PEGylation as a strategy for improving nanoparticle-based drug and gene delivery.

Coating the surface of nanoparticles with polyethylene glycol (PEG), or "PEGylation", is a commonly used approach for improving the efficiency of drug and gene delivery to target cells and tissues. Building from the success of PEGylating proteins to improve systemic circulation time and decrease immunogenicity, the impact of PEG coatings on the fate of systemically administered nanoparticle formulations has, and continues to be, widely studied. PEG coatings on nanoparticles shield the surface from aggregation, opsonization, and phagocytosis, prolonging systemic circulation time. Here, we briefly describe the history of the development of PEGylated nanoparticle formulations for systemic administration, including how factors such as PEG molecular weight, PEG surface density, nanoparticle core properties, and repeated administration impact circulation time. A less frequently discussed topic, we then describe how PEG coatings on nanoparticles have also been utilized for overcoming various biological barriers to efficient drug and gene delivery associated with other modes of administration, ranging from gastrointestinal to ocular. Finally, we describe both methods for PEGylating nanoparticles and methods for characterizing PEG surface density, a key factor in the effectiveness of the PEG surface coating for improving drug and gene delivery.

[1]  Clive J Roberts,et al.  Polyethylenimine-graft-poly(ethylene glycol) copolymers: influence of copolymer block structure on DNA complexation and biological activities as gene delivery system. , 2002, Bioconjugate chemistry.

[2]  J. Feijen,et al.  Polyethylene glycol-grafted polystyrene particles. , 2004, Journal of biomedical materials research. Part A.

[3]  V. Venditto,et al.  The effect of polymer backbone chemistry on the induction of the accelerated blood clearance in polymer modified liposomes. , 2015, Journal of controlled release : official journal of the Controlled Release Society.

[4]  Pascal Richette,et al.  Antibodies against polyethylene glycol in healthy subjects and in patients treated with PEG-conjugated agents , 2012, Expert opinion on drug delivery.

[5]  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.

[6]  S. Goldberg,et al.  Combined radiofrequency ablation and adjuvant liposomal chemotherapy: effect of chemotherapeutic agent, nanoparticle size, and circulation time. , 2005, Journal of vascular and interventional radiology : JVIR.

[7]  Robert Langer,et al.  PLGA-lecithin-PEG core-shell nanoparticles for controlled drug delivery. , 2009, Biomaterials.

[8]  Samuel K. Lai,et al.  Mucoadhesive Nanoparticles May Disrupt the Protective Human Mucus Barrier by Altering Its Microstructure , 2011, PloS one.

[9]  P. Davis,et al.  Cell surface nucleolin serves as receptor for DNA nanoparticles composed of pegylated polylysine and DNA. , 2008, Molecular therapy : the journal of the American Society of Gene Therapy.

[10]  E. Woolf,et al.  Immunoaffinity purification using anti-PEG antibody followed by two-dimensional liquid chromatography/tandem mass spectrometry for the quantification of a PEGylated therapeutic peptide in human plasma. , 2010, Analytical chemistry.

[11]  Soriano,et al.  The role of PEG on the stability in digestive fluids and in vivo fate of PEG-PLA nanoparticles following oral administration. , 2000, Colloids and surfaces. B, Biointerfaces.

[12]  C. Pouton,et al.  'Stealth' lipid-based formulations: poly(ethylene glycol)-mediated digestion inhibition improves oral bioavailability of a model poorly water soluble drug. , 2014, Journal of Controlled Release.

[13]  A. Kim,et al.  Minimizing the non-specific binding of nanoparticles to the brain enables active targeting of Fn14-positive glioblastoma cells. , 2015, Biomaterials.

[14]  K. Ishii,et al.  Hydrophobic blocks of PEG-conjugates play a significant role in the accelerated blood clearance (ABC) phenomenon. , 2013, Journal of controlled release : official journal of the Controlled Release Society.

[15]  J. S. Suk,et al.  Highly compacted biodegradable DNA nanoparticles capable of overcoming the mucus barrier for inhaled lung gene therapy , 2015, Proceedings of the National Academy of Sciences.

[16]  V. Torchilin,et al.  Liposomes : a practical approach , 2003 .

[17]  Hong-Zhuan Chen,et al.  In vivo tumor targeting of tumor necrosis factor-alpha-loaded stealth nanoparticles: effect of MePEG molecular weight and particle size. , 2006, European journal of pharmaceutical sciences : official journal of the European Federation for Pharmaceutical Sciences.

[18]  Dennis E Discher,et al.  Minimal " Self " Peptides That Inhibit Phagocytic Clearance and Enhance Delivery of Nanoparticles References and Notes , 2022 .

[19]  T. Ishida,et al.  Accelerated blood clearance of PEGylated liposomes upon repeated injections: effect of doxorubicin-encapsulation and high-dose first injection. , 2006, Journal of controlled release : official journal of the Controlled Release Society.

[20]  S. W. Kim,et al.  Enhancing the therapeutic efficacy of adenovirus in combination with biomaterials. , 2012, Biomaterials.

[21]  P. Legrand,et al.  Interactions between a macrophage cell line (J774A1) and surface-modified poly (D,L-lactide) nanocapsules bearing poly(ethylene glycol). , 1999, Journal of drug targeting.

[22]  Robert Langer,et al.  Preclinical Development and Clinical Translation of a PSMA-Targeted Docetaxel Nanoparticle with a Differentiated Pharmacological Profile , 2012, Science Translational Medicine.

