DNA nanomaterials for preclinical imaging and drug delivery

Journal of Controlled Release

Volumn 239, Issue , 2016, Pages 27-38

  Jiang, Dawei ^a   England, Christopher G ^b   Cai, Weibo ^a,b,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN   (United States)

Author keywords

DNA; DNA nanoparticle; DNA nanostructure; DNA nanotechnology; Drug delivery; Molecular imaging

Indexed keywords

BIOLOGICAL MATERIALS; BIOLOGY; DIAGNOSIS; DRUG DELIVERY; GENES; MEDICAL APPLICATIONS; MOLECULAR IMAGING; NANOSTRUCTURED MATERIALS; NANOSTRUCTURES; NANOTECHNOLOGY;

BIOLOGICAL APPLICATIONS; BIOMEDICAL APPLICATIONS; DNA NANOPARTICLES; DNA NANOSTRUCTURES; DNA NANOTECHNOLOGY; GENETIC INFORMATION; MATERIAL ENGINEERING; PRECLINICAL IMAGING;

DNA;

DNA; NANOCAGE; NANOMATERIAL;

DNA PURIFICATION; DRUG DELIVERY SYSTEM; IMMUNE RESPONSE; MOLECULAR IMAGING; MOLECULAR STABILITY; NANOTECHNOLOGY; PRIORITY JOURNAL; REVIEW; ANIMAL; CHEMISTRY; HUMAN; PROCEDURES; TRENDS;

ANIMALS; DNA; DRUG DELIVERY SYSTEMS; HUMANS; MOLECULAR IMAGING; NANOSTRUCTURES; NANOTECHNOLOGY;

EID: 84983404807     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2016.08.013     Document Type: Review

References (87)

