RNA: The new revolution in nucleic acid vaccines

Seminars in Immunology

Volumn 25, Issue 2, 2013, Pages 152-159

  Geall, Andrew J ^a   Mandl, Christian W ^a   Ulmer, Jeffrey B ^a  

^a NOVARTIS VACCINES AND DIAGNOSTICS   (United States)

Author keywords

Human; Manufacturing; Replicon; Safety; Stability

Indexed keywords

ANTIGEN; CANCER VACCINE; DNA VACCINE; INACTIVATED VIRUS VACCINE; INFLUENZA VACCINE; MESSENGER RNA; NUCLEIC ACID; PLASMID DNA; RECOMBINANT PROTEIN; RNA VACCINE; VIRUS RNA; VIRUS VECTOR;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ACTIVE TRANSPORT; ADAPTIVE IMMUNITY; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; CELLULAR IMMUNITY; CLINICAL EFFECTIVENESS; DNA TEMPLATE; DRUG SAFETY; ENZYMATIC DEGRADATION; GENE THERAPY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGENICITY; INNATE IMMUNITY; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PATHOGENESIS; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REPLICON; REPORTER GENE; REVIEW; RNA REPLICATION; RNA TRANSLATION; RNA VIRUS; SEMLIKI FOREST ALPHAVIRUS; SINDBIS VIRUS; VACCINATION; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VIRUS ATTENUATION; VIRUS LIKE AGENT; VIRUS PARTICLE; VIRUS REPLICATION;

HUMAN; MANUFACTURING; REPLICON; SAFETY; STABILITY;

ANIMALS; CLINICAL TRIALS AS TOPIC; GENETIC ENGINEERING; HUMANS; PLASMIDS; RNA, VIRAL; VACCINES, DNA;

EID: 84882259948     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2013.05.001     Document Type: Review

References (118)

