Skip to main content
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 2021 Feb 10;26(1):25–38. doi: 10.1007/s12257-020-0383-0

Self-assembled Viral Nanoparticles as Targeted Anticancer Vehicles

Yuanzheng Wu 1, Jishun Li 1, Hyun-Jae Shin 2,
PMCID: PMC7872722  PMID: 33584104

Abstract

Viral nanoparticles (VNPs) comprise a variety of mammalian viruses, plant viruses, and bacteriophages, that have been adopted as building blocks and supra-molecular templates in nanotechnology. VNPs demonstrate the dynamic, monodisperse, polyvalent, and symmetrical architectures which represent examples of such biological templates. These programmable scaffolds have been exploited for genetic and chemical manipulation for displaying of targeted moieties together with encapsulation of various payloads for diagnosis or therapeutic intervention. The drug delivery system based on VNPs offer diverse advantages over synthetic nanoparticles, including biocompatibility, biodegradability, water solubility, and high uptake capability. Here we summarize the recent progress of VNPs especially as targeted anticancer vehicles from the encapsulation and surface modification mechanisms, involved viruses and VNPs, to their application potentials.

Keywords: viral nanoparticles (VNPs), self-assembly, anticancer, drug delivery, nanotechnology

Acknowledgements

This study was funded by Shandong Provincial Key Research and Development Program (International Science and Technology Cooperation, Grant No. 2019GHZ033), International Science and Technology Cooperation Program of Shandong Academy of Sciences (Grant No. 2019GHPY05).

Nomenclature

AAV

adeno-associated virus

Ad

adenovirus

AlDox

aldoxorubicin

ASGPRs

asialoglycoprotein receptors

Apf

apoferritin

biRNA

bifunctional linker RNA

βlac

β-lactamase

BPC

9-biphenylcarbonyl

BSA

bovine serum albumin

CCMV

cowpea chlorotic mottle virus

CPMV

cowpea mosaic virus

CT

computed tomography

CuAAC

copper(I)-catalyzed azide-alkyne cycloaddition

DOC

docetaxel

DOX

doxorubicin

E1A

early 1 A adenoviral

EGFP

enhanced green fluorescent protein

EGFR

epidermal growth factor receptor

FA

folic acid

Fah

fumarylacetoacetate hydrolase

GBM

glioblastoma multiforme

GM-CSF

granulocyte-macro-phage colony-stimulating factor

HBV

hepatitis B virus

HCC

human hepatocellular carcinoma

HepG2

human hepatocellular carcinomas

HER

human epidermal receptor

HPV

human papillomavirus

Hsps

heat shock proteins

HSV

herpes simplex virus

ICP6

infected cell protein 6

MCF7

Michigan cancer foundation-7

MHC

major histocompatibility complex

Mo-MLV

Moloney murine leukemia virus

MRI

magnetic resonance imaging

MTO

mitoxantrone

MV

measles virus

NDV

Newcastle disease virus

NHS

N-hydroxysuccinimide

NIR

near-infrared

NIS

sodium-iodide symporter

NPs

nanoparticles

NSP10

nonstructural protein 10

OVs

oncolytic viruses

PAA

polyacrylamide

PEG

polyethylene glycol

PET

positron emission tomography

PhenPt

phenanthriplatin

PSeD

selenocompound

PVX

potato virus X

RCNMV

red clover necrotic mosaic virus

SARS

severe acute respiratory syndrome

scFv

single-chain antibody variable fragment

SeMV

sesbania mosaic virus

siRNA

small interfering RNA

tHBcAg

truncated hepatitis B virus core antigen

TMV

tobacco mosaic virus

VEGFR

vascular endothelial growth factor receptor

VLPs

virus-like particles

VNPs

viral nanoparticles

Footnotes

Ethical Statements

The authors declare no conflict of interest.

