Next-generation viral nanoparticles for targeted delivery of therapeutics: Fundamentals, methods, biomedical applications, and challenges

References

• Joudeh N, Linke D. Nanoparticle classification, physicochemical properties, characterization, and applications: a comprehensive review for biologists. J Nanobiotechnol. 2022;20(1):1–29. doi: 10.1186/s12951-022-01477-8
   PubMed Web of Science ®Google Scholar
• Grasso S, Santi L. Viral nanoparticles as macromolecular devices for new therapeutic and pharmaceutical approaches. Int J Physiol Physiol Pharmacol. 2010;2(2):161. doi: 10.1016/j.bbagen.2010.03.005
   Google Scholar
• Cheng TM, Chu HY, Huang HM, et al. Toxicologic concerns with current medical nanoparticles. Int J Mol Sci. 2022;23(14):7597. doi: 10.3390/ijms23147597
   PubMed Web of Science ®Google Scholar
• Ealias SAM, Saravanakumar MP. A review on the classification, characterisation, synthesis of nanoparticles and their application. IOP Conf Ser Mater Sci Eng. 2017;263(3):032019. doi: 10.1088/1757-899X/263/3/032019
   Google Scholar
• Oh WK, Yoon H, Jang J. Size control of magnetic carbon nanoparticles for drug delivery. Biomaterials. 2010;31(6):1342–1348. doi: 10.1016/j.biomaterials.2009.10.018
   PubMed Web of Science ®Google Scholar
• Liu M, Zhao F, Zhu D, et al. Ultramicroporous carbon nanoparticles derived from metal–organic framework nanoparticles for high-performance supercapacitors. Mater Chem Phys. 2018;211:234–241. doi: 10.1016/j.matchemphys.2018.02.030
   Web of Science ®Google Scholar
• Chandra S, Das P, Bag S, et al. Synthesis, functionalization and bioimaging applications of highly fluorescent carbon nanoparticles. Nanoscale. 2011;3(4):1533–1540. doi: 10.1039/c0nr00735h
   PubMed Web of Science ®Google Scholar
• Mauter MS, Elimelech M. Environmental applications of carbon-based nanomaterials. Environ Sci Technol. 2008;42(16):5843–5859. doi: 10.1021/es8006904
   PubMed Web of Science ®Google Scholar
• Khan I, Saeed K, Khan I. Nanoparticles: properties, applications and toxicities. Arabian J Chem. 2019;12(7):908–931. doi: 10.1016/j.arabjc.2017.05.011
   Web of Science ®Google Scholar
• Mitchell MJ, Billingsley MM, Haley RM, et al. Engineering precision nanoparticles for drug delivery. Nat Rev Drug Discov. 2020;20(2):101–124. doi: 10.1038/s41573-020-0090-8
   PubMed Web of Science ®Google Scholar
• Pan K, Zhong Q. Organic nanoparticles in foods: fabrication, characterization, and utilization. Annu Rev Food Sci Technol. 2016;7(1):245–266. doi: 10.1146/annurev-food-041715-033215
   PubMedGoogle Scholar
• Gujrati M, Malamas A, Shin T, et al. Multifunctional cationic lipid-based nanoparticles facilitate endosomal escape and reduction-triggered cytosolic siRNA release. Mol Pharm. 2014;11(8):2734–2744. doi: 10.1021/mp400787s
   PubMedGoogle Scholar
• Wu Y, Li J, Shin HJ. Self-assembled viral nanoparticles as targeted anticancer vehicles. Biotechnol Bioproc Eng. 2021;26(1):25–38. doi: 10.1007/s12257-020-0383-0
   PubMed Web of Science ®Google Scholar
• Steinmetz NF. Viral nanoparticles as platforms for next-generation therapeutics and imaging devices. Nanomedicine. 2010;6(5):634–641. doi: 10.1016/j.nano.2010.04.005
   PubMed Web of Science ®Google Scholar
• Nkanga CI, Steinmetz NF. The pharmacology of plant virus nanoparticles. Virology. 2021;556:39–61. doi: 10.1016/j.virol.2021.01.012
   PubMed Web of Science ®Google Scholar
• Wen AM, Steinmetz NF. Design of virus-based nanomaterials for medicine, biotechnology, and energy. Chem Soc Rev. 2016;45(15):4074–4126. doi: 10.1039/C5CS00287G
   PubMed Web of Science ®Google Scholar
• Chung YH, Cai H, Steinmetz NF. Viral nanoparticles for drug delivery, imaging, immunotherapy, and theranostic applications. Adv Drug Delivery Rev. 2020;156:214–235. doi: 10.1016/j.addr.2020.06.024
   PubMed Web of Science ®Google Scholar
• Fang PY, Bowman JC, Gómez Ramos LM, et al. RNA: packaged and protected by VLPs. RSC Adv. 2018;8(38):21399–21406. doi: 10.1039/C8RA02084A
   PubMed Web of Science ®Google Scholar
• Mohsen MO, Gomes AC, Cabral-Miranda G, et al. Delivering adjuvants and antigens in separate nanoparticles eliminates the need of physical linkage for effective vaccination. J Controlled Release. 2017;251:92–100. doi: 10.1016/j.jconrel.2017.02.031
   PubMed Web of Science ®Google Scholar
• Zhang Q, Xu D, Guo Q, et al. Theranostic quercetin nanoparticle for treatment of hepatic fibrosis. Bioconjug Chem. 2019;30(11):2939–2946. doi: 10.1021/acs.bioconjchem.9b00631
   PubMed Web of Science ®Google Scholar
• Banskota S, Raguram A, Suh S, et al. Engineered virus-like particles for efficient in vivo delivery of therapeutic proteins. Cell. 2022;185(2):250–265. doi: 10.1016/j.cell.2021.12.021
   PubMed Web of Science ®Google Scholar
• Vervoort DFM, Heiringhoff R, Timmermans SBPE, et al. Dual site-selective presentation of functional handles on protein-engineered cowpea chlorotic mottle virus-like particles. Bioconjug Chem. 2021;32(5):958–963. doi: 10.1021/acs.bioconjchem.1c00108
   PubMed Web of Science ®Google Scholar
• Tan FH, Kong JC, Ng JF, et al. Recombinant turnip yellow mosaic virus coat protein as a potential nanocarrier. J Appl Microbiol. 2021;131(4):2072–2080. doi: 10.1111/jam.15048
   PubMed Web of Science ®Google Scholar
• Zhao L, Kopylov M, Potter CS, et al. Engineering the PP7 virus capsid as a peptide display platform. ACS Nano. 2019;13(4):4443–4454. doi: 10.1021/acsnano.8b09683
   PubMed Web of Science ®Google Scholar
• Shan X, Gong X, Li J, et al. Current approaches of nanomedicines in the market and various stage of clinical translation. Acta Pharm Sin B. 2022;12(7):3028–3048. doi: 10.1016/j.apsb.2022.02.025
   PubMed Web of Science ®Google Scholar
• Venkataraman S, Apka P, Shoeb E, et al. Plant virus nanoparticles for anti-cancer therapy. Front Bioeng Biotechnol. 2021;9:642794. doi: 10.3389/fbioe.2021.642794
   PubMed Web of Science ®Google Scholar
• Aljabali AAA, Hassan SS, Pabari RM, et al. The viral capsid as novel nanomaterials for drug delivery. Future Sci OA. 2021;7(9):FSO744. doi: 10.2144/fsoa-2021-0031
   PubMed Web of Science ®Google Scholar
• Czapar AE, Zheng YR, Riddell IA, et al. Tobacco mosaic virus delivery of phenanthriplatin for cancer therapy. ACS Nano. 2016;10(4):4119–4126. doi: 10.1021/acsnano.5b07360
   PubMed Web of Science ®Google Scholar
• DHT L, KL L, Shukla S, et al. Potato virus X, a filamentous plant viral nanoparticle for doxorubicin delivery in cancer therapy. Nanoscale. 2017;9(6):2348–2357. doi: 10.1039/C6NR09099K
   PubMed Web of Science ®Google Scholar
• Lomonossoff GP, Wege C. TMV particles: the journey from fundamental studies to bionanotechnology applications. Adv Virus Res. 2018;102:149–176.
