Increased tumor homing and tissue penetration of the filamentous plant viral nanoparticle potato virus X

Molecular Pharmaceutics

Volumn 10, Issue 1, 2013, Pages 33-42

  Shukla, Sourabh ^a   Ablack, Amber L ^d   Wen, Amy M ^a   Lee, Karin L ^a   Lewis, John D ^d   Steinmetz, Nicole F ^a,b,c  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Case Western Reserve University   (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

cowpea mosaic virus; nanoparticle shape; potato virus X; tissue penetration; tumor homing; tumor xenografts; viral nanoparticles

Indexed keywords

COWPEA MOSAIC VIRUS NANOPARTICLE; NANOPARTICLE; POTATO VIRUS X NANOPARTICLE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL HOMING; CHORIOALLANTOIS; COLON CANCER; CONTROLLED STUDY; DRUG DISTRIBUTION; DRUG PENETRATION; EMBRYO; FIBROSARCOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PLANT VIRUS; PRIORITY JOURNAL; SQUAMOUS CELL CARCINOMA; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CHICK EMBRYO; COMOVIRUS; DIAGNOSTIC IMAGING; DRUG DELIVERY SYSTEMS; HT29 CELLS; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; NANOPARTICLES; NEOPLASMS; ONCOLYTIC VIROTHERAPY; PLANTS; POLYETHYLENE GLYCOLS; POTEXVIRUS; TISSUE DISTRIBUTION;

EID: 84872169330     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp300240m     Document Type: Article

References (55)

