Liposomes as non-viral carriers for genetic drugs
Justyna M. Meissner 1 , Monika Toporkiewicz 1 , Lucyna Matusewicz 1 , Beata Machnicka 2Abstract
Methods in cancer therapy particularly in recent years, are rapidly changing, due to the need of design of new, more effective therapeutic strategies. Very promising approach to treatment of the neoplastic diseases is antisense gene therapy. Due to the low toxicity of treatment and eliminating not only the symptoms but also the molecular causes of the disease it may represent a breakthrough in cancer therapies. Delivery of a therapeutic DNA or RNA oligonucleotides to the target cells in vivo requires suitable carrier system. Non-viral drug carriers are increasingly used in new systems of targeted gene therapy. This review presents new generation of non-viral carriers, and is focused on immunoliposomes finding potential application in targeted gene therapy.
References
- 1. Abu Lila A.S., Ishida T., Kiwada H.: Targeting anticancer drugsto tumor vasculature using cationic liposomes. Pharm. Res., 2010;27: 1171-1183
Google Scholar - 2. Agrawal S., Zhao Q.: Mixed backbone oligonucleotides: improvementin oligonucleotide-induced toxicity in vivo. Antisense NucleicAcid Drug Dev., 1998; 8: 135-139
Google Scholar - 3. Al-Dosari M.S., Gao X.: Nonviral gene delivery: principle, limitations,and recent progress. AAPS J., 2009; 11: 671-681
Google Scholar - 4. Alexis F., Pridgen E.M., Langer R., Farokhzad O.C.: Nanoparticletechnologies for cancer therapy. Handb. Exp. Pharmacol., 2010; 197:55-86
Google Scholar - 5. Allen T.M.: Ligand-targeted therapeutics in anticancer therapy.Nat. Rev. Cancer, 2002; 2: 750-763
Google Scholar - 6. Allen T.M., Cullis P.R.: Liposomal drug delivery systems: fromconcept to clinical applications. Adv. Drug Deliv. Rev., 2013; 65: 36-48
Google Scholar - 7. Allen T.M., Mehra T., Hansen C., Chin Y.C.: Stealth liposomes: an improvedsustained release system for 1-β-D-arabinofuranosylcytosine.Cancer Res., 1992; 52: 2431-2439.
Google Scholar - 8. Arias J.L.: Drug targeting strategies in cancer treatment: an overview.Mini Rev. Med. Chem., 2011; 11: 1-17
Google Scholar - 9. Barbet J., Machy P., Leserman L.D.: Monoclonal antibody covalentlycoupled to liposomes: specific targeting to cells. J. Supramol.Struct. Cell. Biochem., 1981; 16: 243-258
Google Scholar - 10. Brignole C., Marimpietri D., Pagnan G., Di Paolo D., Zancolli M.,Pistoia V., Ponzoni M., Pastorino F.: Neuroblastoma targeting by cmyb-selective antisense oligonucleotides entrapped in anti-GD2 immunoliposome:immune cell-mediated anti-tumor activities. CancerLett., 2005; 228: 181-186
Google Scholar - 11. Brignole C., Pagnan G., Marimpietri D., Cosimo E., Allen T.M.,Ponzoni M., Pastorino F.: Targeted delivery system for antisenseoligonucleotides: a novel experimental strategy for neuroblastomatreatment. Cancer Lett., 2003; 197: 231-235
Google Scholar - 12. Byrne J.D., Betancourt T., Brannon-Peppas L.: Active targetingschemes for nanoparticle systems in cancer therapeutics. Adv. DrugDeliv. Rev., 2008; 60: 1615-1626
Google Scholar - 13. Chan J.M., Rhee J.W., Drum C.L., Bronson R.T., Golomb G., LangerR., Farokhzad O.C.: In vivo prevention of arterial restenosis with paclitaxel-encapsulated targeted lipid-polymeric nanoparticles. Proc.Natl. Acad. Sci. USA, 2011; 108: 19347-19352