   PubMed Web of Science ®Google Scholar
• Röder J, Dickmeis C, Commandeur U. Small, smaller, nano: new applications for potato virus X in nanotechnology. Front Plant Sci. 2019;10:158. doi: 10.3389/fpls.2019.00158
   PubMed Web of Science ®Google Scholar
• Bruckman MA, Randolph LN, VanMeter A, et al. Biodistribution, pharmacokinetics, and blood compatibility of native and PEGylated tobacco mosaic virus nano-rods and -spheres in mice. Virology. 2014;449:163–173. doi: 10.1016/j.virol.2013.10.035
   PubMed Web of Science ®Google Scholar
• Hu H, Steinmetz NF. Cisplatin prodrug-loaded nanoparticles based on physalis mottle virus for cancer therapy. Mol Pharm. 2020;17(12):4629–4636. doi: 10.1021/acs.molpharmaceut.0c00834
   PubMedGoogle Scholar
• Hu H, Masarapu H, Gu Y, et al. Physalis mottle virus-like nanoparticles for targeted cancer imaging. ACS Appl Mater Interfaces. 2019;11(20):18213–18223. doi: 10.1021/acsami.9b03956
   PubMed Web of Science ®Google Scholar
• Beatty PH, Lewis JD. Cowpea mosaic virus nanoparticles for cancer imaging and therapy. Adv Drug Deliv Rev. 2019;145:130–144. doi: 10.1016/j.addr.2019.04.005
   PubMed Web of Science ®Google Scholar
• Destito G, Yeh R, Rae CS, et al. Folic acid-mediated targeting of cowpea mosaic virus particles to tumor cells. Chem Biol. 2007;14(10):1152–1162. doi: 10.1016/j.chembiol.2007.08.015
   PubMedGoogle Scholar
• Singh P, Prasuhn D, Yeh RM, et al. Bio-distribution, toxicity and pathology of cowpea mosaic virus nanoparticles in vivo. J Control Release. 2007;120(1–2):41–50. doi: 10.1016/j.jconrel.2007.04.003
   PubMed Web of Science ®Google Scholar
• Shukla S, Hu H, Cai H, et al. Plant viruses and bacteriophage-based reagents for diagnosis and therapy. Annu Rev Virol. 2020;7(1):559–587. doi: 10.1146/annurev-virology-010720-052252
   PubMedGoogle Scholar
• Yan D, Teng Z, Sun S, et al. Foot-and-mouth disease virus-like particles as integrin-based drug delivery system achieve targeting anti-tumor efficacy. Nanomedicine. 2017;13(3):1061–1070. doi: 10.1016/j.nano.2016.12.007
   PubMed Web of Science ®Google Scholar
• Louten J. Chapter 2, Virus structure and classification. Essential Human Virology. 1st ed. Amsterdam (Netherlands): Elsevier Academic Press; 2016. p. 19–29.
   Google Scholar
• Lee KW, Tan WS. Recombinant hepatitis B virus core particles: association, dissociation and encapsidation of green fluorescent protein. J Virol Methods. 2008;151(2):172–180. doi: 10.1016/j.jviromet.2008.05.025
   PubMed Web of Science ®Google Scholar
• Lee KW, Tey BT, Ho KL, et al. Nanoglue: an alternative way to display cell-internalizing peptide at the spikes of hepatitis b virus core nanoparticles for cell-targeting delivery. Mol Pharm. 2012;9(9):2415–2423. doi: 10.1021/mp200389t
   PubMed Web of Science ®Google Scholar
• Akwiditya MA, Yong CY, Yusof MT, et al. Hepatitis B virus-like particle: targeted delivery of plasmid expressing short hairpin RNA for silencing the Bcl-2 gene in cervical cancer cells. Int J Mol Sci. 2021;22(5):2320. doi: 10.3390/ijms22052320
   PubMed Web of Science ®Google Scholar
• Biabanikhankahdani R, Alitheen NBM, Ho KL, et al. pH-responsive virus-like nanoparticles with enhanced tumour-targeting ligands for cancer drug delivery. Sci Rep. 2016;6(1):6. doi: 10.1038/srep37891
   PubMedGoogle Scholar
• Biabanikhankahdani R, Bayat S, Ho KL, et al. A simple add-and-display method for immobilisation of cancer drug on His-tagged virus-like nanoparticles for controlled drug delivery. Sci Rep. 2017;7(1):1–12. doi: 10.1038/s41598-017-05525-4
   PubMedGoogle Scholar
• Biabanikhankahdani R, Ho KL, Alitheen NB, et al. A dual bioconjugated virus-like nanoparticle as a drug delivery system and comparison with a Ph-responsive delivery system. Nanomaterials. 2018;8(4):236. doi: 10.3390/nano8040236
   Web of Science ®Google Scholar
• Gan BK, Yong CY, Ho KL, et al. Targeted delivery of cell penetrating peptide virus-like nanoparticles to skin cancer cells. Sci Rep. 2018;8(1):8499. doi: 10.1038/s41598-018-26749-y
   PubMedGoogle Scholar
• Gan BK, Rullah K, Yong CY, et al. Targeted delivery of 5-fluorouracil-1-acetic acid (5-FA) to cancer cells overexpressing epithelial growth factor receptor (EGFR) using virus-like nanoparticles. Sci Rep. 2020;10(1):16867. doi: 10.1038/s41598-020-73967-4
   PubMed Web of Science ®Google Scholar
• Shan W, Zhang D, Wu Y, et al. Modularized peptides modified HBc virus-like particles for encapsulation and tumor-targeted delivery of doxorubicin. Nanomedicine. 2018;14(3):725–734. doi: 10.1016/j.nano.2017.12.002
   PubMed Web of Science ®Google Scholar
• Cripe TP, Dunphy EJ, Holub AD, et al. Fiber knob modifications overcome low, heterogeneous expression of the coxsackievirus-adenovirus receptor that limits adenovirus gene transfer and oncolysis for human rhabdomyosarcoma cells. Cancer Res. 2001;61(7):2953–2960.
   PubMed Web of Science ®Google Scholar
• Kelly FJ, Miller CR, Buchsbaum DJ, et al. Selectivity of TAG-72-targeted adenovirus gene transfer to primary ovarian carcinoma cells versus autologous mesothelial cells in vitro. Clin Cancer Res. 2000;6(11):4323–4333.
   PubMed Web of Science ®Google Scholar
• Yamamoto Y, Nagasato M, Rin Y, et al. Strong antitumor efficacy of a pancreatic tumor-targeting oncolytic adenovirus for neuroendocrine tumors. Cancer Med. 2017;6(10):2385–2397. doi: 10.1002/cam4.1185
   PubMed Web of Science ®Google Scholar
• Mangeot PE, Risson V, Fusil F, et al. Genome editing in primary cells and in vivo using viral-derived Nanoblades loaded with Cas9-sgRNA ribonucleoproteins. Nat Commun. 2019;10(45). doi: 10.1038/s41467-018-07845-z
   PubMedGoogle Scholar
• Lu Y, Chan W, Ko BY, et al. Assessing sequence plasticity of a virus-like nanoparticle by evolution toward a versatile scaffold for vaccines and drug delivery. Proc Natl Acad Sci U S A. 2015;112(40):12360–12365. doi: 10.1073/pnas.1510533112
   PubMed Web of Science ®Google Scholar
• Thong QX, Biabanikhankahdani R, Ho KL, et al. Thermally-responsive virus-like particle for targeted delivery of cancer drug. Sci Rep. 2019;9(1):1–14. doi: 10.1038/s41598-019-40388-x
   PubMedGoogle Scholar
• Räty JK, Airenne KJ, Marttila AT, et al. Enhanced gene delivery by avidin-displaying baculovirus. Mol Ther. 2004;9(2):282–291. doi: 10.1016/j.ymthe.2003.11.004
   PubMed Web of Science ®Google Scholar
• Hendrix RW. Bacteriophage genomics. Curr Opin Microbiol. 2003;6(5):506–511. doi: 10.1016/j.mib.2003.09.004
   PubMed Web of Science ®Google Scholar
• Fokine A, Rossmann MG. Molecular architecture of tailed double-stranded DNA phages. Bacteriophage. 2014;4(2):e28281. doi: 10.4161/bact.28281
   PubMedGoogle Scholar
• Tao P, Mahalingam M, Marasa BS, et al. In vitro and in vivo delivery of genes and proteins using the bacteriophage T4 DNA packaging machine. Proc Natl Acad Sci U S A. 2013;110(15):5846–5851. doi: 10.1073/pnas.1300867110
   PubMed Web of Science ®Google Scholar
• Murgas P, Bustamante N, Araya N, et al. A filamentous bacteriophage targeted to carcinoembryonic antigen induces tumor regression in mouse models of colorectal cancer. Cancer Immunol Immunother. 2018;67(2):183–193. doi: 10.1007/s00262-017-2076-x
   PubMed Web of Science ®Google Scholar
• Ghosh D, Kohli AG, Moser F, et al. Refactored M13 bacteriophage as a platform for tumor cell imaging and drug delivery. ACS Synth Biol. 2012;1(12):576–582. doi: 10.1021/sb300052u
   PubMed Web of Science ®Google Scholar
• Chen Z, Li N, Chen L, et al. Dual functionalized bacteriophage Qβ as a photocaged drug carrier. Small. 2016;12(33):4563–4571. doi: 10.1002/smll.201601053
   PubMed Web of Science ®Google Scholar
• Bichet MC, Chin WH, Richards W, et al. Bacteriophage uptake by mammalian cell layers represents a potential sink that may impact phage therapy. iScience. 2021;24(4):102287. doi: 10.1016/j.isci.2021.102287
   PubMed Web of Science ®Google Scholar
• Atabekov J, Nikitin N, Arkhipenko M, et al. Thermal transition of native tobacco mosaic virus and RNA-free viral proteins into spherical nanoparticles. J Gen Virol. 2011;92(2):453–456. doi: 10.1099/vir.0.024356-0
   PubMedGoogle Scholar
• McCormick AA, Corbo TA, Wykoff-Clary S, et al. Chemical conjugate TMV−peptide bivalent fusion vaccines improve cellular immunity and tumor protection. Bioconjug Chem. 2006;17(5):1330–1338. doi: 10.1021/bc060124m
   PubMed Web of Science ®Google Scholar
• Baratova LA, Grebenshchikov NI, Dobrov EN, et al. The organization of potato virus X coat proteins in virus particles studied by tritium planigraphy and model building. Virology. 1992;188(1):175–180. doi: 10.1016/0042-6822(92)90747-D
   PubMed Web of Science ®Google Scholar
• Jobsri J, Allen A, Rajagopal D, et al. Plant virus particles carrying tumour antigen activate TLR7 and induce high levels of protective antibody. PLoS One. 2015;10(2):e0118096. doi: 10.1371/journal.pone.0118096
   PubMed Web of Science ®Google Scholar
• Nikitin N, Ksenofontov A, Trifonova E, et al. Thermal conversion of filamentous potato virus X into spherical particles with different properties from virions. FEBS Lett. 2016;590(10):1543–1551. doi: 10.1002/1873-3468.12184
   PubMed Web of Science ®Google Scholar
• Marusic C, Rizza P, Lattanzi L, et al. Chimeric plant virus particles as immunogens for inducing murine and human immune responses against human immunodeficiency virus type 1. J Virol. 2001;75(18):8434. doi: 10.1128/JVI.75.18.8434-8439.2001
   PubMed Web of Science ®Google Scholar
• Shukla S, Dickmeis C, Fischer R, et al. In planta production of fluorescent filamentous plant virus-based nanoparticles. Methods Mol Biol. 2018;1776:61–84.
