Suppressive effects of sugar-modified cationic liposome/NF-κB decoy complexes on adenovirus vector-induced innate immune responses

Journal of Controlled Release

Volumn 133, Issue 2, 2009, Pages 139-145

  Huang, Haiying ^a   Sakurai, Fuminori ^a   Higuchi, Yuriko ^b   Kawakami, Shigeru ^b   Hashida, Mitsuru ^b,c   Kawabata, Kenji ^a   Mizuguchi, Hiroyuki ^a,d  

^a NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

Adenovirus vector; Cationic liposome; Hepatotoxicity; Innate immunity; NF B decoy

Indexed keywords

COMPLEXATION; DENDRIMERS; DYES; ELECTROPHORETIC MOBILITY; GENETIC ENGINEERING; IMMUNOLOGY; LIPOSOMES; MACROPHAGES; PHOSPHOLIPIDS; SUGAR (SUCROSE); SUGARS;

ADENOVIRUS VECTOR; ADENOVIRUS VECTORS; CATIONIC LIPOSOME; CATIONIC LIPOSOMES; COUNTER-MEASURES; CYTOKINE; DENDRITIC CELLS; ELECTROPHORETIC MOBILITY SHIFT ASSAYS; GENE THERAPIES; HEPATOTOXICITY; INNATE IMMUNE RESPONSES; INNATE IMMUNITY; KUPFFER CELLS; SERUM LEVELS; SPLENOCYTES; TWO TYPES;

VECTORS;

ADENOVIRUS VECTOR; CYTOKINE; FUCOSYLATED CATIONIC LIPOSOME NUCLEAR FACTOR KAPPA B; INTERLEUKIN 12; LIPOSOME; MANNOSYLATED CATIONIC LIPOSOME NUCLEAR FACTOR KAPPA B; SUGAR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BLOOD LEVEL; COMPLEX FORMATION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; GEL MOBILITY SHIFT ASSAY; INNATE IMMUNITY; KUPFFER CELL; LIPOSOMAL DELIVERY; LIVER TOXICITY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL;

ACTIVE TRANSPORT, CELL NUCLEUS; ADENOVIRIDAE; ALANINE TRANSAMINASE; ANIMALS; ASPARTATE AMINOTRANSFERASES; FEMALE; FUCOSE; GENE EXPRESSION; GENETIC VECTORS; HEXOSES; IMMUNITY, INNATE; INTERLEUKIN-12; INTERLEUKIN-6; LIPOSOMES; LIVER; LUCIFERASES; MANNOSE; MICE; MICE, INBRED C57BL; NF-KAPPA B; OLIGODEOXYRIBONUCLEOTIDES; PHOSPHATIDYLETHANOLAMINES; SPLEEN; TRANSDUCTION, GENETIC;

EID: 57349098254     PISSN: 01683659     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jconrel.2008.09.081     Document Type: Article

References (51)