Google Scholar - 14. Chapman C.J., Erdahl W.L., Taylor R.W., Pfeiffer D.R.: Factorsaffecting solute entrapment in phospholipid vesicles prepared bythe freeze-thaw extrusion method: a possible general method forimproving the efficiency of entrapment. Chem. Phys. Lipids, 1990;55: 73-83
Google Scholar - 15. Chen Y., Zhu X., Zhang X., Liu B., Huang L.: Nanoparticles modifiedwith tumor-targeting scFv deliver siRNA and miRNA for cancertherapy. Mol. Ther., 2010; 18: 1650-1656
Google Scholar - 16. Cheng W.W., Allen T.M.: Targeted delivery of anti-CD19 liposomal doxorubicin in B-cell lymphoma: a comparison of whole monoclonalantibody, Fab’ fragments and single chain Fv. J. Control. Release,2008; 126: 50-58
Google Scholar - 17. Christian S., Pilch J., Akerman M.E., Porkka K., Laakkonen P.,Ruoslahti E.: Nucleolin expressed at the cell surface is a markerof endothelial cells in angiogenic blood vessels. J. Cell Biol., 2003;163: 871-878
Google Scholar - 18. Collet G., Grillon C., Nadim M., Kieda C.: Trojan horse at cellularlevel for tumor gene therapies. Gene, 2013; 525: 208-216
Google Scholar - 19. Danhier F., Feron O., Preat V.: To exploit the tumor microenvironment:passive and active tumor targeting of nanocarriers foranti-cancer drug delivery. J. Control. Release, 2010; 148: 135-146
Google Scholar - 20. Deamer D.W., Barchfeld G.L.: Encapsulation of macromoleculesby lipid vesicles under simulated prebiotic conditions. J. Mol. Evol.,1982; 18: 203-206
Google Scholar - 21. Deshpande P.P., Biswas S., Torchilin V.P.: Current trends in theuse of liposomes for tumor targeting. Nanomedicine, 2013; 8: 1509-1528
Google Scholar - 22. Dobbs W., Heinrich B., Bourgogne C., Donnio B., Terazzi E., BonnetM.E., Stock F., Erbacher P., Bolcato-Bellemin A.L., Douce L.: Mesomorphicimidazolium salts: new vectors for efficient siRNA transfection.J. Am. Chem. Soc., 2009; 131: 13338-13346
Google Scholar - 23. Dokka S., Toledo D., Shi X., Castranova V., Rojanasakul Y.: Oxygenradical-mediated pulmonary toxicity induced by some cationicliposomes. Pharm. Res., 2000; 17: 521-525
Google Scholar - 24. Eastman S.J., Siegel C., Tousignant J., Smith A.E., Cheng S.H.,Scheule R.K.: Biophysical characterization of cationic lipid: DNAcomplexes. Biochim. Biophys. Acta, 1997; 1325: 41-62
Google Scholar - 25. Elbayoumi T.A., Torchilin V.P.: Current trends in liposome research.Methods Mol. Biol., 2010; 605: 1-27
Google Scholar - 26. Escriou V., Ciolina C., Lacroix F., Byk G., Scherman D., Wils P.:Cationic lipid-mediated gene transfer: effect of serum on cellularuptake and intracellular fate of lipopolyamine/DNA complexes.Biochim. Biophys. Acta, 1998; 1368: 276-288
Google Scholar - 27. Felgner P.L., Gadek T.R., Holm M., Roman R., Chan H.W., WenzM., Northrop J.P., Ringold G.M., Danielsen M.: Lipofection: a highlyefficient, lipid-mediated DNA-transfection procedure. Proc. Natl.Acad. Sci. USA, 1987; 84: 7413-7417
Google Scholar - 28. Gabizon A., Horowitz A.T., Goren D., Tzemach D., Shmeeda H.,Zalipsky S.: In vivo fate of folate-targeted polyethylene-glycol liposomesin tumor-bearing mice. Clin. Cancer Res., 2003; 9: 6551-6559
Google Scholar - 29. Gao J., Sun J., Li H., Liu W., Zhang Y., Li B., Qian W., Wang H., ChenJ., Guo Y.: Lyophilized HER2-specific PEGylated immunoliposomesfor active siRNA gene silencing. Biomaterials, 2010; 31: 2655-2664
