Abstract
As effective tools for public health, vaccines prevent disease by priming the body's adaptive and innate immune responses against an infection. Due to advances in understanding cancers and their relationship with the immune system, there is a growing interest in priming host immune defenses for a targeted and complete antitumor response. Nanoparticle systems have shown to be promising tools for effective antigen delivery as vaccines and/or for potentiating immune response as adjuvants. Here, we highlight relevant physiological processes involved in vaccine delivery, review recent advances in the use of nanoparticle systems for vaccines and discuss pertinent challenges to viably translate nanoparticle-based vaccines and adjuvants for public use.
Papers of special note have been highlighted as: •• of considerable interest
References
- 1 Immunologic memory induced at birth by immunization with inactivated polio vaccine in a reduced schedule. Eur. J. Epidemiol. 5(2), 143–145 (1989).
- 2 . Cancer vaccines: between the idea and the reality. Nat. Rev. Immunol. 3(8), 630 (2003).
- 3 . Targeting the innate immune response with improved vaccine adjuvants. Nat. Med. 10(4s), S63 (2005).
- 4 . The interface between innate and adaptive immunity. Nat. Immunol. 5(10), 971–974 (2004).
- 5 . NK cells at the interface between innate and adaptive immunity. Cell Death Differ. 15(2), 226–233 (2008).
- 6 . Cancer statistics, 2016. CA Cancer J. Clin. 66(1), 7–30 (2016).
- 7 . Nanoparticle drug delivery system for restenosis. Adv. Drug Deliv. Rev. 24(1), 63–85 (1997).
- 8 . Synthesis of Li4Ti5O12 nanostructural anode materials with high charge–discharge capability. Chin. Sci. Bull. 59(18), 2162–2174 (2014).
- 9 Holey two-dimensional transition metal oxide nanosheets for efficient energy storage. Nat. Commun. 8, 15139 (2017).
- 10 . Femtosecond laser-induced robust periodic nanoripple structured mesh for highly efficient oil–water separation. Nanoscale 9(37), 14229–14235 (2017).
- 11 . Vaccine delivery using nanoparticles. Front. Cell Infect. Microbiol. 3, 13 (2013).
- 12 . Nanotechnology based therapeutic modality to boost anti-tumor immunity and collapse tumor defense. J. Control. Rel. 256, 26–45 (2017).
- 13 . Nanoparticle drug delivery systems designed to improve cancer vaccines and immunotherapy. Vaccines 3(3), 662–685 (2015).
- 14 . Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat. Rev. Immunol. 10(11), 787 (2010).
- 15 . N7 methylation alters hydrogen-bonding patterns of guanine in duplex DNA. J. Am. Chem. Soc. 137(44), 14067–14070 (2015).
- 16 . Transition-state destabilization reveals how human DNA polymerase β proceeds across the chemically unstable lesion N7-methylguanine. Nucleic Acids Res. 42(13), 8755–8766 (2014).
- 17 . Role of targeting nanoparticles for cancer immunotherapy and imaging. Trends Immunother. 1(3), 104–113 (2017).
- 18 CD40-targeted dendritic cell delivery of PLGA-nanoparticle vaccines induce potent anti-tumor responses. Biomaterials 40, 88–97 (2015).
- 19 . Synthetic TRP2 long-peptide and α-galactosylceramide formulated into cationic liposomes elicit CD8+ T cell responses and prevent tumour progression. Vaccine 33(43), 5838–5844 (2015).
- 20 Dual stimulation of antigen presenting cells using carbon nanotube-based vaccine delivery system for cancer immunotherapy. Biomaterials 104, 310–322 (2016).
- 21 In situ vaccination with cowpea mosaic virus nanoparticles suppresses metastatic cancer. Nat. Nanotech. 11(3), 295 (2016).
- 22 Tecemotide (L-BLP25) versus placebo after chemoradiotherapy for Stage III non-small-cell lung cancer (START): a randomised, double-blind, Phase 3 trial. Lancet Oncol. 15(1), 59–68 (2014).
- 23 Nanoparticulate vaccine inhibits tumor growth via improved T cell recruitment into melanoma and huHER2 breast cancer. Nanomed. Nanotech. Biol. Med. 14(3), 835–847 (2018).
