Ribonucleases and bacterial virulence

Microbial Biotechnology

Volumn 4, Issue 5, 2011, Pages 558-571

  Lawal, Abidat ^a   Jejelowo, Olufisayo ^a   Chopra, Ashok K ^b   Rosenzweig, Jason A ^a  

^a TEXAS SOUTHERN UNIVERSITY   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DICER; GENE PRODUCT; RIBONUCLEASE; RIBONUCLEASE E; RNA;

BACTERIAL VIRULENCE; CELLULAR STRESS RESPONSE; COLD SHOCK RESPONSE; DICHELOBACTER NODOSUS; ENVIRONMENTAL STRESS; ESCHERICHIA COLI; HOST CELL; HUMAN; IMMUNOCOMPETENT CELL; NONHUMAN; OXIDATIVE STRESS; RNA METABOLISM; SALMONELLA ARIZONAE; SHIGELLA FLEXNERI; SHORT SURVEY; STREPTOCOCCUS;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; BACTERIAL PROTEINS; HUMANS; RIBONUCLEASES; VIRULENCE;

AEROMONAS HYDROPHILA; ANIMALIA; BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI; NEGIBACTERIA; SHIGELLA FLEXNERI;

EID: 84860390512     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/j.1751-7915.2010.00212.x     Document Type: Short Survey

References (81)

