In Situ Gelling Liquid Crystalline System as Local siRNA Delivery System

Molecular Pharmaceutics

Volumn 14, Issue 5, 2017, Pages 1681-1690

  Borgheti Cardoso, Livia N ^a   Kooijmans, Sander A A ^b,c   Fens, Marcel H A M ^b   Van der Meel, Roy ^b,d   Vicentini, Fabiana T M C ^a   Fantini, Marcia C A ^a   Bentley, Maria Vitória L B ^a   Schiffelers, Raymond M ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY OF TURIN   (Italy)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

gene silencing; in situ gelling delivery system; liquid crystal; siRNA

Indexed keywords

BUFFER; MONOACYLGLYCEROL; POLYETHYLENEIMINE; PROPYLENE GLYCOL; SMALL INTERFERING RNA; WATER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DRUG DEGRADATION; DRUG DELIVERY SYSTEM; DRUG FORMULATION; FEMALE; GEL; GENE SILENCING; HUMAN; HUMAN CELL; IN VIVO STUDY; LIQUID CRYSTAL; MOUSE; NONHUMAN; PRECURSOR; PRIORITY JOURNAL; TUMOR CELL; X RAY CRYSTALLOGRAPHY; CHEMISTRY; GENETICS; PHYSIOLOGY;

GENE SILENCING; LIQUID CRYSTALS; MONOGLYCERIDES; POLYETHYLENEIMINE; PROPYLENE GLYCOL; RNA, SMALL INTERFERING;

EID: 85018451427     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/acs.molpharmaceut.6b01141     Document Type: Article

References (46)