1. Cai, S.; Vijayan, K.; Cheng, D.; Lima, E. M.; Discher, D. E. Micelles of Different Morphologies-Advantages of Worm-like Filomicelles of PEO-PCL in Paclitaxel Delivery Pharm. Res. 2007, 24, 2099-2109
2. Chauhan, V. P. Fluorescent nanorods and nanospheres for real-time in vivo probing of nanoparticle shape-dependent tumor penetration Angew. Chem., Int. Ed. 2011, 50, 11417-11420
3. Christian, D. A. Flexible filaments for in vivo imaging and delivery: persistent circulation of filomicelles opens the dosage window for sustained tumor shrinkage Mo.l Pharmaceutics 2009, 6, 1343-1352
4. Decuzzi, P. Size and shape effects in the biodistribution of intravascularly injected particles J. Controlled Release 2010, 141, 320-327
5. Geng, Y. Shape effects of filaments versus spherical particles in flow and drug delivery Nat. Nanotechnol. 2007, 2, 249-255
6. Gentile, F. The effect of shape on the margination dynamics of non-neutrally buoyant particles in two-dimensional shear flows J. Biomech. 2008, 41, 2312-2318
7. Lee, S.-Y.; Ferrari, M.; Decuzzi, P. Shaping nano-/micro-particles for enhanced vascular interaction in laminar flows Nanotechnology 2009, 20, 49510
8. Firme, C. P., 3rd; Bandaru, P. R. Toxicity issues in the application of carbon nanotubes to biological systems Nanomedicine 2010, 6, 245-256
9. Chitale, R. Merck hopes to extend gardasil vaccine to men J. Natl. Cancer Inst. 2009, 101, 222-223
10. Liu, T. C.; Galanis, E.; Kirn, D. Clinical trial results with oncolytic virotherapy: a century of promise, a decade of progress Nat. Clin. Pract. Oncol. 2007, 4, 101-117
11. Shirakawa, T. Clinical trial design for adenoviral gene therapy products Drug News Perspect. 2009, 22, 140-145
12. Kaiser, C. R. Biodistribution studies of protein cage nanoparticles demonstrate broad tissue distribution and rapid clearance in vivo Int. J. Nanomed. 2007, 2, 715-733
13. Singh, P. Bio-distribution, toxicity and pathology of cowpea mosaic virus nanoparticles in vivo J. Controlled Release 2007, 120, 41-50
14. Pokorski, J. K.; Steinmetz, N. F. The art of engineering viral nanoparticles Mol. Pharmaceutics 2011, 8, 29-43
15. Anderson, E. A. Viral nanoparticles donning a paramagnetic coat: conjugation of MRI contrast agents to the MS2 capsid Nano Lett. 2006, 6, 1160-1164
16. Hooker, J. M.; Datta, A.; Botta, M.; Raymond, K. N.; Francis, M. B. Magnetic resonance contrast agents from viral capsid shells: a comparison of exterior and interior cargo strategies Nano Lett. 2007, 7, 2207-2210
17. Hooker, J. M.; ONeil, 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
18. Kovacs, E. W. Dual-surface-modified bacteriophage MS2 as an ideal scaffold for a viral capsid-based drug delivery system Bioconjugate Chem. 2007, 18, 1140-1147
19. Loo, L.; Guenther, R. H.; Lommel, S. A.; Franzen, S. Encapsidation of nanoparticles by red clover necrotic mosaic virus J. Am. Chem. Soc. 2007, 129, 11111-11117
20. Loo, L.; Guenther, R. H.; Lommel, S. A.; Franzen, S. Infusion of dye molecules into Red clover necrotic mosaic virus Chem. Commun. 2008, 88-90
21. Ren, Y.; Wong, S. M.; Lim, L. Y. In vitro-reassembled plant virus-like particles for loading of polyacids J. Gen. Virol. 2006, 87, 2749-2754
22. Ren, Y.; Wong, S. M.; Lim, L. Y. Folic acid-conjugated protein cages of a plant virus: a novel delivery platform for doxorubicin Bioconjugate Chem. 2007, 18, 836-843
23. Suci, P. A. High-density targeting of a viral multifunctional nanoplatform to a pathogenic, biofilm-forming bacterium Chem. Biol. 2007, 14, 387-398
24. Suci, P. A.; 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, 12280-12286
25. Bruckman, M. A. Surface modification of tobacco mosaic virus with click chemistry ChemBioChem 2008, 9, 519-523
26. Rong, J. Oriented cell growth on self-assembled bacteriophage M13 thin films Chem. Commun. 2008, 5185-5187
27. Souza, G. R. Three-dimensional tissue culture based on magnetic cell levitation Nat. Nanotechnol. 2010, 5, 291-296
28. Lewis, J. D. Viral nanoparticles as tools for intravital vascular imaging Nat. Med. 2006, 12, 354-360
29. Steinmetz, N. F. Intravital imaging of human prostate cancer using viral nanoparticles targeted to gastrin-releasing Peptide receptors Small 2011, 7, 1664-1672
30. Steinmetz, N. F.; Cho, C. F.; Ablack, A.; Lewis, J. D.; Manchester, M. Cowpea mosaic virus nanoparticles target surface vimentin on cancer cells Nanomedicine 2011, 6, 351-364
31. Chatterji, A. New addresses on an addressable virus nanoblock: uniquely reactive Lys residues on cowpea mosaic virus Chem. Biol. 2004, 11, 855-863
32. Steinmetz, N. F. Potato virus X as a novel platform for potential biomedical applications Nano Lett. 2010, 10, 305-312
33. Wellink, J. Comovirus isolation and RNA extraction Methods Mol. Biol. 1998, 81, 205-209
34. Raja, K. S. Hybrid virus-polymer materials. 1. Synthesis and properties of PEG-decorated cowpea mosaic virus Biomacromolecules 2003, 4, 472-476
35. Le, H. T.; Yu, Q. C.; Wilson, J. M.; Croyle, M. A. Utility of PEGylated recombinant adeno-associated viruses for gene transfer J. Controlled Release 2005, 108, 161-177
36. Lee, G. K.; Maheshri, N.; Kaspar, B.; Schaffer, D. V. PEG conjugation moderately protects adeno-associated viral vectors against antibody neutralization Biotechnol. Bioeng. 2005, 92, 24-34
37. 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
38. Brunel, F. M. Hydrazone ligation strategy to assemble multifunctional viral nanoparticles for cell imaging and tumor targeting Nano Lett. 2010, 10, 1093-1097
39. 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
40. Steinmetz, N. F. Potato virus X as a novel platform for potential biomedical applications Nano Lett. 2010, 10, 305-312
41. Iyer, A. K.; Khaled, G.; Fang, J.; Maeda, H. Exploiting the enhanced permeability and retention effect for tumor targeting Drug Discovery Today 2006, 11, 812-818
42. Nederman, T.; Acker, H.; Carlsson, J. Penetration of substances into tumor tissue: a methodological study with microelectrodes and cellular spheroids In Vitro 1983, 19, 479-488
43. Netti, P. A.; Berk, D. A.; Swartz, M. A.; Grodzinsky, A. J.; Jain, R. K. Role of extracellular matrix assembly in interstitial transport in solid tumors Cancer Res. 2000, 60, 2497-2503
44. Stylianopoulos, T.; Diop-Frimpong, B.; Munn, L. L.; Jain, R. K. Diffusion anisotropy in collagen gels and tumors: the effect of fiber network orientation Biophys. J. 2010, 99, 3119-3128
45. Stylianopoulos, T. Diffusion of particles in the extracellular matrix: the effect of repulsive electrostatic interactions Biophys. J. 2010, 99, 1342-1349
46. Thurber, G. M.; Schmidt, M. M.; Wittrup, K. D. Antibody tumor penetration: Transport opposed by systemic and antigen-mediated clearance Adv. Drug Delivery Rev. 2008, 60, 1421-1434
47. Jain, R. K.; Stylianopoulos, T. Delivering nanomedicine to solid tumors Nat. Rev. Clin. Oncol. 2010, 7, 653-664
48. Campbell, R. B. Cationic charge determines the distribution of liposomes between the vascular and extravascular compartments of tumors Cancer Res. 2002, 62, 6831-6836
49. Dellian, M.; Yuan, F.; Trubetskoy, V. S.; Torchilin, V. P.; Jain, R. K. Vascular permeability in a human tumour xenograft: molecular charge dependence Br. J. Cancer 2000, 82, 1513-1518
50. Schmitt-Sody, M. Neovascular targeting therapy: paclitaxel encapsulated in cationic liposomes improves antitumoral efficacy Clin. Cancer Res. 2003, 9, 2335-2341
51. Toy, R.; Hayden, E.; Shoup, C.; Baskaran, H.; Karathanasis, E. The effects of particle size, density and shape on margination of nanoparticles in microcirculation Nanotechnology 2011, 22, 115101
52. Champion, J. A.; Mitragotri, S. Role of target geometry in phagocytosis Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 4930-4934
53. Li, S. D.; Huang, L. Pharmacokinetics and Biodistribution of Nanoparticles Mol. Pharmaceutics 2008, 5, 496-504
54. Rae, C. S. Systemic trafficking of plant virus nanoparticles in mice via the oral route Virology 2005, 343, 224-235
55. Peiser, L.; Mukhopadhyay, S.; Gordon, S. Scavenger receptors in innate immunity Curr. Opin. Immunol. 2002, 14, 123-128