1. Anderson, K.L., and Dunman, P.M. (2009) Messenger RNA turnover processes in Escherichia coli, Bacillus subtilis, and emerging studies in Staphylococcus aureus. Int J Microbiol 2009: 525491.
2. Ardelt, W., Ardelt, B., and Darzynkiewicz, Z. (2009) Ribonucleases as potential modalities in anticancer therapy. Eur J Pharmacol 625: 181-189.
3. Barnett, T.C., Bugrysheva, J.V., and Scott, J.R. (2007) Role of mRNA stability in growth phase regulation of gene expression in the group A streptococcus. J Bacteriol 189: 1866-1873.
4. Blum, E., Py, B., Carpousis, A.J., and Higgins, C.F. (1997) Polyphosphate kinase is a component of the Escherichia coli RNA degradosome. Mol Microbiol 26: 387-398.
5. Boisset, S., Geissmann, T., Huntzinger, E., Fechter, P., Bendridi, N., Possedko, M., etal. (2007) Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 21: 1353-1366.
6. Bugrysheva, J.V., and Scott, J.R. (2010) The ribonucleases J1 and J2 are essential for growth and have independent roles in mRNA decay in Streptococcus pyogenes. Mol Microbiol 75: 731-743.
7. 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.
8. Callaghan, A.J., Marcaida, M.J., Stead, J.A., McDowall, K.J., Scott, W.G., and Luisi, B.F. (2005) Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature 437: 1187-1191.
9. Carpousis, A.J. (2002) The Escherichia coli RNA degradosome: structure, function and relationship in other ribonucleolytic multienzyme complexes. Biochem Soc Trans 30: 150-155.
10. Carpousis, A.J., Van Houwe, G., Ehretsmann, C., and Krisch, H.M. (1994) Copurification of E. coli RNAase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation. Cell 76: 889-900.
11. 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.
12. Chevalier, C., Huntzinger, E., Fechter, P., Boisset, S., Vandenesch, F., Romby, P., and Geissmann, T. (2008) Staphylococcus aureus endoribonuclease III purification and properties. Methods Enzymol 447: 309-327.
13. Clements, M.O., Eriksson, S., Thompson, A., Lucchini, S., Hinton, J.C., Normark, S., and Rhen, M. (2002) Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enterica. Proc Natl Acad Sci USA 99: 8784-8789.
14. Cornelis, G.R. (2002) Yersinia type III secretion: send in the effectors. J Cell Biol 158: 401-408.
15. Deutscher, M.P., and Li, Z. (2001) Exoribonucleases and their multiple roles in RNA metabolism. Prog Nucleic Acid Res Mol Biol 66: 67-105.
16. Domingues, S., Matos, R.G., Reis, F.P., Fialho, A.M., Barbas, A., and Arraiano, C.M. (2009) Biochemical characterization of the RNase II family of exoribonucleases from the human pathogens Salmonella typhimurium and Streptococcus pneumoniae. Biochemistry 48: 11848-11857.
17. Durán-Figueroa, N.V., Piña-Escobedo, A., Schroeder, I., Simons, R.W., and García-Mena, J. (2006) Polynucleotide phosphorylase interacts with ribonuclease E through a betabetaalphabetabetaalpha domain. Biochimie 88: 725-735.
18. 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.
19. Even, S., Pellegrini, O., Zig, L., Labas, V., Vinh, J., Bréchemmier-Baey, D., and Putzer, H. (2005) Ribonucleases J1 and J2: two novel endoribonucleases in B. subtilis with functional homology to E. coli RNase E. Nucleic Acids Res 33: 2141-2152.
20. Généreux, C., Dehareng, D., Devreese, B., Van Beeumen, J., Frère, J.M., and Joris, B. (2004) Mutational analysis of the catalytic centre of the Citrobacter freundii AmpD N-acetylmuramyl-L-alanine amidase. Biochem J 377 (Part 1): 111-120.
21. Goldstein, J., Pollitt, N.S., and Inouye, M. (1990) Major cold shock protein of Escherichia coli. Proc Natl Acad Sci USA 87: 283-287.
22. Gómez, M.I., Lee, A., Reddy, B., Muir, A., Soong, G., Pitt, A., etal. (2004) Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nat Med 10: 842-848.
23. Goverde, R.L., Huis in't Veld, J.H., Kusters, J.G., and Mooi, F.R. (1998) The psychrotrophic bacterium Yersinia enterocolitica requires expression of pnp, the gene for polynucleotide phosphorylase, for growth at low temperature (5 degrees C). Mol Microbiol 28: 555-569.
24. Grunberg-Manago, M., Ortiz, P.J., and Ochoa, S. (1955) Enzymatic synthesis of nucleic acid like polynucleotides. Science 122: 907-910.
25. Guarneros, G., and Portier, C. (1990) Different specificities of ribonuclease II and polynucleotide phosphorylase in 3'mRNA decay. Biochimie 72: 771-777.
26. Haddad, N., Burns, C.M., Bolla, J.M., Prévost, H., Fédérighi, M., Drider, D., and Cappelier, J.M. (2009) Long-term survival of Campylobacter jejuni at low temperatures is dependent on polynucleotide phosphorylase activity. Appl Environ Microbiol 75: 7310-7318.
27. Huntzinger, E., Boisset, S., Saveanu, C., Benito, Y., Geissmann, T., Namane, A., etal. (2005) Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J 24: 824-835.
28. Jain, C., and Belasco, J.G. (1995) RNase E autoregulates its synthesis by controlling the degradation rate of its own mRNA in Escherichia coli: unusual sensitivity of the rne transcript to RNase E activity. Genes Dev 9: 84-96.