[23]  Michael P Boyle,et al.  The penetration of fresh undiluted sputum expectorated by cystic fibrosis patients by non-adhesive polymer nanoparticles. , 2009, Biomaterials.

[24]  Jesse V Jokerst,et al.  Nanoparticle PEGylation for imaging and therapy. , 2011, Nanomedicine.

[25]  Mark E. Davis,et al.  Correlating animal and human phase Ia/Ib clinical data with CALAA-01, a targeted, polymer-based nanoparticle containing siRNA , 2014, Proceedings of the National Academy of Sciences.

[26]  Luisa M Russell,et al.  State-ofthe-Art in Design Rules for Drug Delivery Platforms : Lessons from FDA-approved Nanomedicines , 2014 .

[27]  A. Vila,et al.  Transport of PLA-PEG particles across the nasal mucosa: effect of particle size and PEG coating density. , 2004, Journal of controlled release : official journal of the Controlled Release Society.

[28]  Robert Langer,et al.  Precise engineering of targeted nanoparticles by using self-assembled biointegrated block copolymers , 2008, Proceedings of the National Academy of Sciences.

[29]  Justin Hanes,et al.  Biodegradable nanoparticles composed entirely of safe materials that rapidly penetrate human mucus. , 2011, Angewandte Chemie.

[30]  S. Hsiao,et al.  Monoclonal antibody-based quantitation of poly(ethylene glycol)-derivatized proteins, liposomes, and nanoparticles. , 2005, Bioconjugate chemistry.

[31]  B. Li,et al.  PEG-conjugated PAMAM Dendrimers Mediate Efficient Intramuscular Gene Expression , 2009, The AAPS Journal.

[32]  Robert Langer,et al.  Microfluidic technologies for accelerating the clinical translation of nanoparticles. , 2012, Nature nanotechnology.

[33]  M. Alonso,et al.  Stealth PLA-PEG Nanoparticles as Protein Carriers for Nasal Administration , 1998, Pharmaceutical Research.

[34]  N. Peppas,et al.  Design of poly(ethylene glycol)-tethered copolymers as novel mucoadhesive drug delivery systems. , 2006, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[35]  H. Kasukawa,et al.  Comparative studies of polyethylene glycol-modified liposomes prepared using different PEG-modification methods. , 2012, Biochimica et biophysica acta.

[36]  L. Unsworth,et al.  Protein-resistant poly(ethylene oxide)-grafted surfaces: chain density-dependent multiple mechanisms of action. , 2008, Langmuir : the ACS journal of surfaces and colloids.

[37]  P. Couvreur,et al.  Stealth® PEGylated polycyanoacrylate nanoparticles for intravenous administration and splenic targeting , 1999 .

[38]  Mark E. Davis,et al.  Targeting kidney mesangium by nanoparticles of defined size , 2011, Proceedings of the National Academy of Sciences.

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

[40]  K. Jacobson,et al.  PEGylated dendritic unimolecular micelles as versatile carriers for ligands of G protein-coupled receptors. , 2009, Bioconjugate chemistry.

[41]  Claus-Michael Lehr,et al.  PEG-functionalized microparticles selectively target inflamed mucosa in inflammatory bowel disease. , 2013, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[42]  P. Gellert,et al.  Poly(lactic acid)−Poly(ethylene oxide) (PLA−PEG) Nanoparticles: NMR Studies of the Central Solidlike PLA Core and the Liquid PEG Corona , 2002 .

[43]  K. Avgoustakis,et al.  Effect of copolymer composition on the physicochemical characteristics, in vitro stability, and biodistribution of PLGA-mPEG nanoparticles. , 2003, International journal of pharmaceutics.

[44]  A. Lila The accelerated blood clearance (ABC) phenomenon: clinical challenge and approaches to manage , 2013 .

[45]  R. Murray,et al.  Nanometer Gold Clusters Protected by Surface-Bound Monolayers of Thiolated Poly(ethylene glycol) Polymer Electrolyte , 1998 .

[46]  Yang Huang,et al.  The use of PEGylated poly [2-(N,N-dimethylamino) ethyl methacrylate] as a mucosal DNA delivery vector and the activation of innate immunity and improvement of HIV-1-specific immune responses. , 2010, Biomaterials.

[47]  E. Åkerblom,et al.  Polyethylene glycol reactive antibodies in man: titer distribution in allergic patients treated with monomethoxy polyethylene glycol modified allergens or placebo, and in healthy blood donors. , 1984, International archives of allergy and applied immunology.

[48]  Hamidreza Ghandehari,et al.  Geometry and surface characteristics of gold nanoparticles influence their biodistribution and uptake by macrophages. , 2011, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[49]  Yechezkel Barenholz,et al.  Pharmacokinetics of Pegylated Liposomal Doxorubicin , 2003, Clinical pharmacokinetics.

[50]  J. Engbersen,et al.  Measuring the intravitreal mobility of nanomedicines with single-particle tracking microscopy. , 2013, Nanomedicine.

[51]  Parag Aggarwal,et al.  Preclinical studies to understand nanoparticle interaction with the immune system and its potential effects on nanoparticle biodistribution. , 2008, Molecular pharmaceutics.

[52]  Laura M Ensign,et al.  Oral drug delivery with polymeric nanoparticles: the gastrointestinal mucus barriers. , 2012, Advanced drug delivery reviews.

[53]  Justin Hanes,et al.  A poly(ethylene glycol)-based surfactant for formulation of drug-loaded mucus penetrating particles. , 2012, Journal of controlled release : official journal of the Controlled Release Society.

[54]  Michael J Sailor,et al.  Computationally guided photothermal tumor therapy using long-circulating gold nanorod antennas. , 2009, Cancer research.

