Fluorine-modified polymers reduce the adsorption of immune-reactive proteins to PEGylated gold nanoparticles

References

• Forgham H, Liu L, Zhu J et al. Vector enabled CRISPR gene editing – a revolutionary strategy for targeting the diversity of brain pathologies. Coord. Chem. Rev. 487, 215172 (2023).
   PubMed Web of Science ®Google Scholar
• Li Z, Zhang X-Q, Ho W et al. Lipid–polymer hybrid ‘particle-in-particle’ nanostructure gene delivery platform explored for lyophilizable DNA and mRNA COVID-19 vaccines. Adv. Funct. Mater. 32(40), 2204462 (2022).
   PubMed Web of Science ®Google Scholar
• Qiao R, Fu C, Forgham H et al. Magnetic iron oxide nanoparticles for brain imaging and drug delivery. Adv. Drug Deliv. Rev. 197, 114822 (2023).
   PubMed Web of Science ®Google Scholar
• Yalcin S, Gündüz U. Iron oxide-based polymeric magnetic nanoparticles for drug and gene delivery: in vitro and in vivo applications in cancer. In: Handbook of Polymer and Ceramic Nanotechnology. Hussain CM, Thomas S ( Eds). Springer International Publishing, NY, USA, 1–22 (2021).
   Google Scholar
• Ke PC, Lin S, Parak WJ, Davis TP, Caruso F. A decade of the protein corona. ACS Nano 11(12), 11773–11776 (2017).
   PubMed Web of Science ®Google Scholar
• Falahati M, Attar F, Sharifi M et al. A health concern regarding the protein corona, aggregation and disaggregation. Biochim. Biophys. Acta Gen. Subj. 1863(5), 971–991 (2019).
   PubMed Web of Science ®Google Scholar
• Yan Y, Gause KT, Kamphuis MMJ et al. Differential roles of the protein corona in the cellular uptake of nanoporous polymer particles by monocyte and macrophage cell lines. ACS Nano 7(12), 10960–10970 (2013).
   PubMed Web of Science ®Google Scholar
• Chen F, Wang G, Griffin JI et al. Complement proteins bind to nanoparticle protein corona and undergo dynamic exchange in vivo. Nat. Nanotechnol. 12(4), 387–393 (2017).
   PubMed Web of Science ®Google Scholar
• Szebeni J, Storm G, Ljubimova JY et al. Applying lessons learned from nanomedicines to understand rare hypersensitivity reactions to mRNA-based SARS-CoV-2 vaccines. Nat. Nanotechnol. 17(4), 337–346 (2022).
   PubMed Web of Science ®Google Scholar
• Chanan-Khan A, Szebeni J, Savay S et al. Complement activation following first exposure to PEGylated liposomal doxorubicin (Doxil®): possible role in hypersensitivity reactions. Ann. Oncol. 14(9), 1430–1437 (2003).
   PubMed Web of Science ®Google Scholar
• Lowe S, O'Brien-Simpson NM, Connal LA. Antibiofouling polymer interfaces: poly(ethylene glycol) and other promising candidates. Polym. Chem. 6(2), 198–212 (2015).
   Web of Science ®Google Scholar
• Suk JS, Xu Q, Kim N, Hanes J, Ensign LM. PEGylation as a strategy for improving nanoparticle-based drug and gene delivery. Adv. Drug. Deliv. Rev. 99(Pt A), 28–51 (2016).
   PubMed Web of Science ®Google Scholar
• Tao L, Liu J, Xu J, Davis TP. Bio-reversible polyPEGylation. Chem. Commun. (43), 6560–6562 (2009).
   PubMed Web of Science ®Google Scholar
• Papi M, Caputo D, Palmieri V et al. Clinically approved PEGylated nanoparticles are covered by a protein corona that boosts the uptake by cancer cells. Nanoscale 9(29), 10327–10334 (2017).
   PubMed Web of Science ®Google Scholar
• Du X-J, Wang J-L, Liu W-W et al. Regulating the surface poly (ethylene glycol) density of polymeric nanoparticles and evaluating its role in drug delivery in vivo. Biomaterials 69, 1–11 (2015).
   PubMed Web of Science ®Google Scholar
• Qiao R, Fu C, Li Y et al. Sulfoxide-containing polymer-coated nanoparticles demonstrate minimal protein fouling and improved blood circulation. Adv. Sci. 7(13), 2000406 (2020).