29. Jarrige, A., Bréchemier-Baey, D., Mathy, N., Duché, O., and Portier, C. (2002) Mutational analysis of polynucleotide phosphorylase from Escherichia coli. J Mol Biol 321: 397-409.
30. Jarrige, A.C., Mathy, N., and Portier, C. (2001) PNPase autocontrols its expression by degrading a double-stranded structure in the pnp mRNA leader. EMBO J 20: 6845-6855.
31. Jiang, X., Diwa, A., and Belasco, J.G. (2000) Regions of RNase E important for 5'-end-dependent RNA cleavage and autoregulated synthesis. J Bacteriol 182: 2468-2475.
32. Jones, P.G., VanBogelen, R.A., and Neidhardt, F.C. (1987) Induction of proteins in response to low temperature in Escherichia coli. J Bacteriol 169: 2092-2095.
33. Kang, S.O., Caparon, M.G., and Cho, K.H. (2010) Virulence gene regulation by CvfA, a putative RNase: the CvfA-enolase complex in Streptococcus pyogenes links nutritional stress, growth-phase control, and virulence gene expression. Infect Immun 78: 2754-2767.
34. Kasai, T., Gupta, R.S., and Schlessinger, D. (1977) Exoribonucleases in wild type Escherichia coli and RNase II-deficient mutants. J Biol Chem 252: 8950-8956.
35. Khemici, V., and Carpousis, A.J. (2004) The RNA degradosome and poly(A) polymerase of Escherichia coli are required in vivo for the degradation of small mRNA decay intermediates containing REP-stabilizers. Mol Microbiol 51: 777-790.
36. Kido, M., Yamanaka, K., Mitani, T., Niki, H., Ogura, T., and Hiraga, S. (1996) RNase E polypeptides lacking a carboxyl-terminal half suppress a mukB mutation in Escherichia coli. J Bacteriol 178: 3917-3925.
37. Köten, B., Simanski, M., Gläser, R., Podschun, R., Schröder, J.M., and Harder, J. (2009) RNase 7 contributes to the cutaneous defense against Enterococcus faecium. PLoS ONE 4: e6424.
38. Kushner, S.R. (2002) mRNA decay in Escherichia coli comes of age. J Bacteriol 184: 4658-4665; discussion 4657.
39. Lee, E.J., and Groisman, E.A. (2010) An antisense RNA that governs the expression kinetics of a multifunctional virulence gene. Mol Microbiol 76: 1020-1033.
40. Len, A.C., Harty, D.W., and Jacques, N.A. (2004) Stress-responsive proteins are upregulated in Streptococcus mutans during acid tolerance. Microbiology 150 (Part 5): 1339-1351.
41. Leszczyniecka, M., Kang, D.C., Sarkar, D., Su, Z.Z., Holmes, M., Valerie, K., and Fisher, P.B. (2002) Identification and cloning of human polynucleotide phosphorylase, hPNPase old-35, in the context of terminal differentiation and cellular senescence. Proc Natl Acad Sci USA 99: 16636-16641.
42. Leszczyniecka, M., Su, Z.Z., Kang, D.C., Sarkar, D., and Fisher, P.B. (2003) Expression regulation and genomic organization of human polynucleotide phosphorylase, hPNPase(old-35), a Type I interferon inducible early response gene. Gene 316: 143-156.
43. Lewsey, M.G., and Carr, J.P. (2009) Effects of DICER-like proteins 2, 3 and 4 on cucumber mosaic virus and tobacco mosaic virus infections in salicylic acid-treated plants. J Gen Virol 90 (Part 12): 3010-3014.
44. Lin, P.H., and Lin-Chao, S. (2005) RhlB helicase rather than enolase is the beta-subunit of the Escherichia coli polynucleotide phosphorylase (PNPase)-exoribonucleolytic complex. Proc Natl Acad Sci USA 102: 16590-16595.
45. Lindler, L.E., Klempner, M.S., and Straley, S.C. (1990) Yersinia pestis pH 6 antigen: genetic, biochemical, and virulence characterization of a protein involved in the pathogenesis of bubonic plague. Infect Immun 58: 2569-2577
46. Mäder, U., Zig, L., Kretschmer, J., Homuth, G., and Putzer, H. (2008) mRNA processing by RNases J1 and J2 affects Bacillus subtilis gene expression on a global scale. Mol Microbiol 70: 183-196.
47. Miczak, A., Kaberdin, V.R., Wei, C.L., and Lin-Chao, S. (1996) Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc Natl Acad Sci USA 93: 3865-3869.
48. Mitchell, P., Petfalski, E., Shevchenko, A., Mann, M., and Tollervey, D. (1997) The exosome: a conserved eukaryotic RNA processing complex containing multiple 3'->5' exoribonucleases. Cell 91: 457-466.
49. 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.
50. Mudd, E.A., and Higgins, C.F. (1993) Escherichia coli endoribonuclease RNase E: autoregulation of expression and site-specific cleavage of mRNA. Mol Microbiol 9: 557-568.
51. Nagata, M., Kaito, C., and Sekimizu, K. (2008) Phosphodiesterase activity of CvfA is required for virulence in Staphylococcus aureus. J Biol Chem 283: 2176-2184.
52. Neuhaus, K., Rapposch, S., Francis, K.P., and Scherer, S. (2000) Restart of exponential growth of cold-shocked Yersinia enterocolitica occurs after down-regulation of cspA1/A2 mRNA. J Bacteriol 182: 3285-3288.
53. Neuhaus, K., Anastasov, N., Kaberdin, V., Francis, K.P., Miller, V.L., and Scherer, S. (2003) The AGUAAA motif in cspA1/A2 mRNA is important for adaptation of Yersinia enterocolitica to grow at low temperature. Mol Microbiol 50: 1629-1645.
54. Nikolaev, N., Folsom, V., and Schlessinger, D. (1976) Escherichia coli mutants deficient in exoribonucleases. Biochem Biophys Res Commun 70: 920-924.
