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Current Medical Imaging

Editor-in-Chief

ISSN (Print): 1573-4056
ISSN (Online): 1875-6603

Review Article

Innovative Applications of Plant Viruses in Drug Targeting and Molecular Imaging- A Review

Author(s): Alaa A.A. Aljabali*, Mazhar S. Al Zoubi, Khalid M. Al-Batayneh, Dinesh M. Pardhi, Kamal Dua, Kaushik Pal and Murtaza M. Tambuwala

Volume 17, Issue 4, 2021

Published on: 07 October, 2020

Page: [491 - 506] Pages: 16

DOI: 10.2174/1573405616666201007160243

Price: $65

Abstract

Background: Nature had already engineered various types of nanoparticles (NPs), especially viruses, which can deliver their cargo to the host/targeted cells. The ability to selectively target specific cells offers a significant advantage over the conventional approach. Numerous organic NPs, including native protein cages, virus-like particles, polymeric saccharides, and liposomes, have been used for the preparation of nanoparticles. Such nanomaterials have demonstrated better performance as well as improved biocompatibility, devoid of side effects, and stable without any deterioration.

Objective: This review discusses current clinical and scientific research on naturally occurring nanomaterials. It also illustrates and updates the tailor-made approaches for selective delivery and targeted medications that require a high-affinity interconnection to the targeted cells.

Methods: A comprehensive search was performed using keywords for viral nanoparticles, viral particles for drug delivery, viral nanoparticles for molecular imaging, theranostics applications of viral nanoparticles and plant viruses in nanomedicine. We searched on Google Scholar, PubMed, Springer, Medline, and Elsevier from 2000 till date and by the bibliographic review of all identified articles.

Results: The findings demonstrated that structures dependent on nanomaterials might have potential applications in diagnostics, cell marking, comparing agents (computed tomography and magnetic resonance imaging), and antimicrobial drugs, as well as drug delivery structures. However, measures should be taken in order to prevent or mitigate, in pharmaceutical or medical applications, the toxic impact or incompatibility of nanoparticle-based structures with biological systems.

Conclusion: The review provided an overview of the latest advances in nanotechnology, outlining the difficulties and the advantages of in vivo and in vitro structures that are focused on a specific subset of the natural nanomaterials.

Keywords: Viral nanoparticle, molecular imaging, drug targeting, pharmaceutical nanotechnology, drug delivery, bioconjugation.