- 24 Abstract P6-10-01: efficacy and safety of the therapeutic cancer vaccine tecemotide (L-BLP25) in early breast cancer: results from a prospective, randomized, neoadjuvant Phase-II study (ABCSG-34). AACR 77(4), P6-10-01 (2017).
- 25 . Anti-tumor effect of the alphavirus-based virus-like particle vector expressing prostate-specific antigen in a HLA–DR transgenic mouse model of prostate cancer. Vaccine 33(41), 5386–5395 (2015).
- 26 . Tumour virus vaccines: hepatitis B virus and human papillomavirus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372(1732), 20160268 (2017).
- 27 . Nanoparticles as synthetic vaccines. Curr. Opin. Biotechnol. 34, 217–224 (2015).
- 28 . Nanotechnology-inspired tools for mitochondrial dysfunction related diseases. Adv. Drug Deliv. Rev. 99, 52–69 (2016).
- 29 An engineered TIMP2-based and enediyne-integrated fusion protein for targeting MMP-14 shows potent antitumor efficacy. Oncotarget 6(28), 26322 (2015).
- 30 . Targeted drugs for systemic therapy of lung cancer with brain metastases. Oncotarget 9(4), 5459 (2018). •• Excellent review on mitochondria targeting for nanoparticle vaccines.
- 31 . Mitochondrion: a promising target for nanoparticle-based vaccine delivery systems. Vaccines 4(2), 18 (2016).
- 32 . Accessing Mitochondrial Targets Using NanoCargos. In: Intracellular Delivery III. Fundamental Biomedical Technologies. Prokop A, Weissig V (Eds). Springer, Cham, 229–254 (2016).
- 33 Recombinant EGFR/MMP-2 bi-targeted fusion protein markedly binding to non-small-cell lung carcinoma and exerting potent therapeutic efficacy. Pharm. Res. 126, 66–76 (2017).
- 34 . Current status of multiple antigen-presenting peptide vaccine systems: application of organic and inorganic nanoparticles. Chem. Cent. J. 5(1), 48 (2011). •• Excellent review on polymer delivery systems.
- 35 . Polymer-based drug-delivery systems for cancer. Crit. Rev. Ther. Drug Carrier Syst. 35(6), 521–553 (2018).
- 36 . A prodrug of two approved drugs, cisplatin and chlorambucil, for chemo war against cancer. Mol. Cancer Ther. 16(4), 625–636 (2017). •• Significant finding on mitochondria-targeted nanoparticles.
- 37 . Turn up the cellular power generator with vitamin E analogue formulation. Chem. Sci. 7(8), 5559–5567 (2016).
- 38 . Research on big data digging of hot topics about recycled water use on micro-blog based on particle swarm optimization. Sustainability 10(7), 2488 (2018).
- 39 . Poly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers 3(3), 1377–1397 (2011).
- 40 PEGylated PLGA-based nanoparticles targeting M cells for oral vaccination. J. Control. Rel. 120(3), 195–204 (2007).
- 41 A pH-sensitive nanosystem based on carboxymethyl chitosan for tumor-targeted delivery of daunorubicin. J. Biomed. Nanotechnol. 12(8), 1688–1698 (2016).
- 42 . Synthesis and in vitro characterization of carboxymethyl chitosan-CBA-doxorubicin conjugate nanoparticles as pH-sensitive drug delivery systems. J. Biomed. Nanotechnol. 13(9), 1097–1105 (2017).
- 43 . Chitosan and its derivatives in mucosal drug and vaccine delivery. Eur. J. Pharm. Sci. 14(3), 201–207 (2001).
- 44 . Performance-enhanced cementitious materials by cellulose nanocrystal additions. In: Production and Applications of Cellulose Nanomaterials (Eds). Tappi Press, GA, USA, 2 (2013).
- 45 . A VEDA simulation on cement paste: using dynamic atomic force microscopy to characterize cellulose nanocrystal distribution. MRS Commun. 7(3), 672–676 (2017).
- 46 . The influence of cellulose nanocrystal additions on the performance of cement paste. Cement Concrete Comp. 56, 73–83 (2015).
