Biodistribution and clearance of a filamentous plant virus in healthy and tumor-bearing mice

Nanomedicine

Volumn 9, Issue 2, 2014, Pages 221-235

  Shukla, Sourabh ^a   Wen, Amy M ^a   Ayat, Nadia R ^a   Commandeur, Ulrich ^b   Gopalkrishnan, Ramamurthy ^a   Broome, Ann Marie ^a,c   Lozada, Kristen W ^d   Keri, Ruth A ^d,e   Steinmetz, Nicole F ^a,d,f  

^a Case Western Reserve University   (United States)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

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

^e CASE WESTERN RESERVE UNIVERSITY   (United States)

^f Case Western Reserve University   (United States)

Author keywords

Anisotropic nanoparticle; Biodistribution; Immunogenicity; Mononuclear phagocyte system; Nanoparticle shape; PEG; Tumor homing; Viral nanoparticle

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EX VIVO STUDY; FEMALE; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; MOUSE; NONHUMAN; POTEXVIRUS; PRIORITY JOURNAL; RETICULOENDOTHELIAL SYSTEM; TUMOR XENOGRAFT; VIRAL CLEARANCE; VIRAL PHENOMENA AND FUNCTIONS; VIRUS BIODISTRIBUTION;

ANIMALS; HETEROGRAFTS; MICE; MICE, INBRED BALB C; NEOPLASMS, EXPERIMENTAL; PLANT VIRUSES;

EID: 84896721330     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.13.75     Document Type: Article

References (53)

