Intra-endosomal trafficking mediated by lysobisphosphatidic acid contributes to intracellular release of phosphorothioate-modified antisense oligonucleotides

Nucleic Acids Research

Volumn 45, Issue 9, 2017, Pages 5309-5322

  Wang, Shiyu ^a   Sun, Hong ^a   Tanowitz, Michael ^a   Liang, Xue Hai ^a   Crooke, Stanley T ^a  

^a ISIS PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALIX PROTEIN; ANTISENSE OLIGONUCLEOTIDE; BINDING PROTEIN; EARLY ENDOSOME ANTIGEN 1; ENSITUXIMAB; ESCRT PROTEIN; HRS PROTEIN; LYSOBISPHOSPHATIDIC ACID; LYSOPHOSPHATIDIC ACID; OLIGONUCLEOTIDE PHOSPHOROTHIOATE; RAB PROTEIN; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UNCLASSIFIED DRUG; BIS(MONOACYLGLYCERYL)PHOSPHATE; CALCIUM BINDING PROTEIN; CARRIER PROTEIN; CELL CYCLE PROTEIN; LYSOPHOSPHOLIPID; MEMBRANE PROTEIN; MONOACYLGLYCEROL; NPC1 PROTEIN, HUMAN; PDCD6IP PROTEIN, HUMAN;

ARTICLE; CELL CULTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG RELEASE; DRUG UPTAKE; ENDOCYTOSIS; ENDOSOME; FLOW CYTOMETRY; GENE FUSION; GENE TARGETING; HUMAN; HUMAN CELL; INTERNALIZATION; INTRACELLULAR TRANSPORT; LIPID BILAYER; MULTIVESICULAR BODY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; BIOLOGICAL MODEL; CHEMISTRY; INTRACELLULAR SPACE; KINETICS; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE;

BIOLOGICAL TRANSPORT; CALCIUM-BINDING PROTEINS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; ENDOCYTOSIS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; HUMANS; INTRACELLULAR SPACE; KINETICS; LYSOPHOSPHOLIPIDS; MEMBRANE GLYCOPROTEINS; MODELS, BIOLOGICAL; MONOGLYCERIDES; OLIGONUCLEOTIDES, ANTISENSE; PHOSPHOROTHIOATE OLIGONUCLEOTIDES;

EID: 85027244205     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkx231     Document Type: Article

References (44)

