B cell-intrinsic toll-like receptor 7 is responsible for the enhanced anti-PEG IgM production following injection of siRNA-containing PEGylated lipoplex in mice

Journal of Controlled Release

Volumn 184, Issue 1, 2014, Pages 1-8

  Hashimoto, Yosuke ^a   Abu Lila, Amr S ^a,b   Shimizu, Taro ^a   Ishida, Tatsuhiro ^a   Kiwada, Hiroshi ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b Zagazig University   (Egypt)

Author keywords

Anti PEG IgM; Innate immunity; PEGylated liposome; Small interfering RNA (siRNA); Toll like receptor 7 (TLR7)

Indexed keywords

CHEMICAL MODIFICATION; IMMUNE SYSTEM; MAMMALS;

ANTI-PEG IGM; INNATE IMMUNITY; PEGYLATED LIPOSOMES; SMALL INTERFERING RNA (SIRNA); TOLL-LIKE RECEPTORS;

LIPOSOMES;

CYTOKINE; IMMUNOGLOBULIN M; LIPOSOME; MACROGOL DERIVATIVE; MEMBRANE PROTEIN; SMALL INTERFERING RNA; TLR7 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 7;

ADOPTIVE TRANSFER; ANIMAL; B LYMPHOCYTE; BAGG ALBINO MOUSE; BLOOD; CHEMISTRY; CYTOLOGY; DEFICIENCY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MALE; SCID MOUSE; SPLEEN;

ADOPTIVE TRANSFER; ANIMALS; B-LYMPHOCYTES; CYTOKINES; IMMUNOGLOBULIN M; LIPOSOMES; MALE; MEMBRANE GLYCOPROTEINS; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, SCID; POLYETHYLENE GLYCOLS; RNA, SMALL INTERFERING; SPLEEN; TOLL-LIKE RECEPTOR 7;

EID: 84899502162     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.04.003     Document Type: Article

References (42)

