Synthesis and characterization of mRNA cap analogs containing phosphorothioate substitutions that bind tightly to eIF4E and are resistant to the decapping pyrophosphatase DcpS

RNA

Volumn 14, Issue 6, 2008, Pages 1119-1131

  Kowalska, Joanna ^a   Lewdorowicz, Magdalena ^a   Zuberek, Joanna ^a   Grudzien Nogalska, Ewa ^b   Bojarska, Elzbieta ^a   Stepinski, Janusz ^a   Rhoads, Robert E ^b   Darzynkiewicz, Edward ^a   Davis, Richard E ^c   Jemielity, Jacek ^a  

^a UNIVERSITY OF WARSAW   (Poland)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

ARCA; Binding affinity for eIF4E; DcpS; Decapping enzymes; Phosphorothioate cap analogs; Resistance to enzymatic hydrolysis

Indexed keywords

7 METHYLGUANOSINE; DINUCLEOTIDE; GUANOSINE DERIVATIVE; INITIATION FACTOR 4E; INORGANIC PYROPHOSPHATASE; MESSENGER RNA; METHYL GROUP; PHOSPHATE; PHOSPHOROTHIOIC ACID; RNA DERIVATIVE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CAENORHABDITIS ELEGANS; CHEMICAL MODIFICATION; CONTROLLED STUDY; DIASTEREOISOMER; FLUORESCENCE; HYDROLYSIS; IN VITRO STUDY; MESSENGER RNA SYNTHESIS; NONHUMAN; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTON NUCLEAR MAGNETIC RESONANCE; RABBIT; RETICULOCYTE LYSATE; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; STRUCTURE ANALYSIS;

ANIMALS; CAENORHABDITIS ELEGANS PROTEINS; ENDORIBONUCLEASES; EUKARYOTIC INITIATION FACTOR-4E; GUANOSINE; HUMANS; HYDROLYSIS; MOLECULAR STRUCTURE; PHOSPHATES; PHOSPHOROTHIOATE OLIGONUCLEOTIDES; PROTEIN BIOSYNTHESIS; PYROPHOSPHATASES; RNA CAP ANALOGS;

CAENORHABDITIS ELEGANS; ORYCTOLAGUS CUNICULUS;

EID: 44149090552     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.990208     Document Type: Article

References (45)

