Controlling the Stealth Effect of Nanocarriers through Understanding the Protein Corona.

The past decade has seen a significant increase in interest in the use of polymeric nanocarriers in medical applications. In particular, when used as drug vectors in targeted delivery, nanocarriers could overcome many obstacles for drug therapy. Nevertheless, their application is still impeded by the complex composition of the blood proteins covering the particle surface, termed the protein corona. The protein corona complicates any prediction of cell interactions, biodistribution, and toxicity. In particular, the unspecific uptake of nanocarriers is a major obstacle in clinical studies. This Minireview provides an overview of what we currently know about the characteristics of the protein corona of nanocarriers, with a focus on surface functionalization that reduces unspecific uptake (the stealth effect). The ongoing improvement of nanocarriers to allow them to meet all the requirements necessary for successful application, including targeted delivery and stealth, are further discussed.

[1]  Shu Zhang,et al.  Preformed albumin corona, a protective coating for nanoparticles based drug delivery system. , 2013, Biomaterials.

[2]  M. Ferrari,et al.  The nano-plasma interface: Implications of the protein corona. , 2014, Colloids and surfaces. B, Biointerfaces.

[3]  Shi-zhong Luo,et al.  Microfabrication of a new sensor based on silver and silicon nanomaterials, and its application to the enrichment and detection of bovine serum albumin via surface-enhanced Raman scattering , 2009 .

[4]  M. Mahmoudi,et al.  Large Protein Absorptions from Small Changes on the Surface of Nanoparticles , 2011 .

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

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

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

[8]  Albert Duschl,et al.  Time evolution of the nanoparticle protein corona. , 2010, ACS nano.

[9]  Sherief Essa,et al.  Characterization of rhodamine loaded PEG-g-PLA nanoparticles (NPs): effect of poly(ethylene glycol) grafting density. , 2011, International journal of pharmaceutics.

[10]  P. Couvreur,et al.  Low-density lipoprotein receptor-mediated endocytosis of PEGylated nanoparticles in rat brain endothelial cells , 2007, Cellular and Molecular Life Sciences.

[11]  Theresa M. Allen,et al.  Pharmacokinetics of long-circulating liposomes , 1995 .

[12]  I. Delfino,et al.  Optical investigation of the electron transfer protein azurin-gold nanoparticle system. , 2009, Biophysical chemistry.

[13]  C. Lok,et al.  The transferrin receptor: role in health and disease. , 1999, The international journal of biochemistry & cell biology.

[14]  Kazuo Maruyama,et al.  Amphipathic polyethyleneglycols effectively prolong the circulation time of liposomes , 1990, FEBS letters.

[15]  Sara Linse,et al.  Detailed identification of plasma proteins adsorbed on copolymer nanoparticles. , 2007, Angewandte Chemie.

[16]  R. Müller,et al.  Adsorption kinetics of plasma proteins on oil-in-water emulsions for parenteral nutrition. , 2000, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[17]  J. Kreuter,et al.  Covalent attachment of apolipoprotein A-I and apolipoprotein B-100 to albumin nanoparticles enables drug transport into the brain. , 2007, Journal of controlled release : official journal of the Controlled Release Society.

[18]  Mitsuru Hashida,et al.  Fetuin mediates hepatic uptake of negatively charged nanoparticles via scavenger receptor. , 2007, International journal of pharmaceutics.

[19]  K. Landfester,et al.  (Oligo)mannose functionalized hydroxyethyl starch nanocapsules: en route to drug delivery systems with targeting properties. , 2013, Journal of materials chemistry. B.

[20]  Katharina Landfester,et al.  Differential uptake of functionalized polystyrene nanoparticles by human macrophages and a monocytic cell line. , 2011, ACS nano.

[21]  A S Hoffman,et al.  Reduction of fibrinogen adsorption on PEG-coated polystyrene surfaces. , 1992, Journal of biomedical materials research.

[22]  A. Roque,et al.  Anti-CD8 conjugated nanoparticles to target mammalian cells expressing CD8. , 2010, International journal of pharmaceutics.

[23]  K. Landfester,et al.  Surface roughness and charge influence the uptake of nanoparticles: fluorescently labeled pickering-type versus surfactant-stabilized nanoparticles. , 2012, Macromolecular bioscience.

[24]  K. Landfester,et al.  Criteria impacting the cellular uptake of nanoparticles: a study emphasizing polymer type and surfactant effects. , 2011, Acta biomaterialia.

