Translation efficiency of mRNAs is increased by antisense oligonucleotides targeting upstream open reading frames

Nature Biotechnology

Volumn 34, Issue 8, 2016, Pages 875-880

  Liang, Xue Hai ^a   Shen, Wen ^a   Sun, Hong ^a   Migawa, Michael T ^a   Vickers, Timothy A ^a   Crooke, Stanley T ^a  

^a ISIS PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE EXPRESSION; GENES; MAMMALS; NUCLEIC ACIDS; OLIGONUCLEOTIDES; RNA;

ANTISENSE OLIGONUCLEOTIDES; ANTISENSE TECHNOLOGY; DOSE-DEPENDENT MANNER; HELICASE ACTIVITIES; MODIFIED NUCLEOTIDES; PROTEIN EXPRESSIONS; THERAPEUTIC AGENTS; THERAPEUTIC PROTEIN;

PROTEINS;

ANTISENSE OLIGONUCLEOTIDE; DHX29 PROTEIN; FIBROBLAST GROWTH FACTOR RECEPTOR 1; INITIATION FACTOR 2ALPHA; INITIATION FACTOR 4E; INITIATION FACTOR 4G; MESSENGER RNA; PROTEIN; RNA HELICASE; RNASE H1 PROTEIN; SPPL2B PROTEIN; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; BASE PAIRING; BINDING SITE; CONSENSUS SEQUENCE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GENETIC TRANSFECTION; HEK293 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RNA SEQUENCE; RNA TRANSLATION; SYSTEMIC THERAPY; TRANSLATION INITIATION; UPREGULATION; WESTERN BLOTTING; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC ENHANCEMENT; GENETICS; PROCEDURES; PROTEIN ENGINEERING; PROTEIN SYNTHESIS;

GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC ENHANCEMENT; OLIGONUCLEOTIDES, ANTISENSE; OPEN READING FRAMES; PROTEIN BIOSYNTHESIS; PROTEIN ENGINEERING;

EID: 84981294965     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.3589     Document Type: Article

References (34)