1. Yildiz I, Shukla S, Steinmetz NF. Applications of viral nanoparticles in medicine. Curr. Opin. Biotechnol. 22(6), 901-908 (2011).
2. Pokorski JK, Steinmetz NF. The art of engineering viral nanoparticles. Mol. Pharm. 8(1), 29-43 (2011).
3. 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. Nanomed. 2(4), 715-733 (2007).
4. Singh P, Prasuhn D, Yeh RM et al. Biodistribution, toxicity and pathology of cowpea mosaic virus nanoparticles in vivo. J. Control. Release 120(1-2), 41-50 (2007).
5. Decuzzi P, God in B, Tanaka T et al. Size and shape effects in the biodistribution of intravascularly injected particles. J. Control. Release 141(3), 320-327 (2010).
6. Decuzzi P, Ferrari M. The adhesive stre ngth of non-spherical particles mediated by specific interactions. Biomaterials 27(30), 5307-5314 (2006).
7. Gentile F, Chiappini C, Fine D et al. The effect of shape on the margination dynamics of no n-neutrally buoyant particles in two-dimensional shear flows. J. Biomech. 41(10), 2312-2318 (2008).
8. Lee SY, Ferrari M, Decuzzi P. Design of biomimetic particles with enhanced vascular interaction. J. Biomech. 42(12), 1885-1890 (2009).
9. Shukla S, Ablack AL, Wen AM, Lee KL, Lewis JD, Steinmetz NF. Increased tumor homing and tissue penetration of the filamentous plant viral nanoparticle potato virus X. Mol. Pharm. 10(1), 33-42 (2013).
10. Oliveira LT, Garcia GM, Kano EK, Tedesco AC, Mosqueira VC. HPLC-FLD methods to quantify chloroaluminum phthalocyanine in nanoparticles, plasm a and tissue: Application in pharmacokinetic and biodistribution studies. J. Pharm. Biomed. Anal. 56(1), 70-77 (2011).
11. Ocampo-Garcia BE, Ramirez Fde M, Ferro-Floresg et al. (99m)Tc-labelled gold nanoparticles capped with HYNIC-peptide/mannose for sentinel lymph node detection. Nucl. Med. Biol. 38(1), 1-11 (2011).
12. Rojas S, Gispert JD, Martin R et al. Biodistribution of amino-fu nctionalized diamond nanoparticles. In vivo studies based on 18F radionuclide emission. ACS Nano 5(7), 5552-5559 (2011).
13. Artzi N, Oliva N, Puron C et al. In vivo and in vitro trackingo f erosion in biodegradable materials using non-invasive fluorescence imaging. Nat. Mater. 10(9), 704-709 (2011).
14. Vasquez KO, Casavant C, Peterson JD. Quantitative whole body biodistribution of f luorescent-labeled agents by non-invasive tomographic imaging. PLoS ONE 6(6), e20594 (2011).
15. Rae CS, Khor IW, Wang Q et al. Systemic trafficking of plant virus nanoparticles in mice via the oral r oute. Virology 343(2), 224-235 (2005).
16. Liu Z, Davis C, Cai W, He L, Chen X, Dai H. Circulation and long-term fate of functionalized, biocompatible single-walled carbon nanotubes in mice probed by Raman spectroscopy. Proc. Natl Acad. Sci. USA 105(5), 1410-1415 (2008).
17. Yu T, Hubbard D, Ray A, Ghandehari H. In vivo biodistribution and pharmacokinetics of silica nanoparticles as a function of geometry, porosity and surface characteristics. J. Control. Release 163(1), 46-54 (2012).
18. Li SD, Huang L. Pharmacokinetics and biodistribution of nanoparticles. Mol. Pharm. 5(4), 496-504 (2008).
19. Sa LT, Albernaz MD, Patricio BF et al. Biodistribution of nanoparticles: Initial considerations. J. Pharm. Biomed. Anal. 70, 602-604 (2012).
20. Lunov O, Syrovets T, Loos C et al. Differential uptake of functionalized polystyrene nanoparticles by human macrophages and a monocytic cell line. ACS Nano 5(3), 1657-1669 (2011).
21. Maldiney T, Richard C, Seguin J, Wattier N, Bessodes M, Scherman D. Effect of core diameter, surface coat ing, and PEG chain length on the biodistribution of persistent luminescence nanoparticles in mice. ACS Nano 5(2), 854-862 (2011).
22. Bartneck M, Keul HA, Wambach Met al. Effects of nanopa rticle surface-coupled peptides, functional endgroups, and charge on intracellular distribution and functionality of human primary reticuloendothelial cells. Nanomedicine 8(8), 1282-1292 (2012).
23. Cheruku ri P, Gannon CJ, Leeuw TK et al. Mammalian pharmacokinetics of carbon nanotubes using intrinsic near-infrared fluorescence. Proc. Natl Acad. Sci. USA 103(50), 18882-18886 (2006).
24. Lacerda L, Herrero MA, Venner K, Bianco A, Prato M, Kostarelos K. Carbon-nanotube shape and individualization critical for renal excretion. Small 4(8), 1130-1132 (2008).
25. Mcdevitt MR, Chatt opadhyay D, Kappel BJ et al. Tumor targeting with antibody-functionalized, radiolabeled carbon nanotubes. J. Nucl. Med. 48(7), 1180-1189 (2007).
26. Singh R, Pantarotto D, Lacerda L et al. Tissue biodistribution and blood clearance rates of intravenously administered carbon nanotube radiotracers. Proc. Natl Acad. Sci. USA 103(9), 3357-3362 (2006).
