Small antisense oligonucleotides against G-quadruplexes: Specific mRNA translational switches

Nucleic Acids Research

Volumn 43, Issue 1, 2015, Pages 595-606

  Rouleau, Samuel G ^a   Beaudoin, Jean Denis ^a   Bisaillon, Martin ^a   Perreault, Jean Pierre ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; GUANINE QUADRUPLEX; MESSENGER RNA;

CACO 2 CELL LINE; HEK293 CELL LINE; HUMAN; METABOLISM; PROTEIN SYNTHESIS; RNA FOLDING;

CACO-2 CELLS; G-QUADRUPLEXES; HEK293 CELLS; HUMANS; OLIGONUCLEOTIDES, ANTISENSE; PROTEIN BIOSYNTHESIS; RNA FOLDING; RNA, MESSENGER;

EID: 84941070712     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1311     Document Type: Article

References (62)

1. Burge,S., Parkinson,G.N., Hazel,P., Todd,A.K. and Neidle,S. (2006) Quadruplex DNA: sequence, topology and structure. Nucleic Acids Res., 34, 5402-5415.
2. Huppert,J.L. (2008) Four-stranded nucleic acids: structure, function and targeting of G-quadruplexes. Chem. Soc. Rev., 37, 1375-1384.
3. Huppert,J.L. and Balasubramanian,S. (2005) Prevalence of quadruplexes in the human genome. Nucleic Acids Res., 33, 2908-2916.
4. Todd,A.K., Johnston,M. and Neidle,S. (2005) Highly prevalent putative quadruplex sequence motifs in human DNA. Nucleic Acids Res., 33, 2901-2907.
5. Bochman,M.L., Paeschke,K. and Zakian,V.A. (2012) DNA secondary structures: stability and function of G-quadruplex structures. Nat. Rev. Genet., 13, 770-780.
6. Biffi,G., Tannahill,D., McCafferty,J. and Balasubramanian,S. (2013) Quantitative visualization of DNA G-quadruplex structures in human cells. Nat. Chem., 5, 182-186.
7. Biffi,G., Di Antonio,M., Tannahill,D. and Balasubramanian,S. (2014) Visualization and selective chemical targeting of RNA G-quadruplex structures in the cytoplasm of human cells. Nat. Chem., 6, 75-80.
8. Millevoi,S., Moine,H. and Vagner,S. (2012) G-quadruplexes in RNA biology. Wiley Interdiscip. Rev. RNA, 3, 495-507.
9. Beaudoin,J.D. and Perreault,J.P. (2010) 5-UTR G-quadruplex structures acting as translational repressors. Nucleic Acids Res., 38, 7022-7036.
10. Bugaut,A. and Balasubramanian,S. (2012) 5-UTR RNA G-quadruplexes: translation regulation and targeting. Nucleic Acids Res., 40, 4727-4741.
11. Marcel,V., Tran,P.L., Sagne,C., Martel-Planche,G., Vaslin,L., Teulade-Fichou,M.P., Hall,J., Mergny,J.L., Hainaut,P. and Van Dyck,E. (2011) G-quadruplex structures in TP53 intron 3: role in alternative splicing and in production of p53 mRNA isoforms. Carcinogenesis, 32, 271-278.
12. Fisette,J., Montagna,D.R.,Mihailescu,M. and Wolfe,M.S. (2012) AG-Rich element forms a g-quadruplex and regulates BACE1 mRNA alternative splicing. J. Neurochem., 121, 763-773.
13. Decorsiere,A., Cayrel,A., Vagner,S. and Millevoi,S. (2011) Essential role for the interaction between hnRNP H/F and a G quadruplex in maintaining p53 pre-mRNA 3-end processing and function during DNA damage. Genes Dev., 25, 220-225.
14. Beaudoin,J.D. and Perreault,J.P. (2013) Exploring mRNA 3-UTR G-quadruplexes: evidence of roles in both alternative polyadenylation and mRNA shortening. Nucleic Acids Res., 11, 5898-5911.
