Identification of siRNA delivery enhancers by a chemical library screen

Nucleic Acids Research

Volumn 43, Issue 16, 2015, Pages 7984-8001

  Gilleron, Jerome ^a,b,h   Paramasivam, Prasath ^a   Zeigerer, Anja ^a   Querbes, William ^c   Marsico, Giovanni ^a   Andree, Cordula ^a   Seifert, Sarah ^a   Amaya, Pablo ^a   Stöter, Martin ^a   Koteliansky, Victor ^d,e   Waldmann, Herbert ^f,g   Fitzgerald, Kevin ^c   Kalaidzidis, Yannis ^a   Akinc, Akin ^c   Maier, Martin A ^c   Manoharan, Muthiah ^c   Bickle, Marc ^a   Zerial, Marino ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

^c ALNYLAM PHARMACEUTICALS   (United States)

^d MOSCOW STATE UNIVERSITY   (Russian Federation)

^e SKOLKOVO INSTITUTE OF SCIENCE AND TECHNOLOGY   (Russian Federation)

^f MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^g TU DORTMUND UNIVERSITY   (Germany)

^h UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; CHOLESTEROL; GREEN FLUORESCENT PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; RAC1 PROTEIN; SMALL INTERFERING RNA; SOLID LIPID NANOPARTICLE; LIPID; MOLECULAR LIBRARY; NANOPARTICLE;

ANIMAL TISSUE; ARTICLE; CELL TRANSPORT; CONTROLLED STUDY; DRUG RELEASE; DRUG UPTAKE; ENDOCYTOSIS; GENE DELIVERY SYSTEM; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERNALIZATION; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LIPID INTERACTION; RNA INTERFERENCE; ANIMAL; CELL CULTURE; ENDOSOME; ENDOTHELIUM CELL; FIBROBLAST; HELA CELL LINE; LIVER CELL; METABOLISM; MOLECULAR LIBRARY;

ANIMALS; CELLS, CULTURED; CHOLESTEROL; ENDOSOMES; ENDOTHELIAL CELLS; FIBROBLASTS; HELA CELLS; HEPATOCYTES; HUMANS; LIPIDS; MICE; NANOPARTICLES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SMALL MOLECULE LIBRARIES;

EID: 84942278867     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv762     Document Type: Article

References (74)

