Characterization of the vaccinia virus D10 decapping enzyme provides evidence for a two-metal-ion mechanism

Biochemical Journal

Volumn 420, Issue 1, 2009, Pages 27-35

  Soulière, Marie F ^a   Perreault, Jean Pierre ^a   Bisaillon, Martin ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

Decapping enzyme; Enzyme mechanism; MRNA metabolism; Nudix motif; Structural modelling; Vaccinia virus

Indexed keywords

DECAPPING ENZYME; ENZYME MECHANISM; MRNA METABOLISM; NUDIX MOTIF; STRUCTURAL MODELLING; VACCINIA VIRUS;

BINDING ENERGY; BINDING SITES; BIOCHEMISTRY; CATALYSTS; METABOLISM; METAL IONS; METAL RECOVERY; METALS; MODEL STRUCTURES; NUCLEIC ACIDS; RNA; TITRATION; TRACE ANALYSIS;

ENZYMES;

D10 PROTEIN; GLUTAMIC ACID; MAGNESIUM ION; MANGANESE; UNCLASSIFIED DRUG; VIRUS PROTEIN; D10 PROTEIN, VACCINIA VIRUS; DIVALENT CATION; MAGNESIUM; METAL; NUCLEOTIDASE;

ARTICLE; BINDING SITE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME STRUCTURE; METAL BINDING; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; RNA METABOLISM; VACCINIA VIRUS; CHEMISTRY; ENZYMOLOGY;

VACCINIA VIRUS;

BINDING SITES; CATALYTIC DOMAIN; CATIONS, DIVALENT; GLUTAMIC ACID; MAGNESIUM; MANGANESE; METALS; NUCLEOTIDASES; VACCINIA VIRUS; VIRAL PROTEINS;

EID: 65649104068     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20082296     Document Type: Article

References (36)

