Intracellular processing of immunostimulatory CpG-siRNA: Toll-like receptor 9 facilitates siRNA dicing and endosomal escape

Journal of Controlled Release

Volumn 170, Issue 3, 2013, Pages 307-315

  Nechaev, Sergey ^a   Gao, Chan ^a   Moreira, Dayson ^a   Swiderski, Piotr ^a   Jozwiak, Agnieszka ^a   Kowolik, Claudia M ^a   Zhou, Jiehua ^a   Armstrong, Brian ^a   Raubitschek, Andrew ^a   Rossi, John J ^a   Kortylewski, Marcin ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

CpG; Cytoplasmic release; Dicer; Endosomal escape; SiRNA; TLR9

Indexed keywords

CELL MEMBRANES; GENE THERAPY; GENETIC ENGINEERING; MACHINERY; MOLECULAR BIOLOGY; RNA;

CPG; CYTOPLASMIC RELEASE; DICER; ENDOSOMAL ESCAPES; ENDOSOMES; GENE SILENCING; RNA INTERFERENCE; SIRNA; TLR9; TOLL-LIKE RECEPTOR 9;

MACROPHAGES;

CPG OLIGODEOXYNUCLEOTIDE; DICER; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 9;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOSOME; GENE SILENCING; GENE TARGETING; IMMUNOSTIMULATION; MACROPHAGE; MOUSE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PRIORITY JOURNAL; RNA INTERFERENCE; TARGET CELL;

CPG; CYTOPLASMIC RELEASE; DICER; ENDOSOMAL ESCAPE; SIRNA; TLR9;

ANIMALS; CELL LINE; CELL LINE, TUMOR; CPG ISLANDS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RNA, SMALL INTERFERING; STAT3 TRANSCRIPTION FACTOR; TOLL-LIKE RECEPTOR 9;

EID: 84885145424     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.06.007     Document Type: Article

References (43)

