Lipid-Based Vectors for Therapeutic mRNA-Based Anti-Cancer Vaccines

Author(s): Maria L. Guevara, Stefano Persano*, Francesca Persano.

Journal Name: Current Pharmaceutical Design

Volume 25 , Issue 13 , 2019


Abstract:

Cancer vaccines have been widely explored as a key tool for effective cancer immunotherapy. Despite a convincing rationale behind cancer vaccines, extensive past efforts were unsuccessful in mediating significantly relevant anti-tumor activity in clinical studies. One of the major reasons for such poor outcome, among others, is the low immunogenicity of more traditional vaccines, such as peptide-, protein- and DNA- based vaccines. Recently, mRNA emerged as a promising alternative to traditional vaccine strategies due to its high immunogenicity, suitability for large-scale and low-cost production, and superior safety profile. However, the clinical application of mRNA-based anti-cancer vaccines has been limited by their instability and inefficient in vivo delivery. Recent technological advances have now largely overcome these issues and lipid-based vectors have demonstrated encouraging results as mRNA vaccine platforms against several types of cancers. This review intends to provide a detailed overview of lipid-based vectors for the development of therapeutic mRNA-based anti-tumor vaccines.

Keywords: Cancer, immunotherapy, nanoparticles, mRNA, vaccines, liposome, non-viral vectors.

[1]
Deering RP, Kommareddy S, Ulmer JB, Brito LA, Geall AJ. Nucleic acid vaccines: Prospects for non-viral delivery of mRNA vaccines. Expert Opin Drug Deliv 2014; 11(6): 885-99.
[http://dx.doi.org/10.1517/17425247.2014.901308] [PMID: 24665982]
[2]
Oberli MA, Reichmuth AM, Dorkin JR, et al. Lipid nanoparticle assisted mRNA delivery for potent cancer immunotherapy. Nano Lett 2017; 17(3): 1326-35.
[http://dx.doi.org/10.1021/acs.nanolett.6b03329] [PMID: 28273716]
[3]
Kranz LM, Diken M, Haas H, et al. Systemic RNA delivery to dendritic cells exploits antiviral defence for cancer immunotherapy. Nature 2016; 534(7607): 396-401.
[http://dx.doi.org/10.1038/nature18300] [PMID: 27281205]
[4]
Pardi N, Hogan MJ, Naradikian MS, et al. Nucleoside-modified mRNA vaccines induce potent T follicular helper and germinal center B cell responses. J Exp Med 2018; 215(6): 1571-88.
[http://dx.doi.org/10.1084/jem.20171450] [PMID: 29739835]
[5]
Ferraro B, Morrow MP, Hutnick NA, Shin TH, Lucke CE, Weiner DB. Clinical applications of DNA vaccines: Current progress. Clin Infect Dis 2011; 53(3): 296-302.
[http://dx.doi.org/10.1093/cid/cir334] [PMID: 21765081]
[6]
Sahin U, Karikó K, Türeci Ö. mRNA-based therapeutics-developing a new class of drugs. Nat Rev Drug Discov 2014; 13(10): 759-80.
[http://dx.doi.org/10.1038/nrd4278] [PMID: 25233993]
[7]
Pardi N, Hogan MJ, Porter FW, Weissman D. mRNA vaccines - A new era in vaccinology. Nat Rev Drug Discov 2018; 17(4): 261-79.
[http://dx.doi.org/10.1038/nrd.2017.243] [PMID: 29326426]
[8]
Schlake T, Thess A, Fotin-Mleczek M, Kallen KJ. Developing mRNA-vaccine technologies. RNA Biol 2012; 9(11): 1319-30.
[http://dx.doi.org/10.4161/rna.22269] [PMID: 23064118]
[9]
Fotin-Mleczek M, Duchardt KM, Lorenz C, et al. Messenger RNA-based vaccines with dual activity induce balanced TLR-7 dependent adaptive immune responses and provide antitumor activity. J Immunother 2011; 34(1): 1-15.
[http://dx.doi.org/10.1097/CJI.0b013e3181f7dbe8] [PMID: 21150709]
[10]
Youn H, Chung JK. Modified mRNA as an alternative to plasmid DNA (pDNA) for transcript replacement and vaccination therapy. Expert Opin Biol Ther 2015; 15(9): 1337-48.
[http://dx.doi.org/10.1517/14712598.2015.1057563] [PMID: 26125492]
[11]
Zou S, Scarfo K, Nantz MH, Hecker JG. Lipid-mediated delivery of RNA is more efficient than delivery of DNA in non-dividing cells. Int J Pharm 2010; 389(1-2): 232-43.
