Materials for non-viral intracellular delivery of messenger RNA therapeutics

Journal of Controlled Release

Volumn 240, Issue , 2016, Pages 227-234

  Kauffman, Kevin J ^a,b   Webber, Matthew J ^b,c   Anderson, Daniel G ^a,b,c  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Drug delivery; Endosomal escape; Gene therapy; Genome editing; Immunoengineering; mRNA

Indexed keywords

DRUG DELIVERY; GENE THERAPY; GENES; HYBRID MATERIALS; MOLECULAR BIOLOGY; RNA;

ENDOSOMAL ESCAPES; GENOMIC ENGINEERINGS; IMMUNOENGINEERING; INTRACELLULAR DELIVERY; MESSENGER RNAS (MRNA); MRNA; NUCLEIC ACID DELIVERIES; SMALL INTERFERING RNA;

NUCLEIC ACIDS;

LIPID; LIPOPLEX; MESSENGER RNA; NANOCARRIER; NANOPARTICLE; OLIGONUCLEOTIDE; POLYMER; PROTAMINE;

ARTICLE; DRUG FORMULATION; HUMAN; IN VIVO GENE TRANSFER; NONVIRAL GENE DELIVERY SYSTEM; NONVIRAL GENE THERAPY; PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; RNAI THERAPEUTICS; ANIMAL; DRUG DELIVERY SYSTEM; DRUG EFFECTS; GENE THERAPY; GENETICS; INTRACELLULAR FLUID; METABOLISM; PROCEDURES; TRENDS;

ANIMALS; DRUG DELIVERY SYSTEMS; GENETIC THERAPY; HUMANS; INTRACELLULAR FLUID; POLYMERS; PROTAMINES; RNA, MESSENGER;

EID: 84954288084     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.12.032     Document Type: Article

References (114)