   Web of Science ®Google Scholar
• Nandakumar A, Wei W, Siddiqui G et al. Dynamic protein corona of gold nanoparticles with an evolving morphology. ACS Appl. Mater. Interfaces 13(48), 58238–58251 (2021).
   PubMed Web of Science ®Google Scholar
• Grundler J, Shin K, Suh H-W, Zhong M, Saltzman WM. Surface topography of polyethylene glycol shell nanoparticles formed from bottlebrush block copolymers controls interactions with proteins and cells. ACS Nano 15(10), 16118–16129 (2021).
   PubMed Web of Science ®Google Scholar
• Chen L, Glass JJ, De Rose R et al. Influence of charge on hemocompatibility and immunoreactivity of polymeric nanoparticles. ACS Appl. Bio Mater. 1(3), 756–767 (2018).
   PubMedGoogle Scholar
• Zhang Z, Guan J, Jiang Z et al. Brain-targeted drug delivery by manipulating protein corona functions. Nat. Commun. 10(1), 3561 (2019).
   PubMedGoogle Scholar
• Gao Y, Huang Y, Feng S, Gu G, Qing F-L. Novel superhydrophobic and highly oleophobic PFPE-modified silica nanocomposite. J. Mater. Sci. 45(2), 460–466 (2010).
   Web of Science ®Google Scholar
• Zhang L, Zhou Z, Cheng B, Desimone JM, Samulski ET. Superhydrophobic behavior of a perfluoropolyether lotus-leaf-like topography. Langmuir 22(20), 8576–8580 (2006).
   PubMed Web of Science ®Google Scholar
• Guo Z, Zhou F, Hao J, Liu W. Effects of system parameters on making aluminum alloy lotus. J. Colloid Interface Sci. 303(1), 298–305 (2006).
   PubMed Web of Science ®Google Scholar
• Banks RE, Smart BE, Tatlow JC. Organofluorine Chemistry. Springer, NY, USA (1994).
   Google Scholar
• Miller HA, Kusel BS, Danielson ST et al. Metastable nanostructured metallized fluoropolymer composites for energetics. J. Mater. Chem. A 1(24), 7050–7058 (2013).
   Web of Science ®Google Scholar
• Messori M, Fabbri P, Pilati F, Tonelli C, Toselli M. Perfluoropolyether-based organic–inorganic coatings. Prog. Org. Coat. 72(3), 461–468 (2011).
   Web of Science ®Google Scholar
• Wang M, Liu H, Li L, Cheng Y. A fluorinated dendrimer achieves excellent gene transfection efficacy at extremely low nitrogen to phosphorus ratios. Nat. Commun. 5(1), 3053 (2014).
   PubMedGoogle Scholar
• Gessner A, Waicz R, Lieske A, Paulke B, Mader K, Muller RH. Nanoparticles with decreasing surface hydrophobicities: influence on plasma protein adsorption. Int. J. Pharm. 196(2), 245–249 (2000).
   PubMed Web of Science ®Google Scholar
• Yang S, Wu Y, Zhong W, Chen R, Wang M, Chen M. GSH/pH dual activatable cross-linked and fluorinated PEI for cancer gene therapy through endogenous iron de-hijacking and in situ ROS amplification. Adv. Mater. 36(2), 2304098 (2024).
   Web of Science ®Google Scholar
• Ouyang B, Poon W, Zhang Y-N et al. The dose threshold for nanoparticle tumour delivery. Nat. Mater. 19(12), 1362–1371 (2020).
   PubMed Web of Science ®Google Scholar
• Chithrani BD, Ghazani AA, Chan WC. Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett. 6(4), 662–668 (2006).
   PubMed Web of Science ®Google Scholar
• Hammami I, Alabdallah NM, Jomaa AA, Kamoun M. Gold nanoparticles: synthesis properties and applications. J. King Saud Univ. Sci. 33(7), 101560 (2021).
   Web of Science ®Google Scholar
• Sato Y, Kinami Y, Hashiba K, Harashima H. Different kinetics for the hepatic uptake of lipid nanoparticles between the apolipoprotein E/low density lipoprotein receptor and the N-acetyl-d-galactosamine/asialoglycoprotein receptor pathway. J. Control. Rel. 322, 217–226 (2020).
   PubMed Web of Science ®Google Scholar
• Zhang M, Xiong Q, Chen J, Wang Y, Zhang Q. A novel cyclodextrin-containing pH-responsive star polymer for nanostructure fabrication and drug delivery. Polym. Chem. 4(19), 5086–5095 (2013).