[25]  K. Kataoka,et al.  Size-dependent knockdown potential of siRNA-loaded cationic nanohydrogel particles. , 2014, Biomacromolecules.

[26]  M. Krieger,et al.  Role of apoA-I, ABCA1, LCAT, and SR-BI in the biogenesis of HDL , 2006, Journal of Molecular Medicine.

[27]  W. Semmler,et al.  Determination of Plasma Protein Adsorption on Magnetic Iron Oxides: Sample Preparation , 1997, Pharmaceutical Research.

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

[29]  Yoon Yeo,et al.  Recent advances in stealth coating of nanoparticle drug delivery systems. , 2012, Wiley interdisciplinary reviews. Nanomedicine and nanobiotechnology.

[30]  L. Vroman,et al.  Effect of Adsorbed Proteins on the Wettability of Hydrophilic and Hydrophobic Solids , 1962, Nature.

[31]  Christine K Payne,et al.  Nanoparticle surface charge mediates the cellular receptors used by protein-nanoparticle complexes. , 2012, The journal of physical chemistry. B.

[32]  Giulio Caracciolo,et al.  Time evolution of nanoparticle-protein corona in human plasma: relevance for targeted drug delivery. , 2013, Langmuir : the ACS journal of surfaces and colloids.

[33]  Morteza Mahmoudi,et al.  Engineered nanoparticles for biomolecular imaging. , 2011, Nanoscale.

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

[35]  Morteza Mahmoudi,et al.  Protein-Nanoparticle Interactions , 2013 .

[36]  Chad A Mirkin,et al.  Scavenger receptors mediate cellular uptake of polyvalent oligonucleotide-functionalized gold nanoparticles. , 2010, Bioconjugate chemistry.

[37]  Darren J. Martin,et al.  Differential plasma protein binding to metal oxide nanoparticles , 2009, Nanotechnology.

[38]  K. Landfester,et al.  Hematopoietic and mesenchymal stem cells: polymeric nanoparticle uptake and lineage differentiation , 2015, Beilstein journal of nanotechnology.

[39]  K. Landfester,et al.  Nanocapsules generated out of a polymeric dexamethasone shell suppress the inflammatory response of liver macrophages. , 2013, Nanomedicine : nanotechnology, biology, and medicine.

[40]  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.

[41]  José M. Morachis,et al.  Physical and Chemical Strategies for Therapeutic Delivery by Using Polymeric Nanoparticles , 2012, Pharmacological Reviews.

[42]  Katharina Landfester,et al.  Protein adsorption is required for stealth effect of poly(ethylene glycol)- and poly(phosphoester)-coated nanocarriers. , 2016, Nature nanotechnology.

[43]  J. K. Kruijt,et al.  Selective liver targeting of antivirals by recombinant chylomicrons — a new therapeutic approach to hepatitis B , 1995, Nature Medicine.

[44]  T. Groth,et al.  Characterization of PLGA nanospheres stabilized with amphiphilic polymers: hydrophobically modified hydroxyethyl starch vs pluronics. , 2009, Molecular pharmaceutics.

[45]  Jack F Douglas,et al.  Interaction of gold nanoparticles with common human blood proteins. , 2010, ACS nano.

[46]  T. Ishida,et al.  Anti-polyethyleneglycol antibody response to PEGylated substances. , 2013, Biological & pharmaceutical bulletin.

[47]  Wolfgang J Parak,et al.  A quantitative fluorescence study of protein monolayer formation on colloidal nanoparticles. , 2009, Nature nanotechnology.

[48]  Akhilesh Pandey,et al.  Plasma Proteome Database as a resource for proteomics research , 2005, Proteomics.

[49]  K. Landfester,et al.  Pharmacokinetics on a microscale: visualizing Cy5-labeled oligonucleotide release from poly(n-butylcyanoacrylate) nanocapsules in cells , 2014, International journal of nanomedicine.

[50]  K. Landfester,et al.  Uptake mechanism of oppositely charged fluorescent nanoparticles in HeLa cells. , 2008, Macromolecular bioscience.

[51]  Nicolas Bertrand,et al.  The journey of a drug-carrier in the body: an anatomo-physiological perspective. , 2012, Journal of controlled release : official journal of the Controlled Release Society.

[52]  M. Michaelis,et al.  Covalent Linkage of Apolipoprotein E to Albumin Nanoparticles Strongly Enhances Drug Transport into the Brain , 2006, Journal of Pharmacology and Experimental Therapeutics.