Graphical Abstract
[1]
Brown R, Jacobs L, Peet R. Species Richness: Small Scale. New Jersey, NJ: eLS. John Wiley & Sons, Ltd 2001.
[2]
Kropinski AM. Phage therapy-everything old is new again. Can J Infect Dis Med Microbiol 2006; 17(5): 297-306.
[http://dx.doi.org/10.1155/2006/329465] [PMID: 18382643]
[3]
Merril CR, Scholl D, Adhya SL. The prospect for bacteriophage therapy in Western medicine. Nat Rev Drug Discov 2003; 2(6): 489-97.
[http://dx.doi.org/10.1038/nrd1111] [PMID: 12776223]
[4]
Méthot P-O. Writing the history of virology in the twentieth century: Discovery, disciplines, and conceptual change. Stud Hist Philos Biol Biomed Sci 2016; 59: 145-53.
[http://dx.doi.org/10.1016/j.shpsc.2016.02.011] [PMID: 27033340]
[5]
Nayerossadat N, Maedeh T, Ali PA. Viral and nonviral delivery systems for gene delivery. Adv Biomed Res 2012; 1: 27.
[http://dx.doi.org/10.4103/2277-9175.98152] [PMID: 23210086]
[6]
Liu Z, Qiao J, Niu Z, Wang Q. Natural supramolecular building blocks: from virus coat proteins to viral nanoparticles. Chem Soc Rev 2012; 41(18): 6178-94.
[http://dx.doi.org/10.1039/c2cs35108k] [PMID: 22880206]
[7]
Kaiser CR, Flenniken ML, Gillitzer E, et al. Biodistribution studies of protein cage nanoparticles demonstrate broad tissue distribution and rapid clearance in vivo. Int J Nanomedicine 2007; 2(4): 715-33.
[PMID: 18203438]
[8]
Flynn CE, Lee S-W, Peelle BR, Belcher AM. Viruses as vehicles for growth, organization and assembly of materials. Acta Mater 2003; 51(19): 5867-80.
[http://dx.doi.org/10.1016/j.actamat.2003.08.031]
[9]
Aljabali A. Viral nanoparticles: a drug delivery platform. J Pharm Toxicol 2018; 1(1): 1-2.
[10]
Sokullu E, Soleymani Abyaneh H, Gauthier MA. Plant/Bacterial Virus-Based Drug Discovery, Drug Delivery, and Therapeutics. Pharmaceutics 2019; 11(5): 211.
[http://dx.doi.org/10.3390/pharmaceutics11050211] [PMID: 31058814]
[11]
Narayanan KB, Han SS. Icosahedral plant viral nanoparticles - bioinspired synthesis of nanomaterials/nanostructures. Adv Colloid Interface Sci 2017; 248: 1-19.
[http://dx.doi.org/10.1016/j.cis.2017.08.005] [PMID: 28916111]
[12]
Dixit SK, Goicochea NL, Daniel M-C, et al. Quantum dot encapsulation in viral capsids. Nano Lett 2006; 6(9): 1993-9.
[http://dx.doi.org/10.1021/nl061165u] [PMID: 16968014]
[13]
Running WE, Ni P, Kao CC, Reilly JP. Chemical reactivity of brome mosaic virus capsid protein. J Mol Biol 2012; 423(1): 79-95.
[http://dx.doi.org/10.1016/j.jmb.2012.06.031] [PMID: 22750573]
[14]
Suci PA, Varpness Z, Gillitzer E, Douglas T, Young M. Targeting and photodynamic killing of a microbial pathogen using protein cage architectures functionalized with a photosensitizer. Langmuir 2007; 23(24): 12280-6.
[http://dx.doi.org/10.1021/la7021424] [PMID: 17949022]
[15]
Zlotnick A, Aldrich R, Johnson JM, Ceres P, Young MJ. Mechanism of capsid assembly for an icosahedral plant virus. Virology 2000; 277(2): 450-6.
[http://dx.doi.org/10.1006/viro.2000.0619] [PMID: 11080492]
[16]
Gillitzer E, Willits D, Young M, Douglas T. Chemical modification of a viral cage for multivalent presentation. Chem Commun (Camb) 2002; (20): 2390-1.
[http://dx.doi.org/10.1039/b207853h] [PMID: 12430455]
[17]