15. Subramanian,M., Rage,F., Tabet,R., Flatter,E., Mandel,J.L. and Moine,H. (2011) G-quadruplex RNA structure as a signal for neurite mRNA targeting. EMBO Rep., 12, 697-704.
16. Collie,G.W. and Parkinson,G.N. (2011) The application of DNA and RNA G-quadruplexes to therapeutic medicines. Chem. Soc. Rev., 40, 5867-5892.
17. Chen,Y. and Yang,D. (2012) Sequence, stability, and structure of G-quadruplexes and their interactions with drugs. Curr. Protoc. Nucleic Acid Chem., 50, 17.5.1-17.5.17.
18. Read,M., Harrison,R.J., Romagnoli,B., Tanious,F.A., Gowan,S.H., Reszka,A.P., Wilson,W.D., Kelland,L.R. and Neidle,S. (2001) Structure-based design of selective and potent G quadruplex-mediated telomerase inhibitors. Proc. Natl. Acad. Sci. U.S.A., 98, 4844-4849.
19. Di Antonio,M., Biffi,G., Mariani,A., Raiber,E.A., Rodriguez,R. and Balasubramanian,S. (2012) Selective RNA versus DNA G-quadruplex targeting by in situ click chemistry. Angew. Chem. Int. Ed. Engl., 51, 11073-11078.
20. Datta,B. and Armitage,B.A. (2001) Hybridization of PNA to structured DNA targets: quadruplex invasion and the overhang effect. J. Am. Chem. Soc., 123, 9612-9619.
21. Green,J.J., Ying,L., Klenerman,D. and Balasubramanian,S. (2003) Kinetics of unfolding the human telomeric DNA quadruplex using a PNA trap. J. Am. Chem. Soc., 125, 3763-3767.
22. Panyutin,I.G., Onyshchenko,M.I., Englund,E.A., Appella,D.H. and Neumann,R.D. (2012) Targeting DNA G-quadruplex structures with peptide nucleic acids. Curr. Pharm. Des., 18, 1984-1991.
23. Lusvarghi,S., Murphy,C.T., Roy,S., Tanious,F.A., Sacui,I., Wilson,W.D., Ly,D.H. and Armitage,B.A. (2009) Loop and backbone modifications of peptide nucleic acid improve g-quadruplex binding selectivity. J. Am. Chem. Soc., 131, 18415-18424.
24. Roy,S., Tanious,F.A., Wilson,W.D., Ly,D.H. and Armitage,B.A. (2007) High-affinity homologous peptide nucleic acid probes for targeting a quadruplex-forming sequence from a MYC promoter element. Biochemistry, 46, 10433-10443.
25. Ito,K., Go,S., Komiyama,M. and Xu,Y. (2011) Inhibition of translation by small RNA-stabilized mRNA structures in human cells. J. Am. Chem. Soc., 133, 19153-19159.
26. Hagihara,M. (2014) Guanine-tethered antisense oligonucleotides as synthetic riboregulators. Methods Mol. Biol., 1111, 197-207.
27. Hagihara,M., Yamauchi,L., Seo,A., Yoneda,K., Senda,M. and Nakatani,K. (2010) Antisense-induced guanine quadruplexes inhibit reverse transcription by HIV-1 reverse transcriptase. J. Am. Chem. Soc., 132, 11171-11178.
28. Murat,P., Zhong,J., Lekieffre,L., Cowieson,N.P., Clancy,J.L., Preiss,T., Balasubramanian,S., Khanna,R. and Tellam,J. (2014) G-quadruplexes regulate epstein-barr virus-encoded nuclear antigen 1 mRNA translation. Nat. Chem. Biol., 5, 358-364.
29. Creppe,C., Janich,P., Cantarino,N., Noguera,M., Valero,V., Musulen,E., Douet,J., Posavec,M., Martin-Caballero,J., Sumoy,L. et al. (2012) MacroH2A1 regulates the balance between self-renewal and differentiation commitment in embryonic and adult stem cells. Mol. Cell. Biol., 32, 1442-1452.
