Ultrasmall gold nanoparticles as carriers for nucleus-based gene therapy due to size-dependent nuclear entry

ACS Nano

Volumn 8, Issue 6, 2014, Pages 5852-5862

  Huo, Shuaidong ^a,b   Jin, Shubin ^a,b   Ma, Xiaowei ^a,b   Xue, Xiangdong ^a,b   Yang, Keni ^a   Kumar, Anil ^a   Wang, Paul C ^c   Zhang, Jinchao ^d   Hu, Zhongbo ^b   Liang, Xing Jie ^a  

^a NATIONAL CENTER FOR NANOSCIENCE AND TECHNOLOGY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c HOWARD UNIVERSITY   (United States)

^d HEBEI UNIVERSITY   (China)

Author keywords

cancer cell nucleus; cancer therapy; gene regulation; size dependent; ultrasmall gold nanoparticles

Indexed keywords

CELLS; CYTOLOGY; GENE EXPRESSION; METAL NANOPARTICLES; OLIGONUCLEOTIDES;

CANCER CELLS; CANCER THERAPY; GOLD NANOPARTICLES; INTRACELLULAR DISTRIBUTION; MCF-7 BREAST CANCER CELLS; PENETRATION ABILITY; SIZE DEPENDENT; TRIPLEX-FORMING OLIGONUCLEOTIDES;

GOLD;

GOLD; METAL NANOPARTICLE; MYC PROTEIN; OLIGONUCLEOTIDE; RNA;

BREAST NEOPLASMS; CELL NUCLEUS; CELL SURVIVAL; CHEMISTRY; CYTOPLASM; FEMALE; GENE EXPRESSION REGULATION; GENE THERAPY; GENE TRANSFER; GENE VECTOR; HUMAN; MCF 7 CELL LINE; METABOLISM; NANOTECHNOLOGY; PROCEDURES; PROMOTER REGION;

BREAST NEOPLASMS; CELL NUCLEUS; CELL SURVIVAL; CYTOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; GOLD; HUMANS; MCF-7 CELLS; METAL NANOPARTICLES; NANOTECHNOLOGY; OLIGONUCLEOTIDES; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-MYC; RNA;

EID: 84903438002     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn5008572     Document Type: Article

References (51)

