Yeast ribonuclease III uses a network of multiple hydrogen bonds for RNA binding and cleavage

Biochemistry

Volumn 47, Issue 33, 2008, Pages 8514-8526

  Lavoie, Mathieu ^a   Abou Elela, Shérif ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BINDING SITES; CATALYSIS; CHLORINE COMPOUNDS; COMPLEXATION; DISSOCIATION; ENZYMES; FLOW INTERACTIONS; HYDROGEN; HYDROGEN BONDS; NONMETALS; NUCLEIC ACIDS; NUCLEOTIDES; RNA; YEAST;

BINDING DOMAIN; CLEAVAGE SITES; COMMON FEATURES; DISSOCIATION CONSTANTS; MICHAELIS-MENTEN CONSTANT; N-TERMINAL DOMAINS; NUCLEOTIDE SUBSTITUTIONS; RIBONUCLEOTIDE; RIBONUCLEOTIDES; RNA CLEAVAGE; RNA-BINDING; SUBSTRATE STRUCTURES; YEAST ORTHOLOGUE;

SUBSTRATES;

NUCLEASE; NUCLEOTIDE; RIBONUCLEASE III; RIBONUCLEOTIDE; RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CATALYSIS; HYDROGEN BOND; MICHAELIS CONSTANT; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN RNA BINDING; RNA BINDING; RNA CLEAVAGE; STRUCTURE ANALYSIS;

GENE EXPRESSION REGULATION, FUNGAL; HYDROGEN BONDING; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; RIBONUCLEASE III; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

BACTERIA (MICROORGANISMS);

EID: 49749141418     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800238u     Document Type: Article

References (47)