Neither ethical approval nor informed consent was required for this study.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  • 1.Drbohlavova J, Chomoucka J, Adam V, Ryvolova M, Eckschlager T, Hubalek J, Kizek R. Nanocarriers for anticancer drugs — new trends in nanomedicine. Curr. Drug Metab. 2013;14:547–564. doi: 10.2174/1389200211314050005. [DOI] [PubMed] [Google Scholar]
  • 2.Sercombe L, Veerati T, Moheimani F, Wu S Y, Sood A K, Hua S. Advances and challenges of liposome assisted drug delivery. Front. Pharmacol. 2015;6:286. doi: 10.3389/fphar.2015.00286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Kamaly N, Xiao Z, Valencia P M, Radovic-Moreno A F, Farokhzad O C. Targeted polymeric therapeutic nanoparticles: design, development and clinical translation. Chem. Soc. Rev. 2012;41:2971–3010. doi: 10.1039/c2cs15344k. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Wang F, Li C, Cheng J, Yuan Z. Recent advances on inorganic nanoparticle-based cancer therapeutic agents. Int. J. Environ. Res. Public Health. 2016;13:1182. doi: 10.3390/ijerph13121182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Chung Y H, Cai H, Steinmetz N F. Viral nanoparticles for drug delivery, imaging, immunotherapy, and theranostic applications. Adv. Drug Deliv. Rev. 2020;156:214–235. doi: 10.1016/j.addr.2020.06.024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Sanvicens N, Marco M P. Multifunctional nanoparticles-properties and prospects for their use in human medicine. Trends Biotechnol. 2008;26:425–433. doi: 10.1016/j.tibtech.2008.04.005. [DOI] [PubMed] [Google Scholar]
  • 7.Srinivasan M, Rajabi M, Mousa S A. Multifunctional nanomaterials and their applications in drug delivery and cancer therapy. Nanomaterials. 2015;5:1690–1703. doi: 10.3390/nano5041690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Sykes E A, Dai Q, Sarsons C D, Chen J, Rocheleau J V, Hwang D M, Zheng G, Cramb D T, Rinker K D, Chan W C. Tailoring nanoparticle designs to target cancer based on tumor pathophysiology. Proc. Natl. Acad. Sci. U.S.A. 2016;113:E1142–E1151. doi: 10.1073/pnas.1521265113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Steinmetz N F. Viral nanoparticles as platforms for next-generation therapeutics and imaging devices. Nanomedicine. 2010;6:634–641. doi: 10.1016/j.nano.2010.04.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Ma Y, Nolte R J M, Cornelissen J J L M. Virus-based nanocarriers for drug delivery. Adv. Drug Deliv. Rev. 2012;64:811–825. doi: 10.1016/j.addr.2012.01.005. [DOI] [PubMed] [Google Scholar]
  • 11.Xin Y, Yin M, Zhao L, Meng F, Luo L. Recent progress on nanoparticle-based drug delivery systems for cancer therapy. Cancer Biol. Med. 2017;14:228–241. doi: 10.20892/j.issn.2095-3941.2017.0052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Rohovie M J, Nagasawa M, Swartz J R. Virus-like particles: Next-generation nanoparticles for targeted therapeutic delivery. Bioeng. Transl. Med. 2017;2:43–57. doi: 10.1002/btm2.10049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Zdanowicz M, Chroboczek J. Virus-like particles as drug delivery vectors. Acta Biochim. Pol. 2016;63:469–473. doi: 10.18388/abp.2016_1275. [DOI] [PubMed] [Google Scholar]
  • 14.Cho K, Wang X, Nie S, Chen Z G, Shin D M. Therapeutic nanoparticles for drug delivery in cancer. Clin. Cancer Res. 2008;14:1310–1316. doi: 10.1158/1078-0432.CCR-07-1441. [DOI] [PubMed] [Google Scholar]
  • 15.Manchester M, Singh P. Virus-based nanoparticles (VNPs): platform technologies for diagnostic imaging. Adv. Drug Deliv. Rev. 2006;58:1505–1522. doi: 10.1016/j.addr.2006.09.014. [DOI] [PubMed] [Google Scholar]
  • 16.Yildiz I, Shukla S, Steinmetz N F. Applications of viral nanoparticles in medicine. Curr. Opin. Biotechnol. 2011;22:901–908. doi: 10.1016/j.copbio.2011.04.020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Pokorski J K, Steinmetz N F. The art of engineering viral nanoparticles. Mol. Pharm. 2011;8:29–43. doi: 10.1021/mp100225y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Li F, Wang Q. Fabrication of nanoarchitectures templated by virus-based nanoparticles: strategies and applications. Small. 2014;10:230–245. doi: 10.1002/smll.201301393. [DOI] [PubMed] [Google Scholar]
  • 19.Sherman M B, Guenther R H, Tama F, Sit T L, Brooks C L, Mikhailov A M, Orlova E V, Baker T S, Lommel S A. Removal of divalent cations induces structural transitions in red clover necrotic mosaic virus, revealing a potential mechanism for RNA release. J. Virol. 2006;80:10395–10406. doi: 10.1128/JVI.01137-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Kwak M, Minten I J, Anaya D M, Musser A J, Brasch M, Nolte R J M, Müllen K, Cornelissen J J L M, Herrmann A. Virus-like particles templated by DNA micelles: a general method for loading virus nanocarriers. J. Am. Chem. Soc. 2010;132:7834–7835. doi: 10.1021/ja101444j. [DOI] [PubMed] [Google Scholar]
  • 21.Dixit S K, Goicochea N L, Daniel M C, Murali A, Bronstein L, De M, Stein B, Rotello V M, Kao C C, Dragnea B. Quantum dot encapsulation in viral capsids. Nano Lett. 2006;6:1993–1999. doi: 10.1021/nl061165u. [DOI] [PubMed] [Google Scholar]
  • 22.Raja K S, Wang Q, Gonzalez M J, Manchester M, Johnson J E, Finn M G. Hybrid virus-polymer materials. 1. Synthesis and properties of PEG-decorated cowpea mosaic virus. Biomacromolecules. 2003;4:472–476. doi: 10.1021/bm025740+. [DOI] [PubMed] [Google Scholar]