1. Baraniak, J. and Frey, P.A. 1988. Effect of ion pairing on bond order and charge localization in alkyl phosphorothioates. J. Am. Chem. Soc. 110: 4059-4060.
2. Cai, A., Jankowska-Anyszka, M., Centers, A., Chlebicka, L., Stepinski, J., Stolarski, R., Darzynkiewicz, E., and Rhoads, R.E. 1999. Quantitative assessment of mRNA cap analogues as inhibitors of in vitro translation. Biochemistry 38: 8538-8547.
3. 7GpppG to human protein synthesis initiation factor 4E. Biochemistry 28: 8078-8083.
4. 2,2,7GpppG decapping: Activities in Ascaris embryos and characterization of C. elegans scavenger DcpS. RNA 10: 1609-1624.
5. Coller, J. and Parker, R. 2004. Eukaryotic mRNA decapping. Annu. Rev. Biochem. 73: 861-890.
6. Connolly, B.A., Romaniuk, P.J., and Eckstein, F. 1982. Synthesis and characterization of diastereomers of guanosine 5′-O-(1- thiotriphosphate) and guanosine 5′-O-(2-thiotriphosphate). Biochemistry 21: 1983-1989.
7. Contreras, R., Cheroutre, H., Degrave, W., and Fiers, W. 1982. Simple, efficient in vitro synthesis of capped RNA useful for direct expression of cloned eukaryotic genes. Nucleic Acids Res. 10: 6353-6362. doi: 10.1093/nar/10.20.6353.
8. Darzynkiewicz, E., Ekiel, I., Tahara, S.M., Seliger, L.S., and Shatkin, A.J. 1985. Chemical synthesis and characterization of 7-methylguanosine cap analogs. Biochemistry 24: 1701-1707.
9. De Benedetti, A. and Graff, J.R. 2004. eIF-4E expression and its role in malignancies and metastases. Oncogene 23: 3189-3199.
10. Eckstein, F. 1985. Nucleoside phosphorothioates. Annu. Rev. Biochem. 54: 367-402.
11. Eckstein, F. and Goody, R.S. 1976. Synthesis and properties of diastereoisomers of adenosine 5′-(O-1-thiotriphosphate) and adenosine 5′-(O-2-thiotriphosphate). Biochemistry 15: 1685-1691.
12. Frey, P.A. and Sammons, R.D. 1985. Bond order and charge localization in nucleoside phosphorothioates. Science 228: 541-545.
13. Furuichi, Y. and Shatkin, A.J. 2000. Viral and cellular mRNA capping: Past and prospects. Adv. Virus Res. 55: 135-184.
14. Gingras, A.C., Raught, B., and Sonenberg, N. 1999. eIF4 initiation factors: Effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68: 913-963.
15. Grudzien, E., Kalek, M., Jemielity, J., Darzynkiewicz, E., and Rhoads, R.E. 2006. Differential inhibition of mRNA degradation pathways by novel cap analogs. J. Biol. Chem. 281: 1857-1867.
16. Grudzien-Nogalska, E., Jemielity, J., Kowalska, J., Darzynkiewicz, E., and Rhoads, R.E. 2007. Phosphorothioate cap analogs stabilize mRNA and increase translational efficiency in mammalian cells. RNA 13: 1745-1755.
17. Gu, M., Fabrega, C., Liu, S.W., Liu, H., Kiledjian, M., and Lima, C.D. 2004. Insights into the structure, mechanism, and regulation of scavenger mRNA decapping activity. Mol. Cell 14: 67-80.
18. Ho, H.T. and Frey, P.A. 1984. A new method for synthesizing phosphoanhydrides: Synthesis of adenosine 5′-(2-thiodiphosphate) and adenosine 5′-(2-thiotriphosphate). Biochemistry 25: 1978-1983.
19. Jemielity, J., Fowler, T., Zuberek, J., Stepinski, J., Lewdorowicz, M., Niedzwiecka, A., Stolarski, R., Darzynkiewicz, E., and Rhoads, R.E. 2003. Novel "anti-reverse" cap analogs with superior translational properties. RNA 9: 1108-1122.
20. Jones, J.W. and Robins, R.K. 1963. Purine nucleosides. III. Methylation studies of certain naturally occurring purine nucleosides. J. Am. Chem. Soc. 85: 193-201.
21. 2 as a catalyst in DMF under anhydrous conditions. Tetrahedron Lett. 38: 8359-8362.
22. Kalek, M., Jemielity, J., Grudzien, E., Zuberek, J., Bojarska, E., Cohen, L.S., Stepinski, J., Stolarski, R., Davis, R.E., Rhoads, R.E., et al. 2005. Synthesis and biochemical properties of novel mRNA 5′-cap analogs resistant to enzymatic hydrolysis. Nucleosides Nucleotides Nucleic Acids 24: 615-621.
23. Kalek, M., Jemielity, J., Darzynkiewicz, Z.M., Bojarska, E., Stepinski, J., Stolarski, R., Davis, R.E., and Darzynkiewicz, E. 2006. Enzymatically stable 5′ mRNA cap analogs: Synthesis and binding studies with human DcpS decapping enzyme. Bioorg. Med. Chem. 14: 3223-3230.