   Web of Science ®Google Scholar
• Zhang Q, Collins J, Anastasaki A et al. Sequence-controlled multi-block glycopolymers to inhibit DC-SIGN-gp120 binding. Angew. Chem. Int. Ed. 52(16), 4435–4439 (2013).
   PubMed Web of Science ®Google Scholar
• Zou Y, Sun X, Yang Q et al. Blood–brain barrier-penetrating single CRISPR-Cas9 nanocapsules for effective and safe glioblastoma gene therapy. Sci. Adv. 8(16), eabm8011 (2022).
   PubMed Web of Science ®Google Scholar
• Karim M, Dunham I, Ghoussaini M. Mining a GWAS of severe COVID-19. N. Engl. J. Med. 383(26), 2588–2589 (2020).
   PubMed Web of Science ®Google Scholar
• Van Gisbergen KP, Aarnoudse CA, Meijer GA, Geijtenbeek TB, Van Kooyk Y. Dendritic cells recognize tumor-specific glycosylation of carcinoembryonic antigen on colorectal cancer cells through dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin. Cancer Res. 65(13), 5935–5944 (2005).
   PubMed Web of Science ®Google Scholar
• Sethuraman SN, Singh MP, Patil G et al. Novel calreticulin-nanoparticle in combination with focused ultrasound induces immunogenic cell death in melanoma to enhance antitumor immunity. Theranostics 10(8), 3397–3412 (2020).
   PubMed Web of Science ®Google Scholar
• Obeid M. ERP57 membrane translocation dictates the immunogenicity of tumor cell death by controlling the membrane translocation of calreticulin. J. Immunol. 181(4), 2533–2543 (2008).
   PubMed Web of Science ®Google Scholar
• Huang X, Xu T, Shen A, Davis TP, Qiao R, Tang SY. Engineering polymers via understanding the effect of anchoring groups for highly stable liquid metal nanoparticles. ACS Appl. Nano Mater. 5(5), 5959–5971 (2022).
   PubMed Web of Science ®Google Scholar
• Tan X, Dewapriya P, Prasad P et al. Efficient removal of perfluorinated chemicals from contaminated water sources using magnetic fluorinated polymer sorbents. Angew. Chem. Int. Ed. Engl. 61(49), e202213071 (2022).
   PubMed Web of Science ®Google Scholar
• Patil T, Gambhir R, Vibhute A, Tiwari AP. Gold nanoparticles: synthesis methods, functionalization and biological applications. J. Clust. Sci. 34(2), 705–725 (2023).
   Web of Science ®Google Scholar
• Stordy B, Zhang YW, Sepahi Z, Khatami MH, Kim PM, Chan WCW. Conjugating ligands to an equilibrated nanoparticle protein corona enables cell targeting in serum. Chem. Mater. 34(15), 6868–6882 (2022).
   Web of Science ®Google Scholar
• Chang Y, Wang Q, Xu W et al. Low-fouling gold nanorod theranostic agents enabled by a sulfoxide polymer coating. Biomacromolecules 23(9), 3866–3874 (2022).
   PubMed Web of Science ®Google Scholar
• Önal E, Tüncel Ö, Albakour M, Çelik GG, Gürek AG, Özçelik S. Synthesizing and evaluating the photodynamic efficacy of asymmetric heteroleptic A(7)B type novel lanthanide bis-phthalocyanine complexes. RSC Adv. 11(11), 6188–6200 (2021).
   PubMed Web of Science ®Google Scholar
• Qiao R, Esser L, Fu C et al. Bioconjugation and fluorescence labeling of iron oxide nanoparticles grafted with bromomaleimide-terminal polymers. Biomacromolecules 19(11), 4423–4429 (2018).
   PubMed Web of Science ®Google Scholar
• Farkas N, Kramar JA. Dynamic light scattering distributions by any means. J. Nanopart. Res. 23(5), 120 (2021).
   Web of Science ®Google Scholar
• Wang M, Gustafsson OJR, Siddiqui G et al. Human plasma proteome association and cytotoxicity of nano-graphene oxide grafted with stealth polyethylene glycol and poly(2-ethyl-2-oxazoline). Nanoscale 10(23), 10863–10875 (2018).
   PubMed Web of Science ®Google Scholar
• Ebeling B, Vana P. RAFT-polymers with single and multiple trithiocarbonate groups as uniform gold-nanoparticle coatings. Macromolecules 46(12), 4862–4871 (2013).
