Virus-inspired membrane encapsulation of DNA nanostructures to achieve in vivo stability

ACS Nano

Volumn 8, Issue 5, 2014, Pages 5132-5140

  Perrault, Steven D ^a   Shih, William M ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

biodistribution; DNA; imaging; immune; in vivo; lipid bilayer; nanostructure; nanotechnology; PEG; pharmacokinetics

Indexed keywords

BIOCHEMISTRY; CHEMICAL ACTIVATION; IMAGING TECHNIQUES; LIPID BILAYERS; MEDICAL APPLICATIONS; MEDICAL NANOTECHNOLOGY; NANOSTRUCTURES; NANOTECHNOLOGY; PHARMACOKINETICS; POLYETHYLENE GLYCOLS; VIRUSES;

BIODISTRIBUTIONS; BIOLOGICAL ENVIRONMENTS; BIOMEDICAL APPLICATIONS; IMMUNE; IN-VIVO; MOLECULAR-SCALE DEVICES; NUCLEASE DIGESTION; ORDERS OF MAGNITUDE;

DNA;

1,2-OLEOYLPHOSPHATIDYLCHOLINE; CHOLESTEROL; DIOLEOYL-N-(MONOMETHOXYPOLYETHYLENE GLYCOL SUCCINYL)PHOSPHATIDYLETHANOLAMINE; DNA; LIGAND; LIPID; LIPID BILAYER; LIPOSOME; MACROGOL DERIVATIVE; MICELLE; NANOMATERIAL; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; RHODAMINE; SURFACTANT;

ANIMAL; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNE SYSTEM; LIPID BILAYER; MICELLE; MOUSE; NANOMEDICINE; NUDE MOUSE; OPTICS; PROCEDURES; SPLEEN; TRANSMISSION ELECTRON MICROSCOPY; VIRUS; VIRUS CAPSID; VIRUS GENOME;

ANIMALS; CAPSID; CHOLESTEROL; DNA; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENOME, VIRAL; IMMUNE SYSTEM; LIGANDS; LIPID BILAYERS; LIPIDS; LIPOSOMES; MICE; MICE, NUDE; MICELLES; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; NANOMEDICINE; NANOSTRUCTURES; OPTICS AND PHOTONICS; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; POLYETHYLENE GLYCOLS; RHODAMINES; SPLEEN; SURFACE-ACTIVE AGENTS; VIRUSES;

EID: 84901660628     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn5011914     Document Type: Article

References (38)