- 47 The influence of cellulose nanocrystals on the microstructure of cement paste. Cement Concrete Comp. 74, 164–173 (2016).
- 48 . Cellulose nanocrystals: a versatile nanoplatform for emerging biomedical applications. Expert. Opin. Drug Deliv. 13(9), 1243–1256 (2016).
- 49 CD40-targeted dendritic cell delivery of PLGA-nanoparticle vaccines induce potent anti-tumor responses. Biomaterials 40, 88–97 (2015).
- 50 Polymeric nanoparticles for co-delivery of synthetic long peptide antigen and poly IC as therapeutic cancer vaccine formulation. J. Control. Rel. 203, 16–22 (2015).
- 51 . Supramolecular polymers. Chem. Rev. 101(12), 4071–4098 (2001).
- 52 A peptide-based nanofibrous hydrogel as a promising DNA nanovector for optimizing the efficacy of HIV vaccine. Nano Lett. 14(3), 1439–1445 (2014).
- 53 . Effective polymer adjuvants for sustained delivery of protein subunit vaccines. Acta Biomater. 14, 104–114 (2015).
- 54 Nanovaccine loaded with poly I:C and STAT3 siRNA robustly elicits anti-tumor immune responses through modulating tumor-associated dendritic cells in vivo. Biomaterials 38, 50–60 (2015).
- 55 . Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science 324(5923), 59–63 (2009).
- 56 . The relationship between cellulose nanocrystal dispersion and strength. Constr. Build Mater. 119, 71–79 (2016).
- 57 Reduction-sensitive dextran nanogels aimed for intracellular delivery of antigens. Adv. Funct. Mater. 25(20), 2993–3003 (2015).
- 58 . Reduction-sensitive polymer-shell-coated nanogels for intracellular delivery of antigens. ACS Appl. Mater. Interfaces 3(1), 42–48 (2016).
- 59 Engineering polymer hydrogel nanoparticles for lymph node-targeted delivery. Angew. Chem. Int. Ed. 55(4), 1334–1339 (2016).
- 60 Tailoring polymeric hybrid micelles with lymph node targeting ability to improve the potency of cancer vaccines. Biomaterials 122, 105–113 (2017).
- 61 . Acid-degradable polymers for drug delivery: a decade of innovation. Chem. Commun. 49(21), 2082–2102 (2013).
- 62 . Self-assembled hyaluronic acid nanoparticles for pH-sensitive release of doxorubicin: synthesis and in vitro characterization. J. Biomed. Nanotechnol. 13(9), 1058–1068 (2017).
- 63 pH-Responsive nanoparticle vaccines for dual-delivery of antigens and immunostimulatory oligonucleotides. ACS Nano. 7(5), 3912 (2013).
- 64 Cancer cell membrane-coated nanoparticles for anticancer vaccination and drug delivery. Nano. Lett. 14(4), 2181–2188 (2014).
- 65 A generic polymer–protein ligation strategy for vaccine delivery. Biomacromolecules 17(3), 874–881 (2016).
- 66 . Dendrimers for vaccine and immunostimulatory uses. A review. Bioconjug. Chem. 21(3), 405–418 (2009).
- 67 Self-adjuvanting polymer–peptide conjugates as therapeutic vaccine candidates against cervical cancer. Biomacromolecules 14(8), 2798–2806 (2013).
- 68 . Liposomes as immunological adjuvants. Nature 252(5480), 252–252 (1974).
- 69 A7RC peptide modified paclitaxel liposomes dually target breast cancer. Biomater. Sci. 3(12), 1545–1554 (2015).
- 70 Tamoxifen embedded in lipid bilayer improves the oncotarget of liposomal daunorubicin in vivo . . J. Mater. Chem. B 2(12), 1619–1625 (2014).
- 71 . Recent advances in liposome surface modification for oral drug delivery. Nanomedicine 11(9), 1169–1185 (2016).
- 72 . Application of pH-sensitive fusogenic polymer-modified liposomes for development of mucosal vaccines. Vet. Immunol. Immunopathol. 158(1), 62–72 (2014).