1. [1] Youn, H., Hong, K.J., In vivo noninvasive small animal molecular imaging. Osong Public Health Res. Perspect. 3 (2012), 48–59.
2. [2] Hoelder, S., Clarke, P.A., Workman, P., Discovery of small molecule cancer drugs: successes, challenges and opportunities. Mol. Oncol. 6 (2012), 155–176.
3. [3] Adams, J.L., Smothers, J., Srinivasan, R., Hoos, A., Big opportunities for small molecules in immuno-oncology. Nat. Rev. Drug Discov. 14 (2015), 603–622.
4. [4] Kaspar, A.A., Reichert, J.M., Future directions for peptide therapeutics development. Drug Discov. Today 18 (2013), 807–817.
5. [5] Gongora-Benitez, M., Tulla-Puche, J., Albericio, F., Multifaceted roles of disulfide bonds. Peptides as therapeutics. Chem. Rev. 114 (2014), 901–926.
6. [6] Boohaker, R.J., Lee, M.W., Vishnubhotla, P., Perez, J.M., Khaled, A.R., The use of therapeutic peptides to target and to kill cancer cells. Curr. Med. Chem. 19 (2012), 3794–3804.
7. [7] Gambhir, S.S., Molecular imaging of cancer with positron emission tomography. Nat. Rev. Cancer 2 (2002), 683–693.
8. [8] Mammatas, L.H., Verheul, H.M., Hendrikse, N.H., Yaqub, M., Lammertsma, A.A., Menke-van der Houven van Oordt, C.W., Molecular imaging of targeted therapies with positron emission tomography: the visualization of personalized cancer care. Cell Oncol. (Dordr.) 38 (2015), 49–64.
9. [9] England, C.G., Hernandez, R., Eddine, S.B., Cai, W., Molecular imaging of pancreatic cancer with antibodies. Mol. Pharm. 13 (2016), 8–24.
10. [10] Peer, D., Karp, J.M., Hong, S., Farokhzad, O.C., Margalit, R., Langer, R., Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2 (2007), 751–760.
11. [11] Farokhzad, O.C., Langer, R., Impact of nanotechnology on drug delivery. ACS Nano 3 (2009), 16–20.
12. [12] LaVan, D.A., McGuire, T., Langer, R., Small-scale systems for in vivo drug delivery. Nat. Biotechnol. 21 (2003), 1184–1191.
13. [13] Anselmo, A.C., Mitragotri, S., An overview of clinical and commercial impact of drug delivery systems. J. Control. Release 190 (2014), 15–28.
14. [14] Byrne, J.D., Betancourt, T., Brannon-Peppas, L., Active targeting schemes for nanoparticle systems in cancer therapeutics. Adv. Drug Deliv. Rev. 60 (2008), 1615–1626.
15. [15] Lukyanov, A.N., Torchilin, V.P., Micelles from lipid derivatives of water-soluble polymers as delivery systems for poorly soluble drugs. Adv. Drug Deliv. Rev. 56 (2004), 1273–1289.
16. [16] Kabanov, A.V., Batrakova, E.V., Alakhov, V.Y., Pluronic (R) block copolymers as novel polymer therapeutics for drug and gene delivery. J. Control. Release 82 (2002), 189–212.
17. [17] Schmaljohann, D., Thermo- and pH-responsive polymers in drug delivery. Adv. Drug Deliv. Rev. 58 (2006), 1655–1670.
18. [18] Bianco, A., Kostarelos, K., Prato, M., Applications of carbon nanotubes in drug delivery. Curr. Opin. Chem. Biol. 9 (2005), 674–679.
19. [19] Prato, M., Kostarelos, K., Bianco, A., Functionalized carbon nanotubes in drug design and discovery. Acc. Chem. Res. 41 (2008), 60–68.
20. [20] Feng, L., Liu, Z., Graphene in biomedicine: opportunities and challenges. Nanomedicine (Lond.) 6 (2011), 317–324.
21. [21] Smith, A.M., Duan, H., Mohs, A.M., Nie, S., Bioconjugated quantum dots for in vivo molecular and cellular imaging. Adv. Drug Deliv. Rev. 60 (2008), 1226–1240.
22. [22] Zrazhevskiy, P., Sena, M., Gao, X., Designing multifunctional quantum dots for bioimaging, detection, and drug delivery. Chem. Soc. Rev. 39 (2010), 4326–4354.
23. [23] Kamkaew, A., Sun, H., England, C.G., Cheng, L., Liu, Z., Cai, W., Quantum dot-NanoLuc bioluminescence resonance energy transfer enables tumor imaging and lymph node mapping in vivo. Chem. Commun. (Camb.) 52 (2016), 6997–7000.
