A novel mechanism is involved in cationic lipid-mediated functional siRNA delivery

Molecular Pharmaceutics

Volumn 6, Issue 3, 2009, Pages 763-771

  Lu, James J ^a   Langer, Robert ^a,b   Chen, Jianzhu ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

Cationic lipids; Delivery; Pathways mechanisms; siRNA

Indexed keywords

CAVEOLIN; CHOLESTEROL; CLATHRIN; LIPID; LIPOPLEX; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; DRUG DELIVERY SYSTEM; EMBRYO; ENDOCYTOSIS; FEMALE; GENETICS; HUMAN; HUMAN CELL; IMAGING; LIPID RAFT; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; TEMPERATURE;

ANIMALS; CAVEOLINS; CELL LINE; CERCOPITHECUS AETHIOPS; CHLORPROMAZINE; CHOLESTEROL; CLATHRIN; CYTOCHALASIN D; DOPAMINE ANTAGONISTS; ENDOCYTOSIS; HELA CELLS; HUMANS; LIPIDS; NUCLEIC ACID SYNTHESIS INHIBITORS; RNA, SMALL INTERFERING; TEMPERATURE; TRANSFECTION;

EID: 67249105434     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp900023v     Document Type: Article

References (48)

1. Fire, A.; Xu, S.; Montgomery, M. K.; Kostas, S. A.; Driver, S. E.; Mello, C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature (London) 1998, 391, 806-811. (Pubitemid 28099681)
2. Novina, C. D.; Sharp, P. A. The RNAi revolution. Nature (London) 2004, 430, 161-164. (Pubitemid 38902417)
3. Kittler, R.; Buchholz, F. Functional genomic analysis of cell division by endoribonuclease-prepared siRNAs. Cell Cycle 2005, 4, 564-567. (Pubitemid 41359782)
4. Leung, R. K.; Whittaker, P. A. RNA interference: from gene silencing to gene-specific therapeutics. Pharmacol. Ther. 2005, 107, 222-239. (Pubitemid 40910042)
5. Benallaoua, M.; François, M.; Batteux, F.; Thelier, N.; Shyy, J. Y.; Fitting, C.; Tsagris, L.; Boczkowski, J.; Savouret, J. F.; Corvol, M. T.; Poiraudeau, S.; Rannou, F. Pharmacologic induction of heme oxygenase 1 reduces acute inflammatory arthritis in mice. Arthritis Rheum. 2007, 56, 2585-2594. (Pubitemid 47237277)
6. Kong, X.; Zhang, W.; Lockey, R. F.; Auais, A.; Piedimonte, G.; Mohapatra, S. S. Respiratory syncytial virus infection in Fischer 344 rats is attenuated by short interfering RNA against the RSV-NS1 gene. Genet. Vaccines Ther. 2007, 5, 4.
7. 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.; Judge, A. D.; Lam, K.; McClintock, K.; Nechev, L. V.; Palmer, L. R.; Racie, T.; Röhl, I.; Seiffert, S.; Shanmugam, S.; Sood, V.; Soutschek, J.; Toudjarska, I.; Wheat, A. J.; Yaworski, E.; Zedalis, W.; Koteliansky, V.; Manoharan, M.; Vornlocher, H. P.; MacLachlan, I. RNAi-mediated gene silencing in non-human primates. Nature (London) 2006, 441, 111-114. (Pubitemid 43827961)
8. Lau, T. S.; Li, Y.; Kameoka, M.; Ng, T. B.; Wan, D. C. Suppression of HIV replication using RNA interference against HIV-1 integrase. FEBS Lett. 2007, 581, 3253-3259. (Pubitemid 46977367)
9. Thomas, M.; Ge, Q.; Lu, J. J.; Klibanov, A. M.; Chen, J. Polycation-mediated delivery of siRNAs for prophylaxis and treatment of influenza virus infection. Expert Opin. Biol. Ther. 2005, 5, 495-505. (Pubitemid 40593333)
10. Yuan, Z.; Wong, S.; Borrelli, A.; Chung, M. A. Down-regulation of MUC1 in cancer cells inhibits cell migration by promoting E-cadherin/catenin complex formation. Biochem. Biophys. Res. Commun. 2007, 362, 740-746. (Pubitemid 47368156)
11. Larson, S. D.; Jackson, L. N.; Chen, L. A.; Rychahou, P. G.; Evers, B. M. Effectiveness of siRNA uptake in target tissues by various delivery methods. Surgery 2007, 142, 262-269. (Pubitemid 47198678)
12. Fountaine, T. M.; Wood, M. J.; Wade-Martins, R. Delivering RNA interference to the mammalian brain. Curr. Gene Ther. 2005, 5, 399-410. (Pubitemid 41052431)
