Thermodynamics of ligand binding by the yeast mRNA-capping enzyme reveals different modes of binding

Biochemical Journal

Volumn 384, Issue 2, 2004, Pages 411-420

  Bougie, Isabelle ^a   Parent, Amélie ^a   Bisaillon, Martin ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Enzymology; Fluorescence spectroscopy; mRNA capping; Thermodynamics; Yeast

Indexed keywords

BINDING ENERGY; ENZYME KINETICS; FLUORESCENCE; HYDROLYSIS; SPECTROSCOPIC ANALYSIS; THERMODYNAMICS; YEAST;

ENERGETICS; FLUORESCENCE SPECTROSCOPY; LIGANDS; RNA-CAPPING ENZYMES;

RNA;

FUNGAL ENZYME; FUNGAL RNA; GUANOSINE TRIPHOSPHATE; MANGANESE; MESSENGER RNA; PROTEIN CEG1; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENTHALPY; ENTROPY; ENZYME BINDING; ENZYME KINETICS; ENZYME SUBSTRATE; FLUORESCENCE SPECTROSCOPY; HYDROLYSIS KINETICS; LIGAND BINDING; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; RNA BINDING; RNA CAPPING; SACCHAROMYCES CEREVISIAE; THERMODYNAMICS; YEAST;

CATIONS; CIRCULAR DICHROISM; FLUORESCENCE; GUANOSINE TRIPHOSPHATE; LIGANDS; METALS; NUCLEOTIDYLTRANSFERASES; PROTEIN BINDING; PROTEIN FOLDING; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EUKARYOTA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 10644255610     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20041112     Document Type: Article

References (28)