[http://dx.doi.org/10.1016/j.ijpharm.2010.01.019] [PMID: 20080162]
[12]
Andries O, De Filette M, Rejman J, et al. Comparison of the gene transfer efficiency of mRNA/GL67 and pDNA/GL67 complexes in respiratory cells. Mol Pharm 2012; 9(8): 2136-45.
[http://dx.doi.org/10.1021/mp200604h] [PMID: 22676473]
[13]
Thess A, Grund S, Mui BL, et al. Sequence-engineered mRNA without chemical nucleoside modifications enables an effective protein therapy in large animals. Mol Ther 2015; 23(9): 1456-64.
[http://dx.doi.org/10.1038/mt.2015.103] [PMID: 26050989]
[14]
Schlake T, Thess A, Thran M, Jordan I. mRNA as novel technology for passive immunotherapy. Cell Mol Life Sci 2019; 76(2): 301-28.
[PMID: 30334070]
[15]
Hadas Y, Katz MG, Bridges CR, Zangi L. Modified mRNA as a therapeutic tool to induce cardiac regeneration in ischemic heart disease. Wiley Interdiscip Rev Syst Biol Med 2017; 9(1)
[http://dx.doi.org/10.1002/wsbm.1367] [PMID: 27911047]
[16]
Yanez Arteta M, Kjellman T, Bartesaghi S, et al. Successful reprogramming of cellular protein production through mRNA delivered by functionalized lipid nanoparticles. Proc Natl Acad Sci USA 2018; 115(15): E3351-60.
[http://dx.doi.org/10.1073/pnas.1720542115] [PMID: 29588418]
[17]
Schumann C, Nguyen DX, Norgard M, et al. Increasing lean muscle mass in mice via nanoparticle-mediated hepatic delivery of follistatin mRNA. Theranostics 2018; 8(19): 5276-88.
[http://dx.doi.org/10.7150/thno.27847] [PMID: 30555546]
[18]
Bangel-Ruland N, Tomczak K, Fernández Fernández E, et al. Cystic fibrosis transmembrane conductance regulator-mRNA delivery: A novel alternative for cystic fibrosis gene therapy. J Gene Med 2013; 15(11-12): 414-26.
[http://dx.doi.org/10.1002/jgm.2748] [PMID: 24123772]
[19]
Guan S, Rosenecker J. Nanotechnologies in delivery of mRNA therapeutics using nonviral vector-based delivery systems. Gene Ther 2017; 24(3): 133-43.
[http://dx.doi.org/10.1038/gt.2017.5] [PMID: 28094775]
[20]
Hajj KA, Whitehead KA. Tools for translation: Non-viral materials for therapeutic mRNA delivery. Nat Rev Mater 2017; 2(10): 17056.
[http://dx.doi.org/10.1038/natrevmats.2017.56]
[21]
Yin H, Kanasty RL, Eltoukhy AA, Vegas AJ, Dorkin JR, Anderson DG. Non-viral vectors for gene-based therapy. Nat Rev Genet 2014; 15(8): 541-55.
[http://dx.doi.org/10.1038/nrg3763] [PMID: 25022906]
[22]
Naso MF, Tomkowicz B, Perry WL III, Strohl WR. Adeno-associated virus (AAV) as a vector for gene therapy. BioDrugs 2017; 31(4): 317-34.
[http://dx.doi.org/10.1007/s40259-017-0234-5] [PMID: 28669112]
[23]
Reichmuth AM, Oberli MA, Jaklenec A, Langer R, Blankschtein D. mRNA vaccine delivery using lipid nanoparticles. Ther Deliv 2016; 7(5): 319-34.
[http://dx.doi.org/10.4155/tde-2016-0006] [PMID: 27075952]
[24]
Persano S, Guevara ML, Li Z, et al. Lipopolyplex potentiates anti-tumor immunity of mRNA-based vaccination. Biomaterials 2017; 125: 81-9.
[http://dx.doi.org/10.1016/j.biomaterials.2017.02.019] [PMID: 28231510]
[25]
McKinlay CJ, Benner NL, Haabeth OA, Waymouth RM, Wender PA. Enhanced mRNA delivery into lymphocytes enabled by lipid-varied libraries of charge-altering releasable transporters. Proc Natl Acad Sci USA 2018; 115(26): E5859-66.
[http://dx.doi.org/10.1073/pnas.1805358115] [PMID: 29891683]
[26]
Persano S. A self-assembled non-viral vector as potential platform for mRNA-based vaccines. Transl Biomed 2017; 8(3): 119.
