peptide/single-walled carbon nanotube interactions. , 2005, Journal of the American Chemical Society.

[59]  Joseph A. Bank,et al.  Supporting Online Material Materials and Methods Figs. S1 to S10 Table S1 References Movies S1 to S3 Atomic-level Characterization of the Structural Dynamics of Proteins , 2022 .

[60]  Wei Wang,et al.  Folding of a small RNA hairpin based on simulation with replica exchange molecular dynamics. , 2010, The journal of physical chemistry. B.

[61]  A. Marcelli,et al.  Bio-nano interaction of proteins adsorbed on single-walled carbon nanotubes , 2009 .

[62]  L. Mirny,et al.  Protein folding theory: from lattice to all-atom models. , 2001, Annual review of biophysics and biomolecular structure.

[63]  Huang-Hao Yang,et al.  A graphene platform for sensing biomolecules. , 2009, Angewandte Chemie.

[64]  N. Gilbert.  Nanoparticle safety in doubt , 2009, Nature.

[65]  Wei Yang,et al.  A Structure-Based Model for the Synthesis and Hydrolysis of ATP by F1-ATPase , 2005, Cell.

[66]  J. Vandekerckhove,et al.  Villin Function in the Organization of the Actin Cytoskeleton , 1999, The Journal of Biological Chemistry.