   Web of Science ®Google Scholar
• Brown KR, Walter DG, Natan MJ. Seeding of colloidal Au nanoparticle solutions. 2. Improved control of particle size and shape. Chem. Mater. 12(2), 306–313 (2000).
   Web of Science ®Google Scholar
• Moyano DF, Saha K, Prakash G et al. Fabrication of corona-free nanoparticles with tunable hydrophobicity. ACS Nano 8(7), 6748–6755 (2014).
   PubMed Web of Science ®Google Scholar
• Clayton KN, Salameh JW, Wereley ST, Kinzer-Ursem TL. Physical characterization of nanoparticle size and surface modification using particle scattering diffusometry. Biomicrofluidics 10(5), 054107 (2016).
   PubMed Web of Science ®Google Scholar
• Linkous A, Balamatsias D, Snuderl M et al. Modeling patient-derived glioblastoma with cerebral organoids. Cell Rep. 26(12), 3203–3211 e3205 (2019).
   PubMed Web of Science ®Google Scholar
• Strazzullo P, Leclercq C. Sodium. Adv. Nutr. 5(2), 188–190 (2014).
   PubMed Web of Science ®Google Scholar
• Bhattacharjee S. DLS and zeta potential – what they are and what they are not? J. Control. Rel. 235, 337–351 (2016).
   PubMed Web of Science ®Google Scholar
• Givens BE, Wilson E, Fiegel J. The effect of salts in aqueous media on the formation of the BSA corona on SiO2 nanoparticles. Colloids Surf. B Biointerfaces 179, 374–381 (2019).
   PubMed Web of Science ®Google Scholar
• Strojan K, Leonardi A, Bregar VB, Krizaj I, Svete J, Pavlin M. Dispersion of nanoparticles in different media importantly determines the composition of their protein corona. PLOS ONE 12(1), e0169552 (2017).
   PubMed Web of Science ®Google Scholar
• Shih Y-H, Zhuang C-M, Tso C-P, Lin C-H. The effect of electrolytes on the aggregation kinetics of titanium dioxide nanoparticle aggregates. J. Nanopart. Res. 14(8), 924 (2012).
   Web of Science ®Google Scholar
• Wang X, Yang B, Li L et al. Probing the fluorination effect on the self-assembly characteristics, in vivo fate and antitumor efficacy of paclitaxel prodrug nanoassemblies. Theranostics 11(16), 7896–7910 (2021).
   PubMed Web of Science ®Google Scholar
• Moghimi SM, Simberg D. Critical issues and pitfalls in serum and plasma handling for complement analysis in nanomedicine and bionanotechnology. Nano Today 44, 101479 (2022).
   Web of Science ®Google Scholar
• Rus H, Cudrici C, Niculescu F. The role of the complement system in innate immunity. Immunol. Res. 33(2), 103–112 (2005).
   PubMed Web of Science ®Google Scholar
• Moghimi SM, Haroon HB, Yaghmur A et al. Perspectives on complement and phagocytic cell responses to nanoparticles: from fundamentals to adverse reactions. J. Control. Rel. 356, 115–129 (2023).
   PubMed Web of Science ®Google Scholar
• Wang Z, Hood ED, Nong J et al. Combating complement's deleterious effects on nanomedicine by conjugating complement regulatory proteins to nanoparticles. Adv. Mater. 34(8), 2107070 (2022).
   Web of Science ®Google Scholar
• Mahmoudi M, Landry MP, Moore A, Coreas R. The protein corona from nanomedicine to environmental science. Nat. Rev. Mater. 8(7), 422–438 (2023).
   Web of Science ®Google Scholar
• Pisalyaput K, Tenner AJ. Complement component C1q inhibits β-amyloid- and serum amyloid P-induced neurotoxicity via caspase- and calpain-independent mechanisms. J. Neurochem. 104(3), 696–707 (2008).
   PubMed Web of Science ®Google Scholar
• Aoyama M, Hata K, Higashisaka K, Nagano K, Yoshioka Y, Tsutsumi Y. Clusterin in the protein corona plays a key role in the stealth effect of nanoparticles against phagocytes. Biochem. Biophys. Res. Commun. 480(4), 690–695 (2016).
   PubMed Web of Science ®Google Scholar
• Dabur M, Loureiro JA, Pereira MC. Fluorinated molecules and nanotechnology: future ‘avengers’ against the Alzheimer's disease? Int. J. Mol. Sci. 21(8), 2989 (2020).
