Biochemical characterization of the RNase II family of exoribonucleases from the human pathogens Salmonella typhimurium and Streptococcus pneumoniae

Biochemistry

Volumn 48, Issue 50, 2009, Pages 11848-11857

  Domingues, Susana ^a   Matos, Rute G ^a   Reis, Filipa P ^a   Fialho, Arsénio M ^b   Barbas, Ana ^a   Arraiano, Cecília M ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b INSTITUTO SUPERIOR TÉCNICO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SUBSTITUTION; BIOCHEMICAL CHARACTERIZATION; CATALYTIC DOMAINS; E. COLI; EXORIBONUCLEASES; HUMAN PATHOGENS; MODULAR ARCHITECTURES; POSTTRANSCRIPTIONAL CONTROL; RNA METABOLISMS; SALMONELLA TYPHIMURIUM; SEQUENCE ANALYSIS; STREPTOCOCCUS PNEUMONIAE;

AMINES; AMINO ACIDS; CATALYSTS; ESCHERICHIA COLI; NUCLEIC ACIDS; ORGANIC ACIDS; QUALITY CONTROL; QUALITY FUNCTION DEPLOYMENT; RNA; TOTAL QUALITY MANAGEMENT;

ENZYMES;

EXORIBONUCLEASE; HYDROLASE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL STRAIN; CHEMICAL ANALYSIS; ENZYME ACTIVE SITE; ESCHERICHIA COLI; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SALMONELLA TYPHIMURIUM; STREPTOCOCCUS PNEUMONIAE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; COMPUTER SIMULATION; ESCHERICHIA COLI PROTEINS; EXORIBONUCLEASES; HUMANS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PROTEIN BINDING; SALMONELLA TYPHIMURIUM; SEQUENCE HOMOLOGY, AMINO ACID; STREPTOCOCCUS PNEUMONIAE; SUBSTRATE SPECIFICITY; VIRULENCE;

ESCHERICHIA COLI; SALMONELLA TYPHIMURIUM; STREPTOCOCCUS PNEUMONIAE;

EID: 72449207486     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901105n     Document Type: Article

References (55)