   PubMedGoogle Scholar
• Shukla S, Jandzinski M, Wang C, et al. A viral nanoparticle cancer vaccine delays tumor progression and prolongs survival in a HER2+ tumor mouse model. Adv Ther. 2019;2(4):1800139. doi: 10.1002/adtp.201800139
   Google Scholar
• Ma Y, Nolte RJM, JJLM C. Virus-based nanocarriers for drug delivery. Adv Drug Deliv Rev. 2012;64(9):811–825. doi: 10.1016/j.addr.2012.01.005
   PubMed Web of Science ®Google Scholar
• Steinmetz NF, Ablack AL, Hickey JL, et al. Intravital imaging of human prostate cancer using viral nanoparticles targeted to gastrin-releasing peptide receptors. Small. 2011;7(12):1664–1672. doi: 10.1002/smll.201000435
   PubMed Web of Science ®Google Scholar
• Leong HS, Steinmetz NF, Ablack A, et al. Intravital imaging of embryonic and tumor neovasculature using viral nanoparticles. Nat Protoc. 2010;5(8):1406–1417. doi: 10.1038/nprot.2010.103
   PubMed Web of Science ®Google Scholar
• Suffian IFM, Wang JTW, Faruqu FN, et al. Engineering human epidermal growth receptor 2-targeting hepatitis b virus core nanoparticles for siRNA delivery in vitro and in vivo. ACS Appl Nano Mater. 2018;1(7):3269–3282. doi: 10.1021/acsanm.8b00480
   PubMed Web of Science ®Google Scholar
• Bredehorst R, Von Wulffen H, Granato C. Quantitation of hepatitis B virus (HBV) core antigen in serum in the presence of antibodies to HBV core antigen: comparison with assays of serum HBV DNA, DNA polymerase, and HBV e antigen. J Clin Microbiol. 1985;21(4):593–598. doi: 10.1128/jcm.21.4.593-598.1985
   PubMed Web of Science ®Google Scholar
• Newman M, Suk FM, Cajimat M, et al. Stability and morphology comparisons of self-assembled virus-like particles from wild-type and mutant human hepatitis B virus capsid proteins. J Virol. 2003;77(24):12950–12960. doi: 10.1128/JVI.77.24.12950-12960.2003
   PubMed Web of Science ®Google Scholar
• Lundstrom K. Viral vectors in gene therapy. Diseases. 2018;6(2):42. doi: 10.3390/diseases6020042
   PubMedGoogle Scholar
• Tamura RE, Lana MG, Costanzi-Strauss E, et al. Combination of cabazitaxel and p53 gene therapy abolishes prostate carcinoma tumor growth. Genet Ther. 2019;27(1):15–26. doi: 10.1038/s41434-019-0071-x
   PubMed Web of Science ®Google Scholar
• Wu DT, Roth MJ. MLV based viral-like-particles for delivery of toxic proteins and nuclear transcription factors. Biomaterials. 2014;35(29):8416–8426. doi: 10.1016/j.biomaterials.2014.06.006
   PubMed Web of Science ®Google Scholar
• Yong CY, Yeap SK, Ho KL, et al. Potential recombinant vaccine against influenza a virus based on M2e displayed on nodaviral capsid nanoparticles. Int J Nanomedicine. 2015;10:2751–2763. doi: 10.2147/IJN.S77405
   PubMed Web of Science ®Google Scholar
• Ong HK, Yong CY, Tan WS, et al. An influenza a vaccine based on the extracellular domain of matrix 2 protein protects BALB/C mice against H1N1 and H3N2. Vaccines (Basel). 2019;7(3):91. doi: 10.3390/vaccines7030091
   PubMed Web of Science ®Google Scholar
• Kueh CL, Yong CY, Seyedehsara MD, et al. Virus-like particle of Macrobrachium rosenbergii nodavirus produced in Spodoptera frugiperda (Sf9) cells is distinctive from that produced in Escherichia coli. Biotechnol Prog. 2017;33(2):549–557. doi: 10.1002/btpr.2409
   PubMed Web of Science ®Google Scholar
• van Houten NE, Henry KA, Smith GP, et al. Engineering filamentous phage carriers to improve focusing of antibody responses against peptides. Vaccine. 2010;28(10):2174–2185. doi: 10.1016/j.vaccine.2009.12.059
   PubMed Web of Science ®Google Scholar
• Ksendzovsky A, Walbridge S, Saunders RC, et al. Convection-enhanced delivery of M13 bacteriophage to the brain: laboratory investigation. J Neurosurg. 2012;117(2):197–203. doi: 10.3171/2012.4.JNS111528
   PubMed Web of Science ®Google Scholar
• Karimi M, Mirshekari H, Moosavi Basri SM, et al. Bacteriophages and phage-inspired nanocarriers for targeted delivery of therapeutic cargos. Adv Drug Deliv Rev. 2016;106(Pt A):45–62. doi: 10.1016/j.addr.2016.03.003
   PubMedGoogle Scholar
• Martino ML, Crooke SN, Manchester M, et al. Single-point mutations in qβ virus-like particles change binding to cells. Biomacromolecules. 2021;22(8):3332–3341. doi: 10.1021/acs.biomac.1c00443
   PubMed Web of Science ®Google Scholar
• Cellular & Gene Therapy Products [Internet]. Silver Spring (MD): food and Drug Administration (FDA); 2023 [updated 2023 March 20; cited 2023 April 15]. Available from: https://www.fda.gov/vaccines-blood-biologics/cellular-gene-therapy-products
   Google Scholar
• Ma CC, Wang ZL, Xu T, et al. The approved gene therapy drugs worldwide: from 1998 to 2019. Biotechnol Adv. 2020;40:107502. doi: 10.1016/j.biotechadv.2019.107502
   PubMed Web of Science ®Google Scholar
• Marcucci KT, Jadlowsky JK, Hwang WT, et al. Retroviral and lentiviral safety analysis of gene-modified T cell products and infused HIV and oncology patients. Mol Ther. 2018;26(1):269–279. doi: 10.1016/j.ymthe.2017.10.012
   PubMed Web of Science ®Google Scholar
• Gordon EM, Hall FL. Rexin-G, a targeted genetic medicine for cancer. Expert Opin Biol Ther. 2010;10(5):819–382. doi: 10.1517/14712598.2010.481666
   PubMed Web of Science ®Google Scholar
• Chawla SP, Bruckner H, Morse MA, et al. A phase I-II study using Rexin-G tumor-targeted retrovector encoding a dominant-negative Cyclin G1 inhibitor for advanced pancreatic cancer. Mol Ther Oncolytics. 2019;12:56–67. doi: 10.1016/j.omto.2018.12.005
   PubMed Web of Science ®Google Scholar
• Peng Z. Current status of gendicine in china: recombinant human Ad-p53 agent for treatment of cancers. Hum Gene Ther. 2005;16(9):1016–1027. doi: 10.1089/hum.2005.16.1016
   PubMed Web of Science ®Google Scholar
• Zhang WW, Li L, Li D, et al. The first approved gene therapy product for cancer Ad-p53 (Gendicine): 12 years in the clinic. Hum Gene Ther. 2018;29(2):160–179. doi: 10.1089/hum.2017.218
   PubMed Web of Science ®Google Scholar
• Ran FA, Cong L, Yan WX, et al. In vivo genome editing using Staphylococcus aureus Cas9. Nature. 2015;520(7546):186–191. doi: 10.1038/nature14299
   PubMed Web of Science ®Google Scholar
• Rodrigues GA, Shalaev E, Karami TK, et al. Pharmaceutical development of AAV-based gene therapy products for the eye. Pharm Res. 2018;36(2):1–20. doi: 10.1007/s11095-018-2554-7
   PubMed Web of Science ®Google Scholar
• Russell S, Bennett J, Wellman JA, et al. Efficacy and safety of voretigene neparvovec (AAV2-hRpe65v2) in patients with RPE65-mediated inherited retinal dystrophy: a randomised, controlled, open-label, phase 3 trial. Lancet. 2017;390(10097):849–860. doi: 10.1016/S0140-6736(17)31868-8
   PubMed Web of Science ®Google Scholar