27. Ruggiero A, Villa CH, Bander E et al. Paradoxical glomerular filtration of carbon nanotubes. Proc. Natl Acad. Sci. USA 107(27), 12369-12374 (2010).
28. Huang X, Li L, Liu T et al. The shape effect of mesoporous silica n anoparticles on biodistribution, clearance, and biocompatibility in vivo. ACS Nano 5(7), 5390-5399 (2011).
29. Choi HS, Liu W, Misra P et al. Renal clearance of quantum dots. Nat. Biotechnol. 25(10), 1165-1170 (2007).
30. Owens De 3rd, Peppas NA. Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int. J. Pharm. 307(1), 93-102 (2006).
31. Malugin A, Ghandehari H. Cellular uptake and toxicity of gold nanoparticles in prostate cancer cells: A comparative study of rods and spheres. J. Appl. Toxicol. 30(3), 212-217 (2010).
32. Fischer HC, Liu LC, Pang KS, Chan WC. Pharmacokinetics of nanoscale quantum dots: In vivo distribution, sequestration, and clearance in the rat. Adv. Funct. Mater. 16(10), 1299-1305 (2006).
33. Sadauskas E, Wallin H, Stoltenberg Met al. Kupffer cells are central in the removal of nanoparticles from the organism. Part Fibre Toxicol. 4, 10 (2007).
34. Bohnsack JF, Brown EJ. The role of the spleen in resistance to infection. Annu. Rev. Med. 37, 49-59 (1986).
35. Cho NH, Cheong TC, Min JH et al. A multifunctional core-shell nanoparticle for dendritic cell-based cancer immunotherapy. Nat. Nanotechnol. 6(10), 675-682 (2011).
36. Manolova V, Flace A, Bauer M, Schwarz K, Saudan P, Bachmann MF. Nanoparticles target distinct dendritic cell populations acco rding to their size. Eur. J. Immunol. 38(5), 1404-1413 (2008).
37. Dinauer N, Balthasar S, Weber C, Kreuter J, Langer K, Von Briesen H. Selective targeting of antibody-conjugated nanoparti cles to leukemic cells and primary T-lymphocytes. Biomaterials 26(29), 5898-5906 (2005).
38. Richter K, Agnellini P, Oxenius A. On the role of the inhibitory receptor LAG-3 in acute and chronic LCMV infection. Int. Immunol. 22(1), 13-23 (2010).
39. Murakami T, Chen X, Hase K, Sakamoto A, Nishigaki C, Ohno H. Splenic CD19-CD35+B220+ cells function as an inducer of follicular den dritic cell network formation. Blood 110(4), 1215-1224 (2007).
40. Goldberg MV, Drake CG. LAG-3 in cancer Immunotherapy. Curr. Top. Microbiol. Immunol. 344, 269-278 (2011).
41. Steinmetz NF, Ablack AL, Hickey JL et al. Intravital imaging of human prostate cancer using viral nanoparticles targeted to gastrin-releasing peptide receptors. Small 7(12), 1664-1672 (2011).
42. Steinmetz NF, Mertens ME, Taurog RE et al. Potato virus X as a novel platform for potential biomedical applications. Nano Lett. 10(1), 305-312 (2010).
43. Chri stian DA, Cai S, Garbuzenko OB et al. Flexible filaments for in vivo imaging and delivery: Persistent circulation of filomicelles opens the dosage window for sustained tumor shrinkage. Mol. Pharm. 6(5), 1343-1352 (200 9).
44. Moghimi SM, Hunter AC, Andresen TL. Factors controlling nanoparticle pharmacokinetics: An integrated analysis and perspective. Annu. Rev. Pharmacol. Toxicol. 52, 481-503 (2012).
45. Toraya-Brown S, Sheen MR, Baird JR et al. Phagocytes mediate targeting of iron oxide nanoparticles to tumors for cancer therapy. Integr. Biol. (Camb.) 5(1), 159-171 (2012).
46. Li M, Al-Jamal KT, Kostarelos K, Reineke J. Physiologically based pharmacokinetic modeling of nanoparticles. ACS Nano 4(11), 6303-6317 (2010).
47. Torosean S, Flynn B , Axelsson J et al. Nanoparticle uptake in tumors is mediated by the interplay of vascular and collagen density with interstitial pressure. Nanomedicine 9(2), 151-158 (2012).
48. Lico C, Ma ncini C, Italiani P et al. Plant-produced potato virus X chimeric particles displaying an influenza virus-derived peptide activate specific CD8+ T cells in mice. Vaccine 27(37), 5069-5076 (2009).
49. Steinmetz NF, Manchester M. PEGylated viral nanoparticles for biomedicine: The impact of PEG chain length on VNP cell interactions in vitro and ex vivo. Biomacromolecules 10(4), 784-792 (2009).
50. Raja KS, Wang Q, Gonzalez MJ, Manchester M, Johnson JE, Finn MG. Hybrid virus-polymer materials. 1. Synthesis and properties of PEG-decorated cowpea mosaic virus. Biomacromolecules 4(3), 472-476 (2003).
51. Perry JL, Reuter KG, Kai MP et al. PEGylated PRINT nanoparticles: The impact of PEG density on protein binding, macrophage association, biodistribution, and pharmacokinetics. Nano Lett. 12(10), 5304-5310 (2012).
52. Svergun DI, Ekstrom F, Vandegriff KD et al. Solution structure of poly(ethylene) glycol-conjugated hemoglobin revealed by small-angle X-ray scattering: Implications for a new oxygen therape utic. Biophys. J. 94(1), 173-181 (2008).
53. Degennes PG. Polymers at an interface-A simplified view. Adv. Colloid Interfac. 27(3-4), 189-209 (1987).