[http://dx.doi.org/10.21767/2172-0479.100119]
[27]
Midoux P, Pichon C. Lipid-based mRNA vaccine delivery systems. Expert Rev Vaccines 2015; 14(2): 221-34.
[http://dx.doi.org/10.1586/14760584.2015.986104] [PMID: 25540984]
[28]
Perche F, Benvegnu T, Berchel M, et al. Enhancement of dendritic cells transfection in vivo and of vaccination against B16F10 melanoma with mannosylated histidylated lipopolyplexes loaded with tumor antigen messenger RNA. Nanomedicine 2011; 7(4): 445-53.
[http://dx.doi.org/10.1016/j.nano.2010.12.010] [PMID: 21220051]
[29]
Verbeke R, Lentacker I, Wayteck L, et al. Co-delivery of nucleoside-modified mRNA and TLR agonists for cancer immunotherapy: Restoring the immunogenicity of immunosilent mRNA. J Control Release 2017; 266: 287-300.
[http://dx.doi.org/10.1016/j.jconrel.2017.09.041] [PMID: 28987878]
[30]
Recent advances in mRNA vaccine delivery. Nano Res 2018; 11(10): 5338-54.
[http://dx.doi.org/10.1007/s12274-018-2091-z]
[31]
Fischer D, Bieber T, Li Y, Elsässer HP, Kissel T. A novel non-viral vector for DNA delivery based on low molecular weight, branched polyethylenimine: Effect of molecular weight on transfection efficiency and cytotoxicity. Pharm Res 1999; 16(8): 1273-9.
[http://dx.doi.org/10.1023/A:1014861900478] [PMID: 10468031]
[32]
Choi HY, Lee TJ, Yang GM, et al. Efficient mRNA delivery with graphene oxide-polyethylenimine for generation of footprint-free human induced pluripotent stem cells. J Control Release 2016; 235: 222-35.
[http://dx.doi.org/10.1016/j.jconrel.2016.06.007] [PMID: 27266364]
[33]
Uchida S, Itaka K, Chen Q, et al. Combination of chondroitin sulfate and polyplex micelles from Poly(ethylene glycol)-polyN′-[N-(2-aminoethyl)-2-aminoethyl]aspartamide block copolymer for prolonged in vivo gene transfection with reduced toxicity. J Control Release 2011; 155(2): 296-302.
[http://dx.doi.org/10.1016/j.jconrel.2011.04.026] [PMID: 21571018]
[34]
Matsui A, Uchida S, Ishii T, Itaka K, Kataoka K. Messenger RNA-based therapeutics for the treatment of apoptosis-associated diseases. Sci Rep 2015; 5: 15810.
[http://dx.doi.org/10.1038/srep15810] [PMID: 26507781]
[35]
Uchida S, Itaka K, Uchida H, et al. In vivo messenger RNA introduction into the central nervous system using polyplex nanomicelle. PLoS One 2013; 8(2)E56220
[http://dx.doi.org/10.1371/journal.pone.0056220] [PMID: 23418537]
[36]
Cheng C, Convertine AJ, Stayton PS, Bryers JD. Multifunctional triblock copolymers for intracellular messenger RNA delivery. Biomaterials 2012; 33(28): 6868-76.
[http://dx.doi.org/10.1016/j.biomaterials.2012.06.020] [PMID: 22784603]
[37]
Kamat CD, Shmueli RB, Connis N, Rudin CM, Green JJ, Hann CL. Poly(β-amino ester) nanoparticle delivery of TP53 has activity against small cell lung cancer in vitro and in vivo. Mol Cancer Ther 2013; 12(4): 405-15.
[http://dx.doi.org/10.1158/1535-7163.MCT-12-0956] [PMID: 23364678]
[38]
Mastorakos P, da Silva AL, Chisholm J, et al. Highly compacted biodegradable DNA nanoparticles capable of overcoming the mucus barrier for inhaled lung gene therapy. Proc Natl Acad Sci USA 2015; 112(28): 8720-5.
[http://dx.doi.org/10.1073/pnas.1502281112] [PMID: 26124127]
[39]
McKinlay CJ, Vargas JR, Blake TR, et al. Charge-altering releasable transporters (CARTs) for the delivery and release of mRNA in living animals. Proc Natl Acad Sci USA 2017; 114(4): E448-56.
[http://dx.doi.org/10.1073/pnas.1614193114] [PMID: 28069945]
[40]
Cheng Q, Wei T, Jia Y, et al. Dendrimer-based lipid nanoparticles deliver therapeutic FAH mRNA to normalize liver function and extend survival in a mouse model of hepatorenal tyrosinemia type I. Adv Mater 2018; 30(52)E1805308
[http://dx.doi.org/10.1002/adma.201805308] [PMID: 30368954]
[41]
Kaczmarek JC, Kauffman KJ, Fenton OS, et al. Optimization of a degradable polymer-lipid nanoparticle for potent systemic delivery of mRNA to the lung endothelium and immune cells. Nano Lett 2018; 18(10): 6449-54.