Huynh NT, Hesketh EL, Saxena P, et al. Crystal structure and proteomics analysis of empty virus-like particles of cowpea mosaic virus. Structure 2016; 24(4): 567-75.
[http://dx.doi.org/10.1016/j.str.2016.02.011] [PMID: 27021160]
[18]
Aljabali AA, Barclay JE, Butt JN, Lomonossoff GP, Evans DJ. Redox-active ferrocene-modified Cowpea mosaic virus nanoparticles. Dalton Trans 2010; 39(32): 7569-74.
[http://dx.doi.org/10.1039/c0dt00495b] [PMID: 20623052]
[19]
Wen AM, Shukla S, Saxena P, et al. Interior engineering of a viral nanoparticle and its tumor homing properties. Biomacromolecules 2012; 13(12): 3990-4001.
[http://dx.doi.org/10.1021/bm301278f] [PMID: 23121655]
[20]
Zeng Q, Wen H, Wen Q, et al. Cucumber mosaic virus as drug delivery vehicle for doxorubicin. Biomaterials 2013; 34(19): 4632-42.
[http://dx.doi.org/10.1016/j.biomaterials.2013.03.017] [PMID: 23528229]
[21]
Dreher TW. Turnip yellow mosaic virus: transfer RNA mimicry, chloroplasts and a C-rich genome. Mol Plant Pathol 2004; 5(5): 367-75.
[http://dx.doi.org/10.1111/j.1364-3703.2004.00236.x] [PMID: 20565613]
[22]
Finbloom JA, Han K, Aanei IL, et al. Stable disk assemblies of a tobacco mosaic virus mutant as nanoscale scaffolds for applications in drug delivery. Bioconjug Chem 2016; 27(10): 2480-5.
[http://dx.doi.org/10.1021/acs.bioconjchem.6b00424] [PMID: 27712069]
[23]
Bazzini AA, Hopp HE, Beachy RN, Asurmendi S. Infection and coaccumulation of tobacco mosaic virus proteins alter microRNA levels, correlating with symptom and plant development. Proc Natl Acad Sci USA 2007; 104(29): 12157-62.
[http://dx.doi.org/10.1073/pnas.0705114104] [PMID: 17615233]
[24]
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.
[http://dx.doi.org/10.1021/bc100361z] [PMID: 21126069]
[25]
Ren Y, Wong S-M, Lim L-Y. In vitro-reassembled plant virus-like particles for loading of polyacids. J Gen Virol 2006; 87(Pt 9): 2749-54.
[http://dx.doi.org/10.1099/vir.0.81944-0] [PMID: 16894216]
[26]
Barnhill HN, Reuther R, Ferguson PL, Dreher T, Wang Q. Turnip yellow mosaic virus as a chemoaddressable bionanoparticle. Bioconjug Chem 2007; 18(3): 852-9.
[http://dx.doi.org/10.1021/bc060391s] [PMID: 17428027]
[27]
Kwak M, Minten IJ, Anaya DM, et al. Virus-like particles templated by DNA micelles: a general method for loading virus nanocarriers. J Am Chem Soc 2010; 132(23): 7834-5.
[http://dx.doi.org/10.1021/ja101444j] [PMID: 20481536]
[28]
Saunders K, Sainsbury F, Lomonossoff GP. Efficient generation of cowpea mosaic virus empty virus-like particles by the proteolytic processing of precursors in insect cells and plants. Virology 2009; 393(2): 329-37.
[http://dx.doi.org/10.1016/j.virol.2009.08.023] [PMID: 19733890]
[29]
Aljabali AA, Sainsbury F, Lomonossoff GP, Evans DJ. Cowpea mosaic virus unmodified empty viruslike particles loaded with metal and metal oxide. Small 2010; 6(7): 818-21.
[http://dx.doi.org/10.1002/smll.200902135] [PMID: 20213652]
[30]
Li F, Wang Q. Fabrication of nanoarchitectures templated by virus-based nanoparticles: strategies and applications. Small 2014; 10(2): 230-45.
[http://dx.doi.org/10.1002/smll.201301393] [PMID: 23996911]
[31]
Bronstein LM. Virus-based nanoparticles with inorganic cargo: what does the future hold? Small 2011; 7(12): 1609-18.