[55]  J. S. Suk,et al.  Highly compacted DNA nanoparticles with low MW PEG coatings: in vitro, ex vivo and in vivo evaluation. , 2012, Journal of controlled release : official journal of the Controlled Release Society.

[56]  J. Benoit,et al.  Evaluation of pegylated lipid nanocapsules versus complement system activation and macrophage uptake. , 2006, Journal of biomedical materials research. Part A.

[57]  Tohru Mizushima,et al.  Accelerated Blood Clearance Phenomenon Upon Repeated Injection of PEG-modified PLA-nanoparticles , 2009, Pharmaceutical Research.

[58]  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.

[59]  Benjamin C. Tang,et al.  PEGylation of nanoparticles improves their cytoplasmic transport , 2007, International journal of nanomedicine.

[60]  D. Fischer,et al.  Synthesis, Characterization, and Biocompatibility of Polyethylenimine-graft-poly(ethylene glycol) Block Copolymers , 2002 .

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

[62]  R. Cavalli,et al.  Intravenous Administration to Rabbits of Non-stealth and Stealth Doxorubicin-loaded Solid Lipid Nanoparticles at Increasing Concentrations of Stealth Agent: Pharmacokinetics and Distribution of Doxorubicin in Brain and Other Tissues , 2002, Journal of drug targeting.

[63]  Woo-Sik Kim,et al.  Interpretation of protein adsorption phenomena onto functional microspheres , 1998 .

[64]  Samir Mitragotri,et al.  Factors that control the circulation time of nanoparticles in blood: challenges, solutions and future prospects. , 2010, Current pharmaceutical design.

[65]  D. Brooks,et al.  Unimolecular micelles based on hydrophobically derivatized hyperbranched polyglycerols: biodistribution studies. , 2008, Bioconjugate chemistry.

[66]  J. Hanes,et al.  Scalable method to produce biodegradable nanoparticles that rapidly penetrate human mucus. , 2013, Journal of controlled release : official journal of the Controlled Release Society.

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

[68]  S. Lai,et al.  Anti-PEG immunity: emergence, characteristics, and unaddressed questions. , 2015, Wiley interdisciplinary reviews. Nanomedicine and nanobiotechnology.

[69]  T. Ishida,et al.  Effect of siRNA in PEG-coated siRNA-lipoplex on anti-PEG IgM production. , 2009, Journal of controlled release : official journal of the Controlled Release Society.

[70]  Si-Shen Feng,et al.  Nanoparticles of poly(lactide)/vitamin E TPGS copolymer for cancer chemotherapy: synthesis, formulation, characterization and in vitro drug release. , 2006, Biomaterials.

[71]  T. Ishida,et al.  The contribution of phagocytic activity of liver macrophages to the accelerated blood clearance (ABC) phenomenon of PEGylated liposomes in rats. , 2008, Journal of controlled release : official journal of the Controlled Release Society.

[72]  Chun Xing Li,et al.  Polymer-drug conjugates: recent development in clinical oncology. , 2008, Advanced drug delivery reviews.

[73]  Joseph M. DeSimone,et al.  Using mechanobiological mimicry of red blood cells to extend circulation times of hydrogel microparticles , 2011, Proceedings of the National Academy of Sciences.

[74]  A. Ray,et al.  Transepithelial transport of PEGylated anionic poly(amidoamine) dendrimers: implications for oral drug delivery. , 2009, Journal of controlled release : official journal of the Controlled Release Society.

[75]  S. Davis,et al.  Transport of Nanoparticles Across the Rat Nasal Mucosa , 2001, Journal of drug targeting.

[76]  Tomi Järvinen,et al.  Ocular absorption following topical delivery , 1995 .

[77]  Samuel K. Lai,et al.  Biodegradable mucus-penetrating nanoparticles composed of diblock copolymers of polyethylene glycol and poly(lactic-co-glycolic acid) , 2011, Drug Delivery and Translational Research.

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

[79]  S. Sahoo,et al.  Residual polyvinyl alcohol associated with poly (D,L-lactide-co-glycolide) nanoparticles affects their physical properties and cellular uptake. , 2002, Journal of controlled release : official journal of the Controlled Release Society.

[80]  Gert Storm,et al.  Sheddable Coatings for Long-Circulating Nanoparticles , 2007, Pharmaceutical Research.

[81]  T. Ishida,et al.  Influence of the physicochemical properties of liposomes on the accelerated blood clearance phenomenon in rats. , 2005, Journal of controlled release : official journal of the Controlled Release Society.

[82]  T. Ishida,et al.  Use of polyglycerol (PG), instead of polyethylene glycol (PEG), prevents induction of the accelerated blood clearance phenomenon against long-circulating liposomes upon repeated administration. , 2013, International journal of pharmaceutics.

[83]  Benjamin C. Tang,et al.  Mucus-Penetrating Nanoparticles for Vaginal Drug Delivery Protect Against Herpes Simplex Virus , 2012, Science Translational Medicine.

[84]  Chi‐Hwa Wang,et al.  Effect of PEG conformation and particle size on the cellular uptake efficiency of nanoparticles with the HepG2 cells. , 2007, Journal of controlled release : official journal of the Controlled Release Society.

[85]  P. Edman,et al.  Acrylic microspheres in vivo IX: Blood elimination kinetics and organ distribution of microparticles with different surface characteristics. , 1983, Journal of pharmaceutical sciences.

[86]  Christopher E. Nelson,et al.  Tuning PEGylation of mixed micelles to overcome intracellular and systemic siRNA delivery barriers. , 2015, Biomaterials.