55. Ono, M., and Kuwano, M. (1979) A conditional lethal mutation in an Escherichia coli strain with a longer chemical lifetime of messenger RNA. J Mol Biol 129: 343-357.
56. Palanisamy, S.K., Fletcher, C., Tanjung, L., Katz, M.E., and Cheetham, B.F. (2010) Deletion of the C-terminus of polynucleotide phosphorylase increases twitching motility, a virulence characteristic of the anaerobic bacterial pathogen Dichelobacter nodosus. FEMS Microbiol Lett 302: 39-45.
57. Patrick, K.L., Shi, H., Kolev, N.G., Ersfeld, K., Tschudi, C., and Ullu, E. (2009) Distinct and overlapping roles for two Dicer-like proteins in the RNA interference pathways of the ancient eukaryote Trypanosoma brucei. Proc Natl Acad Sci USA 106: 17933-17938.
58. Polissi, A., De Laurentis, W., Zangrossi, S., Briani, F., Longhi, V., Pesole, G., and Dehò, G. (2003) Changes in Escherichia coli transcriptome during acclimatization at low temperature. Res Microbiol 154: 573-580.
59. Portier, C. (1975) Quaternary structure of polynucleotide phosphorylase from Escherichia coli: evidence of a complex between two types of polypeptide chains. Eur J Biochem 55: 573-582.
60. Purusharth, R.I., Klein, F., Sulthana, S., Jäger, S., Jagannadham, M.V., Evguenieva-Hackenberg, E., etal. (2005) Exoribonuclease R interacts with endoribonuclease E and an RNA helicase in the psychrotrophic bacterium Pseudomonas syringae Lz4W. J Biol Chem 280: 14572-14578.
61. Purusharth, R.I., Madhuri, B., and Ray, M.K. (2007) Exoribonuclease R in Pseudomonas syringae is essential for growth at low temperature and plays a novel role in the 3' end processing of 16 and 5 S ribosomal RNA. J Biol Chem 282: 16267-16277.
62. Rosenzweig, J.A., and Schesser, K. (2007) Polynucleotide phosphorylase and the T3SS. Adv Exp Med Biol 603: 217-224.
63. Rosenzweig, J.A., Weltman, G., Plano, G.V., and Schesser, K. (2005) Modulation of yersinia type three secretion system by the S1 domain of polynucleotide phosphorylase. J Biol Chem 280: 156-163.
64. Rosenzweig, J.A., Chromy, B., Echeverry, A., Yang, J., Adkins, B., Plano, G.V., etal. (2007) Polynucleotide phosphorylase independently controls virulence factor expression levels and export in Yersinia spp. FEMS Microbiol Lett 270: 255-264.
65. Schaeffer, D., Tsanova, B., Barbas, A., Reis, F.P., Dastidar, E.G., Sanchez-Rotunno, M., etal. (2008) The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struct Mol Biol 16: 56-62.
66. Söderberg, M.A., and Cianciotto, N.P. (2010) Mediators of lipid A modification, RNA degradation, and central intermediary metabolism facilitate the growth of Legionella pneumophila at low temperatures. Curr Microbiol 60: 59-65.
67. Sousa, S., Marchand, I., and Dreyfus, M. (2001) Autoregulation allows Escherichia coli RNase E to adjust continuously its synthesis to that of its substrates. Mol Microbiol 42: 867-878.
68. Sun, Q., Choi, G.H., and Nuss, D.L. (2009) A single Argonaute gene is required for induction of RNA silencing antiviral defense and promotes viral RNA recombination. Proc Natl Acad Sci USA 106: 17927-17932.
69. 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.
70. Torruellas, J., Jackson, M.W., Pennock, J.W., and Plano, G.V. (2005) The Yersinia pestis type III secretion needle plays a role in the regulation of Yop secretion. Mol Microbiol 57: 1719-1733.
71. Tsao, M.Y., Lin, T.L., Hsieh, P.F., and Wang, J.T. (2009) The 3'-to-5' exoribonuclease (encoded by HP1248) of Helicobacter pylori regulates motility and apoptosis-inducing genes. J Bacteriol 191: 2691-2702.
72. Umitsuki, G., Wachi, M., Takada, A., Hikichi, T., and Nagai, K. (2001) Involvement of RNase G in in vivo mRNA metabolism in Escherichia coli. Genes Cells 6: 403-410.
73. Van Maerken, T., Sarkar, D., Speleman, F., Dent, P., Weiss, W.A., and Fisher, P.B. (2009) Adenovirus-mediated hPNPase(old-35) gene transfer as a therapeutic strategy for neuroblastoma. J Cell Physiol 219: 707-715.
74. Vanzo, N.F., Li, Y.S., Py, B., Blum, E., Higgins, C.F., Raynal, L.C., etal. (1998) Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev 12: 2770-2781.
75. Viboud, G.I., and Bliska, J.B. (2005) Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol 59: 69-89.
76. 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.
77. Wang, W., and Bechhofer, D.H. (1996) Properties of a Bacillus subtilis polynucleotide phosphorylase deletion strain. J Bacteriol 178: 2375-2382.
78. Wu, J., Jiang, Z., Liu, M., Gong, X., Wu, S., Burns, C.M., and Li, Z. (2009) Polynucleotide phosphorylase protects Escherichia coli against oxidative stress. Biochemistry 48: 2012-2020.
79. Yamanaka, K., and Inouye, M. (2001) Selective mRNA degradation by polynucleotide phosphorylase in cold shock adaptation in Escherichia coli. J Bacteriol 183: 2808-2816.
80. Yang, J., Jain, C., and Schesser, K. (2008) RNase E regulates the Yersinia type 3 secretion system. J Bacteriol 190: 3774-3778.
81. Ygberg, S.E., Clements, M.O., Rytkönen, 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.