Swapping the domains of exoribonucleases RNase II and RNase R: Conferring upon RNase II the ability to degrade ds RNA

Proteins: Structure, Function and Bioinformatics

Volumn 79, Issue 6, 2011, Pages 1853-1867

  Matos, Rute Gonçalves ^a   Barbas, Ana ^a   Gómez Puertas, Paulino ^b   Arraiano, Cecília Maria ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

Exosome; Protein domains; Protein modeling; Protein structure; Ribonuclease; RNA; RNA degradation; RNA metabolism

Indexed keywords

DOUBLE STRANDED RNA; EXORIBONUCLEASE; LYSINE; RIBONUCLEASE II; RNASE R; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; RNA DEGRADATION;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EXORIBONUCLEASES; PROTEIN STRUCTURE, TERTIARY; RNA, BACTERIAL; RNA, DOUBLE-STRANDED; UP-REGULATION;

EID: 79955713801     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.23010     Document Type: Article

References (52)

1. Grossman D, van Hoof A. RNase II structure completes group portrait of 3' exoribonucleases. Nat Struct Mol Biol 2006; 13: 760-761.
2. Mian IS. Comparative sequence analysis of ribonucleases HII, III, II PH and D. Nucleic Acids Res 1997; 25: 3187-3195.
3. Mitchell P, Petfalski E, Shevchenko A, Mann M, Tollervey D. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3'->5' exoribonucleases. Cell 1997; 91: 457-466.
4. Zuo Y, Deutscher MP. Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res 2001; 29: 1017-1026.
5. Arraiano CM, Andrade JM, Domingues S, Guinote IB, Malecki M, Matos RG, Moreira RN, Pobre V, Reis FP, Saramago M, Silva IJ, Viegas SC. The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol Rev 2010; 34: 883-923.
6. Cheng ZF, Zuo Y, Li Z, Rudd KE, Deutscher MP. The vacB gene required for virulence in Shigella flexneri and Escherichia coli encodes the exoribonuclease RNase R. J Biol Chem 1998; 273: 14077-14080.
7. Cheng ZF, Deutscher MP. An important role for RNase R in mRNA decay. Mol Cell 2005; 17: 313-318.
8. Cairrão F, Arraiano CM. The role of endoribonucleases in the regulation of RNase R. Biochem Biophys Res Commun 2006; 343: 731-737.
9. Cairrão F, Cruz A, Mori H, Arraiano CM. Cold shock induction of RNase R and its role in the maturation of the quality control mediator SsrA/tmRNA. Mol Microbiol 2003; 50: 1349-1360.
10. Andrade JM, Cairrão F, Arraiano CM. RNase R affects gene expression in stationary phase: regulation of ompA. Mol Microbiol 2006; 60: 219-228.
11. Dziembowski A, Lorentzen E, Conti E, Seraphin B. A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat Struct Mol Biol 2007; 14: 15-22.
12. Schaeffer D, Tsanova B, Barbas A, Reis FP, Dastidar EG, Sanchez-Rotunno M, Arraiano CM, van Hoof A. The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struct Mol Biol 2009; 16: 56-62.
13. Lebreton A, Tomecki R, Dziembowski A, Seraphin B. Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 2008; 456: 993-996.
14. Cheng ZF, Deutscher MP. Purification and characterization of the Escherichia coli exoribonuclease RNase R. Comparison with RNase II. J Biol Chem 2002; 277: 21624-21629.
15. Amblar M, Barbas A, Fialho AM, Arraiano CM. Characterization of the functional domains of Escherichia coli RNase II. J Mol Biol 2006; 360: 921-933.
16. Matos RG, Barbas A, Arraiano CM. RNase R mutants elucidate the catalysis of structured RNA: RNA-binding domains select the RNAs targeted for degradation. Biochem J 2009; 423: 291-301.
17. Vincent HA, Deutscher MP. The roles of individual domains of RNase R in substrate binding and exoribonuclease activity: the nuclease domain is sufficient for digestion of structured RNA. J Biol Chem 2009; 284: 486-494.
18. Vincent HA, Deutscher MP. Substrate recognition and catalysis by the exoribonuclease RNase R. J Biol Chem 2006; 281: 29769-29775.
19. Amblar M, Barbas A, Gomez-Puertas P, Arraiano CM. The role of the S1 domain in exoribonucleolytic activity: substrate specificity and multimerization. RNA 2007; 13: 317-327.
20. Cannistraro VJ, Kennell D. The processive reaction mechanism of ribonuclease II. J Mol Biol 1994; 243: 930-943.
21. Domingues S, Matos RG, Reis FP, Fialho AM, Barbas A, Arraiano CM. Biochemical characterization of the RNase II family of exoribonucleases from the human pathogens Salmonella typhimurium and Streptococcus pneumoniae. Biochemistry 2009; 48: 11848-11857.
22. Deutscher MP, Reuven NB. Enzymatic basis for hydrolytic versus phosphorolytic mRNA degradation in Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci USA 1991; 88: 3277-3280.