1. Liu M.A. Immunologic basis of vaccine vectors. Immunity 2010, 33:504-515.
2. Ferraro B., Morrow M.P., Hutnick N.A., Shin T.H., Lucke C.E., Weiner D.B. Clinical applications of DNA vaccines: current progress. Clinical Infectious Disease 2011, 53:296-302.
3. Liu M.A. DNA vaccines: an historical perspective and view to the future. Immunological Reviews 2011, 239:62-84.
4. Ulmer J.B., Mason P.W., Geall A., Mandl C.W. RNA-based vaccines. Vaccine 2012, 30:4414-4418.
5. Wolff J.A., Malone R.W., Williams P., Chong W., Acsadi G., Jani A., et al. Direct gene transfer into mouse muscle in vivo. Science 1990, 247:1465-1468.
6. Kutzler M.A., Weiner D.B. DNA vaccines: ready for prime time?. Nature Reviews Genetics 2008, 9:776-788.
7. Sardesai N.Y., Weiner D.B. Electroporation delivery of DNA vaccines: prospects for success. Current Opinion in Immunology 2011, 23:421-429.
8. Jensen S., Thomsen A.R. Sensing of RNA viruses: a review of innate immune receptors involved in recognizing RNA virus invasion. Journal of Virology 2012, 86:2900-2910.
9. Martinez-Gil L., Goff P.H., Hai R., Garcia-Sastre A., Shaw M.L., Palese P. A Sendai virus-derived RNA agonist of RIG-I as a virus vaccine adjuvant. Journal of Virology 2013, 87:1290-1300.
10. Jin B., Sun T., Yu X.H., Liu C.Q., Yang Y.X., Lu P., et al. Immunomodulatory effects of dsRNA and its potential as vaccine adjuvant. Journal of Biomedicine and Biotechnology 2010, 2010:690438.
11. Caskey M., Lefebvre F., Filali-Mouhim A., Cameron M.J., Goulet J.P., Haddad E.K., et al. Synthetic double-stranded RNA induces innate immune responses similar to a live viral vaccine in humans. Journal of Experimental Medicine 2011, 208:2357-2366.
12. Leavy O. Vaccines: dual TLR hit for vaccine success. Nature Reviews Immunology 2011, 11:234-235.
13. Gaucher D., Therrien R., Kettaf N., Angermann B.R., Boucher G., Filali-Mouhim A., et al. Yellow fever vaccine induces integrated multilineage and polyfunctional immune responses. Journal of Experimental Medicine 2008, 205:3119-3131.
14. Querec T., Bennouna S., Alkan S., Laouar Y., Gorden K., Flavell R., et al. Yellow fever vaccine YF-17D activates multiple dendritic cell subsets via TLR2, 7, 8, and 9 to stimulate polyvalent immunity. Journal of Experimental Medicine 2006, 203:413-424.
15. Garcon N., Chomez P., Van Mechelen M. GlaxoSmithKline adjuvant systems in vaccines: concepts, achievements and perspectives. Expert Review of Vaccines 2007, 6:723-739.
16. Mutwiri G., Gerdts V., van Drunen Littel-van den Hurk S., Auray G., Eng N., Garlapati S., et al. Combination adjuvants: the next generation of adjuvants?. Expert Review of Vaccines 2011, 10:95-107.
17. O'Hagan D.T., De Gregorio E. The path to a successful vaccine adjuvant - 'the long and winding road'. Drug Discovery Today 2009, 14:541-551.
18. Pashine A., Valiante N.M., Ulmer J.B. Targeting the innate immune response with improved vaccine adjuvants. Nature Medicine 2005, 11:S63-S68.
19. Reed S.G., Bertholet S., Coler R.N., Friede M. New horizons in adjuvants for vaccine development. Trends in Immunology 2009, 30:23-32.
20. Schlake T., Thess A., Fotin-Mleczek M., Kallen K.J. Developing mRNA-vaccine technologies. RNA Biology 2012, 9:1319-1330.
21. Ross J. mRNA stability in mammalian cells. Microbiological Reviews 1995, 59:423-450.
22. Atkins G.J., Fleeton M.N., Sheahan B.J. Therapeutic and prophylactic applications of alphavirus vectors. Expert Reviews in Molecular Medicine 2008, 10:e33.
23. Lundstrom K. Alphavirus vectors: applications for DNA vaccine production and gene expression. Intervirology 2000, 43:247-257.
24. Schlesinger S. Alphavirus vectors: development and potential therapeutic applications. Expert Opinion on Biological Therapy 2001, 1:177-191.