[87]  Xuan Cheng,et al.  PEGylated Adenoviruses for Gene Delivery to the Intestinal Epithelium by the Oral Route , 2003, Pharmaceutical Research.

[88]  C. Vervaet,et al.  Sizing Nanomatter in Biological Fluids by Fluorescence Single Particle Tracking , 2011 .

[89]  H. Soleimanjahi,et al.  Accelerated Blood Clearance of PEGylated PLGA Nanoparticles Following Repeated Injections: Effects of Polymer Dose, PEG Coating, and Encapsulated Anticancer Drug , 2012, Pharmaceutical Research.

[90]  Filip Braet,et al.  Contribution of high‐resolution correlative imaging techniques in the study of the liver sieve in three‐dimensions , 2007, Microscopy research and technique.

[91]  Mark E. Davis,et al.  PEGylation significantly affects cellular uptake and intracellular trafficking of non-viral gene delivery particles. , 2004, European journal of cell biology.

[92]  M. Barry,et al.  Effects of shielding adenoviral vectors with polyethylene glycol on vector-specific and vaccine-mediated immune responses. , 2008, Human gene therapy.

[93]  T. Ishida,et al.  Anti-PEG IgM production by siRNA encapsulated in a PEGylated lipid nanocarrier is dependent on the sequence of the siRNA. , 2011, Journal of controlled release : official journal of the Controlled Release Society.

[94]  M. R. Sherman,et al.  Role of the Methoxy Group in Immune Responses to mPEG-Protein Conjugates , 2012, Bioconjugate chemistry.

[95]  Theresa M. Allen,et al.  Determination of Doxorubicin Levels in Whole Tumor and Tumor Nuclei in Murine Breast Cancer Tumors , 2005, Clinical Cancer Research.

[96]  T. Ishida,et al.  Application of polyglycerol coating to plasmid DNA lipoplex for the evasion of the accelerated blood clearance phenomenon in nucleic acid delivery. , 2014, Journal of pharmaceutical sciences.

[97]  A. Aderem,et al.  Mechanisms of phagocytosis in macrophages. , 1999, Annual review of immunology.

[98]  Robert Langer,et al.  Engineering of self-assembled nanoparticle platform for precisely controlled combination drug therapy , 2010, Proceedings of the National Academy of Sciences.

[99]  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.

[100]  Jianlin Shi,et al.  The effect of PEGylation of mesoporous silica nanoparticles on nonspecific binding of serum proteins and cellular responses. , 2010, Biomaterials.

[101]  A. Kros,et al.  The chemical modification of liposome surfaces via a copper-mediated [3 + 2] azide-alkyne cycloaddition monitored by a colorimetric assay. , 2006, Chemical communications.

[102]  Elizabeth Nance,et al.  Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood-brain barrier using MRI-guided focused ultrasound. , 2014, Journal of controlled release : official journal of the Controlled Release Society.

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

[104]  T. Ishida,et al.  Transport of PEGylated liposomes from the splenic marginal zone to the follicle in the induction phase of the accelerated blood clearance phenomenon. , 2013, Immunobiology.

[105]  J. Hanes,et al.  Effect of surface chemistry on nanoparticle interaction with gastrointestinal mucus and distribution in the gastrointestinal tract following oral and rectal administration in the mouse. , 2015, Journal of controlled release : official journal of the Controlled Release Society.

[106]  J. Armstrong The occurrence, induction, specificity and potential effect of antibodies against poly(ethylene glycol) , 2009 .

[107]  Robert Langer,et al.  Effects of ligands with different water solubilities on self-assembly and properties of targeted nanoparticles. , 2011, Biomaterials.

[108]  Benjamin C. Tang,et al.  N-acetylcysteine enhances cystic fibrosis sputum penetration and airway gene transfer by highly compacted DNA nanoparticles. , 2011, Molecular therapy : the journal of the American Society of Gene Therapy.

[109]  G. Woodworth,et al.  Nanoparticle diffusion in respiratory mucus from humans without lung disease. , 2013, Biomaterials.

[110]  James E Bear,et al.  PEGylated PRINT nanoparticles: the impact of PEG density on protein binding, macrophage association, biodistribution, and pharmacokinetics. , 2012, Nano letters.

[111]  Samir Mitragotri,et al.  Role of target geometry in phagocytosis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[113]  F. Gleeson,et al.  High-intensity focused ultrasound for the treatment of liver tumours. , 2004, Ultrasonics.

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

[115]  Omid C Farokhzad,et al.  Targeted delivery of a cisplatin prodrug for safer and more effective prostate cancer therapy in vivo , 2011, Proceedings of the National Academy of Sciences.

[116]  Samir Mitragotri,et al.  Delivering nanoparticles to lungs while avoiding liver and spleen through adsorption on red blood cells. , 2013, ACS nano.

[117]  Yen Cu,et al.  In vivo distribution of surface-modified PLGA nanoparticles following intravaginal delivery. , 2011, Journal of controlled release : official journal of the Controlled Release Society.

[118]  Jung Soo Suk,et al.  Addressing the PEG mucoadhesivity paradox to engineer nanoparticles that "slip" through the human mucus barrier. , 2008, Angewandte Chemie.

[119]  J. Hanes,et al.  Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues. , 2009, Advanced drug delivery reviews.

[120]  Robert Langer,et al.  Targeted delivery of cisplatin to prostate cancer cells by aptamer functionalized Pt(IV) prodrug-PLGA–PEG nanoparticles , 2008, Proceedings of the National Academy of Sciences.