• Hoy SM. Onasemnogene abeparvovec: first global approval. Drugs. 2019;79(11):1255–1262. doi: 10.1007/s40265-019-01162-5
   PubMed Web of Science ®Google Scholar
• Mercuri E, Muntoni F, Baranello G, et al. Onasemnogene abeparvovec gene therapy for symptomatic infantile-onset spinal muscular atrophy type 1 (Str1VE-EU): an open-label, single-arm, multicentre, phase 3 trial. Lancet Neurol. 2021;20(10):832–841. doi: 10.1016/S1474-4422(21)00251-9
   PubMed Web of Science ®Google Scholar
• Wang X, Ma C, Labrada RR, et al. Recent advances in lentiviral vectors for gene therapy. Sci China Life Sci. 2021;64(11):1842–1857. doi: 10.1007/s11427-021-1952-5
   PubMed Web of Science ®Google Scholar
• Kohn DB, Booth C, Shaw KL, et al. Autologous ex vivo lentiviral gene therapy for adenosine deaminase deficiency. N Engl J Med. 2021;384(21):2002–2013. doi: 10.1056/NEJMoa2027675
   PubMed Web of Science ®Google Scholar
• Bulcha JT, Wang Y, Ma H, et al. Viral vector platforms within the gene therapy landscape. Sig Transduct Target Ther. 2021;6(1):1–24. doi: 10.1038/s41392-021-00487-6
   PubMed Web of Science ®Google Scholar
• Wraith DC. The future of immunotherapy: a 20-year perspective. Front Immunol. 2017;8:1668. doi: 10.3389/fimmu.2017.01668
   PubMed Web of Science ®Google Scholar
• Rolih V, Caldeira J, Bolli E, et al. Development of a vlp-based vaccine displaying an XCT extracellular domain for the treatment of metastatic breast cancer. Cancers. 2020;12(6):1492. doi: 10.3390/cancers12061492
   PubMed Web of Science ®Google Scholar
• Maurer P, Jennings GT, Willers J, et al. A therapeutic vaccine for nicotine dependence: preclinical efficacy, and Phase I safety and immunogenicity. Eur J Immunol. 2005;35(7):2031–2040. doi: 10.1002/eji.200526285
   PubMed Web of Science ®Google Scholar
• Cornuz J, Zwahlen S, Jungi WF, et al. A vaccine against nicotine for smoking cessation: a randomized controlled trial. PLoS One. 2008;3(6):e2547. doi: 10.1371/journal.pone.0002547
   PubMed Web of Science ®Google Scholar
• Jin H, Wang W, Zhao S, et al. Aβ-HBc virus-like particles immunization without additional adjuvant ameliorates the learning and memory and reduces Aβ deposit in PDAPP mice. Vaccine. 2014;32(35):4450–4456. doi: 10.1016/j.vaccine.2014.06.051
   PubMed Web of Science ®Google Scholar
• Vahdat MM, Hemmati F, Ghorbani A, et al. Hepatitis B core-based virus-like particles: a platform for vaccine development in plants. Biotechnol Rep (Amst). 2021;29:e00605. doi: 10.1016/j.btre.2021.e00605
   PubMedGoogle Scholar
• McCann N, O’Connor D, Lambe T, et al. Viral vector vaccines. Curr Opin Immunol. 2022;77:102210. doi: 10.1016/j.coi.2022.102210
   PubMed Web of Science ®Google Scholar
• Brown DR, Garland S, Ferris DG, et al. The humoral response to Gardasil over four years as defined by total IgG and competitive Luminex immunoassay. Hum Vaccin. 2011;7(2):230–238. doi: 10.4161/hv.7.2.13948
   PubMed Web of Science ®Google Scholar
• Zhang X, Wei M, Pan H, et al. Robust manufacturing and comprehensive characterization of recombinant hepatitis E virus-like particles in Hecolin®. Vaccine. 2014;32(32):4039–4050. doi: 10.1016/j.vaccine.2014.05.064
   PubMed Web of Science ®Google Scholar
• Zhu FC, Li YH, Guan XH, et al. Safety, tolerability, and immunogenicity of a recombinant adenovirus type-5 vectored COVID-19 vaccine: a dose-escalation, open-label, non-randomised, first-in-human trial. Lancet. 2020;395(10240):1845–1854. doi: 10.1016/S0140-6736(20)31208-3
   PubMed Web of Science ®Google Scholar
• Falsey AR, Sobieszczyk ME, Hirsch I, et al. Phase 3 safety and efficacy of AZD1222 (ChAdox1 nCoV-19) Covid-19 vaccine. N Engl J Med. 2021;385(25):2348–2360. doi: 10.1056/NEJMoa2105290
   PubMed Web of Science ®Google Scholar
• Logunov DY, Dolzhikova IV, Shcheblyakov DV, et al. Safety and efficacy of an rAd26 and rAd5 vector-based heterologous prime-boost COVID-19 vaccine: an interim analysis of a randomised controlled phase 3 trial in Russia. Lancet. 2021;397(10275):671–681. doi: 10.1016/S0140-6736(21)00234-8
   PubMed Web of Science ®Google Scholar
• Malik N, Arfin T, Khan AU. Graphene nanomaterials: chemistry and pharmaceutical perspectives. In: Alexandru MG, editor. Nanomaterials for Drug Delivery and Therapy. Amsterdam (Netherlands): Elsevier Academic Press; 2019. p. 373–402. doi: 10.1016/B978-0-12-816505-8.00002-3.
   Google Scholar
• Min X, Zhang J, Li RH, et al. Encapsulation of NIR-II AIEgens in virus-like particles for bioimaging. ACS Appl Mater Interfaces. 2021;13(15):17372–17379. doi: 10.1021/acsami.1c02691
   PubMed Web of Science ®Google Scholar
• Nuñez-Rivera A, Fournier PGJ, Arellano DL, et al. Brome mosaic virus-like particles as siRNA nanocarriers for biomedical purposes. Beilstein J Nanotechnol. 2020;11(1):372–382. doi: 10.3762/bjnano.11.28
   PubMedGoogle Scholar
• Xue F, Cornelissen JJLM, Yuan Q, et al. Delivery of MicroRNAs by plant virus-based nanoparticles to functionally alter the osteogenic differentiation of human mesenchymal stem cells. Chin Chem Lett. 2023;34(1):107448. doi: 10.1016/j.cclet.2022.04.046
   Web of Science ®Google Scholar
• Ribas A, Medina T, Kirkwood JM, et al. Overcoming PD-1 blockade resistance with CpG-A toll-like receptor 9 agonist vidutolimod in patients with metastatic melanoma. Cancer Discov. 2021;11(12):2998–3007. doi: 10.1158/2159-8290.CD-21-0425
   PubMed Web of Science ®Google Scholar
• Herrera Estrada LP, Champion JA. Protein nanoparticles for therapeutic protein delivery. Biomater Sci. 2015;3(6):787–799. doi: 10.1039/C5BM00052A
   PubMed Web of Science ®Google Scholar
• Chauhan K, Olivares-Medina CN, M V V-E, et al. Targeted enzymatic VLP-nanoreactors with β-glucocerebrosidase activity as potential enzyme replacement therapy for gaucher’s disease. ChemMedchem. 2022;17(19):e202200384. doi: 10.1002/cmdc.202200384
   PubMed Web of Science ®Google Scholar
• Hamilton JR, Tsuchida CA, Nguyen DN, et al. Targeted delivery of CRISPR-Cas9 and transgenes enables complex immune cell engineering. Cell Rep. 2021;35(9):109207. doi: 10.1016/j.celrep.2021.109207
   PubMed Web of Science ®Google Scholar
• Man L, Zhen L, Xun S, et al. A polymeric prodrug of 5-fluorouracil-1-acetic acid using a multi-hydroxyl polyethylene glycol derivative as the drug carrier. PLoS One. 2014;9(11):e112888. doi: 10.1371/journal.pone.0112888
   PubMed Web of Science ®Google Scholar
• Fu DY, Zhang S, Qu Z, et al. Hybrid assembly toward enhanced thermal stability of virus-like particles and antibacterial activity of polyoxometalates. ACS Appl Mater Interfaces. 2018;10(7):6137–6145. doi: 10.1021/acsami.7b17082
   PubMed Web of Science ®Google Scholar
• European Medicines Agency (EMA). Zolgensma. (EMA/200482/2020). Amsterdam(Netherlands): EMA; 2020.