1. Lamontagne, B., Larose, S., Boulanger, J., and Elela, S. A. (2001) The RNase III family: a conserved structure and expanding functions in eukaryotic dsRNA metabolism. Curr. Issues Mol. Biol. 3, 71-78.
2. Ritchie, W., Legendre, M., and Gautheret, D. (2007) RNA stem-loops: to be or not to be cleaved by RNAse III. RNA 13, 457-462.
3. Lykke-Andersen, K. (2006) Regulation of gene expression in mouse embryos and its embryonic cells through RNAi. Mol. Biotechnol. 34, 271-278.
4. Ghazal, G., Ge, D., Gervais-Bird, J., Gagnon, J., and Abou Elela, S. (2005) Genome-wide prediction and analysis of yeast RNase III-dependent snoRNA processing signals. Mol. Cell. Biol. 25, 2981-2994.
5. Regnier, P., and Grunberg-Manago, M. (1990) RNase III cleavages in non-coding leaders of Escherichia coli transcripts control mRNA stability and genetic expression. Biochimie 72, 825-834.
6. Saito, K., Ishizuka, A., Siomi, H., and Siomi, M. C. (2005) Processing of pre-microRNAs by the Dicer-1-Loquacious complex in Drosophila cells. PLoS Biol. 3, e235.
7. Gatignol, A., Laine, S., and Clerzius, G. (2005) Dual role of TRBP in HIV replication and RNA interference: viral diversion of a cellular pathway or evasion from antiviral immunity? Retrovirology 2, 65.
8. Nicholson, A. W. (1999) Function, mechanism and regulation of bacterial ribonucleases. FEMS Microbiol. Rev. 23, 371-390.
9. Collins, R. E., and Cheng, X. (2005) Structural domains in RNAi. FEBS Lett. 579, 5841-5849.
10. Carmell, M. A., and Hannon, G. J. (2004) RNase III enzymes and the initiation of gene silencing. Nat. Struct. Mol. Biol. 11, 214-218.
11. Abou Elela, S., Igel, H., and Ares, M., Jr. (1996) RNase III cleaves eukaryotic preribosomal RNA at a U3 snoRNP-dependent site. Cell 85, 115-124.
12. Catala, M., Lamontagne, B., Larose, S., Ghazal, G., and Abou Elela, S. (2004) Cell cycle-dependent nuclear localization of yeast RNase III is required for efficient cell division. Mol. Biol. Cell 15, 3015-3030.
13. Lamontagne, B., Tremblay, A., and Abou Elela, S. (2000) The N-terminal domain that distinguishes yeast from bacterial RNase III contains a dimerization signal required for efficient double-stranded RNA cleavage. Mol. Cell. Biol. 20, 1104-1115.
14. Leulliot, N., Quevillon-Cheruel, S., Graille, M., Van Tilbeurgh, H., Leeper, T. C., Godin, K. S., Edwards, T. E., Sigurdsson, S. T., Rozenkrants, N., Nagel, R. J., Ares, M., and Varani, G. (2004) A new α-helical extension promotes RNA binding by the dsRBD of Rntlp RNAse III. EMBO J. 23, 2468-2477.
15. Wu, H., Henras, A., Chanfreau, G., and Feigon, J. (2004) Structural basis for recognition of the AGNN tetraloop RNA fold by the double-stranded RNA-binding domain of Rnt1p RNase III. Proc. Natl. Acad. Sci. U.S.A. 101, 8307-8312.
16. Zhang, K., and Nicholson, A. W. (1997) Regulation of ribonuclease III processing by double-helical sequence antideterminants. Proc. Natl. Acad. Sci. U.S.A. 94, 13437-13441.
17. Lamontagne, B., and Abou Elela, S. (2004) Evaluation of the RNA determinants for bacterial and yeast RNase III binding and cleavage. J. Biol. Chem. 279, 2231-2241.
18. Ghazal, G., and Elela, S. A. (2006) Characterization of the reactivity determinants of a novel hairpin substrate of yeast RNase III. J. Mol. Biol. 363, 332-344.
19. Lamontagne, B., Ghazal, G., Lebars, I., Yoshizawa, S., Fourmy, D., and Abou Elela, S. (2003) Sequence dependence of substrate recognition and cleavage by yeast RNase III. J. Mol. Biol. 327, 985-1000.
20. Lebars, I., Lamontagne, B., Yoshizawa, S., Aboul-Elela, S., and Fourmy, D. (2001) Solution structure of conserved AGNN tetraloops: insights into Rntlp RNA processing. EMBO J. 20, 7250-7258.
21. Staple, D. W., and Butcher, S. E. (2003) Solution structure of the HIV-1 frameshift inducing stem-loop RNA. Nucleic Acids Res. 31, 4326-4331.
22. Gaudin, C., Ghazal, G., Yoshizawa, S., Elela, S. A., and Fourmy, D. (2006) Structure of an AAGU tetraloop and its contribution to substrate selection by yeast RNase III. J. Mol. Biol. 363, 322-331.
23. Gan, J., Tropea, J. E., Austin, B. P., Court, D. L., Waugh, D. S., and Ji, X. (2006) Structural insight into the mechanism of double-stranded RNA processing by ribonuclease III. Cell 124, 355-366.
24. Guthrie, C., and Fink, G. R. (1991) Guide to Yeast Genetics and Molecular Biology, Academic Press, San Diego, CA.
25. Rose, M. D., Winston, F., and Hieter, P. (1990) Methods in Yeast Genetics: A Laboratory Course Manual, Cold Spring Harbor Press, Cold Spring Harbor, NY.