1. Wickens, M. and Goldstrohm, A. (2003) A place to die, a place to sleep. Science 300, 753-755
2. Sheth, U. and Parker, R. (2003) Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300, 805-808
3. Wang, Z., Jiao, X., Carr-Schmid, A. and Kiledjian, M. (2002) The hDcp2 protein is a mammalian mRNA decapping enzyme. Proc. Natl. Acad. Sci. U.S.A. 99, 12663-12668
4. Gunawardana, D., Cheng, H. C. and Gayler, K. R. (2008) Identification of functional domains in Arabidopsis thaliana mRNA decapping enzyme (AtDcp2) Nucleic Acids Res. 36, 203-216
5. Steiger, M., Carr-Schmid, A., Schwartz, D. C., Kiledjian, M. and Parker, R. (2003) Analysis of recombinant yeast decapping enzyme. RNA 9, 231-238
6. She, M., Decker, C. J., Chen, N., Tumati, S., Parker, R. and Song, H. (2006) Crystal structure and functional analysis of Dcp2p from Schizosaccharomyces pombe. Nat. Struct. Mol. Biol. 13, 63-70
7. 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
8. Parrish, S., Resch, W. and Moss, B. (2007) Vaccinia virus D10 protein has mRNA decapping activity, providing a mechanism for control of host and viral gene expression. Proc. Natl. Acad. Sci. U.S.A. 104, 2139-2144
9. Parrish, S. and Moss, B. (2006) Characterization of a vaccinia virus mutant with a deletion of the D10R gene encoding a putative negative regulator of gene expression. J. Virol. 80, 553-561
10. Parrish, S. and Moss, B. (2007) Characterization of a second vaccinia virus mRNA-decapping enzyme conserved in poxviruses. J. Virol. 81, 12973-12978
11. Shors, T., Keck, J. G. and Moss, B. (1999) Down regulation of gene expression by the vaccinia virus D10 protein. J. Virol. 73, 791-796
12. Mildvan, A. S., Xia, Z., Azurmendi, H. F., Saraswat, V., Legler, P. M., Massiah, M. A., Gabelli, S. B., Bianchet, M. A., Kang, L. W. and Amzel, L. M. (2005) Structures and mechanisms of Nudix hydrolases. Arch. Biochem. Biophys. 433, 129-143
13. McLennan, A. G. (2006) The Nudix hydrolase superfamily. Cell. Mol. Life Sci. 63, 123-143
14. Dunckley, T. and Parker, R. (1999) The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif. EMBO J. 18, 5411-5422
15. Liu, H. and Kiledjian, M. (2006) Decapping the message: a beginning or an end. Biochem. Soc. Trans. 34, 35-38
16. Ooga, T., Yoshiba, S., Nakagawa, N., Kuramitsu, S. and Masui, R. (2005) Molecular mechanism of the Thermus thermophilus ADP-ribose pyrophosphatase from mutational and kinetic studies. Biochemistry 44, 9320-9329
17. Legler, P. M., Massiah, M. A. and Mildvan, A. S. (2002) Mutational, kinetic, and NMR studies of the mechanism of E. coli GDP-mannose mannosyl hydrolase, an unusual Nudix enzyme. Biochemistry 41, 10834-10848
18. 2+. Biochemistry 39, 2347-2354
19. Gabelli, S. B., Bianchet, M. A., Ohnishi, Y., Ichikawa, Y., Bessman, M. J. and Amzel, L. M. (2002) Mechanism of the Escherichia coli ADP-ribose pyrophosphatase, a Nudix hydrolase. Biochemistry 41, 9279-9285
20. 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
21. 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
22. Guranowski, A. (1990) Fluoride is a strong and specific inhibitor of (asymmetrical) Ap4A hydrolases. FEBS Lett. 262, 205-208
23. 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
24. Bougie, I., Charpentier, S. and Bisaillon, M. (2003) Characterization of the metal ion binding properties of the hepatitis C virus RNA polymerase. J. Biol. Chem. 278, 3868-3875
25. Martins, A. and Shuman, S. (2003) Mapping the triphosphatase active site of baculovirus mRNA capping enzyme LEF4 and evidence for a two-metal mechanism. Nucleic Acids Res. 31, 1455-1463
26. Gong, C., Martins, A. and Shuman, S. (2003) Structure-function analysis of Trypanosoma brucei RNA triphosphatase and evidence for a two-metal mechanism. J. Biol. Chem. 278, 50843-50852
27. Steitz, T. A. and Steitz, J. A. (1993) A general two-metal-ion mechanism for catalytic RNA. Proc. Natl. Acad. Sci. U.S.A. 90, 6498-6502
28. Iwasaki, S., Takeda, A., Motose, H. and Watanabe, Y. (2007) Characterization of Arabidopsis decapping proteins AtDCP1 and AtDCP2, which are essential for post-embryonic development. FEBS Lett. 581, 2455-2459
29. Steiger, M., Carr-Schmid, A., Schwartz, D. C., Kiledjian, M. and Parker, R. (2003) Analysis of recombinant yeast decapping enzyme. RNA 9, 231-238
30. Mishima, M., Sakai, Y., Itoh, N., Kamiya, H., Furuichi, M., Takahashi, M., Yamagata, Y., Iwai, S., Nakabeppu, Y. and Shirakawa, M. (2004) Structure of human MTH1, a Nudix family hydrolase that selectively degrades oxidized purine nucleoside triphosphates. J. Biol. Chem. 279, 33806-33815
31. She, M., Decker, C. J., Svergun, D. I., Round, A., Chen, N., Muhlrad, D., Parker, R. and Song, H. (2008) Structural basis of Dcp2 recognition and activation by Dcp1. Mol. Cell 29, 337-349
32. van Dijk, E., Cougot, N., Meyer, S., Babajko, S., Wahle, E. and Séraphin, B. (2002) Human Dcp2: a catalytically active mRNA decapping enzyme located in specific cytoplasmic structures. EMBO J. 21, 6915-6924
33. Liu, S. W., Rajagopal, V., Patel, S. S. and Kiledjian, M. (2008) Mechanistic and kinetic analysis of the DcpS scavenger decapping enzyme. J. Biol. Chem. 283, 16427-16436
34. Xu, J., Yang, J. Y., Niu, Q. W. and Chua, N. H. (2006) Arabidopsis DCP2, DCP1, and VARICOSE form a decapping complex required for postembryonic development. Plant Cell 18, 3386-3398
35. Fenger-Gron, M., Fillman, C., Norrild, B. and Lykke-Andersen, J. (2005) Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol. Cell 20, 905-915
36. Yu, J. H., Yang, W. H., Gulick, T., Bloch, K. D. and Bloch, D. B. (2005) Ge-1 is a central component of the mammalian cytoplasmic mRNA processing body. RNA 11, 1795-1802