- 73 . A new adjuvant delivery system ‘cyclic di-GMP/YSK05 liposome’ for cancer immunotherapy. J. Control. Rel. 184, 20–27 (2014).
- 74 . Nanoparticle-delivered transforming growth factor-β siRNA enhances vaccination against advanced melanoma by modifying tumor microenvironment. ACS Nano. 8(4), 3636 (2014).
- 75 . Cationic liposomes loaded with a synthetic long peptide and poly (I:C): a defined adjuvanted vaccine for induction of antigen-specific T cell cytotoxicity. AAPS J. 17(1), 216–226 (2015).
- 76 . Synthesis and evaluation of monophosphoryl lipid A derivatives as fully synthetic self-adjuvanting glycoconjugate cancer vaccine carriers. Org. Biomol. Chem. 12(20), 3238–3245 (2014).
- 77 Cytosolic delivery of liposomal vaccines by means of the concomitant photosensitization of phagosomes. Mol. Pharm. 13(2), 320–329 (2016).
- 78 . Synthesis of a liposomal MUC1 glycopeptide-based immunotherapeutic and evaluation of the effect of L-rhamnose targeting on cellular immune responses. Bioconjug. Chem. 27(1), 110 (2016).
- 79 Effect of TLR ligands co-encapsulated with multiepitopic antigen in nanoliposomes targeted to human DCs via Fc receptor for cancer vaccines. Immunobiology 222(11), 989–997 (2017).
- 80 . Dextran derivative-based pH-sensitive liposomes for cancer immunotherapy. Biomaterials 35(9), 3091–3101 (2014).
- 81 . Cationic liposomes promote antigen cross-presentation in dendritic cells by alkalizing the lysosomal pH and limiting the degradation of antigens. Int. J. Nanomed. 12, 1251 (2017).
- 82 Induction of CD8+ T cell responses against subunit antigens by the novel cationic liposomal CAF09 adjuvant. Vaccine 32(31), 3927–3935 (2014).
- 83 . Genetic immunization with in vivo dendritic cell-targeting liposomal DNA vaccine carrier induces long-lasting antitumor immune response. Mol. Ther. 24(2), 385–397 (2016).
- 84 . Cationic liposomes modified with polyallylamine as a gene carrier: preparation, characterization and transfection efficiency evaluation. Adv. Pharm. Bull. 6(4), 515 (2016).
- 85 Vaccination with liposome-coupled glypican-3-derived epitope peptide stimulates cytotoxic T lymphocytes and inhibits GPC3-expressing tumor growth in mice. Biochem. Biophys. Res. Commun. 469(1), 138–143 (2016).
- 86 P5 HER2/neu-derived peptide conjugated to liposomes containing MPL adjuvant as an effective prophylactic vaccine formulation for breast cancer. Cancer Lett. 355(1), 54–60 (2014).
- 87 Lymphatic-targeted cationic liposomes: a robust vaccine adjuvant for promoting long-term immunological memory. Vaccine 32(42), 5475–5483 (2014).
- 88 Galactosylated liposome as a dendritic cell-targeted mucosal vaccine for inducing protective anti-tumor immunity. Acta Biomater. 11, 356–367 (2015).
- 89 Glycan-modified liposomes boost CD4+ and CD8+ T cell responses by targeting DC-SIGN on dendritic cells. J. Control. Rel. 160(1), 88–95 (2012).
- 90 Negatively charged carbon nanohorn supported cationic liposome nanoparticles: a novel delivery vehicle for anti-nicotine vaccine. J. Biomed. Nanotechnol. 11(12), 2197–2210 (2015).
- 91 . Cationic liposome–hyaluronic acid hybrid nanoparticles for intranasal vaccination with subunit antigens. J. Control. Rel. 208, 121–129 (2015).
- 92 High-density sub-100-nm peptide-gold nanoparticle complexes improve vaccine presentation by dendritic cells in vitro. Nanoscale Res. Lett. 8(1), 72 (2013).
- 93 . Cytotoxicity and immunological responses following oral vaccination of nanoencapsulated avian influenza virus H5 DNA vaccine with green synthesis silver nanoparticles. J. Control. Rel. 161(1), 116–123 (2012).