25. Smerdou C., Liljestrom P. Non-viral amplification systems for gene transfer: vectors based on alphaviruses. Current Opinion in Molecular Therapeutics 1999, 1:244-251.
26. Perri S., Greer C.E., Thudium K., Doe B., Legg H., Liu H., et al. An alphavirus replicon particle chimera derived from Venezuelan equine encephalitis and Sindbis viruses is a potent gene-based vaccine delivery vector. Journal of Virology 2003, 77:10394-10403.
27. Rayner J.O., Dryga S.A., Kamrud K.I. Alphavirus vectors and vaccination. Reviews in Medical Virology 2002, 12:279-296.
28. Fleeton M.N., Chen M., Berglund P., Rhodes G., Parker S.E., Murphy M., et al. Self-replicative RNA vaccines elicit protection against influenza A virus, respiratory syncytial virus, and a tickborne encephalitis virus. Journal of Infectious Diseases 2001, 183:1395-1398.
29. Bernstein D.I., Reap E.A., Katen K., Watson A., Smith K., Norberg P., et al. Randomized, double-blind, Phase 1 trial of an alphavirus replicon vaccine for cytomegalovirus in CMV seronegative adult volunteers. Vaccine 2009, 28:484-493.
30. Geall A.J., Verma A., Otten G.R., Shaw C.A., Hekele A., Banerjee K., et al. Nonviral delivery of self-amplifying RNA vaccines. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:14604-14609.
31. Pichlmair A., Kandasamy K., Alvisi G., Mulhern O., Sacco R., Habjan M., et al. Viral immune modulators perturb the human molecular network by common and unique strategies. Nature 2012, 487:486-490.
32. Martinon F., Krishnan S., Lenzen G., Magne R., Gomard E., Guillet J.G., et al. Induction of virus-specific cytotoxic T lymphocytes in vivo by liposome-entrapped mRNA. European Journal of Immunology 1993, 23:1719-1722.
33. Petsch B., Schnee M., Vogel A.B., Lange E., Hoffmann B., Voss D., et al. Protective efficacy of in vitro synthesized, specific mRNA vaccines against influenza A virus infection. Nature Biotechnology 2012, 30:1210-1216.
34. Pijlman G.P., Suhrbier A., Khromykh A.A. Kunjin virus replicons: an RNA-based, non-cytopathic viral vector system for protein production, vaccine and gene therapy applications. Expert Opinion on Biological Therapy 2006, 6:135-145.
35. Saxena S., Dahiya S.S., Sonwane A.A., Patel C.L., Saini M., Rai A., et al. A Sindbis virus replicon-based DNA vaccine encoding the rabies virus glycoprotein elicits immune responses and complete protection in mice from lethal challenge. Vaccine 2008, 26:6592-6601.
36. Saxena S., Sonwane A.A., Dahiya S.S., Patel C.L., Saini M., Rai A., et al. Induction of immune responses and protection in mice against rabies using a self-replicating RNA vaccine encoding rabies virus glycoprotein. Veterinary Microbiology 2009, 136:36-44.
37. Zhou X., Berglund P., Rhodes G., Parker S.E., Jondal M., Liljestrom P. Self-replicating Semliki Forest virus RNA as recombinant vaccine. Vaccine 1994, 12:1510-1514.
38. Dalemans W., Delers A., Delmelle C., Denamur F., Meykens R., Thiriart C., et al. Protection against homologous influenza challenge by genetic immunization with SFV-RNA encoding Flu-HA. Annals of the New York Academy of Sciences 1995, 772:255-256.
39. Conry R.M., LoBuglio A.F., Wright M., Sumerel L., Pike M.J., Johanning F., et al. Characterization of a messenger RNA polynucleotide vaccine vector. Cancer Research 1995, 55:1397-1400.
40. Granstein R.D., Ding W., Ozawa H. Induction of anti-tumor immunity with epidermal cells pulsed with tumor-derived RNA or intradermal administration of RNA. Journal of Investigative Dermatology 2000, 114:632-636.
41. Kreiter S., Selmi A., Diken M., Koslowski M., Britten C.M., Huber C., et al. Intranodal vaccination with naked antigen-encoding RNA elicits potent prophylactic and therapeutic antitumoral immunity. Cancer Research 2010, 70:9031-9040.