  • 23.Chen Z, Li N, Chen L, Lee J, Gassensmith J J. Dual functionalized bacteriophage Qβ as a photocaged drug carrier. Small. 2016;12:4563–4571. doi: 10.1002/smll.201601053. [DOI] [PubMed] [Google Scholar]
  • 24.Lu Y, Madu C O. Viral-based gene delivery and regulated gene expression for targeted cancer therapy. Expert Opin. Drug Deliv. 2010;7:19–35. doi: 10.1517/17425240903419608. [DOI] [PubMed] [Google Scholar]
  • 25.Jin S, Ye K. Nanoparticle-mediated drug delivery and gene therapy. Biotechnol. Prog. 2007;23:32–41. doi: 10.1021/bp060348j. [DOI] [PubMed] [Google Scholar]
  • 26.Liu T C, Kirn D. Gene therapy progress and prospects cancer: oncolytic viruses. Gene Ther. 2008;15:877–884. doi: 10.1038/gt.2008.72. [DOI] [PubMed] [Google Scholar]
  • 27.Elzoghby A O, Samy W M, Elgindy N A. Protein-based nanocarriers as promising drug and gene delivery systems. J. Control. Release. 2012;161:38–49. doi: 10.1016/j.jconrel.2012.04.036. [DOI] [PubMed] [Google Scholar]
  • 28.Ng B C H. Ph.D. Thesis. LA, USA: University of California; 2010. Encapsulation of synthetic materials in biological self-assembled systems. [Google Scholar]
  • 29.Shen L, Bao N, Zhou Z, Prevelige P E, Gupta A. Materials design using genetically engineered proteins. J. Mater. Chem. 2011;21:18868–18876. doi: 10.1039/c1jm12238j. [DOI] [Google Scholar]
  • 30.Liu Z, Qiao J, Niu Z, Wang Q. Natural supramolecular building blocks: from virus coat proteins to viral nanoparticles. Chem. Soc. Rev. 2012;41:6178–6194. doi: 10.1039/c2cs35108k. [DOI] [PubMed] [Google Scholar]
  • 31.Zlotnick A, Stray S J. How does your virus grow? Understanding and interfering with virus assembly. Trends Biotechnol. 2003;21:536–542. doi: 10.1016/j.tibtech.2003.09.012. [DOI] [PubMed] [Google Scholar]
  • 32.Bancroft J B, Hiebert E, Bracker C E. The effects of various polyanions on shell formation of some spherical viruses. Virology. 1969;39:924–930. doi: 10.1016/0042-6822(69)90029-4. [DOI] [PubMed] [Google Scholar]
  • 33.Hu Y, Zandi R, Anavitarte A, Knobler C M, Gelbart W M. Packaging of a polymer by a viral capsid: the interplay between polymer length and capsid size. Biophys. J. 2008;94:1428–1436. doi: 10.1529/biophysj.107.117473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Douglas T, Young M. Host-guest encapsulation of materials by assembled virus protein cages. Nature. 1998;393:152–155. doi: 10.1038/30211. [DOI] [Google Scholar]
  • 35.Comellas-Aragonès M, Engelkamp H, Claessen V I, Sommerdijk N A J M, Rowan A E, Christianen P C M, Maan J C, Verduin B J M, Cornelissen J J L M, Nolte R J. A virus-based single-enzyme nanoreactor. Nat. Nanotechnol. 2007;2:635–639. doi: 10.1038/nnano.2007.299. [DOI] [PubMed] [Google Scholar]
  • 36.Wu Y, Yang H, Shin H J. Encapsulation and crystallization of Prussian blue nanoparticles by cowpea chlorotic mottle virus capsids. Biotechnol. Lett. 2014;36:515–521. doi: 10.1007/s10529-013-1399-8. [DOI] [PubMed] [Google Scholar]
  • 37.Speir J A, Munshi S, Wang G, Baker T S, Johnson J E. Structures of the native and swollen forms of cowpea chlorotic mottle virus determined by X-ray crystallography and cryo-electron microscopy. Structure. 1995;3:63–78. doi: 10.1016/S0969-2126(01)00135-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Douglas T, Strable E, Willits D, Aitouchen A, Libera M, Young M. Protein engineering of a viral cage for constrained nanomaterials synthesis. Adv. Mater. 2002;14:415–418. doi: 10.1002/1521-4095(20020318)14:6<415::AID-ADMA415>3.0.CO;2-W. [DOI] [Google Scholar]
  • 39.Brasch M, de la Escosura A, Ma Y, Uetrecht C, Heck A J R, Torres T, Cornelissen J J L M. Encapsulation of phthalocyanine supramolecular stacks into virus-like particles. J. Am. Chem. Soc. 2011;133:6878–6881. doi: 10.1021/ja110752u. [DOI] [PubMed] [Google Scholar]
  • 40.Zhang Y, Dong Y, Zhou J, Li X, Wang F. Application of plant viruses as a biotemplate for nanomaterial fabrication. Molecules. 2018;23:2311. doi: 10.3390/molecules23092311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Tama F, Brooks C L., 3rd The mechanism and pathway of pH induced swelling in cowpea chlorotic mottle virus. J. Mol. Biol. 2002;318:733–747. doi: 10.1016/S0022-2836(02)00135-3. [DOI] [PubMed] [Google Scholar]
  • 42.Lockney D M, Guenther R N, Loo L, Overton W, Antonelli R, Clark J, Hu M, Luft C, Lommel S A, Franzen S. The red clover necrotic mosaic virus capsid as a multifunctional cell targeting plant viral nanoparticle. Bioconjug. Chem. 2011;22:67–73. doi: 10.1021/bc100361z. [DOI] [PubMed] [Google Scholar]
  • 43.Huang Y, Chiang C Y, Lee S K, Gao Y, Hu E L, De Yoreo J, Belcher A M. Programmable assembly of nanoarchitectures using genetically engineered viruses. Nano Lett. 2005;5:1429–1434. doi: 10.1021/nl050795d. [DOI] [PubMed] [Google Scholar]
  • 44.Aniagyei S E, DuFort C, Kao C C, Dragnea B. Self-assembly approaches to nanomaterial encapsulation in viral protein cages. J. Mater. Chem. 2008;18:3763–3774. doi: 10.1039/b805874c. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Zhao Q, Chen W, Chen Y, Zhang L, Zhang J, Zhang Z. Self-assembled virus-like particles from rotavirus structural protein VP6 for targeted drug delivery. Bioconjug. Chem. 2011;22:346–352. doi: 10.1021/bc1002532. [DOI] [PubMed] [Google Scholar]
  • 46.Fiedler J D, Fishman M R, Brown S D, Lau J, Finn M G. Multifunctional enzyme packaging and catalysis in the Qβ protein nanoparticle. Biomacromolecules. 2018;19:3945–3957. doi: 10.1021/acs.biomac.8b00885. [DOI] [PubMed] [Google Scholar]