24. [24] Ahmad, M.Z., Akhter, S., Jain, G.K., Rahman, M., Pathan, S.A., Ahmad, F.J., Khar, R.K., Metallic nanoparticles: technology overview & drug delivery applications in oncology. Expert Opin. Drug Deliv. 7 (2010), 927–942.
25. [25] Boisselier, E., Astruc, D., Gold nanoparticles in nanomedicine: preparations, imaging, diagnostics, therapies and toxicity. Chem. Soc. Rev. 38 (2009), 1759–1782.
26. [26] Duncan, B., Kim, C., Rotello, V.M., Gold nanoparticle platforms as drug and biomacromolecule delivery systems. J. Control. Release 148 (2010), 122–127.
27. [27] England, C.G., Miller, M.C., Kuttan, A., Trent, J.O., Frieboes, H.B., Release kinetics of paclitaxel and cisplatin from two and three layered gold nanoparticles. Eur. J. Pharm. Biopharm. 92 (2015), 120–129.
28. [28] Slowing, I.I., Vivero-Escoto, J.L., Wu, C.W., Lin, V.S., Mesoporous silica nanoparticles as controlled release drug delivery and gene transfection carriers. Adv. Drug Deliv. Rev. 60 (2008), 1278–1288.
29. [29] Cheng, Y., Samia, A.C., Meyers, J.D., Panagopoulos, I., Fei, B., Burda, C., Highly efficient drug delivery with gold nanoparticle vectors for in vivo photodynamic therapy of cancer. J. Am. Chem. Soc. 130 (2008), 10643–10647.
30. [30] Choi, K.Y., Liu, G., Lee, S., Chen, X., Theranostic nanoplatforms for simultaneous cancer imaging and therapy: current approaches and future perspectives. Nanoscale 4 (2012), 330–342.
31. [31] Niemeyer, C.M., Self-assembled nanostructures based on DNA: towards the development of nanobiotechnology. Curr. Opin. Chem. Biol. 4 (2000), 609–618.
32. [32] Pinheiro, A.V., Han, D., Shih, W.M., Yan, H., Challenges and opportunities for structural DNA nanotechnology. Nat. Nanotechnol. 6 (2011), 763–772.
33. [33] Sacca, B., Niemeyer, C.M., Functionalization of DNA nanostructures with proteins. Chem. Soc. Rev. 40 (2011), 5910–5921.
34. [34] Chen, Y.J., Groves, B., Muscat, R.A., Seelig, G., DNA nanotechnology from the test tube to the cell. Nat. Nanotechnol. 10 (2015), 748–760.
35. [35] Zhang, F., Nangreave, J., Liu, Y., Yan, H., Structural DNA nanotechnology: state of the art and future perspective. J. Am. Chem. Soc. 136 (2014), 11198–11211.
36. [36] Li, J., Fan, C., Pei, H., Shi, J., Huang, Q., Smart drug delivery nanocarriers with self-assembled DNA nanostructures. Adv. Mater. 25 (2013), 4386–4396.
37. [37] Chao, J., Liu, H., Su, S., Wang, L., Huang, W., Fan, C., Structural DNA nanotechnology for intelligent drug delivery. Small 10 (2014), 4626–4635.
38. [38] Yang, D., Hartman, M.R., Derrien, T.L., Hamada, S., An, D., Yancey, K.G., Cheng, R., Ma, M., Luo, D., DNA materials: bridging nanotechnology and biotechnology. Acc. Chem. Res. 47 (2014), 1902–1911.
39. [39] Duckett, D.R., Lilley, D.M.J., The 3-way DNA junction is a Y-Shaped molecule in which there is no helix helix stacking. EMBO J. 9 (1990), 1659–1664.
40. [40] Seeman, N.C., Nanotechnology and the double helix. Sci. Am. 290 (2004), 64–69 (72–65).
41. [41] Seeman, N.C., Nucleic acid junctions and lattices. J. Theor. Biol. 99 (1982), 237–247.
42. [42] Kallenbach, N.R., Ma, R.I., Seeman, N.C., An immobile nucleic-acid junction constructed from oligonucleotides. Nature 305 (1983), 829–831.
43. [43] Ma, R.I., Kallenbach, N.R., Sheardy, R.D., Petrillo, M.L., Seeman, N.C., Three-arm nucleic acid junctions are flexible. Nucleic Acids Res. 14 (1986), 9745–9753.
44. [44] Fu, T.J., Seeman, N.C., DNA double-crossover molecules. Biochemistry 32 (1993), 3211–3220.
45. [45] Winfree, E., Liu, F., Wenzler, L.A., Seeman, N.C., Design and self-assembly of two-dimensional DNA crystals. Nature 394 (1998), 539–544.
46. [46] Liu, D., Wang, M., Deng, Z., Walulu, R., Mao, C., Tensegrity: construction of rigid DNA triangles with flexible four-arm DNA junctions. J. Am. Chem. Soc. 126 (2004), 2324–2325.