42. Ying H., Zaks T.Z., Wang R.F., Irvine K.R., Kammula U.S., Marincola F.M., et al. Cancer therapy using a self-replicating RNA vaccine. Nature Medicine 1999, 5:823-827.
43. Zhou W.Z., Hoon D.S., Huang S.K., Fujii S., Hashimoto K., Morishita R., et al. RNA melanoma vaccine: induction of antitumor immunity by human glycoprotein 100 mRNA immunization. Human Gene Therapy 1999, 10:2719-2724.
44. Roesler E., Weiss R., Weinberger E.E., Fruehwirth A., Stoecklinger A., Mostbock S., et al. Immunize and disappear-safety-optimized mRNA vaccination with a panel of 29 allergens. Journal of Allergy and Clinical Immunology 2009, 124:1070-1077. e1-11.
45. Weiss R., Scheiblhofer S., Roesler E., Ferreira F., Thalhamer J. Prophylactic mRNA vaccination against allergy. Current Opinion in Allergy and Clinical Immunology 2010, 10:567-574.
46. Aberle J.H., Aberle S.W., Kofler R.M., Mandl C.W. Humoral and cellular immune response to RNA immunization with flavivirus replicons derived from tick-borne encephalitis virus. Journal of Virology 2005, 79:15107-15113.
47. Hoerr I., Obst R., Rammensee H.G., Jung G. In vivo application of RNA leads to induction of specific cytotoxic T lymphocytes and antibodies. European Journal of Immunology 2000, 30:1-7.
48. Johanning F.W., Conry R.M., LoBuglio A.F., Wright M., Sumerel L.A., Pike M.J., et al. A Sindbis virus mRNA polynucleotide vector achieves prolonged and high level heterologous gene expression in vivo. Nucleic Acids Research 1995, 23:1495-1501.
49. Johansson D.X., Ljungberg K., Kakoulidou M., Liljestrom P. Intradermal electroporation of naked replicon RNA elicits strong immune responses. PLoS One 2012, 7:e29732.
50. 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. Molecular Medicine Reports 2009, 2:753-756.
51. Carralot J.P., Probst J., Hoerr I., Scheel B., Teufel R., Jung G., et al. Polarization of immunity induced by direct injection of naked sequence-stabilized mRNA vaccines. Cellular and Molecular Life Sciences 2004, 61:2418-2424.
52. Kreiter S., Diken M., Selmi A., Tureci O., Sahin U. Tumor vaccination using messenger RNA: prospects of a future therapy. Current Opinion in Immunology 2011, 23:399-406.
53. Weide B., Carralot J.P., Reese A., Scheel B., Eigentler T.K., Hoerr I., et al. Results of the first phase I/II clinical vaccination trial with direct injection of mRNA. Journal of Immunotherapy 2008, 31:180-188.
54. Weide B., Pascolo S., Scheel B., Derhovanessian E., Pflugfelder A., Eigentler T.K., et al. Direct injection of protamine-protected mRNA: results of a phase 1/2 vaccination trial in metastatic melanoma patients. Journal of Immunotherapy 2009, 32:498-507.
55. Rittig S.M., Haentschel M., Weimer K.J., Heine A., Muller M.R., Brugger W., et al. Intradermal vaccinations with RNA coding for TAA generate CD8+ and CD4+ immune responses and induce clinical benefit in vaccinated patients. Molecular Therapy 2011, 19:990-999.
56. Fotin-Mleczek M., Zanzinger K., Heidenreich R., Lorenz C., Thess A., Duchardt K.M., et al. Highly potent mRNA based cancer vaccines represent an attractive platform for combination therapies supporting an improved therapeutic effect. Journal of Gene Medicine 2012, 14:428-439.
57. Jafari M., Soltani M., Naahidi S., Karunaratne D.N., Chen P. Nonviral approach for targeted nucleic acid delivery. Current Medicinal Chemistry 2012, 19:197-208.
58. Lorenz C., Fotin-Mleczek M., Roth G., Becker C., Dam T.C., Verdurmen W.P., et al. Protein expression from exogenous mRNA: uptake by receptor-mediated endocytosis and trafficking via the lysosomal pathway. RNA Biology 2011, 8:627-636.
59. Probst J., Weide B., Scheel B., Pichler B.J., Hoerr I., Rammensee H.G., et al. Spontaneous cellular uptake of exogenous messenger RNA in vivo is nucleic acid-specific, saturable and ion dependent. Gene Therapy 2007, 14:1175-1180.
