Efficient invivo transfection and safety profile of a CpG-free and codon optimized luciferase plasmid using a cationic lipophosphoramidate in a multiple intravenous administration procedure

Biomaterials

Volumn 59, Issue , 2015, Pages 1-11

  Lindberg, Mattias F ^a   Le Gall, Tony ^a   Carmoy, Nathalie ^a,b   Berchel, Mathieu ^b   Hyde, Stephen C ^d   Gill, Deborah R ^d   Jaffrès, Paul Alain ^b   Lehn, Pierre ^a,c   Montier, Tristan ^a,b,c  

^a FACULTÉ DE MÉDECINE ET DES SCIENCES DE LA SANTÉ   (France)

^b UNIVERSITÉ DE BRETAGNE OCCIDENTALE   (France)

^c CHU MORVAN   (France)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cationic lipids; CpG; Inflammation; Invivo bioluminescence; Non viral gene transfer; Repeated administration; Transfection

Indexed keywords

ARTIFICIAL LIFE; BIOLUMINESCENCE; DISEASES; DNA; GENE THERAPY; GENE TRANSFER; LIPOSOMES; MAMMALS; PATHOLOGY; PHOSPHORESCENCE; TARGETED DRUG DELIVERY;

CATIONIC LIPIDS; IN-VIVO; INFLAMMATION; NONVIRAL; TRANSFECTION;

CONTROLLED DRUG DELIVERY;

CATIONIC LIPOPHOSPHORAMIDATE BSV4; ELONGATION FACTOR 1ALPHA; LIPOPLEX; LIPOSOME; LUCIFERASE; PHOSPHORAMIDIC ACID DERIVATIVE; UNCLASSIFIED DRUG; AMIDE; CATION; CODON; DNA; PHOSPHORAMIDIC ACID; PHOSPHORIC ACID;

ANIMAL EXPERIMENT; ARTICLE; BIOLUMINESCENCE; CODON; CONTROLLED STUDY; CYTOMEGALOVIRUS; FEMALE; GENE EXPRESSION PROFILING; IMMUNE RESPONSE; IN VIVO GENE TRANSFER; KINETICS; LIVER TOXICITY; LUNG; MOUSE; NONHUMAN; PHYSICAL CHEMISTRY; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; TRANSGENE; ZETA POTENTIAL; ANIMAL; CELL LINE; CHEMISTRY; CPG ISLAND; GENETIC TRANSFECTION; GENETICS; INTRAVENOUS DRUG ADMINISTRATION;

CYTOMEGALOVIRUS; MUS;

ADMINISTRATION, INTRAVENOUS; AMIDES; ANIMALS; CATIONS; CELL LINE; CODON; CPG ISLANDS; DNA; FEMALE; LUCIFERASES; MICE; PHOSPHORIC ACIDS; PLASMIDS; TRANSFECTION;

EID: 84930162893     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.04.024     Document Type: Article

References (52)