1. Mian, I. S. (1997) Comparative sequence analysis of ribonucleases HII, III, II, PH and D. Nucleic Acids Res. 25, 3187-3195.
2. Zuo, Y., and Deutscher, M. P. (2001) Survey and Summary. Exoribonuclease superfamilies: Structural analysis and phylogenetic distribution. Nucleic Acids Res. 209, 1017-1026.
3. Andrade, J. M., Pobre, V., Silva, I. J., Domingues, S., and Arraiano, C. M. (2009) The role of 3′-5′ exoribonucleases in RNA degradation. Prog. Nucleic Acid Res. Mol. Biol. 85, 187-229.
4. Deutscher, M. P., and Reuven, N. B. (1991) Enzymatic basis for hydrolytic versus phosphorolytic mRNA degradation in Escherichia coli and Bacillus subtilis. Proc. Natl. Acad. Sci. U.S.A. 88, 3277-3280.
5. Marujo, P. E., Hajnsdorf, E., Le Derout, J., Arraiano, C. M., and Régnier, P. (2000) RNase II removes the oligo(A) tails that destabilize the rpsO mRNA of Escherichia coli. RNA 6, 1185-1193. (Pubitemid 30620401)
6. Mohanty, B. K., and Kushner, S. R. (2000) Polynucleotide phosphorylase, RNase II and RNase E play different roles in the in vivo modulation of polyadenylation in Escherichia coli. Mol. Microbiol. 36, 982-994.
7. Cairrão, F., Chora, A., Zilhão, R., Carpousis, J., and Arraiano, C. M. (2001) 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. 276, 19172-19181.
8. Zilhão, R., Cairrão, F., Régnier, P., and Arraiano, C. M. (1996) PNPase modulates RNase II expression in Escherichia coli: Implications for mRNA decay and cell metabolism. Mol. Microbiol. 20, 1033-1042.
9. Frazão, C., McVey, C. E., Amblar, M., Barbas, A., Vonrhein, C., Arraiano, C. M., and Carrondo, M. A. (2006) Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 443, 110-114. (Pubitemid 44344058)
10. Zuo, Y., Vincent, H. A., Zhang, J., Wang, Y., Deutscher, M. P., and Malhotra, A. (2006) Structural basis for processivity and single-strand specificity of RNase II. Mol. Cell 24, 149-156. (Pubitemid 44466687)
11. Barbas, A., Matos, R. G., Amblar, M., Lopez-Vinas, E., Gomez- Puertas, P., and Arraiano, C. M. (2008) 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. 283, 13070-13076.
12. Andrade, J. M., Cairrão, F., and Arraiano, C. M. (2006) RNase R affects gene expression in stationary phase: Regulation of ompA. Mol. Microbiol. 60, 219-228.
13. Cairrão, F., Cruz, A., Mori, H., and Arraiano, C. M. (2003) Cold shock induction of RNase R and its role in the maturation of the quality control mediator SsrA/tmRNA. Mol. Microbiol. 50, 1349-1360.
14. Cheng, Z. F., and Deutscher, M. P. (2003) Quality control of ribosomal RNA mediated by polynucleotide phosphorylase and RNase R. Proc. Natl. Acad. Sci. U.S.A. 100, 6388-6393.
15. Mahan, M. J., Slauch, J. M., and Mekalanos, J. J. (1996) Environmental regulation of virulence gene expression in Escherichia, Salmonella and Shigella spp. In E. coli and Salmonella: Cell and Molecular Biology , 2nd ed., pp 2803-2815, American Society for Microbiology Press, Washington, DC.
16. Li, Z., Reimers, S., Pandit, S., and Deutscher, M. P. (2002) RNA quality control: Degradation of defective transfer RNA. EMBO J. 21, 1132-1138. (Pubitemid 34206186)
17. Chen, C., and Deutscher, M. P. (2005) Elevation of RNase R in response to multiple stress conditions. J. Biol. Chem. 280, 34393-34396.
18. Charpentier, X., Faucher, S. P., Kalachikov, S., and Shuman, H. A. (2008) Loss of RNase R induces competence development in Legionella pneumophila. J. Bacteriol. 190, 8126-8136.
19. Purusharth, R. I., Klein, F., Sulthana, S., Jager, S., Jagannadham, M. V., Evguenieva-Hackenberg, E., Ray, M. K., and Klug, G. (2005) Exoribonuclease R interacts with endoribonuclease E and an RNA helicase in the psychrotrophic bacterium Pseudomonas syringae Lz4W. J. Biol. Chem. 280, 14572-14578.