[http://dx.doi.org/10.1002/smll.201001992] [PMID: 21520496]
[32]
Aljabali AA, Barclay JE, Lomonossoff GP, Evans DJ. Virus templated metallic nanoparticles. Nanoscale 2010; 2(12): 2596-600.
[http://dx.doi.org/10.1039/c0nr00525h] [PMID: 20877898]
[33]
Aljabali AA, Evans DJ. Polyelectrolyte-modified cowpea mosaic virus for the synthesis of gold nanoparticles. Methods Mol Biol 2014; 1108: 97-103.
[http://dx.doi.org/10.1007/978-1-62703-751-8_7] [PMID: 24243243]
[34]
Aljabali AA, Evans DJ. Templated mineralization by charge-modified cowpea mosaic virus. Methods Mol Biol 2014; 1108: 89-95.
[http://dx.doi.org/10.1007/978-1-62703-751-8_6] [PMID: 24243242]
[35]
Aljabali AA, Shah SN, Evans-Gowing R, Lomonossoff GP, Evans DJ. Chemically-coupled-peptide-promoted virus nanoparticle templated mineralization. Integr Biol 2011; 3(2): 119-25.
[http://dx.doi.org/10.1039/C0IB00056F] [PMID: 21031174]
[36]
Douglas T, Young M. Host–guest encapsulation of materials by assembled virus protein cages. Nature 1998; 393(6681): 152-5.
[http://dx.doi.org/10.1038/30211]
[37]
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(6): 415-8.
[http://dx.doi.org/10.1002/1521-4095(20020318)14:6<415::AID-ADMA415>3.0.CO;2-W]
[38]
Aljabali AA, Lomonossoff GP, Evans DJ. CPMV-polyelectrolyte-templated gold nanoparticles. Biomacromolecules 2011; 12(7): 2723-8.
[http://dx.doi.org/10.1021/bm200499v] [PMID: 21657200]
[39]
Aljabali AAA, Evans DJ. Internal Deposition of Cobalt Metal and Iron Oxide Within CPMV eVLPs. Methods Mol Biol 2018; 1776: 189-201.
[http://dx.doi.org/10.1007/978-1-4939-7808-3_12] [PMID: 29869242]
[40]
Tsukamoto R, Muraoka M, Seki M, Tabata H, Yamashita I. Synthesis of CoPt and FePt3 nanowires using the central channel of tobacco mosaic virus as a biotemplate. Chem Mater 2007; 19(10): 2389-91.
[http://dx.doi.org/10.1021/cm062187k]
[41]
Chen C, Daniel M-C, Quinkert ZT, et al. Nanoparticle-templated assembly of viral protein cages. Nano Lett 2006; 6(4): 611-5.
[http://dx.doi.org/10.1021/nl0600878] [PMID: 16608253]
[42]
Daniel M-C, Tsvetkova IB, Quinkert ZT, et al. Role of surface charge density in nanoparticle-templated assembly of bromovirus protein cages. ACS Nano 2010; 4(7): 3853-60.
[http://dx.doi.org/10.1021/nn1005073] [PMID: 20575505]
[43]
Kusters R, Lin H-K, Zandi R, Tsvetkova I, Dragnea B, van der Schoot P. Role of charge regulation and size polydispersity in nanoparticle encapsulation by viral coat proteins. J Phys Chem B 2015; 119(5): 1869-80.
[http://dx.doi.org/10.1021/jp5108125] [PMID: 25562399]
[44]
Twort F W. An investigation on the nature of ultra-microscopic viruses Acta Kravsi 1961.
[45]
Huh H, Wong S, St Jean J, Slavcev R. Bacteriophage interactions with mammalian tissue: Therapeutic applications. Adv Drug Deliv Rev 2019; 145: 4-17.
[http://dx.doi.org/10.1016/j.addr.2019.01.003] [PMID: 30659855]
[46]
Li K, Chen Y, Li S, et al. Chemical modification of M13 bacteriophage and its application in cancer cell imaging. Bioconjug Chem 2010; 21(7): 1369-77.
[http://dx.doi.org/10.1021/bc900405q] [PMID: 20499838]
[47]
Farkas ME, Aanei IL, Behrens CR, et al. PET Imaging and biodistribution of chemically modified bacteriophage MS2. Mol Pharm 2013; 10(1): 69-76.
[http://dx.doi.org/10.1021/mp3003754] [PMID: 23214968]
[48]