1. [1] Carlberg, C., Molnár, F., Mechanisms of Gene Regulation. 2014, 3–15.
2. [2] Holoch, D., Moazed, D., RNA-mediated epigenetic regulation of gene expression. Nat. Rev. Genet. 16 (2015), 71–84.
3. [3] Yin, H., et al. Non-viral vectors for gene-based therapy. Nat. Rev. Genet. 15 (2014), 541–555.
4. [4] Hillaireau, H., Couvreur, P., Nanocarriers' entry into the cell: relevance to drug delivery. Cell. Mol. Life Sci. 66 (2009), 2873–2896.
5. [5] Whitehead, K.A., Langer, R., Anderson, D.G., Knocking down barriers: advances in siRNA delivery. Nat. Rev. Drug Discov. 8 (2009), 129–138.
6. [6] Karikó, K., Buckstein, M., Ni, H., Weissman, D., Suppression of RNA recognition by toll-like receptors: the impact of nucleoside modification and the evolutionary origin of RNA. Immunity 23 (2005), 165–175.
7. [7] Whitehead, K.A., Dahlman, J.E., Langer, R.S., Anderson, D.G., Silencing or stimulation? siRNA delivery and the immune system. Annu. Rev. Chem. Biomol. Eng. 2 (2011), 77–96.
8. [8] Luo, D., Saltzman, W.M., Synthetic DNA delivery systems. Nat. Biotechnol. 18 (2000), 33–37.
9. [9] Scheicher, B., Schachner-Nedherer, A.-L., Zimmer, A., Protamine-oligonucleotide-nanoparticles: recent advances in drug delivery and drug targeting. Eur. J. Pharm. Sci. 75 (2015), 54–59.
10. [10] Bettinger, T., Carlisle, R.C., Read, M.L., Ogris, M., Seymour, L.W., Peptide-mediated RNA delivery: a novel approach for enhanced transfection of primary and post-mitotic cells. Nucleic Acids Res. 29 (2001), 3882–3891.
11. [11] Green, J.J., Langer, R., Anderson, D.G., A combinatorial polymer library approach yields insight into nonviral gene delivery. Acc. Chem. Res. 41 (2008), 749–759.
12. [12] Heyes, J., Palmer, L., Bremner, K., MacLachlan, I., Cationic lipid saturation influences intracellular delivery of encapsulated nucleic acids. J. Control. Release 107 (2005), 276–287.
13. [13] Fire, A., et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391 (1998), 806–811.
14. [14] Akinc, A., et al. A combinatorial library of lipid-like materials for delivery of RNAi therapeutics. Nat. Biotechnol. 26 (2008), 561–569.
15. [15] Semple, S.C., et al. Rational design of cationic lipids for siRNA delivery. Nat. Biotechnol. 28 (2010), 172–176.
16. [16] McIvor, R.S., Therapeutic delivery of mRNA: the medium is the message. Mol. Ther. 19 (2011), 822–823.
17. [17] Weissman, D., mRNA transcript therapy. Expert Rev. Vaccines 14 (2015), 265–281.
18. [18] Sahin, U., Karikó, K., Türeci, Ö., mRNA-based therapeutics — developing a new class of drugs. Nat. Rev. Drug Discov. 13 (2014), 759–780.
19. [19] Vallazza, B., et al. Recombinant messenger RNA technology and its application in cancer immunotherapy, transcript replacement therapies, pluripotent stem cell induction, and beyond. Wiley Interdiscip. Rev. RNA 6 (2015), 471–499, 10.1002/wrna.1288.
20. [20] Hacein-Bey-Abina, S., et al. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N. Engl. J. Med. 348 (2003), 255–256.
21. [21] Kreiter, S., Diken, M., Sahin, U., Britten, C.M., (eds.) Cancer Immunotherapy Meets Oncology, 2014, 21–27.
22. [22] Pollard, C., De Koker, S., Saelens, X., Vanham, G., Grooten, J., Challenges and advances towards the rational design of mRNA vaccines. Trends Mol. Med. 19 (2013), 705–713.
23. [23] Weiss, R., Scheiblhofer, S., Roesler, E., Weinberger, E., Thalhamer, J., mRNA vaccination as a safe approach for specific protection from type I allergy. Expert Rev. Vaccines 11 (2012), 55–67.
24. [24] Wang, H., et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/cas-mediated genome engineering. Cell 153 (2013), 910–918.
25. [25] Bernal, J.A., RNA-based tools for nuclear reprogramming and lineage-conversion: towards clinical applications. J. Cardiovasc. Transl. Res. 6 (2013), 956–968.