1. A. Fire, S.Q. Xu, M.K. Montgomery, S.A. Kostas, S.E. Driver, and C.C. Mello Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans Nature 391 1998 806 811
2. M.A. Behlke Progress towards in vivo use of siRNAs Mol. Ther. 13 2006 644 670
3. K.A. Whitehead, R. Langer, and D.G. Anderson Knocking down barriers: advances in siRNA delivery Nat. Rev. Drug Discov. 8 2009 129 138
4. J. Sparks, G. Slobodkin, M. Matar, R. Congo, D. Ulkoski, A. Rea-Ramsey, C. Pence, J. Rice, D. McClure, K.J. Polach, E. Brunhoeber, L. Wilkinson, K. Wallace, K. Anwer, and J.G. Fewell Versatile cationic lipids for siRNA delivery J. Control. Release 158 2012 269 276
5. S. Akhtar, and I.F. Benter Nonviral delivery of synthetic siRNAs in vivo J. Clin. Invest. 117 2007 3623 3632
6. J. Wang, Z. Lu, M.G. Wientjes, and J.L.S. Au Delivery of siRNA therapeutics: barriers and carriers AAPS J. 12 2010 492 503
7. Q. Leng, M.C. Woodle, P.Y. Lu, and A.J. Mixson Advances in systemic siRNA delivery Drug Futur. 34 2009 721 737
8. C. Allen, N. Dos Santos, R. Gallagher, G.N.C. Chiu, Y. Shu, W.M. Li, S.A. Johnstone, A.S. Janoff, L.D. Mayer, M.S. Webb, and M.B. Bally Controlling the physical behavior and biological performance of liposome formulations through use of surface grafted poly(ethylene glycol) Biosci. Rep. 22 2002 225 250
9. T. Ishida, K. Atobe, X.Y. Wang, and H. Kiwada Accelerated blood clearance of PEGylated liposomes upon repeated injections: effect of doxorubicin- encapsulation and high-dose first injection J. Control. Release 115 2006 251 258
10. A. Judge, K. McClintock, J.R. Phelps, and I. Maclachlan Hypersensitivity and loss of disease site targeting caused by antibody responses to PEGylated liposomes Mol. Ther. 13 2006 328 337
11. C.L. Li, X. Zhao, Y.J. Wang, H.Y. Yang, H.X. Li, H. Li, W. Tian, J. Yang, and J.X. Cui Prolongation of time interval between doses could eliminate accelerated blood clearance phenomenon induced by pegylated liposomal topotecan Int. J. Pharm. 443 2013 17 25
12. L.M. Kaminskas, V.M. Mcleod, C.J.H. Porter, and B.J. Boyd Differences in colloidal structure of PEGylated nanomaterials dictate the likelihood of accelerated blood clearance J. Pharm. Sci. 100 2011 5069 5077
13. T. Ishida, M. Ichihara, X.Y. Wang, and H. Kiwada Spleen plays an important role in the induction of accelerated blood clearance of PEGylated liposomes J. Control. Release 115 2006 243 250
14. X.Y. Wang, T. Ishida, and H. Kiwada Anti-PEG IgM elicited by injection of liposomes is involved in the enhanced blood clearance of a subsequent dose of PEGylated liposomes J. Control. Release 119 2007 236 244
15. T. Tagami, K. Nakamura, T. Shimizu, N. Yamazaki, T. Ishida, and H. Kiwada CpG motifs in pDNA-sequences increase anti-PEG IgM production induced by PEG-coated pDNA-lipoplexes J. Control. Release 142 2010 160 166
16. T. Tagami, Y. Uehara, N. Moriyoshi, T. Ishida, and H. Kiwada Anti-PEG IgM production by siRNA encapsulated in a PEGylated lipid nanocarrier is dependent on the sequence of the siRNA J. Control. Release 151 2011 149 154
17. A. Goodchild, N. Nopper, A. King, T. Doan, M. Tanudji, G.M. Arndt, M. Poidinger, L.P. Rivory, and T. Passioura Sequence determinants of innate immune activation by short interfering RNAs BMC Immunol. 10 2009 40
18. V. Hornung, M. Guenthner-Biller, C. Bourquin, A. Ablasser, M. Schlee, S. Uematsu, A. Noronha, M. Manoharan, S. Akira, A. de Fougerolles, S. Endres, and G. Hartmann Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7 Nat. Med. 11 2005 263 270
19. M. Sioud Single-stranded small interfering RNA are more immunostimulatory than their double-stranded counterparts: a central role for 2′-hydroxyl uridines in immune responses Eur. J. Immunol. 36 2006 1222 1230
20. M. Robbins, A. Judge, L. Liang, K. McClintock, E. Yaworski, and I. MacLachlan 2′-O-methyl-modified RNAs act as TLR7 antagonists Mol. Ther. 15 2007 1663 1669
21. C.J. Desmet, and K.J. Ishii Nucleic acid sensing at the interface between innate and adaptive immunity in vaccination Nat. Rev. Immunol. 12 2012 479 491