60. Probst J., Brechtel S., Scheel B., Hoerr I., Jung G., Rammensee H.G., et al. Characterization of the ribonuclease activity on the skin surface. Genetic Vaccines and Therapy 2006, 4:4.
61. Pollard C., Rejman J., De Haes W., Verrier B., Van Gulck E., Naessens T., et al. Type I IFN counteracts the induction of antigen-specific immune responses by lipid-based delivery of mRNA vaccines. Molecular Therapy 2013, 21:251-259.
62. Mandl C.W., Aberle J.H., Aberle S.W., Holzmann H., Allison S.L., Heinz F.X. In vitro-synthesized infectious RNA as an attenuated live vaccine in a flavivirus model. Nature Medicine 1998, 4:1438-1440.
63. Kofler R.M., Aberle J.H., Aberle S.W., Allison S.L., Heinz F.X., Mandl C.W. Mimicking live flavivirus immunization with a noninfectious RNA vaccine. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:1951-1956.
64. Sun S., Li W., Sun Y., Pan Y., Li J. A new RNA vaccine platform based on MS2 virus-like particles produced in Saccharomyces cerevisiae. Biochemical and Biophysical Research Communications 2011, 407:124-128.
65. Heyes J., Palmer L., Bremner K., MacLachlan I. Cationic lipid saturation influences intracellular delivery of encapsulated nucleic acids. Journal of Controlled Release 2005, 107:276-287.
66. Fotin-Mleczek M., Duchardt K.M., Lorenz C., Pfeiffer R., Ojkic-Zrna S., Probst J., et al. Messenger RNA-based vaccines with dual activity induce balanced TLR-7 dependent adaptive immune responses and provide antitumor activity. Journal of Immunotherapy 2011, 34:1-15.
67. Scheel B., Teufel R., Probst J., Carralot J.P., Geginat J., Radsak M., et al. Toll-like receptor-dependent activation of several human blood cell types by protamine-condensed mRNA. European Journal of Immunology 2005, 35:1557-1566.
68. Krieg P.A., Melton D.A. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Research 1984, 12:7057-7070.
69. Melton D.A., Krieg P.A., Rebagliati M.R., Maniatis T., Zinn K., Green M.R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Research 1984, 12:7035-7056.
70. Milligan J.F., Groebe D.R., Witherell G.W., Uhlenbeck O.C. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Research 1987, 15:8783-8798.
71. Guo P., Haque F., Hallahan B., Reif R., Li H. Uniqueness, advantages, challenges, solutions, and perspectives in therapeutics applying RNA nanotechnology. Nucleic Acid Therapeutics 2012, 22:226-245.
72. Marshall W.S., Kaiser R.J. Recent advances in the high-speed solid phase synthesis of RNA. Current Opinion in Chemical Biology 2004, 8:222-229.
73. Davis R.H. Large-scale oligoribonucleotide production. Current Opinion in Biotechnology 1995, 6:213-217.
74. Pascolo S. Messenger RNA-based vaccines. Expert Opinion on Biological Therapy 2004, 4:1285-1294.
75. Pascolo S. Vaccination with messenger RNA (mRNA). Handbook of experimental pharmacology 2008, 221-235. Springer Berlin Heidelberg, Gemany.
76. Higman M.A., Bourgeois N., Niles E.G. The vaccinia virus mRNA (guanine-N7-)-methyltransferase requires both subunits of the mRNA capping enzyme for activity. Journal of Biological Chemistry 1992, 267:16430-16437.
77. Grudzien-Nogalska E., Stepinski J., Jemielity J., Zuberek J., Stolarski R., Rhoads R.E., et al. Synthesis of anti-reverse cap analogs (ARCAs) and their applications in mRNA translation and stability. Methods in Enzymology 2007, 431:203-227.
78. Peng Z.H., Sharma V., Singleton S.F., Gershon P.D. Synthesis and application of a chain-terminating dinucleotide mRNA cap analog. Organic Letters 2002, 4:161-164.
79. Grudzien E., Stepinski J., Jankowska-Anyszka M., Stolarski R., Darzynkiewicz E., Rhoads R.E. Novel cap analogs for in vitro synthesis of mRNAs with high translational efficiency. RNA 2004, 10:1479-1487.