1. Koizumi N., Kawabata K., Sakurai F., Watanabe Y., Hayakawa T., and Mizuguchi H. Modified adenoviral vectors ablated for coxsackievirus-adenovirus receptor, alphav integrin, and heparan sulfate binding reduce in vivo tissue transduction and toxicity. Hum. Gene Ther. 17 (2006) 264-279
2. Koizumi N., Yamaguchi T., Kawabata K., Sakurai F., Sasaki T., Watanabe Y., Hayakawa T., and Mizuguchi H. Fiber-modified adenovirus vectors decrease liver toxicity through reduced IL-6 production. J. Immunol. 178 (2007) 1767-1773
3. Lieber A., He C.Y., Meuse L., Schowalter D., Kirillova I., Winther B., and Kay M.A. The role of Kupffer cell activation and viral gene expression in early liver toxicity after infusion of recombinant adenovirus vectors. J. Virol. 71 (1997) 8798-8807
4. Muruve D.A. The innate immune response to adenovirus vectors. Hum. Gene Ther. 15 (2004) 1157-1166
5. Liu Q., Zaiss A.K., Colarusso P., Patel K., Haljan G., Wickham T.J., and Muruve D.A. The role of capsid-endothelial interactions in the innate immune response to adenovirus vectors. Hum. Gene Ther. 14 (2003) 627-643
6. Raper S.E., Chirmule N., Lee F.S., Wivel N.A., Bagg A., Gao G.P., Wilson J.M., and Batshaw M.L. Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol. Genet. Metab. 80 (2003) 148-158
7. Tamanini A., Rolfini R., Nicolis E., Melotti P., and Cabrini G. MAP kinases and NF-kappaB collaborate to induce ICAM-1 gene expression in the early phase of adenovirus infection. Virology 307 (2003) 228-242
8. Melotti P., Nicolis E., Tamanini A., Rolfini R., Pavirani A., and Cabrini G. Activation of NF-kB mediates ICAM-1 induction in respiratory cells exposed to an adenovirus-derived vector. Gene Ther. 8 (2001) 1436-1442
9. Pahl H.L. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18 (1999) 6853-6866
10. Tomita N., Morishita R., Lan H.Y., Yamamoto K., Hashizume M., Notake M., Toyosawa K., Fujitani B., Mu W., Nikolic-Paterson D.J., Atkins R.C., Kaneda Y., Higaki J., and Ogihara T. In vivo administration of a nuclear transcription factor-kappaB decoy suppresses experimental crescentic glomerulonephritis. J. Am. Soc. Nephrol. 11 (2000) 1244-1252
11. Yoshimura S., Morishita R., Hayashi K., Yamamoto K., Nakagami H., Kaneda Y., Sakai N., and Ogihara T. Inhibition of intimal hyperplasia after balloon injury in rat carotid artery model using cis-element 'decoy' of nuclear factor-kappaB binding site as a novel molecular strategy. Gene Ther. 8 (2001) 1635-1642
12. Nakamura H., Aoki M., Tamai K., Oishi M., Ogihara T., Kaneda Y., and Morishita R. Prevention and regression of atopic dermatitis by ointment containing NF-kB decoy oligodeoxynucleotides in NC/Nga atopic mouse model. Gene Ther. 9 (2002) 1221-1229
13. Kupatt C., Wichels R., Deiss M., Molnar A., Lebherz C., Raake P., von Degenfeld G., Hahnel D., and Boekstegers P. Retroinfusion of NFkappaB decoy oligonucleotide extends cardioprotection achieved by CD18 inhibition in a preclinical study of myocardial ischemia and retroinfusion in pigs. Gene Ther. 9 (2002) 518-526
14. Ogushi I., Iimuro Y., Seki E., Son G., Hirano T., Hada T., Tsutsui H., Nakanishi K., Morishita R., Kaneda Y., and Fujimoto J. Nuclear factor kappa B decoy oligodeoxynucleotides prevent endotoxin-induced fatal liver failure in a murine model. Hepatology 38 (2003) 335-344
15. McKenzie E.J., Taylor P.R., Stillion R.J., Lucas A.D., Harris J., Gordon S., and Martinez-Pomares L. Mannose receptor expression and function define a new population of murine dendritic cells. J. Immunol. 178 (2007) 4975-4983
16. Linehan S.A., Martinez-Pomares L., Stahl P.D., and Gordon S. Mannose receptor and its putative ligands in normal murine lymphoid and nonlymphoid organs: in situ expression of mannose receptor by selected macrophages, endothelial cells, perivascular microglia, and mesangial cells, but not dendritic cells. J. Exp. Med. 189 (1999) 1961-1972
17. Linehan S.A. The mannose receptor is expressed by subsets of APC in non-lymphoid organs. BMC Immunol. 6 (2005) 4