1. Dreaden, E. C.; Alkilany, A. M.; Huang, X. H.; Murphy, C. J.; El-Sayed, M. A. The Golden Age: Gold Nanoparticles for Biomedicine Chem. Soc. Rev. 2012, 41, 2740-2779
2. Ghosh, P.; Han, G.; De, M.; Kim, C. K.; Rotello, V. M. Gold Nanoparticles in Delivery Applications Adv. Drug Delivery Rev. 2008, 60, 1307-1315
3. Pissuwan, D.; Niidome, T.; Cortie, M. B. The Forthcoming Applications of Gold Nanoparticles in Drug and Gene Delivery Systems J. Controlled Release 2011, 149, 65-71
4. 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
5. Huang, K. Y.; Ma, H. L.; Liu, J.; Huo, S. D.; Kumar, A.; Wei, T.; Zhang, X.; Jin, S. B.; Gan, Y. L.; Wang, P. C. et al. Size-Dependent Localization and Penetration of Ultrasmall Gold Nanoparticles in Cancer Cells, Multicellular Spheroids, and Tumors in Vivo ACS Nano 2012, 6, 4483-4493
6. De Jong, W. H.; Hagens, W. I.; Krystek, P.; Burger, M. C.; Sips, A. J. A. M.; Geertsma, R. E. Particle Size-Dependent Organ Distribution of Gold Nanoparticles after Intravenous Administration Biomaterials 2008, 29, 1912-1919
7. Pan, Y.; Neuss, S.; Leifert, A.; Fischler, M.; Wen, F.; Simon, U.; Schmid, G.; Brandau, W.; Jahnen-Dechent, W. Size-Dependent Cytotoxicity of Gold Nanoparticles Small 2007, 3, 1941-1949 (Pubitemid 350099867)
8. Zhang, X. D.; Wu, D.; Shen, X.; Chen, J.; Sun, Y. M.; Liu, P. X.; Liang, X. J. Size-Dependent Radiosensitization of PEG-Coated Gold Nanoparticles for Cancer Radiation Therapy Biomaterials 2012, 33, 6408-6419
9. Lesniak, A.; Salvati, A.; Santos-Martinez, M. J.; Radomski, M. W.; Dawson, K. A.; Aberg, C. Nanoparticle Adhesion to the Cell Membrane and Its Effect on Nanoparticle Uptake Efficiency J. Am. Chem. Soc. 2013, 135, 1438-1444
10. Jiang, W.; Kim, B. Y. S.; Rutka, J. T.; Chan, W. C. W. Nanoparticle-Mediated Cellular Response Is Size-Dependent Nat. Nanotechnol. 2008, 3, 145-150 (Pubitemid 351355131)
11. Zhu, M. T.; Li, Y. Y.; Shi, J.; Feng, W. Y.; Nie, G. J.; Zhao, Y. L. Exosomes as Extrapulmonary Signaling Conveyors for Nanoparticle-Induced Systemic Immune Activation Small 2012, 8, 404-412
12. Huo, S. D.; Ma, H. L.; Huang, K. Y.; Liu, J.; Wei, T.; Jin, S. B.; Zhang, J. C.; He, S. T.; Liang, X. J. Superior Penetration and Retention Behavior of 50 nm Gold Nanoparticles in Tumors Cancer Res. 2013, 73, 319-330
13. Chauhan, V. P.; Popovic, Z.; Chen, O.; Cui, J.; Fukumura, D.; Bawendi, M. G.; Jain, R. K. Fluorescent Nanorods and Nanospheres for Real-Time In Vivo Probing of Nanoparticle Shape-Dependent Tumor Penetration Angew. Chem., Int. Ed. 2011, 50, 11417-11420
14. Kim, B.; Han, G.; Toley, B. J.; Kim, C.-k.; Rotello, V. M.; Forbes, N. S. Tuning Payload Delivery in Tumour Cylindroids Using Gold Nanoparticles Nat. Nanotechnol. 2010, 5, 465-472
15. Perrault, S. D.; Walkey, C.; Jennings, T.; Fischer, H. C.; Chan, W. C. Mediating Tumor Targeting Efficiency of Nanoparticles through Design Nano Lett. 2009, 9, 1909-1915
16. Chithrani, B. D.; Ghazani, A. A.; Chan, W. C. W. Determining the Size and Shape Dependence of Gold Nanoparticle Uptake into Mammalian Cells Nano Lett. 2006, 6, 662-668
17. Chen, J.; Saeki, F.; Wiley, B. J.; Cang, H.; Cobb, M. J.; Li, Z.-Y.; Au, L.; Zhang, H.; Kimmey, M. B.; Li, X. et al. Gold Nanocages: Bioconjugation and Their Potential Use as Optical Imaging Contrast Agents Nano Lett. 2005, 5, 473-477 (Pubitemid 40449718)
