Visualizing lipid-formulated siRNA release from endosomes and target gene knockdown

Nature Biotechnology

Volumn 33, Issue 8, 2015, Pages 870-876

  Wittrup, Anders ^a,b   Ai, Angela ^a   Liu, Xing ^a   Hamar, Peter ^a,c   Trifonova, Radiana ^a   Charisse, Klaus ^d   Manoharan, Muthiah ^d   Kirchhausen, Tomas ^a,e   Lieberman, Judy ^a,e  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b LUND UNIVERSITY   (Sweden)

^c SEMMELWEIS UNIVERSITY   (Hungary)

^d ALNYLAM PHARMACEUTICALS   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENES; MACHINERY; MOLECULAR BIOLOGY; NUCLEIC ACIDS;

CANDIDATE DRUGS; ENDOSOMAL MEMBRANE; ENDOSOMAL RELEASE; GENE KNOCK DOWN; LIPID NANOPARTICLES; LIVE-CELL IMAGING; RNA INTERFERENCE; SMALL INTERFERING RNA;

RNA;

GALECTIN; GREEN FLUORESCENT PROTEIN; LIPID; LIPOPLEX; NANOPARTICLE; SMALL INTERFERING RNA; PHOTOPROTEIN;

ARTICLE; CYTOSOL; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; FEMALE; FLOW CYTOMETRY; GENE DELIVERY SYSTEM; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; INTERNALIZATION; LIMIT OF DETECTION; MACROAUTOPHAGY; PRIORITY JOURNAL; REPORTER GENE; CHEMISTRY; GENETICS; HELA CELL LINE; METABOLISM; PROCEDURES; RNA INTERFERENCE;

ENDOSOMES; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; LIPIDS; LUMINESCENT PROTEINS; NANOPARTICLES; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84938898581     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.3298     Document Type: Article

References (29)

1. Felgner, P.L. et al. Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. Proc. Natl. Acad. Sci. USA 84, 7413-7417 (1987).
2. Elouahabi, A. & Ruysschaert, J.-M. Formation and intracellular trafficking of lipoplexes and polyplexes. Mol. Ther. 11, 336-347 (2005).
3. Kanasty, R., Dorkin, J.R., Vegas, A. & Anderson, D. Delivery materials for siRNA therapeutics. Nat. Mater. 12, 967-977 (2013).
4. Zimmermann, T.S. et al. RNAi-mediated gene silencing in nonhuman primates. Nature 441, 111-114 (2006).
5. Semple, S.C. et al. Rational design of cationic lipids for siRNA delivery. Nat. Biotechnol. 28, 172-176 (2010).
6. Coelho, T. et al. Safety and efficacy of RNAi therapy for transthyretin amyloidosis. N. Engl. J. Med. 369, 819-829 (2013).
7. Gilleron, J. et al. Image-based analysis of lipid nanoparticle-mediated siRNA delivery, intracellular trafficking and endosomal escape. Nat. Biotechnol. 31, 638-646 (2013).
8. Sahay, G. et al. Efficiency of siRNA delivery by lipid nanoparticles is limited by endocytic recycling. Nat. Biotechnol. 31, 653-658 (2013).
9. Payne, C.K., Jones, S.A., Chen, C. & Zhuang, X. Internalization and trafficking of cell surface proteoglycans and proteoglycan-binding ligands. Traffic 8, 389-401 (2007).
10. ur Rehman, Z., Hoekstra, D. & Zuhorn, I.S. Mechanism of polyplex- and lipoplex-mediated delivery of nucleic acids: real-time visualization of transient membrane destabilization without endosomal lysis. ACS Nano 7, 3767-3777 (2013).
11. Li, X. et al. Generation of destabilized green fluorescent protein as a transcription reporter. J. Biol. Chem. 273, 34970-34975 (1998).
12. Thurston, T.L.M., Wandel, M.P., von Muhlinen, N., Foeglein, Á. & Randow, F. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 482, 414-418 (2012).
13. Stalder, L. et al. The rough endoplasmatic reticulum is a central nucleation site of siRNA-mediated RNA silencing. EMBO J. 32, 1115-1127 (2013).
14. Mu, F.T. et al. EEA1 is a conserved a-helical peripheral membrane protein flanked by cysteine "fingers" and contains a calmodulin-binding IQ motif. J. Biol. Chem. 270, 13503-13511 (1995).
15. Huotari, J. & Helenius, A. Endosome maturation. EMBO J. 30, 3481-3500 (2011).
16. Poteryaev, D., Datta, S., Ackema, K., Zerial, M. & Spang, A. Identification of the switch in early-to-late endosome transition. Cell 141, 497-508 (2010).
17. Nechaev, S. et al. Intracellular processing of immunostimulatory CpG-siRNA: Toll-like receptor 9 facilitates siRNA dicing and endosomal escape. J. Control. Release 170, 307-315 (2013).
18. Chen, X. et al. Autophagy induced by calcium phosphate precipitates targets damaged endosomes. J. Biol. Chem. 289, 11162-11174 (2014).
19. Roberts, R. et al. Autophagy and formation of tubulovesicular autophagosomes provide a barrier against nonviral gene delivery. Autophagy 9, 667-682 (2013).
20. Kimura, S., Noda, T. & Yoshimori, T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3, 452-460 (2007).
21. Paz, I. et al. Galectin-3, a marker for vacuole lysis by invasive pathogens. Cell. Microbiol. 12, 530-544 (2010).
22. Maier, M.A. et al. Biodegradable lipids enabling rapidly eliminated lipid nanoparticles for systemic delivery of RNAi therapeutics. Mol. Ther. 21, 1570-1578 (2013).
23. Akinc, A. et al. Targeted delivery of RNAi therapeutics with endogenous and exogenous ligand-based mechanisms. Mol. Ther. 18, 1357-1364 (2010).
24. Alabi, C.A. et al. Multiparametric approach for the evaluation of lipid nanoparticles for siRNA delivery. Proc. Natl. Acad. Sci. USA 110, 12881-12886 (2013).
25. Jayaraman, M. et al. Maximizing the potency of siRNA lipid nanoparticles for hepatic gene silencing in vivo. Angew. Chem. Int. Ed. Engl. 51, 8529-8533 (2012).
26. McNamara, J.O. et al. Cell type-specific delivery of siRNAs with aptamer-siRNA chimeras. Nat. Biotechnol. 24, 1005-1015 (2006).
27. Stewart, S.A. et al. Lentivirus-delivered stable gene silencing by RNAi in primary cells. RNA 9, 493-501 (2003).
28. Sharma, D.K. et al. Glycosphingolipids internalized via caveolar-related endocytosis rapidly merge with the clathrin pathway in early endosomes and form microdomains for recycling. J. Biol. Chem. 278, 7564-7572 (2003).
29. Choudhury, A. et al. Rab proteins mediate Golgi transport of caveola-internalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J. Clin. Invest. 109, 1541-1550 (2002).