[53]  D. Hochstrasser,et al.  Kinetics of plasma protein adsorption on model particles for controlled drug delivery and drug targeting , 1996 .

[54]  Anil K Patri,et al.  Protein corona composition does not accurately predict hematocompatibility of colloidal gold nanoparticles. , 2014, Nanomedicine : nanotechnology, biology, and medicine.

[55]  K. Dawson,et al.  Magnetic nanoparticles to recover cellular organelles and study the time resolved nanoparticle-cell interactome throughout uptake. , 2014, Small.

[56]  K. Chittur,et al.  FTIR/ATR for protein adsorption to biomaterial surfaces. , 1998, Biomaterials.

[57]  N. Anderson,et al.  The Human Plasma Proteome , 2002, Molecular & Cellular Proteomics.

[58]  R. Müller,et al.  Nanoparticles with decreasing surface hydrophobicities: influence on plasma protein adsorption. , 2000, International journal of pharmaceutics.

[59]  Jean-Pierre Benoit,et al.  Parameters influencing the stealthiness of colloidal drug delivery systems. , 2006, Biomaterials.

[60]  K. Landfester,et al.  Protein source and choice of anticoagulant decisively affect nanoparticle protein corona and cellular uptake. , 2016, Nanoscale.

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

[62]  Stefan Tenzer,et al.  Protein corona of nanoparticles: distinct proteins regulate the cellular uptake. , 2015, Biomacromolecules.

[63]  Rassoul Dinarvand,et al.  Characterization, blood profile and biodistribution properties of surface modified PLGA nanoparticles of SN-38. , 2011, International journal of pharmaceutics.

[64]  E. Brun,et al.  Could nanoparticle corona characterization help for biological consequence prediction? , 2014, Cancer Nanotechnology.

[65]  A. Dasgupta,et al.  Interaction of hemoglobin and copper nanoparticles: implications in hemoglobinopathy. , 2006, Nanomedicine : nanotechnology, biology, and medicine.

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

[67]  K. Williams,et al.  Effects of apolipoproteins A-IV and A-I on the uptake of phospholipid liposomes by hepatocytes. , 1989, The Journal of biological chemistry.

[68]  W. Kreyling,et al.  Serum protein identification and quantification of the corona of 5, 15 and 80 nm gold nanoparticles , 2013, Nanotechnology.

[69]  Philip M. Kelly,et al.  Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. , 2013, Nature nanotechnology.

[70]  Sara Linse,et al.  Complete high‐density lipoproteins in nanoparticle corona , 2009, The FEBS journal.

[71]  Sara Linse,et al.  Modeling the Time Evolution of the Nanoparticle-Protein Corona in a Body Fluid , 2010, PloS one.

[72]  Samir Mitragotri,et al.  Overcoming the challenges in administering biopharmaceuticals: formulation and delivery strategies , 2014, Nature Reviews Drug Discovery.

[73]  P. Couvreur,et al.  Analysis of plasma protein adsorption onto PEGylated nanoparticles by complementary methods: 2‐DE, CE and Protein Lab‐on‐chip® system , 2007, Electrophoresis.

[74]  M. Mahmoudi,et al.  Significance of cell "observer" and protein source in nanobiosciences. , 2013, Journal of colloid and interface science.

[75]  James L. McGrath,et al.  The influence of protein adsorption on nanoparticle association with cultured endothelial cells. , 2009, Biomaterials.

[76]  R. Müller,et al.  Adsorption kinetics of plasma proteins on solid lipid nanoparticles for drug targeting. , 2005, International journal of pharmaceutics.

[77]  Joseph D. Andrade,et al.  Protein—surface interactions in the presence of polyethylene oxide , 1991 .

[78]  Istvan Toth,et al.  Nanoparticle-induced unfolding of fibrinogen promotes Mac-1 receptor activation and inflammation. , 2011, Nature nanotechnology.

[79]  Feng Zhang,et al.  Quantitative analysis of the protein corona on FePt nanoparticles formed by transferrin binding , 2010, Journal of The Royal Society Interface.

[80]  Mark E. Davis,et al.  Nanoparticle therapeutics: an emerging treatment modality for cancer , 2008, Nature Reviews Drug Discovery.