18. Kawakami S., Sato A., Nishikawa M., Yamashita F., and Hashida M. Mannose receptor-mediated gene transfer into macrophages using novel mannosylated cationic liposomes. Gene Ther. 7 (2000) 292-299
19. Lu Y., Kawakami S., Yamashita F., and Hashida M. Development of an antigen-presenting cell-targeted DNA vaccine against melanoma by mannosylated liposomes. Biomaterials 28 (2007) 3255-3262
20. Higuchi Y., Kawakami S., Oka M., Yabe Y., Yamashita F., and Hashida M. Intravenous administration of mannosylated cationic liposome/NFkappaB decoy complexes effectively prevent LPS-induced cytokine production in a murine liver failure model. FEBS Lett. 580 (2006) 3706-3714
21. Higuchi Y., Kawakami S., Yamashita F., and Hashida M. The potential role of fucosylated cationic liposome/NFkappaB decoy complexes in the treatment of cytokine-related liver disease. Biomaterials 28 (2007) 532-539
22. Mizuguchi H., Koizumi N., Hosono T., Utoguchi N., Watanabe Y., Kay M.A., and Hayakawa T. A simplified system for constructing recombinant adenoviral vectors containing heterologous peptides in the HI loop of their fiber knob. Gene Ther. 8 (2001) 730-735
23. Maizel Jr. J.V., White D.O., and Scharff M.D. The polypeptides of adenovirus. I. Evidence for multiple protein components in the virion and a comparison of types 2, 7A, and 12. Virology 36 (1968) 115-125
24. Xu Z.L., Mizuguchi H., Ishii-Watabe A., Uchida E., Mayumi T., and Hayakawa T. Optimization of transcriptional regulatory elements for constructing plasmid vectors. Gene 272 (2001) 149-156
25. Peng Y., Falck-Pedersen E., and Elkon K.B. Variation in adenovirus transgene expression between BALB/c and C57BL/6 mice is associated with differences in interleukin-12 and gamma interferon production and NK cell activation. J. Virol. 75 (2001) 4540-4550
26. Sakurai H., Sakurai F., Kawabata K., Sasaki T., Koizumi N., Huang H., Tashiro K., Kurachi S., Nakagawa S., and Mizuguchi H. Comparison of gene expression efficiency and innate immune response induced by Ad vector and lipoplex. J. Control. Release 117 (2007) 430-437
27. Sakurai F., Nishioka T., Saito H., Baba T., Okuda A., Matsumoto O., Taga T., Yamashita F., Takakura Y., and Hashida M. Interaction between DNA-cationic liposome complexes and erythrocytes is an important factor in systemic gene transfer via the intravenous route in mice: the role of the neutral helper lipid. Gene Ther. 8 (2001) 677-686
28. Sakurai F., Nishioka T., Yamashita F., Takakura Y., and Hashida M. Effects of erythrocytes and serum proteins on lung accumulation of lipoplexes containing cholesterol or DOPE as a helper lipid in the single-pass rat lung perfusion system. Eur. J. Pharm. Biopharm. 52 (2001) 165-172
29. Fumoto S., Kawakami S., Ito Y., Shigeta K., Yamashita F., and Hashida M. Enhanced hepatocyte-selective in vivo gene expression by stabilized galactosylated liposome/plasmid DNA complex using sodium chloride for complex formation. Mol. Ther. 10 (2004) 719-729
30. Hattori Y., Kawakami S., Nakamura K., Yamashita F., and Hashida M. Efficient gene transfer into macrophages and dendritic cells by in vivo gene delivery with mannosylated lipoplex via the intraperitoneal route. J. Pharmacol. Exp. Ther. 318 (2006) 828-834
31. Haltiwanger R.S., Lehrman M.A., Eckhardt A.E., and Hill R.L. The distribution and localization of the fucose-binding lectin in rat tissues and the identification of a high affinity form of the mannose/N-acetylglucosamine-binding lectin in rat liver. J. Biol. Chem. 261 (1986) 7433-7439
32. Lehrman M.A., Haltiwanger R.S., and Hill R.L. The binding of fucose-containing glycoproteins by hepatic lectins. The binding specificity of the rat liver fucose lectin. J. Biol. Chem. 261 (1986) 7426-7432
33. Goriely S., Molle C., Nguyen M., Albarani V., Haddou N.O., Lin R., De Wit D., Flamand V., Willems F., and Goldman M. Interferon regulatory factor 3 is involved in Toll-like receptor 4 (TLR4)- and TLR3-induced IL-12p35 gene activation. Blood 107 (2006) 1078-1084