1. Sliva, K. And Schnierle, B. S. (2010) Selective gene silencing by viral delivery of short hairpin RNA. Virol. J., 7, 248-258.
2. Buyens, K., De Smedt, S. C., Braeckmans, K., Demeester, J., Peeters, L., van Grunsven, L. A., de Mollerat du Jeu, X., Sawant, R., Torchilin, V., Farkasova, K. et al. (2012) Liposome based systems for systemic siRNA delivery: Stability in blood sets the requirements for optimal carrier design. J. Control. Release, 158, 362-370.
3. Castillo, B., Bromberg, L., Lopez, X., Badillo, V., Gonzalez Feliciano, J. A., Gonzalez, C. I., Hatton, T. A. And Barletta, G. (2012) Intracellular Delivery of siRNA by Polycationic Superparamagnetic Nanoparticles. J. Drug Deliv., 2012, 218940-218951.
4. Lopez-Davila, V., Seifalian, A. M. And Loizidou, M. (2012) Organic nanocarriers for cancer drug delivery. Curr. Opin. Pharmacol., 12, 414-419.
5. Nair, J., Willoughby, J., Chan, A., Charisse, K., Alam, R. M., Wang, Q., Hoekstra, M., Kandasamy, P., Kel'in, A. V., Milstein, S. et al. (2014) Multivalent N-Acetylgalactosamine-Conjugated siRNA Localizes in Hepatocytes and Elicits Robust RNAi-mediated Gene Silencing. J. Am. Chem. Soc., 136, 16958-16961.
6. Gilleron, J., Querbes, W., Zeigerer, A., Borodovsky, A., Marsico, G., Schubert, U., Manygoats, K., Seifert, S., Andree, C., Stoter, M. et al. (2013) Image-based analysis of lipid nanoparticle-mediated siRNA delivery, intracellular trafficking and endosomal escape. Nat. Biotechnol., 31, 638-646.
7. Akinc, A., Goldberg, M., Qin, J., Dorkin, J. R., Gamba-Vitalo, C., Maier, M., Jayaprakash, K. N., Jayaraman, M., Rajeev, K. G., Manoharan, M. et al. (2009) Development of Lipidoid-siRNA Formulations for Systemic Delivery to the Liver. Mol. Ther., 17, 872-879.
8. Akinc, A., Querbes, W., De, S., Qin, J., Frank-Kamenetsky, M., Jayaprakash, K. N., Jayaraman, M., Rajeev, K. G., Cantley, W. L., Dorkin, J. R. et al. (2010) Targeted delivery of RNAi therapeutics with endogenous and exogenous ligand-based mechanisms. Mol. Ther., 18, 1357-1364.
9. Jayaraman, M., Ansell, S. M., Mui, B. L., Tam, Y. K., Chen, J., Du, X., Butler, D., Eltepu, L., Matsuda, S., Narayanannair, J. K. et al. (2012) Maximizing the potency of siRNA lipid nanoparticles for hepatic gene silencing in vivo. Angew. Chem. Int. Ed. Engl., 51, 8529-8533.
10. Love, K. T., Mahon, K. P., Levins, C. G., Whitehead, K. A., Querbes, W., Dorkin, J. R., Qin, J., Cantley, W., Qin, L. L., Racie, T. et al. (2010) Lipid-like materials for low-dose, in vivo gene silencing. Proc. Nat. Acad. Sci. U. S. A., 107, 1864-1869.
11. Zimmermann, T. S., Lee, A. C., Akinc, A., Bramlage, B., Bumcrot, D., Fedoruk, M. N., Harborth, J., Heyes, J. A., Jeffs, L. B., John, M. et al. (2006) RNAi-mediated gene silencing in non-human primates. Nature, 441, 111-114.
12. Kanasty, R., Dorkin, J. R., Vegas, A. And Anderson, D. (2013) Delivery materials for siRNA therapeutics. Nat. Mater., 12, 967-977.
13. Coelho, T., Adams, D., Silva, A., Lozeron, P., Hawkins, P. N., Mant, T., Perez, J., Chiesa, J., Warrington, S., Tranter, E. et al. (2013) Safety and Efficacy of RNAi Therapy for Transthyretin Amyloidosis. N. Engl. J. Med., 369, 819-829.
14. Pei, Y., Hancock, P. J., Zhang, H., Bartz, R., Cherrin, C., Innocent, N., Pomerantz, C. J., Seitzer, J., Koser, M. L., Abrams, M. T. et al. (2010) Quantitative evaluation of siRNA delivery in vivo. RNA, 16, 2553-2563.
15. Xu, Y., Ou, M., Keough, E., Roberts, J., Koeplinger, K., Lyman, M., Fauty, S., Carlini, E., Stern, M., Zhang, R. et al. (2014) Quantitation of physiological and biochemical barriers to siRNA liver delivery via lipid nanoparticle platform. Mol. Pharm., 11, 1424-1434.
16. Akinc, A. And Battaglia, G. (2013) Exploiting endocytosis for nanomedicines. Cold Spring Harb. Perspect. Biol., 5, a016980.
17. Lee, S. K., Siefert, A., Beloor, J., Fahmy, T. M. And Kumar, P. (2012) Cell-specific siRNA delivery by peptides and antibodies. Methods Enzymol., 502, 91-122.
18. Nielsen, C., Kjems, J., Sorensen, K. R., Engelholm, L. H. And Behrendt, N. (2014) Advances in targeted delivery of small interfering RNA using simple bioconjugates. Expert Opin. Drug. Deliv., 11, 791-822.