[81]  Katharina Landfester,et al.  Kohlenhydrat‐basierte Nanocarrier mit spezifischem Zell‐Targeting und minimalem Einfluss durch die Proteinkorona , 2015 .

[82]  Kenneth A Dawson,et al.  Nanoparticle adhesion to the cell membrane and its effect on nanoparticle uptake efficiency. , 2013, Journal of the American Chemical Society.

[83]  T. Xia,et al.  Understanding biophysicochemical interactions at the nano-bio interface. , 2009, Nature materials.

[84]  J. Diederichs,et al.  Plasma protein adsorption patterns on liposomes: Establishment of analytical procedure , 1996, Electrophoresis.

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

[86]  K. Landfester,et al.  Carbohydrate-Based Nanocarriers Exhibiting Specific Cell Targeting with Minimum Influence from the Protein Corona. , 2015, Angewandte Chemie.

[87]  Kenneth A. Dawson,et al.  Transferrin Coated Nanoparticles: Study of the Bionano Interface in Human Plasma , 2012, PloS one.

[88]  R. Müller,et al.  'Stealth' corona-core nanoparticles surface modified by polyethylene glycol (PEG): influences of the corona (PEG chain length and surface density) and of the core composition on phagocytic uptake and plasma protein adsorption. , 2000, Colloids and surfaces. B, Biointerfaces.

[89]  Y. Barenholz Doxil®--the first FDA-approved nano-drug: lessons learned. , 2012, Journal of controlled release : official journal of the Controlled Release Society.

[90]  William M. Lee,et al.  Efficacy and safety of pegylated (40‐kd) interferon α‐2a compared with interferon α‐2a in noncirrhotic patients with chronic hepatitis C , 2001 .

[91]  Mansoor M Amiji,et al.  Multi-functional polymeric nanoparticles for tumour-targeted drug delivery , 2006, Expert opinion on drug delivery.

[92]  K. Landfester,et al.  Tailoring the stealth properties of biocompatible polysaccharide nanocontainers. , 2015, Biomaterials.

[93]  G. Nienhaus,et al.  Toward a molecular understanding of nanoparticle–protein interactions , 2012, Biophysical Reviews.

[94]  Liping Sun,et al.  Conjugating folic acid to gold nanoparticles through glutathione for targeting and detecting cancer cells. , 2010, Bioorganic & medicinal chemistry.

[95]  Christoffer Åberg,et al.  Mapping protein binding sites on the biomolecular corona of nanoparticles. , 2015, Nature nanotechnology.

[96]  K. Landfester,et al.  Complementary analysis of the hard and soft protein corona: sample preparation critically effects corona composition. , 2015, Nanoscale.

[97]  V. Rotello,et al.  Engineering the nanoparticle-protein interface for cancer therapeutics. , 2015, Cancer treatment and research.

[98]  Takuro Niidome,et al.  PEG-modified gold nanorods with a stealth character for in vivo applications. , 2006, Journal of controlled release : official journal of the Controlled Release Society.

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

[100]  S. Retterer,et al.  Dynamic development of the protein corona on silica nanoparticles: composition and role in toxicity. , 2013, Nanoscale.

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

[102]  F. Davis,et al.  Effect of covalent attachment of polyethylene glycol on immunogenicity and circulating life of bovine liver catalase. , 1977, The Journal of biological chemistry.

[103]  C. Royer Probing protein folding and conformational transitions with fluorescence. , 2006, Chemical reviews.

[104]  Patrick Couvreur,et al.  Translocation of poly(ethylene glycol-co-hexadecyl)cyanoacrylate nanoparticles into rat brain endothelial cells: role of apolipoproteins in receptor-mediated endocytosis. , 2007, Biomacromolecules.

[105]  C. Werner,et al.  Adsorption-induced conformational changes of proteins onto ceramic particles: differential scanning calorimetry and FTIR analysis. , 2006, Journal of colloid and interface science.

[106]  Parag Aggarwal,et al.  Nanoparticle interaction with plasma proteins as it relates to particle biodistribution, biocompatibility and therapeutic efficacy. , 2009, Advanced drug delivery reviews.

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

[108]  Jianjun Cheng,et al.  Protein corona significantly reduces active targeting yield. , 2013, Chemical communications.

[109]  S. Tenzer,et al.  Mass spectrometry and imaging analysis of nanoparticle-containing vesicles provide a mechanistic insight into cellular trafficking. , 2014, ACS nano.