1. Crooke, S.T., Vickers, T., Lima, W. & Wu, H.-J. Mechanisms of antisense drug action, an introduction. In Antisense Drug Technology - Principles, Strategies, and Application (ed. Crooke, S.T.) 3-46 (CRC Press, 2008).
2. Hua, Y., Vickers, T.A., Baker, B.F., Bennett, C.F. & Krainer, A.R. Enhancement of SMN2 exon 7 inclusion by antisense oligonucleotides targeting the exon. PLoS Biol. 5, e73 (2007).
3. Mourich, D.V. et al. Alternative splice forms of CTLA-4 induced by antisense mediated splice-switching influences autoimmune diabetes susceptibility in NOD mice. Nucleic Acid Ther. 24, 114-126 (2014).
4. Pearson, S., Jia, H. & Kandachi, K. China approves first gene therapy. Nat. Biotechnol. 22, 3-4 (2004).
5. Hoyng, S.A. et al. Gene therapy and peripheral nerve repair: a perspective. Front. Mol. Neurosci. 8, 32 (2015).
6. Leader, B., Baca, Q.J. & Golan, D.E. Protein therapeutics: a summary and pharmacological classification. Nat. Rev. Drug Discov. 7, 21-39 (2008).
7. Meng, L. et al. Towards a therapy for Angelman syndrome by targeting a long non-coding RNA. Nature 518, 409-412 (2015).
8. Kozak, M. Pushing the limits of the scanning mechanism for initiation of translation. Gene 299, 1-34 (2002).
9. Kozak, M. Evaluation of the "scanning model" for initiation of protein synthesis in eucaryotes. Cell 22, 7-8 (1980).
10. Sonenberg, N. & Hinnebusch, A.G. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136, 731-745 (2009).
11. Kozak, M. Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 361, 13-37 (2005).
12. Araujo, P.R. et al. Before it gets started: regulating translation at the 5′ UTR. Comp. Funct. Genomics 2012, 475731 (2012).
13. Pichon, X. et al. RNA binding protein/RNA element interactions and the control of translation. Curr. Protein Pept. Sci. 13, 294-304 (2012).
14. Xue, S. & Barna, M. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat. Rev. Mol. Cell Biol. 13, 355-369 (2012).
15. Wethmar, K., Smink, J.J. & Leutz, A. Upstream open reading frames: molecular switches in (patho)physiology. BioEssays: News and Reviews Mol. Cell. Dev. Biol. 32, 885-893 (2010).
16. Barbosa, C., Peixeiro, I. & Romão, L. Gene expression regulation by upstream open reading frames and human disease. PLoS Genet. 9, e1003529 (2013).
17. Calvo, S.E., Pagliarini, D.J. & Mootha, V.K. Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. Proc. Natl. Acad. Sci. USA 106, 7507-7512 (2009).
18. Lee, S. et al. Global mapping of translation initiation sites in mammalian cells at single-nucleotide resolution. Proc. Natl. Acad. Sci. USA 109, E2424-E2432 (2012).
19. Suzuki, Y. et al. An upstream open reading frame and the context of the two AUG codons affect the abundance of mitochondrial and nuclear RNase H1. Mol. Cell. Biol. 30, 5123-5134 (2010).
20. Liang, X.H., Sun, H., Shen, W. & Crooke, S.T. Identification and characterization of intracellular proteins that bind oligonucleotides with phosphorothioate linkages. Nucleic Acids Res. 43, 2927-2945 (2015).
21. Deng, Y. et al. Therapeutic potentials of gene silencing by RNA interference: principles, challenges, and new strategies. Gene 538, 217-227 (2014).
22. Freier, S.M. & Altmann, K.H. The ups and downs of nucleic acid duplex stability: structure-stability studies on chemically-modified DNA:RNA duplexes. Nucleic Acids Res. 25, 4429-4443 (1997).
23. Seth, P.P. et al. Synthesis and biophysical evaluation of 2′,4′-constrained 2′O-methoxyethyl and 2′,4′-constrained 2′O-ethyl nucleic acid analogues. J. Org. Chem. 75, 1569-1581 (2010).
24. Ling, J., Morley, S.J. & Traugh, J.A. Inhibition of cap-dependent translation via phosphorylation of eIF4G by protein kinase Pak2. EMBO J. 24, 4094-4105 (2005).
25. Chiang, M.Y. et al. Antisense oligonucleotides inhibit intercellular adhesion molecule 1 expression by two distinct mechanisms. J. Biol. Chem. 266, 18162-18171 (1991).
26. Pisareva, V.P., Pisarev, A.V., Komar, A.A., Hellen, C.U. & Pestova, T.V. Translation initiation on mammalian mRNAs with structured 5′UTRs requires DExH-box protein DHX29. Cell 135, 1237-1250 (2008).
27. Koller, E. et al. Mechanisms of single-stranded phosphorothioate modified antisense oligonucleotide accumulation in hepatocytes. Nucleic Acids Res. 39, 4795-4807 (2011).
28. Wethmar, K. The regulatory potential of upstream open reading frames in eukaryotic gene expression. Wiley Interdiscip. Rev. RNA 5, 765-768 (2014).
29. Postina, R. et al. A disintegrin-metalloproteinase prevents amyloid plaque formation and hippocampal defects in an Alzheimer disease mouse model. J. Clin. Invest. 113, 1456-1464 (2004).
30. Liang, X.H., Liu, Q. & Fournier, M.J. rRNA modifications in an intersubunit bridge of the ribosome strongly affect both ribosome biogenesis and activity. Mol. Cell 28, 965-977 (2007).
31. Liang, X.H., Hart, C.E. & Crooke, S.T. Transfection of siRNAs can alter miRNA levels and trigger non-specific protein degradation in mammalian cells. Biochim. Biophys. Acta 1829, 455-468 (2013).
32. Bleriot, Y. et al. Synthesis and acid catalyzed hydrolysis of B2,5 type conformationally constrained glucopyranosides: incorporation into a cellobiose analog. Tetrahedron 60, 6813-6828 (2004).
33. Liang, X.H., Liu, Q. & Michaeli, S. Small nucleolar RNA interference induced by antisense or double-stranded RNA in trypanosomatids. Proc. Natl. Acad. Sci. USA 100, 7521-7526 (2003).
34. Liang, X.H., Vickers, T.A., Guo, S. & Crooke, S.T. Efficient and specific knockdown of small non-coding RNAs in mammalian cells and in mice. Nucleic Acids Res. 39, e13 (2011).