  • 47.Wu Y, Yang H, Shin H J. Viruses as self-assembled nanocontainers for encapsulation of functional cargoes. Korean J. Chem. Eng. 2013;30:1359–1367. doi: 10.1007/s11814-013-0083-y. [DOI] [Google Scholar]
  • 48.Balke I, Zeltins A. Use of plant viruses and viruslike particles for the creation of novel vaccines. Adv. Drug Deliv. Rev. 2019;145:119–129. doi: 10.1016/j.addr.2018.08.007. [DOI] [PubMed] [Google Scholar]
  • 49.Minten I J, Hendriks L J A, Nolte R J M, Cornelissen J J L M. Controlled encapsulation of multiple proteins in virus capsids. J. Am. Chem. Soc. 2009;131:17771–17773. doi: 10.1021/ja907843s. [DOI] [PubMed] [Google Scholar]
  • 50.Sharma J, Uchida M, Miettinen H M, Douglas T. Modular interior loading and exterior decoration of a virus-like particle. Nanoscale. 2017;9:10420–10430. doi: 10.1039/C7NR03018E. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Francis M B, Carrico I S. New frontiers in protein bioconjugation. Curr. Opin. Chem. Biol. 2010;14:771–773. doi: 10.1016/j.cbpa.2010.11.006. [DOI] [PubMed] [Google Scholar]
  • 52.Lee L A, Niu Z, Wang Q. Viruses and virus-like protein assemblies-chemically programmable nanoscale building blocks. Nano Res. 2009;2:349–364. doi: 10.1007/s12274-009-9033-8. [DOI] [Google Scholar]
  • 53.Smith M T, Hawes A K, Bundy B C. Reengineering viruses and virus-like particles through chemical functionalization strategies. Curr. Opin. Biotechnol. 2013;24:620–626. doi: 10.1016/j.copbio.2013.01.011. [DOI] [PubMed] [Google Scholar]
  • 54.Abello N, Kerstjens H A M, Postma D S, Bischoff R. Selective acylation of primary amines in peptides and proteins. J. Proteome Res. 2007;6:4770–4776. doi: 10.1021/pr070154e. [DOI] [PubMed] [Google Scholar]
  • 55.Wang Q, Kaltgrad E, Lin T, Johnson J E, Finn M G. Natural supramolecular building blocks: Wild-type cowpea mosaic virus. Chem. Biol. 2002;9:805–811. doi: 10.1016/S1074-5521(02)00165-5. [DOI] [PubMed] [Google Scholar]
  • 56.Strable E, Finn M G. Chemical modification of viruses and virus-like particles. Curr. Top Microbiol. Immunol. 2009;327:1–21. doi: 10.1007/978-3-540-69379-6_1. [DOI] [PubMed] [Google Scholar]
  • 57.Rostovtsev V V, Green L G, Fokin V V, Sharpless K B. A stepwise huisgen cycloaddition process: copper(I)-catalyzed regioselective “ligation” of azides and terminal alkynes. Angew. Chem. Int. Ed. Engl. 2002;41:2596–2599. doi: 10.1002/1521-3773(20020715)41:14<2596::AID-ANIE2596>3.0.CO;2-4. [DOI] [PubMed] [Google Scholar]
  • 58.Gupta S S, Kuzelka J, Singh P, Lewis W G, Manchester M, Finn M G. Accelerated bioorthogonal conjugation: A practical method for the ligation of diverse functional molecules to a polyvalent virus scaffold. Bioconjug. Chem. 2005;16:1572–1579. doi: 10.1021/bc050147l. [DOI] [PubMed] [Google Scholar]
  • 59.Hong V, Presolski S I, Ma C, Finn M G. Analysis and optimization of copper-catalyzed azide-alkyne cycloaddition for bioconjugation. Angew. Chem. Int. Ed. Engl. 2009;48:9879–9883. doi: 10.1002/anie.200905087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Wang Q, Chan T R, Hilgraf R, Fokin V V, Sharpless K B, Finn M G. Bioconjugation by copper(I)-catalyzed azide-alkyne [3 + 2] cycloaddition. J. Am. Chem. Soc. 2003;125:3192–3193. doi: 10.1021/ja021381e. [DOI] [PubMed] [Google Scholar]
  • 61.Destito G, Yeh R, Rae C S, Finn M G, Manchester M. Folic acid-mediated targeting of cowpea mosaic virus particles to tumor cells. Chem. Biol. 2007;14:1152–1162. doi: 10.1016/j.chembiol.2007.08.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Wu Y, Yang H, Jeon Y J, Lee M Y, Li J, Shin H J. Surface modification of cowpea chlorotic mottle virus capsids via a copper(I)-catalyzed azide-alkyne cycloaddition (CuAAC) reaction and their adhesion behavior with HeLa cells. Biotechnol. Bioprocess Eng. 2014;19:747–753. doi: 10.1007/s12257-014-0145-y. [DOI] [Google Scholar]
  • 63.Dirksen A, Dawson P E. Rapid oxime and hydrazone ligations with aromatic aldehydes for biomolecular labeling. Bioconjug. Chem. 2008;19:2543–2548. doi: 10.1021/bc800310p. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Brunel F M, Lewis J D, Destito G, Steinmetz N F, Manchester M, Stuhlmann H, Dawson P E. Hydrazone ligation strategy to assemble multifunctional viral nanoparticles for cell imaging and tumor targeting. Nano Lett. 2010;10:1093–1097. doi: 10.1021/nl1002526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Mateu M G. Virus engineering: functionalization and stabilization. Protein Eng. Des. Sel. 2011;24:53–63. doi: 10.1093/protein/gzq069. [DOI] [PubMed] [Google Scholar]
  • 66.Ruoslahti E. Peptides as targeting elements and tissue penetration devices for nanoparticles. Adv. Mater. 2012;24:3747–3756. doi: 10.1002/adma.201200454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 67.Wen A M, Rambhia P H, French R H, Steinmetz N F. Design rules for nanomedical engineering: from physical virology to the applications of virus-based materials in medicine. J. Biol. Phys. 2013;39:301–325. doi: 10.1007/s10867-013-9314-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 68.Mohanty C, Das M, Kanwar J R, Sahoo S K. Receptor mediated tumor targeting: an emerging approach for cancer therapy. Curr. Drug Deliv. 2011;8:45–58. doi: 10.2174/156720111793663606. [DOI] [PubMed] [Google Scholar]
  • 69.Lund P E, Hunt R C, Gottesman M M, Kimchi-Sarfaty C. Pseudovirions as vehicles for the delivery of siRNA. Pharm. Res. 2010;27:400–420. doi: 10.1007/s11095-009-0012-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 70.Giacca M, Zacchigna S. Virus-mediated gene delivery for human gene therapy. J. Control. Release. 2012;161:377–388. doi: 10.1016/j.jconrel.2012.04.008. [DOI] [PubMed] [Google Scholar]