1. Alexis F., Pridgen E., Molnar L.K., Farokhzad O.C. Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol Pharm 2008, 5:505-515. 10.1021/mp800051m.
2. Montier T., Benvegnu T., Jaffrès P.-A., Yaouanc J.-J., Lehn P. Progress in cationic lipid-mediated gene transfection: a series of bio-inspired lipids as an example. Curr Gene Ther 2008, 8:296-312.
3. Le Gall T., Loizeau D., Picquet E., Carmoy N., Yaouanc J.-J., Burel-Deschamps L., et al. Anovel cationic lipophosphoramide with diunsaturated lipid chains: synthesis, physicochemical properties, and transfection activities. JMed Chem 2010, 53:1496-1508. 10.1021/jm900897a.
4. Lindberg M.F., Carmoy N., Le Gall T., Fraix A., Berchel M., Lorilleux C., et al. The gene transfection properties of a lipophosphoramidate derivative with two phytanyl chains. Biomaterials 2012, 33:6240-6253. 10.1016/j.biomaterials.2012.05.014.
5. Le Gall T., Berchel M., Le Hir S., Fraix A., Salaün J.Y., Férec C., et al. Arsonium-containing lipophosphoramides, poly-functional nano-carriers for simultaneous antibacterial action and eukaryotic cell transfection. Adv Healthc Mater 2013, 2:1513-1524. 10.1002/adhm.201200478.
6. Rawlins E.L., Hogan B.L.M. Ciliated epithelial cell lifespan in the mouse trachea and lung. Am J Physiol Lung Cell Mol Physiol 2008, 295:L231-L234. 10.1152/ajplung.90209.2008.
7. Herzog R.W., Cao O., Srivastava A. Two decades of clinical gene therapy-success is finally mounting. Discov Med 2010, 9:105-111.
8. Gill D.R., Pringle I.A., Hyde S.C. Progress and prospects: the design and production of plasmid vectors. Gene Ther 2009, 16:165-171. 10.1038/gt.2008.183.
9. Gill D.R., Smyth S.E., Goddard C.A., Pringle I.A., Higgins C.F., Colledge W.H., et al. Increased persistence of lung gene expression using plasmids containing the ubiquitin C or elongation factor 1alpha promoter. Gene Ther 2001, 8:1539-1546. 10.1038/sj.gt.3301561.
10. Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., et al. Atoll-like receptor recognizes bacterial DNA. Nature 2000, 408:740-745. 10.1038/35047123.
11. Hyde S.C., Pringle I.A., Abdullah S., Lawton A.E., Davies L.A., Varathalingam A., et al. CpG-free plasmids confer reduced inflammation and sustained pulmonary gene expression. Nat Biotechnol 2008, 26:549-551. 10.1038/nbt1399.
12. Davies L.A., Hyde S.C., Nunez-Alonso G., Bazzani R.P., Harding-Smith R., Pringle I.A., et al. The use of CpG-free plasmids to mediate persistent gene expression following repeated aerosol delivery of pDNA/PEI complexes. Biomaterials 2012, 33:5618-5627. 10.1016/j.biomaterials.2012.04.019.
13. Alton E.W.F.W., Boyd A.C., Cheng S.H., Cunningham S., Davies J.C., Gill D.R., et al. Arandomised, double-blind, placebo-controlled phase IIB clinical trial of repeated application of gene therapy in patients with cystic fibrosis. Thorax 2013, 68:1075-1077. 10.1136/thoraxjnl-2013-203309.
14. Paillard F. Promoter attenuation in gene therapy: causes and remedies. Hum Gene Ther 1997, 8:2009-2010.
15. Qin L., Ding Y., Pahud D.R., Chang E., Imperiale M.J., Bromberg J.S. Promoter attenuation in gene therapy: interferon-gamma and tumor necrosis factor-alpha inhibit transgene expression. Hum Gene Ther 1997, 8:2019-2029. 10.1089/hum.1997.8.17-2019.
16. Kuriyama S., Sakamoto T., Kikukawa M., Nakatani T., Toyokawa Y., Tsujinoue H., et al. Expression of a retrovirally transduced gene under control of an internal housekeeping gene promoter does not persist due to methylation and is restored partially by 5-azacytidine treatment. Gene Ther 1998, 5:1299-1305. 10.1038/sj.gt.3300738.
17. Chen Z.Y., He C.Y., Meuse L., Kay M.A. Silencing of episomal transgene expression by plasmid bacterial DNA elements invivo. Gene Ther 2004, 11:856-864. 10.1038/sj.gt.3302231.
18. Chen Z.-Y., Riu E., He C.-Y., Xu H., Kay M.A. Silencing of episomal transgene expression in liver by plasmid bacterial backbone DNA is independent of CpG methylation. Mol Ther 2008, 16:548-556. 10.1038/sj.mt.6300399.
