Multiple-Armed Tetrahedral DNA Nanostructures for Tumor-Targeting, Dual-Modality in Vivo Imaging

ACS Applied Materials and Interfaces

Volumn 8, Issue 7, 2016, Pages 4378-4384

  Jiang, Dawei ^a   Sun, Yanhong ^a   Li, Jiang ^a   Li, Qian ^a   Lv, Min ^a   Zhu, Bing ^a   Tian, Tian ^a   Cheng, Dengfeng ^b   Xia, Jiaoyun ^c   Zhang, Lan ^a   Wang, Lihua ^a   Huang, Qing ^a   Shi, Jiye ^d   Fan, Chunhai ^a  

^a SHANGHAI INSTITUTE OF APPLIED PHYSICS   (China)

^b FUDAN UNIVERSITY   (China)

^c CHANGSHA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^d UCB PHARMA   (Belgium)

Author keywords

dual modality imaging; near infrared fluorescence; single photon emission computed tomography; tetrahedral DNA nanostructures; tumor targeting

Indexed keywords

COMPUTERIZED TOMOGRAPHY; DNA; FLUORESCENCE; INFRARED DEVICES; MAMMALS; NANOSTRUCTURES; PARTICLE BEAMS; PHOTONS; TECHNETIUM; TOMOGRAPHY; TUMORS;

CIRCULATION TIME; DNA NANOSTRUCTURES; DOUBLE STRANDED (DS) DNA; DUAL-MODALITY IMAGING; NEAR-INFRARED FLUORESCENCE; NIR FLUORESCENCE IMAGING; TARGETED IMAGING; TUMOR TARGETING;

SINGLE PHOTON EMISSION COMPUTED TOMOGRAPHY;

DNA; FOLIC ACID; NANOMATERIAL;

ANIMAL; CHEMISTRY; DIAGNOSTIC IMAGING; DRUG SCREENING; FLUORESCENCE; HUMAN; MOUSE; NEAR INFRARED SPECTROSCOPY; NEOPLASM; PATHOLOGY; PROCEDURES; SINGLE PHOTON EMISSION COMPUTED TOMOGRAPHY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; DNA; FLUORESCENCE; FOLIC ACID; HUMANS; MICE; NANOSTRUCTURES; NEOPLASMS; SPECTROSCOPY, NEAR-INFRARED; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84962487331     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b10792     Document Type: Article

References (50)