13. Kumar, P.; Wu, H.; McBride, J. L.; Jung, K. E.; Kim, M. H.; Davidson, B. L.; Lee, S. K.; Shankar, P.; Manjunath, N. Transvascular delivery of small interfering RNA to the central nervous system. Nature (London) 2007, 448, 39-43. (Pubitemid 47037001)
14. Veldhoen, S.; Laufer, S. D.; Trampe, A.; Restle, T. Cellular delivery of small interfering RNA by a non-covalently attached cell-penetrating peptide: quantitative analysis of uptake and biological effect. Nucleic Acids Res. 2006, 34, 6561-6573. (Pubitemid 46017951)
15. Yadava, P.; Roura, D.; Hughes, J. A. Evaluation of two cationic delivery systems for siRNA. Oligonucleotides 2007, 17, 213-222.
16. Gary, D. J.; Puri, N.; Won, Y. Y. Polymer-based siRNA delivery: perspectives on the fundamental and phenomenological distinctions from polymer-based DNA delivery. J. Controlled Release 2007, 121, 64-73. (Pubitemid 47126065)
17. Racz, Z.; Hamar, P. Can siRNA technology provide the tools for gene therapy of the future. Curr. Med. Chem. 2006, 13, 2299-2307. (Pubitemid 44184654)
18. Sen, G. L.; Blau, H. M. Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat. Cell Biol. 2005, 7, 633-636. (Pubitemid 40796987)
19. 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)
20. Godbey, W. T.; Wu, K. K.; Mikos, A. G. Tracking the intracellular path of poly(ethylenimine)/DNA complexes for gene delivery. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 5177-5181. (Pubitemid 29214556)
21. Hoekstra, D.; Rejman, J.; Wasungu, L.; Shi, F.; Zuhorn, I. Gene delivery by cationic lipids: in and out of an endosome. Biochem. Soc. Trans. 2007, 35, 68-71. (Pubitemid 46271811)
22. Zhou, J.; Yockman, J. W.; Kim, S. W.; Kern, S. E. Intracellular kinetics of non-viral gene delivery using polyethylenimine carriers. Pharm. Res. 2007, 24, 1079-1087. (Pubitemid 46798885)
23. Simoes, S.; Pires, P.; Duzgunes, N.; Pedrosa de Lima, M. C. Cationic liposomes as gene transfer vectors: barriers to successful application in gene therapy. Curr. Opin. Mol. Ther. 1999, 1, 147-157. (Pubitemid 29238420)
24. Zabner, J.; Fasbender, A. J.; Moninger, T.; Poellinger, K. A.; Welsh, M. J. Cellular and molecular barriers to gene transfer by a cationic lipid. J. Biol. Chem. 1995, 270, 18997-19007.
25. Orth, J. D.; Krueger, E. W.; Cao, H.; McNiven, M. A. The large GTPase dynamin regulates Actin comet formation and movement in living cells. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 167-172. (Pubitemid 34060335)
26. Trouet, D.; Hermans, D.; Droogmans, G.; Nilius, B.; Eggermont, J. Inhibition of volume-regulated anion channels by dominant-negative caveolin-1. Biochem. Biophys. Res. Commun. 2001, 284, 461-465. (Pubitemid 32917999)
27. Dautry-Varsat, A. Receptor-mediated endocytosis: the intracellular journey of transferrin and its receptor. Biochimie 1986, 68, 375-381. (Pubitemid 16075046)
28. Subtil, A.; Hemar, A.; Dautry-Varsat, A. Rapid endocytosis of interleukin 2 receptors when clathrin-coated pit endocytosis is inhibited. J. Cell Sci. 1994, 107, 3461-3468.
29. van der Bliek, A. M.; Redelmeier, T. E.; Damke, H.; Tisdale, E. J.; Meyerowitz, E. M.; Schmid, S. L. Mutations in human dynamin block an intermediate stage in coated vesicle formation. J. Cell Biol. 1993, 122, 553-563. (Pubitemid 23226673)
30. Herskovits, J. S.; Burgess, C. C.; Obar, R. A.; Vallee, R. B. Effects of mutant rat dynamin on endocytosis. J. Cell Biol. 1993, 122, 565-578. (Pubitemid 23226674)
31. Umeda, M.; Nojima, S.; Inoue, K. Effect of lipid composition on HVJ-mediated fusion of glycophorin liposomes to erythrocytes. J. Biochem. 1985, 97, 1301-1310. (Pubitemid 15098397)