Anderson EA, Isaacman S, Peabody DS, Wang EY, Canary JW, Kirshenbaum K. Viral nanoparticles donning a paramagnetic coat: conjugation of MRI contrast agents to the MS2 capsid. Nano Lett 2006; 6(6): 1160-4.
[http://dx.doi.org/10.1021/nl060378g] [PMID: 16771573]
[49]
Liu Z, Pawliszyn J. Behaviors of the MS2 virus and related antibodies in capillary isoelectric focusing with whole-column imaging detection. Electrophoresis 2005; 26(3): 556-62.
[http://dx.doi.org/10.1002/elps.200410075] [PMID: 15690457]
[50]
Aanei IL, Francis MB. Dual surface modification of genome-free MS2 capsids for delivery applications. Methods Mol Biol 2018; 1776: 629-42.
[http://dx.doi.org/10.1007/978-1-4939-7808-3_40] [PMID: 29869270]
[51]
Meldrum T, Seim KL, Bajaj VS, et al. A xenon-based molecular sensor assembled on an MS2 viral capsid scaffold. J Am Chem Soc 2010; 132(17): 5936-7.
[http://dx.doi.org/10.1021/ja100319f] [PMID: 20392049]
[52]
Aanei IL, Glasgow JE, Capehart SL, Francis MB. Encapsulation of negatively charged cargo in MS2 viral capsids. Methods Mol Biol 2018; 1776: 303-17.
[http://dx.doi.org/10.1007/978-1-4939-7808-3_21] [PMID: 29869251]
[53]
Jeong K, Netirojjanakul C, Munch HK, et al. Targeted molecular imaging of cancer cells using MS2-based (129)Xe NMR. Bioconjug Chem 2016; 27(8): 1796-801.
[http://dx.doi.org/10.1021/acs.bioconjchem.6b00275] [PMID: 27454679]
[54]
Yacoby I, Bar H, Benhar I. Targeted drug-carrying bacteriophages as antibacterial nanomedicines. Antimicrob Agents Chemother 2007; 51(6): 2156-63.
[http://dx.doi.org/10.1128/AAC.00163-07] [PMID: 17404004]
[55]
Yacoby I, Shamis M, Bar H, Shabat D, Benhar I. Targeting antibacterial agents by using drug-carrying filamentous bacteriophages. Antimicrob Agents Chemother 2006; 50(6): 2087-97.
[http://dx.doi.org/10.1128/AAC.00169-06] [PMID: 16723570]
[56]
Zhang L-J, Xia L, Liu S-L, et al. A “driver switchover” mechanism of influenza virus transport from microfilaments to microtubules. ACS Nano 2018; 12(1): 474-84.
[http://dx.doi.org/10.1021/acsnano.7b06926] [PMID: 29232101]
[57]
Pan H, Li W j, Yao X j, et al. In situ bioorthogonal metabolic labeling for fluorescence imaging of virus infection in vivo. Small 2017; 13(17): 1604036.
[58]
Zhang P, Liu S, Gao D, et al. Click-functionalized compact quantum dots protected by multidentate-imidazole ligands: conjugation-ready nanotags for living-virus labeling and imaging. J Am Chem Soc 2012; 134(20): 8388-91.
[http://dx.doi.org/10.1021/ja302367s] [PMID: 22568447]
[59]
Ke X, Zhang Y, Zheng F, et al. SpyCatcher-SpyTag mediated in situ labelling of progeny baculovirus with quantum dots for tracking viral infection in living cells. Chem Commun (Camb) 2018; 54(10): 1189-92.
[http://dx.doi.org/10.1039/C7CC08880A] [PMID: 29334085]
[60]
Shu Y, Lu W, Liu S-L, et al. Site-specific labeling of baculovirus in an integrated microfluidic device. Lab Chip 2013; 13(5): 860-5.
[http://dx.doi.org/10.1039/c2lc41120b] [PMID: 23299251]
[61]
Carvalho SB, Freire JM, Moleirinho MG, et al. Bioorthogonal strategy for bioprocessing of specific-site-functionalized enveloped influenza-virus-like particles. Bioconjug Chem 2016; 27(10): 2386-99.
[http://dx.doi.org/10.1021/acs.bioconjchem.6b00372] [PMID: 27652605]