19. Prakash, T. P., Graham, M. J., Yu, J., Carty, R., Low, A., Chappell, A., Schmidt, K., Zhao, C., Aghajan, M., Murray, H. F. et al. (2014) Targeted delivery of antisense oligonucleotides to hepatocytes using triantennary N-acetyl galactosamine improves potency 10-fold in mice. Nucleic Acids Res., 42, 8796-8807.
20. Hibbitts, A., Lieggi, N., McCabe, O., Thomas, W., Barlow, J., O'Brien, F. And Cryan, S. A. (2011) Screening of siRNA nanoparticles for delivery to airway epithelial cells using high-content analysis. Ther. Deliv., 2, 987-999.
21. Li, L., Wang, F., Wu, Y., Davidson, G. And Levkin, P. A. (2013) Combinatorial synthesis and high-throughput screening of alkyl amines for nonviral gene delivery. Bioconjug. Chem., 24, 1543-1551.
22. Zugates, G. T., Anderson, D. G. And Langer, R. (2013) High-throughput methods for screening polymeric transfection reagents. Cold Spring Harb. Protoc., 11, 1-14.
23. Wang, A., Marinakos, S. M., Badireddy, A. R., Powers, C. M. And Houck, K. A. (2013) Characterization of physicochemical properties of nanomaterials and their immediate environments in high-throughput screening of nanomaterial biological activity. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol., 5, 430-448.
24. Nabzdyk, C. S., Chun, M., Pradhan, L. And Logerfo, F. W. (2011) High throughput RNAi assay optimization using adherent cell cytometry. J. Transl. Med., 9, 48-56.
25. Ming, X., Carver, K., Fisher, M., Noel, R., Cintrat, J. C., Gillet, D., Barbier, J., Cao, C., Bauman, J. And Juliano, R. L. (2013) The small molecule Retro-1 enhances the pharmacological actions of antisense and splice switching oligonucleotides. Nucleic Acids Res., 41, 3673-3687.
26. Yang, B., Ming, X., Cao, C., Laing, B., Yuan, A., Porter, M. A., Hull-Ryde, E. A., Maddry, J., Suto, M., Janzen, W. P. et al. (2015) High-throughput screening identifies small molecules that enhance the pharmacological effects of oligonucleotides. Nucleic Acids Res., 43, 1987-1996.
27. Cotten, M., Langle-Rouault, F., Kirlappos, H., Wagner, E., Mechtler, K., Zenke, M., Beug, H. And Birnstiel, M. L. (1990) Transferrin-polycation-mediated introduction of DNA into human leukemic cells: Stimulation by agents that affect the survival of transfected DNA or modulate transferrin receptor levels. Proc. Natl. Acad. Sci. U. S. A., 87, 4033-4037.
28. Bhattarai, S. R., Muthuswamy, E., Wani, A., Brichacek, M., Castaneda, A. L., Brock, S. L. And Oupicky, D. (2010) Enhanced gene and siRNA delivery by polycation-modified mesoporous silica nanoparticles loaded with chloroquine. Pharm. Res., 27, 2556-2568.
29. Settembre, C., Fraldi, A., Medina, D. L. And Ballabio, A. (2013) Signals from the lysosome: A control centre for cellular clearance and energy metabolism. Nat. Rev. Mol. Cell Biol., 14, 283-296.
30. Sorkin, A. And von Zastrow, M. (2009) Endocytosis and signalling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10, 609-622.
31. Saftig, P. And Klumperman, J. (2009) Lysosome biogenesis and lysosomal membrane proteins: Trafficking meets function. Nat. Rev. Mol. Cell Biol., 10, 623-635.
32. Wei, J., Jones, J., Kang, J., Card, A., Krimm, M., Hancock, P., Pei, Y., Ason, B., Payson, E., Dubinina, N. et al. (2011) RNA-induced silencing complex-bound small interfering RNA is a determinant of RNA interference-mediated gene silencing in mice. Mol. Pharmacol., 79, 953-963.
33. Landesman, Y., Svrzikapa, N., Cognetta, A. 3rd, Zhang, X., Bettencourt, B. R., Kuchimanchi, S., Dufault, K., Shaikh, S., Gioia, M., Akinc, A. et al. (2010) In vivo quantification of formulated and chemically modified small interfering RNA by heating-in-Triton quantitative reverse transcription polymerase chain reaction (HIT qRT-PCR). Silence, 1, 16-29.
34. Basha, G., Novobrantseva, T. I., Rosin, N., Tam, Y. Y., Hafez, I. M., Wong, M. K., Sugo, T., Ruda, V. M., Qin, J., Klebanov, B. et al. (2011) Influence of Cationic Lipid Composition on Gene Silencing Properties of Lipid Nanoparticle Formulations of siRNA in Antigen-Presenting Cells. Mol. Ther., 19, 2186-2200.