30. Li,X., Kuang,J., Shen,Y., Majer,M.M., Nelson,C.C., Parsawar,K., Heichman,K.A. and Kuwada,S.K. (2012) The atypical histone macroH2A1.2 interacts with HER-2 protein in cancer cells. J. Biol. Chem., 287, 23171-23183.
31. Sporn,J.C. and Jung,B. (2012) Differential regulation and predictive potential of MacroH2A1 isoforms in colon cancer. Am. J. Pathol., 180, 2516-2526.
32. Rappa,F., Greco,A., Podrini,C., Cappello,F., Foti,M., Bourgoin,L., Peyrou,M., Marino,A., Scibetta,N., Williams,R. et al. (2013) Immunopositivity for histone macroH2A1 isoforms marks steatosis-associated hepatocellular carcinoma. PLoS One, 8, e54458.
33. Sporn,J.C., Kustatscher,G., Hothorn,T., Collado,M., Serrano,M., Muley,T., Schnabel,P. and Ladurner,A. (2009) Histone macroH2A isoforms predict the risk of lung cancer recurrence. Oncogene, 28, 3423-3428.
34. Beaudoin,J.D., Jodoin,R. and Perreault,J.P. (2013) In-line probing of RNA G-quadruplexes. Methods, 1, 79-87.
35. Das,R., Laederach,A., Pearlman,S.M., Herschlag,D. and Altman,R.B. (2005) SAFA: semi-automated footprinting analysis software for high-throughput quantification of nucleic acid footprinting experiments. RNA, 11, 344-354.
36. Mergny,J.L. and Lacroix,L. (2009) UV melting of G-quadruplexes. Curr. Protoc. Nucleic Acid Chem., 37, 17.1.1-17.1.15.
37. Brosseau,J.P., Lucier,J.F., Lapointe,E., Durand,M., Gendron,D., Gervais-Bird,J., Tremblay,K., Perreault,J.P. and Elela,S.A. (2010) High-throughput quantification of splicing isoforms. RNA, 16, 442-449.
38. Hellemans,J., Mortier,G., De Paepe,A., Speleman,F. and Vandesompele,J. (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol., 8, R19.
39. Guedin,A., Gros,J., Alberti,P. and Mergny,J.L. (2010) How long is too long? Effects of loop size on G-quadruplex stability. Nucleic Acids Res., 38, 7858-7868.
40. Pandey,S., Agarwala,P. and Maiti,S. (2013) Effect of loops, G-quartets on the stability of RNA G-quadruplexes. J. Phys. Chem. B, 23, 6896-6905.
41. Jodoin,R., Bauer,L., Garant,J.M., Mahdi Laaref,A., Phaneuf,F. and Perreault,J.P. (2014) The folding of 5-UTR human G-quadruplexes possessing a long central loop. RNA, 7, 1129-1141.
42. Stein,D., Foster,E., Huang,S.B., Weller,D. and Summerton,J. (1997) A specificity comparison of four antisense types: morpholino, 2'-O-methyl RNA, DNA, and phosphorothioate DNA. Antisense Nucleic Acid Drug Dev., 7, 151-157.
43. Allerson,C.R., Sioufi,N., Jarres,R., Prakash,T.P., Naik,N., Berdeja,A.,Wanders,L., Griffey,R.H., Swayze,E.E. and Bhat,B. (2005) Fully 2'-modified oligonucleotide duplexes with improved in vitro potency and stability compared to unmodified small interfering RNA. J. Med. Chem., 48, 901-904.
44. Lambert,G., Fattal,E. and Couvreur,P. (2001) Nanoparticulate systems for the delivery of antisense oligonucleotides. Adv. Drug Deliv. Rev., 47, 99-112.
45. Regulski,E.E. and Breaker,R.R. (2008) In-line probing analysis of riboswitches. Methods Mol. Biol., 419, 53-67.
46. Sundquist,W.I. and Klug,A. (1989) Telomeric DNA dimerizes by formation of guanine tetrads between hairpin loops. Nature, 342, 825-829.