20. Erova, T. E., Kosykh, V. G., Fadl, A. A., Sha, J., Horneman, A. J., and Chopra, A. K. (2008) Cold shock exoribonuclease R (VacB) is involved in Aeromonas hydrophila pathogenesis. J. Bacteriol. 190, 3467-3474.
21. Reva, O. N., Weinel, C., Weinel, M., Bohm, K., Stjepandic, D., Hoheisel, J. D., and Tummler, B. (2006) Functional genomics of stress response in Pseudomonas putida KT2440. J. Bacteriol. 188, 4079-4092. (Pubitemid 43825411)
22. Cheng, Z. F., and Deutscher, M. P. (2005) An important role for RNase R in mRNA decay. Mol. Cell 17, 313-318. (Pubitemid 40138624)
23. Cheng, Z. F., Zuo, Y., Li, Z., Rudd, K. E., and Deutscher, M. P. (1998) The vacB gene required for virulence in Shigella flexneri and Escherichia coli encodes the exoribonuclease RNase R. J. Biol. Chem. 273, 14077-14080.
24. Tobe, T., Sasakawa, C., Okada, N., Honma, Y., and Yoshikawa, M. (1992) vacB, a novel chromosomal gene required for expression of virulence genes on the large plasmid of Shigella flexneri. J. Bacteriol. 174, 6359-6367.
25. Tsao, M. Y., Lin, T. L., Hsieh, P. F., and Wang, J. T. (2009) The 3′-to- 5′ exoribonuclease (HP1248) of Helicobacter pylori regulates motility and apoptosis-inducing genes. J. Bacteriol. 191, 2691-2702.
26. Lalonde, M. S., Zuo, Y., Zhang, J., Gong, X., Wu, S., Malhotra, A., and Li, Z. (2007) Exoribonuclease R in Mycoplasma genitalium can carry out both RNA processing and degradative functions and is sensitive to RNA ribose methylation. RNA 13, 1957-1968. (Pubitemid 350005221)
27. Zuo, Y., and Deutscher, M. P. (2001) Exoribonuclease superfamilies: Structural analysis and phylogenetic distribution. Nucleic Acids Res. 29, 1017-1026. (Pubitemid 32186186)
28. Hutchison, C. A., Peterson, S. N., Gill, S. R., Cline, R. T., White, O., Fraser, C. M., Smith, H. O., and Venter, J. C. (1999) Global transposon mutagenesis and a minimal Mycoplasma genome. Science 286, 2165-2169. (Pubitemid 129516293)
29. Tomasz, A. (1999) New faces of an old pathogen: Emergence and spread of multidrug-resistant Streptococcus pneumoniae. Am. J. Med. 107, 55S-62S.
30. Hoskins, J., Alborn, W. E. Jr., Arnold, J., Blaszczak, L. C., Burgett, S., DeHoff, B. S., Estrem, S. T., Fritz, L., Fu, D. J., Fuller, W., Geringer, C., Gilmour, R., Glass, J. S., Khoja, H., Kraft, A. R., Lagace, R. E., LeBlanc, D. J., Lee, L. N., Lefkowitz, E. J., Lu, J., Matsushima, P., McAhren, S. M., McHenney, M., McLeaster, K., Mundy, C. W., Nicas, T. I., Norris, F. H., O'Gara, M., Peery, R. B., Robertson, G. T., Rockey, P., Sun, P. M., Winkler, M. E., Yang, Y., Young-Bellido, M., Zhao, G., Zook, C. A., Baltz, R. H., Jaskunas, S. R., Rosteck, P. R. Jr., Skatrud, P. L., and Glass, J. I. (2001) Genome of the bacterium Streptococcus pneumoniae strain R6. J. Bacteriol. 183, 5709-5717. (Pubitemid 32898618)
31. Taylor, R. G., Walker, D. C., and McInnes, R. R. (1993) E. coli host strains significantly affect the quality of small scale plasmid DNA preparations used for sequencing. Nucleic Acids Res. 21, 1677-1678. (Pubitemid 23146348)
32. Studier, F. W., and Moffatt, B. A. (1986) Selective expression of cloned genes directed by T7 RNA polymease. J. Mol. Biol. 189, 113-130.
33. Amblar, M., Barbas, A., Fialho, A. M., and Arraiano, C. M. (2006) Characterization of the Functional Domains of Escherichia coli RNase II. J. Mol. Biol. 360, 921-933.
34. Amblar, M., Barbas, A., Gomez-Puertas, P., and Arraiano, C. M. (2007) The role of the S1 domain in exoribonucleolytic activity: Substrate specificity and multimerization. RNA 13, 317-327. (Pubitemid 46327535)
35. Viegas, S. C., Pfeiffer, V., Sittka, A., Silva, I. J., Vogel, J., and Arraiano, C. M. (2007) Characterization of the role of ribonucleases in Salmonella small RNA decay. Nucleic Acids Res. 35, 7651-7664.