[121]  A. Boletta,et al.  Comparison between cationic polymers and lipids in mediating systemic gene delivery to the lungs , 1999, Gene Therapy.

[122]  Benjamin C. Tang,et al.  Vaginal Delivery of Paclitaxel via Nanoparticles with Non‐Mucoadhesive Surfaces Suppresses Cervical Tumor Growth , 2014, Advanced healthcare materials.

[123]  Benjamin C. Tang,et al.  Biodegradable polymer nanoparticles that rapidly penetrate the human mucus barrier , 2009, Proceedings of the National Academy of Sciences.

[124]  Charles Nicholson,et al.  In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[125]  U. Schubert,et al.  Poly(ethylene glycol) in Drug Delivery: Pros and Cons as Well as Potential Alternatives. , 2011 .

[126]  Joseph J. Richardson,et al.  Engineering poly(ethylene glycol) particles for improved biodistribution. , 2015, ACS nano.

[127]  Seiji Miura,et al.  Mind the gap: a survey of how cancer drug carriers are susceptible to the gap between research and practice. , 2013, Journal of controlled release : official journal of the Controlled Release Society.

[128]  T. Cheng,et al.  Measurement of poly(ethylene glycol) by cell-based anti-poly(ethylene glycol) ELISA. , 2010, Analytical chemistry.

[129]  S. Lai,et al.  Evading immune cell uptake and clearance requires PEG grafting at densities substantially exceeding the minimum for brush conformation. , 2014, Molecular pharmaceutics.

[130]  R. Cone,et al.  Barrier properties of mucus. , 2009, Advanced drug delivery reviews.

[131]  H. Sasaki,et al.  Chondroitin sulfate capsule system for efficient and secure gene delivery. , 2010, Journal of pharmacy & pharmaceutical sciences : a publication of the Canadian Society for Pharmaceutical Sciences, Societe canadienne des sciences pharmaceutiques.

[132]  Jin Chang,et al.  PLGA/polymeric liposome for targeted drug and gene co-delivery. , 2010, Biomaterials.

[133]  Y. Huang,et al.  Molecular aspects of muco- and bioadhesion: tethered structures and site-specific surfaces. , 2000, Journal of controlled release : official journal of the Controlled Release Society.

[134]  Dexi Liu,et al.  Serum independent liposome uptake by mouse liver. , 1996, Biochimica et biophysica acta.

[135]  Samuel K. Lai,et al.  Nanoparticles reveal that human cervicovaginal mucus is riddled with pores larger than viruses , 2009, Proceedings of the National Academy of Sciences.

[136]  Y. Barenholz,et al.  Lipoplex-induced hemagglutination: potential involvement in intravenous gene delivery , 2002, Gene Therapy.

[137]  Alan E. Smith,et al.  PEGylation of adenovirus with retention of infectivity and protection from neutralizing antibody in vitro and in vivo. , 1999, Human gene therapy.

[138]  H. D. Liggitt,et al.  Factors influencing the efficiency of cationic liposome-mediated intravenous gene delivery , 1997, Nature Biotechnology.

[139]  D. Fischer,et al.  Surface-modified biodegradable albumin nano- and microspheres. II: effect of surface charges on in vitro phagocytosis and biodistribution in rats. , 1998, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[140]  Jenn‐Shing Chen,et al.  Folic acid-Pluronic F127 magnetic nanoparticle clusters for combined targeting, diagnosis, and therapy applications. , 2009, Biomaterials.

[141]  Ting-Yu Shih,et al.  Brain-Penetrating Nanoparticles Improve Paclitaxel Efficacy in Malignant Glioma Following Local Administration , 2014, ACS nano.

[142]  Xi Zhan,et al.  Effect of the poly(ethylene glycol) (PEG) density on the access and uptake of particles by antigen-presenting cells (APCs) after subcutaneous administration. , 2012, Molecular pharmaceutics.

[143]  T. Ishida,et al.  Spleen plays an important role in the induction of accelerated blood clearance of PEGylated liposomes. , 2006, Journal of controlled release : official journal of the Controlled Release Society.

[144]  S. D. De Smedt,et al.  Wanted and unwanted properties of surface PEGylated nucleic acid nanoparticles in ocular gene transfer. , 2007, Journal of controlled release : official journal of the Controlled Release Society.

[145]  V. Torchilin,et al.  Biodegradable long-circulating polymeric nanospheres. , 1994, Science.

[146]  K. Jacobson,et al.  Systematic investigation of polyamidoamine dendrimers surface-modified with poly(ethylene glycol) for drug delivery applications: synthesis, characterization, and evaluation of cytotoxicity. , 2008, Bioconjugate chemistry.

[147]  G. Winter,et al.  Method for quantifying the PEGylation of gelatin nanoparticle drug carrier systems using asymmetrical flow field-flow fractionation and refractive index detection. , 2007, Analytical chemistry.

[148]  Y. Yoshioka,et al.  Intravenous administration of polyethylene glycol-coated (PEGylated) proteins and PEGylated adenovirus elicits an anti-PEG immunoglobulin M response. , 2012, Biological & pharmaceutical bulletin.

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

[150]  V. Khutoryanskiy,et al.  On the barrier properties of the cornea: a microscopy study of the penetration of fluorescently labeled nanoparticles, polymers, and sodium fluorescein. , 2014, Molecular pharmaceutics.

[151]  J. Engbersen,et al.  Shielding the cationic charge of nanoparticle-formulated dermal DNA vaccines is essential for antigen expression and immunogenicity. , 2010, Journal of controlled release : official journal of the Controlled Release Society.