26. [26] Kotterman, M.A., Schaffer, D.V., Engineering adeno-associated viruses for clinical gene therapy. Nat. Rev. Genet. 15 (2014), 445–451.
27. [27] Giacca, M., Zacchigna, S., Virus-mediated gene delivery for human gene therapy. J. Control. Release 161 (2012), 377–388.
28. [28] Lorenz, C., et al. Protein expression from exogenous mRNA: uptake by receptor-mediated endocytosis and trafficking via the lysosomal pathway. RNA Biol. 8 (2011), 627–636.
29. [29] Zhao, Y., et al. High-efficiency transfection of primary human and mouse T lymphocytes using RNA electroporation. Mol. Ther. 13 (2006), 151–159.
30. [30] Piggott, J.M., Sheahan, B.J., Soden, D.M., O'Sullivan, G.C., Atkins, G.J., Electroporation of RNA stimulates immunity to an encoded reporter gene in mice. Mol. Med. Rep. 2 (2009), 753–756.
31. [31] Ainger, K., et al. Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes. J. Cell Biol. 123 (1993), 431–441.
32. [32] Mehier-Humbert, S., Guy, R.H., Physical methods for gene transfer: improving the kinetics of gene delivery into cells. Adv. Drug Deliv. Rev. 57 (2005), 733–753.
33. [33] Vassilev, V.B., Gil, L.H.V.G., Donis, R.O., Microparticle-mediated RNA immunization against bovine viral diarrhea virus. Vaccine 19 (2001), 2012–2019.
34. [34] Phua, K.K.L., Leong, K.W., Nair, S.K., Transfection efficiency and transgene expression kinetics of mRNA delivered in naked and nanoparticle format. J. Control. Release 166 (2013), 227–233.
35. [35] Wolff, J.A., et al. Direct gene transfer into mouse muscle in vivo. Science 247 (1990), 1465–1468.
36. [36] Van Lint, S., et al. Preclinical evaluation of TriMix and antigen mRNA-based antitumor therapy. Cancer Res. 72 (2012), 1661–1671.
37. [37] Soutschek, J., et al. Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature 432 (2004), 173–178.
38. [38] Wolfrum, C., et al. Mechanisms and optimization of in vivo delivery of lipophilic siRNAs. Nat. Biotechnol. 25 (2007), 1149–1157.
39. [39] Rensen, P.C., et al. Determination of the upper size limit for uptake and processing of ligands by the asialoglycoprotein receptor on hepatocytes in vitro and in vivo. J. Biol. Chem. 276 (2001), 37577–37584.
40. [40] Drickamer, K., Selective sugar binding to the carbohydrate recognition domains of the rat hepatic and macrophage asialoglycoprotein receptors. J. Biol. Chem. 271 (1996), 6686–6693.
41. [41] Mamidyala, S.K., et al. Glycomimetic ligands for the human asialoglycoprotein receptor. J. Am. Chem. Soc. 134 (2012), 1978–1981.
42. [42] Nair, J.K., et al. Multivalent N-acetylgalactosamine-conjugated siRNA localizes in hepatocytes and elicits robust RNAi-mediated gene silencing. J. Am. Chem. Soc., 2014, 10.1021/ja505986a.
43. [43] Matsuda, S., et al. siRNA conjugates carrying sequentially assembled trivalent N-acetylgalactosamine linked through nucleosides elicit robust gene silencing in vivo in hepatocytes. ACS Chem. Biol., 2015 (150302145121004).
44. [44] Rand, T.A., Petersen, S., Du, F., Wang, X., Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell 123 (2005), 621–629.
45. [45] Deleavey, G.F., Damha, M.J., Designing chemically modified oligonucleotides for targeted gene silencing. Chem. Biol. 19 (2012), 937–954.
46. [46] Calabretta, A., Kupfer, P.A., Leumann, C.J., The effect of RNA base lesions on mRNA translation. Nucleic Acids Res., 2015, 1–8.
47. [47] Wang, X., et al. N6-methyladenosine modulates messenger RNA translation efficiency. Cell 161 (2015), 1388–1399.
48. [48] Karikó, K., et al. Incorporation of pseudouridine into mRNA yields superior nonimmunogenic vector with increased translational capacity and biological stability. Mol. Ther. 16 (2008), 1833–1840.