32. Grimmer, S.; van Deurs, B.; Sandvig, K. Membrane ruffling and macropinocytosis in A431 cells require cholesterol. J. Cell Sci. 2002, 115, 2953-2962. (Pubitemid 34905660)
33. Ushio-Fukai, M.; Hilenski, L.; Santanam, N.; Becker, P. L.; Ma, Y.; Griendling, K. K.; Alexander, R. W. Cholesterol depletion inhibits epidermal growth factor receptor transactivation by angiotensin II in vascular smooth muscle cells: role of cholesterol-rich microdomains and focal adhesions in angiotensin II signaling. J. Biol. Chem. 2001, 276, 48269-48275. (Pubitemid 37370733)
34. Rothberg, K. G.; Ying, Y. S.; Kamen, B. A.; Anderson, R. G. Cholesterol controls the clustering of the glycophospholipid-anchored membrane receptor for 5-methyltetrahydrofolate. J. Cell Biol. 1990, 111, 2931-2938. (Pubitemid 120034032)
35. Nichols, B. Caveosomes and endocytosis of lipid rafts. J. Cell Sci. 2003, 116, 4707-4714.
36. Parton, R. G.; Richards, A. A. Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 2003, 4, 724-738. (Pubitemid 37361854)
37. Kobayashi, T.; Takahashi, M.; Nagatsuka, Y.; Hirabayashi, Y. Lipid rafts: new tools and a new component. Biol. Pharm. Bull. 2006, 29, 1526-1531. (Pubitemid 44166345)
38. Sillence, D. J. New insights into glycosphingolipid functionss storage, lipid rafts, and translocators. Int. Rev. Cytol. 2007, 262, 151-189. (Pubitemid 47031308)
39. von Delwig, A.; Hilkens, C. M.; Altmann, D. M.; Holmdahl, R.; Isaacs, J. D.; Harding, C. V.; Robertson, H.; McKie, N.; Robinson, J. H. Inhibition of macropinocytosis blocks antigen presentation of type II collagen in vitro and in vivo in HLA-DR1 transgenic mice. Arthritis Res. Ther. 2006, 8, R93.
40. Zuhorn, I. S.; Kalicharan, R.; Hoekstra, D. Lipoplex-mediated transfection of mammalian cells occurs through the cholesterol-dependent clathrin-mediated pathway of endocytosis. J. Biol. Chem. 2002, 277, 18021-18028. (Pubitemid 34967614)
41. Zhou, X.; Huang, L. DNA transfection mediated by cationic liposomes containing lipopolylysine: characterization and mechanism of action. Biochim. Biophys. Acta 1994, 1189, 195-203. (Pubitemid 24042719)
42. Friend, D. S.; Papahadjopoulos, D.; Debs, R. J. Endocytosis and intracellular processing accompanying transfection mediated by cationic liposomes. Biochim. Biophys. Acta 1996, 1278, 41-50. (Pubitemid 26042269)
43. Gao, X.; Huang, L. Cationic liposome-mediated gene transfer. Gene Ther. 1995, 2, 710-722. (Pubitemid 26043284)
44. Kawaura, C.; Noguchi, A.; Furuno, T.; Nakanishi, M. Atomic force microscopy for studying gene transfection mediated by cationic liposomes with a cationic cholesterol derivative. FEBS Lett. 1998, 421, 69-72. (Pubitemid 28068821)
45. Oberle, V.; Bakowsky, U.; Zuhorn, I. S.; Hoekstra, D. Lipoplex formation under equilibrium conditions reveals a three-step mechanism. Biophys. J. 2000, 79, 1447-1454. (Pubitemid 30677061)
46. Pires, P.; Simões, S.; Nir, S.; Gaspar, R.; Düzgünes, N.; Pedroso de Lima, M. C. Interaction of cationic liposomes and their DNA complexes with monocytic leukemia cells. Biochim. Biophys. Acta 1999, 1418, 71-84. (Pubitemid 29182747)
47. Stegmann, T.; Legendre, J. Y. Gene transfer mediated by cationic lipids: lack of a correlation between lipid mixing and transfection. Biochim. Biophys. Acta 1997, 1325, 71-79. (Pubitemid 27138477)
48. Elouahabi, A.; Thiry, M.; Pector, V.; Ruysschaert, J. M.; Vandenbranden, M. Calorimetry of cationic liposome-DNA complex and intracellular visualization of the complexes. Methods Enzymol. 2003, 373, 313-332. (Pubitemid 41103291)