- 94 . Alpha-alumina nanoparticles induce efficient autophagy-dependent cross-presentation and potent antitumour response. Nat. Nanotechnol. 6(10), 645–650 (2011).
- 95 Carbon nanotubes’ surface chemistry determines their potency as vaccine nanocarriers in vitro and in vivo. J. Control. Rel. 225, 205–216 (2016).
- 96 . Silica nanoparticle as a lymph node targeting platform for vaccine delivery. ACS Appl. Mater. Interfaces 9(28), 23466–23475 (2017).
- 97 Magnetic nanovectors for the development of DNA blood-stage malaria vaccines. Nanomaterials 7(2), 30 (2017).
- 98 Delivery of the TLR ligand poly (I:C) to liver cells in vitro and in vivo by calcium phosphate nanoparticles leads to a pronounced immunostimulation. Acta Biomater. 64, 401–410 (2017).
- 99 IgA response and protection following nasal vaccination of chickens with Newcastle disease virus DNA vaccine nanoencapsulated with Ag@ SiO2 hollow nanoparticles. Sci. Rep. 6, 25720 (2016).
- 100 . Aluminum hydroxide nanoparticles show a stronger vaccine adjuvant activity than traditional aluminum hydroxide microparticles. J. Control. Rel. 173, 148–157 (2014).
- 101 . Phospholipid bilayer-coated aluminum nanoparticles as an effective vaccine adjuvant-delivery system. ACS Appl. Mater. Interfaces 7(12), 6391–6396 (2015).
- 102 Effects of gold nanoparticle-based vaccine size on lymph node delivery and cytotoxic T-lymphocyte responses. J. Control. Rel. 256, 56–67 (2017).
- 103 Gold nanoparticles as a vaccine platform: influence of size and shape on immunological responses in vitro and in vivo. ACS Nano. 7(5), 3926–3938 (2013).
- 104 . In vivo gold nanoparticle delivery of peptide vaccine induces anti-tumor immune response in prophylactic and therapeutic tumor models. Small 11(12), 1453–1459 (2015).
- 105 . ‘Multicopy multivalent’ glycopolymer-stabilized gold nanoparticles as potential synthetic cancer vaccines. J. Am. Chem. Soc. 135(25), 9362–9365 (2013).
- 106 . Superparamagnetic nanoparticle delivery of DNA vaccine. Methods Mol. Biol. 1143, 181–194 (2014).
- 107 Design of magnetic polyplexes taken up efficiently by dendritic cell for enhanced DNA vaccine delivery. Gene Ther. 21(2), 212 (2014).
- 108 . Magnetic nanomaterials for hyperthermia-based therapy and controlled drug delivery. Adv. Drug Deliv. Rev. 63(9), 789–808 (2011).
- 109 . Antitumor immunity by magnetic nanoparticle-mediated hyperthermia. Nanomedicine 9(11), 1715–1726 (2014).
- 110 Intratumoral injection of immature dendritic cells enhances antitumor effect of hyperthermia using magnetic nanoparticles. Int. J. Cancer 116(4), 624–633 (2005).
- 111 Magnetic enrichment of dendritic cell vaccine in lymph node with fluorescent-magnetic nanoparticles enhanced cancer immunotherapy. Theranostics 6(11), 2000 (2016).
- 112 Hydrolysis of model cellulose films by cellulosomes: extension of quartz crystal microbalance technique to multienzymatic complexes. J. Biotechnol. 241, 42–49 (2017).
- 113 . Lipid pore-filled silica thin-film membranes for biomimetic recovery of dilute carbohydrates. Langmuir 33(49), 14156–14166 (2017).
- 114 . Functionalized mesoporous silica materials for controlled drug delivery. Chem. Soc. Rev. 41(9), 3679–3698 (2012).
- 115 . Mesoporous silica nanoparticles act as a self-adjuvant for ovalbumin model antigen in mice. Small 9(18), 3138–3146 (2013).
- 116 . Assessment of the adjuvant activity of mesoporous silica nanoparticles in recombinant Mycoplasma hyopneumoniae antigen vaccines. Heliyon 3(1), e00225 (2017).
- 117 Sustained efficacy up to 4· 5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus Types 16 and 18: follow-up from a randomised control trial. Lancet 367(9518), 1247–1255 (2006).