  • 71.Chiocca E A, Rabkin S D. Oncolytic viruses and their application to cancer immunotherapy. Cancer Immunol. Res. 2014;2:295–300. doi: 10.1158/2326-6066.CIR-14-0015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Breyer B, Jiang W, Cheng H, Zhou L, Paul R, Feng T, He T C. Adenoviral vector-mediated gene transfer for human gene therapy. Curr. Gene Ther. 2001;1:149–162. doi: 10.2174/1566523013348689. [DOI] [PubMed] [Google Scholar]
  • 73.Fueyo J, Alemany R, Gomez-Manzano C, Fuller G N, Khan A, Conrad C A, Liu T J, Jiang H, Lemoine M G, Suzuki K, Sawaya R, Curiel D T, Yung W K A, Lang F F. Preclinical characterization of the antiglioma activity of a tropism-enhanced adenovirus targeted to the retinoblastoma pathway. J. Natl. Cancer Inst. 2003;95:652–660. doi: 10.1093/jnci/95.9.652. [DOI] [PubMed] [Google Scholar]
  • 74.Lang F F, Conrad C, Gomez-Manzano C, Yung W K A, Sawaya R, Weinberg J S, Prabhu S S, Rao G, Fuller G N, Aldape K D, Gumin J, Vence L M, Wistuba I, Rodriguez-Canales J, Villalobos P A, Dirven C M F, Tejada S, Valle R D, Alonso M M, Ewald B, Peterkin J J, Tufaro F, Fueyo J. Phase I study of DNX-2401 (Delta-24-RGD) oncolytic adenovirus: replication and immunotherapeutic effects in recurrent malignant glioma. J. Clin. Oncol. 2018;36:1419–1427. doi: 10.1200/JCO.2017.75.8219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 75.Schmid M, Ernst P, Honegger A, Suomalainen M, Zimmermann M, Braun L, Stauffer S, Thom C, Dreier B, Eibauer M, Kipar A, Vogel V, Greber U F, Medalia O, Plückthun A. Adenoviral vector with shield and adapter increases tumor specificity and escapes liver and immune control. Nat. Commun. 2018;9:450. doi: 10.1038/s41467-017-02707-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Ma G, Shimada H, Hiroshima K, Tada Y, Suzuki N, Tagawa M. Gene medicine for cancer treatment: commercially available medicine and accumulated clinical data in China. Drug Des. Devel. Ther. 2009;2:115–122. doi: 10.2147/dddt.s3535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77.Sanchala D S, Bhatt L K, Prabhavalkar K S. Oncolytic herpes simplex viral therapy: a stride toward selective targeting of cancer cells. Front. Pharmacol. 2017;8:270. doi: 10.3389/fphar.2017.00270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 78.Todo T, Martuza R L, Rabkin S D, Johnson P A. Oncolytic herpes simplex virus vector with enhanced MHC class I presentation and tumor cell killing. Proc. Natl. Acad. Sci. U S A. 2001;98:6396–6401. doi: 10.1073/pnas.101136398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79.Passer B J, Cheema T, Zhou B, Wakimoto H, Zaupa C, Razmjoo M, Sarte J, Wu S, Wu C, Noah J W, Li Q, Buolamwini J K, Yen Y, Rabkin S D, Martuza R L. Identification of the ENT1 antagonists dipyridamole and dilazep as amplifiers of oncolytic herpes simplex virus-1 replication. Cancer Res. 2010;70:3890–3895. doi: 10.1158/0008-5472.CAN-10-0155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80.Thomas E D, Meza-Perez S, Bevis K S, Randall T D, Gillespie G Y, Langford C, Alvarez R D. IL-12 Expressing oncolytic herpes simplex virus promotes anti-tumor activity and immunologic control of metastatic ovarian cancer in mice. J. Ovarian Res. 2016;9:70. doi: 10.1186/s13048-016-0282-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.Pol J, Kroemer G, Galluzzi L. First oncolytic virus approved for melanoma immunotherapy. Oncoimmunology. 2016;5:e1115641. doi: 10.1080/2162402X.2015.1115641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 82.Kelly E, Russell S J. History of oncolytic viruses: genesis to genetic engineering. Mol. Ther. 2007;15:651–659. doi: 10.1038/sj.mt.6300108. [DOI] [PubMed] [Google Scholar]
  • 83.Haralambieva I, Iankov I, Hasegawa K, Harvey M, Russell S J, Peng K W. Engineering oncolytic measles virus to circumvent the intracellular innate immune response. Mol. Ther. 2007;15:588–597. doi: 10.1038/sj.mt.6300076. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 84.Allen C, Opyrchal M, Aderca I, Schroeder M A, Sarkaria J N, Domingo E, Federspiel M J, Galanis E. Oncolytic measles virus strains have significant antitumor activity against glioma stem cells. Gene Ther. 2013;20:444–449. doi: 10.1038/gt.2012.62. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 85.Dispenzieri A, Tong C, LaPlant B, Lacy M Q, Laumann K, Dingli D, Zhou Y, Federspiel M J, Gertz M A, Hayman S, Buadi F, O’Connor M, Lowe V J, Peng K W, Russell S J. Phase I trial of systemic administration of Edmonston strain of measles virus genetically engineered to express the sodium iodide symporter in patients with recurrent or refractory multiple myeloma. Leukemia. 2017;31:2791–2798. doi: 10.1038/leu.2017.120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 86.Biabanikhankahdani R, Alitheen N B M, Ho K L, Tan W S. pH-responsive virus-like nanoparticles with enhanced tumour-targeting ligands for cancer drug delivery. Sci. Rep. 2016;6:37891. doi: 10.1038/srep37891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 87.Deniger D C, Kolokoltsov A A, Moore A C, Albrecht T B, Davey R A. Targeting and penetration of virus receptor bearing cells by nanoparticles coated with envelope proteins of Moloney murine leukemia virus. Nano Lett. 2006;6:2414–2421. doi: 10.1021/nl061180z. [DOI] [PubMed] [Google Scholar]
