Interaction of gold nanoparticles with common human blood proteins.

In order to better understand the physical basis of the biological activity of nanoparticles (NPs) in nanomedicine applications and under conditions of environmental exposure, we performed an array of photophysical measurements to quantify the interaction of model gold NPs having a wide range of NP diameters with common blood proteins. In particular, absorbance, fluorescence quenching, circular dichroism, dynamic light scattering, and electron microscopy measurements were performed on surface-functionalized water-soluble gold NPs having a diameter range from 5 to 100 nm in the presence of common human blood proteins: albumin, fibrinogen, gamma-globulin, histone, and insulin. We find that the gold NPs strongly associate with these essential blood proteins where the binding constant, K, as well as the degree of cooperativity of particle--protein binding (Hill constant, n), depends on particle size and the native protein structure. We also find tentative evidence that the model proteins undergo conformational change upon association with the NPs and that the thickness of the adsorbed protein layer (bare NP diameter <50 nm) progressively increases with NP size, effects that have potential general importance for understanding NP aggregation in biological media and the interaction of NP with biological materials broadly.

[1]  A. Heeger,et al.  Beyond superquenching: Hyper-efficient energy transfer from conjugated polymers to gold nanoparticles , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[2]  J. Lakowicz Principles of fluorescence spectroscopy , 1983 .

[3]  L. Libertini,et al.  The intrinsic tyrosine fluorescence of histone H1. Steady state and fluorescence decay studies reveal heterogeneous emission. , 1985, Biophysical Journal.

[4]  F. Cui,et al.  Fluorescent investigation of the interactions between N-(p-chlorophenyl)-N'-(1-naphthyl) thiourea and serum albumin: synchronous fluorescence determination of serum albumin. , 2006, Analytica chimica acta.

[5]  K. Dawson,et al.  Interaction of soft condensed materials with living cells: Phenotype/transcriptome correlations for the hydrophobic effect , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Xiaohuan Zang,et al.  Interaction of Tetrandrine with Human Serum Albumin: a Fluorescence Quenching Study , 2007, Analytical sciences : the international journal of the Japan Society for Analytical Chemistry.

[7]  Yuan Tian,et al.  Studies on the interaction of colloidal gold and serum albumins by spectral methods. , 2005, Spectrochimica acta. Part A, Molecular and biomolecular spectroscopy.

[8]  S. Moncheva,et al.  Intrinsic Tryptophan Fluorescence of Human Serum Proteins and Related Conformational Changes , 2000, Journal of protein chemistry.

[9]  L. Greillier,et al.  Mesothelioma and Asbestos-Related Pleural Diseases , 2008, Respiration.

[10]  M. J. Swamy,et al.  Interaction of the major protein from bovine seminal plasma, PDC-109 with phospholipid membranes and soluble ligands investigated by fluorescence approaches. , 2008, Biochimica et biophysica acta.

[11]  J. A. Forrest,et al.  Size-dependent denaturing kinetics of bovine serum albumin adsorbed onto gold nanospheres , 2008, The European physical journal. E, Soft matter.

[12]  P. Courtoy,et al.  A model of protein-colloidal gold interactions. , 1987, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[13]  M. Karlsson,et al.  Protein adsorption orientation in the light of fluorescent probes: mapping of the interaction between site-directly labeled human carbonic anhydrase II and silica nanoparticles. , 2005, Biophysical journal.

[14]  Enrique M. De La Cruz,et al.  Cofilin binding to muscle and non-muscle actin filaments: isoform-dependent cooperative interactions. , 2005 .

[15]  J. West,et al.  Immunotargeted nanoshells for integrated cancer imaging and therapy. , 2005, Nano letters.

[16]  Laser-induced fluorescence quenching of tagged oligonucleotide probes by gold nanoparticles , 2005 .

[17]  M. El-Sayed,et al.  Tryptophan fluorescence quenching as a monitor for the protein conformation changes occurring during the photocycle of bacteriorhodopsin under different perturbations. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Martin W Goldberg Immunolabeling for scanning electron microscopy (SEM) and field emission SEM. , 2008, Methods in cell biology.

[19]  B. Jonsson,et al.  Proteolytic cleavage reveals interaction patterns between silica nanoparticles and two variants of human carbonic anhydrase. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[20]  D. Reinhoudt,et al.  Fluorescence quenching of dye molecules near gold nanoparticles: radiative and nonradiative effects. , 2002, Physical review letters.