   Google Scholar
• Carbonaro DA, Zhang L, Jin X, et al. Preclinical demonstration of lentiviral vector-mediated correction of immunological and metabolic abnormalities in models of adenosine deaminase deficiency. Mol Ther. 2014;22(3):607–622. doi: 10.1038/mt.2013.265
   PubMed Web of Science ®Google Scholar
• Feng G, Wang W, Qian Y, et al. Anti-Aβ antibodies induced by Aβ-HBc virus-like particles prevent Aβ aggregation and protect PC12 cells against toxicity of Aβ1–40. J Neurosci Methods. 2013;218(1):48–54. doi: 10.1016/j.jneumeth.2013.05.006
   PubMed Web of Science ®Google Scholar
• Emini EA, Ellis RW, Miller WJ, et al. Production and immunological analysis of recombinant hepatitis B vaccine. J Infect. 1986;13(SUPPL. A):3–9. doi: 10.1016/S0163-4453(86)92563-6
   PubMed Web of Science ®Google Scholar
• European Medicines Agency (EMA). Gardasil 9. (EMA/CHMP/76591/2015). London(UK): EMA; 2015.
   Google Scholar
• Committee for Medicinal Product for Human Use (CHMP). Caervarix – Scientific Discussion. Amsterdam: European Medicines Agency; 2007.
   Google Scholar
• Yang C, Pan H, Wei M, et al. Hepatitis E virus capsid protein assembles in 4M urea in the presence of salts. Protein Sci. 2013;22(3):314–326. doi: 10.1002/pro.2213
   PubMed Web of Science ®Google Scholar
• Halperin SA, Ye L, MacKinnon-Cameron D, et al. Final efficacy analysis, interim safety analysis, and immunogenicity of a single dose of recombinant novel coronavirus vaccine (adenovirus type 5 vector) in adults 18 years and older: an international, multicentre, randomised, double-blinded, placebo-controlled phase 3 trial. Lancet. 2022;399(10321):237–248. doi: 10.1016/S0140-6736(21)02753-7
   PubMed Web of Science ®Google Scholar
• Joe CCD, Jiang J, Linke T, et al. Manufacturing a chimpanzee adenovirus-vectored SARS-CoV-2 vaccine to meet global needs. Biotechnol Bioeng. 2022;119(1):48–58. doi: 10.1002/bit.27945
   PubMed Web of Science ®Google Scholar
• The Gamaleya Center statement [Internet]. Moscow: The Gamaleya National Center; [cited 2023 May 23]. Available from: https://sputnikvaccine.com/newsroom/pressreleases/the-gamaleya-center-statement/.
   Google Scholar
• Roos WH, Ivanovska IL, Evilevitch A, et al. Viral capsids: mechanical characteristics, genome packaging and delivery mechanisms. Cellular Mol Lide Sci. 2007;64(12):1484–1497. doi: 10.1007/s00018-007-6451-1
   PubMed Web of Science ®Google Scholar
• Fiedler JD, Brown SD, Lau JL, et al. RNA-directed packaging of enzymes within virus-like particles. Angew Chem Int Ed Engl. 2010;49(50):9648–9651. doi: 10.1002/anie.201005243
   PubMed Web of Science ®Google Scholar
• Roldão A, Silva AC, Mellado MCM, et al. Chapter 1.47, Viruses and virus-like particles in biotechnology: fundamentals and applications. Compr biotechno. 3rd edAmsterdam (Netherlands): Elsevier; 2017. p. 633–656.
   Google Scholar
• Selivanovitch E, LaFrance B, Douglas T. Molecular exclusion limits for diffusion across a porous capsid. Nat Commun. 2021;12(1):1–12. doi: 10.1038/s41467-021-23200-1
   PubMed Web of Science ®Google Scholar
• Chou MI, Hsieh YF, Wang M, et al. In vitro and in vivo targeted delivery of IL-10 interfering RNA by JC virus-like particles. J Biomed Sci. 2010;17(1):51. doi: 10.1186/1423-0127-17-51
   PubMedGoogle Scholar
• Touze A, Bousarghin L, Ster C, et al. Gene transfer using human polyomavirus BK virus-like particles expressed in insect cells. J Gen Virol. 2001;82(12):3005–3009. doi: 10.1099/0022-1317-82-12-3005
   PubMedGoogle Scholar
• Uchida M, Klem MT, Allen M, et al. Biological containers: protein cages as multifunctional nanoplatforms. Adv Mater. 2007;19(8):1025–1042. doi: 10.1002/adma.200601168
   Web of Science ®Google Scholar
• Choi KM, Choi SH, Jeon H, et al. Chimeric capsid protein as a nanocarrier for siRNA delivery: stability and cellular uptake of encapsulated siRNA. ACS Nano. 2011;5(11):8690–8699. doi: 10.1021/nn202597c
   PubMed Web of Science ®Google Scholar
• Ashley CE, Carnes EC, Phillips GK, et al. Cell-specific delivery of diverse cargos by bacteriophage MS2 virus-like particles. ACS Nano. 2011;5(7):5729–5745. doi: 10.1021/nn201397z
   PubMed Web of Science ®Google Scholar
• Galaway FA, Stockley PG. MS2 virus like particles: a robust, semisynthetic targeted drug delivery platform. Mol Pharm. 2013;10(1):59–68. doi: 10.1021/mp3003368
   PubMedGoogle Scholar
• Comellas-Aragonès M, Engelkamp H, Claessen VI, et al. A virus-based single-enzyme nanoreactor. Nat Nanotech. 2007;2(10):635–639. doi: 10.1038/nnano.2007.299
   PubMed Web of Science ®Google Scholar
• Yang Z, Wang X, Diao H, et al. Encapsulation of platinum anticancer drugs by apoferritin. Chem Commun. 2007;33:3453–3455. doi: 10.1039/b705326f
   PubMed Web of Science ®Google Scholar
• He J, Yu L, Lin X, et al. Virus-like particles as nanocarriers for intracellular delivery of biomolecules and compounds. Viruses. 2022;14(9):1905. doi: 10.3390/v14091905
   PubMed Web of Science ®Google Scholar
• Wang Q, Chan TR, Hilgraf R, et al. Bioconjugation by copper(I)-catalyzed azide-alkyne [3 + 2] cycloaddition. J Am Chem Soc. 2003;125(11):3192–3193. doi: 10.1021/ja021381e
   PubMed Web of Science ®Google Scholar
• Meunier S, Strable E, Finn MG. Crosslinking of and coupling to viral capsid proteins by tyrosine oxidation. Chem Biol. 2004;11(3):319–326. doi: 10.1016/j.chembiol.2004.02.019
   PubMedGoogle Scholar
• Sen GS, Kuzelka J, Singh P, et al. Accelerated bioorthogonal conjugation: a practical method for the ligation of diverse functional molecules to a polyvalent virus scaffold. Bioconjug Chem. 2005;16(6):1572–1579. doi: 10.1021/bc050147l
   PubMed Web of Science ®Google Scholar
• Zochowska M, Paca A, Schoehn G, et al. Adenovirus dodecahedron, as a drug delivery vector. PLoS One. 2009;4(5):e5569. doi: 10.1371/journal.pone.0005569
   PubMed Web of Science ®Google Scholar
• Zhao Q, Chen W, Chen Y, et al. Self-assembled virus-like particles from rotavirus structural protein VP6 for targeted drug delivery. Bioconjug Chem. 2011;22(3):346–352. doi: 10.1021/bc1002532
   PubMed Web of Science ®Google Scholar
• Ren D, Kratz F, Wang SW. Engineered drug-protein nanoparticle complexes for folate receptor targeting. Biochem Eng J. 2014 Aug 15;89:33–41.
