About this Journal Submit a Manuscript Table of Contents
International Journal of Microbiology
Volume 2012 (2012), Article ID 592196, 18 pages
http://dx.doi.org/10.1155/2012/592196
Review Article

When Ribonucleases Come into Play in Pathogens: A Survey of Gram-Positive Bacteria

Architecture et réactivité de l'ARN, UPR 9002 CNRS, IBMC, Université de Strasbourg, 15 rue René Descartes, 67084 Strasbourg, France

Received 17 October 2011; Accepted 27 November 2011

Academic Editor: John Tagg

Copyright © 2012 Brian C. Jester et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Storz, J. Vogel, and K. Wassarman, “Regulation by small RNAs in bacteria: expanding frontiers,” Molecular Cell, vol. 43, no. 6, pp. 880–891, 2011. View at Publisher · View at Google Scholar
  2. P. Romby and M. Springer, “Bacterial translational control at atomic resolution,” Trends in Genetics, vol. 19, no. 3, pp. 155–161, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. J. G. Belasco, “All things must pass: contrasts and commonalities in eukaryotic and bacterial mRNA decay,” Nature Reviews Molecular Cell Biology, vol. 11, no. 7, pp. 467–478, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. K. L. Anderson and P. M. Dunman, “Messenger RNA turnover processes in Escherichia coli, Bacillus subtilis, and emerging studies in Staphylococcus aureus,” International Journal of Microbiology, vol. 2009, Article ID 525491, 15 pages, 2009. View at Publisher · View at Google Scholar
  5. C. Condon, “Maturation and degradation of RNA in bacteria,” Current Opinion in Microbiology, vol. 10, no. 3, pp. 271–278, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. A. J. Carpousis, B. F. Luisi, and K. J. McDowall, “Endonucleolytic initiation of mRNA decay in Escherichia coli,” Progress in Molecular Biology and Translational Science, vol. 85, pp. 91–135, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. D. H. Bechhofer, “Messenger RNA decay and maturation in Bacillus subtilis,” Progress in Molecular Biology and Translational Science, vol. 85, pp. 231–273, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Beaume, D. Hernandez, L. Farinelli et al., “Cartography of methicillin-resistant S. aureus transcripts: detection, orientation and temporal expression during growth phase and stress conditions,” PLoS ONE, vol. 5, no. 5, Article ID e10725, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. C. M. Sharma, S. Hoffmann, F. Darfeuille et al., “The primary transcriptome of the major human pathogen Helicobacter pylori,” Nature, vol. 464, no. 7286, pp. 250–255, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Toledo-Arana, O. Dussurget, G. Nikitas et al., “The Listeria transcriptional landscape from saprophytism to virulence,” Nature, vol. 459, no. 7249, pp. 950–956, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Rasmussen, H. B. Nielsen, and H. Jarmer, “The transcriptionally active regions in the genome of Bacillus subtilis,” Molecular Microbiology, vol. 73, no. 6, pp. 1043–1057, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Shahbabian, A. Jamalli, L. Zig, and H. Putzer, “RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis,” EMBO Journal, vol. 28, no. 22, pp. 3523–3533, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. F. M. Commichau, F. M. Rothe, C. Herzberg et al., “Novel activities of glycolytic enzymes in Bacillus subtilis: interactions with essential proteins involved in mRNA processing,” Molecular and Cellular Proteomics, vol. 8, no. 6, pp. 1350–1360, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Lehnik-Habrink, J. Newman, F. M. Rothe et al., “RNase Y in Bacillus subtilis: a natively disordered protein that is the functional equivalent of RNase E from Escherichia coli,” Journal of Bacteriology, vol. 193, no. 19, pp. 5431–5441, 2011. View at Publisher · View at Google Scholar
  15. M. Lehnik-Habrink, M. Schaffer, U. Mäder, C. Diethmaier, C. Herzberg, and J. Stülke, “RNA processing in Bacillus subtilis: identification of targets of the essential RNase Y,” Molecular Microbiology, vol. 81, no. 6, pp. 1459–1473, 2011. View at Publisher · View at Google Scholar
  16. C. Diethmaier, N. Pietack, K. Gunka et al., “A novel factor controlling bistability in Bacillus subtilis: the ymdb protein affects flagellin expression and biofilm formation,” Journal of Bacteriology, vol. 193, no. 21, pp. 5997–6007, 2011. View at Publisher · View at Google Scholar