1. Fire, A.; Xu, S.; Montgomery, M. K.; Kostas, S. A.; Driver, S. E.; Mello, C. C. Potent and Specific Genetic Interference by Double-Stranded RNA in Caenorhabditis Elegans Nature 1998, 391, 806-811 10.1038/35888
2. Sarett, S. M.; Nelson, C. E.; Duvall, C. L. Technologies for Controlled, Local Delivery of siRNA J. Controlled Release 2015, 218, 94-113 10.1016/j.jconrel.2015.09.066
3. Bumcrot, D.; Manoharan, M.; Koteliansky, V.; Sah, D. W. RNAi Therapeutics: A Potential New Class of Pharmaceutical Drugs Nat. Chem. Biol. 2006, 2, 711-719 10.1038/nchembio839
4. Zhou, J.; Shum, K.-T. T.; Burnett, J. C.; Rossi, J. J. Nanoparticle-Based Delivery of RNAi Therapeutics: Progress and Challenges Pharmaceuticals 2013, 6, 85-107 10.3390/ph6010085
5. Schroeder, A.; Levins, C. G.; Cortez, C.; Langer, R.; Anderson, D. G. Lipid-Based Nanotherapeutics for siRNA Delivery J. Intern. Med. 2010, 267 ( 1 ) 9-21 10.1111/j.1365-2796.2009.02189.x
6. Conde, J.; Ambrosone, A.; Hernandez, Y.; Tian, F.; Mccully, M.; Berry, C. C.; Baptista, P. V.; Tortiglione, C.; de la Fuente, J. M. 15 Years on siRNA Delivery: Beyond the State-of-the-Art on Inorganic Nanoparticles for RNAi Therapeutics Nano Today 2015, 10, 421-450 10.1016/j.nantod.2015.06.008
7. Kapoor, M.; Burgess, D. J. Cellular Uptake Mechanisms of Novel Anionic siRNA Lipoplexes Pharm. Res. 2013, 30, 1161-1175 10.1007/s11095-012-0952-9
8. Kim, Y. M.; Park, M. R.; Song, S. C. An Injectable Cell Penetrable Nano-Polyplex Hydrogel for Localized siRNA Delivery Biomaterials 2013, 34 ( 18 ) 4493-4500 10.1016/j.biomaterials.2013.02.050
9. Vicentini, F. T. M. d. C.; Borgheti-Cardoso, L. N.; Depieri, L. V.; de Macedo Mano, D.; Abelha, T. F.; Petrilli, R.; Bentley, M. V. L. B. Delivery Systems and Local Administration Routes for Therapeutic siRNA Pharm. Res. 2013, 30 ( 4 ) 915-931 10.1007/s11095-013-0971-1
10. Borgheti-Cardoso, L. N.; Depieri, L. V.; Diniz, H.; Calzzani, R. A. J.; De Abreu Fantini, M. C.; Iyomasa, M. M.; Moura De Carvalho Vicentini, F. T.; Bentley, M. V. L. B. Self-Assembling Gelling Formulation Based on a Crystalline-Phase Liquid as a Non-Viral Vector for siRNA Delivery Eur. J. Pharm. Sci. 2014, 58 ( 1 ) 72-82 10.1016/j.ejps.2014.04.001
11. Borgheti-Cardoso, L. N.; Depieri, L. V.; Kooijmans, S. A. A.; Diniz, H.; Calzzani, R. A. J.; Vicentini, F. T. M. d. C.; van der Meel, R.; de Abreu Fantini, M. C.; Iyomasa, M. M.; Schiffelers, R. M.; Bentley, M. V. L. B. An in Situ Gelling Liquid Crystalline System Based on Monoglycerides and Polyethylenimine for Local Delivery of siRNAs Eur. J. Pharm. Sci. 2015, 74, 103-117 10.1016/j.ejps.2015.04.017
12. Han, H. D.; Mora, E. M.; Roh, J. W.; Nishimura, M.; Lee, S. J.; Stone, R. L.; Bar-Eli, M.; Lopez-Berestein, G.; Sood, A. K. Chitosan Hydrogel for Localized Gene Silencing Cancer Biol. Ther. 2011, 11 ( 9 ) 839-845 10.4161/cbt.11.9.15185
13. Kim, Y. M.; Park, M. R.; Song, S. C. Injectable Polyplex Hydrogel for Localized and Long-Term Delivery of siRNA ACS Nano 2012, 6 ( 7 ) 5757-5766 10.1021/nn300842a
14. Krebs, M. D.; Jeon, O.; Alsberg, E. Localized and Sustained Delivery of Silencing RNA from Macroscopic Biopolymer Hydrogels J. Am. Chem. Soc. 2009, 131 ( 26 ) 9204-9206 10.1021/ja9037615
15. Nguyen, K.; Dang, P. N.; Alsberg, E. Functionalized, Biodegradable Hydrogels for Control over Sustained and Localized siRNA Delivery to Incorporated and Surrounding Cells Acta Biomater. 2013, 9, 4487-4495 10.1016/j.actbio.2012.08.012
16. Packhaeuser, C. B.; Schnieders, J.; Oster, C. G.; Kissel, T. In Situ Forming Parenteral Drug Delivery Systems: An Overview Eur. J. Pharm. Biopharm. 2004, 58 ( 2 ) 445-455 10.1016/j.ejpb.2004.03.003