   PubMed Web of Science ®Google Scholar
• O’Neil A, Reichhardt C, Johnson B, et al. Genetically programmed in vivo packaging of protein cargo and its controlled release from bacteriophage P22. Angew Chem Int Ed Engl. 2011;50(32):7425–7428. doi: 10.1002/anie.201102036
   PubMed Web of Science ®Google Scholar
• O’Neil A, Prevelige PE, Basu G, et al. Coconfinement of fluorescent proteins: spatially enforced communication of GFP and mCherry encapsulated within the P22 capsid. Biomacromolecules. 2012;13(12):3902–3907. doi: 10.1021/bm301347x
   PubMed Web of Science ®Google Scholar
• Wang Y, Uchida M, Waghwani HK, et al. Synthetic virus-like particles for glutathione biosynthesis. ACS Synth Biol. 2020;9(12):3298–3310. doi: 10.1021/acssynbio.0c00368
   PubMed Web of Science ®Google Scholar
• Sharma J, Uchida M, Miettinen HM, et al. Modular interior loading and exterior decoration of a virus-like particle. Nanoscale. 2017;9(29):10420–10430. doi: 10.1039/C7NR03018E
   PubMed Web of Science ®Google Scholar
• Sharma J, Douglas T. Tuning the catalytic properties of P22 nanoreactors through compositional control. Nanoscale. 2020;12(1):336–346. doi: 10.1039/C9NR08348K
   PubMed Web of Science ®Google Scholar
• Brune KD, Leneghan DB, Brian IJ, et al. Plug-and-Display: decoration of Virus-Like Particles via isopeptide bonds for modular immunization. Sci Rep. 2016;6(1):1–13. doi: 10.1038/srep19234
   PubMedGoogle Scholar
• Kim H, Choi H, Bae Y, et al. Development of target-tunable P22 VLP-based delivery nanoplatforms using bacterial superglue. Biotechnol Bioeng. 2019;116(11):2843–2851. doi: 10.1002/bit.27129
   PubMed Web of Science ®Google Scholar
• Hartzell EJ, Lieser RM, Sullivan MO, et al. Modular hepatitis B virus-like particle platform for biosensing and drug delivery. ACS Nano. 2020;14(10):12642–12651. doi: 10.1021/acsnano.9b08756
   PubMed Web of Science ®Google Scholar
• Tan S, Wang G. Lung cancer targeted therapy: folate and transferrin dual targeted, glutathione responsive nanocarriers for the delivery of cisplatin. Biomed Pharmacother. 2018;102:55–63. doi: 10.1016/j.biopha.2018.03.046
   PubMed Web of Science ®Google Scholar
• Mateu MG. Virus engineering: functionalization and stabilization. Protein Eng Des And Sel. 2011;24(1–2):53–63. doi: 10.1093/protein/gzq069
   PubMed Web of Science ®Google Scholar
• Yildiz I, Lee KL, Chen K, et al. Infusion of imaging and therapeutic molecules into the plant virus-based carrier cowpea mosaic virus: cargo-loading and delivery. J Controlled Release. 2013;172(2):568–578. doi: 10.1016/j.jconrel.2013.04.023
   PubMed Web of Science ®Google Scholar
• Zeng Q, Wen H, Wen Q, et al. Cucumber mosaic virus as drug delivery vehicle for doxorubicin. Biomaterials. 2013;34(19):4632–4642. doi: 10.1016/j.biomaterials.2013.03.017
   PubMed Web of Science ®Google Scholar
• Ren Y, Sek MW, Lim LY. Folic acid-conjugated protein cages of a plant virus: a novel delivery platform for doxorubicin. Bioconjug Chem. 2007;18(3):836–843. doi: 10.1021/bc060361p
   PubMed Web of Science ®Google Scholar
• Brasch M, Putri RM, De Ruiter MV, et al. Assembling enzymatic cascade pathways inside virus-based nanocages using dual-tasking nucleic acid tags. J Am Chem Soc. 2017;139(4):1512–1519. doi: 10.1021/jacs.6b10948
   PubMed Web of Science ®Google Scholar
• Glasgow JE, Capehart SL, Francis MB, et al. Osmolyte-mediated encapsulation of proteins inside MS2 viral capsids. ACS Nano. 2012;6(10):8658–8664. doi: 10.1021/nn302183h
   PubMed Web of Science ®Google Scholar
• Lu X, Thompson JR, Perry KL. Encapsidation of DNA, a protein and a fluorophore into virus-like particles by the capsid protein of cucumber mosaic virus. J Gen Virol. 2012;93(5):1120–1126. doi: 10.1099/vir.0.040170-0
   PubMedGoogle Scholar
• Aljabali AAA, Shukla S, Lomonossoff GP, et al. CPMV-DOX Delivers. Mol Pharm. 2013;10(1):3–10. doi: 10.1021/mp3002057
   PubMedGoogle Scholar
• Herbert FC, Brohlin OR, Galbraith T, et al. Supramolecular encapsulation of small-ultrared fluorescent proteins in virus-like nanoparticles for noninvasive in vivo imaging agents. Bioconjug Chem. 2020;31(5):1529–1536. doi: 10.1021/acs.bioconjchem.0c00190
   PubMed Web of Science ®Google Scholar
• Koo OM, Rubinstein I, Onyuksel H. Role of nanotechnology in targeted drug delivery and imaging: a concise review. Nanomedicine. 2005;1(3):193–212. doi: 10.1016/j.nano.2005.06.004
   PubMed Web of Science ®Google Scholar
• Plummer EM, Manchester M. Endocytic uptake pathways utilized by CPMV nanoparticles. Mol Pharm. 2013;10(1):26–32. doi: 10.1021/mp300238w
   PubMedGoogle Scholar
• Donahue ND, Acar H, Wilhelm S. Concepts of nanoparticle cellular uptake, intracellular trafficking, and kinetics in nanomedicine. Adv Drug Deliv Rev. 2019;143:68–96. doi: 10.1016/j.addr.2019.04.008
   PubMed Web of Science ®Google Scholar
• Makvandi P, Chen M, Sartorius R, et al. Endocytosis of abiotic nanomaterials and nanobiovectors: inhibition of membrane trafficking. Nano Today. 2021;40:101279. doi: 10.1016/j.nantod.2021.101279
   PubMed Web of Science ®Google Scholar
• Jain KK. Drug delivery systems - an overview. Methods Mol Biol. 2008;437:1–50.
   PubMedGoogle Scholar
• Casi G, Neri D. Antibody-drug conjugates and small molecule-drug conjugates: opportunities and challenges for the development of selective anticancer cytotoxic agents. J Med Chem. 2015;58(22):8751–8761. doi: 10.1021/acs.jmedchem.5b00457
   PubMed Web of Science ®Google Scholar
• Lewis Phillips GD, Li G, Dugger DL, et al. Targeting HER2-positive breast cancer with trastuzumab-DM1, an antibody–cytotoxic drug conjugate. Cancer Res. 2008;68(22):9280–9290. doi: 10.1158/0008-5472.CAN-08-1776
   PubMed Web of Science ®Google Scholar
• Goldenberg MM. Trastuzumab, a recombinant DNA-derived humanized monoclonal antibody, a novel agent for the treatment of metastatic breast cancer. Clin Ther. 1999;21(2):309–318. doi: 10.1016/S0149-2918(00)88288-0
   PubMed Web of Science ®Google Scholar
• Zhang F, Shan L, Liu Y, et al. An anti-PSMA bivalent immunotoxin exhibits specificity and efficacy for prostate cancer imaging and therapy. Adv Healthc Mater. 2013;2(5):736–744. doi: 10.1002/adhm.201200254
   PubMed Web of Science ®Google Scholar
• Dawidczyk CM, Kim C, Park JH, et al. State-of-the-art in design rules for drug delivery platforms: lessons learned from FDA-approved nanomedicines. J Control Release. 2014;187:133–144. doi: 10.1016/j.jconrel.2014.05.036
   PubMed Web of Science ®Google Scholar
• Rohovie MJ, Nagasawa M, Swartz JR. Virus-like particles: next-generation nanoparticles for targeted therapeutic delivery. Bioeng Transl Med. 2017;2(1):43–57. doi: 10.1002/btm2.10049
   PubMed Web of Science ®Google Scholar
• Lu RM, Chang YL, Chen MS, et al. Single chain anti-c-Met antibody conjugated nanoparticles for in vivo tumor-targeted imaging and drug delivery. Biomaterials. 2011;32(12):3265–3274. doi: 10.1016/j.biomaterials.2010.12.061
   PubMed Web of Science ®Google Scholar
• Hadjipanayis CG, Machaidze R, Kaluzova M, et al. EGFRvIII antibody-conjugated iron oxide nanoparticles for magnetic resonance imaging-guided convection-enhanced delivery and targeted therapy of glioblastoma. Cancer Res. 2010;70(15):6303–6312. doi: 10.1158/0008-5472.CAN-10-1022
   PubMed Web of Science ®Google Scholar
• Ling Y, Wei K, Luo Y, et al. Dual docetaxel/superparamagnetic iron oxide loaded nanoparticles for both targeting magnetic resonance imaging and cancer therapy. Biomaterials. 2011;32(29):7139–7150. doi: 10.1016/j.biomaterials.2011.05.089
   PubMed Web of Science ®Google Scholar
• Murphy EA, Majeti BK, Barnes LA, et al. Nanoparticle-mediated drug delivery to tumor vasculature suppresses metastasis. Proc Natl Acad Sci U S A. 2008;105(27):9343–9348. doi: 10.1073/pnas.0803728105