47. Andronescu,M., Aguirre-Hernandez,R., Condon,A. and Hoos,H.H. (2003) RNAsoft: A suite of RNA secondary structure prediction and design software tools. Nucleic Acids Res., 31, 3416-3422.
48. Zuker,M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
49. Gaspar-Maia,A., Qadeer,Z.A., Hasson,D., Ratnakumar,K., Leu,N.A., Leroy,G., Liu,S., Costanzi,C., Valle-Garcia,D., Schaniel,C. et al. (2013) MacroH2A histone variants act as a barrier upon reprogramming towards pluripotency. Nat. Commun., 4, 1565.
50. Novikov,L., Park,J.W., Chen,H., Klerman,H., Jalloh,A.S. and Gamble,M.J. (2011) QKI-mediated alternative splicing of the histone variant MacroH2A1 regulates cancer cell proliferation. Mol. Cell. Biol., 31, 4244-4255.
51. Dardenne,E., Pierredon,S., Driouch,K., Gratadou,L., Lacroix-Triki,M., Espinoza,M.P., Zonta,E., Germann,S., Mortada,H., Villemin,J.P. et al. (2012) Splicing switch of an epigenetic regulator by RNA helicases promotes tumor-cell invasiveness. Nat. Struct. Mol. Biol., 19, 1139-1146.
52. Lorenz,R., Bernhart,S.H., Zu Siederdissen,C.H., Tafer,H., Flamm,C., Stadler,P.F. and Hofacker,I.L. (2011) ViennaRNA package 2.0. Algorithms Mol. Biol., 6, 26.
53. Goto,A., Matsushita,K., Gesellchen,V., El Chamy,L., Kuttenkeuler,D., Takeuchi,O., Hoffmann,J.A., Akira,S., Boutros,M. and Reichhart,J.M. (2008) Akirins are highly conserved nuclear proteins required for NF-kappaB-dependent gene expression in drosophila and mice. Nat. Immunol., 9, 97-104.
54. Petersen,M. and Wengel,J. (2003) LNA: a versatile tool for therapeutics and genomics. Trends Biotechnol., 21, 74-81.
55. Cell,B. (1983) Enterocyte-like differentiation and polarization of the human colon carcinoma cell line caco-2 in culture. Biol. Cell, 47, 323-330.
56. Bugaut,A., Murat,P. and Balasubramanian,S. (2012) An RNA hairpin to G-quadruplex conformational transition. J. Am. Chem. Soc., 49, 19953-19956.
57. Zhang,A.Y. and Balasubramanian,S. (2012) The kinetics and folding pathways of intramolecular g-quadruplex nucleic acids. J. Am. Chem. Soc., 134, 19297-19308.
58. Postberg,J., Tsytlonok,M., Sparvoli,D., Rhodes,D. and Lipps,H.J. (2012) A telomerase-associated RecQ protein-like helicase resolves telomeric G-quadruplex structures during replication. Gene, 497, 147-154.
59. Booy,E.P., Meier,M., Okun,N., Novakowski,S.K., Xiong,S., Stetefeld,J. and McKenna,S.A. (2012) The RNA helicase RHAU (DHX36) unwinds a G4-quadruplex in human telomerase RNA and promotes the formation of the P1 helix template boundary. Nucleic Acids Res., 40, 4110-4124.
60. Paeschke,K., Capra,J.A. and Zakian,V.A. (2011) DNA replication through G-quadruplex motifs is promoted by the saccharomyces cerevisiae Pif1 DNA helicase. Cell, 145, 678-691.
61. Irimia,M. and Blencowe,B.J. (2012) Alternative splicing: decoding an expansive regulatory layer. Curr. Opin. Cell Biol., 24, 323-332.
62. Di Giammartino,D.C., Nishida,K. and Manley,J.L. (2011) Mechanisms and consequences of alternative polyadenylation. Mol. Cell, 43, 853-866.