[http://dx.doi.org/10.1021/acs.nanolett.8b02917] [PMID: 30211557]
[42]
Finn JD, Smith AR, Patel MC, et al. A single administration of CRISPR/Cas9 lipid nanoparticles achieves robust and persistent in vivo genome editing. Cell Rep 2018; 22(9): 2227-35.
[http://dx.doi.org/10.1016/j.celrep.2018.02.014] [PMID: 29490262]
[43]
Fenton OS, Kauffman KJ, Kaczmarek JC, et al. Synthesis and biological evaluation of ionizable lipid materials for the in vivo delivery of messenger RNA to B lymphocytes. Adv Mater 2017; 29(33)
[http://dx.doi.org/10.1002/adma.201606944] [PMID: 28681930]
[44]
Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392(6673): 245-52.
[http://dx.doi.org/10.1038/32588] [PMID: 9521319]
[45]
Leone P, Shin EC, Perosa F, Vacca A, Dammacco F, Racanelli V. MHC class I antigen processing and presenting machinery: Organization, function, and defects in tumor cells. J Natl Cancer Inst 2013; 105(16): 1172-87.
[http://dx.doi.org/10.1093/jnci/djt184] [PMID: 23852952]
[46]
Kreiter S, Selmi A, Diken M, et al. Increased antigen presentation efficiency by coupling antigens to MHC class I trafficking signals. J Immunol 2008; 180(1): 309-18.
[http://dx.doi.org/10.4049/jimmunol.180.1.309] [PMID: 18097032]
[47]
Bonehill A, Heirman C, Tuyaerts S, et al. Efficient presentation of known HLA class II-restricted MAGE-A3 epitopes by dendritic cells electroporated with messenger RNA encoding an invariant chain with genetic exchange of class II-associated invariant chain peptide. Cancer Res 2003; 63(17): 5587-94.
[PMID: 14500399]
[48]
Bonehill A, Heirman C, Thielemans K. Genetic approaches for the induction of a CD4+ T cell response in cancer immunotherapy. J Gene Med 2005; 7(6): 686-95.
[http://dx.doi.org/10.1002/jgm.713] [PMID: 15693037]
[49]
Zhang XX, McIntosh TJ, Grinstaff MW. Functional lipids and lipoplexes for improved gene delivery. Biochimie 2012; 94(1): 42-58.
[http://dx.doi.org/10.1016/j.biochi.2011.05.005] [PMID: 21621581]
[50]
Habrant D, Peuziat P, Colombani T, et al. Design of ionizable lipids to overcome the limiting step of endosomal escape: Application in the intracellular delivery of mRNA, DNA, and siRNA. J Med Chem 2016; 59(7): 3046-62.
[http://dx.doi.org/10.1021/acs.jmedchem.5b01679] [PMID: 26943260]
[51]
Filion MC, Phillips NC. Toxicity and immunomodulatory activity of liposomal vectors formulated with cationic lipids toward immune effector cells. Biochim Biophys Acta 1997; 1329(2): 345-56.
[http://dx.doi.org/10.1016/S0005-2736(97)00126-0] [PMID: 9371426]
[52]
Knudsen KB, Northeved H, Kumar PE, et al. In vivo toxicity of cationic micelles and liposomes. Nanomedicine 2015; 11(2): 467-77.
[http://dx.doi.org/10.1016/j.nano.2014.08.004] [PMID: 25168934]
[53]
Wei X, Shao B, He Z, et al. Cationic nanocarriers induce cell necrosis through impairment of Na(+)/K(+)-ATPase and cause subsequent inflammatory response. Cell Res 2015; 25(2): 237-53.
[http://dx.doi.org/10.1038/cr.2015.9] [PMID: 25613571]
[54]
Liu Y, Huang L. Designer lipids advance systemic siRNA delivery. Mol Ther 2010; 18(4): 669-70.
[http://dx.doi.org/10.1038/mt.2010.39] [PMID: 20357780]
[55]
Rappolt M, Hickel A, Bringezu F, Lohner K. Mechanism of the lamellar/inverse hexagonal phase transition examined by high resolution x-ray diffraction. Biophys J 2003; 84(5): 3111-22.