19. Haase R., Argyros O., Wong S.-P., Harbottle R.P., Lipps H.J., Ogris M., et al. pEPito: a significantly improved non-viral episomal expression vector for mammalian cells. BMC Biotechnol 2010, 10:20. 10.1186/1472-6750-10-20.
20. Weber M., Hellmann I., Stadler M.B., Ramos L., Pääbo S., Rebhan M., et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 2007, 39:457-466. 10.1038/ng1990.
21. Grassi G., Maccaroni P., Meyer R., Kaiser H., D'Ambrosio E., Pascale E., et al. Inhibitors of DNA methylation and histone deacetylation activate cytomegalovirus promoter-controlled reporter gene expression in human glioblastoma cell line U87. Carcinogenesis 2003, 24:1625-1635. 10.1093/carcin/bgg118.
22. Kong Q., Wu M., Huan Y., Zhang L., Liu H., Bou G., et al. Transgene expression is associated with copy number and cytomegalovirus promoter methylation in transgenic pigs. PLoS One 2009, 4:e6679. 10.1371/journal.pone.0006679.
23. Brooks A.R., Harkins R.N., Wang P., Qian H.S., Liu P., Rubanyi G.M. Transcriptional silencing is associated with extensive methylation of the CMV promoter following adenoviral gene delivery to muscle. JGene Med 2004, 6:395-404. 10.1002/jgm.516.
24. Navarro G., Maiwald G., Haase R., Rogach A.L., Wagner E., de Ilarduya C.T., et al. Low generation PAMAM dendrimer and CpG free plasmids allow targeted and extended transgene expression in tumors after systemic delivery. JControl Release 2010, 146:99-105. 10.1016/j.jconrel.2010.04.030.
25. Magnusson T., Haase R., Schleef M., Wagner E., Ogris M. Sustained, high transgene expression in liver with plasmid vectors using optimized promoter-enhancer combinations. JGene Med 2011, 13:382-391. 10.1002/jgm.1585.
26. Le Gall T., Barbeau J., Barrier S., Berchel M., Lemiègre L., Jeftić J., et al. Effects of a novel archaeal tetraether-based colipid on the invivo gene transfer activity of two cationic amphiphiles. Mol Pharm 2014, 11:2973-2988. 10.1021/mp4006276.
27. Liu Y., Liggitt D., Zhong W., Tu G., Gaensler K., Debs R. Cationic liposome-mediated intravenous gene delivery. JBiol Chem 1995, 270:24864-24870.
28. Liu Y., Mounkes L.C., Liggitt H.D., Brown C.S., Solodin I., Heath T.D., et al. Factors influencing the efficiency of cationic liposome-mediated intravenous gene delivery. Nat Biotech 1997, 15:167-173. 10.1038/nbt0297-167.
29. Li S., Tseng W.C., Stolz D.B., Wu S.P., Watkins S.C., Huang L. Dynamic changes in the characteristics of cationic lipidic vectors after exposure to mouse serum: implications for intravenous lipofection. Gene Ther 1999, 6:585-594. 10.1038/sj.gt.3300865.
30. McLean J.W., Fox E.A., Baluk P., Bolton P.B., Haskell A., Pearlman R., et al. Organ-specific endothelial cell uptake of cationic liposome-DNA complexes in mice. Am J Physiol 1997, 273:H387-H404.
31. Osaka G., Carey K., Cuthbertson A., Godowski P., Patapoff T., Ryan A., et al. Pharmacokinetics, tissue distribution, and expression efficiency of plasmid [33P]DNA following intravenous administration of DNA/cationic lipid complexes in mice: use of a novel radionuclide approach. JPharm Sci 1996, 85:612-618. 10.1021/js9504494.
32. Delépine P., Guillaume C., Montier T., Clément J.C., Yaouanc J.J., Des Abbayes H., et al. Biodistribution study of phosphonolipids: a class of non-viral vectors efficient in mice lung-directed gene transfer. JGene Med 2003, 5:600-608. 10.1002/jgm.385.
33. Mian A., Guenther M., Finegold M., Ng P., Rodgers J., Lee B. Toxicity and adaptive immune response to intracellular transgenes delivered by helper-dependent vs. first generation adenoviral vectors. Mol Genet Metab 2005, 84:278-288. 10.1016/j.ymgme.2004.11.005.
34. Jeon Y.H., Choi Y., Kang J.H., Kim C.W., Jeong J.M., Lee D.S., et al. Immune response to firefly luciferase as a naked DNA. Cancer Biol Ther 2007, 6:781-786.
35. Alton E.W.F.W., Boyd A.C., Cheng S.H., Davies J.C., Davies L.A., Dayan A., et al. Toxicology study assessing efficacy and safety of repeated administration of lipid/DNA complexes to mouse lung. Gene Ther 2014, 21:89-95. 10.1038/gt.2013.61.