- 118 . A review of clinical trials of human papillomavirus prophylactic vaccines. Vaccine 30, F123–F138 (2012).
- 119 A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N. Engl. J. Med. 372(8), 711–723 (2015).
- 120 In situ vaccination with cowpea mosaic virus nanoparticles suppresses metastatic cancer. Nat. Nanotechnol. 11(3), 295 (2016).
- 121 . Assessing sequence plasticity of a virus-like nanoparticle by evolution toward a versatile scaffold for vaccines and drug delivery. Proc. Natl. Acad. Sci. USA 112(40), 12360–12365 (2015).
- 122 A recombinant modified vaccinia ankara vaccine encoding Epstein–Barr virus (EBV) target antigens: a Phase I trial in UK patients with EBV-positive cancer. Clin. Cancer. Res. 20, 5009–5022 (2014).
- 123 Rational design of an Epstein-Barr virus vaccine targeting the receptor-binding site. Cell 162(5), 1090–1100 (2015).
- 124 . Viral-mimicking protein nanoparticle vaccine for eliciting anti-tumor responses. Biomaterials 86, 83–91 (2016).
- 125 A soluble form of the Mer receptor tyrosine kinase inhibits macrophage clearance of apoptotic cells and platelet aggregation. Blood 109(3), 1026–1033 (2007).
- 126 . Measurement of the clearance function of macrophages with (125)I-labelled polyvinyl pyrrolidone. Clin. Exp. Immunol. 20(3), 489–498 (1975).
- 127 Zwitterionic-coated “Stealth” nanoparticles for biomedical applications: recent advances in countering biomolecular corona formation and uptake by the mononuclear phagocyte system. Small 10(13), 2516–2529 (2014).
- 128 The interplay of lung surfactant proteins and lipids assimilates the macrophage clearance of nanoparticles. PLoS ONE 7(7), e40775 (2012).
- 129 . Serum-mediated recognition of liposomes by phagocytic cells of the reticuloendothelial system – The concept of tissue specificity. Adv. Drug Deliv. Rev. 32(1–2), 45–60 (1998).
- 130 Renal clearance of nanoparticles. Nat. Biotechnol. 25(10), 1165 (2007).
- 131 . Luminescent gold nanoparticles with efficient renal clearance. Angew. Chem. 123(14), 3226–3230 (2011).
- 132 Renal clearance and degradation of glutathione-coated copper nanoparticles. Bioconjug. Chem. 26(3), 511–519 (2015).
- 133 . Sub-10-nm Pd nanosheets with renal clearance for efficient near-infrared photothermal cancer therapy. Small 10(15), 3139–3144 (2014).
- 134 The biodistribution of gold nanoparticles designed for renal clearance. Nanoscale 5(13), 5930–5939 (2013).
- 135 . Drug delivery in poly(lactide-co-glycolide) nanoparticles surface modified with poloxamer 407 and poloxamine 908: in vitro characterisation and in vivo evaluation. J. Control. Rel. 70(3), 353–363 (2001).
- 136 Particle size-dependent and surface charge-dependent biodistribution of gold nanoparticles after intravenous administration. Eur. J. Pharm. Biopharm. 77(3), 407–416 (2011).
- 137 . Circulation and long-term fate of functionalized, biocompatible single-walled carbon nanotubes in mice probed by Raman spectroscopy. Proc. Natl. Acad. Sci. USA 105(5), 1410–1415 (2008).
- 138 . MR cholangiography demonstrates unsuspected rapid biliary clearance of nanoparticles in rodents: implications for clinical translation. Nanomed. Nanotech. Biol. Med. 10(7), 1385–1388 (2014).
- 139 Analysis of nanoparticle delivery to tumours. Nat. Rev. Mater. 1, 16014 (2016).
- 140 . Effect of chitosan coating in overcoming the phagocytosis of insulin loaded solid lipid nanoparticles by mononuclear phagocyte system. Carbohydr. Polym. 84(3), 919–925 (2011).
- 141 . Nanoparticles evading the reticuloendothelial system: role of the supported bilayer. BBA Biomemb. 1788(10), 2259–2266 (2009).