35. Tamura, A., Oishi, M. And Nagasaki, Y. (2009) Enhanced cytoplasmic delivery of siRNA using a stabilized polyion complex based on PEGylated nanogels with a cross-linked polyamine structure. Biomacromolecules, 10, 1818-1827.
36. Akita, H., Kogure, K., Moriguchi, R., Nakamura, Y., Higashi, T., Nakamura, T., Serada, S., Fujimoto, M., Naka, T., Futaki, S. et al. (2010) Nanoparticles for ex vivo siRNA delivery to dendritic cells for cancer vaccines: programmed endosomal escape and dissociation. J. Control. Release, 143, 311-317.
37. Sakurai, Y., Hatakeyama, H., Sato, Y., Akita, H., Takayama, K., Kobayashi, S., Futaki, S. And Harashima, H. (2011) Endosomal escape and the knockdown efficiency of liposomal-siRNA by the fusogenic peptide shGALA. Biomaterials, 32, 5733-5742.
38. Soutschek, J., Akinc, A., Bramlage, B., Charisse, K., Constien, R., Donoghue, M., Elbashir, S., Geick, A., Hadwiger, P., Harborth, J. et al. (2004) Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature, 432, 173-178.
39. 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. et al. (2009) A large-scale chemical modification screen identifies design rules to generate siRNAs with high activity, high stability and low toxicity. Nucleic Acids Res., 37, 2867-2881.
40. Pal, A., Severin, F., Lommer, B., Shevchenko, A. And Zerial, M. (2006) Huntingtin-HAP40 complex is a novel Rab5 effector that regulates early endosome motility and is up-regulated in Huntington's disease. J. Cell Biol., 172, 605-618.
41. Riedl, J., Flynn, K. C., Raducanu, A., Gartner, F., Beck, G., Bosl, M., Bradke, F., Massberg, S., Aszodi, A., Sixt, M. et al. (2010) Lifeact mice for studying F-actin dynamics. Nat. Methods, 7, 168-169.
42. Zeigerer, A., Gilleron, J., Bogorad, R. L., Marsico, G., Nonaka, H., Seifert, S., Epstein-Barash, H., Kuchimanchi, S., Peng, C. G., Ruda, V. M. et al. (2012) Rab5 is necessary for the biogenesis of the endolysosomal system in vivo. Nature, 485, 465-470.
43. Limmer, A., Ohl, J., Kurts, C., Ljunggren, H. G., Reiss, Y., Groettrup, M., Momburg, F., Arnold, B. And Knolle, P. A. (2000) Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Nat. Med., 6, 1348-1354.
44. Collinet, C., Stoter, M., Bradshaw, C. R., Samusik, N., Rink, J. C., Kenski, D., Habermann, B., Buchholz, F., Henschel, R., Mueller, M. S. et al. (2010) Systems survey of endocytosis by multiparametric image analysis. Nature, 464, 243-249.
45. Karnovsky, M. J. (1971) Proceedings of the Eleventh Annual Meeting of the American Society for Cell Biology. 11th Am Soc Cell Biol New Orleans, Vol. 284, p. 146.
46. Lucocq, J. M. (2007) Efficient quantitative morphological phenotyping of genetically altered organisms using stereology. Transgenic Res., 16, 133-145.
47. Soille, P. (1999) Morphological Image Analysis: Principles and Applications. Springer-Verlag Telos, London.
48. Rink, J., Ghigo, E., Kalaidzidis, Y. And Zerial, M. (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell, 122, 735-749.
49. Wolfrum, C., Shi, S., Jayaprakash, K. N., Jayaraman, M., Wang, G., Pandey, R. K., Rajeev, K. G., Nakayama, T., Charrise, K., Ndungo, E. M. et al. (2007) Mechanisms and optimization of in vivo delivery of lipophilic siRNAs. Nat. Biotechnol., 25, 1149-1157.
50. Frank-Kamenetsky, M., Grefhorst, A., Anderson, N. N., Racie, T. S., Bramlage, B., Akinc, A., Butler, D., Charisse, K., Dorkin, R., Fan, Y. et al. (2008) Therapeutic RNAi targeting PCSK9 acutely lowers plasma cholesterol in rodents and LDL cholesterol in nonhuman primates. Proc. Natl. Acad. Sci. U. S. A., 105, 11915-11920.
51. Semple, S. C., Akinc, A., Chen, J., Sandhu, A. P., Mui, B. L., Cho, C. K., Sah, D. W., Stebbing, D., Crosley, E. J., Yaworski, E. et al. (2010) Rational design of cationic lipids for siRNA delivery. Nat. Biotechnol., 28, 172-176.
52. Mukherjee, S., Zha, X., Tabas, I. And Maxfield, F. R. (1998) Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. Biophys. J., 75, 1915-1925.
53. Ikonen, E. (2008) Cellular cholesterol trafficking and compartmentalization. Nat. Rev. Mol. Cell Biol., 9, 125-138.
54. Brown, M. S. And Goldstein, J. L. (1986) A receptor-mediated pathway for cholesterol homeostasis. Science, 232, 34-47.