80. Grudzien-Nogalska E., Jemielity J., Kowalska J., Darzynkiewicz E., Rhoads R.E. Phosphorothioate cap analogs stabilize mRNA and increase translational efficiency in mammalian cells. RNA 2007, 13:1745-1755.
81. Jemielity J., Fowler T., Zuberek J., Stepinski J., Lewdorowicz M., Niedzwiecka A., et al. Novel "anti-reverse" cap analogs with superior translational properties. RNA 2003, 9:1108-1122.
82. Jemielity J., Stepinski J., Jaremko M., Haber D., Stolarski R., Rhoads R.E., et al. Synthesis of novel mRNA 5' cap-analogues: dinucleoside P1, P3-tri-, P1, P4-tetra-, and P1, P5-pentaphosphates. Nucleosides, Nucleotides and Nucleic Acids 2003, 22:691-694.
83. Kowalska J., Lewdorowicz M., Zuberek J., Grudzien-Nogalska E., Bojarska E., Stepinski J., et al. Synthesis and characterization of mRNA cap analogs containing phosphorothioate substitutions that bind tightly to eIF4E and are resistant to the decapping pyrophosphatase DcpS. RNA 2008, 14:1119-1131.
84. Kowalska J., Zuberek J., Darzynkiewicz Z.M., Lukaszewicz M., Darzynkiewicz E., Jemielity J. The first examples of mRNA cap analogs bearing boranophosphate modification. Nucleic Acids Symposium Series (Oxford) 2008, 289-290.
85. Stepinski J., Waddell C., Stolarski R., Darzynkiewicz E., Rhoads R.E. Synthesis and properties of mRNAs containing the novel "anti-reverse" cap analogs 7-methyl(3'-O-methyl)GpppG and 7-methyl (3'-deoxy)GpppG. RNA 2001, 7:1486-1495.
86. Guo P.X., Moss B. Interaction and mutual stabilization of the two subunits of vaccinia virus mRNA capping enzyme coexpressed in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 1990, 87:4023-4027.
87. Mao X., Shuman S. Intrinsic RNA (guanine-7) methyltransferase activity of the vaccinia virus capping enzyme D1 subunit is stimulated by the D12 subunit. Identification of amino acid residues in the D1 protein required for subunit association and methyl group transfer. Journal of Biological Chemistry 1994, 269:24472-24479.
88. Lukavsky P.J., Puglisi J.D. Large-scale preparation and purification of polyacrylamide-free RNA oligonucleotides. RNA 2004, 10:889-893.
89. Puglisi J.D., Wyatt J.R. Biochemical and NMR studies of RNA conformation with an emphasis on RNA pseudoknots. Methods in Enzymology 1995, 261:323-350.
90. Wyatt J.R., Chastain M., Puglisi J.D. Synthesis and purification of large amounts of RNA oligonucleotides. Biotechniques 1991, 11:764-769.
91. Breckenridge N.C., Davis R.H. Optimization of repeated-batch transcription for RNA production. Biotechnology and Bioengineering 2000, 69:679-687.
92. Kariko K., Muramatsu H., Ludwig J., Weissman D. Generating the optimal mRNA for therapy: HPLC purification eliminates immune activation and improves translation of nucleoside-modified, protein-encoding mRNA. Nucleic Acids Research 2011, 39:e142.
93. Evans R.K., Xu Z., Bohannon K.E., Wang B., Bruner M.W., Volkin D.B. Evaluation of degradation pathways for plasmid DNA in pharmaceutical formulations via accelerated stability studies. Journal of Pharmaceutical Sciences 2000, 89:76-87.
94. Jones K.L., Drane D., Gowans E.J. Long-term storage of DNA-free RNA for use in vaccine studies. Biotechniques 2007, 43:675-681.
95. Houseley J., Tollervey D. The many pathways of RNA degradation. Cell 2009, 136:763-776.
96. Al-Saif M., Khabar K.S. UU/UA dinucleotide frequency reduction in coding regions results in increased mRNA stability and protein expression. Molecular Therapy 2012, 20:954-959.
97. Anderson B.R., Muramatsu H., Nallagatla S.R., Bevilacqua P.C., Sansing L.H., Weissman D., et al. Incorporation of pseudouridine into mRNA enhances translation by diminishing PKR activation. Nucleic Acids Research 2010, 38:5884-5892.