22. H. Hemmi, T. Kaisho, O. Takeuchi, S. Sato, H. Sanjo, K. Hoshino, T. Horiuchi, H. Tomizawa, K. Takeda, and S. Akira Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway Nat. Immunol. 3 2002 196 200
23. S. Hamm, E. Latz, D. Hangel, T. Muller, P. Yu, D. Golenbock, T. Sparwasser, H. Wagner, and S. Bauer Alternating 2′-O-ribose methylation is a universal approach for generating non-stimulatory siRNA by acting as TLR7 antagonist Immunobiology 215 2010 559 569
24. T. Tagami, T. Suzuki, M. Matsunaga, K. Nakamura, N. Moriyoshi, T. Ishida, and H. Kiwada Anti-angiogenic therapy via cationic liposome-mediated systemic siRNA delivery Int. J. Pharm. 422 2012 280 289
25. T. Ishida, D.L. Iden, and T.M. Allen A combinatorial approach to producing sterically stabilized (Stealth) immunoliposomal drugs FEBS Lett. 460 1999 129 133
26. T. Ishida, X. Wang, T. Shimizu, K. Nawata, and H. Kiwada PEGylated liposomes elicit an anti-PEG IgM response in a T cell-independent manner J. Control. Release 122 2007 349 355
27. H. Harashima, Y. Midori, S. Ohshima, K. Yachi, H. Kikuchi, and H. Kiwada Kinetic analysis of tissue distribution of doxorubicin incorporated in liposomes in rats (II) Biopharm. Drug Dispos. 14 1993 595 608
28. M. Robbins, A. Judge, E. Ambegia, C. Choi, E. Yaworski, L. Palmer, K. McClintock, and I. MacLachlan Misinterpreting the therapeutic effects of small interfering RNA caused by immune stimulation Hum. Gene Ther. 19 2008 991 999
29. A.D. Judge, V. Sood, J.R. Shaw, D. Fang, K. McClintock, and I. MacLachlan Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA Nat. Biotechnol. 23 2005 457 462
30. T. Ishida, M. Harada, X.Y. Wang, M. Ichihara, K. Irimura, and H. Kiwada Accelerated blood clearance of PEGylated liposomes following preceding liposome injection: effects of lipid dose and PEG surface-density and chain length of the first-dose liposomes J. Control. Release 105 2005 305 317
31. A. Judge, and I. Maclachlan Overcoming the innate immune response to small interfering RNA Hum. Gene Ther. 19 2008 111 124
32. M.E. Kleinman, K. Yamada, A. Takeda, V. Chandrasekaran, M. Nozaki, J.Z. Baffi, R.J.C. Albuquerque, S. Yamasaki, M. Itaya, Y.Z. Pan, B. Appukuttan, D. Gibbs, Z.L. Yang, K. Kariko, B.K. Ambati, T.A. Wilgus, L.A. DiPietro, E. Sakurai, K. Zhang, J.R. Smith, E.W. Taylor, and J. Ambati Sequence- and target-independent angiogenesis suppression by siRNA via TLR3 Nature 452 2008 591 597
33. H. Kanzler, F.J. Barrat, E.M. Hessel, and R.L. Coffman Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists Nat. Med. 13 2007 552 559
34. S.R. Crampton, E. Voynova, and S. Bolland Innate pathways to B-cell activation and tolerance Ann. N. Y. Acad. Sci. 1183 2010 58 68
35. D.J. Rawlings, M.A. Schwartz, S.W. Jackson, and A. Meyer-Bahlburg Integration of B cell responses through Toll-like receptors and antigen receptors Nat. Rev. Immunol. 12 2012 282 294
36. C. Pasare, and R. Medzhitov Control of B-cell responses by Toll-like receptors Nature 438 2005 364 368
37. S.P. Kasturi, I. Skountzou, R.A. Albrecht, D. Koutsonanos, T. Hua, H.I. Nakaya, R. Ravindran, S. Stewart, M. Alam, M. Kwissa, F. Villinger, N. Murthy, J. Steel, J. Jacob, R.J. Hogan, A. Garcia-Sastre, R. Compans, and B. Pulendran Programming the magnitude and persistence of antibody responses with innate immunity Nature 470 2011 543 547
38. S. Iwata, K. Yamaoka, H. Niiro, K. Nakano, S.P. Wang, K. Akashi, and Y. Tanaka Amplification of Toll-like receptor-mediated signaling through spleen tyrosine kinase in human B-cell activation J. Allergy Clin. Immunol. 129 2012 1594 1601
39. K. Takeda, T. Kaisho, and S. Akira Toll-like receptors Annu. Rev. Immunol. 21 2003 335 376
40. O. Leavy Dual TLR hit for vaccine success Nat. Rev. Immunol. 11 2011 234 235
41. J. Eckl-Dorna, and F.D. Batista BCR-mediated uptake of antigen linked to TLR9 ligand stimulates B-cell proliferation and antigen-specific plasma cell formation Blood 113 2009 3969 3977
42. S. Shah, and H.J. Federoff Therapeutic potential of vaccines for Alzheimer's disease Immunotherapy 3 2011 287 298