49. [49] Karikó, K., Muramatsu, H., Keller, J.M., Weissman, D., Increased erythropoiesis in mice injected with submicrogram quantities of pseudouridine-containing mRNA encoding erythropoietin. Mol. Ther. 20 (2012), 948–953.
50. [50] Anderson, B.R., et al. Incorporation of pseudouridine into mRNA enhances translation by diminishing PKR activation. Nucleic Acids Res. 38 (2010), 5884–5892.
51. [51] Wilusz, C.J., Wormington, M., Peltz, S.W., The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell Biol. 2 (2001), 237–246.
52. [52] Gallie, D.R., The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev. 5 (1991), 2108–2116.
53. [53] Jackson, R.J., Cytoplasmic regulation of mRNA function: the importance of the 3′ untranslated region. Cell 74 (1993), 9–14.
54. [54] Wilkie, G.S., Dickson, K.S., Gray, N.K., Regulation of mRNA translation by 5′- and 3'-UTR-binding factors. Trends Biochem. Sci. 28 (2003), 182–188.
55. [55] Thess, A., et al. Sequence-engineered mRNA without chemical nucleoside modifications enables an effective protein therapy in large animals. Mol. Ther., 2015, 1–9.
56. [56] Mauro, V.P., Chappell, S.A., A critical analysis of codon optimization in human therapeutics. Trends Mol. Med. 20 (2014), 604–613.
57. [57] Amos, H., Protamine enhancement of RNA uptake by cultured chick cells. Biochem. Biophys. Res. Commun. 5 (1961), 1–4.
58. [58] Choi, Y.S., et al. The systemic delivery of siRNAs by a cell penetrating peptide, low molecular weight protamine. Biomaterials 31 (2010), 1429–1443.
59. [59] Kallen, K.J., et al. A novel, disruptive vaccination technology: self-adjuvanted RNActive vaccines. Hum. Vaccin. Immunother. 9 (2013), 2263–2276.
60. [60] Fotin-Mleczek, M., et al. Messenger RNA-based vaccines with dual activity induce balanced TLR-7 dependent adaptive immune responses and provide antitumor activity. J. Immunother. 34 (2011), 1–15.
61. [61] Scheel, B., et al. Toll-like receptor-dependent activation of several human blood cell types by protamine-condensed mRNA. Eur. J. Immunol. 35 (2005), 1557–1566.
62. [62] Schell, B., et al. Immunostimulating capacities of stabilized RNA molecules. Eur. J. Immunol. 34 (2004), 537–547.
63. [63] Heil, F., et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303 (2004), 1526–1529.
64. [64] Petsch, B., et al. Protective efficacy of in vitro synthesized, specific mRNA vaccines against influenza A virus infection. Nat. Biotechnol. 30 (2012), 1210–1216.
65. [65] Weide, B., et al. Direct injection of protamine-protected mRNA: results of a phase 1/2 vaccination trial in metastatic melanoma patients. J. Immunother. 32 (2009), 498–507.
66. [66] Sebastian, M., et al. Phase Ib study evaluating a self-adjuvanted mRNA cancer vaccine (RNActive®) combined with local radiation as consolidation and maintenance treatment for patients with stage IV non-small cell lung cancer. BMC Cancer, 14, 2014, 748.
67. [67] Kübler, H., et al. Self-adjuvanted mRNA vaccination in advanced prostate cancer patients: a first-in-man phase I/IIa study. J. Immunother. Cancer, 3, 2015, 26.
68. [68] Kanasty, R., Dorkin, J.R., Vegas, A., Anderson, D., Delivery materials for siRNA therapeutics. Nat. Mater. 12 (2013), 967–977.
69. [69] Midoux, P., Pichon, C., Lipid-based mRNA vaccine delivery systems. Expert Rev. Vaccines 14 (2015), 221–234.
70. [70] Kormann, M.S.D., et al. Expression of therapeutic proteins after delivery of chemically modified mRNA in mice. Nat. Biotechnol. 29 (2011), 154–157.
71. [71] Rejman, J., Tavernier, G., Bavarsad, N., Demeester, J., De Smedt, S.C., MRNA transfection of cervical carcinoma and mesenchymal stem cells mediated by cationic carriers. J. Control. Release 147 (2010), 385–391.