1. Rudin, M.; Weissleder, R. Molecular Imaging in Drug Discovery and Development Nat. Rev. Drug Discovery 2003, 2, 123-131 10.1038/nrd1007
2. Willmann, J. K.; van Bruggen, N.; Dinkelborg, L. M.; Gambhir, S. S. Molecular Imaging in Drug Development Nat. Rev. Drug Discovery 2008, 7, 591-607 10.1038/nrd2290
3. Hussain, T.; Nguyen, Q. T. Molecular Imaging for Cancer Diagnosis and Surgery Adv. Drug Delivery Rev. 2014, 66, 90-100 10.1016/j.addr.2013.09.007
4. Herschman, H. R. Molecular Imaging: Looking at Problems, Seeing Solutions Science 2003, 302, 605-608 10.1126/science.1090585
5. Mulder, W. J.; Castermans, K.; van Beijnum, J. R.; Oude Egbrink, M. G.; Chin, P. T.; Fayad, Z. A.; Lowik, C. W.; Kaijzel, E. L.; Que, I.; Storm, G.; Strijkers, G. J.; Griffioen, A. W.; Nicolay, K. Molecular Imaging of Tumor Angiogenesis Using Alpha v Beta 3-integrin Targeted Multimodal Quantum Dots Angiogenesis 2009, 12, 17-24 10.1007/s10456-008-9124-2
6. Massoud, T. F.; Gambhir, S. S. Molecular Imaging in Living Subjects: Seeing Fundamental Biological Processes in a New Light Genes Dev. 2003, 17, 545-580 10.1101/gad.1047403
7. Frangioni, J. V. In Vivo Near-infrared Fluorescence Imaging Curr. Opin. Chem. Biol. 2003, 7, 626-634 10.1016/j.cbpa.2003.08.007
8. Gambhir, S. S. Molecular Imaging of Cancer with Positron Emission Tomography Nat. Rev. Cancer 2002, 2, 683-693 10.1038/nrc882
9. Sharma, V.; Luker, G. D.; Piwnica-Worms, D. Molecular Imaging of Gene Expression and Protein Function in Vivo with PET and SPECT J. Magn. Reson. Imaging 2002, 16, 336-351 10.1002/jmri.10182
10. Culver, J.; Akers, W.; Achilefu, S. Multimodality Molecular Imaging with Combined Optical and SPECT/PET Modalities J. Nucl. Med. 2008, 49, 169-172 10.2967/jnumed.107.043331
11. Louie, A. Y. Multimodality Imaging Probes: Design and Challenges Chem. Rev. 2010, 110, 3146-3195 10.1021/cr9003538
12. Swierczewska, M.; Lee, S.; Chen, X. Y. Inorganic Nanoparticles for Multimodal Molecular Imaging Mol. Imaging 2011, 10, 3-16
13. Huang, H. C.; Barua, S.; Sharma, G.; Dey, S. K.; Rege, K. Inorganic nanoparticles for cancer imaging and therapy J. Controlled Release 2011, 155, 344-357 10.1016/j.jconrel.2011.06.004
14. Gao, X.; Cui, Y.; Levenson, R. M.; Chung, L. W.; Nie, S. In Vivo Cancer Targeting and Imaging with Semiconductor Quantum Dots Nat. Biotechnol. 2004, 22, 969-976 10.1038/nbt994
15. Smith, A. M.; Duan, H.; Mohs, A. M.; Nie, S. Bioconjugated Quantum Dots for in Vivo Molecular and Cellular Imaging Adv. Drug Delivery Rev. 2008, 60, 1226-1240 10.1016/j.addr.2008.03.015
16. 64Cu]CuInS/ZnS Quantum Dots for PET and Optical Imaging: Improved Radiochemical Stability and Controllable Cerenkov Luminescence ACS Nano 2015, 9, 488-495 10.1021/nn505660r
17. Cai, W.; Chen, K.; Li, Z. B.; Gambhir, S. S.; Chen, X. Dual-function Probe for PET and Near-infrared Fluorescence Imaging of Tumor Vasculature J. Nucl. Med. 2007, 48, 1862-1870 10.2967/jnumed.107.043216
18. Bag, N.; Mathur, R.; Singh, S.; Hussain, F.; Chauhan, R. P.; Chuttani, K.; Mishra, A. K. Design, Synthesis and Evaluation of the QD-DTC-bisbiotin Nanobioconjugate as a Potential Optical-SPECT Imaging Agent MedChemComm 2015, 6, 363-371 10.1039/C4MD00294F