  17. A. Hunt, J. P. Rawlins, H. B. Thomaides, and J. Errington, “Functional analysis of 11 putative essential genes in Bacillus subtilis,” Microbiology, vol. 152, part 10, pp. 2895–2907, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. V. Khemici, L. Poljak, B. F. Luisi, and A. J. Carpousis, “The RNase E of Escherichia coli is a membrane-binding protein,” Molecular Microbiology, vol. 70, no. 4, pp. 799–813, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Even, O. Pellegrini, L. Zig et al., “Ribonucleases J1 and J2: two novel endoribonucleases in B.subtilis with functional homology to E.coli RNase E,” Nucleic Acids Research, vol. 33, no. 7, pp. 2141–2152, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Kobayashi, S. D. Ehrlich, A. Albertini et al., “Essential Bacillus subtilis genes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 8, pp. 4678–4683, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. J. A. Newman, L. Hewitt, C. Rodrigues, A. Solovyova, C. R. Harwood, and R. J. Lewis, “Unusual, dual endo-and exonuclease activity in the degradosome explained by crystal structure analysis of RNase J1,” Structure, vol. 19, no. 9, pp. 1241–1251, 2011. View at Publisher · View at Google Scholar
  22. N. Mathy, L. Bénard, O. Pellegrini, R. Daou, T. Wen, and C. Condon, “5-to-3 exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5 stability of mRNA,” Cell, vol. 129, no. 4, pp. 681–692, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. N. Mathy, A. Hébert, P. Mervelet et al., “Bacillus subtilis ribonucleases J1 and J2 form a complex with altered enzyme behaviour,” Molecular Microbiology, vol. 75, no. 2, pp. 489–498, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. U. Mäder, L. Zig, J. Kretschmer, G. Homuth, and H. Putzer, “mRNA processing by RNases J1 and J2 affects Bacillus subtilis gene expression on a global scale,” Molecular Microbiology, vol. 70, no. 1, pp. 183–196, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Redko and C. Condon, “Maturation of 23S rRNA in Bacillus subtilis in the absence of mini-III,” Journal of Bacteriology, vol. 192, no. 1, pp. 356–359, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. I. L. de la Sierra-Gallay, L. Zig, A. Jamalli, and H. Putzer, “Structural insights into the dual activity of RNase J,” Nature Structural and Molecular Biology, vol. 15, no. 2, pp. 206–212, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Lehnik-Habrink, H. Pförtner, L. Rempeters, N. Pietack, C. Herzberg, and J. Stülke, “The RNA degradosome in bacillus subtilis: identification of csha as the major RNA helicase in the multiprotein complex,” Molecular Microbiology, vol. 77, no. 4, pp. 958–971, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Dorléans, I. li de la Sierra-Gallay, J. Piton et al., “Molecular basis for the recognition and cleavage of RNA by the bifunctional 5-3 exo/endoribonuclease RNase J,” Structure, vol. 19, no. 9, pp. 1252–1261, 2011. View at Publisher · View at Google Scholar
  29. M. F. Symmons, G. H. Jones, and B. F. Luisi, “A duplicated fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity, and regulation,” Structure, vol. 8, no. 11, pp. 1215–1226, 2000. View at Publisher · View at Google Scholar · View at Scopus
  30. W. Wang and D. H. Bechhofer, “Properties of a Bacillus subtilis polynucleotide phosphorylase deletion strain,” Journal of Bacteriology, vol. 178, no. 8, pp. 2375–2382, 1996. View at Scopus
  31. M. P. Deutscher and N. B. Reuven, “Enzymatic basis for hydrolytic versus phosphorolytic mRNA degradation in Escherichia coli and Bacillus subtilis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 8, pp. 3277–3280, 1991. View at Scopus
  32. S. Mitra, K. Hue, and D. H. Bechhofer, “In vitro processing activity of Bacillus subtilis polynucleotide phosphorylase,” Molecular Microbiology, vol. 19, no. 2, pp. 329–342, 1996. View at Scopus
  33. G. Deikus and D. H. Bechhofer, “Bacillus subtilis trp leader RNA. Rnase J1 endonuclease cleavage specificity and PNPase processing,” Journal of Biological Chemistry, vol. 284, no. 39, pp. 26394–26401, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. P. P. Cardenas, B. Carrasco, H. Sanchez, G. Deikus, D. H. Bechhofer, and J. C. Alonso, “Bacillus subtilis polynucleotide phosphorylase 3-to-5 DNase activity is involved in DNA repair,” Nucleic Acids Research, vol. 37, no. 12, pp. 4157–4169, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. P. P. Cardenas, T. Carzaniga, S. Zangrossi et al., “Polynucleotide phosphorylase exonuclease and polymerase activities on single-stranded DNA ends are modulated by RecN, SsbA and RecA proteins,” Nucleic Acids Research, vol. 39, no. 21, pp. 9250–9261, 2011. View at Publisher · View at Google Scholar
