Cellular delivery and photochemical activation of antisense agents through a nucleobase caging strategy

ACS Chemical Biology

Volumn 8, Issue 10, 2013, Pages 2272-2282

  Govan, Jeane M ^a   Uprety, Rajendra ^a   Thomas, Meryl ^a   Lusic, Hrvoje ^a   Lively, Mark O ^b   Deiters, Alexander ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; FOLATE RECEPTOR; FOLIC ACID; TRANSACTIVATOR PROTEIN;

ARTICLE; DRUG ACTIVITY; DRUG CONJUGATION; DRUG DELIVERY SYSTEM; GENE EXPRESSION; HUMAN IMMUNODEFICIENCY VIRUS; NONHUMAN; PHOTOCHEMISTRY; PRIORITY JOURNAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; GENE TRANSFER; GENETICS; HELA CELL LINE; HUMAN; LIGHT; METABOLISM; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION;

BASE SEQUENCE; GENE TRANSFER TECHNIQUES; HELA CELLS; HUMANS; LIGHT; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE; OLIGONUCLEOTIDES, ANTISENSE; POLYMERASE CHAIN REACTION; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84886501627     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400293e     Document Type: Article

References (74)

1. Tupler, R., Perini, G., Pellegrino, M. A., and Green, M. R. (1999) Profound misregulation of muscle-specific gene expression in facioscapulohumeral muscular dystrophy Proc. Natl. Acad. Sci. U.S.A. 96, 12650-12654
2. Waterfall, J. J. and Meltzer, P. S. (2012) Targeting epigenetic misregulation in synovial sarcoma Cancer Cell 21, 323-324
3. Buée, L., Bussière, T., Buée-Scherrer, V., Delacourte, A., and Hof, P. R. (2000) Tau protein isoforms, phosphorylation, and role in neurodegenerative disorders Brain Res. Brain Res. Rev. 33, 95-130
4. Tian Wang, Q. (2012) Epigenetic regulation of cardiac development and function by polycomb group and trithorax group proteins Dev. Dyn. 241, 1021-1033
5. Deleavey, G. F. and Damha, M. J. (2012) Designing chemically modified oligonucleotides for targeted gene silencing Chem. Biol. 19, 937-954
6. Brennan, P., Donev, R., and Hewamana, S. (2008) Targeting transcription factors for therapeutic benefit Mol. Biosyst. 4, 909-919
7. Jain, A., Wang, G., and Vasquez, K. M. (2008) DNA triple helices: Biological consequences and therapeutic potential Biochimie 90, 1117-1130
8. Heitz, F., Morris, M. C., and Divita, G. (2009) Twenty years of cell-penetrating peptides: From molecular mechanisms to therapeutics Br. J. Pharmacol. 157, 195-206
9. Milletti, F. (2012) Cell-penetrating peptides: Classes, origin, and current landscape Drug Discov. Today. 15, 850-860
10. Schmidt, N., Mishra, A., Lai, G. H., and Wong, G. C. (2010) Arginine-rich cell-penetrating peptides FEBS Lett. 584, 1806-1813
11. Mann, A., Thakur, G., Shukla, V., Singh, A. K., Khanduri, R., Naik, R., Jiang, Y., Kalra, N., Dwarakanath, B. S., Langel, U., and Ganguli, M. (2011) Differences in DNA condensation and release by lysine and arginine homopeptides govern their DNA delivery efficiencies Mol. Pharm. 8, 1729-1741
12. Turner, J. J., Jones, S., Fabani, M. M., Ivanova, G., Arzumanov, A. A., and Gait, M. J. (2007) RNA targeting with peptide conjugates of oligonucleotides, siRNA, and PNA Blood Cells Mol. Dis. 38, 1-7
13. El-Andaloussi, S., Johansson, H. J., Holm, T., and Langel, U. (2007) A novel cell-penetrating peptide, M918, for efficient delivery of proteins and peptide nucleic acids Mol. Ther. 15, 1820-1826
14. Madani, F., Lindberg, S., Langel, U., Futaki, S., and Gräslund, A. (2011) Mechanisms of cellular uptake of cell-penetrating peptides J. Biophys. 2011, 414729
15. Juliano, R., Alam, M. R., Dixit, V., and Kang, H. (2008) Mechanisms and strategies for effective delivery of antisense and siRNA oligonucleotides Nucleic Acids Res. 36, 4158-4171
16. Chiu, Y. L., Ali, A., Chu, C. Y., Cao, H., and Rana, T. M. (2004) Visualizing a correlation between siRNA localization, cellular uptake, and RNAi in living cells Chem. Biol. 11, 1165-1175