1. Bennett,C.F. and Swayze,E.E. RNA targeting therapeutics: molecular mechanisms of antisense oligonucleotides as a therapeutic platform. Annu. Rev. Pharmacol. Toxicol., 50, 259-293.
2. Beltinger,C., Saragovi,H.U., Smith,R.M., LeSauteur,L., Shah,N., DeDionisio,L., Christensen,L., Raible,A., Jarett,L. and Gewirtz,A.M. (1995) Binding, uptake, and intracellular trafficking of phosphorothioate-modified oligodeoxynucleotides. J. Clin. Invest., 95, 1814-1823.
3. Crooke,S.T. (2004) Progress in antisense technology. Annu. Rev. Med., 55, 61-95.
4. Juliano,R.L. and Carver,K. (2015) Cellular uptake and intracellular trafficking of oligonucleotides. Adv. Drug Deliv. Rev., 87, 35-45.
5. Juliano,R.L., Ming,X. and Nakagawa,O. (2012) Cellular uptake and intracellular trafficking of antisense and siRNA oligonucleotides. Bioconjug. Chem., 23, 147-157.
6. Koller,E., Vincent,T.M., Chappell,A., De,S., Manoharan,M. and Bennett,C.F. (2011) Mechanisms of single-stranded phosphorothioate modified antisense oligonucleotide accumulation in hepatocytes. Nucleic Acids Res., 39, 4795-4807.
7. Juliano,R.L., Ming,X., Carver,K. and Laing,B. (2014) Cellular uptake and intracellular trafficking of oligonucleotides: implications for oligonucleotide pharmacology. Nucleic Acid Therap., 24, 101-113.
8. Wang,S., Sun,H., Tanowitz,M., Liang,X.H. and Crooke,S.T. (2016) Annexin A2 facilitates endocytic trafficking of antisense oligonucleotides. Nucleic Acids Res., 44, 7314-7330.
9. Scott,C.C., Vacca,F. and Gruenberg,J. (2014) Endosome maturation, transport and functions. Semin. Cell Dev. Biol., 31, 2-10.
10. Im,Y.J., Wollert,T., Boura,E. and Hurley,J.H. (2009) Structure and function of the ESCRT-II-III interface in multivesicular body biogenesis. Dev. Cell, 17, 234-243.
11. Piper,R.C. and Katzmann,D.J. (2007) Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol., 23, 519-547.
12. Odorizzi,G. (2006) The multiple personalities of Alix. J. Cell Sci., 119, 3025-3032.
13. Kobayashi,T., Stang,E., Fang,K.S., de Moerloose,P., Parton,R.G. and Gruenberg,J. (1998) A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature, 392, 193-197.
14. Wickner,W. and Schekman,R. (2008) Membrane fusion. Nat. Struct. Mol. Biol., 15, 658-664.
15. Bissig,C. and Gruenberg,J. (2014) ALIX and the multivesicular endosome: ALIX in Wonderland. Trends Cell Biol., 24, 19-25.
16. Liang,X.H., Sun,H., Shen,W. and Crooke,S.T. (2015) Identification and characterization of intracellular proteins that bind oligonucleotides with phosphorothioate linkages. Nucleic Acids Res., 43, 2927-2945.
17. Ceresa,B.P., Lotscher,M. and Schmid,S.L. (2001) Receptor and membrane recycling can occur with unaltered efficiency despite dramatic Rab5(q79l)-induced changes in endosome geometry. J. Biol. Chem., 276, 9649-9654.
18. Li,G. and Stahl,P.D. (1993) Structure-function relationship of the small GTPase rab5. J. Biol. Chem., 268, 24475-24480.
19. Ghossoub,R., Lembo,F., Rubio,A., Gaillard,C.B., Bouchet,J., Vitale,N., Slavik,J., Machala,M. and Zimmermann,P. (2014) Syntenin-ALIX exosome biogenesis and budding into multivesicular bodies are controlled by ARF6 and PLD2. Nat. Commun., 5, 3477.
20. Jefferies,H.B., Cooke,F.T., Jat,P., Boucheron,C., Koizumi,T., Hayakawa,M., Kaizawa,H., Ohishi,T., Workman,P., Waterfield,M.D. et al. (2008) A selective PIKfyve inhibitor blocks PtdIns (3,5) P (2) production and disrupts endomembrane transport and retroviral budding. EMBO Rep., 9, 164-170.
21. Savina,A., Furlan,M., Vidal,M. and Colombo,M.I. (2003) Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J. Biol. Chem., 278, 20083-20090.
22. Varkouhi,A.K., Scholte,M., Storm,G. and Haisma,H.J. (2011) Endosomal escape pathways for delivery of biologicals. J. Controlled Release, 151, 220-228.
23. Kobayashi,T., Beuchat,M.H., Chevallier,J., Makino,A., Mayran,N., Escola,J.M., Lebrand,C., Cosson,P., Kobayashi,T. and Gruenberg,J. (2002) Separation and characterization of late endosomal membrane domains. J. Biol. Chem., 277, 32157-32164.