47. [47] Yan, H., Park, S.H., Finkelstein, G., Reif, J.H., LaBean, T.H., DNA-templated self-assembly of protein arrays and highly conductive nanowires. Science 301 (2003), 1882–1884.
48. [48] Rothemund, P.W., Folding DNA to create nanoscale shapes and patterns. Nature 440 (2006), 297–302.
49. [49] Matthies, M., Agarwal, N.P., Schmidt, T.L., Design and synthesis of triangulated DNA origami trusses. Nano Lett. 16 (2016), 2108–2113.
50. [50] Selnihhin, D., Andersen, E.S., Computer-aided design of DNA origami structures. Methods Mol. Biol. 1244 (2015), 23–44.
51. [51] Kuzuya, A., Komiyama, M., Design and construction of a box-shaped 3D-DNA origami. Chem. Commun. (Camb.), 2009, 4182–4184.
52. [52] Goodman, R.P., Schaap, I.A., Tardin, C.F., Erben, C.M., Berry, R.M., Schmidt, C.F., Turberfield, A.J., Rapid chiral assembly of rigid DNA building blocks for molecular nanofabrication. Science 310 (2005), 1661–1665.
53. [53] Goodman, R.P., Berry, R.M., Turberfield, A.J., The single-step synthesis of a DNA tetrahedron. Chem. Commun. (Camb.), 2004, 1372–1373.
54. [54] Erben, C.M., Goodman, R.P., Turberfield, A.J., A self-assembled DNA bipyramid. J. Am. Chem. Soc. 129 (2007), 6992–6993.
55. [55] Ke, Y., Ong, L.L., Shih, W.M., Yin, P., Three-dimensional structures self-assembled from DNA bricks. Science 338 (2012), 1177–1183.
56. [56] Ke, Y., Ong, L.L., Sun, W., Song, J., Dong, M., Shih, W.M., Yin, P., DNA brick crystals with prescribed depths. Nat. Chem. 6 (2014), 994–1002.
57. [57] Goodman, R.P., Heilemann, M., Doose, S., Erben, C.M., Kapanidis, A.N., Turberfield, A.J., Reconfigurable, braced, three-dimensional DNA nanostructures. Nat. Nanotechnol. 3 (2008), 93–96.
58. [58] Stellwagen, N.C., Electrophoresis of DNA in agarose gels, polyacrylamide gels and in free solution. Electrophoresis 30:Suppl. 1 (2009), S188–S195.
59. [59] Bellot, G., McClintock, M.A., Lin, C., Shih, W.M., Recovery of intact DNA nanostructures after agarose gel-based separation. Nat. Methods 8 (2011), 192–194.
60. [60] Xing, S., Jiang, D., Li, F., Li, J., Li, Q., Huang, Q., Guo, L., Xia, J., Shi, J., Fan, C., Zhang, L., Wang, L., Constructing higher-order DNA nanoarchitectures with highly purified DNA nanocages. ACS Appl. Mater. Interfaces 7 (2015), 13174–13179.
61. [61] Lin, C., Perrault, S.D., Kwak, M., Graf, F., Shih, W.M., Purification of DNA-origami nanostructures by rate-zonal centrifugation. Nucleic Acids Res., 41, 2013, e40.
62. [62] Wei, X., Nangreave, J., Liu, Y., Uncovering the self-assembly of DNA nanostructures by thermodynamics and kinetics. Acc. Chem. Res. 47 (2014), 1861–1870.
63. [63] Shaw, A., Benson, E., Hogberg, B., Purification of functionalized DNA origami nanostructures. ACS Nano 9 (2015), 4968–4975.
64. [64] Schuller, 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 5 (2011), 9696–9702.
65. [65] Keum, J.W., Bermudez, H., Enhanced resistance of DNA nanostructures to enzymatic digestion. Chem. Commun. (Camb.), 2009, 7036–7038.
66. [66] 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 5 (2011), 8783–8789.
67. [67] Conway, J.W., McLaughlin, C.K., Castor, K.J., Sleiman, H., DNA nanostructure serum stability: greater than the sum of its parts. Chem. Commun. (Camb.) 49 (2013), 1172–1174.
68. [68] Hamblin, G.D., Carneiro, K.M., Fakhoury, J.F., Bujold, K.E., Sleiman, H.F., Rolling circle amplification-templated DNA nanotubes show increased stability and cell penetration ability. J. Am. Chem. Soc. 134 (2012), 2888–2891.
69. [69] Aldaye, F.A., Lo, P.K., Karam, P., McLaughlin, C.K., Cosa, G., Sleiman, H.F., Modular construction of DNA nanotubes of tunable geometry and single- or double-stranded character. Nat. Nanotechnol. 4 (2009), 349–352.