- 142 Passing through the renal clearance barrier: toward ultrasmall sizes with stable ligands for potential clinical applications. Int. J. Nanomedicine 9, 2069 (2014).
- 143 The effect of PEGylation of mesoporous silica nanoparticles on nonspecific binding of serum proteins and cellular responses. Biomaterials 31(6), 1085–1092 (2010).
- 144 . Compact zwitterion-coated iron oxide nanoparticles for in vitro and in vivo imaging. Integr. Biol. 5(1), 108–114 (2013).
- 145 . Glutathione. Annu. Rev. Biochem. 52(1), 711–760 (1983).
- 146 Glutathione-coated luminescent gold nanoparticles: a surface ligand for minimizing serum protein adsorption. ACS Appl. Mater. Interfaces 6(15), 11829–11833 (2014).
- 147 Size-and charge-dependent non-specific uptake of PEGylated nanoparticles by macrophages. Int. J. Nanomedicine 7, 799 (2012).
- 148 . High-density lipoprotein. Circ. Res. 114(1), 171–182 (2014).
- 149 . A high-density lipoprotein-mediated drug delivery system. Adv. Drug Deliv. Rev. 106, 132–147 (2016).
- 150 . Nanotechnology for synthetic high-density lipoproteins. Trends Mol. Med. 16(12), 553–560 (2010).
- 151 High-density lipoprotein-biomimetic nanocarriers for glioblastoma-targeting delivery: the effect of shape. Pharmazie Int. J. Pharm. Sci. 71(12), 709–714 (2016).
- 152 Nanocrystal core high-density lipoproteins: a multimodality contrast agent platform. Nano Lett. 8(11), 3715 (2008).
- 153 High-density lipoprotein-like magnetic nanostructures (HDL-MNS): theranostic agents for cardiovascular disease. Chem. Mater. 29(5), 2276–2282 (2017).
- 154 Targeting dendritic cells in lymph node with an antigen peptide-based nanovaccine for cancer immunotherapy. Biomaterials 98, 171–183 (2016).
- 155 Molecular-targeted immunotherapeutic strategy for melanoma via dual-targeting nanoparticles delivering small interfering RNA to tumor-associated macrophages. ACS Nano. 11(9), 9536–9549 (2017).
- 156 Biomimetic nanocarrier for direct cytosolic drug delivery. Angew. Chem. Int. Ed. 48(48), 9171–9175 (2009). •• Excellent research on using high-density lipoprotein-mimicking nanoparticles.
- 157 Core hydrophobicity tuning of a self-assembled particle results in efficient lipid reduction and favorable organ distribution. Nanoscale 10(1), 366–377 (2018).
- 158 . Designer vaccine nanodiscs for personalized cancer immunotherapy. Nat. Mater. 16(4), 489 (2017).
- 159 Synthetic high-density lipoprotein nanodisks for targeted withalongolide delivery to adrenocortical carcinoma. Int. J. Nanomedicine 12, 6581 (2017).
- 160 . Synthetic nano-low density lipoprotein as targeted drug delivery vehicle for glioblastoma multiforme. Int. J. Pharm. 328(1), 86–94 (2007).
- 161 . Role of high-, low-and very low-density lipoproteins in the transport and tumor-delivery of hematoporphyrin in vivo . . Cancer Lett. 32(2), 145–150 (1986).
- 162 Reconstituted low density lipoprotein: a vehicle for the delivery of hydrophobic fluorescent probes to cells. J. Cell. Biochem. 10(4), 467–478 (1979).
- 163 Reconstitution of low-density lipoproteins with fatty acids for the targeted delivery of drugs into cancer cells. Angew. Chem. Int. Ed. Engl. 56, 10399–10402 (2017).
- 164 Antigen-loaded upconversion nanoparticles for dendritic cell stimulation, tracking, and vaccination in dendritic cell-based immunotherapy. ACS Nano. 9(6), 6401–6411 (2015).
- 165 Upconversion nanoparticles modified with aminosilanes as carriers of DNA vaccine for foot-and-mouth disease. Appl. Microbiol. Biotechnol. 95(5), 1253–1263 (2012).