   PubMed Web of Science ®Google Scholar
• Tian Y, Zhou M, Shi H, et al. Integration of cell-penetrating peptides with rod-like bionanoparticles: virus-inspired gene-silencing technology. Nano Lett. 2018;18(9):5453–5460. doi: 10.1021/acs.nanolett.8b01805
   PubMed Web of Science ®Google Scholar
• Sharma G, Modgil A, Zhong T, et al. Influence of short-chain cell-penetrating peptides on transport of doxorubicin encapsulating receptor-targeted liposomes across brain endothelial barrier. Pharm Res. 2014;31(5):1194–1209. doi: 10.1007/s11095-013-1242-x
   PubMed Web of Science ®Google Scholar
• Jayapaul J, Hodenius M, Arns S, et al. FMN-coated fluorescent iron oxide nanoparticles for RCP-mediated targeting and labeling of metabolically active cancer and endothelial cells. Biomaterials. 2011;32(25):5863–5871. doi: 10.1016/j.biomaterials.2011.04.056
   PubMed Web of Science ®Google Scholar
• Rhee JK, Baksh M, Nycholat C, et al. Glycan-targeted virus-like nanoparticles for photodynamic therapy. Biomacromolecules. 2012;13(8):2333–2338. doi: 10.1021/bm300578p
   PubMed Web of Science ®Google Scholar
• Ferreira CSM, Cheung MC, Missailidis S, et al. Phototoxic aptamers selectively enter and kill epithelial cancer cells. Nucleic Acids Res. 2009;37(3):866–876. doi: 10.1093/nar/gkn967
   PubMed Web of Science ®Google Scholar
• Meng L, Yang L, Zhao X, et al. Targeted delivery of chemotherapy agents using a liver cancer-specific aptamer. PLoS One. 2012;7(4):e33434. doi: 10.1371/journal.pone.0033434
   PubMed Web of Science ®Google Scholar
• Yu MK, Kim D, Lee IH, et al. Image-guided prostate cancer therapy using aptamer-functionalized thermally cross-linked superparamagnetic iron oxide nanoparticles. Small. 2011;7(15):2241–2249. doi: 10.1002/smll.201100472
   PubMed Web of Science ®Google Scholar
• Wu W, Shen J, Banerjee P, et al. Core–shell hybrid nanogels for integration of optical temperature-sensing, targeted tumor cell imaging, and combined chemo-photothermal treatment. Biomaterials. 2010;31(29):7555–7566. doi: 10.1016/j.biomaterials.2010.06.030
   PubMed Web of Science ®Google Scholar
• Yu MK, Park J, Jon S. Targeting strategies for multifunctional nanoparticles in cancer imaging and therapy. Theranostics. 2012;2(1):3–44. doi: 10.7150/thno.3463
   PubMed Web of Science ®Google Scholar
• Banerjee D, Liu AP, Voss NR, et al. Multivalent display and receptor-mediated endocytosis of transferrin on virus-like particles. Chembiochem. 2010;11(9):1273–1279. doi: 10.1002/cbic.201000125
   PubMed Web of Science ®Google Scholar
• Kaltgrad E, O’Reilly MK, Liao L, et al. On-virus construction of polyvalent glycan ligands for cell-surface receptors. J Am Chem Soc. 2008;130(14):4578–4579. doi: 10.1021/ja077801n
   PubMed Web of Science ®Google Scholar
• Lu B, Javidi-Parsijani P, Makani V, et al. Delivering SaCas9 mRNA by lentivirus-like bionanoparticles for transient expression and efficient genome editing. Nucleic Acids Res. 2019;47(8):e44. doi: 10.1093/nar/gkz093
   PubMed Web of Science ®Google Scholar
• Coroadinha AS. Cancer gene therapy: development and production of lentiviral vectors for gene therapy. Methods Mol Biol. 2022;2521:297–315.
   PubMedGoogle Scholar
• Deng L, Liang P, Cui H. Pseudotyped lentiviral vectors: ready for translation into targeted cancer gene therapy? Genes Dis. 2022. doi: 10.1016/j.gendis.2022.03.007
   Web of Science ®Google Scholar
• Shapira S, Finkelshtein E, Kazanov D, et al. Integrase-derived peptides together with CD24-targeted lentiviral particles inhibit the growth of CD24 expressing cancer cells. Oncogene. 2021;40(22):3815–3825. doi: 10.1038/s41388-021-01779-5
   PubMed Web of Science ®Google Scholar
• Lei Y, Il JK, Zarzar J, et al. Targeting lentiviral vector to specific cell types through surface displayed single chain antibody and fusogenic molecule. Virol J. 2010;7(1):1–12. doi: 10.1186/1743-422X-7-35
   PubMedGoogle Scholar
• Kasaraneni N, Chamoun-Emanuelli AM, Wright G, et al. Retargeting lentiviruses via spyCatcher-spyTag chemistry for gene delivery into specific cell types. MBio. 2017;8(6):e01860–17. doi: 10.1128/mBio.01860-17
   PubMed Web of Science ®Google Scholar
• Xing H, Yang X, Xu Y, et al. Anti-tumor effects of vascular endothelial growth factor/vascular endothelial growth factor receptor binding domain-modified chimeric antigen receptor T cells. Cytotherapy. 2021;23(9):810–819. doi: 10.1016/j.jcyt.2021.05.008
   PubMed Web of Science ®Google Scholar
• Wathoni N, Puluhulawa LE, Joni IM, et al. Monoclonal antibody as a targeting mediator for nanoparticle targeted delivery system for lung cancer. Drug Deliv. 2022;29(1):2959–2970. doi: 10.1080/10717544.2022.2120566
   PubMed Web of Science ®Google Scholar
• Arslan FB, Ozturk AK, Calis S. Antibody-mediated drug delivery. Int J Pharm. 2021;596:120268. doi: 10.1016/j.ijpharm.2021.120268
   PubMedGoogle Scholar
• Guo YY, Huang L, Zhang ZP, et al. Strategies for precise engineering and conjugation of antibody targeted-nanoparticles for cancer therapy. Curr Med Sci. 2020;40(3):463–473. doi: 10.1007/s11596-020-2200-6
   PubMed Web of Science ®Google Scholar
• Aanei IL, ElSohly Am, Farkas ME, et al. Biodistribution of antibody-MS2 viral capsid conjugates in breast cancer models. Mol Pharm. 2016;13(11):3764–3772. doi: 10.1021/acs.molpharmaceut.6b00566
   PubMedGoogle Scholar
• Du B, Qian M, Zhou Z, et al. In vitro panning of a targeting peptide to hepatocarcinoma from a phage display peptide library. Biochem Biophys Res Commun. 2006;342(3):956–962. doi: 10.1016/j.bbrc.2006.02.050
   PubMed Web of Science ®Google Scholar
• Zhao P, Grabinski T, Gao C, et al. Identification of a met-binding peptide from a phage display library. Clin Cancer Res. 2007;13(20):6049–6055. doi: 10.1158/1078-0432.CCR-07-0035
   PubMed Web of Science ®Google Scholar
• Mohamed Suffian IFB, Wang JT, Hodgins NO, et al. Engineering hepatitis B virus core particles for targeting HER2 receptors in vitro and in vivo. Biomaterials. 2017;120:126–138. doi: 10.1016/j.biomaterials.2016.12.012
   PubMed Web of Science ®Google Scholar
• Jiang YQ, Wang HR, Li HP, et al. Targeting of hepatoma cell and suppression of tumor growth by a novel 12mer peptide fused to superantigen TSST-1. Mol Med. 2006;12(4–6):81–87. doi: 10.2119/2006-00011.Jiang
   PubMed Web of Science ®Google Scholar
• Lo A, Lin CT, Wu HC. Hepatocellular carcinoma cell-specific peptide ligand for targeted drug delivery. Mol Cancer Ther. 2008;7(3):579–589. doi: 10.1158/1535-7163.MCT-07-2359
   PubMed Web of Science ®Google Scholar
• Zhang B, Zhang Y, Wang J, et al. Screening and identification of a targeting peptide to hepatocarcinoma from a phage display peptide library. Mol Med. 2007;13(5–6):246–254. doi: 10.2119/2006-00115.Zhang
   PubMed Web of Science ®Google Scholar
• Zang L, Shi L, Guo J, et al. Screening and Identification of a peptide specifically targeted to NCI-H1299 from a phage display peptide library. Cancer Lett. 2009;281(1):64–70. doi: 10.1016/j.canlet.2009.02.021
   PubMed Web of Science ®Google Scholar
• Chang DK, Lin CT, Wu CH, et al. A novel peptide enhances therapeutic efficacy of liposomal anti-cancer drugs in mice models of human lung cancer. PLoS One. 2009;4(1):e4171. doi: 10.1371/journal.pone.0004171
   PubMed Web of Science ®Google Scholar
• Zhu Y, Feijen J, Zhong Z. Dual-targeted nanomedicines for enhanced tumor treatment. Nano Today. 2018;18:65–85. doi: 10.1016/j.nantod.2017.12.007
   Web of Science ®Google Scholar
• Mishra N, Pant P, Porwal A, et al. Targeted drug delivery: a review. Am J PharmTech. 2016;6:1–24.