1. Glauert, A. M.; Dingle, J. T.; Lucy, J. A. Action of Saponin on Biological Cell Membranes Nature 1962, 196, 953-955
2. Horne, R. W.; Bangham, A. D.; Whittaker, V. P. Negatively Stained Lipoprotein Membranes Nature 1963, 200, 1340
3. Douglas, S. M.; Bachelet, I.; Church, G. M. A Logic-Gated Nanorobot for Targeted Transport of Molecular Payloads Science 2012, 335, 831-834
4. Klibanov, A. L.; Maruyama, K.; Torchilin, V. P.; Huang, L. Amphipathic Polyethyleneglycols Effectively Prolong the Circulation Time of Liposomes FEBS Lett. 1990, 268, 235-237
5. Perrault, S. D.; Walkey, C.; Jennings, T.; Fischer, H. C.; Chan, W. C. W. Mediating Tumor Targeting Efficiency of Nanoparticles through Design Nano Lett. 2009, 9, 1909-1915
6. Rodriguez, P. L.; Harada, T.; Christian, D. A.; Pantano, D. A.; Tsai, R. K.; Discher, D. E. Minimal "Self" Peptides That Inhibit Phagocytic Clearance and Enhance Delivery of Nanoparticles Science 2013, 339, 971-975
7. Åkerman, M. E.; Chan, W. C. W.; Laakkonen, P.; Bhatia, S. N.; Ruoslahti, E. Nanocrystal Targeting in Vivo Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 12617-12621
8. Farokhzad, O.; Jon, S.; Khademhosseini, A.; Tran, T.; LaVan, D.; Langer, R. Nanopartide-Aptamer Bioconjugates: A New Approach for Targeting Prostate Cancer Cells RID A-9435-2010 Cancer Res. 2004, 64, 7668-7672
9. Perrault, S. D.; Chan, W. C. W. In Vivo Assembly of Nanoparticle Components To Improve Targeted Cancer Imaging Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 11194-11199
10. Park, J.-H.; von Maltzahn, G.; Xu, M. J.; Fogal, V.; Kotamraju, V. R.; Ruoslahti, E.; Bhatia, S. N.; Sailor, M. J. Cooperative Nanomaterial System To Sensitize, Target, and Treat Tumors Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 981-986
11. Von Maltzahn, G.; Park, J.-H.; Lin, K. Y.; Singh, N.; Schwoeppe, C.; Mesters, R.; Berdel, W. E.; Ruoslahti, E.; Sailor, M. J.; Bhatia, S. N. Nanoparticles That Communicate in Vivo To Amplify Tumour Targeting Nat. Mater. 2011, 10, 545-552
12. Seeman, N. C. Nanomaterials Based on DNA Annu. Rev. Biochem. 2010, 79, 65-87
13. Rothemund, P. W. K. Folding DNA To Create Nanoscale Shapes and Patterns Nature 2006, 440, 297-302
14. Douglas, S. M.; Dietz, H.; Liedl, T.; Högberg, B.; Graf, F.; Shih, W. M. Self-Assembly of DNA into Nanoscale Three-Dimensional Shapes Nature 2009, 459, 414-418
15. Dietz, H.; Douglas, S. M.; Shih, W. M. Folding DNA into Twisted and Curved Nanoscale Shapes Science 2009, 325, 725-730
16. Ke, Y.; Ong, L. L.; Shih, W. M.; Yin, P. Three-Dimensional Structures Self-Assembled from DNA Bricks Science 2012, 338, 1177-1183
17. Schüller, V. J.; Heidegger, S.; Sandholzer, N.; Nickels, P. C.; Suhartha, N. A.; Endres, S.; Bourquin, C.; Liedl, T. Cellular Immunostimulation by CpG-Sequence-Coated DNA Origami Structures ACS Nano 2011, 5, 9696-9702
18. Li, J.; Pei, H.; Zhu, B.; Liang, L.; Wei, M.; He, Y.; Chen, N.; Li, D.; Huang, Q.; Fan, C. Self-Assembled Multivalent DNA Nanostructures for Noninvasive Intracellular Delivery of Immunostimulatory CpG Oligonucleotides ACS Nano 2011, 5, 8783-8789
19. Langecker, M.; Arnaut, V.; Martin, T. G.; List, J.; Renner, S.; Mayer, M.; Dietz, H.; Simmel, F. C. Synthetic Lipid Membrane Channels Formed by Designed DNA Nanostructures Science 2012, 338, 932-936