19. Wang, J. T. W.; Cabana, L.; Bourgognon, M.; Kafa, H.; Protti, A.; Venner, K.; Shah, A. M.; Sosabowski, J. K.; Mather, S. J.; Roig, A. et al. Magnetically Decorated Multiwalled Carbon Nanotubes as Dual MRI and SPECT Contrast Agents Adv. Funct. Mater. 2014, 24, 1880-1894 10.1002/adfm.201302892
20. Hong, H.; Yang, K.; Zhang, Y.; Engle, J. W.; Feng, L. Z.; Yang, Y. A.; Nayak, T. R.; Goel, S.; Bean, J.; Theuer, C. P.; Barnhart, T. E.; Liu, Z.; Cai, W. B. In Vivo Targeting and Imaging of Tumor Vasculature with Radiolabeled, Antibody-Conjugated Nanographene ACS Nano 2012, 6, 2361-2370 10.1021/nn204625e
21. Ghosh, D.; Bagley, A. F.; Na, Y. J.; Birrer, M. J.; Bhatia, S. N.; Belcher, A. M. Deep, Noninvasive Imaging and Surgical Guidance of Submillimeter Tumors Using Targeted M13-stabilized Single-walled Carbon Nanotubes Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 13948-13953 10.1073/pnas.1400821111
22. Dreaden, E. C.; Mackey, M. A.; Huang, X. H.; Kang, B.; El-Sayed, M. A. Beating Cancer in Multiple Ways Using Nanogold Chem. Soc. Rev. 2011, 40, 3391-3404 10.1039/c0cs00180e
23. Park, K.; Lee, S.; Kang, E.; Kim, K.; Choi, K.; Kwon, I. C. New Generation of Multifunctional Nanoparticles for Cancer Imaging and Therapy Adv. Funct. Mater. 2009, 19, 1553-1566 10.1002/adfm.200801655
24. Kim, J.; Piao, Y.; Hyeon, T. Multifunctional Nanostructured Materials for Multimodal Imaging, and Simultaneous Imaging and Therapy Chem. Soc. Rev. 2009, 38, 372-390 10.1039/B709883A
25. Yang, Z.; Zheng, S.; Harrison, W. J.; Harder, J.; Wen, X.; Gelovani, J. G.; Qiao, A.; Li, C. Long-circulating Near-infrared Fluorescence Core-Cross-linked Polymeric Micelles: Synthesis, Characterization, and Dual Nuclear/optical Imaging Biomacromolecules 2007, 8, 3422-3428 10.1021/bm7005399
26. Peer, D.; Karp, J. M.; Hong, S.; FarokHzad, O. C.; Margalit, R.; Langer, R. Nanocarriers as an Emerging Platform for Cancer Therapy Nat. Nanotechnol. 2007, 2, 751-760 10.1038/nnano.2007.387
27. Criscione, J. M.; Dobrucki, L. W.; Zhuang, Z. W.; Papademetris, X.; Simons, M.; Sinusas, A. J.; Fahmy, T. M. Development And Application Of A Multimodal Contrast Agent For Spect/Ct Hybrid Imaging Bioconjugate Chem. 2011, 22, 1784-1792 10.1021/bc200162r
28. Zhang, Y.; Sun, Y.; Xu, X.; Zhu, H.; Huang, L.; Zhang, X.; Qi, Y.; Shen, Y. Radiosynthesis and Micro-SPECT Imaging of Tc-99m-dendrimer Poly(amido)-amine Folic Acid Conjugate Bioorg. Med. Chem. Lett. 2010, 20, 927-931 10.1016/j.bmcl.2009.12.075
29. Lee, D. E.; Koo, H.; Sun, I. C.; Ryu, J. H.; Kim, K.; Kwon, I. C. Multifunctional Nanoparticles for Multimodal Imaging and Theragnosis Chem. Soc. Rev. 2012, 41, 2656-2672 10.1039/C2CS15261D
30. van Anders, G.; Glotzer, S. C. DNA Nanotechnology: The World's Smallest Assembly Line Nat. Chem. 2012, 4, 79-80 10.1038/nchem.1251
31. 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. 2014, 47, 1902-1911 10.1021/ar5001082
32. Ge, Z. L.; Fan, C. H.; Yan, H. Research Progress and Applications of Self-assembled DNA Nanostructures Kexue Tongbao 2014, 59, 146-157 10.1360/972013-307
33. Zhang, Q.; Jiang, Q.; Li, N.; Dai, L. R.; Liu, Q.; Song, L. L.; Wang, J. Y.; Li, Y. Q.; Tian, J.; Ding, B. Q.; Du, Y. DNA Origami as an in Vivo Drug Delivery Vehicle for Cancer Therapy ACS Nano 2014, 8, 6633-6643 10.1021/nn502058j