  • 88.Russell S J, Peng K W, Bell J C. Oncolytic virotherapy. Nat. Biotechnol. 2012;30:658–670. doi: 10.1038/nbt.2287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 89.Kaiser C R, Flenniken M L, Gillitzer E, Harmsen A L, Harmsen A G, Jutila M A, Douglas T, Young M J. Biodistribution studies of protein cage nanoparticles demonstrate broad tissue distribution and rapid clearance in vivo. Int. J. Nanomed. 2007;2:715–733. [PMC free article] [PubMed] [Google Scholar]
  • 90.Le D H T, Méndez-López E, Wang C, Commandeur U, randa M A, Steinmetz N F. Biodistribution of filamentous plant virus nanoparticles: pepino mosaic virus versus potato virus X. Biomacromolecules. 2018;20:469–477. doi: 10.1021/acs.biomac.8b01365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 91.Beatty P H, Lewis J D. 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. [DOI] [PubMed] [Google Scholar]
  • 92.Lam P, Lin R D, Steinmetz N F. Delivery of mitoxantrone using a plant virus-based nanoparticle for the treatment of glioblastomas. J. Mater. Chem. B. 2018;6:5888–5895. doi: 10.1039/C8TB01191E. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 93.Shukla S, Jandzinski M, Wang C, Gong X, Bonk K W, Keri R A, Steinmetz N F. A viral nanoparticle cancer vaccine delays tumor progression and prolongs survival in a HER2+ tumor mouse model. Adv. Ther. 2019;2:1800139. doi: 10.1002/adtp.201800139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 94.Culver J N, Brown A D, Zang F, Gnerlich M, Gerasopoulos K, Ghodssi R. Plant virus directed fabrication of nanoscale materials and devices. Virology. 2015;479–480:200–212. doi: 10.1016/j.virol.2015.03.008. [DOI] [PubMed] [Google Scholar]
  • 95.Barwal I, Kumar R, Kateriya S, Dinda A K, Yadav S C. Targeted delivery system for cancer cells consist of multiple ligands conjugated genetically modified CCMV capsid on doxorubicin GNPs complex. Sci. Rep. 2016;6:37096. doi: 10.1038/srep37096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 96.Wu Y, Li J, Yang H, Seoung J, Lim H D, Kim G J, Shin H J. Targeted cowpea chlorotic mottle virus-based nanoparticles with tumor-homing peptide F3 for photothermal therapy. Biotechnol. Bioprocess Eng. 2017;22:700–708. doi: 10.1007/s12257-017-0443-2. [DOI] [Google Scholar]
  • 97.Shimizu T, Ding W, Kameta N. Soft-matter nanotubes: A platform for diverse functions and applications. Chem. Rev. 2020;120:2347–2407. doi: 10.1021/acs.chemrev.9b00509. [DOI] [PubMed] [Google Scholar]
  • 98.Vernekar G B, Czapar A E, Veliz F A, Wang D I, Steinmetz N F, Lippard S J. Speciation of phenanthriplatin and its analogs in the core of tobacco mosaic virus. J. Am. Chem. Soc. 2018;140:4279–4287. doi: 10.1021/jacs.7b12697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 99.Franke C E, Czapar A E, Patel R B, Steinmetz N F. Tobacco mosaic virus-delivered cisplatin restores efficacy in platinum-resistant ovarian cancer cells. Mol. Pharm. 2018;15:2922–2931. doi: 10.1021/acs.molpharmaceut.7b00466. [DOI] [PubMed] [Google Scholar]
  • 100.Chariou P L, Lee K L, Wen A M, Gulati N M, Stewart P L, Steinmetz N F. Detection and imaging of aggressive cancer cells using an epidermal growth factor receptor (EGFR)-targeted filamentous plant virus-based nanoparticle. Bioconjugate Chem. 2015;26:262–269. doi: 10.1021/bc500545z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 101.Esfandiari N, Arzanani M K, Soleimani M, Kohi-Habibi M, Svendsen W E. A new application of plant virus nanoparticles as drug delivery in breast cancer. Tumor Biol. 2016;37:1229–1236. doi: 10.1007/s13277-015-3867-3. [DOI] [PubMed] [Google Scholar]
  • 102.Ashley C E, Carnes E C, Phillips G K, Durfee P N, Buley M D, Lino C A, Padilla D P, Phillips B, Carter M B, Willman C L, Brinker C J, do Carmo Caldeira J, Chackerian B, Wharton W, Peabody D S. Cell-specific delivery of diverse cargos by bacteriophage MS2 virus-like particles. ACS Nano. 2011;5:5729–5745. doi: 10.1021/nn201397z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 103.Kolesanova E F, Melnikova M V, Bolshakova T N, Rybalkina E Y, Sivov I G. Bacteriophage MS2 as a tool for targeted delivery in solid tumor chemotherapy. Acta Naturae. 2019;11:98–101. doi: 10.32607/20758251-2019-11-2-98-101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 104.Rhee J K, Hovlid M, Fiedler J D, Brown S D, Manzenrieder F, Kitagishi H, Nycholat C, Paulson J C, Finn M G. Colorful virus-like particles: fluorescent protein packaging by the Qβ capsid. Biomacromolecules. 2011;12:3977–3981. doi: 10.1021/bm200983k. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 105.Uchida M, Klem M T, Allen M, Suci P, Flenniken M, Gillitzer E, Varpness Z, Liepold L O, Young M, Douglas T. Biological containers: protein cages as multifunctional nanoplatforms. Adv. Mater. 2007;19:1025–1042. doi: 10.1002/adma.200601168. [DOI] [Google Scholar]
  • 106.Flenniken M L, Willits D A, Harmsen A L, Liepold L O, Harmsen A G, Young M J, Douglas T. Melanoma and lymphocyte cell-specific targeting incorporated into a heat shock protein cage architecture. Chem. Biol. 2006;13:161–170. doi: 10.1016/j.chembiol.2005.11.007. [DOI] [PubMed] [Google Scholar]
  • 107.Flenniken M L, Liepold L O, Crowley B E, Willits D A, Young M J, Douglas T. Selective attachment and release of a chemotherapeutic agent from the interior of a protein cage architecture. Chem. Commun. 2005;4:447–449. doi: 10.1039/b413435d. [DOI] [PubMed] [Google Scholar]
  • 108.Wang Z, Li C, Ellenburg M, Soistman E, Ruble J, Wright B, Ho J X, Carter D C. Structure of human ferritin L chain. Acta Crystallogr. D Biol. Crystallogr. 2006;62:800–806. doi: 10.1107/S0907444906018294. [DOI] [PubMed] [Google Scholar]