26. Madhani, H. D., and Guthrie, C. (1992) A novel base-pairing interaction between U2 and U6 snRNAs suggests a mechanism for the catalytic activation of the spliceosome. Cell 71, 803-817.
27. Lamontagne, B., and Abou Elela, S. (2007) Short RNA guides cleavage by eukaryotic RNase III. PLoS ONE 2, e472.
28. Lamontagne, B., and Abou Elela, S. (2001) Purification and characterization of Saccharomyces cerevisiae Rnt1p nuclease. Methods Enzymol. 342, 159-167.
29. Lamontagne, B., Hannoush, R. N., Damha, M. J., and Abou Elela, S. (2004) Molecular requirements for duplex recognition and cleavage by eukaryotic RNase III: discovery of an RNA-dependent DNA cleavage activity of yeast Rntlp. J. Mol. Biol. 338, 401-418.
30. Chanfreau, G., Abou Elela, S., Ares, M., Jr., and Guthrie, C. (1997) Alternative 3′-end processing of U5 snRNA by RNase III. Genes Dev. 11, 2741-2751.
31. Burgers, P. M., and Eckstein, F. (1979) Diastereomers of 5′-O-adenosyl 3′-O-uridyl phosphorothioate: chemical synthesis and enzymatic properties. Biochemistry 18, 592-596.
32. Burgers, P. M., Sathyanarayana, B. K., Saenger, W., and Eckstein, F. (1979) Crystal and molecular structure of adenosine 5′-O-phosphorothioate O-p-nitrophenyl ester (Sp diastereomer). Substrate stereospecificity of snake venom phosphodiesterase. Eur. J. Biochem. 100, 585-591.
33. Yamanaka, G., Eckstein, F., and Stryer, L. (1985) Stereochemistry of the guanyl nucleotide binding site of transducin probed by phosphorothioate analogues of GTP and GDP. Biochemistry 24, 8094-8101.
34. Giorgi, C., Fatica, A., Nagel, R., and Bozzoni, I. (2001) Release of U18 snoRNA from its host intron requires interaction of Nop1p with the Rnt1p endonuclease. EMBO J. 20, 6856-6865.
35. Kraynack, B. A., and Baker, B. F. (2006) Small interfering RNAs containing full 2′-O-methylribonucleotide-modified sense strands display Argonaute2/eIF2C2-dependent activity. RNA 12, 163-176.
36. Henras, A. K., Sam, M., Hiley, S. L., Wu, H., Hughes, T. R., Feigon, J., and Chanfreau, G. F. (2005) Biochemical and genomic analysis of substrate recognition by the double-stranded RNA binding domain of yeast RNase III. RNA 11, 1225-1237.
37. Egli, M., and Gryaznov, S. M. (2000) Synthetic oligonucleotides as RNA mimetics: 2′-modified RNAs and N3′→P5′ phosphoramidates. Cell. Mol. Life Sci. 57, 1440-1456.
38. Gan, J., Shaw, G., Tropea, J. E., Waugh, D. S., Court, D. L., and Ji, X. (2008) A stepwise model for double-stranded RNA processing by ribonuclease III. Mol. Microbiol. 67, 143-154.
39. Li, H., and Nicholson, A. W. (1996) Defining the enzyme binding domain of a ribonuclease III processing signal. Ethylation interference and hydroxyl radical footprinting using catalytically inactive RNase III mutants. EMBO J. 15, 1421-1433.
40. Ray, A. S., Schinazi, R. F., Murakami, E., Basavapathruni, A., Shi, J., Zorca, S. M., Chu, C. K., and Anderson, K. S. (2003) Probing the mechanistic consequences of 5-fluorine substitution on cytidine nucleotide analogue incorporation by HIV-1 reverse transcriptase. Antivir. Chem. Chemother. 14, 115-125.
41. Derringer, D., Dale, T., and Uhlenbeck, O. C. (2001) Modifying the specificity of an RNA backbone contact. J. Mol. Biol. 314, 649-654.
42. Howard, J. A. K., Hoy, V. J., O'Hagan, D., and Smith, G. T. (1996) How good is fluorine as a hydrogen bond acceptor. Tetrahedron 52, 12613-12622.
43. Nidetzky, B., Mayr, P., Hadwiger, P., and Stutz, A. E. (1999) Binding energy and specificity in the catalytic mechanism of yeast aldose reductases. Biochem. J. 344 (Part 1), 101-107.
44. Blaszczyk, J., Gan, J., Tropea, J. E., Court, D. L., Waugh, D. S., and Ji, X. (2004) Noncatalytic assembly of ribonuclease III with double-stranded RNA. Structure (Cambridge) 12, 457-466.
45. Blaszczyk, J., Tropea, J. E., Bubunenko, M., Routzahn, K. M., Waugh, D. S., Court, D. L., and Ji, X. (2001) Crystallographic and modeling studies of RNase III suggest a mechanism for double-stranded RNA cleavage. Structure (Cambridge) 9, 1225-1236.
46. Sun, W., Jun, E., and Nicholson, A. W. (2001) Intrinsic double-stranded-RNA processing activity of Escherichia coli ribonuclease III lacking the dsRNA-binding domain. Biochemistry 40, 14976-14984.
47. Calin-Jageman, I., and Nicholson, A. W. (2003) RNA structure-dependent uncoupling of substrate recognition and cleavage by Escherichia coli ribonuclease III. Nucleic Acids Res. 31, 2381-2392.