[62]
Finnefrock AC, Freed DC, Tang A, et al. Preclinical evaluations of peptide-conjugate vaccines targeting the antigenic domain-2 of glycoprotein B of human cytomegalovirus. Hum Vaccin Immunother 2016; 12(8): 2106-12.
[http://dx.doi.org/10.1080/21645515.2016.1164376] [PMID: 26986197]
[63]
Wang I-H, Suomalainen M, Andriasyan V, et al. Tracking viral genomes in host cells at single-molecule resolution. Cell Host Microbe 2013; 14(4): 468-80.
[http://dx.doi.org/10.1016/j.chom.2013.09.004] [PMID: 24139403]
[64]
Fischlechner M, Zschörnig O, Hofmann J, Donath E. Engineering virus functionalities on colloidal polyelectrolyte lipid composites. Angew Chem Int Ed Engl 2005; 44(19): 2892-5.
[http://dx.doi.org/10.1002/anie.200460763] [PMID: 15827976]
[65]
Joling P, Bakker LJ, Van Strijp JA, et al. Binding of human immunodeficiency virus type-1 to follicular dendritic cells in vitro is complement dependent. J Immunol 1993; 150(3): 1065-73.
[PMID: 8423332]
[66]
Li Q, Li W, Yin W, et al. Single-particle tracking of human immunodeficiency virus type 1 productive entry into human primary macrophages. ACS Nano 2017; 11(4): 3890-903.
[http://dx.doi.org/10.1021/acsnano.7b00275] [PMID: 28371581]
[67]
Pereira CF, Ellenberg PC, Jones KL, et al. Labeling of multiple HIV-1 proteins with the biarsenical-tetracysteine system. PLoS One 2011; 6(2): e17016.
[http://dx.doi.org/10.1371/journal.pone.0017016] [PMID: 21347302]
[68]
Parveen N, Borrenberghs D, Rocha S, Hendrix J. Single viruses on the fluorescence microscope: imaging molecular mobility, interactions and structure sheds new light on viral replication. Viruses 2018; 10(5): E250.
[http://dx.doi.org/10.3390/v10050250] [PMID: 29748498]
[69]
Francis AC, Melikyan GB. Live-cell imaging of early steps of single HIV-1 infection. Viruses 2018; 10(5): E275.
[http://dx.doi.org/10.3390/v10050275] [PMID: 29783762]
[70]
Okada T, Uto K, Sasai M, Lee CM, Ebara M, Aoyagi T. Nano-decoration of the Hemagglutinating Virus of Japan envelope (HVJ-E) using a layer-by-layer assembly technique. Langmuir 2013; 29(24): 7384-92.
[http://dx.doi.org/10.1021/la304572s] [PMID: 23441859]
[71]
Kang S-M, Yao Q, Guo L, Compans RW. Mucosal immunization with virus-like particles of simian immunodeficiency virus conjugated with cholera toxin subunit B. J Virol 2003; 77(18): 9823-30.
[http://dx.doi.org/10.1128/JVI.77.18.9823-9830.2003] [PMID: 12941891]
[72]
Ntziachristos V. Fluorescence molecular imaging. Annu Rev Biomed Eng 2006; 8: 1-33.
[http://dx.doi.org/10.1146/annurev.bioeng.8.061505.095831] [PMID: 16834550]
[73]
Li F, Zhang ZP, Peng J, et al. Imaging viral behavior in Mammalian cells with self-assembled capsid-quantum-dot hybrid particles. Small 2009; 5(6): 718-26.
[http://dx.doi.org/10.1002/smll.200801303] [PMID: 19242943]
[74]
Li C, Li F, Zhang Y, Zhang W, Zhang X-E, Wang Q. Real-time monitoring surface chemistry-dependent in vivo behaviors of protein nanocages via encapsulating an NIR-II Ag2S quantum dot. ACS Nano 2015; 9(12): 12255-63.
[http://dx.doi.org/10.1021/acsnano.5b05503] [PMID: 26496067]
[75]
Niehl A, Appaix F, Boscá S, et al. Fluorescent Tobacco mosaic virus-derived bio-nanoparticles for intravital two-photon imaging. Front Plant Sci 2016; 6: 1244.