18. Hirsch, L. R.; Stafford, R. J.; Bankson, J. A.; Sershen, S. R.; Rivera, B.; Price, R. E.; Hazle, J. D.; Halas, N. J.; West, J. L. Nanoshell-Mediated Near-Infrared Thermal Therapy of Tumors under Magnetic Resonance Guidance Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 13549-13554 (Pubitemid 37444779)
19. Dykman, L.; Khlebtsov, N. Gold Nanoparticles in Biomedical Applications: Recent Advances and Perspectives Chem. Soc. Rev. 2012, 41, 2256-2282
20. Dam, D. H. M.; Lee, J. H.; Sisco, P. N.; Co, D. T.; Zhang, M.; Wasielewski, M. R.; Odom, T. W. Direct Observation of Nanoparticle-Cancer Cell Nucleus Interactions ACS Nano 2012, 6, 3318-3326
21. Kang, B.; Mackey, M. A.; El-Sayed, M. A. Nuclear Targeting of Gold Nanoparticles in Cancer Cells Induces DNA Damage, Causing Cytokinesis Arrest and Apoptosis J. Am. Chem. Soc. 2010, 132, 1517-1519
22. Dobson, J. Gene Therapy Progress and Prospects: Magnetic Nanoparticle-Based Gene Delivery Gene Ther. 2006, 13, 283-287 (Pubitemid 43223096)
23. Patil, S. D.; Rhodes, D. G.; Burgess, D. J. DNA-Based Therapeutics and DNA Delivery Systems: A Comprehensive Review AAPS J. 2005, 7, E61-E77 (Pubitemid 41554297)
24. McManus, M. T.; Sharp, P. A. Gene Silencing in Mammals by Small Interfering RNAs Nat. Rev. Genet. 2002, 3, 737-747
25. Lebedeva, I.; Stein, C. A. Antisense Oligonucleotides: Promise and Reality Annu. Rev. Pharmacol. 2001, 41, 403-419 (Pubitemid 32385893)
26. Jason, T. L. H.; Koropatnick, J.; Berg, R. W. Toxicology of Antisense Therapeutics Toxicol. Appl. Pharmacol. 2004, 201, 66-83 (Pubitemid 39446327)
27. Rosi, N. L.; Giljohann, D. A.; Thaxton, C. S.; Lytton-Jean, A. K. R.; Han, M. S.; Mirkin, C. A. Oligonucleotide-Modified Gold Nanoparticles for Intracellular Gene Regulation Science 2006, 312, 1027-1030
28. Jin, R. C.; Wu, G. S.; Li, Z.; Mirkin, C. A.; Schatz, G. C. What Controls the Melting Properties of DNA-Linked Gold Nanoparticle Assemblies? J. Am. Chem. Soc. 2003, 125, 1643-1654 (Pubitemid 36206246)
29. Lytton-Jean, A. K. R.; Mirkin, C. A. A Thermodynamic Investigation into the Binding Properties of DNA Functionalized Gold Nanoparticle Probes and Molecular Fluorophore Probes J. Am. Chem. Soc. 2005, 127, 12754-12755 (Pubitemid 41339136)
30. Goldsborough, A. S.; Handley, M. D.; Dulcey, A. E.; Pluchino, K. M.; Kannan, P.; Brimacombe, K. R.; Hall, M. D.; Griffiths, G.; Gottesman, M. M. Collateral Sensitivity of Multidrug-Resistant Cells to the Orphan Drug Tiopronin J. Med. Chem. 2011, 54, 4987-4997
31. Dahl, J. A.; Maddux, B. L. S.; Hutchison, J. E. Toward Greener Nanosynthesis Chem. Rev. 2007, 107, 2228-2269 (Pubitemid 47029093)
32. Petkov, V.; Peng, Y.; Williams, G.; Huang, B. H.; Tomalia, D.; Ren, Y. Structure of Gold Nanoparticles Suspended in Water Studied by X-ray Diffraction and Computer Simulations Phys. Rev. B 2005, 72, 195402
33. Li, Z. P.; Duan, X. R.; Liu, C. H.; Du, B. A. Selective Determination of Cysteine by Resonance Light Scattering Technique Based on Self-Assembly of Gold Nanoparticles Anal. Biochem. 2006, 351, 18-25
34. Albanese, A.; Chan, W. C. W. Effect of Gold Nanoparticle Aggregation on Cell Uptake and Toxicity ACS Nano 2011, 5, 5478-5489
35. Ao, L. M.; Gao, F.; Pan, B. F.; He, R.; Cui, D. X. Fluoroimmunoassay for Antigen Based on Fluorescence Quenching Signal of Gold Nanoparticles Anal. Chem. 2006, 78, 1104-1106 (Pubitemid 43271839)