[152]  T. Ishida,et al.  Anti-PEG IgM Response against PEGylated Liposomes in Mice and Rats , 2010, Pharmaceutics.

[153]  Denis Wirtz,et al.  Micro- and macrorheology of mucus. , 2009, Advanced drug delivery reviews.

[154]  H. Harashima,et al.  The polyethyleneglycol dilemma: advantage and disadvantage of PEGylation of liposomes for systemic genes and nucleic acids delivery to tumors. , 2013, Biological & pharmaceutical bulletin.

[155]  Robert Langer,et al.  Microfluidic platform for controlled synthesis of polymeric nanoparticles. , 2008, Nano letters.

[156]  Laura M Ensign,et al.  Ex vivo characterization of particle transport in mucus secretions coating freshly excised mucosal tissues. , 2013, Molecular pharmaceutics.

[157]  Use of single-site-functionalized PEG dendrons to prepare gene vectors that penetrate human mucus barriers. , 2013, Angewandte Chemie.

[158]  M. McMahon,et al.  Liposome-based mucus-penetrating particles (MPP) for mucosal theranostics: demonstration of diamagnetic chemical exchange saturation transfer (diaCEST) magnetic resonance imaging (MRI). , 2015, Nanomedicine : nanotechnology, biology, and medicine.

[159]  Warren C W Chan,et al.  Mediating tumor targeting efficiency of nanoparticles through design. , 2009, Nano letters.

[160]  Si-Shen Feng,et al.  Nanoparticles of poly(lactide)-tocopheryl polyethylene glycol succinate (PLA-TPGS) copolymers for protein drug delivery. , 2007, Biomaterials.

[161]  Sanchita Bhattacharya,et al.  Characterization of cationic lipid-protamine–DNA (LPD) complexes for intravenous gene delivery , 1998, Gene Therapy.

[162]  Junghae Suh,et al.  Real-time multiple-particle tracking: applications to drug and gene delivery. , 2005, Advanced drug delivery reviews.

[163]  J. S. Suk,et al.  Biodegradable DNA Nanoparticles that Provide Widespread Gene Delivery in the Brain. , 2016, Small.

[164]  H. Nelis,et al.  Transport of nanoparticles in cystic fibrosis sputum and bacterial biofilms by single-particle tracking microscopy. , 2013, Nanomedicine.

[165]  K. Caldwell,et al.  Surface modification of nanoparticles by PEO/PPO block copolymers to minimize interactions with blood components and prolong blood circulation in rats. , 1993, Biomaterials.

[166]  Michel Vert,et al.  Biodistribution of Long-Circulating PEG-Grafted Nanocapsules in Mice: Effects of PEG Chain Length and Density , 2001, Pharmaceutical Research.

[167]  Thomas Kissel,et al.  In vitro cytotoxicity testing of polycations: influence of polymer structure on cell viability and hemolysis. , 2003, Biomaterials.

[168]  Justin Hanes,et al.  Nanoparticle penetration of human cervicovaginal mucus: the effect of polyvinyl alcohol. , 2014, Journal of controlled release : official journal of the Controlled Release Society.

[169]  M. Yokoyama,et al.  Particle size-dependent triggering of accelerated blood clearance phenomenon. , 2008, International journal of pharmaceutics.

[170]  T. Anchordoquy,et al.  Potential induction of anti-PEG antibodies and complement activation toward PEGylated therapeutics. , 2014, Drug discovery today.

[171]  V. Torchilin,et al.  Influence of the steric barrier activity of amphipathic poly(ethyleneglycol) and ganglioside GM1 on the circulation time of liposomes and on the target binding of immunoliposomes in vivo , 1991, FEBS letters.

[172]  D. Bazile,et al.  Stealth Me.PEG-PLA nanoparticles avoid uptake by the mononuclear phagocytes system. , 1995, Journal of pharmaceutical sciences.

[173]  S. Feng,et al.  Vitamin E TPGS used as emulsifier in the solvent evaporation/extraction technique for fabrication of polymeric nanospheres for controlled release of paclitaxel (Taxol). , 2002, Journal of controlled release : official journal of the Controlled Release Society.

[174]  Yihui Deng,et al.  Influence of phospholipid types and animal models on the accelerated blood clearance phenomenon of PEGylated liposomes upon repeated injection , 2015, Drug delivery.

[175]  M. Martín-Pastor,et al.  Application of NMR spectroscopy to the characterization of PEG-stabilized lipid nanoparticles. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[176]  Taro Shimizu,et al.  PEGylated liposomes elicit an anti-PEG IgM response in a T cell-independent manner. , 2007, Journal of controlled release : official journal of the Controlled Release Society.

[177]  Xiaoqun Gong,et al.  Impact of Surface Polyethylene Glycol (PEG) Density on Biodegradable Nanoparticle Transport in Mucus ex Vivo and Distribution in Vivo. , 2015, ACS nano.

[178]  Mark E. Davis The first targeted delivery of siRNA in humans via a self-assembling, cyclodextrin polymer-based nanoparticle: from concept to clinic. , 2009, Molecular pharmaceutics.

[179]  Tracy K. Pettinger,et al.  Nanopharmaceuticals (part 1): products on the market , 2014, International journal of nanomedicine.

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

[181]  Hideyoshi Harashima,et al.  A multifunctional envelope type nano device (MEND) for gene delivery to tumours based on the EPR effect: a strategy for overcoming the PEG dilemma. , 2011, Advanced drug delivery reviews.