17. Deiters, A. (2009) Light activation as a method of regulating and studying gene expression Curr. Opin. Chem. Biol. 13, 678-686
18. Young, D. D. and Deiters, A. (2007) Photochemical control of biological processes Org. Biomol. Chem. 5, 999-1005
19. Deiters, A. (2010) Principles and applications of the photochemical control of cellular processes ChemBioChem 11, 47-53
20. Riggsbee, C. W. and Deiters, A. (2010) Recent advances in the photochemical control of protein function Trends Biotechnol. 28, 468-475
21. Dmochowski, I. J. and Tang, X. J. (2007) Taking control of gene expression with light-activated oligonucleotides Biotechniques 43, 161-163
22. Mayer, G. and Heckel, A. (2006) Biologically active molecules with a "light switch" Angew. Chem., Int. Ed. 45, 4900-4921
23. Young, D., Lively, M., and Deiters, A. (2010) Activation and deactivation of DNAzyme and antisense function with light for the photochemical regulation of gene expression in mammalian cells J. Am. Chem. Soc. 132, 6183-6193
24. Young, D. D., Lusic, H., Lively, M. O., Yoder, J. A., and Deiters, A. (2008) Gene silencing in mammalian cells with light-activated antisense agents Chembiochem 9, 2937-2940
25. Tang, X., Swaminathan, J., Gewirtz, A. M., and Dmochowski, I. J. (2008) Regulating gene expression in human leukemia cells using light-activated oligodeoxynucleotides Nucleic Acids Res. 36, 559-569
26. Deiters, A., Garner, R. A., Lusic, H., Govan, J. M., Dush, M., Nascone-Yoder, N. M., and Yoder, J. A. (2010) Photocaged morpholino oligomers for the light-regulation of gene function in zebrafish and xenopus embryos J. Am. Chem. Soc. 132, 15644-15650
27. Ouyang, X., Shestopalov, I. A., Sinha, S., Zheng, G., Pitt, C. L., Li, W. H., Olson, A. J., and Chen, J. K. (2009) Versatile synthesis and rational design of caged morpholinos J. Am. Chem. Soc. 131, 13255-13269
28. Govan, J. M., Lively, M. O., and Deiters, A. (2011) Photochemical control of DNA decoy function enables precise regulation of nuclear factor κB activity J. Am. Chem. Soc. 133, 13176-13182
29. Govan, J. M., Uprety, R., Hemphill, J., Lively, M. O., and Deiters, A. (2012) Regulation of transcription through light-activation and light-deactivation of triplex-forming oligonucleotides in mammalian cells ACS Chem. Biol. 7, 1247-1256
30. Mikat, V. and Heckel, A. (2007) Light-dependent RNA interference with nucleobase-caged siRNAs RNA 13, 2341-2347
31. Jain, P. K., Shah, S., and Friedman, S. H. (2010) Patterning of gene expression using new photolabile groups applied to light activated RNAi J. Am. Chem. Soc. 133, 440-446
32. Casey, J. P., Blidner, R. A., and Monroe, W. T. (2009) Caged siRNAs for spatiotemporal control of gene silencing Mol. Pharmaceutics 6, 669-685
33. Edwards, W. F., Young, D. D., and Deiters, A. (2009) Light-activated Cre recombinase as a tool for the spatial and temporal control of gene function in mammalian cells ACS Chem. Biol. 4, 441-445
34. Chou, C. J., Young, D. D., and Deiters, A. (2010) Photocaged T7 RNA polymerase for the light activation of transcription and gene function in pro- and eukaryotic cells ChemBioChem 11, 972-977
35. Kamal, A., Prabhakar, S., Janaki Ramaiah, M., Venkat Reddy, P., Ratna Reddy, C., Mallareddy, A., Shankaraiah, N., Lakshmi Narayan Reddy, T., Pushpavalli, S. N., and Pal-Bhadra, M. (2011) Synthesis and anticancer activity of chalcone-pyrrolobenzodiazepine conjugates linked via 1,2,3-triazole ring side-armed with alkane spacers Eur. J. Med. Chem. 46, 3820-3831
36. Abdelgany, A., Wood, M., and Beeson, D. (2007) Hairpin DNAzymes: A new tool for efficient cellular gene silencing J. Gene Med. 9, 727-738
37. Agrawal, S. (1999) Importance of nucleotide sequence and chemical modifications of antisense oligonucleotides Biochim. Biophys. Acta 1489, 53-68
