Regulation of Macrophage Recognition through the Interplay of Nanoparticle Surface Functionality and Protein Corona.

Using a family of cationic gold nanoparticles (NPs) with similar size and charge, we demonstrate that proper surface engineering can control the nature and identity of protein corona in physiological serum conditions. The protein coronas were highly dependent on the hydrophobicity and arrangement of chemical motifs on NP surface. The NPs were uptaken in macrophages in a corona-dependent manner, predominantly through recognition of specific complement proteins in the NP corona. Taken together, this study shows that surface functionality can be used to tune the protein corona formed on NP surface, dictating the interaction of NPs with macrophages.

[1]  V. Rotello,et al.  Beauty is skin deep: a surface monolayer perspective on nanoparticle interactions with cells and bio-macromolecules. , 2011, Small.

[2]  Robert Langer,et al.  Degradable Lipid Nanoparticles with Predictable In Vivo siRNA Delivery Activity , 2014, Nature Communications.

[3]  Farhad Rezaee,et al.  Proteomic analysis of high‐density lipoprotein , 2006, Proteomics.

[4]  Denis Hochstrasser,et al.  How shall we use the proteomics toolbox for biomarker discovery? , 2007, Journal of proteome research.

[5]  K. Hamad-Schifferli,et al.  Protein coronas on gold nanorods passivated with amphiphilic ligands affect cytotoxicity and cellular response to penicillin/streptomycin. , 2014, ACS nano.

[6]  Elodie Boisselier,et al.  Gold nanoparticles in nanomedicine: preparations, imaging, diagnostics, therapies and toxicity. , 2009, Chemical Society reviews.

[7]  Nicholas A Peppas,et al.  Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. , 2006, International journal of pharmaceutics.

[8]  V. Puntes,et al.  Inorganic nanoparticle biomolecular corona: formation, evolution and biological impact. , 2012, Nanomedicine.

[9]  Iseult Lynch,et al.  What the cell "sees" in bionanoscience. , 2010, Journal of the American Chemical Society.

[10]  Andrew Emili,et al.  Nanoparticle size and surface chemistry determine serum protein adsorption and macrophage uptake. , 2012, Journal of the American Chemical Society.

[11]  Vincent M Rotello,et al.  Intracellular delivery of a membrane-impermeable enzyme in active form using functionalized gold nanoparticles. , 2010, Journal of the American Chemical Society.

[12]  M. Mahmoudi,et al.  Superparamagnetic iron oxide nanoparticles (SPIONs): development, surface modification and applications in chemotherapy. , 2011, Advanced drug delivery reviews.

[13]  Christopher J. Kiely,et al.  Synthesis and reactions of functionalised gold nanoparticles , 1995 .

[14]  A. Blom,et al.  Vitamin K-Dependent Protein S Localizing Complement Regulator C4b-Binding Protein to the Surface of Apoptotic Cells1 , 2002, The Journal of Immunology.

[15]  V. Rotello,et al.  Electrostatic selectivity in protein-nanoparticle interactions. , 2011, Biomacromolecules.

[16]  James Chen Yong Kah,et al.  Optimizing the properties of the protein corona surrounding nanoparticles for tuning payload release. , 2013, ACS nano.

[17]  V. Rotello,et al.  Probing the protein–nanoparticle interface: the role of aromatic substitution pattern on affinity , 2015, Supramolecular chemistry.

[18]  K. Hamad-Schifferli.  Exploiting the novel properties of protein coronas: emerging applications in nanomedicine. , 2015, Nanomedicine.

[19]  A. Blom,et al.  Surface of Apoptotic Cells Complement Regulator C 4 b-Binding Protein Vitamin K-Dependent Protein S Localizing , 2002 .

[20]  Iseult Lynch,et al.  Protein-nanoparticle interactions: What does the cell see? , 2009, Nature nanotechnology.

[21]  M. Mahmoudi,et al.  Impact of protein pre-coating on the protein corona composition and nanoparticle cellular uptake. , 2016, Biomaterials.

[22]  Andrew Emili,et al.  Protein corona fingerprinting predicts the cellular interaction of gold and silver nanoparticles. , 2014, ACS nano.

[23]  Eric Pridgen,et al.  Factors Affecting the Clearance and Biodistribution of Polymeric Nanoparticles , 2008, Molecular pharmaceutics.

[24]  Pablo Del Pino,et al.  Interfacing engineered nanoparticles with biological systems: anticipating adverse nano-bio interactions. , 2013, Small.

[25]  Daniel G. Anderson,et al.  Non-viral vectors for gene-based therapy , 2014, Nature Reviews Genetics.

[26]  Eric R. Ziegel,et al.  Statistics and Chemometrics for Analytical Chemistry , 2004, Technometrics.

[27]  Vincent M Rotello,et al.  Detection and identification of proteins using nanoparticle-fluorescent polymer 'chemical nose' sensors. , 2007, Nature nanotechnology.

[28]  V. Rotello,et al.  Size and geometry dependent protein-nanoparticle self-assembly. , 2009, Chemical communications.

[29]  Alexander Kabanov,et al.  Facilitated Monocyte-Macrophage Uptake and Tissue Distribution of Superparmagnetic Iron-Oxide Nanoparticles , 2009, PloS one.