Google Scholar - 30. Gao K., Huang L.: Non-viral methods for siRNA delivery. Mol.Pharm., 2009; 6: 651-658
Google Scholar - 31. Gao Y., McLuckey S.A.: Electron transfer followed by collision-induceddissociation (NET-CID) for generating sequence informationfrom backbone-modified oligonucleotide anions. Rapid Commun.Mass Spectrom., 2013; 27: 249-257
Google Scholar - 32. Goldenbogen B., Brodersen N., Gramatica A., Loew M., LiebscherJ., Herrmann A., Egger H., Budde B., Arbuzova A.: Reduction-sensitiveliposomes from a multifunctional lipid conjugate and naturalphospholipids: reduction and release kinetics and cellular uptake.Langmuir, 2011; 27: 10820-10829
Google Scholar - 33. Gomes-da-Silva L.C., Ramalho J.S., Pedroso de Lima M.C., SimoesS., Moreira J.N.: Impact of anti-PLK1 siRNA-containing F3-targetedliposomes on the viability of both cancer and endothelial cells. Eur.J. Pharm. Biopharm., 2013; 85: 356-364
Google Scholar - 34. Goyal P., Goyal K., Vijaya Kumar S.G., Singh A., Katare O.P., MishraD.N.: Liposomal drug delivery systems–clinical applications.Acta Pharm., 2005; 55: 1-25
Google Scholar - 35. Haley B., Frenkel E.: Nanoparticles for drug delivery in cancertreatment. Urol. Oncol., 2008; 26: 57-64
Google Scholar - 36. Harding F.A., Stickler M.M., Razo J., DuBridge R.B.: The immunogenicityof humanized and fully human antibodies: residual immunogenicityresides in the CDR regions. MAbs, 2010; 2: 256-265
Google Scholar - 37. Hayes M.E., Drummond D.C., Kirpotin D.B., Zheng W.W., NobleC.O., Park J.W., Marks J.D., Benz C.C., Hong K.: Genospheres: self-assemblingnucleic acid-lipid nanoparticles suitable for targeted genedelivery. Gene Ther., 2006; 13: 646-651
Google Scholar - 38. Heath T.D., Macher B.A., Papahadjopoulos D.: Covalent attachmentof immunoglobulins to liposomes via glycosphingolipids. Biochim.Biophys. Acta, 1981; 640: 66-81
Google Scholar - 39. Hu C.M., Kaushal S., Tran Cao H.S., Aryal S., Sartor M., EsenerS., Bouvet M., Zhang L.: Half-antibody functionalized lipid-polymerhybrid nanoparticles for targeted drug delivery to carcinoembryonicantigen (CEA) presenting pancreatic cancer cells. Mol. Pharm.,2010; 7: 914-920
Google Scholar - 40. Huang G., Zhou Z., Srinivasan R., Penn M.S., Kottke-MarchantK., Marchant R.E., Gupta A.S.: Affinity manipulation of surface-conjugatedRGD peptide to modulate binding of liposomes to activatedplatelets. Biomaterials, 2008; 29: 1676-1685
Google Scholar - 41. Hwang W.Y., Foote J.: Immunogenicity of engineered antibodies.Methods, 2005; 36: 3-10
Google Scholar - 42. Ibsen S., Benchimol M., Simberg D., Esener S.: Ultrasound mediatedlocalized drug delivery. Adv. Exp. Med. Biol., 2012; 733: 145-153
Google Scholar - 43. Immordino M.L., Dosio F., Cattel L.: Stealth liposomes: review ofthe basic science, rationale, and clinical applications, existing andpotential. Int. J. Nanomedicine, 2006; 1: 297-315
Google Scholar - 44. Ishida T., Atobe K., Wang X., Kiwada H.: Accelerated blood clearanceof PEGylated liposomes upon repeated injections: effect ofdoxorubicin-encapsulation and high-dose first injection. J. Control.Release, 2006; 115: 251-258
Google Scholar - 45. Ito K., Chen J., Asano T., Vaughan E.D.Jr., Poppas D.P., HayakawaM., Felsen D.: Liposome-mediated gene therapy in the kidney. Hum.Cell, 2004; 17: 17-28
Google Scholar - 46. Jin L., Zeng X., Liu M., Deng Y., He N.: Current progress in genedelivery technology based on chemical methods and nano-carriers.Theranostics, 2014; 4: 240-255