38. Brown, D. A., Kang, S. H., Gryaznov, S. M., DeDionisio, L., Heidenreich, O., Sullivan, S., Xu, X., and Nerenberg, M. I. (1994) Effect of phosphorothioate modification of oligodeoxynucleotides on specific protein binding J. Biol. Chem. 269, 26801-26805
39. Xu, Y., Zhang, H. Y., Thormeyer, D., Larsson, O., Du, Q., Elmén, J., Wahlestedt, C., and Liang, Z. (2003) Effective small interfering RNAs and phosphorothioate antisense DNAs have different preferences for target sites in the luciferase mRNAs Biochem. Biophys. Res. Commun. 306, 712-717
40. Koller, E., Propp, S., Zhang, H., Zhao, C., Xiao, X., Chang, M., Hirsch, S. A., Shepard, P. J., Koo, S., Murphy, C., Glazer, R. I., and Dean, N. M. (2006) Use of a chemically modified antisense oligonucleotide library to identify and validate Eg5 (kinesin-like 1) as a target for antineoplastic drug development Cancer Res. 66, 2059-2066
41. Young, D. D., Edwards, W. F., Lusic, H., Lively, M. O., and Deiters, A. (2008) Light-triggered polymerase chain reaction Chem. Commun. 462-464
42. Vivès, E., Brodin, P., and Lebleu, B. (1997) A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus J. Biol. Chem. 272, 16010-16017
43. Grandjean, C., Boutonnier, A., Guerreiro, C., Fournier, J. M., and Mulard, L. A. (2005) On the preparation of carbohydrate-protein conjugates using the traceless Staudinger ligation J. Org. Chem. 70, 7123-7132
44. Lallana, E., Riguera, R., and Fernandez-Megia, E. (2011) Reliable and efficient procedures for the conjugation of biomolecules through Huisgen azide-alkyne cycloadditions Angew. Chem., Int. Ed. 50, 8794-8804
45. Hong, V., Presolski, S. I., Ma, C., and Finn, M. G. (2009) Analysis and optimization of copper-catalyzed azide-alkyne cycloaddition for bioconjugation Angew. Chem., Int. Ed. 48, 9879-9883
46. Presolski, S. I., Hong, V., Cho, S. H., and Finn, M. G. (2010) Tailored ligand acceleration of the Cu-catalyzed azide-alkyne cycloaddition reaction: Practical and mechanistic implications J. Am. Chem. Soc. 132, 14570-14576
47. Shelbourne, M., Brown, T., and El-Sagheer, A. H. (2012) Fast and efficient DNA crosslinking and multiple orthogonal labelling by copper-free click chemistry Chem. Commun. 48, 11184-11186
48. Cole, D. G., Saxton, W. M., Sheehan, K. B., and Scholey, J. M. (1994) A "slow" homotetrameric kinesin-related motor protein purified from Drosophila embryos J. Biol. Chem. 269, 22913-22916
49. Ma, N., Tulu, U. S., Ferenz, N. P., Fagerstrom, C., Wilde, A., and Wadsworth, P. (2010) Poleward transport of TPX2 in the mammalian mitotic spindle requires dynein, Eg5, and microtubule flux Mol. Biol. Cell 21, 979-988
50. Zhu, C., Zhao, J., Bibikova, M., Leverson, J. D., Bossy-Wetzel, E., Fan, J. B., Abraham, R. T., and Jiang, W. (2005) Functional analysis of human microtubule-based motor proteins, the kinesins and dyneins, in mitosis/cytokinesis using RNA interference Mol. Biol. Cell 16, 3187-3199
51. Zhang, Y. and Xu, W. (2008) Progress on kinesin spindle protein inhibitors as anti-cancer agents Anticancer Agents Med. Chem. 8, 698-704
52. Knight, S. D. and Parrish, C. A. (2008) Recent progress in the identification and clinical evaluation of inhibitors of the mitotic kinesin KSP Curr. Top. Med. Chem. 8, 888-904
53. Dias, N. and Stein, C. (2002) Antisense oligonucleotides: Basic concepts and mechanisms Mol. Cancer Ther. 1, 347-355
54. Bennett, C. F. and Swayze, E. E. (2010) RNA targeting therapeutics: Molecular mechanisms of antisense oligonucleotides as a therapeutic platform Annu. Rev. Pharmacol. Toxicol. 50, 259-293
55. Stewart, K. M., Horton, K. L., and Kelley, S. O. (2008) Cell-penetrating peptides as delivery vehicles for biology and medicine Org. Biomol. Chem. 6, 2242-2255
56. van den Berg, A. and Dowdy, S. F. (2011) Protein transduction domain delivery of therapeutic macromolecules Curr. Opin. Biotechnol. 22, 888-893