[110]  Cheng Zong,et al.  Label-free detection of native proteins by surface-enhanced Raman spectroscopy using iodide-modified nanoparticles. , 2014, Analytical chemistry.

[111]  L. Balant,et al.  Kinetics of blood component adsorption on poly(D,L-lactic acid) nanoparticles: evidence of complement C3 component involvement. , 1997, Journal of biomedical materials research.

[112]  K. Higaki,et al.  Time-dependent changes in opsonin amount associated on nanoparticles alter their hepatic uptake characteristics. , 2007, International journal of pharmaceutics.

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

[114]  Rainer H Müller,et al.  Functional groups on polystyrene model nanoparticles: influence on protein adsorption. , 2003, Journal of biomedical materials research. Part A.

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

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

[117]  M. Lück,et al.  Analysis of plasma protein adsorption on polymeric nanoparticles with different surface characteristics. , 1998, Journal of biomedical materials research.

[118]  K. Landfester,et al.  BSA adsorption on differently charged polystyrene nanoparticles using isothermal titration calorimetry and the influence on cellular uptake. , 2011, Macromolecular bioscience.

[119]  Jonathan S Dordick,et al.  Silica nanoparticle size influences the structure and enzymatic activity of adsorbed lysozyme. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[120]  Morteza Mahmoudi,et al.  Irreversible changes in protein conformation due to interaction with superparamagnetic iron oxide nanoparticles. , 2011, Nanoscale.

[121]  Madhusudhan R. Papasani,et al.  Gold-peptide nanoconjugate cellular uptake is modulated by serum proteins. , 2012, Nanomedicine : nanotechnology, biology, and medicine.

[122]  D. Begley,et al.  Albumin nanoparticles targeted with Apo E enter the CNS by transcytosis and are delivered to neurones. , 2009, Journal of controlled release : official journal of the Controlled Release Society.

[123]  Ying Liu,et al.  Biosafety and bioapplication of nanomaterials by designing protein-nanoparticle interactions. , 2013, Small.

[124]  Iseult Lynch,et al.  The evolution of the protein corona around nanoparticles: a test study. , 2011, ACS nano.

[125]  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.

[126]  Peter Wick,et al.  The adsorption of biomolecules to multi-walled carbon nanotubes is influenced by both pulmonary surfactant lipids and surface chemistry , 2010, Journal of nanobiotechnology.

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

[128]  T. Ishida,et al.  Injection of PEGylated liposomes in rats elicits PEG-specific IgM, which is responsible for rapid elimination of a second dose of PEGylated liposomes. , 2006, Journal of controlled release : official journal of the Controlled Release Society.

[129]  R. Müller,et al.  Adsorption kinetics of plasma proteins on ultrasmall superparamagnetic iron oxide (USPIO) nanoparticles. , 2012, International journal of pharmaceutics.

[130]  Jing Bai,et al.  Cellular uptake of nanoparticles by membrane penetration: a study combining confocal microscopy with FTIR spectroelectrochemistry. , 2012, ACS nano.

[131]  Shaojun Dong,et al.  pH-dependent protein conformational changes in albumin:gold nanoparticle bioconjugates: a spectroscopic study. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[132]  Morteza Mahmoudi,et al.  Personalized protein coronas: a "key" factor at the nanobiointerface. , 2014, Biomaterials science.

[133]  N. Adkinson,et al.  Hypersensitivity to Polyethylene Glycols , 2013, Journal of clinical pharmacology.

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

[135]  Sara Linse,et al.  Understanding the nanoparticle–protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles , 2007, Proceedings of the National Academy of Sciences.

[136]  David Goldstein,et al.  Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. , 2013, The New England journal of medicine.

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

[138]  G. Borghs,et al.  Gold nanoparticle dimers for plasmon sensing. , 2011, Langmuir : the ACS journal of surfaces and colloids.

[139]  L. Vroman,et al.  Interaction of high molecular weight kininogen, factor XII, and fibrinogen in plasma at interfaces. , 1980, Blood.

[140]  K. Landfester,et al.  Suppressing unspecific cell uptake for targeted delivery using hydroxyethyl starch nanocapsules. , 2012, Biomacromolecules.

[141]  Kenneth A. Dawson,et al.  Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. , 2012, ACS nano.

[142]  Stefan Tenzer,et al.  Nanoparticle size is a critical physicochemical determinant of the human blood plasma corona: a comprehensive quantitative proteomic analysis. , 2011, ACS nano.