34. Kollet J.I., and Petro T.M. IRF-1 and NF-kappaB p50/cRel bind to distinct regions of the proximal murine IL-12 p35 promoter during costimulation with IFN-gamma and LPS. Mol. Immunol. 43 (2006) 623-633
35. Liu J., Guan X., Tamura T., Ozato K., and Ma X. Synergistic activation of interleukin-12 p35 gene transcription by interferon regulatory factor-1 and interferon consensus sequence-binding protein. J. Biol. Chem. 279 (2004) 55609-55617
36. Kiang A., Hartman Z.C., Everett R.S., Serra D., Jiang H., Frank M.M., and Amalfitano A. Multiple innate inflammatory responses induced after systemic adenovirus vector delivery depend on a functional complement system. Mol. Ther. 14 (2006) 588-598
37. McCaffrey A.P., Fawcett P., Nakai H., McCaffrey R.L., Ehrhardt A., Pham T.T., Pandey K., Xu H., Feuss S., Storm T.A., and Kay M.A. The host response to adenovirus, helper-dependent adenovirus, and adeno-associated virus in mouse liver. Mol. Ther. 16 (2008) 931-941
38. Zhu J., Huang X., and Yang Y. A critical role for type I IFN-dependent NK cell activation in innate immune elimination of adenoviral vectors in vivo. Mol. Ther. 16 (2008) 1300-1307
39. Zhu J., Huang X., and Yang Y. Innate immune response to adenoviral vectors is mediated by both Toll-like receptor-dependent and -independent pathways. J. Virol. 81 (2007) 3170-3180
40. Stadlbauer T.H., Wagner A.H., Holschermann H., Fiedel S., Fingerhuth H., Tillmanns H., Bohle R.M., and Hecker M. AP-1 and STAT-1 decoy oligodeoxynucleotides attenuate transplant vasculopathy in rat cardiac allografts. Cardiovasc. Res. 79 (2008) 698-705
41. Zhang X., Zhang J., Wei H., and Tian Z. STAT3-decoy oligodeoxynucleotide inhibits the growth of human lung cancer via down-regulating its target genes. Oncol. Rep. 17 (2007) 1377-1382
42. Sakurai F., Mizuguchi H., Yamaguchi T., and Hayakawa T. Characterization of in vitro and in vivo gene transfer properties of adenovirus serotype 35 vector. Mol. Ther. 8 (2003) 813-821
43. Alemany R., Suzuki K., and Curiel D.T. Blood clearance rates of adenovirus type 5 in mice. J. Gen. Virol. 81 (2000) 2605-2609
44. Mok H., Palmer D.J., Ng P., and Barry M.A. Evaluation of polyethylene glycol modification of first-generation and helper-dependent adenoviral vectors to reduce innate immune responses. Mol. Ther. 11 (2005) 66-79
45. Yotnda P., Chen D.H., Chiu W., Piedra P.A., Davis A., Templeton N.S., and Brenner M.K. Bilamellar cationic liposomes protect adenovectors from preexisting humoral immune responses. Mol. Ther. 5 (2002) 233-241
46. Ma Z., Mi Z., Wilson A., Alber S., Robbins P.D., Watkins S., Pitt B., and Li S. Redirecting adenovirus to pulmonary endothelium by cationic liposomes. Gene Ther. 9 (2002) 176-182
47. Hofherr S.E., Shashkova E.V., Weaver E.A., Khare R., and Barry M.A. Modification of adenoviral vectors with polyethylene glycol modulates in vivo tissue tropism and gene expression. Mol. Ther. 16 (2008) 1276-1282
48. Gao J.Q., Eto Y., Yoshioka Y., Sekiguchi F., Kurachi S., Morishige T., Yao X., Watanabe H., Asavatanabodee R., Sakurai F., Mizuguchi H., Okada Y., Mukai Y., Tsutsumi Y., Mayumi T., Okada N., and Nakagawa S. Effective tumor targeted gene transfer using PEGylated adenovirus vector via systemic administration. J. Control. Release 122 (2007) 102-110
49. Jun-Ichi S., Hiroshi I., Ryo G., Ryuichi M., Kensuke E., and Mitsuaki I. Initial clinical cases of the use of a NF-kappaB decoy at the site of coronary stenting for the prevention of restenosis. Circ. J. 68 (2004) 270-271
50. Egashira K., Suzuki J., Ito H., Aoki M., Isobe M., and Morishita R. Long-term follow up of initial clinical cases with NF-kappaB decoy oligodeoxynucleotide transfection at the site of coronary stenting. J. Gene Med. 10 (2008) 805-809
51. Snoeys J., Mertens G., Lievens J., van Berkel T., Collen D., Biessen E.A., and De Geest B. Lipid emulsions potently increase transgene expression in hepatocytes after adenoviral transfer. Mol. Ther. 13 (2006) 98-107