[http://dx.doi.org/10.3389/fpls.2015.01244] [PMID: 26793221]
[76]
Huang X, Stein BD, Cheng H, et al. Magnetic virus-like nanoparticles in N. benthamiana plants: a new paradigm for environmental and agronomic biotechnological research. ACS Nano 2011; 5(5): 4037-45.
[http://dx.doi.org/10.1021/nn200629g] [PMID: 21452886]
[77]
Chen W, Cao Y, Liu M, et al. Rotavirus capsid surface protein VP4-coated Fe(3)O(4) nanoparticles as a theranostic platform for cellular imaging and drug delivery. Biomaterials 2012; 33(31): 7895-902.
[http://dx.doi.org/10.1016/j.biomaterials.2012.07.016] [PMID: 22841921]
[78]
Prasuhn DE Jr, Yeh RM, Obenaus A, Manchester M, Finn MG. Viral MRI contrast agents: coordination of Gd by native virions and attachment of Gd complexes by azide-alkyne cycloaddition. Chem Commun (Camb) 2007; (12): 1269-71.
[http://dx.doi.org/10.1039/B615084E] [PMID: 17356779]
[79]
Allen M, Bulte JW, Liepold L, et al. Paramagnetic viral nanoparticles as potential high-relaxivity magnetic resonance contrast agents. Magn Reson Med 2005; 54(4): 807-12.
[http://dx.doi.org/10.1002/mrm.20614] [PMID: 16155869]
[80]
Basu G, Allen M, Willits D, Young M, Douglas T. Metal binding to cowpea chlorotic mottle virus using terbium(III) fluorescence. J Biol Inorg Chem 2003; 8(7): 721-5.
[http://dx.doi.org/10.1007/s00775-003-0470-7] [PMID: 14505076]
[81]
Liepold L, Anderson S, Willits D, et al. Viral capsids as MRI contrast agents. Magn Reson Med 2007; 58(5): 871-9.
[http://dx.doi.org/10.1002/mrm.21307] [PMID: 17969126]
[82]
Pokorski JK, Breitenkamp K, Liepold LO, Qazi S, Finn MG. Functional virus-based polymer-protein nanoparticles by atom transfer radical polymerization. J Am Chem Soc 2011; 133(24): 9242-5.
[http://dx.doi.org/10.1021/ja203286n] [PMID: 21627118]
[83]
Qazi S, Liepold LO, Abedin MJ, et al. P22 viral capsids as nanocomposite high-relaxivity MRI contrast agents. Mol Pharm 2013; 10(1): 11-7.
[http://dx.doi.org/10.1021/mp300208g] [PMID: 22656692]
[84]
Ghosh D, Lee Y, Thomas S, et al. M13-templated magnetic nanoparticles for targeted in vivo imaging of prostate cancer. Nat Nanotechnol 2012; 7(10): 677-82.
[http://dx.doi.org/10.1038/nnano.2012.146] [PMID: 22983492]
[85]
Doshi N, Prabhakarpandian B, Rea-Ramsey A, Pant K, Sundaram S, Mitragotri S. Flow and adhesion of drug carriers in blood vessels depend on their shape: a study using model synthetic microvascular networks. J Control Release 2010; 146(2): 196-200.
[http://dx.doi.org/10.1016/j.jconrel.2010.04.007] [PMID: 20385181]
[86]
Botta M, Tei L. Relaxivity enhancement in macromolecular and nanosized GdIII‐based MRI contrast agents. Eur J Inorg Chem 2012; 2012(12): 1945-60.
[http://dx.doi.org/10.1002/ejic.201101305]
[87]
Caravan P. Strategies for increasing the sensitivity of gadolinium based MRI contrast agents. Chem Soc Rev 2006; 35(6): 512-23.
[http://dx.doi.org/10.1039/b510982p] [PMID: 16729145]
[88]
Aljabali AAA, Zoubi MSA, Al-Batanyeh KM, et al. Gold-coated plant virus as computed tomography imaging contrast agent. Beilstein J Nanotechnol 2019; 10: 1983-93.
[http://dx.doi.org/10.3762/bjnano.10.195] [PMID: 31667046]
[89]
Cole LE, Ross RD, Tilley JM, Vargo-Gogola T, Roeder RK. Gold nanoparticles as contrast agents in x-ray imaging and computed tomography. Nanomedicine (Lond) 2015; 10(2): 321-41.