Google Scholar - 47. Kale A.A., Torchilin V.P.: Environment-responsive multifunctionalliposomes. Methods Mol. Biol., 2010; 605: 213-242
Google Scholar - 48. Kim S.S., Peer D., Kumar P., Subramanya S., Wu H., Asthana D.,Habiro K., Yang Y.G., Manjunath N., Shimaoka M., Shankar P.: RNAi–mediated CCR5 silencing by LFA-1-targeted nanoparticles preventsHIV infection in BLT mice. Mol. Ther., 2010; 18: 370-376
Google Scholar - 49. Klein E., Ciobanu M., Klein J., Machi V., Leborgne C., VandammeT., Frisch B., Pons F., Kichler A., Zuber G., Lebeau L.: “HFP” fluorinatedcationic lipids for enhanced lipoplex stability and gene delivery.Bioconjug. Chem., 2010; 21: 360-371
Google Scholar - 50. Koren E., Apte A., Jani A., Torchilin V.P.: Multifunctional PEGylated2C5-immunoliposomes containing pH-sensitive bonds and TATpeptide for enhanced tumor cell internalization and cytotoxicity. J.Control. Release, 2012; 160: 264-273
Google Scholar - 51. Kularatne S.A., Low P.S.: Targeting of nanoparticles: folate receptor.Methods Mol. Biol., 2010; 624: 249-265
Google Scholar - 52. Kurreck J.: Antisense technologies. Improvement through novelchemical modifications. Eur. J. Biochem., 2003; 270: 1628-1644
Google Scholar - 53. Laakkonen P., Vuorinen K.: Homing peptides as targeted deliveryvehicles. Integr. Biol., 2010; 2: 326-337
Google Scholar - 54. Lammers T., Kiessling F., Hennink W.E., Storm G.: Drug targetingto tumors: principles, pitfalls and (pre-) clinical progress. J. Control.Release, 2012; 161: 175-187
Google Scholar - 55. Lee J.M., Yoon T.J., Cho Y.S.: Recent developments in nanoparticle-based siRNA delivery for cancer therapy. Biomed Res. Int., 2013;2013: 782041
Google Scholar - 56. Liberska A., Unciti-Broceta A., Bradley M.: Very long-chain fattytails for enhanced transfection. Org. Biomol. Chem., 2009; 7: 61-68
Google Scholar - 57. Liu D., Hu J., Qiao W., Li Z., Zhang S., Cheng L.: Synthesis of carbamate-linked lipids for gene delivery. Bioorg. Med. Chem. Lett.,2005; 15: 3147-3150
Google Scholar - 58. Lv H., Zhang S., Wang B., Cui S., Yan J.: Toxicity of cationic lipidsand cationic polymers in gene delivery. J. Control. Release,2006; 114: 100-109
Google Scholar - 59. Maeda H.: Macromolecular therapeutics in cancer treatment:the EPR effect and beyond. J. Control. Release, 2012; 164: 138-144
Google Scholar - 60. Maeda H., Nakamura H., Fang J.: The EPR effect for macromoleculardrug delivery to solid tumors: improvement of tumor uptake,lowering of systemic toxicity, and distinct tumor imaging in vivo.Adv. Drug Deliv. Rev., 2013; 65: 71-79
Google Scholar - 61. Manjila S.B., Baby J.N., Bijin E.N., Constantine I., Pramod K.,Valsalakumari J.: Novel gene delivery systems. Int. J. Pharm. Investig.,2013; 3: 1-7
Google Scholar - 62. Markman J.L., Rekechenetskiy A., Holler E., Ljubimova J.Y.: Nanomedicinetherapeutic approaches to overcome cancer drug resistance.Adv. Drug Deliv. Rev., 2013; 65: 1866-1879
Google Scholar - 63. Martin B., Sainlos M., Aissaoui A., Oudrhiri N., Hauchecorne M.,Vigneron J.P., Lehn J.M., Lehn P.: The design of cationic lipids forgene delivery. Curr. Pharm. Des., 2005; 11: 375-394
Google Scholar - 64. Martin F.J., Hubbell W.L., Papahadjopoulos D.: Immunospecifictargeting of liposomes to cells: a novel and efficient method for covalentattachment of Fab’ fragments via disulfide bonds. Biochemistry,1981; 20: 4229-4238