17. Yaghmur, A.; Rappolt, M.; Larsen, S. W. In Situ Forming Drug Delivery Systems Based on Lyotropic Liquid Crystalline Phases: Structural Characterization and Release Properties J. Drug Delivery Sci. Technol. 2013, 23 ( 4 ) 325-332 10.1016/S1773-2247(13)50049-9
18. Chang, C. M.; Bodmeier, R. Low Viscosity Monoglyceride-Based Drug Delivery Systems Transforming into a Highly Viscous Cubic Phase Int. J. Pharm. 1998, 173 ( 1-2 ) 51-60 10.1016/S0378-5173(98)00180-X
19. Mitchell, D. J.; Ninham, B. W. Micelles, Vesicles and Micro-Emulsions J. Chem. Soc., Faraday Trans. 2 1981, 77 ( 4 ) 601-629 10.1039/f29817700601
20. Amar-Yuli, I.; Garti, N. Transitions Induced by Solubilized Fat into Reverse Hexagonal Mesophases Colloids Surf., B 2005, 43 ( 2 ) 72-82 10.1016/j.colsurfb.2005.03.011
21. Souza, C.; Watanabe, E.; Borgheti-Cardoso, L. N.; Fantini, M. C. D. A.; Lara, M. G. Mucoadhesive System Formed by Liquid Crystals for Buccal Administration of PHMB J. Pharm. Sci. 2014, 103, 3914-3923 10.1002/jps.24198
22. Vicentini, F. T. M. D. C.; Depieri, L. V.; Polizello, A. C. M.; Ciampo, J. O. D.; Spadaro, A. C. C.; Fantini, M. C. A.; Bentley, M. V. L. B. Liquid Crystalline Phase Nanodispersions Enable Skin Delivery of siRNA Eur. J. Pharm. Biopharm. 2013, 83 ( 1 ) 16-24 10.1016/j.ejpb.2012.08.011
23. Rizwan, S. B.; Hanley, T.; Boyd, B. J.; Rades, T.; Hook, S. Liquid Crystalline Systems of Phytantriol and Glyceryl Monooleate Containing a Hydrophilic Protein: Characterisation, Swelling and Release Kinetics J. Pharm. Sci. 2009, 98 ( 11 ) 4191-4204 10.1002/jps.21724
24. Tran, M. a; Gowda, R.; Sharma, A.; Park, E.-J.; Adair, J.; Kester, M.; Smith, N. B.; Robertson, G. P. Targeting V600EB-Raf and Akt3 Using Nanoliposomal-Small Interfering RNA Inhibits Cutaneous Melanocytic Lesion Development Cancer Res. 2008, 68 ( 18 ) 7638-7649 10.1158/0008-5472.CAN-07-6614
25. Shen, Y.; Wang, B.; Lu, Y.; Ouahab, A.; Li, Q.; Tu, J. A Novel Tumor-Targeted Delivery System with Hydrophobized Hyaluronic Acid-Spermine Conjugates (HHSCs) for Efficient Receptor-Mediated siRNA Delivery Int. J. Pharm. 2011, 414, 233-243 10.1016/j.ijpharm.2011.04.049
26. Vader, P.; van der Aa, L. J.; Engbersen, J. F. J.; Storm, G.; Schiffelers, R. M. A Method for Quantifying Cellular Uptake of Fluorescently Labeled siRNA J. Controlled Release 2010, 148 ( 1 ) 106-109 10.1016/j.jconrel.2010.06.019
27. Rossetti, F. C.; Fantini, M. C.; Carollo, A. R.; Tedesco, A. C.; Bentley, M. V. L. B. Analysis of Liquid Crystalline Nanoparticles by Small Angle X-Ray Diffraction: Evaluation of Drug and Pharmaceutical Additives Influence on the Internal Structure J. Pharm. Sci. 2011, 100, 2849-2857 10.1002/jps.22522
28. Clogston, J.; Rathman, J.; Tomasko, D.; Walker, H.; Caffrey, M. Phase Behavior of a Monoacylglycerol (Myverol 18-99K):water System Chem. Phys. Lipids 2000, 107, 191-220 10.1016/S0009-3084(00)00182-1
29. Günther, M.; Lipka, J.; Malek, A.; Gutsch, D.; Kreyling, W.; Aigner, A. Polyethylenimines for RNAi-Mediated Gene Targeting in Vivo and siRNA Delivery to the Lung Eur. J. Pharm. Biopharm. 2011, 77 ( 3 ) 438-449 10.1016/j.ejpb.2010.11.007
30. Xiong, X.-B.; Uludag, H.; Lavasanifar, A. Biomaterials Biodegradable Amphiphilic Poly(ethylene Oxide)-Block-Polyesters with Grafted Polyamines as Supramolecular Nanocarriers for Efficient siRNA Delivery Biomaterials 2009, 30, 242-253 10.1016/j.biomaterials.2008.09.025
31. Vercauteren, D.; Rejman, J.; Martens, T. F.; Demeester, J.; De Smedt, S. C.; Braeckmans, K. On the Cellular Processing of Non-Viral Nanomedicines for Nucleic Acid Delivery: Mechanisms and Methods J. Controlled Release 2012, 161 ( 2 ) 566-581 10.1016/j.jconrel.2012.05.020
32. Beyerle, A.; Braun, A.; Merkel, O.; Koch, F.; Kissel, T.; Stoeger, T. Comparative in Vivo Study of Poly(ethylene imine)/siRNA Complexes for Pulmonary Delivery in Mice J. Controlled Release 2011, 151 ( 1 ) 51-56 10.1016/j.jconrel.2010.12.017