72. [72] Pollard, C., et al. Type I IFN counteracts the induction of antigen-specific immune responses by lipid-based delivery of mRNA vaccines. Mol. Ther. 21 (2012), 251–259.
73. [73] Akinc, A., et al. Targeted delivery of RNAi therapeutics with endogenous and exogenous ligand-based mechanisms. Mol. Ther. 18 (2010), 1357–1364.
74. [74] Sahay, G., et al. Efficiency of siRNA delivery by lipid nanoparticles is limited by endocytic recycling. Nat. Biotechnol. 31 (2013), 653–658.
75. [75] Wittrup, A., et al. Visualizing lipid-formulated siRNA release from endosomes and target gene knockdown. Nat. Biotechnol., 2015, 1–9.
76. [76] Dong, Y., et al. Lipopeptide nanoparticles for potent and selective siRNA delivery in rodents and nonhuman primates. Proc. Natl. Acad. Sci. 111 (2014), 3955–3960.
77. [77] Zimmermann, T.S., et al. RNAi-mediated gene silencing in non-human primates. Nature 441 (2006), 111–114.
78. [78] Geall, A.J., et al. Nonviral delivery of self-amplifying RNA vaccines. Proc. Natl. Acad. Sci. 109 (2012), 14604–14609.
79. [79] Jayaraman, M., et al. Maximizing the potency of siRNA lipid nanoparticles for hepatic gene silencing in vivo. Angew. Chem. Int. Ed. Engl. 51 (2012), 8529–8533.
80. [80] Maier, M.A., et al. Biodegradable lipids enabling rapidly eliminated lipid nanoparticles for systemic delivery of RNAi therapeutics. Mol. Ther. 21 (2013), 1570–1578.
81. [81] Love, K.T., et al. Lipid-like materials for low-dose, in vivo gene silencing. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 1864–1869.
82. [82] Whitehead, K.A., et al. Degradable lipid nanoparticles with predictable in vivo siRNA delivery activity. Nat. Commun., 5, 2014, 4277.
83. [83] Kauffman, K.J., et al. Optimization of Lipid Nanoparticle Formulations for mRNA Delivery in Vivo with Fractional Factorial and Definitive Screening Designs. Nano Lett. 15 (2015), 7300–7306.
84. [84] Chen, D., et al. Rapid discovery of potent siRNA-containing lipid nanoparticles enabled by controlled microfluidic formulation. J. Am. Chem. Soc. 134 (2012), 6948–6951.
85. [85] Brito, L.A., et al. A cationic nanoemulsion for the delivery of next generation RNA vaccines. Mol. Ther. 22 (2014), 2118–2129.
86. [86] Bogers, W.M., et al. Potent immune responses in rhesus macaques induced by nonviral delivery of a self-amplifying RNA vaccine expressing HIV type 1 envelope with a cationic nanoemulsion. J. Infect. Dis. 211 (2014), 947–955.
87. [87] Kanasty, R.L., Whitehead, K.A., Vegas, A.J., Anderson, D.G., Action and reaction: the biological response to siRNA and its delivery vehicles. Mol. Ther. 20 (2012), 513–524.
88. [88] Mundargi, R.C., Babu, V.R., Rangaswamy, V., Patel, P., Aminabhavi, T.M., Nano/micro technologies for delivering macromolecular therapeutics using poly(d,l-lactide-co-glycolide) and its derivatives. J. Control. Release 125 (2008), 193–209.
89. [89] Lungwitz, U., Breunig, M., Blunk, T., Göpferich, A., Polyethylenimine-based non-viral gene delivery systems. Eur. J. Pharm. Biopharm. 60 (2005), 247–266.
90. [90] Günther, M., et al. Polyethylenimines for RNAi-mediated gene targeting in vivo and siRNA delivery to the lung. Eur. J. Pharm. Biopharm. 77 (2011), 438–449.
91. [91] Lv, H., Zhang, S., Wang, B., Cui, S., Yan, J., Toxicity of cationic lipids and cationic polymers in gene delivery. J. Control. Release 114 (2006), 100–109.
92. [92] Agarwal, S., Zhang, Y., Maji, S., Greiner, A., PDMAEMA based gene delivery materials. Mater. Today 15 (2012), 388–393.
93. [93] Üzgün, S., et al. PEGylation improves nanoparticle formation and transfection efficiency of messenger RNA. Pharm. Res. 28 (2011), 2223–2232.
94. [94] Kim, S.W., Polylysine copolymers for gene delivery. Cold Spring Harb. Protoc. 7 (2012), 433–438.