[http://dx.doi.org/10.1016/S0006-3495(03)70036-8] [PMID: 12719241]
[56]
Salim M, Minamikawa H, Sugimura A, Hashim R. Amphiphilic designer nano-carriers for controlled release: From drug delivery to diagnostics. MedChemComm 2014; 5: 1602.
[http://dx.doi.org/10.1039/C4MD00085D]
[57]
Lasic DD. Novel applications of liposomes. Trends Biotechnol 1998; 16(7): 307-21.
[http://dx.doi.org/10.1016/S0167-7799(98)01220-7] [PMID: 9675915]
[58]
Kanasty R, Dorkin JR, Vegas A, Anderson D. Delivery materials for siRNA therapeutics. Nat Mater 2013; 12(11): 967-77.
[http://dx.doi.org/10.1038/nmat3765] [PMID: 24150415]
[59]
Sercombe L, Veerati T, Moheimani F, Wu SY, Sood AK, Hua S. Advances and challenges of liposome assisted drug delivery. Front Pharmacol 2015; 6: 286.
[http://dx.doi.org/10.3389/fphar.2015.00286] [PMID: 26648870]
[60]
Pasut G, Paolino D, Celia C, et al. Polyethylene glycol (PEG)-dendron phospholipids as innovative constructs for the preparation of super stealth liposomes for anticancer therapy. J Control Release 2015; 199: 106-13.
[http://dx.doi.org/10.1016/j.jconrel.2014.12.008] [PMID: 25499917]
[61]
Vertut-Doï A, Ishiwata H, Miyajima K. Binding and uptake of liposomes containing a poly(ethylene glycol) derivative of cholesterol (stealth liposomes) by the macrophage cell line J774: Influence of PEG content and its molecular weight. Biochim Biophys Acta 1996; 1278(1): 19-28.
[http://dx.doi.org/10.1016/0005-2736(95)00185-9] [PMID: 8611602]
[62]
Zhang L, Wang Y, Yang Y, et al. High tumor penetration of paclitaxel loaded pH sensitive cleavable liposomes by depletion of tumor collagen I in breast cancer. ACS Appl Mater Interfaces 2015; 7(18): 9691-701.
[http://dx.doi.org/10.1021/acsami.5b01473] [PMID: 25845545]
[63]
Terada T, Iwai M, Kawakami S, Yamashita F, Hashida M. Novel PEG-matrix metalloproteinase-2 cleavable peptide-lipid containing galactosylated liposomes for hepatocellular carcinoma-selective targeting. J Control Release 2006; 111(3): 333-42.
[http://dx.doi.org/10.1016/j.jconrel.2005.12.023] [PMID: 16488046]
[64]
Khalil IA, Kogure K, Futaki S, et al. Octaarginine-modified multifunctional envelope-type nanoparticles for gene delivery. Gene Ther 2007; 14(8): 682-9.
[http://dx.doi.org/10.1038/sj.gt.3302910] [PMID: 17268535]
[65]
Gjetting T, Arildsen NS, Christensen CL, et al. In vitro and in vivo effects of polyethylene glycol (PEG)-modified lipid in DOTAP/cholesterol-mediated gene transfection. Int J Nanomedicine 2010; 5: 371-83.
[PMID: 20957159]
[66]
Rafael D, Andrade F, Arranja A, Luis AS, Videira M. Lipoplexes and polyplexes: Gene therapyencyclopedia of biomedical polymers and polymeric biomaterials. 1st ed. CRC Press 2015; pp. 335-4347.
[http://dx.doi.org/10.1081/E-EBPP-120050058]
[67]
Hess PR, Boczkowski D, Nair SK, Snyder D, Gilboa E. Vaccination with mRNAs encoding tumor-associated antigens and granulocyte-macrophage colony-stimulating factor efficiently primes CTL responses, but is insufficient to overcome tolerance to a model tumor/self antigen. Cancer Immunol Immunother 2006; 55(6): 672-83.
[http://dx.doi.org/10.1007/s00262-005-0064-z] [PMID: 16133108]
[68]
Pollard C, Rejman J, De Haes W, et al. Type I IFN counteracts the induction of antigen-specific immune responses by lipid-based delivery of mRNA vaccines. Mol Ther 2013; 21(1): 251-9.
[http://dx.doi.org/10.1038/mt.2012.202] [PMID: 23011030]
[69]
De Beuckelaer A, Pollard C, Van Lint S, et al. Type I interferons interfere with the capacity of mRNA lipoplex vaccines to elicit cytolytic T cell responses. Mol Ther 2016; 24(11): 2012-20.
[http://dx.doi.org/10.1038/mt.2016.161] [PMID: 27506450]
[70]
Su X, Fricke J, Kavanagh DG, Irvine DJ. In vitro and in vivo mRNA delivery using lipid-enveloped pH-responsive polymer nanoparticles. Mol Pharm 2011; 8(3): 774-87.