33. Rejman, J.; Bragonzi, A.; Conese, M. Role of Clathrin-and Caveolae-Mediated Endocytosis in Gene Transfer Mediated by Lipo-and Polyplexes Mol. Ther. 2005, 12 ( 3 ) 468-474 10.1016/j.ymthe.2005.03.038
34. Wang, H.; Liu, W.; Yu, F.; Lu, L. Disruption of Clathrin-Dependent Trafficking Results in the Failure of Grass Carp Reovirus Cellular Entry Virol. J. 2016, 13 ( 25 ) 1-10 10.1186/s12985-016-0485-7
35. Gilleron, J.; Querbes, W.; Zeigerer, A.; Borodovsky, A.; Marsico, G.; Schubert, U.; Manygoats, K.; Seifert, S.; Andree, C.; Stöter, M.; Epstein-barash, H.; Zhang, L.; Koteliansky, V.; Fitzgerald, K.; Fava, E.; Bickle, M.; Kalaidzidis, Y.; Akinc, A.; Maier, M.; Zerial, M. Image-Based Analysis of Lipid Nanoparticle- Mediated siRNA Delivery, Intracellular Trafficking and Endosomal Escape Nat. Biotechnol. 2013, 31 ( 7 ) 638-646 10.1038/nbt.2612
36. Nelson, C. E.; Gupta, M. K.; Adolph, E. J.; Shannon, J. M.; Guelcher, S. A.; Duvall, C. L. Sustained Local Delivery of siRNA from an Injectable Scaffold Biomaterials 2012, 33 ( 4 ) 1154-1161 10.1016/j.biomaterials.2011.10.033
37. Manaka, T.; Suzuki, A.; Takayama, K.; Imai, Y.; Nakamura, H.; Takaoka, K. Local Delivery of siRNA Using a Biodegradable Polymer Application to Enhance BMP-Induced Bone Formation Biomaterials 2011, 32, 9642-9648 10.1016/j.biomaterials.2011.08.026
38. Zhao, Y.; Zhang, S.; Zhang, Y.; Cui, S.; Chen, H.; Zhi, D.; Zhen, Y.; Zhang, S.; Huang, L. Tri-Peptide Cationic Lipids for Gene Delivery J. Mater. Chem. B 2015, 3, 119-126 10.1039/C4TB01312C
39. Zhao, Y.-N.; Qureshi, F.; Zhang, S.-B.; Cui, S.-H.; Wang, B.; Chen, H.-Y.; Lv, H.-T.; Zhang, S.-F.; Huang, L. Novel Gemini Cationic Lipids with Carbamate Groups for Gene Delivery J. Mater. Chem. B 2014, 2 ( 19 ) 2920-2928 10.1039/c3tb21506g
40. Navarro, G.; Essex, S.; Sawant, R. R.; Biswas, S.; Nagesha, D.; Sridhar, S.; de Ilarduya, C. T.; Torchilin, V. P. Phospholipid-Modified Polyethylenimine-Based Nanopreparations for siRNA-Mediated Gene Silencing: Implications for Transfection and the Role of Lipid Components Nanomedicine 2014, 10 ( 2 ) 411-419 10.1016/j.nano.2013.07.016
41. Oliveira, S.; Fretz, M. M.; Høgset, A.; Storm, G.; Schiffelers, R. M. Photochemical Internalization Enhances Silencing of Epidermal Growth Factor Receptor through Improved Endosomal Escape of siRNA Biochim. Biophys. Acta, Biomembr. 2007, 1768, 1211-1217 10.1016/j.bbamem.2007.01.013
42. Sahay, G.; Querbes, W.; Alabi, C.; Eltoukhy, A.; Sarkar, S.; Zurenko, C.; Karagiannis, E.; Love, K.; Chen, D.; Zoncu, R.; Buganim, Y.; Schroeder, A.; Langer, R.; Anderson, D. G. Efficiency of siRNA Delivery by Lipid Nanoparticles Is Limited by Endocytic Recycling Nat. Biotechnol. 2013, 31 ( 7 ) 653-658 10.1038/nbt.2614
43. Matsui, K.; Horiuchi, S.; Sando, S.; Sera, T.; Aoyama, Y. RNAi Silencing of Exogenous and Endogenous Reporter Genes Using a Macrocyclic Octaamine as a “Compact” siRNA Carrier. Studies on the Nonsilenced Residual Activity Bioconjugate Chem. 2006, 17, 132-138 10.1021/bc050112l
44. Weecharangsan, W.; Opanasopit, P.; Lee, R. J. In Vitro Gene Transfer Using Cationic Vectors, Electroporation and Their Combination Anticancer Res. 2007, 27, 309-314
45. Bertrand, N.; Wu, J.; Xu, X.; Kamaly, N.; Farokhzad, O. C. Cancer Nanotechnology: The Impact of Passive and Active Targeting in the Era of Modern Cancer Biology Adv. Drug Delivery Rev. 2014, 66, 2-25 10.1016/j.addr.2013.11.009
46. Ozcan, G.; Ozpolat, B.; Coleman, R. L.; Sood, A. K.; Lopez-berestein, G. Preclinical and Clinical Development of siRNA-Based Therapeutics Adv. Drug Delivery Rev. 2015, 87, 108-119 10.1016/j.addr.2015.01.007