34. Perrault, S. D.; Shih, W. M. Virus-Inspired Membrane Encapsulation of DNA Nanostructures To Achieve in Vivo Stability ACS Nano 2014, 8, 5132-5140 10.1021/nn5011914
35. Goodman, R. P.; Berry, R. M.; Turberfield, A. J. The Single-step Synthesis of a DNA Tetrahedron Chem. Commun. 2004, 12, 1372-1373 10.1039/b402293a
36. Erben, C. M.; Goodman, R. P.; Turberfield, A. J. Single-Molecule Protein Encapsulation in a Rigid DNA Cage Angew. Chem., Int. Ed. 2006, 45, 7414-7417 10.1002/anie.200603392
37. Charoenphol, P.; Bermudez, H. Aptamer-Targeted DNA Nanostructures for Therapeutic Delivery Mol. Pharmaceutics 2014, 11, 1721-1725 10.1021/mp500047b
38. Walsh, A. S.; Yin, H.; Erben, C. M.; Wood, M. J.; Turberfield, A. J. DNA Cage Delivery to Mammalian Cells ACS Nano 2011, 5, 5427-5432 10.1021/nn2005574
39. 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 10.1021/nn202774x
40. Li, J.; Fan, C.; Pei, H.; Shi, J.; Huang, Q. Smart Drug Delivery Nanocarriers with Self-Assembled DNA Nanostructures Adv. Mater. 2013, 25, 4386-4396 10.1002/adma.201300875
41. Keum, J. W.; Bermudez, H. Enhanced Resistance of DNA Nanostructures to Enzymatic Digestion Chem. Commun. 2009, 45, 7036-7038 10.1039/b917661f
42. Conway, J. W.; McLaughlin, C. K.; Castor, K. J.; Sleiman, H. DNA Nanostructure Serum Stability: Greater than the Sum of Its Parts Chem. Commun. 2013, 49, 1172-1174 10.1039/c2cc37556g
43. Sacca, B.; Niemeyer, C. M. Functionalization of DNA Nanostructures with Proteins Chem. Soc. Rev. 2011, 40, 5910-5921 10.1039/c1cs15212b
44. 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. 2012, 7, 389-393 10.1038/nnano.2012.73
45. 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 2013, 34, 5226-5235 10.1016/j.biomaterials.2013.03.074
46. Longmire, M.; Choyke, P. L.; Kobayashi, H. Clearance Properties of Nano-Sized Particles and Molecules as Imaging Agents: Considerations and Caveats Nanomedicine 2008, 3, 703-717 10.2217/17435889.3.5.703
47. 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 2015, 7, 13174-13179 10.1021/am505592e
48. Bramsen, J. B.; Laursen, M. B.; Nielsen, A. F.; Hansen, T. B.; Bus, C.; Langkjaer, N.; Babu, B. R.; Hojland, T.; Abramov, M.; Van Aerschot, A.; Odadzic, D.; Smicius, R.; Haas, J.; Andree, C.; Barman, J.; Wenska, M.; Srivastava, P.; Zhou, C. Z.; Honcharenko, D.; Hess, S.; Muller, E.; Bobkov, G. V.; Mikhailov, S. N.; Fava, E.; Meyer, T. F.; Chattopadhyaya, J.; Zerial, M.; Engels, J. W.; Herdewijn, P.; Wengel, J.; Kjems, J. A Large-scale Chemical Modification Screen Identifies Design Rules to Generate SiRNAs with high Activity, High Stability and Low Toxicity Nucleic Acids Res. 2009, 37, 2867-2881 10.1093/nar/gkp106
49. Ross, T. L.; Honer, M.; Muller, C.; Groehn, V.; Schibli, R.; Ametamey, S. M. A New 18F-labeled Folic acid Derivative with Improved Properties for the PET Imaging of Folate Receptor-positive Tumors J. Nucl. Med. 2010, 51, 1756-1762 10.2967/jnumed.110.079756
50. Zhang, Y. Q.; Xu, X. P.; Wang, L.; Lin, J.; Zhu, Y.; Guo, Z.; Sun, Y. H.; Wang, H.; Zhao, Y.; Tai, R. Z.; Yu, X. H.; Fan, C. H.; Huang, Q. Dendrimer-folate-copper Conjugates as Bioprobes for Synchrotron X-ray Fluorescence Imaging Chem. Commun. 2013, 49, 10388-10390 10.1039/c3cc46057f