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

[22]  S. Radford,et al.  Nucleation of protein fibrillation by nanoparticles , 2007, Proceedings of the National Academy of Sciences.

[23]  David Farrar,et al.  Interpretation of protein adsorption: surface-induced conformational changes. , 2005, Journal of the American Chemical Society.

[24]  H. Dai,et al.  PEG branched polymer for functionalization of nanomaterials with ultralong blood circulation. , 2009, Journal of the American Chemical Society.

[25]  A V Hill The Combinations of Haemoglobin with Oxygen and Carbon Monoxide, and the effects of Acid and Carbon Dioxide. , 1921, The Biochemical journal.

[26]  Prashant K. Jain,et al.  On the Universal Scaling Behavior of the Distance Decay of Plasmon Coupling in Metal Nanoparticle Pairs: A Plasmon Ruler Equation , 2007 .

[27]  C. Mirkin Programming the assembly of two- and three-dimensional architectures with DNA and nanoscale inorganic building blocks. , 2000, Inorganic chemistry.

[28]  Benjamin G Keselowsky,et al.  Surface chemistry modulates fibronectin conformation and directs integrin binding and specificity to control cell adhesion. , 2003, Journal of biomedical materials research. Part A.

[29]  C. Suri,et al.  Synthesis and capping of water-dispersed gold nanoparticles by an amino acid: bioconjugation and binding studies. , 2008, Journal of colloid and interface science.

[30]  Kenneth A. Dawson,et al.  Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts , 2008, Proceedings of the National Academy of Sciences.

[31]  Ravi S Kane,et al.  The protein-nanomaterial interface. , 2006, Current opinion in biotechnology.

[32]  Zhike He,et al.  Conformation, thermodynamics and stoichiometry of HSA adsorbed to colloidal CdSe/ZnS quantum dots. , 2008, Biochimica et biophysica acta.

[33]  Y. Ikeda,et al.  Dominant Negative Role of the Glutamic Acid Residue Conserved in the Pyruvate Kinase M1 Isozyme in the Heterotropic Allosteric Effect Involving Fructose-1,6-bisphosphate* , 2000, The Journal of Biological Chemistry.

[34]  Anjali Pal,et al.  Fluorescence quenching of 1-methylaminopyrene near gold nanoparticles: size regime dependence of the small metallic particles , 2004 .

[35]  D. E. Benson,et al.  General, high-affinity approach for the synthesis of fluorophore appended protein nanoparticle assemblies. , 2005, Chemical communications.

[36]  B. Jonsson,et al.  Adsorption of Human Carbonic Anhydrase II Variants to Silica Nanoparticles Occur Stepwise: Binding Is Followed by Successive Conformational Changes to a Molten-Globule-like State , 2000 .

[37]  G. Berdyshev,et al.  Intrinsic fluorescence, difference spectrophotometry and theoretical studies on tertiary structure of calf thymus histone H1. , 1985, The International journal of biochemistry.

[38]  S. Ragsdale,et al.  A conformational change in the methyltransferase from Clostridium thermoaceticum facilitates the methyl transfer from (6S)-methyltetrahydrofolate to the corrinoid/iron-sulfur protein in the Acetyl-CoA pathway. , 1996, Biochemistry.

[39]  D. Astruc,et al.  Gold Nanoparticles: Assembly, Supramolecular Chemistry, Quantum‐Size‐Related Properties, and Applications Toward Biology, Catalysis, and Nanotechnology. , 2004 .

[40]  A. Dasgupta,et al.  Controllable self‐assembly from fibrinogen–gold (fibrinogen–Au) and thrombin–silver (thrombin–Ag) nanoparticle interaction , 2007, FEBS letters.

[41]  J. Douglas Theoretical issues relating to thermally reversible gelation by supermolecular fiber formation. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[42]  R. Guo,et al.  Comparative studies on adsorption behavior of thionine on gold nanoparticles with different sizes. , 2008, Journal of colloid and interface science.

[43]  S. Franzen,et al.  Probing BSA binding to citrate-coated gold nanoparticles and surfaces. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[44]  Xing-Can Shen,et al.  Spectroscopic studies on the interaction between human hemoglobin and CdS quantum dots. , 2007, Journal of colloid and interface science.