1. E. Song, P. Zhu, S.K. Lee, D. Chowdhury, S. Kussman, D.M. Dykxhoorn, Y. Feng, D. Palliser, D.B. Weiner, P. Shankar, W.A. Marasco, J. Lieberman, Antibody mediated in vivo delivery of small interfering RNAs via cell-surface receptors, Nat. Biotechnol. 23 (6) (2005) 709-717. (Pubitemid 41716361)
2. J.O. McNamara II, E.R. Andrechek, Y. Wang, K.D. Viles, R.E. Rempel, E. Gilboa, B.A. Sullenger, P.H. Giangrande, Cell type-specific delivery of siRNAs with aptamer-siRNA chimeras, Nat. Biotechnol. 24 (8) (2006) 1005-1015. (Pubitemid 44215395)
3. H. Poeck, R. Besch, C. Maihoefer, M. Renn, D. Tormo, S.S. Morskaya, S. Kirschnek, E. Gaffal, J. Landsberg, J. Hellmuth, A. Schmidt, D. Anz, M. Bscheider, T. Schwerd, C. Berking, C. Bourquin, U. Kalinke, E. Kremmer, H. Kato, S. Akira, R. Meyers, G. Hacker, M. Neuenhahn, D. Busch, J. Ruland, S. Rothenfusser, M. Prinz, V. Hornung, S. Endres, T. Tuting, G. Hartmann, 5'-Triphosphate-siRNA: turning gene silencing and Rig-I activation against melanoma, Nat. Med. 14 (11) (2008) 1256-1263.
4. J.P. Dassie, X.Y. Liu, G.S. Thomas, R.M. Whitaker, K.W. Thiel, K.R. Stockdale, D.K. Meyerholz, A.P. McCaffrey, J.O. McNamara II, P.H. Giangrande, Systemic administration of optimized aptamer-siRNA chimeras promotes regression of PSMA-expressing tumors, Nat. Biotechnol. 27 (9) (2009) 839-849.
5. F. Pastor, D. Kolonias, P.H. Giangrande, E. Gilboa, Induction of tumour immunity by targeted inhibition of nonsense-mediated mRNA decay, Nature 465 (7295) (2010) 227-230.
6. B.J. Li, Q. Tang, D. Cheng, C. Qin, F.Y. Xie, Q. Wei, J. Xu, Y. Liu, B.J. Zheng, M.C. Woodle, N. Zhong, P.Y. Lu, Using siRNA in prophylactic and therapeutic regimens against SARS coronavirus in Rhesus macaque, Nat. Med. 11 (9) (2005) 944-951. (Pubitemid 41294439)
7. T.S. Zimmermann, A.C. Lee, A. Akinc, B. Bramlage, D. Bumcrot, M.N. Fedoruk, J. Harborth, J.A. Heyes, L.B. Jeffs, M. John, A.D. Judge, K. Lam, K. McClintock, L.V. Nechev, L.R. Palmer, T. Racie, I. Rohl, S. Seiffert, S. Shanmugam, V. Sood, J. Soutschek, I. Toudjarska, A.J. Wheat, E. Yaworski, W. Zedalis, V. Koteliansky, M. Manoharan, H.P. Vornlocher, I. MacLachlan, RNAi-mediated gene silencing in non-human primates, Nature 441 (7089) (2006) 111-114.
8. M.E. Davis, J.E. Zuckerman, C.H. Choi, D. Seligson, A. Tolcher, C.A. Alabi, Y. Yen, J.D. Heidel, A. Ribas, Evidence of RNAi in humans from systemically administered siRNA via targeted nanoparticles, Nature 464 (7291) (2010) 1067-1070.
9. D. Castanotto, J.J. Rossi, The promises and pitfalls of RNA-interference-based therapeutics, Nature 457 (7228) (2009) 426-433.
10. J. Nguyen, F.C. Szoka, Nucleic acid delivery: the missing pieces of the puzzle? Acc. Chem. Res. 45 (7) (2012) 1153-1162.
11. G.R. Rettig, M.A. Behlke, Progress toward in vivo use of siRNAs-II, Mol. Ther. 20 (3) (2012) 483-512.
12. O.V. Vieira, R.J. Botelho, S. Grinstein, Phagosome maturation: aging gracefully, Biochem. J. 366 (Pt. 3) (2002) 689-704.
13. E. Billy, V. Brondani, H. Zhang, U. Muller, W. Filipowicz, Specific interference with gene expression inducedbylong, double-stranded RNA inmouse embryonal terato-carcinoma cell lines, Proc. Natl. Acad. Sci. U. S. A. 98 (25) (2001) 14428-14433. (Pubitemid 33121408)
14. P. Provost, D. Dishart, J. Doucet, D. Frendewey, B. Samuelsson, O. Radmark, Ribo-nuclease activity and RNA binding of recombinant human Dicer, EMBO J. 21 (21) (2002) 5864-5874. (Pubitemid 35315284)
15. D. Gibbings, O. Voinnet, Control of RNA silencing and localization by endolysosomes, Trends Cell Biol. 20 (8) (2010) 491-501.
16. T.P. Chendrimada, K.J. Finn, X. Ji, D. Baillat, R.I. Gregory, S.A. Liebhaber, A.E. Pasquinelli, R. Shiekhattar, MicroRNA silencing through RISC recruitment of eIF6, Nature 447 (7146) (2007) 823-828. (Pubitemid 46920131)
17. D.H. Kim, M.A. Behlke, S.D. Rose, M.S. Chang, S. Choi, J.J. Rossi, Synthetic dsRNA Dicer substrates enhance RNAi potency and efficacy, Nat. Biotechnol. 23 (2) (2005) 222-226. (Pubitemid 40255333)
18. M. Kortylewski, P. Swiderski, A. Herrmann, L. Wang, C. Kowolik, M. Kujawski, H. Lee, A. Scuto, Y. Liu, C. Yang, J. Deng, H.S. Soifer, A. Raubitschek, S. Forman, J.J. Rossi, D.M. Pardoll, R. Jove, H. Yu, In vivo delivery of siRNA to immune cells by conjugation to a TLR9 agonist enhances antitumor immune responses, Nat. Biotechnol. 27 (10) (2009) 925-932.
19. H. Lee, J. Deng, M. Kujawski, C. Yang, Y. Liu, A. Herrmann, M. Kortylewski, D. Horne, G. Somlo, S. Forman, R. Jove, H. Yu, STAT3-induced S1PR1 expression is crucial for persistent STAT3 activation in tumors, Nat. Med. 16 (12) (2010) 1421-1428.
20. J. Deng, Y. Liu, H. Lee, A. Herrmann, W. Zhang, C. Zhang, S. Shen, S.J. Priceman, M. Kujawski, S.K. Pal, A. Raubitschek, D.S. Hoon, S. Forman, R.A. Figlin, J. Liu, R. Jove, H. Yu, S1PR1-STAT3 signaling is crucial for myeloid cell colonization at future metastatic sites, Cancer Cell 21 (5) (2012) 642-654.