24. Konarska, M.M., Padgett, R.A., and Sharp, P.A. 1984. Recognition of cap structure in splicing in vitro of mRNA precursors. Cell 38: 731-736.
25. Kowalska, J., Lewdorowicz, M., Darzynkiewicz, E., and Jemielity, J. 2007. A simple and rapid synthesis of nucleotide analogues containing a phosphorothioate moiety at the terminal position of the phosphate chain. Tetrahedron Lett. 48: 5475-5479.
26. Kusmierek, J. and Shugar, D. 1978. A new route to 2′(3′)- O-alkyl purine nucleosides. Nucleic Acids Res. Special Publ. No. 4: s73-s77.
27. Li, P., Xu, Z., Liu, H., Wennefors, C.K., Dobrikov, M.I., Ludwig, J., and Shaw, B.R. 2005. Synthesis of α-P-modified nucleoside diphosphates with ethylenediamine. J. Am. Chem. Soc. 127: 16782-16783.
28. Lima, C.D., Klein, M.G., and Hendrickson, W.A. 1997. Structure-based analysis of catalysis and substrate definition in the HIT protein family. Science 278: 286-290.
29. Liu, H., Rodgers, N.D., Jiao, X., and Kiledjian, M. 2002. The scavenger mRNA decapping enzyme DcpS is a member of the HIT family of pyrophosphatases. EMBO J. 21: 4699-4708.
30. Ludwig, J. and Eckstein, F. 1989. Rapid and efficient synthesis of nucleoside 5′-O-(1-thiotriphosphates), 5′-triphosphates and 2′,3′-cyclophosphorothioates using 2-chloro-4H-1,3,2- benzodioxaphosphorin-4-one. J. Org. Chem. 54: 631-635.
31. McCubbin, W.D., Edery, I., Altmann, M., Sonenberg, N., and Kay, C.M. 1988. Circular dichroism and fluorescence studies on protein synthesis initiation factor eIF-4E and two mutant forms from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 263: 17663-17671.
32. Mitchell, D.A. and Nair, S.K. 2000. RNA-transfected dendritic cells in cancer immunotherapy. J. Clin. Invest. 106: 1065-1069.
33. Mockey, M., Goncalves, C., Dupuy, F.P., Lemoine, F.M., Pichon, C., and Midoux, P. 2006. mRNA transfection of dendritic cells: Synergistic effect of ARCA mRNA capping with Poly(A) chains in cis and in trans for a high protein expression level. Biochem. Biophys. Res. Commun. 340: 1062-1068.
34. P)-ATP-α-S). J. Org. Chem. 49: 704-706.
35. Mukaiyama, T. and Hashimoto, M. 1971. Phosphorylation by oxidation-reduction condensation. Preparation of active phosphorylating reagents. Bull. Chem. Soc. Jpn. 44: 2284.
36. Niedzwiecka, A., Marcotrigiano, J., Stepinski, J., Jankowska-Anyszka, M., Wyslouch-Cieszynska, A., Dadlez, M., Gingras, A.C., Mak, P., Darzynkiewicz, E., Sonenberg, N., et al. 2002. Biophysical studies of eIF4E cap-binding protein: Recognition of mRNA 5≮-cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins. J. Mol. Biol. 319: 615-635.
37. Pasquinelli, A.E., Dahlberg, J.E., and Lund, E. 1995. Reverse 5′ caps in RNAs made in vitro by phage RNA polymerases. RNA 1: 957-967.
38. Peng, Z.H., Sharma, V., Singleton, S.F., and Gershon, P.D. 2002. Synthesis and application of a chain-terminating dinucleotide mRNA cap analog. Org. Lett. 4: 161-164.
39. 18O]phosphorothioate analogs of adenine nucleotides. J. Am. Chem. Soc. 104: 3476-3481.
40. Richter, J.D. and Sonenberg, N. 2005. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433: 477-480.
41. Saenger, W. and Eckstein, F. 1970. Stereochemistry of a substrate for pancreatic ribonuclease. Crystal and molecular structure of the triethylammonium salt of uridine 2′,3′-O,O-cyclophosphorothioate. J. Am. Chem. Soc. 92: 4712-4718.
42. Stepinski, J., Waddell, C., Stolarski, R., Darzynkiewicz, E., and Rhoads, R.E. 2001. 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 7: 1486-1495.
43. van Dijk, E., Cougot, N., Meyer, S., Babajko, S., Wahle, E., and Seraphin, B. 2002. Human Dcp2: A catalytically active mRNA decapping enzyme located in specific cytoplasmic structures. EMBO J. 21: 6915-6924.
44. Wang, Z., Jiao, X., Carr-Schmid, A., and Kiledjian, M. 2002. The hDcp2 protein is a mammalian mRNA decapping enzyme. Proc. Natl. Acad. Sci. 99: 12663-12668.
45. Yisraeli, J.K. and Melton, D.A. 1989. Synthesis of long, capped transcripts in vitro by SP6 and T7 RNA polymerases. Methods Enzymol. 180: 42-50.