36. Rudolph C., Schillinger U., Ortiz A., Plank C., Golas M.M., Sander B., et al. Aerosolized nanogram quantities of plasmid DNA mediate highly efficient gene delivery to mouse airway epithelium. Mol Ther 2005, 12:493-501. 10.1016/j.ymthe.2005.03.002.
37. Davies L.A., Seguela C., Varathalingam A., Cheng S.H., Hyde S.C., Gill D.R. Identification of transfected cell types following non-viral gene transfer to the murine lung. JGene Med 2007, 9:184-196. 10.1002/jgm.1007.
38. Davies L.A., McLachlan G., Sumner-Jones S.G., Ferguson D., Baker A., Tennant P., et al. Enhanced lung gene expression after aerosol delivery of concentrated pDNA/PEI complexes. Mol Ther 2008, 16:1283-1290. 10.1038/mt.2008.96.
39. Li S., Huang L. Invivo gene transfer via intravenous administration of cationic lipid-protamine-DNA (LPD) complexes. Gene Ther 1997, 4:891-900. 10.1038/sj.gt.3300482.
40. Dif F., Djediat C., Alegria O., Demeneix B., Levi G. Transfection of multiple pulmonary cell types following intravenous injection of PEI-DNA in normal and CFTR mutant mice. JGene Med 2006, 8:82-89. 10.1002/jgm.831.
41. Bazzani R.P., Cai Y., Hebel H.L., Hyde S.C., Gill D.R. The significance of plasmid DNA preparations contaminated with bacterial genomic DNA on inflammatory responses following delivery of lipoplexes to the murine lung. Biomaterials 2011, 32:9854-9865. 10.1016/j.biomaterials.2011.08.092.
42. Tan Y., Li S., Pitt B.R., Huang L. The inhibitory role of CpG immunostimulatory motifs in cationic lipid vector-mediated transgene expression invivo. Hum Gene Ther 1999, 10:2153-2161. 10.1089/10430349950017149.
43. Loisel S., Le Gall C., Doucet L., Ferec C., Floch V. Contribution of plasmid DNA to hepatotoxicity after systemic administration of lipoplexes. Hum Gene Ther 2001, 12:685-696. 10.1089/104303401300057405.
44. Ito Y., Kawakami S., Charoensit P., Higuchi Y., Hashida M. Evaluation of proinflammatory cytokine production and liver injury induced by plasmid DNA/cationic liposome complexes with various mixing ratios in mice. Eur J Pharm Biopharm 2009, 71:303-309. 10.1016/j.ejpb.2008.09.005.
45. Kako K., Nishikawa M., Yoshida H., Takakura Y. Effects of inflammatory response on invivo transgene expression by plasmid DNA in mice. JPharm Sci 2008, 97:3074-3083. 10.1002/jps.21254.
46. Kawakami S., Ito Y., Fumoto S., Yamashita F., Hashida M. Enhanced gene expression in lung by a stabilized lipoplex using sodium chloride for complex formation. JGene Med 2005, 7:1526-1533. 10.1002/jgm.813.
47. Orson F.M., Song L., Gautam A., Densmore C.L., Bhogal B.S., Kinsey B.M. Gene delivery to the lung using protein/polyethylenimine/plasmid complexes. Gene Ther 2002, 9:463-471. 10.1038/sj.gt.3301666.
48. Song Y.K., Liu F., Chu S., Liu D. Characterization of cationic liposome-mediated gene transfer invivo by intravenous administration. Hum Gene Ther 1997, 8:1585-1594. 10.1089/hum.1997.8.13-1585.
49. Alton E.W.F.W., Baker A., Baker E., Boyd A.C., Cheng S.H., Coles R.L., et al. The safety profile of a cationic lipid-mediated cystic fibrosis gene transfer agent following repeated monthly aerosol administration to sheep. Biomaterials 2013, 34:10267-10277. 10.1016/j.biomaterials.2013.09.023.
50. Knudsen K.B., Northeved H., Kumar P.E.K., Permin A., Gjetting T., Andresen T.L., et al. Invivo toxicity of cationic micelles and liposomes. Nanomedicine 2015, 11:467-477. 10.1016/j.nano.2014.08.004.
51. Wiseman J.W., Goddard C.A., McLelland D., Colledge W.H. Acomparison of linear and branched polyethylenimine (PEI) with DCChol/DOPE liposomes for gene delivery to epithelial cells invitro and invivo. Gene Ther 2003, 10:1654-1662. 10.1038/sj.gt.3302050.
52. Dames P., Ortiz A., Schillinger U., Lesina E., Plank C., Rosenecker J., et al. Aerosol gene delivery to the murine lung is mouse strain dependent. JMol Med 2007, 85:371-378. 10.1007/s00109-006-0130-9.