55. Brown, M. S. And Goldstein, J. L. (1997) The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell, 89, 331-340.
56. Maxfield, F. R. And Tabas, I. (2005) Role of cholesterol and lipid organization in disease. Nature, 438, 612-621.
57. Chen, Y. H., Lin, W. W., Liu, C. S., Hsu, L. S., Lin, Y. M. And Su, S. L. (2014) Caveolin-1 provides palliation for adverse hepatic reactions in hypercholesterolemic rabbits. PLoS One, 9, e71862.
58. Simeoni, F., Morris, M. C., Heitz, F. And Divita, G. (2003) Insight into the mechanism of the peptide-based gene delivery system MPG: implications for delivery of siRNA into mammalian cells. Nucleic Acids Res., 31, 2717-2724.
59. Luthman, H. And Magnusson, G. (1983) High efficiency polyoma DNA transfection of chloroquine treated cells. Nucleic Acids Res., 11, 1295-1308.
60. Pack, D. W., Hoffman, A. S., Pun, S. And Stayton, P. S. (2005) Design and development of polymers for gene delivery. Nature reviews. Drug discovery, 4, 581-593.
61. Tietze, C., Schlesinger, P. And Stahl, P. (1980) Chloroquine and ammonium ion inhibit receptor-mediated endocytosis of mannose-glycoconjugates by macrophages: Apparent inhibition of receptor recycling. Biochemical and biophysical research communications, 93, 1-8.
62. Starai, V. J., Jun, Y. And Wickner, W. (2007) Excess vacuolar SNAREs drive lysis and Rab bypass fusion. Proc. Natl. Acad. Sci. U. S. A., 104, 13551-13558.
63. Ohya, T., Miaczynska, M., Coskun, U., Lommer, B., Runge, A., Drechsel, D., Kalaidzidis, Y. And Zerial, M. (2009) Reconstitution of Rab-and SNARE-dependent membrane fusion by synthetic endosomes. Nature, 459, 1091-1097.
64. Sundaramurthy, V., Barsacchi, R., Samusik, N., Marsico, G., Gilleron, J., Kalaidzidis, I., Meyenhofer, F., Bickle, M., Kalaidzidis, Y. And Zerial, M. (2013) Integration of chemical and RNAi multiparametric profiles identifies triggers of intracellular mycobacterial killing. Cell Host Microbe, 13, 129-142.
65. Akinc, A., Goldberg, M., Qin, J., Dorkin, J. R., Gamba-Vitalo, C., Maier, M., Jayaprakash, K. N., Jayaraman, M., Rajeev, K. G., Manoharan, M. et al. (2009) Development of Lipidoid-siRNA Formulations for Systemic Delivery to the Liver. Mol. Ther., 17, 872-879.
66. Belliveau, N. M., Huft, J., Lin, P. J., Chen, S., Leung, A. K., Leaver, T. J., Wild, A. W., Lee, J. B., Taylor, R. J., Tam, Y. K. et al. (2012) Microfluidic Synthesis of Highly Potent Limit-size Lipid Nanoparticles for In Vivo Delivery of siRNA. Mol. Ther. Nucleic Acids, 1, e37.
67. Tam, Y. Y., Chen, S. And Cullis, P. R. (2013) Advances in Lipid Nanoparticles for siRNA Delivery. Pharmaceutics, 5, 498-507.
68. Dahlman, J. E., Barnes, C., Khan, O. F., Thiriot, A., Jhunjunwala, S., Shaw, T. E., Xing, Y., Sager, H. B., Sahay, G., Speciner, L. et al. (2014) In vivo endothelial siRNA delivery using polymeric nanoparticles with low molecular weight. Nat Nanotechnol., 9, 648-655.
69. Tan, K. T., Guiu-Rozas, E., Bon, R. S., Guo, Z., Delon, C., Wetzel, S., Arndt, S., Alexandrov, K., Waldmann, H., Goody, R. S. et al. (2009) Design, synthesis, and characterization of peptide-based rab geranylgeranyl transferase inhibitors. J. Med. Chem., 52, 8025-8037.
70. Ma, D. (2014) Enhancing endosomal escape for nanoparticle mediated siRNA delivery. Nanoscale, 6, 6415-6425.
71. Thoren, P. E., Persson, D., Esbjorner, E. K., Goksor, M., Lincoln, P. And Norden, B. And Norden, B. (2004) Membrane binding and translocation of cell-penetrating peptides. Biochemistry, 43, 3471-3489.
72. El-Andaloussi, S., Holm, T. And Langel, U. (2005) Cell-penetrating peptides: mechanisms and applications. Curr. Pharm. Des., 11, 3597-3611.
73. Bissig, C. And Gruenberg, J. (2014) ALIX and the multivesicular endosome: ALIX in Wonderland. Trends Cell. Biol., 24, 19-25.
74. Bartz, R., Fan, H., Zhang, J., Innocent, N., Cherrin, C., Beck, S. C., Pei, Y., Momose, A., Jadhav, V., Tellers, D. M. et al. (2011) Effective siRNA delivery and target mRNA degradation using an amphipathic peptide to facilitate pH-dependent endosomal escape. Biochem. J., 435, 475-487.