1. Furuichi, Y. and Shatkin, S. (2000) Viral and cellular mRNA-capping: past and prospects. Adv. Virol. Res. 55, 135-184
2. Shuman, S. (2000) Structure, mechanism, and evolution of the mRNA-capping apparatus. Prog. Nucleic Acids Res. Mol. Biol. 66, 1-40
3. Shibagaki, Y., Itoh, N., Yamada, H., Nagata, S. and Mizumoto, K. (1992) mRNA-capping enzyme. Isolation and characterization of the gene encoding mRNA guanylyltransferase subunit from Saccharomyces cerevisiae. J. Biol. Chem. 267, 9521-9528
4. Schwer, B. and Shuman, S. (1994) Mutational analysis of yeast mRNA-capping enzyme. Proc. Natl. Acad. Sci. U.S.A. 91, 4328-4332
5. Mao, X., Schwer, B. and Shuman, S. (1996) Mutational analysis of the Saccharomyces cerevisiae ABD1 gene: cap methyltransferase activity is essential for cell growth. Mol. Cell. Biol. 16, 475-480
6. Wang, S. P. and Shuman, S. (1997) Structure-function analysis of the mRNA cap methyltransferase of Saccharomyces cerevisiae. J. Biol. Chem. 272, 14683-14689
7. Tsukamoto, T., Shibagaki, Y., Imajoh-Ohmi, S., Murakoshi, T., Suzuki, M., Nakamura, A., Gotoh, H. and Mizumoto, K. (1997) Isolation and characterization of the yeast mRNA-capping enzyme beta subunit gene encoding RNA 5′-triphosphatase, which is essential for cell viability. Biochem. Biophys. Res. Commun. 239, 116-122
8. Ho, C. K., Pei, Y. and Shuman, S. (1998) Yeast and viral RNA 5′ triphosphatases comprise a new nucleoside triphosphatase family. J. Biol. Chem. 273, 34151-34156
9. Cong, P. and Shuman, S. (1993) Covalent catalysis in nucleotidyl transfer. A KTDG motif essential for enzyme-GMP complex formation by mRNA-capping enzyme is conserved at the active sites of RNA and DNA ligases. J. Biol. Chem. 268, 7256-7260
10. Miles, E. G. and Christen, L. (1993) Identification of the vaccinia virus mRNA guanyltransferase active site lysine. J. Biol. Chem. 268, 24986-24989
11. Shuman, S., Liu, Y. and Schwer, B. (1994) Covalent catalysis in nucleotidyl transfer reactions: essential motifs in Saccharomyces cerevisiae RNA-capping enzyme are conserved in Schizosaccharomyces pombe and viral capping enzymes and among polynucleotide ligases. Proc. Natl. Acad. Sci. U.S.A. 91, 12046-12050
12. Subramanya, H. S., Doherty, A. J., Ashford, S. R. and Wigley, D. B. (1996) Crystal structure of an ATP-dependent DNA ligase from bacteriophage T7. Cell (Cambridge, Mass.) 85, 607-615
13. Hakansson, K., Doherty, A. J., Shuman, S. and Wigley, D. B. (1997) X-ray crystallography reveals a large conformational change during guanyl transfer by mRNA-capping enzymes. Cell (Cambridge, Mass.) 89, 545-553
14. Hakansson, K. and Wigley, D. B. (1998) Structure of a complex between a cap analogue and mRNA guanylyl transferase demonstrates the structural chemistry of RNA-capping. Proc. Natl. Acad. Sci. U.S.A. 95, 1505-1510
15. Fabrega, C., Shen, V., Shuman, S. and Lima, C. D. (2003) Structure of an mRNA-capping enzyme bound to the phosphorylated carboxy-terminal domain of RNA polymerase II. Mol. Cell 11, 1549-1561
16. Painter, G. R., Wright, L. L., Hopkins, S. and Furman, P. A. (1991) Initial binding of 2′-deoxynucleoside 5′-triphosphates to human immunodeficiency virus type 1 reverse transcriptase. J. Biol. Chem. 266, 19362-19368
17. Eftink, M. R. and Ghiron, C. A. (1976) Exposure of tryptophanyl residues in proteins. Quantitative determination by fluorescence quenching studies. Biochemistry 15, 672-680
18. Flowers, S., Biswas, E. E. and Biswas, S. B. (2003) Conformational dynamics of DnaB helicase upon DNA and nucleotide binding: analysis by intrinsic tryptophan fluorescence quenching. Biochemistry 42, 1910-1921
19. Pan, J. Y., Sanford, J. C. and Wessling-Resnick, M. (1995) Effect of guanine nucleotide binding on the intrinsic tryptophan fluorescence properties of Rab5. J. Biol. Chem. 270, 24204-24208
20. Zhou, T. and Rosen, B. P. (1997) Tryptophan fluorescence reports nucleotide-induced conformational changes in a domain of the ArsA ATPase. J. Biol. Chem. 272, 19731-19737
21. Henn, A., Shi, S. P., Zarivach, R., Ben-Zeev, E. and Sagi, I. (2002) The RNA helicase DbpA exhibits a markedly different conformation in the ADP-bound state when compared with the ATP- or RNA-bound states. J. Biol. Chem. 277, 46559-46565
22. Record, M. T., Lohman, M. L. and de Haseth, P. L. (1976) Ion effects on ligand-nucleic acid interactions. J. Mol. Biol. 107, 145-158
23. Andrade, M. A., Chacon, P., Merelo, J. J. and Moran, F. (1993) Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network. Protein Eng. 6, 383-390
24. Beaudette, N. V. and Langerman, N. (1980) The thermodynamics of nucleotide binding to proteins. Crit. Rev. Biochem. 9, 145-169
25. Tame, J. R. H., O'Brien, R. and Ladbury, J. E. (1998) Isothermal titration calorimetry of biomolecules. In Biocalorimetry: Applications of Calorimetry in the Biological Sciences (Ladbury, J. E. and Chowdhry, B. Z., eds.), pp. 27-38. John Wiley and Sons, London
26. Hall, K. B. and Kranz, J. K. (1995) Thermodynamics and mutations in RNA-protein interactions. Methods Enzymol. 259, 261-281
27. Sawaya, R. and Shuman, S. (2003) Mutational analysis of the guanylyltransferase component of mammalian mRNA-capping enzyme. Biochemistry 42, 8240-8249
28. Schwede, T., Kopp, J., Guex, N. and Peitsch, M. C. (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31, 3381-3385