[http://dx.doi.org/10.1021/mp100390w] [PMID: 21417235]
[71]
Mockey M, Bourseau E, Chandrashekhar V, et al. mRNA-based cancer vaccine: Prevention of B16 melanoma progression and metastasis by systemic injection of MART1 mRNA histidylated lipopolyplexes. Cancer Gene Ther 2007; 14(9): 802-14.
[http://dx.doi.org/10.1038/sj.cgt.7701072] [PMID: 17589432]
[72]
Madeira C, Loura LM, Prieto M, Fedorov A, Aires-Barros MR. Effect of ionic strength and presence of serum on lipoplexes structure monitorized by FRET. BMC Biotechnol 2008; 8: 20.
[http://dx.doi.org/10.1186/1472-6750-8-20] [PMID: 18302788]
[73]
Rezaee M, Oskuee RK, Nassirli H, Malaekeh-Nikouei B. Progress in the development of lipopolyplexes as efficient non-viral gene delivery systems. J Control Release 2016; 236: 1-14.
[http://dx.doi.org/10.1016/j.jconrel.2016.06.023] [PMID: 27317365]
[74]
van Broekhoven CL, Parish CR, Demangel C, Britton WJ, Altin JG. Targeting dendritic cells with antigen-containing liposomes: A highly effective procedure for induction of antitumor immunity and for tumor immunotherapy. Cancer Res 2004; 64(12): 4357-65.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-0138] [PMID: 15205352]
[75]
Qian Y, Jin H, Qiao S, et al. Targeting dendritic cells in lymph node with an antigen peptide-based nanovaccine for cancer immunotherapy. Biomaterials 2016; 98: 171-83.
[http://dx.doi.org/10.1016/j.biomaterials.2016.05.008] [PMID: 27192420]
[76]
Smith KA, Meisenburg BL, Tam VL, et al. Lymph node-targeted immunotherapy mediates potent immunity resulting in regression of isolated or metastatic HPV-transformed tumors. Clin Cancer Res 2009; 15(19): 6167-76.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-0645] [PMID: 19789304]
[77]
Trevaskis NL, Kaminskas LM, Porter CJ. From sewer to saviour - targeting the lymphatic system to promote drug exposure and activity. Nat Rev Drug Discov 2015; 14(11): 781-803.
[http://dx.doi.org/10.1038/nrd4608] [PMID: 26471369]
[78]
Manolova V, Flace A, Bauer M, Schwarz K, Saudan P, Bachmann MF. Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol 2008; 38(5): 1404-13.
[http://dx.doi.org/10.1002/eji.200737984] [PMID: 18389478]
[79]
Bachmann MF, Jennings GT. Vaccine delivery: A matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol 2010; 10(11): 787-96.
[http://dx.doi.org/10.1038/nri2868] [PMID: 20948547]
[80]
Andorko JI, Hess KL, Jewell CM. Harnessing biomaterials to engineer the lymph node microenvironment for immunity or tolerance. AAPS J 2015; 17(2): 323-38.
[http://dx.doi.org/10.1208/s12248-014-9708-2] [PMID: 25533221]
[81]
Segura E, Valladeau-Guilemond J, Donnadieu MH, Sastre-Garau X, Soumelis V, Amigorena S. Characterization of resident and migratory dendritic cells in human lymph nodes. J Exp Med 2012; 209(4): 653-60.
[http://dx.doi.org/10.1084/jem.20111457] [PMID: 22430490]
[82]
Kreutz M, Tacken PJ, Figdor CG. Targeting dendritic cells-why bother? Blood 2013; 121(15): 2836-44.
[http://dx.doi.org/10.1182/blood-2012-09-452078] [PMID: 23390195]
[83]
Oussoren C, Zuidema J, Crommelin DJA, Storm G. Lymphatic uptake and biodistribution of liposomes after subcutaneous injection. II. Influence of liposomal size, lipid compostion and lipid dose. Biochim Biophys Acta 1997; 1328(2): 261-72.
[http://dx.doi.org/10.1016/S0005-2736(97)00122-3] [PMID: 9315622]
[84]
Carstens MG, Camps MGM, Henriksen-Lacey M, et al. Effect of vesicle size on tissue localization and immunogenicity of liposomal DNA vaccines. Vaccine 2011; 29(29-30): 4761-70.