  • 109.Kanekiyo M, Bu W, Joyce M G, Meng G, Whittle J R R, Baxa U, Yamamoto T, Narpala S, Todd J P, Rao S S, McDermott A B, Koup R A, Rossmann M G, Mascola J R, Graham B S, Cohen J I, Nabel G J. Rational design of an Epstein-Barr virus vaccine targeting the receptor-binding site. Cell. 2015;162:1090–1100. doi: 10.1016/j.cell.2015.07.043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 110.Ghosh S, Mohapatra S, Thomas A, Bhunia D, Saha A, Das G, Jana B, Ghosh S. Apoferritin nanocage delivers combination of microtubule and nucleus targeting anticancer drugs. ACS Appl. Mater. Interfaces. 2016;8:30824–30832. doi: 10.1021/acsami.6b11798. [DOI] [PubMed] [Google Scholar]
  • 111.Huang Y, Luo Y, Zheng W, Chen T. Rational design of cancer-targeted BSA protein nanoparticles as radiosensitizer to overcome cancer radioresistance. ACS Appl. Mater. Interfaces. 2014;6:19217–19228. doi: 10.1021/am505246w. [DOI] [PubMed] [Google Scholar]
  • 112.Moon H, Lee J, Min J, Kang S. Developing genetically engineered encapsulin protein cage nanoparticles as a targeted delivery nanoplatform. Biomacromolecules. 2014;15:3794–3801. doi: 10.1021/bm501066m. [DOI] [PubMed] [Google Scholar]
  • 113.Ren D, Kratz F, Wang S W. Engineered drug-protein nanoparticle complexes for folate receptor targeting. Biochem. Eng. J. 2013;89:33–41. doi: 10.1016/j.bej.2013.09.008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 114.Barreto J A, O’Malley W, Kubeil M, Graham B, Stephan H, Spiccia L. Nanomaterials: applications in cancer imaging and therapy. Adv. Mater. 2011;23:H18–H40. doi: 10.1002/adma.201100140. [DOI] [PubMed] [Google Scholar]
  • 115.Park K, Lee S, Kang E, Kim K, Choi K, Kwon I C. New generation of multifunctional nanoparticles for cancer imaging and therapy. Adv. Funct. Mater. 2009;19:1553–1566. doi: 10.1002/adfm.200801655. [DOI] [Google Scholar]
  • 116.Choi K Y, Liu G, Lee S, Chen X. Theranostic nanoplatforms for simultaneous cancer imaging and therapy: current approaches and future perspectives. Nanoscale. 2012;4:330–342. doi: 10.1039/C1NR11277E. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 117.Yu M K, Park J, Jon S. Targeting strategies for multifunctional nanoparticles in cancer imaging and therapy. Theranostics. 2012;2:3–44. doi: 10.7150/thno.3463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 118.Datta A, Hooker J M, Botta M, Francis M B, Aime S, Raymond K N. High relaxivity gadolinium hydroxy-pyridonate-viral capsid conjugates: Nanosized MRI contrast agents. J. Am. Chem. Soc. 2008;130:2546–2552. doi: 10.1021/ja0765363. [DOI] [PubMed] [Google Scholar]
  • 119.Le D H T, Hu H, Commandeur U, Steinmetz N F. Chemical addressability of potato virus X for its applications in bio/nanotechnology. J. Struct. Biol. 2017;200:360–368. doi: 10.1016/j.jsb.2017.06.006. [DOI] [PubMed] [Google Scholar]
  • 120.Hu H, Zhang Y, Shukla S, Gu Y, Yu X, Steinmetz N F. Dysprosium-modified tobacco mosaic virus nanoparticles for ultra-high-field magnetic resonance and near-infrared fluorescence imaging of prostate cancer. ACS Nano. 2017;11:9249–9258. doi: 10.1021/acsnano.7b04472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 121.Hooker J M, O’Neil J P, Romanini D W, Taylor S E, Francis M B. Genome-free viral capsids as carriers for positron emission tomography radiolabels. Mol. Imaging Biol. 2008;10:182–191. doi: 10.1007/s11307-008-0136-5. [DOI] [PubMed] [Google Scholar]
  • 122.Lewis J D, Destito G, Zijlstra A, Gonzalez M J, Quigley J P, Manchester M, Stuhlmann H. Viral nanoparticles as tools for intravital vascular imaging. Nat. Med. 2006;12:354–360. doi: 10.1038/nm1368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 123.Woods N B, Bottero V, Schmidt M, von Kalle C, Verma I M. Gene therapy: therapeutic gene causing lymphoma. Nature. 2006;440:1123. doi: 10.1038/4401123a. [DOI] [PubMed] [Google Scholar]
  • 124.Wang Z, Liu G, Zheng H, Chen X. Rigid nanoparticle-based delivery of anti-cancer siRNA: challenges and opportunities. Biotechnol. Adv. 2014;32:831–843. doi: 10.1016/j.biotechadv.2013.08.020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 125.Maggio I, Holkers M, Liu J, Janssen J M, Chen X, Gonçalves M A. Adenoviral vector delivery of RNA-guided CRISPR/Cas9 nuclease complexes induces targeted mutagenesis in a diverse array of human cells. Sci. Rep. 2014;4:5105. doi: 10.1038/srep05105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 126.Li H, Sheng C, Liu H, Wang S, Zhao J, Yang L, Jia L, Li P, Wang L, Xie J, Xu D, Sun Y, Qiu S, Song H. Inhibition of HBV expression in HBV transgenic mice using AAV-delivered CRISPR-SaCas9. Front. Immunol. 2018;9:2080. doi: 10.3389/fimmu.2018.02080. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 127.Yin H, Song C Q, Dorkin J R, Zhu L J, Li Y, Wu Q, Park A, Yang J, Suresh S, Bizhanova A, Gupta A, Bolukbasi M F, Walsh S, Bogorad R L, Gao G, Weng Z, Dong Y, Koteliansky V, Wolfe S A, Langer R, Xue W, Anderson D G. Therapeutic genome editing by combined viral and non-viral delivery of CRISPR system components in vivo. Nat. Biotechnol. 2016;34:328–333. doi: 10.1038/nbt.3471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 128.Kay M A, Glorioso J C, Naldini L. Viral vectors for gene therapy: the art of turning infectious agents into vehicles of therapeutics. Nat. Med. 2001;7:33–40. doi: 10.1038/83324. [DOI] [PubMed] [Google Scholar]