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

[183]  Y Li,et al.  PEGylated PLGA nanoparticles as protein carriers: synthesis, preparation and biodistribution in rats. , 2001, Journal of controlled release : official journal of the Controlled Release Society.

[184]  P. McDonnell,et al.  Nanoparticle diffusion in, and microrheology of, the bovine vitreous ex vivo. , 2013, Journal of controlled release : official journal of the Controlled Release Society.

[185]  Xun Sun,et al.  Adenoviral vectors coated with cationic PEG derivatives for intravaginal vaccination against HIV-1. , 2014, Biomaterials.

[186]  Xin Yu Wang,et al.  Accelerated blood clearance of PEGylated liposomes following preceding liposome injection: effects of lipid dose and PEG surface-density and chain length of the first-dose liposomes. , 2005, Journal of controlled release : official journal of the Controlled Release Society.

[187]  M. van Lookeren Campagne,et al.  Macrophage complement receptors and pathogen clearance , 2007, Cellular microbiology.

[188]  T. Allen,et al.  Insertion of poly(ethylene glycol) derivatized phospholipid into pre‐formed liposomes results in prolonged in vivo circulation time , 1996, FEBS letters.

[189]  Yuan Yuan,et al.  Long-circulating polymeric nanoparticles bearing a combinatorial coating of PEG and water-soluble chitosan. , 2009, Biomaterials.

[190]  H M Patel,et al.  Serum opsonins and liposomes: their interaction and opsonophagocytosis. , 1992, Critical reviews in therapeutic drug carrier systems.

[191]  Sidhartha Hazari,et al.  Cellular delivery of PEGylated PLGA nanoparticles , 2012, The Journal of pharmacy and pharmacology.

[192]  J. Irache,et al.  In vivo study of the mucus-permeating properties of PEG-coated nanoparticles following oral administration. , 2015, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[193]  M. R. Sherman,et al.  Selectivity of binding of PEGs and PEG-like oligomers to anti-PEG antibodies induced by methoxyPEG-proteins. , 2014, Molecular Immunology.

[194]  Feng Xu,et al.  In vitro macrophage uptake and in vivo biodistribution of PLA–PEG nanoparticles loaded with hemoglobin as blood substitutes: effect of PEG content , 2009, Journal of materials science. Materials in medicine.

[195]  Rassoul Dinarvand,et al.  PLGA nanoparticles of different surface properties: preparation and evaluation of their body distribution. , 2008, International journal of pharmaceutics.

[196]  J. Leroux,et al.  Long Circulating Poly(Ethylene Glycol)-Decorated Lipid Nanocapsules Deliver Docetaxel to Solid Tumors , 2006, Pharmaceutical Research.

[197]  W. Chan,et al.  Synthesis and surface modification of highly monodispersed, spherical gold nanoparticles of 50-200 nm. , 2009, Journal of the American Chemical Society.

[198]  R. Müller,et al.  The controlled intravenous delivery of drugs using PEG-coated sterically stabilized nanospheres. , 1995, Advanced drug delivery reviews.

[199]  V. H. Lee,et al.  Influence of Preparation Conditions on Acyclovir-Loaded Poly-d,l-Lactic Acid Nanospheres and Effect of PEG Coating on Ocular Drug Bioavailability , 2003, Pharmaceutical Research.

[200]  Si-Shen Feng,et al.  Formulation of Docetaxel by folic acid-conjugated d-α-tocopheryl polyethylene glycol succinate 2000 (Vitamin E TPGS(2k)) micelles for targeted and synergistic chemotherapy. , 2011, Biomaterials.

[201]  T. Cheng,et al.  Sensitive quantification of PEGylated compounds by second-generation anti-poly(ethylene glycol) monoclonal antibodies. , 2010, Bioconjugate chemistry.

[202]  Luciana Facco Dalmolin,et al.  Pharmacokinetics of curcumin-loaded PLGA and PLGA-PEG blend nanoparticles after oral administration in rats. , 2013, Colloids and surfaces. B, Biointerfaces.

[203]  D. Schaffer,et al.  PEG conjugation moderately protects adeno-associated viral vectors against antibody neutralization. , 2005, Biotechnology and bioengineering.

[204]  D. Brooks,et al.  In vivo biological evaluation of high molecular weight hyperbranched polyglycerols. , 2007, Biomaterials.

[205]  J. S. Suk,et al.  Mucus Penetrating Nanoparticles: Biophysical Tool and Method of Drug and Gene Delivery , 2012, Advanced materials.

[206]  C. Eberhart,et al.  Highly PEGylated DNA Nanoparticles Provide Uniform and Widespread Gene Transfer in the Brain , 2015, Advanced healthcare materials.

[207]  Yong Ren,et al.  Plasmid‐Templated Shape Control of Condensed DNA–Block Copolymer Nanoparticles , 2013, Advanced materials.

[208]  Samuel K. Lai,et al.  Lung gene therapy with highly compacted DNA nanoparticles that overcome the mucus barrier. , 2014, Journal of controlled release : official journal of the Controlled Release Society.

[209]  Hongming Chen,et al.  Topical Ocular Drug Delivery to the Back of the Eye by Mucus-Penetrating Particles. , 2015, Translational vision science & technology.

[210]  H. Maeda,et al.  A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. , 1986, Cancer research.

[211]  S. L. Hyatt,et al.  Compacted DNA nanoparticles administered to the nasal mucosa of cystic fibrosis subjects are safe and demonstrate partial to complete cystic fibrosis transmembrane regulator reconstitution. , 2004, Human gene therapy.