[30]  V. Rotello,et al.  Modulating Pharmacokinetics, Tumor Uptake and Biodistribution by Engineered Nanoparticles , 2011, PloS one.

[31]  Iseult Lynch,et al.  Designing the nanoparticle-biomolecule interface for "targeting and therapeutic delivery". , 2012, Journal of controlled release : official journal of the Controlled Release Society.

[32]  Morteza Mahmoudi,et al.  Protein Corona Composition of Superparamagnetic Iron Oxide Nanoparticles with Various Physico-Chemical Properties and Coatings , 2014, Scientific Reports.

[33]  Marco P Monopoli,et al.  Biomolecular coronas provide the biological identity of nanosized materials. , 2012, Nature nanotechnology.

[34]  Warren C W Chan,et al.  Understanding and controlling the interaction of nanomaterials with proteins in a physiological environment. , 2012, Chemical Society reviews.

[35]  Vincent M Rotello,et al.  Efficient gene delivery vectors by tuning the surface charge density of amino acid-functionalized gold nanoparticles. , 2008, ACS nano.

[36]  James Chen Yong Kah,et al.  Exploiting the protein corona around gold nanorods for loading and triggered release. , 2012, ACS nano.

[37]  Andrzej S Pitek,et al.  Reversible versus irreversible binding of transferrin to polystyrene nanoparticles: soft and hard corona. , 2012, ACS nano.

[38]  M. Peppelenbosch,et al.  Proteome of human plasma very low-density lipoprotein and low-density lipoprotein exhibits a link with coagulation and lipid metabolism , 2014, Thrombosis and Haemostasis.

[39]  Stefan Tenzer,et al.  Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology. , 2013, Nature nanotechnology.

[40]  V. Rotello,et al.  Protein coronas suppress the hemolytic activity of hydrophilic and hydrophobic nanoparticles. , 2014, Materials horizons.

[41]  Tamara Posati,et al.  The interplay of monolayer structure and serum protein interactions on the cellular uptake of gold nanoparticles. , 2012, Small.

[42]  Vincent M Rotello,et al.  Nano meets biology: structure and function at the nanoparticle interface. , 2011, Langmuir : the ACS journal of surfaces and colloids.

[43]  Raimo Hartmann,et al.  Temperature: the "ignored" factor at the NanoBio interface. , 2013, ACS nano.

[44]  M. Mahmoudi,et al.  Protein-nanoparticle interactions: opportunities and challenges. , 2011, Chemical reviews.

[45]  Cui Tang,et al.  Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. , 2010, Biomaterials.

[46]  Iseult Lynch,et al.  Formation and characterization of the nanoparticle-protein corona. , 2013, Methods in molecular biology.

[47]  E. Sijbrands,et al.  Characterization of coagulation factor synthesis in nine human primary cell types , 2012, Scientific Reports.

[48]  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.

[49]  Parag Aggarwal,et al.  Interaction of colloidal gold nanoparticles with human blood: effects on particle size and analysis of plasma protein binding profiles. , 2009, Nanomedicine : nanotechnology, biology, and medicine.

[50]  Sung Tae Kim,et al.  Gold nanoparticles for nucleic acid delivery. , 2014, Molecular therapy : the journal of the American Society of Gene Therapy.

[51]  Dan Peer,et al.  Nanoparticle hydrophobicity dictates immune response. , 2012, Journal of the American Chemical Society.

[52]  F. Mooi,et al.  Bordetella pertussis binds the human complement regulator C4BP: role of filamentous hemagglutinin , 1997, Infection and immunity.

[53]  M. Mahmoudi,et al.  Plasma concentration gradient influences the protein corona decoration on nanoparticles , 2013 .

[54]  Ho Sup Yoon,et al.  Co-delivery of drugs and DNA from cationic core–shell nanoparticles self-assembled from a biodegradable copolymer , 2006, Nature materials.

[55]  V. Rotello,et al.  Preparation of 2 nm gold nanoparticles for in vitro and in vivo applications. , 2013, Methods in molecular biology.

[56]  Iseult Lynch,et al.  Physical-chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. , 2011, Journal of the American Chemical Society.

[57]  E. Johnsson,et al.  A highly variable region in members of the streptococcal M protein family binds the human complement regulator C4BP. , 1996, Journal of Immunology.

[58]  J. Vallée,et al.  Ex situ evaluation of the composition of protein corona of intravenously injected superparamagnetic nanoparticles in rats. , 2014, Nanoscale.

[59]  A. Blom,et al.  C4b-binding Protein and Factor H Compensate for the Loss of Membrane-bound Complement Inhibitors to Protect Apoptotic Cells against Excessive Complement Attack* , 2007, Journal of Biological Chemistry.

[60]  Marc D. Porter,et al.  Alkanethiolate Gold Cluster Molecules with Core Diameters from 1.5 to 5.2 nm: Core and Monolayer Properties as a Function of Core Size , 1998 .

[61]  Bruno F B Silva,et al.  Uptake and transfection efficiency of PEGylated cationic liposome-DNA complexes with and without RGD-tagging. , 2014, Biomaterials.

[62]  G. Lindahl,et al.  Ig-binding surface proteins of Streptococcus pyogenes also bind human C4b-binding protein (C4BP), a regulatory component of the complement system. , 1995, Journal of immunology.