Google Scholar - 65. Mevel M., Kamaly N., Carmona S., Oliver M.H., Jorgensen M.R.,Crowther C., Salazar F.H., Marion P.L., Fujino M., Natori Y., ThanouM., Arbuthnot P., Yaouanc J.J., Jaffres P.A., Miller A.D.: DODAG; a versatilenew cationic lipid that mediates efficient delivery of pDNAand siRNA. J. Control. Release, 2010; 143: 222-232
Google Scholar - 66. Milla P., Dosio F., Cattel L.: PEGylation of proteins and liposomes:a powerful and flexible strategy to improve the drug delivery. Curr.Drug. Metab., 2012; 13: 105-119
Google Scholar - 67. Mok H., Zhang M.: Superparamagnetic iron oxide nanoparticle-based delivery systems for biotherapeutics. Expert Opin. DrugDeliv., 2013; 10: 73-87
Google Scholar - 68. Morille M., Montier T., Legras P., Carmoy N., Brodin P., PitardB., Benoit J.P., Passirani C.: Long-circulating DNA lipid nanocapsulesas new vector for passive tumor targeting. Biomaterials, 2010; 31:321-329
Google Scholar - 69. Mufamadi M.S., Pillay V., Choonara Y.E., Du Toit L.C., Modi G.,Naidoo D., Ndesendo V.M.: A review on composite liposomal technologiesfor specialized drug delivery. J. Drug Deliv., 2011; 2011: 939851
Google Scholar - 70. Nie Y., Ji L., Ding H., Xie L., Li L., He B., Wu Y., Gu Z.: Cholesterolderivatives based charged liposomes for doxorubicin delivery:preparation, in vitro and in vivo characterization. Theranostics,2012; 2: 1092-1103
Google Scholar - 71. Ozpolat B., Sood A.K., Lopez-Berestein G.: Nanomedicine basedapproaches for the delivery of siRNA in cancer. J. Intern. Med., 2010;267: 44-53
Google Scholar - 72. Pastorino F., Brignole C., Loi M., Di Paolo D., Di Fiore A., Perri P.,Pagnan G., Ponzoni M.: Nanocarrier-mediated targeting of tumorand tumor vascular cells improves uptake and penetration of drugsinto neuroblastoma. Front. Oncol., 2013; 3: 190
Google Scholar - 73. Patil S.D., Rhodes D.G., Burgess D.J.: Biophysical characterizationof anionic lipoplexes. Biochim. Biophys. Acta, 2005; 1711: 1-11
Google Scholar - 74. Pirollo K.F., Zon G., Rait A., Zhou Q., Yu W., Hogrefe R., Chang E.H.: Tumor-targeting nanoimmunoliposome complex for short interferingRNA delivery. Hum. Gene Ther., 2006; 17: 117-124
Google Scholar - 75. Pisani M., Mobbili G., Bruni P.: Neutral liposomes and DNA transfection.W: Non-Viral Gene Therapy, red.: X. Yuan. InTech., 2011:319-348
Google Scholar - 76. Powoźnik B., Kubowicz P., Pękala E.: Przeciwciała monoklonalnew terapii celowanej. Postępy Hig. Med. Dośw., 2012; 66: 663-673
Google Scholar - 77. Reichert J.M., Rosensweig C.J., Faden L.B., Dewitz M.C.: Monoclonalantibody successes in the clinic. Nat. Biotechnol., 2005; 23:1073-1078
Google Scholar - 78. Rolland A., Sullivan S.M.: Pharmaceutical Gene Delivery Systems.Marcel Dekker, New York 2003: 99-101
Google Scholar - 79. Ropert C.: Liposomes as a gene delivery system. Braz. J. Med.Biol. Res., 1999; 32: 163-169
Google Scholar - 80. Rothdiener M., Muller D., Castro P.G., Scholz A., SchwemmleinM., Fey G., Heidenreich O., Kontermann R.E.: Targeted delivery ofSiRNA to CD33-positive tumor cells with liposomal carrier systems.J. Control. Release, 2010; 144: 251-258
Google Scholar - 81. Sahu N.K., Shilakari G., Nayak A., Kohli D.V.: Antisense technology:a selective tool for gene expression regulation and gene targeting.Curr. Pharm. Biotechnol., 2007; 8: 291-304