   PubMed Web of Science ®Google Scholar
• Gonzalez-Quintela A, Alende R, Gude F et al. Serum levels of immunoglobulins (IgG, IgA, IgM) in a general adult population and their relationship with alcohol consumption, smoking and common metabolic abnormalities. Clin. Exp. Immunol. 151(1), 42–50 (2008).
   PubMed Web of Science ®Google Scholar
• Roos A, Bouwman LH, Van Gijlswijk-Janssen DLJ, Faber-Krol MC, Stahl GL, Daha MR. Human IgA activates the complement system via the mannan-binding lectin pathway1. J. Immunol. 167(5), 2861–2868 (2001).
   PubMed Web of Science ®Google Scholar
• Schenkein H, Ruddy S. The role of immunoglobulins in alternative pathway activation by zymosan. II. The effect of IgG on the kinetics of the alternative pathway. J. Immunol. 126(1), 11–15 (1981).
   PubMed Web of Science ®Google Scholar
• Smith NLD, Bromley MJ, Denning DW, Simpson A, Bowyer P. Elevated levels of the neutrophil chemoattractant pro-platelet basic protein in macrophages from individuals with chronic and allergic aspergillosis. J. Infect. Dis. 211(4), 651–660 (2015).
   PubMed Web of Science ®Google Scholar
• Keshavan S, Calligari P, Stella L, Fusco L, Delogu LG, Fadeel B. Nano–bio interactions: a neutrophil-centric view. Cell Death Dis. 10(8), 569 (2019).
   PubMedGoogle Scholar
• Kelley WJ, Fromen CA, Lopez-Cazares G, Eniola-Adefeso O. PEGylation of model drug carriers enhances phagocytosis by primary human neutrophils. Acta Biomater. 79, 283–293 (2018).
   PubMed Web of Science ®Google Scholar
• Mak TW, Saunders ME (Eds). Complement. In: The Immune Response. Academic Press, VT, USA, 553–581 (2006).
   Google Scholar
• Jang GJ, Jeong JY, Kang J, Cho W, Han SY. Size dependence unveiling the adsorption interaction of high-density lipoprotein particles with PEGylated gold nanoparticles in biomolecular corona formation. Langmuir 37(32), 9755–9763 (2021).
   PubMed Web of Science ®Google Scholar
• Li Z, Zhu J, Wang Y et al. In situ apolipoprotein E-enriched corona guides dihydroartemisinin-decorating nanoparticles towards LDLr-mediated tumor-homing chemotherapy. Asian J. Pharm. Sci. 15(4), 482–491 (2020).
   PubMed Web of Science ®Google Scholar
• Rojo J, Sousa-Herves A, Mascaraque A. Perspectives of carbohydrates in drug discovery. In: Comprehensive Medicinal Chemistry III. Chackalamannil S, Rotella D, Ward SE ( Eds). Elsevier, Oxford, UK, 577–610 (2017).
   Google Scholar
• Garg AD, Elsen S, Krysko DV, Vandenabeele P, De Witte P, Agostinis P. Resistance to anticancer vaccination effect is controlled by a cancer cell-autonomous phenotype that disrupts immunogenic phagocytic removal. Oncotarget 6(29), 26841–26860 (2015).
   PubMed Web of Science ®Google Scholar
• Moyano DF, Goldsmith M, Solfiell DJ et al. Nanoparticle hydrophobicity dictates immune response. J. Am. Chem. Soc. 134(9), 3965–3967 (2012).
   PubMed Web of Science ®Google Scholar
• Yu Q, Zhao L, Guo C, Yan B, Su G. Regulating protein corona formation and dynamic protein exchange by controlling nanoparticle hydrophobicity. Front. Bioeng. Biotechnol. 8, 210 (2020).
   PubMed Web of Science ®Google Scholar
• Huang HY, Chen LQ, Sun W et al. Collagenase IV and clusterin-modified polycaprolactone-polyethylene glycol nanoparticles for penetrating dense tumor tissues. Theranostics 11(2), 906–924 (2021).
   PubMed Web of Science ®Google Scholar
• Bashiri G, Padilla MS, Swingle KL, Shepherd SJ, Mitchell MJ, Wang K. Nanoparticle protein corona: from structure and function to therapeutic targeting. Lab Chip 23(6), 1432–1466 (2023).
   PubMed Web of Science ®Google Scholar