[http://dx.doi.org/10.1016/j.vaccine.2011.04.081] [PMID: 21565240]
[85]
Badiee A, Khamesipour A, Samiei A, et al. The role of liposome size on the type of immune response induced in BALB/c mice against leishmaniasis: Rgp63 as a model antigen. Exp Parasitol 2012; 132(4): 403-9.
[http://dx.doi.org/10.1016/j.exppara.2012.09.001] [PMID: 22982807]
[86]
Henriksen-Lacey M, Devitt A, Perrie Y. The vesicle size of DDA:TDB liposomal adjuvants plays a role in the cell-mediated immune response but has no significant effect on antibody production. J Control Release 2011; 154(2): 131-7.
[http://dx.doi.org/10.1016/j.jconrel.2011.05.019] [PMID: 21640145]
[87]
Brewer JM, Tetley L, Richmond J, Liew FY, Alexander J. Lipid vesicle size determines the Th1 or Th2 response to entrapped antigen. J Immunol 1998; 161(8): 4000-7.
[PMID: 9780169]
[88]
Nakamura T, Yamazaki D, Yamauchi J, Harashima H. The nanoparticulation by octaarginine-modified liposome improves α-galactosylceramide-mediated antitumor therapy via systemic administration. J Control Release 2013; 171(2): 216-24.
[http://dx.doi.org/10.1016/j.jconrel.2013.07.004] [PMID: 23860186]
[89]
Foged C, Arigita C, Sundblad A, Jiskoot W, Storm G, Frokjaer S. Interaction of dendritic cells with antigen-containing liposomes: Effect of bilayer composition. Vaccine 2004; 22(15-16): 1903-13.
[http://dx.doi.org/10.1016/j.vaccine.2003.11.008] [PMID: 15121302]
[90]
Ma Y, Zhuang Y, Xie X, et al. The role of surface charge density in cationic liposome-promoted dendritic cell maturation and vaccine-induced immune responses. Nanoscale 2011; 3(5): 2307-14.
[http://dx.doi.org/10.1039/c1nr10166h] [PMID: 21499635]
[91]
Barnier-Quer C, Elsharkawy A, Romeijn S, Kros A, Jiskoot W. Adjuvant effect of cationic liposomes for subunit influenza vaccine: Influence of antigen loading method, cholesterol and immune modulators. Pharmaceutics 2013; 5(3): 392-410.
[http://dx.doi.org/10.3390/pharmaceutics5030392] [PMID: 24300513]
[92]
Badiee A, Jaafari MR, Khamesipour A, et al. The role of liposome charge on immune response generated in BALB/c mice immunized with recombinant major surface glycoprotein of Leishmania (rgp63). Exp Parasitol 2009; 121(4): 362-9.
[http://dx.doi.org/10.1016/j.exppara.2008.12.015] [PMID: 19211022]
[93]
Henriksen-Lacey M, Christensen D, Bramwell VW, et al. Liposomal cationic charge and antigen adsorption are important properties for the efficient deposition of antigen at the injection site and ability of the vaccine to induce a CMI response. J Control Release 2010; 145(2): 102-8.
[http://dx.doi.org/10.1016/j.jconrel.2010.03.027] [PMID: 20381556]
[94]
Kaur R, Bramwell VW, Kirby DJ, Perrie Y. Manipulation of the surface pegylation in combination with reduced vesicle size of cationic liposomal adjuvants modifies their clearance kinetics from the injection site, and the rate and type of T cell response. J Control Release 2012; 164(3): 331-7.
[http://dx.doi.org/10.1016/j.jconrel.2012.07.012] [PMID: 22800572]
[95]
Kaur R, Bramwell VW, Kirby DJ, Perrie Y. Pegylation of DDA:TDB liposomal adjuvants reduces the vaccine depot effect and alters the Th1/Th2 immune responses. J Control Release 2012; 158(1): 72-7.
[http://dx.doi.org/10.1016/j.jconrel.2011.10.012] [PMID: 22032883]
[96]
Tanaka Y, Taneichi M, Kasai M, Kakiuchi T, Uchida T. Liposome-coupled antigens are internalized by antigen-presenting cells via pinocytosis and cross-presented to CD8 T cells. PLoS One 2010; 5(12)e15225
[http://dx.doi.org/10.1371/journal.pone.0015225] [PMID: 21179411]
[97]
Christensen D, Henriksen-Lacey M, Kamath AT, et al. A cationic vaccine adjuvant based on a saturated quaternary ammonium lipid have different in vivo distribution kinetics and display a distinct CD4 T cell-inducing capacity compared to its unsaturated analog. J Control Release 2012; 160(3): 468-76.