57. Juliano, R. L., Ming, X., and Nakagawa, O. (2012) The chemistry and biology of oligonucleotide conjugates Acc. Chem. Res. 45, 1067-1076
58. Guterstam, P., Madani, F., Hirose, H., Takeuchi, T., Futaki, S., El Andaloussi, S., Gräslund, A., and Langel, U. (2009) Elucidating cell-penetrating peptide mechanisms of action for membrane interaction, cellular uptake, and translocation utilizing the hydrophobic counter-anion pyrenebutyrate Biochim. Biophys. Acta 1788, 2509-2517
59. Wolfrum, C., Shi, S., Jayaprakash, K. N., Jayaraman, M., Wang, G., Pandey, R. K., Rajeev, K. G., Nakayama, T., Charrise, K., Ndungo, E. M., Zimmermann, T., Koteliansky, V., Manoharan, M., and Stoffel, M. (2007) Mechanisms and optimization of in vivo delivery of lipophilic siRNAs Nat. Biotechnol. 25, 1149-1157
60. Vlahov, I. R. and Leamon, C. P. (2012) Engineering folate-drug conjugates to target cancer: From chemistry to clinic Bioconjug. Chem. 23, 1357-1369
61. Leamon, C. P. (2008) Folate-targeted drug strategies for the treatment of cancer Curr. Opin. Investig. Drugs 9, 1277-1286
62. Li, S., Deshmukh, H. M., and Huang, L. (1998) Folate-mediated targeting of antisense oligodeoxynucleotides to ovarian cancer cells Pharm. Res. 15, 1540-1545
63. Romuald, C., Busseron, E., and Coutrot, F. (2010) Very contracted to extended co-conformations with or without oscillations in two- and three-station [c2]daisy chains J. Org. Chem. 75, 6516-6531
64. Schneider, R., Schmitt, F., Frochot, C., Fort, Y., Lourette, N., Guillemin, F., Müller, J. F., and Barberi-Heyob, M. (2005) Design, synthesis, and biological evaluation of folic acid targeted tetraphenylporphyrin as novel photosensitizers for selective photodynamic therapy Bioorg. Med. Chem. 13, 2799-2808
65. Willibald, J., Harder, J., Sparrer, K., Conzelmann, K. K., and Carell, T. (2012) Click-modified anandamide siRNA enables delivery and gene silencing in neuronal and immune cells J. Am. Chem. Soc. 134, 12330-12333
66. Shakeri-Zadeh, A., Ghasemifard, M., and Mansoor, G. (2010) Structural and optical characterization of folate-conjugated gold-nanoparticles Phys. E 42, 1272-1280
67. Lee, S. M., Chen, H., O'Halloran, T. V., and Nguyen, S. T. (2009) Clickable polymer-caged nanobins as a modular drug delivery platform J. Am. Chem. Soc. 131, 9311-9320
68. Nakagawa, O., Ming, X., Huang, L., and Juliano, R. L. (2010) Targeted intracellular delivery of antisense oligonucleotides via conjugation with small-molecule ligands J. Am. Chem. Soc. 132, 8848-8849
69. Lusic, H., Uprety, R., and Deiters, A. (2010) Improved synthesis of the two-photon caging group 3-nitro-2-ethyldibenzofuran and its application to a caged thymidine phosphoramidite Org. Lett. 12, 916-919
70. Momotake, A., Lindegger, N., Niggli, E., Barsotti, R. J., and Ellis-Davies, G. C. (2006) The nitrodibenzofuran chromophore: A new caging group for ultra-efficient photolysis in living cells Nat. Methods 3, 35-40
71. Ando, H., Furuta, T., Tsien, R. Y., and Okamoto, H. (2001) Photo-mediated gene activation using caged RNA/DNA in zebrafish embryos Nat. Genet. 28, 317-325
72. Nielsen, R., Courtoy, P. J., Jacobsen, C., Dom, G., Lima, W. R., Jadot, M., Willnow, T. E., Devuyst, O., and Christensen, E. I. (2007) Endocytosis provides a major alternative pathway for lysosomal biogenesis in kidney proximal tubular cells Proc. Natl. Acad. Sci. U.S.A. 104, 5407-5412
73. Denny, W. A., Leupin, W., and Kearns, D. R. (1982) Simplified liquid-phase preparation of four decadeoxyribonucleotides and their preliminary spectroscopic characterization Helvetica Chem. Acta 65, 2372-2393
74. Mindt, T. L., Müller, C., Melis, M., de Jong, M., and Schibli, R. (2008) "Click-to-chelate": in vitro and in vivo comparison of a 99mTc(CO)3-labeled N(tau)-histidine folate derivative with its isostructural, clicked 1,2,3-triazole analogue Bioconjug. Chem. 19, 1689-1695