95. [95] Mao, S., Sun, W., Kissel, T., Chitosan-based formulations for delivery of DNA and siRNA. Adv. Drug Deliv. Rev. 62 (2010), 12–27.
96. [96] Nafee, N., Taetz, S., Schneider, M., Schaefer, U.F., Lehr, C.M., Chitosan-coated PLGA nanoparticles for DNA/RNA delivery: effect of the formulation parameters on complexation and transfection of antisense oligonucleotides. Nanomed. Nanotechnol. Biol. Med. 3 (2007), 173–183.
97. [97] Mahiny, A.J., et al. In vivo genome editing using nuclease-encoding mRNA corrects SP-B deficiency. Nat. Biotechnol., 2015, 2–6.
98. [98] Lynn, D.M., Langer, R., Degradable poly (beta-amino esters): synthesis, characterization, and self-assembly with plasmid DNA. J. Am. Chem. Soc. 122 (2000), 10761–10768.
99. [99] Anderson, D.G., Lynn, D.M., Langer, R., Semi-automated synthesis and screening of a large library of degradable cationic polymers for gene delivery. Angew. Chem. Int. Ed. Engl. 42 (2003), 3153–3158.
100. [100] Anderson, D.G., Akinc, A., Hossain, N., Langer, R., Structure/property studies of polymeric gene delivery using a library of poly(beta-amino esters). Mol. Ther. 11 (2005), 426–434.
101. [101] Zugates, G.T., et al. Rapid optimization of gene delivery by parallel end-modification of poly(β-amino ester)s. Mol. Ther. 15 (2007), 1306–1312.
102. [102] Eltoukhy, A.A., Chen, D., Alabi, C.A., Langer, R., Anderson, D.G., Degradable terpolymers with alkyl side chains demonstrate enhanced gene delivery potency and nanoparticle stability. Adv. Mater., 2013, 1–7, 10.1002/adma.201204346.
103. [103] Su, X., Fricke, J., Kavanagh, D., Irvine, D.J., Chase, C., In vitro and in vivo mRNA delivery using lipid-enveloped pH-responsive polymer nanoparticles. Mol. Pharm. 8 (2011), 774–787.
104. [104] Dorbnik, J., Saudek, V., Vlasak, J., Kalal, J., Polyaspartamide—a potential drug carrier. J. Polym. Sci. Polym. Symp. 66 (1979), 65–74.
105. [105] Kim, H.J., et al. PEG-detachable cationic polyaspartamide derivatives bearing stearoyl moieties for systemic siRNA delivery toward subcutaneous BxPC3 pancreatic tumor. J. Drug Target. 20 (2012), 33–42.
106. [106] Miyata, K., et al. Polyplexes from poly(aspartamide) bearing 1,2-diaminoethane side chains induce pH-selective, endosomal membrane destabilization with amplified transfection and negligible cytotoxicity. J. Am. Chem. Soc. 130 (2008), 16287–16294.
107. [107] Zhang, M., Liu, M., Xue, Y., Huang, S., Zhuo, R., Polyaspartamide-based oligo-ethylenimine brushes with high buffer capacity and low cytotoxicity for highly efficient gene delivery. Bioconjug. Chem., 2009, 440–446.
108. [108] Baba, M., Itaka, K., Kondo, K., Yamasoba, T., Kataoka, K., Treatment of neurological disorders by introducing mRNA in vivo using polyplex nanomicelles. J. Control. Release 201 (2015), 41–48.
109. [109] Uchida, H., et al. Modulated protonation of side chain aminoethylene repeats in. J. Am. Chem. Soc. 136 (2014), 12396–12405.
110. [110] Uchida, H., et al. Odd-even effect of repeating aminoethylene units in the side chain of N-substituted polyaspartamides on gene transfection profiles. J. Am. Chem. Soc. 133 (2011), 15524–15532.
111. [111] Li, S.D., Huang, L., Surface-modified LPD nanoparticles for tumor targeting. Ann. N. Y. Acad. Sci. 1082 (2006), 1–8.
112. [112] Li, S.-D., Chen, Y.-C., Hackett, M.J., Huang, L., Tumor-targeted delivery of siRNA by self-assembled nanoparticles. Mol. Ther. 16 (2008), 163–169.
113. [113] Wang, Y., et al. Systemic delivery of modified mRNA encoding herpes simplex virus 1 thymidine kinase for targeted cancer gene therapy. Mol. Ther. 21 (2012), 1–10.
114. [114] Palamà, I.E., Cortese, B., D'Amone, S., Gigli, G., mRNA delivery using non-viral PCL nanoparticles. Biomater. Sci. 3 (2015), 144–151.