[212]  V. Torchilin Recent advances with liposomes as pharmaceutical carriers , 2005, Nature Reviews Drug Discovery.

[213]  A. Judge,et al.  Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA , 2005, Nature Biotechnology.

[214]  A. I. Yudin,et al.  Diffusion of macromolecules and virus-like particles in human cervical mucus. , 2001, Biophysical journal.

[215]  F. Boury,et al.  Dynamic Properties of Poly(DL-lactide) and Polyvinyl Alcohol Monolayers at the Air/Water and Dichloromethane/Water Interfaces , 1995 .

[216]  P. Fong,et al.  PEGylated PLGA nanoparticles for the improved delivery of doxorubicin. , 2009, Nanomedicine : nanotechnology, biology, and medicine.

[217]  R. Jain,et al.  Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[218]  C. Cai,et al.  "Clickable", polymerized liposomes as a versatile and stable platform for rapid optimization of their peripheral compositions. , 2010, Chemical communications.

[219]  W. Oyen,et al.  Accelerated blood clearance and altered biodistribution of repeated injections of sterically stabilized liposomes. , 2000, The Journal of pharmacology and experimental therapeutics.

[220]  Younan Xia,et al.  Quantifying the coverage density of poly(ethylene glycol) chains on the surface of gold nanostructures. , 2012, ACS nano.

[221]  L. Nair,et al.  Comparison of electrospray ionization mass spectrometry and evaporative light scattering detections for the determination of Poloxamer 188 in itraconazole injectable formulation. , 2006, Journal of pharmaceutical and biomedical analysis.

[222]  Thomas Wirth,et al.  Three-step tumor targeting of paclitaxel using biotinylated PLA-PEG nanoparticles and avidin-biotin technology: Formulation development and in vitro anticancer activity. , 2008, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[223]  Elizabeth Nance,et al.  A Dense Poly(Ethylene Glycol) Coating Improves Penetration of Large Polymeric Nanoparticles Within Brain Tissue , 2012, Science Translational Medicine.

[224]  R. Kok,et al.  Ligand-targeted particulate nanomedicines undergoing clinical evaluation: current status. , 2013, Advanced drug delivery reviews.

[225]  Yen Cu,et al.  Controlled surface modification with poly(ethylene)glycol enhances diffusion of PLGA nanoparticles in human cervical mucus. , 2009, Molecular pharmaceutics.

[226]  S. Van Vlierberghe,et al.  Immobilization of Pseudorabies Virus in Porcine Tracheal Respiratory Mucus Revealed by Single Particle Tracking , 2012, PloS one.

[227]  Barbara Klajnert,et al.  Influence of dendrimers on red blood cells , 2011, Cellular & Molecular Biology Letters.

[228]  S. Mitragotri,et al.  Elasticity of nanoparticles influences their blood circulation, phagocytosis, endocytosis, and targeting. , 2015, ACS nano.

[229]  A. Judge,et al.  Hypersensitivity and loss of disease site targeting caused by antibody responses to PEGylated liposomes. , 2006, Molecular therapy : the journal of the American Society of Gene Therapy.

[230]  S M Moghimi,et al.  Long-circulating and target-specific nanoparticles: theory to practice. , 2001, Pharmacological reviews.

[231]  N. Peppas,et al.  Enhanced hydrogel adhesion by polymer interdiffusion: use of linear poly(ethylene glycol) as an adhesion promoter. , 1997, Journal of biomaterials science. Polymer edition.

[232]  C Vigneron,et al.  Influence of experimental parameters on the characteristics of poly(lactic acid) nanoparticles prepared by a double emulsion method. , 1998, Journal of controlled release : official journal of the Controlled Release Society.

[233]  Hong Yuan,et al.  Improved transport and absorption through gastrointestinal tract by PEGylated solid lipid nanoparticles. , 2013, Molecular pharmaceutics.

[234]  T. Ishida,et al.  Multiple administration of PEG-coated liposomal oxaliplatin enhances its therapeutic efficacy: a possible mechanism and the potential for clinical application. , 2012, International journal of pharmaceutics.

[235]  N. Yamazaki,et al.  CpG motifs in pDNA-sequences increase anti-PEG IgM production induced by PEG-coated pDNA-lipoplexes. , 2010, Journal of controlled release : official journal of the Controlled Release Society.

[236]  O. Mert,et al.  Drug carrier nanoparticles that penetrate human chronic rhinosinusitis mucus. , 2011, Biomaterials.

[237]  G. Kenner,et al.  Influence of poly(ethylene glycol) grafting density and polymer length on liposomes: relating plasma circulation lifetimes to protein binding. , 2007, Biochimica et biophysica acta.

[238]  Justin Hanes,et al.  Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus , 2007, Proceedings of the National Academy of Sciences.

[239]  Forrest M Kievit,et al.  PEG-mediated synthesis of highly dispersive multifunctional superparamagnetic nanoparticles: their physicochemical properties and function in vivo. , 2010, ACS nano.

[240]  J. Irache,et al.  An HPLC with evaporative light scattering detection method for the quantification of PEGs and Gantrez in PEGylated nanoparticles. , 2007, Journal of pharmaceutical and biomedical analysis.

[241]  D. Hoekstra,et al.  Interference of poly(ethylene glycol)-lipid analogues with cationic-lipid-mediated delivery of oligonucleotides; role of lipid exchangeability and non-lamellar transitions. , 2002, The Biochemical journal.

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

[243]  D. Bazile,et al.  Effect of PEO surface density on long-circulating PLA-PEO nanoparticles which are very low complement activators. , 1996, Biomaterials.