21. Q. Zhang, D.M. Hossain, S. Nechaev, A. Kozlowska, W. Zhang, Y. Liu, C.M. Kowolik, P. Swiderski, J.J. Rossi, S. Forman, S. Pal, R. Bhatia, A. Raubitschek, H. Yu, M. Kortylewski, TLR9-mediated siRNA delivery for targeting of normal and malignant human hematopoietic cells in vivo, Blood 121 (8) (2013) 1304-1315.
22. S.D. Rose, D.H. Kim, M. Amarzguioui, J.D. Heidel, M.A. Collingwood, M.E. Davis, J.J. Rossi, M.A. Behlke, Functional polarity is introduced by Dicer processing of short substrate RNAs, Nucleic Acids Res. 33 (13) (2005) 4140-4156. (Pubitemid 41487274)
23. F.M. Marim, T.N. Silveira, D.S. Lima Jr., D.S. Zamboni, A method for generation of bone marrow-derived macrophages from cryopreserved mouse bone marrow cells, PLoS One 5 (12) (2010) e15263.
24. M. Kortylewski, M. Kujawski, T. Wang, S. Wei, S. Zhang, S. Pilon-Thomas, G. Niu, H. Kay, J. Mule, W.G. Kerr, R. Jove, D. Pardoll, H. Yu, Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity, Nat. Med. 11 (12) (2005) 1314-1321. (Pubitemid 41752912)
25. M. Gursel, I. Gursel, H.S. Mostowski, D.M. Klinman, CXCL16 influences the nature and specificity of CpG-induced immune activation, J. Immunol. 177 (3) (2006) 1575-1580. (Pubitemid 44092492)
26. P. Zhu, X. Liu, L.S. Treml, M.P. Cancro, B.D. Freedman, Mechanism and regulatory function of CpG signaling via scavenger receptor B1 in primary B cells, J. Biol. Chem. 284 (34) (2009) 22878-22887.
27. S. Acton, D. Resnick, M. Freeman, Y. Ekkel, J. Ashkenas, M. Krieger, The collagenous domains of macrophage scavenger receptors and complement component C1q mediate their similar, but not identical, binding specificities for polyanionic ligands, J. Biol. Chem. 268 (5) (1993) 3530-3537. (Pubitemid 23070994)
28. O. Soderberg, M. Gullberg, M. Jarvius, K. Ridderstrale, K.J. Leuchowius, J. Jarvius, K. Wester, P. Hydbring, F. Bahram, L.G. Larsson, U. Landegren, Direct observation of individual endogenous protein complexes in situ by proximity ligation, Nat. Methods 3 (12) (2006) 995-1000. (Pubitemid 44782698)
29. S.E. Ewald, B.L. Lee, L. Lau, K.E. Wickliffe, G.P. Shi, H.A. Chapman, G.M. Barton, The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor, Nature 456 (7222) (2008) 658-662.
30. M. Robbins, A. Judge, L. Liang, K. McClintock, E. Yaworski, I. MacLachlan, 2'-O-methyl-modified RNAs act as TLR7 antagonists, Mol. Ther. 15 (9) (2007) 1663-1669. (Pubitemid 47289010)
31. F.R. Maxfield, T.E. McGraw, Endocytic recycling, Nat. Rev. Mol. Cell Biol. 5 (2) (2004) 121-132. (Pubitemid 38160255)
32. B. Park, L. Buti, S. Lee, T. Matsuwaki, E. Spooner, M.M. Brinkmann, M. Nishihara, H.L. Ploegh, Granulin is a soluble cofactor for toll-like receptor 9 signaling, Immunity 34 (4) (2011) 505-513.
33. E. Latz, A. Schoenemeyer, A. Visintin, K.A. Fitzgerald, B.G. Monks, C.F. Knetter, E. Lien, N.J. Nilsen, T. Espevik, D.T. Golenbock, TLR9 signals after translocating from the ER to CpG DNA in the lysosome, Nat. Immunol. 5 (2) (2004) 190-198. (Pubitemid 38208361)
34. M. Dominska, D.M. Dykxhoorn, Breaking down the barriers: siRNA delivery and endosome escape, J. Cell Sci. 123 (Pt. 8) (2010) 1183-1189.
35. T.P. Chendrimada, R.I. Gregory, E. Kumaraswamy, J. Norman, N. Cooch, K. Nishikura, R. Shiekhattar, TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing, Nature 436 (7051) (2005) 740-744. (Pubitemid 41117280)
36. L. Li, D. Zhu, L. Huang, J. Zhang, Z. Bian, X. Chen, Y. Liu, C.Y. Zhang, K. Zen, Argonaute 2 complexes selectively protect the circulating microRNAs in cell-secreted microvesicles, PLoS One 7 (10) (2012) e46957.
37. M.A. Welte, Bidirectional transport along microtubules, Curr. Biol. 14 (13) (2004) R525-R537. (Pubitemid 38893974)
38. E. Gagnon, S. Duclos, C. Rondeau, E. Chevet, P.H. Cameron, O. Steele-Mortimer, J. Paiement, J.J. Bergeron, M. Desjardins, Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages, Cell 110 (1) (2002) 119-131. (Pubitemid 34874611)
39. C. Kurts, B.W. Robinson, P.A. Knolle, Cross-priming in health and disease, Nat. Rev. Immunol. 10 (6) (2010) 403-414.
40. S.P. Kasturi, B. Pulendran, Cross-presentation: avoiding trafficking chaos? Nat. Immunol. 9 (5) (2008) 461-463. (Pubitemid 351560512)
41. J.M. Blander, R. Medzhitov, On regulation of phagosome maturation and antigen presentation, Nat. Immunol. 7 (10) (2006) 1029-1035. (Pubitemid 44420647)
42. S.K. Datta, V. Redecke, K.R. Prilliman, K. Takabayashi, M. Corr, T. Tallant, J. DiDonato, R. Dziarski, S. Akira, S.P. Schoenberger, E. Raz, A subset of Toll-like receptor ligands induces cross-presentation by bone marrow-derived dendritic cells, J. Immunol. 170 (8) (2003) 4102-4110. (Pubitemid 36428173)
43. J. Mouries, G. Moron, G. Schlecht, N. Escriou, G. Dadaglio, C. Leclerc, Plasmacytoid dendritic cells efficiently cross-prime naive T cells in vivo after TLR activation, Blood 112 (9) (2008) 3713-3722.