Google Scholar - 82. Sawant R.R., Torchilin V.P.: Challenges in development of targetedliposomal therapeutics. AAPS J., 2012; 14: 303-315
Google Scholar - 83. Shu Y., Pi F., Sharma A., Rajabi M., Haque F., Shu D., Leggas M.,Evers B.M., Guo P.: Stable RNA nanoparticles as potential new generationdrugs for cancer therapy. Adv. Drug Deliv. Rev., 2014; 66: 74-89
Google Scholar - 84. Sorkin A., Von Zastrow M.: Signal transduction and endocytosis:close encounters of many kinds. Nat. Rev. Mol. Cell Biol., 2002;3: 600-614
Google Scholar - 85. Spelios M., Kearns M., Savva M.: From gene delivery to gene silencing:plasmid DNA-transfecting cationic lipid 1,3-dimyristoylamidopropane-2-[bis(2-dimethylaminoethane)] carbamate efficientlypromotes small interfering RNA-induced RNA interference. Biochemistry,2010; 49: 5753-5759
Google Scholar - 86. Stabelska K., Wyrozumska P., Grzybek M., Sikorski A.F.: Charakterystykai medyczne zastosowania konstrukcji liposomowych. Adv.Clin. Exp. Med., 2002; 11: 229-242
Google Scholar - 87. Strebhardt K., Ullrich A.: Paul Ehrlich’s magic bullet concept: 100 years of progress. Nat. Rev. Cancer, 2008; 8: 473-480
Google Scholar - 88. Stuart D.D., Allen T.M.: A new liposomal formulation for antisenseoligodeoxynucleotides with small size, high incorporation efficiencyand good stability. Biochim. Biophys. Acta, 2000; 1463: 219-229
Google Scholar - 89. Szoka F.Jr., Papahadjopoulos D.: Procedure for preparation ofliposomes with large internal aqueous space and high capture byreverse-phase evaporation. Proc. Natl. Acad. Sci. USA, 1978; 75: 4194-4198
Google Scholar - 90. Szybalska E.H., Szybalski W.: Genetics of human cess line. IV.DNA-mediated heritable transformation of a biochemical trait. Proc.Natl. Acad. Sci. USA, 1962; 48: 2026-2034
Google Scholar - 91. Thierry A.R., Lunardi-Iskandar Y., Bryant J.L., Rabinovich P.,Gallo R.C., Mahan L.C.: Systemic gene therapy: biodistribution andlong-term expression of a transgene in mice. Proc. Natl. Acad. Sci.USA, 1995; 92: 9742-9746
Google Scholar - 92. Toporkiewicz M., Meissner J., Matusewicz L., Czogalla A., SikorskiA.F.: Toward a magic or imaginary bullet? Ligands for drug targetingto cancer cells: principles, hopes, and challenges. Int. J. Nanomedicine,2015; 10: 1399-1414
Google Scholar - 93. Torchilin V.: Tumor delivery of macromolecular drugs based onthe EPR effect. Adv. Drug Deliv. Rev., 2011; 63: 131-135
Google Scholar - 94. Torchilin V.P.: Recent advances with liposomes as pharmaceuticalcarriers. Nat. Rev. Drug Discov., 2005; 4: 145-160
Google Scholar - 95. Torchilin V.P.: Targeted pharmaceutical nanocarriers for cancertherapy and imaging. AAPS J., 2007; 9: E128-E147
Google Scholar - 96. Torchilin V.P.: Passive and active drug targeting: drug deliveryto tumors as an example. Handb. Exp. Pharmacol., 2010; 197: 3-53
Google Scholar - 97. Tyagi P., Kashyap M.P., Kawamorita N., Yoshizawa T., ChancellorM., Yoshimura N.: Intravesical liposome and antisense treatment fordetrusor overactivity and interstitial cystitis/painful bladder syndrome.ISRN Pharmacol., 2014; 2014: 601653
Google Scholar - 98. van Rooijen N., van Nieuwmegen R.: Liposomes in immunology:multilamellar phosphatidylcholine liposomes as a simple, biodegradableand harmless adjuvant without any immunogenic activityof its own. Immunol. Commun., 1980; 9: 243-256