20. Rudchenko, M.; Taylor, S.; Pallavi, P.; Dechkovskaia, A.; Khan, S.; Butler, V. P., Jr.; Rudchenko, S.; Stojanovic, M. N. Autonomous Molecular Cascades for Evaluation of Cell Surfaces Nat. Nanotechnol. 2013, 8, 580-586
21. Nadano, D.; Yasuda, T.; Kishi, K. Measurement of Deoxyribonuclease I Activity in Human Tissues and Body Fluids by a Single Radial Enzyme-Diffusion Method Clin. Chem. 1993, 39, 448-452
22. Kawai, T.; Akira, S. The Role of Pattern-Recognition Receptors in Innate Immunity: Update on Toll-like Receptors Nat. Immunol. 2010, 11, 373-384
23. Douglas, S. M.; Marblestone, A. H.; Teerapittayanon, S.; Vazquez, A.; Church, G. M.; Shih, W. M. Rapid Prototyping of 3D DNA-Origami Shapes with caDNAno Nucleic Acids Res. 2009, 37, 5001-5006
24. Mathieu, F.; Liao, S.; Kopatsch, J.; Wang, T.; Mao, C.; Seeman, N. C. Six-Helix Bundles Designed from DNA Nano Lett. 2005, 5, 661-665
25. Douglas, S. M.; Chou, J. J.; Shih, W. M. DNA-Nanotube-Induced Alignment of Membrane Proteins for NMR Structure Determination Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 6644-6648
26. Lin, C.; Perrault, S. D.; Kwak, M.; Graf, F.; Shih, W. M. Purification of DNA-Origami Nanostructures by Rate-Zonal Centrifugation Nucleic Acids Res. 2013, 41, e40
27. Chan, Y. H.; Van Lengerich, B.; Boxer, S. G. Effects of Linker Sequences on Vesicle Fusion Mediated by Lipid-Anchored DNA Oligonucleotides Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 979-984
28. Ollivon, M.; Lesieur, S.; Grabielle-Madelmont, C.; Paternostre, M. Vesicle Reconstitution from Lipid-Detergent Mixed Micelles Biochim. Biophys. Acta, Biomembr. 2000, 1508, 34-50
29. Noda, T. Native Morphology of Influenza Virions Front. Virol. 2012, 2, 269-273
30. Soo Choi, H.; Liu, W.; Misra, P.; Tanaka, E.; Zimmer, J. P.; Itty Ipe, B.; Bawendi, M. G.; Frangioni, J. V. Renal Clearance of Quantum Dots Nat. Biotechnol. 2007, 25, 1165-1170
31. Mei, Q.; Wei, X.; Su, F.; Liu, Y.; Youngbull, C.; Johnson, R.; Lindsay, S.; Yan, H.; Meldrum, D. Stability of DNA Origami Nanoarrays in Cell Lysate Nano Lett. 2011, 11, 1477-1482
32. Surana, S.; Bhatia, D.; Krishnan, Y. A Method To Study In Vivo Stability of DNA Nanostructures Methods 2013, 64, 94-100
33. Lee, H.; Lytton-Jean, A. K. R.; Chen, Y.; Love, K. T.; Park, A. I.; Karagiannis, E. D.; Sehgal, A.; Querbes, W.; Zurenko, C. S.; Jayaraman, M. et al. Molecularly Self-Assembled Nucleic Acid Nanoparticles for Targeted In Vivo siRNA Delivery Nat. Nanotechnol. 2012, 7, 389-393
34. Liu, H.; Xu, Y.; Li, F.; Yang, Y.; Wang, W.; Song, Y.; Liu, D. Light-Driven Conformational Switch of I-Motif DNA Angew. Chem., Int. Ed. 2007, 46, 2515-2517
35. Juul, S.; Iacovelli, F.; Falconi, M.; Kragh, S. L.; Christensen, B.; Frøhlich, R.; Franch, O.; Kristoffersen, E. L.; Stougaard, M.; Leong, K. W. et al. Temperature-Controlled Encapsulation and Release of an Active Enzyme in the Cavity of a Self-Assembled DNA Nanocage ACS Nano 2013, 7, 9724-9734
36. Banerjee, A.; Bhatia, D.; Saminathan, A.; Chakraborty, S.; Kar, S.; Krishnan, Y. Controlled Release of Encapsulated Cargo from a DNA Icosahedron Using a Chemical Trigger Angew. Chem., Int. Ed. 2013, 52, 6854-6857
37. Karanth, H.; Murthy, R. S. R. pH-Sensitive Liposomes - Principle and Application in Cancer Therapy J. Pharm. Pharmacol. 2007, 59, 469-483
38. Kaliss, N.; Pressman, D. Plasma and Blood Volumes of Mouse Organs, As Determined with Radioactive Iodoproteins Exp. Biol. Med. 1950, 75, 16-20