36. Loumaigne, M.; Praho, R.; Nutarelli, D.; Werts, M. H. V.; Debarre, A. Fluorescence Correlation Spectroscopy Reveals Strong Fluorescence Quenching of FITC Adducts on PEGylated Gold Nanoparticles in Water and the Presence of Fluorescent Aggregates of Desorbed Thiolate Ligands Phys. Chem. Chem. Phys. 2010, 12, 11004-11014
37. Foss, C. A.; Hornyak, G. L.; Stockert, J. A.; Martin, C. R. Template-Synthesized Nanoscopic Gold Particles-Optical-Spectra and the Effects of Particle-Size and Shape J. Phys. Chem. 1994, 98, 2963-2971
38. Paine, P. L.; Moore, L. C.; Horowitz, S. B. Nuclear-Envelope Permeability Nature 1975, 254, 109-114
39. Jain, A.; Magistri, M.; Napoli, S.; Carbone, G. M.; Catapano, C. V. Mechanisms of Triplex DNA-Mediated Inhibition of Transcription Initiation in Cells Biochimie 2010, 92, 317-320
40. Seferos, D. S.; Prigodich, A. E.; Giljohann, D. A.; Patel, P. C.; Mirkin, C. A. Polyvalent DNA Nanoparticle Conjugates Stabilize Nucleic Acids Nano Lett. 2009, 9, 308-311
41. Han, G.; Martin, C. T.; Rotello, V. M. Stability of Gold Nanoparticle-Bound DNA toward Biological, Physical, and Chemical Agents Chem. Biol. Drug Des. 2006, 67, 78-82 (Pubitemid 43881390)
42. McGuffie, E. M.; Pacheco, D.; Carbone, G. M. R.; Catapano, C. V. Antigene and Antiproliferative Effects of a c-Myc-Targeting Phosphorothioate Triple Helix-Forming Oligonucleotide in Human Leukemia Cells Cancer Res. 2000, 60, 3790-3799 (Pubitemid 32204570)
43. Dang, C. V. c-Myc Target Genes Involved in Cell Growth, Apoptosis, and Metabolism Mol. Cell. Biol. 1999, 19, 1-11 (Pubitemid 29018404)
44. Leifert, A.; Pan, Y.; Kinkeldey, A.; Schiefer, F.; Setzler, J.; Scheel, O.; Lichtenbeld, H.; Schmid, G.; Wenzel, W.; Jahnen-Dechent, W. et al. Differential hERG Ion Channel Activity of Ultrasmall Gold Nanoparticles Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 8004-8009
45. Guntaka, R. V.; Varma, B. R.; Weber, K. T. Triplex-Forming Oligonucleotides as Modulators of Gene Expression Int. J. Biochem. Cell Biol. 2003, 35, 22-31 (Pubitemid 35449170)
46. Rogers, F. A.; Manoharan, M.; Rabinovitch, P.; Ward, D. C.; Glazer, P. M. Peptide Conjugates for Chromosomal Gene Targeting by Triplex-Forming Oligonucleotides Nucleic Acids Res. 2004, 32, 6595-6604 (Pubitemid 40220371)
47. Harris, J. D.; Lemoine, N. R. Strategies for Targeted Gene Therapy Trends Genet. 1996, 12, 400-405 (Pubitemid 26336482)
48. Stein, C. A.; Cheng, Y. C. Antisense Oligonucleotides as Therapeutic Agents: Is the Bullet Really Magical Science 1993, 261, 1004-1012 (Pubitemid 23300859)
49. Felgner, J. H.; Kumar, R.; Sridhar, C. N.; Wheeler, C. J.; Tsai, Y. J.; Border, R.; Ramsey, P.; Martin, M.; Felgner, P. L. Enhanced Gene Delivery and Mechanism Studies with a Novel Series of Cationic Lipid Formulations J. Biol. Chem. 1994, 269, 2550-2561 (Pubitemid 24235749)
50. Lewis, J. G.; Lin, K. Y.; Kothavale, A.; Flanagan, W. M.; Matteucci, M. D.; DePrince, R. B.; Mook, R. A.; Hendren, R. W.; Wagner, R. W. A Serum-Resistant Cytofectin for Cellular Delivery of Antisense Oligodeoxynucleotides and Plasmid DNA Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 3176-3181 (Pubitemid 26127586)
51. Wing, R.; Drew, H.; Takano, T.; Broka, C.; Tanaka, S.; Itakura, K.; Dickerson, R. E. Crystal-Structure Analysis of a Complete Turn of B-DNA Nature 1980, 287, 755-758