[http://dx.doi.org/10.1016/j.jconrel.2012.03.016] [PMID: 22709414]
[98]
Mazumdar T, Anam K, Ali N. Influence of phospholipid composition on the adjuvanticity and protective efficacy of liposome-encapsulated Leishmania donovani antigens. J Parasitol 2005; 91(2): 269-74.
[http://dx.doi.org/10.1645/GE-356R1] [PMID: 15986599]
[99]
Van der Jeught K, Joe PT, Bialkowski L, et al. Intratumoral administration of mRNA encoding a fusokine consisting of IFN-β and the ectodomain of the TGF-β receptor II potentiates antitumor immunity. Oncotarget 2014; 5(20): 10100-13.
[http://dx.doi.org/10.18632/oncotarget.2463] [PMID: 25338019]
[100]
Marabelle A, Kohrt H, Caux C, Levy R. Intratumoral immunization: A new paradigm for cancer therapy. Clin Cancer Res 2014; 20(7): 1747-56.
[http://dx.doi.org/10.1158/1078-0432.CCR-13-2116] [PMID: 24691639]
[101]
Dorrani M, Garbuzenko OB, Minko T, Michniak-Kohn B. Development of edge-activated liposomes for siRNA delivery to human basal epidermis for melanoma therapy. J Control Release 2016; 228: 150-8.
[http://dx.doi.org/10.1016/j.jconrel.2016.03.010] [PMID: 26965957]
[102]
Garbuzenko OB, Saad M, Betigeri S, et al. Intratracheal versus intravenous liposomal delivery of siRNA, antisense oligonucleotides and anticancer drug. Pharm Res 2009; 26(2): 382-94.
[http://dx.doi.org/10.1007/s11095-008-9755-4] [PMID: 18958402]
[103]
Üner M, Yener G. Importance of solid lipid nanoparticles (SLN) in various administration routes and future perspectives. Int J Nanomedicine 2007; 2(3): 289-300.
[PMID: 18019829]
[104]
Blanco E, Shen H, Ferrari M. Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat Biotechnol 2015; 33(9): 941-51.
[http://dx.doi.org/10.1038/nbt.3330] [PMID: 26348965]
[105]
Wu Y, Crawford M, Yu B, Mao Y, Nana-Sinkam SP, Lee LJ. MicroRNA delivery by cationic lipoplexes for lung cancer therapy. Mol Pharm 2011; 8(4): 1381-9.
[http://dx.doi.org/10.1021/mp2002076] [PMID: 21648427]
[106]
Wu Y, Crawford M, Mao Y, et al. Therapeutic delivery of MicroRNA-29b by cationic lipoplexes for lung cancer. Mol Ther Nucleic Acids 2013; 2e84
[http://dx.doi.org/10.1038/mtna.2013.14] [PMID: 23591808]
[107]
Wang X, Yu B, Ren W, et al. Enhanced hepatic delivery of siRNA and microRNA using oleic acid based lipid nanoparticle formulations. J Control Release 2013; 172(3): 690-8.
[http://dx.doi.org/10.1016/j.jconrel.2013.09.027] [PMID: 24121065]
[108]
Joshi S, Cooke JR, Chan DK, et al. Liposome size and charge optimization for intraarterial delivery to gliomas. Drug Deliv Transl Res 2016; 6(3): 225-33.
[http://dx.doi.org/10.1007/s13346-016-0294-y] [PMID: 27091339]
[109]
Sahin U, Derhovanessian E, Miller M, et al. Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer. Nature 2017; 547(7662): 222-6.
[http://dx.doi.org/10.1038/nature23003] [PMID: 28678784]
[110]
Gfeller D, Bassani-Sternberg M, Schmidt J, Luescher IF. Current tools for predicting cancer-specific T cell immunity. OncoImmunology 2016; 5(7)E1177691
[http://dx.doi.org/10.1080/2162402X.2016.1177691] [PMID: 27622028]
[111]
Bol KF, Schreibelt G, Gerritsen WR, de Vries IJ, Figdor CG. Dendritic cell-based immunotherapy: State of the art and beyond. Clin Cancer Res 2016; 22(8): 1897-906.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-1399] [PMID: 27084743]
[112]
Pepini T, Pulichino AM, Carsillo T, et al. Induction of an IFN-mediated antiviral response by a self-amplifying RNA Vaccine: Implications for vaccine design. J Immunol 2017; 198(10): 4012-24.
[http://dx.doi.org/10.4049/jimmunol.1601877] [PMID: 28416600]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 25
ISSUE: 13
Year: 2019
Page: [1443 - 1454]
Pages: 12
DOI: 10.2174/1381612825666190619150221
Price: $58

Article Metrics

PDF: 28
HTML: 6

Special-new-year-discount