[45]  A. Hill The Combinations of Haemoglobin with Oxygen and with Carbon Monoxide. I. , 1913, The Biochemical journal.

[46]  J. Lakowicz,et al.  Fluorescence Quenching of CdTe Nanocrystals by Bound Gold Nanoparticles in Aqueous Solution , 2008, Plasmonics.

[47]  Kenneth A. Dawson,et al.  Protein–Nanoparticle Interactions , 2008, Nano-Enabled Medical Applications.

[48]  Vincent M Rotello,et al.  Tunable inhibition and denaturation of alpha-chymotrypsin with amino acid-functionalized gold nanoparticles. , 2005, Journal of the American Chemical Society.

[49]  Chad A Mirkin,et al.  Maximizing DNA loading on a range of gold nanoparticle sizes. , 2006, Analytical chemistry.

[50]  J. West,et al.  Near-infrared resonant nanoshells for combined optical imaging and photothermal cancer therapy. , 2007, Nano letters.

[51]  Bengt-Harald Jonsson,et al.  Protein adsorption onto silica nanoparticles: conformational changes depend on the particles' curvature and the protein stability. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[52]  Siddhartha Roy,et al.  A cognate tRNA specific conformational change in glutaminyl‐tRNA synthetase and its implication for specificity , 1998, Protein science : a publication of the Protein Society.

[53]  M. Singh,et al.  Fluorescent lifetime quenching near d = 1.5 nm gold nanoparticles: probing NSET validity. , 2006, Journal of the American Chemical Society.

[54]  Warren C W Chan,et al.  Nanoparticle-mediated cellular response is size-dependent. , 2008, Nature nanotechnology.

[55]  B. Rosen,et al.  Tryptophan Fluorescence Reports Nucleotide-induced Conformational Changes in a Domain of the ArsA ATPase* , 1997, The Journal of Biological Chemistry.

[56]  K. Dawson,et al.  Systematic investigation of the thermodynamics of HSA adsorption to N-iso-propylacrylamide/N-tert-butylacrylamide copolymer nanoparticles. Effects of particle size and hydrophobicity. , 2007, Nano letters.

[57]  T. Kimura,et al.  Conformation-associated anomalous tyrosine fluorescence of adrenodoxin. , 1980, The Journal of biological chemistry.

[58]  Sara Linse,et al.  The nanoparticle-protein complex as a biological entity; a complex fluids and surface science challenge for the 21st century. , 2007, Advances in colloid and interface science.

[59]  L. Li,et al.  Diameter-dependent electrical transport properties of bismuth nanowire arrays , 2007 .

[60]  G. de Panfilis,et al.  Simultaneous colloidal gold immunoelectronmicroscopy labeling of CD1a, HLA-DR, and CD4 surface antigens of human epidermal Langerhans cells. , 1988, The Journal of investigative dermatology.

[61]  Vladimir P Zharov,et al.  Covalently linked Au nanoparticles to a viral vector: potential for combined photothermal and gene cancer therapy. , 2006, Nano letters.

[62]  J. Klein Probing the interactions of proteins and nanoparticles , 2007, Proceedings of the National Academy of Sciences.

[63]  A. Clayton,et al.  Site-specific tryptophan fluorescence spectroscopy as a probe of membrane peptide structure and dynamics , 2002, European Biophysics Journal.

[64]  D. Kosk-Kosicka,et al.  Spectroscopic analysis of halothane binding to the plasma membrane Ca2+-ATPase. , 1998, Biophysical journal.

[65]  Yuguang Ma,et al.  The binding of phosphorothioate oligonucleotides to CdS nanoparticles , 2003 .

[66]  Craig A. Poland,et al.  Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. , 2008, Nature nanotechnology.

[67]  Paresh Chandra Ray,et al.  Size- and distance-dependent nanoparticle surface-energy transfer (NSET) method for selective sensing of hepatitis C virus RNA. , 2009, Chemistry.

[68]  Yongan Xu,et al.  Effects of film thickness on moisture sorption, glass transition temperature and morphology of poly(chloro-p-xylylene) film , 2005 .

[69]  H. Santos,et al.  Tracking local conformational changes of ribonuclease A using picosecond time-resolved fluorescence of the six tyrosine residues. , 2007, Biophysical journal.

[70]  J Bryant,et al.  Ligand-dependent conformational equilibria of serum albumin revealed by tryptophan fluorescence quenching. , 1999, Biophysical journal.