98. Kariko 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 2005, 23:165-175.
99. Kariko K., Muramatsu H., Welsh F.A., Ludwig J., Kato H., Akira S., et al. Incorporation of pseudouridine into mRNA yields superior nonimmunogenic vector with increased translational capacity and biological stability. Molecular Therapy 2008, 16:1833-1840.
100. Kariko K., Weissman D. Naturally occurring nucleoside modifications suppress the immunostimulatory activity of RNA: implication for therapeutic RNA development. Current Opinion in Drug Discovery and Development 2007, 10:523-532.
101. Kormann M.S., Hasenpusch G., Aneja M.K., Nica G., Flemmer A.W., Herber-Jonat S., et al. Expression of therapeutic proteins after delivery of chemically modified mRNA in mice. Nature Biotechnology 2011, 29:154-157.
102. Nallagatla S.R., Bevilacqua P.C. Nucleoside modifications modulate activation of the protein kinase PKR in an RNA structure-specific manner. RNA 2008, 14:1201-1213.
103. Nallagatla S.R., Toroney R., Bevilacqua P.C. A brilliant disguise for self RNA: 5'-end and internal modifications of primary transcripts suppress elements of innate immunity. RNA Biology 2008, 5:140-144.
104. Nagy P.D. The roles of host factors in tombusvirus RNA recombination. Advances in Virus Research 2011, 81:63-84.
105. Nagy P.D., Pogany J. The dependence of viral RNA replication on co-opted host factors. Nature Reviews Microbiology 2012, 10:137-149.
106. Dickson A.M., Anderson J.R., Barnhart M.D., Sokoloski K.J., Oko L., Opyrchal M., et al. Dephosphorylation of HuR protein during alphavirus infection is associated with HuR relocalization to the cytoplasm. Journal of Biological Chemistry 2012, 287:36229-36238.
107. Gaglia M.M., Glaunsinger B.A. Viruses and the cellular RNA decay machinery. Wiley Interdisciplinary Reviews: RNA 2010, 1:47-59.
108. Moon S.L., Barnhart M.D., Wilusz J. Inhibition and avoidance of mRNA degradation by RNA viruses. Current Opinion in Microbiology 2012, 15:500-505.
109. Meyer S., Temme C., Wahle E. Messenger RNA turnover in eukaryotes: pathways and enzymes. Critical Reviews in Biochemistry and Molecular Biology 2004, 39:197-216.
110. Brennan C.M., Steitz J.A. HuR and mRNA stability. Cellular and Molecular Life Sciences 2001, 58:266-277.
111. Tavernier G., Andries O., Demeester J., Sanders N.N., De Smedt S.C., Rejman J. mRNA as gene therapeutic: how to control protein expression. Journal of Controlled Release 2011, 150:238-247.
112. Yamamoto A., Kormann M., Rosenecker J., Rudolph C. Current prospects for mRNA gene delivery. European Journal of Pharmaceutics and Biopharmaceutics 2009, 71:484-489.
113. Graham R.L., Becker M.M., Eckerle L.D., Bolles M., Denison M.R., Baric R.S. A live, impaired-fidelity coronavirus vaccine protects in an aged, immunocompromised mouse model of lethal disease. Nature Medicine 2012, 18:1820-1826.
114. 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 Research 2001, 29:3882-3891.
115. Huth S., Hoffmann F., von Gersdorff K., Laner A., Reinhardt D., Rosenecker J., et al. Interaction of polyamine gene vectors with RNA leads to the dissociation of plasmid DNA-carrier complexes. Journal of Gene Medicine 2006, 8:1416-1424.
116. Wang Y., Su H.H., Yang Y., Hu Y., Zhang L., Blancafort P., et al. Systemic delivery of modified mRNA encoding herpes simplex virus 1 thymidine kinase for targeted cancer gene therapy. Molecular Therapy 2013, 21:358-367.
117. Fahmy T.M., Demento S.L., Caplan M.J., Mellman I., Saltzman W.M. Design opportunities for actively targeted nanoparticle vaccines. Nanomedicine (London) 2008, 3:343-355.
118. Boudreau J.E., Bonehill A., Thielemans K., Wan Y. Engineering dendritic cells to enhance cancer immunotherapy. Molecular Therapy 2011, 19:841-853.