36. Arraiano, C. M., Barbas, A., and Amblar, M. (2008) Characterizing Ribonucleases in vitro: Examples of Synergies between Biochemical and Structural Analysis. Methods Enzymol. 447, 131-160.
37. Amblar, M., and Arraiano, C. M. (2005) A single mutation in Escherichia coli ribonuclease II inactivates the enzyme without affecting RNA binding. FEBS J. 272, 363-374.
38. Park, S., Myszka, D. G., Yu, M., Littler, S. J., and Laird-Offringa, I. A. (2000) HuD RNA recognition motifs play distinct roles in the formation of a stable complex with AU-rich RNA. Mol. Cell. Biol. 20, 4765-4772.
39. Higgins, D. G., and Sharp, P. M. (1988) CLUSTAL: A package for performing multiple sequence alignment on a microcomputer. Gene 73, 237-244.
40. Schmidt, H. A., Strimmer, K., Vingron, M., and von Haeseler, A. (2002) TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502-504. (Pubitemid 34284960)
41. Saitou, N., and Nei, M. (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
42. Felsenstein, J. (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783-791.
43. Finn, R. D., Tate, J., Mistry, J., Coggill, P. C., Sammut, S. J., Hotz, H. R., Ceric, G., Forslund, K., Eddy, S. R., Sonnhammer, E. L., and Bateman, A. (2008) The Pfam protein families database. Nucleic Acids Res. 36, D281-D288.
44. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web: A case study using the Phyre server. Nat. Protoc. 4, 363-371.
45. Zhang, R. G., Kim, Y., Skarina, T., Beasley, S., Laskowski, R., Arrowsmith, C., Edwards, A., Joachimiak, A., and Savchenko, A. (2002) Crystal structure of Thermotoga maritima 0065, a member of the IclR transcriptional factor family. J. Biol. Chem. 277, 19183-19190.
46. DeLano, W. L. (2002) The PyMOL Molecular Graphics System , 0.83 ed., DeLano Scientific, San Carlos, CA.
47. Ygberg, S. E., Clements, M. O., Rytkonen, A., Thompson, A., Holden, D. W., Hinton, J. C., and Rhen, M. (2006) Polynucleotide phosphorylase negatively controls spv virulence gene expression in Salmonella enterica. Infect. Immun. 74, 1243-1254.
48. Miyoshi, A., Rosinha, G. M., Camargo, I. L., Trant, C. M., Cardoso, F. C., Azevedo, V., and Oliveira, S. C. (2007) The role of the vacB gene in the pathogenesis of Brucella abortus. Microbes Infect. 9, 375-381. (Pubitemid 46343880)
49. Brennan, R. G., and Matthews, B. W. (1989) The helix-turn-helix DNA binding motif. J. Biol. Chem. 264, 1903-1906.
50. Liu, W., Seto, J., Sibille, E., and Toth, M. (2003) The RNA binding domain of Jerky consists of tandemly arranged helix-turn-helix/homeodomain-like motifs and binds specific sets of mRNAs. Mol. Cell. Biol. 23, 4083-4093.
51. Hosaka, H., Nakagawa, A., Tanaka, I., Harada, N., Sano, K., Kimura, M., Yao, M., and Wakatsuki, S. (1997) Ribosomal protein S7: A new RNA-binding motif with structural similarities to a DNA architectural factor. Structure 5, 1199-1208. (Pubitemid 27416027)
52. Matos, R. G., Barbas, A., and Arraiano, C. M. (2009) RNase R mutants elucidate the catalysis of structured RNA: RNA-binding domains select the RNAs targeted for degradation. Biochem. J. 423, 291-301.
53. Coburn, G. A., and Mackie, G. A. (1996) Overexpression, purification and properties of Escherichia coli ribonuclease II. J. Biol. Chem. 271, 1048-1053.
54. Barbas, A., Matos, R. G., Amblar, M., Lopez-Vinas, E., Gomez- Puertas, P., and Arraiano, C. M. (2009) Determination of key residues for catalysis and RNA-cleavage specificity: One mutation turns RNase II into a "super"-enzyme. J. Biol. Chem. 284, 20486-20498.
55. Vincent, H. A., and Deutscher, M. P. (2009) 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. 284, 486-494.