Google Scholar - 99. Wang M., Thanou M.: Targeting nanoparticles to cancer. Pharmacol.Res., 2010; 62: 90-99
Google Scholar - 100. Williford J.M., Wu J., Ren Y., Archang M.M., Leong K.W., MaoH.Q.: Recent advances in nanoparticle-mediated siRNA delivery.Annu. Rev. Biomed. Eng., 2014; 16: 347-370
Google Scholar - 101. Wyrozumska P., Meissner J., Toporkiewicz M., Szarawarska M.,Kuliczkowski K., Ugorski M., Walasek M.A., Sikorski A.F.: Liposomecoatedlipoplex-based carrier for antisense oligonucleotides. CancerBiol. Ther., 2015; 16: 66-76
Google Scholar - 102. Yang H.W., Yi J.W., Bang E.K., Jeon E.M., Kim B.H.: Cationicnucleolipids as efficient siRNA carriers. Org. Biomol. Chem., 2011;9: 291-296
Google Scholar - 103. Yu B., Mao Y., Bai L.Y., Herman S.E., Wang X., Ramanunni A.,Jin Y., Mo X., Cheney C., Chan K.K., Jarjoura D., Marcucci G., Lee R.J.,Byrd J.C., Lee L.J., Muthusamy N.: Targeted nanoparticle deliveryovercomes off-target immunostimulatory effects of oligonucleotidesand improves therapeutic efficacy in chronic lymphocytic leukemia.Blood, 2013; 121: 136-147
Google Scholar - 104. Yu R.Z., Grundy J.S., Geary R.S.: Clinical pharmacokinetics ofsecond generation antisense oligonucleotides. Expert. Opin. DrugMetab. Toxicol., 2013; 9: 169-182
Google Scholar - 105. Zelphati O., Nguyen C., Ferrari M., Felgner J., Tsai Y., FelgnerP.L.: Stable and monodisperse lipoplex formulations for gene delivery.Gene Ther., 1998; 5: 1272-1282
Google Scholar - 106. Zelphati O., Uyechi L.S., Barron L.G., Szoka F.C.Jr.: Effect of serumcomponents on the physico-chemical properties of cationiclipid/oligonucleotide complexes and on their interactions with cells.Biochim. Biophys. Acta, 1998; 1390: 119-133
Google Scholar - 107. Zhang L., Chan J.M., Gu F.X., Rhee J.W., Wang A.Z., Radovic-Moreno A.F., Alexis F., Langer R., Farokhzad O.C.: Self-assembledlipid–polymer hybrid nanoparticles: a robust drug delivery platform.ACS Nano., 2008; 2: 1696-1702
Google Scholar - 108. Zhao W., Zhuang S., Qi X.R.: Comparative study of the in vitroand in vivo characteristics of cationic and neutral liposomes. Int. J.Nanomedicine, 2011; 6: 3087-3098
Google Scholar - 109. Zheng Y., Yu B., Weecharangsan W., Piao L., Darby M., Mao Y.,Koynova R., Yang X., Li H., Xu S., Lee L.J., Sugimoto Y., BrueggemeierR.W., Lee R.J.: Transferrin-conjugated lipid-coated PLGA nanoparticlesfor targeted delivery of aromatase inhibitor 7α-APTADD tobreast cancer cells. Int. J. Pharm., 2010; 390: 234-241
Google Scholar - 110. Zhi D., Zhang S., Wang B., Zhao Y., Yang B., Yu S.: Transfectionefficiency of cationic lipids with different hydrophobic domains ingene delivery. Bioconjug. Chem., 2010; 21: 563-577
Google Scholar - 111. Zhu L., Kate P., Torchilin V.P.: Matrix metalloprotease 2-responsivemultifunctional liposomal nanocarrier for enhanced tumortargeting. ACS Nano., 2012; 6: 3491-3498
Google Scholar - 112. Zhu L., Lu Y., Miller D.D., Mahato R.I.: Structural and formulationfactors influencing pyridinium lipid-based gene transfer. Bioconjug.Chem., 2008; 19: 2499-2512
Google Scholar - 113. Zhu L., Torchilin V.P.: Stimulus-responsive nanopreparationsfor tumor targeting. Integr. Biol., 2013; 5: 96-107
Google Scholar - 114. Zuhorn I.S., Engberts J.B., Hoekstra D.: Gene delivery by cationiclipid vectors: overcoming cellular barriers. Eur. Biophys. J.,2007; 36: 349-362
Google Scholar