   Google Scholar
• Gujral S, Khatri S. A review on basic concept of drug targeting and drug carrier system. IJAPBC. 2013;2(1):130–136.
   Google Scholar
• Jain A, Jain SK. Pegylation: an approach for drug delivery. A review. Crit Rev Ther Drug Carrier Syst. 2008;25(5):403–447. doi: 10.1615/CritRevTherDrugCarrierSyst.v25.i5.10
   PubMed Web of Science ®Google Scholar
• Fam SY, Chee CF, Yong CY, et al. Shielding of hepatitis B virus-like nanoparticle with poly(2-ethyl-2-oxazoline). J Mol Sci. 2019;20(19):4903. doi: 10.3390/ijms20194903
   Google Scholar
• Das S, Yau MK, Noble J, et al. Transport of molecular cargo by interaction with virus-like particle RNA. Angew Chem Int Ed Engl. 2022;61(2):e202111687. doi: 10.1002/anie.202111687
   PubMed Web of Science ®Google Scholar
• Lockney DM, Guenther RN, Loo L, et al. The Red clover necrotic mosaic virus capsid as a multifunctional cell targeting plant viral nanoparticle. Bioconjug Chem. 2011;22(1):67–73. doi: 10.1021/bc100361z
   PubMed Web of Science ®Google Scholar
• Cao J, Guenther RH, Sit TL, et al. Loading and release mechanism of Red clover necrotic mosaic virus derived plant viral nanoparticles for drug delivery of doxorubicin. Small. 2014;10(24):5126–5136. doi: 10.1002/smll.201400558
   PubMed Web of Science ®Google Scholar
• Alemzadeh E, Dehshahri A, Dehghanian AR, et al. Enhanced anti-tumor efficacy and reduced cardiotoxicity of doxorubicin delivered in a novel plant virus nanoparticle. Colloids Surf B Biointerfaces. 2019;174:80–86. doi: 10.1016/j.colsurfb.2018.11.008
   PubMed Web of Science ®Google Scholar
• Kelly MP, Napolitano T, Anand P, et al. Induced disassembly of a virus-like particle under physiological conditions for venom peptide delivery. Bioconjug Chem. 2021;32(1):111–120. doi: 10.1021/acs.bioconjchem.0c00494
   PubMed Web of Science ®Google Scholar
• Fang PY, LM G, Omez R, et al. Functional RNAs: combined assembly and packaging in VLPs. Nucleic Acids Res. 2016;45(6):3519–3527. doi: 10.1093/nar/gkw1154
   Web of Science ®Google Scholar
• Shahrivarkevishahi A, Luzuriaga MA, Herbert FC, et al. PhotothermalPhage: a virus-based photothermal therapeutic agent. J Am Chem Soc. 2021;143(40):16428–16438. doi: 10.1021/jacs.1c05090
   PubMed Web of Science ®Google Scholar
• Benjamin CE, Chen Z, Kang P, et al. Site-selective nucleation and size control of gold nanoparticle photothermal antennae on the pore structures of a virus. J Am Chem Soc. 2018;140(49):17226–1723. doi: 10.1021/jacs.8b10446
   PubMed Web of Science ®Google Scholar
• Hu H, Steinmetz NF. Doxorubicin-loaded physalis mottle virus particles function as a ph-responsive prodrug enabling cancer therapy. Biotechnol J. 2020;15(12):e2000077. doi: 10.1002/biot.202000077
   PubMed Web of Science ®Google Scholar
• Sushant T, Avinash G, Onkar S. Nanomedicine market size and share. Growth Prediction-2030. (A01691) . London (UK): Allied Market Research; 2020.
   Google Scholar
• Chang L, Wang G, Jia T, et al. Armored long non-coding RNA MEG3 targeting EGFR based on recombinant MS2 bacteriophage virus-like particles against hepatocellular carcinoma. Oncotarget. 2016;7(17):23988–24004. doi: 10.18632/oncotarget.8115
   PubMedGoogle Scholar
• Los GV, Encell LP, McDougall MG, et al. HaloTag: a novel protein labeling technology for cell imaging and protein analysis. ACS Chem Biol. 2008;3(6):373–382. doi: 10.1021/cb800025k
   PubMed Web of Science ®Google Scholar
• Keppler A, Kindermann M, Gendreizig S, et al. Labeling of fusion proteins of O6-alkylguanine-DNA alkyltransferase with small molecules in vivo and in vitro. Methods. 2004;32(4):437–444. doi: 10.1016/j.ymeth.2003.10.007
   PubMed Web of Science ®Google Scholar
• Mao H, Hart SA, Schink A, et al. Sortase-Mediated Protein Ligation: a New Method for Protein Engineering. J Am Chem Soc. 2004;126(9):2670–2671. doi: 10.1021/ja039915e
   PubMed Web of Science ®Google Scholar
• Stevens AJ, Brown ZZ, Shah NH, et al. Design of a split intein with exceptional protein splicing activity. J Am Chem Soc. 2016;138(7):2162–2165. doi: 10.1021/jacs.5b13528
   PubMed Web of Science ®Google Scholar
• Lilie H, Richter S, Bergelt S, et al. Polyionic and cysteine-containing fusion peptides as versatile protein tags. Biol Chem. 2013;394(8):995–1004. doi: 10.1515/hsz-2013-0116
   PubMed Web of Science ®Google Scholar
• Wijesundara DK, Avumegah MS, Lackenby J, et al. Rapid response subunit vaccine design in the absence of structural information. Front Immunol. 2020;11:592370. doi: 10.3389/fimmu.2020.592370
   PubMed Web of Science ®Google Scholar
• Chappell KJ, Mordant FL, Li Z, et al. Safety and immunogenicity of an MF59-adjuvanted spike glycoprotein-clamp vaccine for SARS-CoV-2: a randomised, double-blind, placebo-controlled, phase 1 trial. Lancet Infect Dis. 2021;21(10):1383–1394. doi: 10.1016/S1473-3099(21)00200-0
   PubMed Web of Science ®Google Scholar
• Krutzke L, Rösler R, Allmendinger E, et al. Process- and product-related impurities in the ChAdOx1 nCov-19 vaccine. Elife. 2022;11:e78513. doi: 10.7554/eLife.78513
   PubMed Web of Science ®Google Scholar
• Boado RJ, Hui EKW, Lu JZ, et al. Selective targeting of a TNFR decoy receptor pharmaceutical to the primate brain as a receptor-specific IgG fusion protein. J Biotechnol. 2010;146(1–2):84–91. doi: 10.1016/j.jbiotec.2010.01.011
   PubMed Web of Science ®Google Scholar
• van den Broek SL, Shalgunov V, Herth MM, et al. Transport of nanomedicines across the blood-brain barrier: challenges and opportunities for imaging and therapy. Biomater Adv. 2022;141:213125. doi: 10.1016/j.bioadv.2022.213125
   PubMedGoogle Scholar
• Zhang Y, Pardridge WM. Near complete rescue of experimental parkinson’s disease with intravenous, non-viral GDNF gene therapy. Pharm Res. 2009;26(5):1059–1063. doi: 10.1007/s11095-008-9815-9
   PubMed Web of Science ®Google Scholar
• Zhang L, Guo X, Chu J, et al. Potential hippocampal genes and pathways involved in Alzheimer’s disease: a bioinformatic analysis. Genet Mol Res. 2015;14(2):7218–7232. doi: 10.4238/2015.June.29.15
   PubMed Web of Science ®Google Scholar
• Wang X, Matteson J, An Y, et al. COPII-dependent export of cystic fibrosis transmembrane conductance regulator from the ER uses a di-acidic exit code. J Cell Bio. 2004;167(1):65–74. doi: 10.1083/jcb.200401035
   PubMed Web of Science ®Google Scholar
• Cohen-Tannoudji M, Marchand P, Akli S, et al. Disruption of murine Hexa gene leads to enzymatic deficiency and to neuronal lysosomal storage, similar to that observed in Tay-Sachs disease. Mammalian Genome. 1995;6(12):844–849. doi: 10.1007/BF00292433
   PubMed Web of Science ®Google Scholar
• Eckhardt SG, Milich DR, McLachlan A. Hepatitis B virus core antigen has two nuclear localization sequences in the arginine-rich carboxyl terminus. J Virol. 1991;65(2):575. doi: 10.1128/jvi.65.2.575-582.1991
   PubMed Web of Science ®Google Scholar
• Hanapi UF, Yong CY, Goh ZH, et al. Tracking the virus-like particles of Macrobrachium rosenbergii nodavirus in insect cells. PeerJ. 2017;5(2):e2947. doi: 10.7717/peerj.2947
   PubMedGoogle Scholar
• Yu H, Koilkonda RD, Chou TH, et al. Gene delivery to mitochondria by targeting modified adenoassociated virus suppresses Leber’s hereditary optic neuropathy in a mouse model. Proc Natl Acad Sci U S A. 2012;109(20):1238–1247. doi: 10.1073/pnas.1119577109
   PubMed Web of Science ®Google Scholar