70. [70] 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. 11 (2011), 1477–1482.
71. [71] Hahn, J., Wickham, S.F., Shih, W.M., Perrault, S.D., Addressing the instability of DNA nanostructures in tissue culture. ACS Nano 8 (2014), 8765–8775.
72. [72] Wen, Y.L., Li, L.Y., Wang, L.L., Xu, L., Liang, W., Ren, S.Z., Liu, G., Biomedical applications of DNA-nanomaterials based on metallic nanoparticles and DNA self-assembled nanostructures. Chin. J. Chem. 34 (2016), 283–290.
73. [73] Yang, F., Zhang, X., Song, L., Cui, H., Myers, J.N., Bai, T., Zhou, Y., Chen, Z., Gu, N., Controlled drug release and hydrolysis mechanism of polymer-magnetic nanoparticle composite. ACS Appl. Mater. Interfaces 7 (2015), 9410–9419.
74. [74] Lee, H., Lytton-Jean, A.K., Chen, Y., Love, K.T., Park, A.I., Karagiannis, E.D., Sehgal, A., Querbes, W., Zurenko, C.S., Jayaraman, M., Peng, C.G., Charisse, K., Borodovsky, A., Manoharan, M., Donahoe, J.S., Truelove, J., Nahrendorf, M., Langer, R., Anderson, D.G., Molecularly self-assembled nucleic acid nanoparticles for targeted in vivo siRNA delivery. Nat. Nanotechnol. 7 (2012), 389–393.
75. [75] Kim, K.R., Lee, Y.D., Lee, T., Kim, B.S., Kim, S., Ahn, D.R., Sentinel lymph node imaging by a fluorescently labeled DNA tetrahedron. Biomaterials 34 (2013), 5226–5235.
76. [76] Jiang, D., Sun, Y., Li, J., Li, Q., Lv, M., Zhu, B., Tian, T., Cheng, D., Xia, J., Zhang, L., Wang, L., Huang, Q., Shi, J., Fan, C., Multiple-armed tetrahedral DNA nanostructures for tumor-targeting, dual-modality in vivo imaging. ACS Appl. Mater. Interfaces 8 (2016), 4378–4384.
77. [77] Kim, K.R., Bang, D., Ahn, D.R., Nano-formulation of a photosensitizer using a DNA tetrahedron and its potential for in vivo photodynamic therapy. Biomater. Sci. 4 (2016), 605–609.
78. [78] Bhatia, D., Surana, S., Chakraborty, S., Koushika, S.P., Krishnan, Y., A synthetic icosahedral DNA-based host-cargo complex for functional in vivo imaging. Nat. Commun., 2, 2011, 339.
79. [79] Perrault, S.D., Shih, W.M., Virus-inspired membrane encapsulation of DNA nanostructures to achieve in vivo stability. ACS Nano 8 (2014), 5132–5140.
80. [80] Zhang, Q., Jiang, Q., Li, N., Dai, L., Liu, Q., Song, L., Wang, J., Li, Y., Tian, J., Ding, B., Du, Y., DNA origami as an in vivo drug delivery vehicle for cancer therapy. ACS Nano 8 (2014), 6633–6643.
81. [81] Kobayashi, H., Watanabe, R., Choyke, P.L., Improving conventional enhanced permeability and retention (EPR) effects; what is the appropriate target?. Theranostics 4 (2013), 81–89.
82. [82] Jiang, Q., Shi, Y., Zhang, Q., Li, N., Zhan, P., Song, L., Dai, L., Tian, J., Du, Y., Cheng, Z., Ding, B., A Self-assembled DNA origami-gold nanorod complex for cancer theranostics. Small 11 (2015), 5134–5141.
83. [83] Liu, X., Xu, Y., Yu, T., Clifford, C., Liu, Y., Yan, H., Chang, Y., A DNA nanostructure platform for directed assembly of synthetic vaccines. Nano Lett. 12 (2012), 4254–4259.
84. [84] Mohri, K., Nishikawa, M., Takahashi, N., Shiomi, T., Matsuoka, N., Ogawa, K., Endo, M., Hidaka, K., Sugiyama, H., Takahashi, Y., Takakura, Y., Design and development of nanosized DNA assemblies in polypod-like structures as efficient vehicles for immunostimulatory CpG motifs to immune cells. ACS Nano 6 (2012), 5931–5940.
85. [85] Surana, S., Shenoy, A.R., Krishnan, Y., Designing DNA nanodevices for compatibility with the immune system of higher organisms. Nat. Nanotechnol. 10 (2015), 741–747.
86. [86] Ivashkiv, L.B., Donlin, L.T., Regulation of type I interferon responses. Nat. Rev. Immunol. 14 (2014), 36–49.
87. [87] Wu, J., Chen, Z.J., Innate immune sensing and signaling of cytosolic nucleic acids. Annu. Rev. Immunol. 32 (2014), 461–488.