24. Dumas,J.J., Merithew,E., Sudharshan,E., Rajamani,D., Hayes,S., Lawe,D., Corvera,S. and Lambright,D.G. (2001) Multivalent endosome targeting by homodimeric EEA1. Mol. Cell, 8, 947-958.
25. Bissig,C. and Gruenberg,J. (2013) Lipid sorting and multivesicular endosome biogenesis. Cold Spring Harbor Perspect. Biol., 5, a016816.
26. Pasqual,G., Rojek,J.M., Masin,M., Chatton,J.Y. and Kunz,S. (2011) Old world arenaviruses enter the host cell via the multivesicular body and depend on the endosomal sorting complex required for transport. PLoS Pathogens, 7, e1002232.
27. Sparrow,S.M., Carter,J.M., Ridgway,N.D., Cook,H.W. and Byers,D.M. (1999) U18666A inhibits intracellular cholesterol transport and neurotransmitter release in human neuroblastoma cells. Neurochem. Res., 24, 69-77.
28. Sobo,K., Le Blanc,I., Luyet,P.P., Fivaz,M., Ferguson,C., Parton,R.G., Gruenberg,J. and van der Goot,F.G. (2007) Late endosomal cholesterol accumulation leads to impaired intra-endosomal trafficking. PLoS One, 2, e851.
29. Liscum,L. (2000) Niemann-Pick type C mutations cause lipid traffic jam. Traffic, 1, 218-225.
30. Lima,W.F., Murray,H.M., Damle,S.S., Hart,C.E., Hung,G., De Hoyos,C.L., Liang,X.H. and Crooke,S.T. (2016) Viable RNaseH1 knockout mice show RNaseH1 is essential for R loop processing, mitochondrial and liver function. Nucleic Acids Res., 44, 5299-5312.
31. Shen,W., Liang,X.H. and Crooke,S.T. (2014) Phosphorothioate oligonucleotides can displace NEAT1 RNA and form nuclear paraspeckle-like structures. Nucleic Acids Res., 42, 8648-8662.
32. Liang,X.H., Shen,W., Sun,H., Kinberger,G.A., Prakash,T.P., Nichols,J.G. and Crooke,S.T. (2016) Hsp90 protein interacts with phosphorothioate oligonucleotides containing hydrophobic 2-modifications and enhances antisense activity. Nucleic Acids Res., 44, 3892-3907.
33. Shahabipour,F., Barati,N., Johnston,T.P., Derosa,G., Maffioli,P. and Sahebkar,A. (2017) Exosomes: Nanoparticulate tools for RNA interference and drug delivery. J. Cell. Physiol., doi:10.1002/jcp.25766.
34. Alam,M.R., Dixit,V., Kang,H., Li,Z.B., Chen,X., Trejo,J., Fisher,M. and Juliano,R.L. (2008) Intracellular delivery of an anionic antisense oligonucleotide via receptor-mediated endocytosis. Nucleic Acids Res., 36, 2764-2776.
35. Ming,X., Alam,M.R., Fisher,M., Yan,Y., Chen,X. and Juliano,R.L. (2010) Intracellular delivery of an antisense oligonucleotide via endocytosis of a G protein-coupled receptor. Nucleic Acids Res., 38, 6567-6576.
36. Miller,C.M., Donner,A.J., Blank,E.E., Egger,A.W., Kellar,B.M., Ostergaard,M.E., Seth,P.P. and Harris,E.N. (2016) Stabilin-1 and Stabilin-2 are specific receptors for the cellular internalization of phosphorothioate-modified antisense oligonucleotides (ASOs) in the liver. Nucleic Acids Res., 44, 2782-2794.
37. Crooke,S.T.,Wang,S., Vickers,T.A., Shen,W. and Liang,X.H. (2017) Cellular uptake and trafficking of antisense oligonucleotides. Nat. Biotechnol., 35, 230-237.
38. Wollert,T., Yang,D., Ren,X., Lee,H.H., Im,Y.J. and Hurley,J.H. (2009) The ESCRT machinery at a glance. J. Cell Sci., 122, 2163-2166.
39. Stuffers,S., Sem Wegner,C., Stenmark,H. and Brech,A. (2009) Multivesicular endosome biogenesis in the absence of ESCRTs. Traffic, 10, 925-937.
40. Martens,S. and McMahon,H.T. (2008) Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol., 9, 543-556.
41. Frolov,V.A., Dunina-Barkovskaya,A.Y., Samsonov,A.V. and Zimmerberg,J. (2003) Membrane permeability changes at early stages of influenza hemagglutinin-mediated fusion. Biophys. J., 85, 1725-1733.
42. Blumenthal,R., Clague,M.J., Durell,S.R. and Epand,R.M. (2003) Membrane fusion. Chem. Rev., 103, 53-69.
43. 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.
44. 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.