23. Cairrão F, Chora A, Zilhao R, Carpousis AJ, Arraiano CM. RNase II levels change according to the growth conditions: characterization of gmr, a new Escherichia coli gene involved in the modulation of RNase II. Mol Microbiol 2001; 39: 1550-1561.
24. Zilhão R, Cairrão F, Régnier P, Arraiano CM. PNPase modulates RNase II expression in Escherichia coli: implications for mRNA decay and cell metabolism. Mol Microbiol 1996; 20: 1033-1042.
25. Zilhão R, Camelo L, Arraiano CM. DNA sequencing and expression of the gene rnb encoding Escherichia coli ribonuclease II. Mol Microbiol 1993; 8: 43-51.
26. Arraiano CM, Matos RG, Barbas A. RNase II: the finer details of the Modus Operandi of a molecular killer. RNA Biol 2010; 7: 276-278.
27. Frazão C, McVey CE, Amblar M, Barbas A, Vonrhein C, Arraiano CM, Carrondo MA. Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 2006; 443: 110-114.
28. Zuo Y, Vincent HA, Zhang J, Wang Y, Deutscher MP, Malhotra A. Structural basis for processivity and single-strand specificity of RNase II. Mol Cell 2006; 24: 149-156.
29. Barbas A, Matos RG, Amblar M, Lopez-Viñas E, Gomez-Puertas P, Arraiano CM. New insights into the mechanism of RNA degradation by ribonuclease II: identification of the residue responsible for setting the RNase II end product. J Biol Chem 2008; 283: 13070-13076.
30. Barbas A, Matos RG, Amblar M, Lopez-Vinas E, Gomez-Puertas P, Arraiano CM. Determination of key residues for catalysis and RNA cleavage specificity: one mutation turns RNase II into a "super-enzyme." J Biol Chem 2009; 284: 20486-20498.
31. Matos RG, Barbas A, Arraiano CM. Comparison of EMSA and SPR for the characterization of RNA-RNase II complexes. Protein J 2010; 29: 394-397.
32. Andrade JM, Hajnsdorf E, Regnier P, Arraiano CM. The poly(A)-dependent degradation pathway of rpsO mRNA is primarily mediated by RNase R. RNA 2009; 15: 316-326.
33. Erova TE, Kosykh VG, Fadl AA, Sha J, Horneman AJ, Chopra AK. Cold shock exoribonuclease R (VacB) is involved in Aeromonas hydrophila pathogenesis. J Bacteriol 2008; 190: 3467-3474.
34. Tobe T, Sasakawa C, Okada N, Honma Y, Yoshikawa M. vacB, a novel chromosomal gene required for expression of virulence genes on the large plasmid of Shigella flexneri. J Bacteriol 1992; 174: 6359-6367.
35. Tsao MY, Lin TL, Hsieh PF, Wang JT. The 3'-to-5' exoribonuclease (encoded by HP1248) of Helicobacter pylori regulates motility and apoptosis-inducing genes. J Bacteriol 2009; 191: 2691-2702.
36. Taylor RG, Walker DC, McInnes RR. E. coli host strains significantly affect the quality of small scale plasmid DNA preparations used for sequencing. Nucleic Acids Res 1993; 21: 1677-1678.
37. Studier FW, Moffatt BA. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 1986; 189: 113-130.
38. Arraiano CM, Barbas A, Amblar M. Characterizing ribonucleases in vitro examples of synergies between biochemical and structural analysis. Methods Enzymol 2008; 447: 131-160.
39. Park S, Myszka DG, Yu M, Littler SJ, Laird-Offringa IA. HuD RNA recognition motifs play distinct roles in the formation of a stable complex with AU-rich RNA. Mol Cell Biol 2000; 20: 4765-4772.
40. Combet C, Blanchet C, Geourjon C, Deleage G. NPS@: network protein sequence analysis. Trends Biochem Sci 2000; 25: 147-150.
41. Garnier J, Gibrat JF, Robson B. GOR method for predicting protein secondary structure from amino acid sequence. Methods Enzymol 1996; 266: 540-553.
42. Guex N, Peitsch MC. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 1997; 18: 2714-2723.
43. Kiefer F, Arnold K, Kunzli M, Bordoli L, Schwede T. The SWISS-MODEL repository and associated resources. Nucleic Acids Res 2009; 37(Database issue): D387-D392.
44. Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006; 22: 195-201.
45. Schwede T, Kopp J, Guex N, Peitsch MC. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 2003; 31: 3381-3385.
46. DeLano WL. The PyMOL molecular graphics system, 0.83 ed. San Carlos, CA: DeLano Scientific; 2002.
47. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25: 3389-3402.
48. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22: 4673-4680.
49. Notredame C, Higgins DG, Heringa J. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 2000; 302: 205-217.
50. Amblar M, Arraiano CM. A single mutation in Escherichia coli ribonuclease II inactivates the enzyme without affecting RNA binding. FEBS J 2005; 272: 363-374.
51. Ge Z, Mehta P, Richards J, Karzai AW. Non-stop mRNA decay initiates at the ribosome. Mol Microbiol 2010; 78: 1159-1170.
52. Awano N, Rajagopal V, Arbing M, Patel S, Hunt J, Inouye M, Phadtare S. Escherichia coli RNase R has dual activities, helicase and ribonuclease. J Bacteriol 2010; 192: 1344-1352.