[http://dx.doi.org/10.2217/nnm.14.171] [PMID: 25600973]
[90]
Dragnea B, Chen C, Kwak E-S, Stein B, Kao CC. Gold nanoparticles as spectroscopic enhancers for in vitro studies on single viruses. J Am Chem Soc 2003; 125(21): 6374-5.
[http://dx.doi.org/10.1021/ja0343609] [PMID: 12785770]
[91]
Capehart SL, Coyle MP, Glasgow JE, Francis MB. Controlled integration of gold nanoparticles and organic fluorophores using synthetically modified MS2 viral capsids. J Am Chem Soc 2013; 135(8): 3011-6.
[http://dx.doi.org/10.1021/ja3078472] [PMID: 23402352]
[92]
Li F, Gao D, Zhai X, et al. Tunable, discrete, three-dimensional hybrid nanoarchitectures. Angew Chem Int Ed Engl 2011; 50(18): 4202-5.
[http://dx.doi.org/10.1002/anie.201007433] [PMID: 21472923]
[93]
Frenkel D, Solomon B. Filamentous phage as vector-mediated antibody delivery to the brain. Proc Natl Acad Sci USA 2002; 99(8): 5675-9.
[http://dx.doi.org/10.1073/pnas.072027199] [PMID: 11960022]
[94]
Kumar K, Kumar Doddi S, Arunasree MK, Paik P. CPMV-induced synthesis of hollow mesoporous SiO2 nanocapsules with excellent performance in drug delivery. Dalton Trans 2015; 44(9): 4308-17.
[http://dx.doi.org/10.1039/C4DT02549K] [PMID: 25640798]
[95]
Aljabali AA, Shukla S, Lomonossoff GP, Steinmetz NF, Evans DJ. CPMV-DOX delivers. Mol Pharm 2013; 10(1): 3-10.
[http://dx.doi.org/10.1021/mp3002057] [PMID: 22827473]
[96]
Liu X, Liu B, Gao S, et al. Glyco-decorated tobacco mosaic virus as a vector for cisplatin delivery. J Mater Chem B Mater Biol Med 2017; 5(11): 2078-85.
[http://dx.doi.org/10.1039/C7TB00100B] [PMID: 32263681]
[97]
Sánchez-Sánchez L, Cadena-Nava RD, Palomares LA, et al. Chemotherapy pro-drug activation by biocatalytic virus-like nanoparticles containing cytochrome P450. Enzyme Microb Technol 2014; 60: 24-31.
[http://dx.doi.org/10.1016/j.enzmictec.2014.04.003] [PMID: 24835096]
[98]
Aljabali AA, Barclay JE, Steinmetz NF, Lomonossoff GP, Evans DJ. Controlled immobilisation of active enzymes on the cowpea mosaic virus capsid. Nanoscale 2012; 4(18): 5640-5.
[http://dx.doi.org/10.1039/c2nr31485a] [PMID: 22865109]
[99]
Brasch M, de la Escosura A, Ma Y, et al. Encapsulation of phthalocyanine supramolecular stacks into virus-like particles. J Am Chem Soc 2011; 133(18): 6878-81.
[http://dx.doi.org/10.1021/ja110752u] [PMID: 21506537]
[100]
Lee KL, Carpenter BL, Wen AM, Ghiladi RA, Steinmetz NF. High aspect ratio nanotubes formed by tobacco mosaic virus for delivery of photodynamic agents targeting melanoma. ACS Biomater Sci Eng 2016; 2(5): 838-44.
[http://dx.doi.org/10.1021/acsbiomaterials.6b00061] [PMID: 28713855]
[101]
Ngweniform P, Abbineni G, Cao B, Mao C. Self-assembly of drug-loaded liposomes on genetically engineered target-recognizing M13 phage: a novel nanocarrier for targeted drug delivery. Small 2009; 5(17): 1963-9.
[http://dx.doi.org/10.1002/smll.200801902] [PMID: 19415651]
[102]
Oh MH, Yu JH, Kim I, Nam YS. Genetically programmed clusters of gold nanoparticles for cancer cell-targeted photothermal therapy. ACS Appl Mater Interfaces 2015; 7(40): 22578-86.
[http://dx.doi.org/10.1021/acsami.5b07029] [PMID: 26413999]

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