  • 129.Burton E A, Glorioso J C. Herpes simplex virus vector-based gene therapy for malignant glioma. Gene Ther. Mol. Biol. 2000;5:131–145. [Google Scholar]
  • 130.Roehm P C, Shekarabi M, Wollebo H S, Bellizzi A, He L, Salkind J, Khalili K. Inhibition of HSV-1 replication by gene editing strategy. Sci. Rep. 2016;6:23146. doi: 10.1038/srep23146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 131.Lin C, Li H, Hao M, Xiong D, Luo Y, Huang C, Yuan Q, Zhang J, Xia N. Increasing the efficiency of CRISPR/ Cas9-mediated precise genome editing of HSV-1 virus in human cells. Sci. Rep. 2016;6:34531. doi: 10.1038/srep34531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 132.Allen T M, Cullis P R. Drug delivery systems: entering the mainstream. Science. 2004;303:1818–1822. doi: 10.1126/science.1095833. [DOI] [PubMed] [Google Scholar]
  • 133.Emerich D F, Thanos C G. The pinpoint promise of nanoparticle-based drug delivery and molecular diagnosis. Biomol. Eng. 2006;23:171–184. doi: 10.1016/j.bioeng.2006.05.026. [DOI] [PubMed] [Google Scholar]
  • 134.Jain A, Jain S K. PEGylation: an approach for drug delivery. A review. Crit. Rev. Ther. Drug Carrier Syst. 2008;25:403–447. doi: 10.1615/CritRevTherDrugCarrierSyst.v25.i5.10. [DOI] [PubMed] [Google Scholar]
  • 135.Steinmetz N F, Manchester M. PEGylated viral nanoparticles for biomedicine: the impact of PEG chain length on VNP cell interactions in vitro and ex vivo. Biomacromolecules. 2009;10:784–792. doi: 10.1021/bm8012742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 136.Steinmetz N F, Mertens M E, Taurog R E, Johnson J E, Commandeur U, Fischer R, Manchester M. Potato virus X as a novel platform for potential biomedical applications. Nano Lett. 2009;10:305–312. doi: 10.1021/nl9035753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 137.Bruckman M A, Kaur G, Lee L A, Xie F, Sepulveda J, Breitenkamp R, Zhang X, Joralemon M, Russell T P, Emrick T, Wang Q. Surface modification of tobacco mosaic virus with “click” chemistry. Chembiochem. 2008;9:519–523. doi: 10.1002/cbic.200700559. [DOI] [PubMed] [Google Scholar]
  • 138.Mikkila J, Eskelinen A P, Niemelä E H, Linko V, Frilander M J, Törmä P, Kostiainen M A. Virus-encapsulated DNA origami nanostructures for cellular delivery. Nano Lett. 2014;14:2196–2200. doi: 10.1021/nl500677j. [DOI] [PubMed] [Google Scholar]
  • 139.Lupia T, Scabini S, Pinna S M, Di Perri G, De Rosa F G, Corcione S. 2019 novel coronavirus (2019-nCoV) outbreak: A new challenge. J. Glob. Antimicrob. Resist. 2020;21:22–27. doi: 10.1016/j.jgar.2020.02.021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 140.Carter D C, Wright B, Jerome W G, Rose J P, Wilson E. A unique protein self-assembling nanoparticle with significant advantages in vaccine development and production. J. Nanomater. 2020;2020:4297937. doi: 10.1155/2020/4297937. [DOI] [Google Scholar]
  • 141.Mohsen M O, Speiser D E, Knuth A, Bachmann M F. Virus-like particles for vaccination against cancer. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2020;12:e1579. doi: 10.1002/wnan.1579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 142.Zhai L, Yadav R, Kunda N K, Anderson D, Bruckner E, Miller E K, Basu R, Muttil P, Tumban E. Oral immunization with bacteriophage MS2-L2 VLPs protects against oral and genital infection with multiple HPV types associated with head & neck cancers and cervical cancer. Antiviral Res. 2019;166:56–65. doi: 10.1016/j.antiviral.2019.03.012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 143.Speiser D E, Schwarz K, Baumgaertner P, Manolova V, Devevre E, Sterry W, Walden P, Zippelius A, Conzett K B, Senti G, Voelter V, Cerottini J P, Guggisberg D, Willers J, Geldhof C, Romero P, Kündig T, Knuth A, Dummer R, Trefzer U, Bachmann M F. Memory and effector CD8 T-cell responses after nanoparticle vaccination of melanoma patients. J. Immunother. 2010;33:848–858. doi: 10.1097/CJI.0b013e3181f1d614. [DOI] [PubMed] [Google Scholar]
  • 144.Cai H, Shukla S, Wang C, Masarapu H, Steinmetz N F. Heterologous prime-boost enhances the antitumor immune response elicited by plant-virus-based cancer vaccine. J. Am. Chem. Soc. 2019;141:6509–6518. doi: 10.1021/jacs.9b01523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 145.Gomes A C, Mohsen M, Bachmann M F. Harnessing nanoparticles for immunomodulation and vaccines. Vaccines. 2017;5:6. doi: 10.3390/vaccines5010006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 146.Schwarz B, Douglas T. Development of virus-like particles for diagnostic and prophylactic biomedical applications. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2015;7:722–735. doi: 10.1002/wnan.1336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 147.Mohsen M O, Gomes A C, Vogel M, Bachmann M F. Interaction of viral capsid-derived virus-like particles (VLPs) with the innate immune system. Vaccines. 2018;6:37. doi: 10.3390/vaccines6030037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 148.Chen D S, Wu Y Q, Zhang W, Jiang S J, Chen S Z. Horizontal gene transfer events reshape the global landscape of arm race between viruses and homo sapiens. Sci. Rep. 2016;6:26934. doi: 10.1038/srep26934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 149.Kotterman M A, Chalberg T W, Schaffer D V. Viral vectors for gene therapy: translational and clinical outlook. Annu. Rev. Biomed. Eng. 2015;17:63–89. doi: 10.1146/annurev-bioeng-071813-104938. [DOI] [PubMed] [Google Scholar]

Articles from Biotechnology and Bioprocess Engineering are provided here courtesy of Nature Publishing Group

RESOURCES