  36. I. J. MacRae and J. A. Doudna, “Ribonuclease revisited: structural insights into ribonuclease III family enzymes,” Current Opinion in Structural Biology, vol. 17, no. 1, pp. 138–145, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. V. N. Kim, J. Han, and M. C. Siomi, “Biogenesis of small RNAs in animals,” Nature Reviews Molecular Cell Biology, vol. 10, no. 2, pp. 126–139, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Blaszczyk, J. E. Tropea, M. Bubunenko et al., “Crystallographic and modeling studies of RNase III suggest a mechanism for double-stranded RNA cleavage,” Structure, vol. 9, no. 12, pp. 1225–1236, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Zhang, F. A. Kolb, L. Jaskiewicz, E. Westhof, and W. Filipowicz, “Single processing center models for human Dicer and bacterial RNase III,” Cell, vol. 118, no. 1, pp. 57–68, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Redko, D. H. Bechhofer, and C. Condon, “Mini-III, an unusual member of the RNase III family of enzymes, catalyses 23S ribosomal RNA maturation in B. subtilis,” Molecular Microbiology, vol. 68, no. 5, pp. 1096–1106, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. I. Calin-Jageman and A. W. Nicholson, “Mutational analysis of an RNA internal loop as a reactivity epitope for Escherichia coli ribonuclease III substrates,” Biochemistry, vol. 42, no. 17, pp. 5025–5034, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Li and A. W. Nicholson, “Defining the enzyme binding domain of a ribonuclease III processing signal. Ethylation interference and hydroxyl radical footprinting using catalytically inactive RNase III mutants,” EMBO Journal, vol. 15, no. 6, pp. 1421–1433, 1996. View at Scopus
  43. T. Franch, T. Thisted, and K. Gerdes, “Ribonuclease III processing of coaxially stacked RNA helices,” Journal of Biological Chemistry, vol. 274, no. 37, pp. 26572–26578, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Chevalier, S. Boisset, C. Romilly et al., “Staphylococcus aureus RNAIII binds to two distant regions of coa mRNA to arrest translation and promote mRNA degradation,” PLoS Pathogens, vol. 6, no. 3, Article ID e1000809, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. W. Wang and D. H. Bechhofer, “Bacillus subtilis RNase III gene: cloning, function of the gene in Escherichia coli, and construction of Bacillus subtilis strains with altered rnc loci,” Journal of Bacteriology, vol. 179, no. 23, pp. 7379–7385, 1997. View at Scopus
  46. M. B. Stead, S. Marshburn, B. K. Mohanty et al., “Analysis of Escherichia coli RNase e and RNase III activity in vivo using tiling microarrays,” Nucleic Acids Research, vol. 39, no. 8, pp. 3188–3203, 2011. View at Publisher · View at Google Scholar
  47. S. Yao, J. B. Blaustein, and D. H. Bechhofer, “Processing of Bacillus subtilis small cytoplasmic RNA: evidence for an additional endonuclease cleavage site,” Nucleic Acids Research, vol. 35, no. 13, pp. 4464–4473, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. M. A. Herskovitz and D. H. Bechhofer, “Endoribonuclease RNase III is essential in Bacillus subtilis,” Molecular Microbiology, vol. 38, no. 5, pp. 1027–1033, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Oguro, H. Kakeshita, K. Nakamura, K. Yamane, W. Wang, and D. H. Bechhofer, “Bacillus subtilis RNase III cleaves both 5-and 3-sites of the small cytoplasmic RNA precursor,” Journal of Biological Chemistry, vol. 273, no. 31, pp. 19542–19547, 1998. View at Publisher · View at Google Scholar · View at Scopus
  50. A. V. Pertzev and A. W. Nicholson, “Characterization of RNA sequence determinants and antideterminants of processing reactivity for a minimal substrate of Escherichia coli ribonuclease III,” Nucleic Acids Research, vol. 34, no. 13, pp. 3708–3721, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. A. V. Kazantsev and N. R. Pace, “Bacterial RNase P: a new view of an ancient enzyme,” Nature Reviews Microbiology, vol. 4, no. 10, pp. 729–740, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. J. Hsieh, A. J. Andrews, and C. A. Fierke, “Roles of protein subunits in RNA-protein complexes: lessons from Ribonuclease P,” Biopolymers, vol. 73, no. 1, pp. 79–89, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. E. Seif and S. Altman, “RNase P cleaves the adenine riboswitch and stabilizes pbuE mRNA in Bacillus subtilis,” RNA, vol. 14, no. 6, pp. 1237–1243, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Altman, “A view of RNase P,” Molecular BioSystems, vol. 3, no. 9, pp. 604–607, 2007. View at Publisher · View at Google Scholar
  55. A. Torres-Larios, K. K. Swinger, A. S. Krasilnikov, T. Pan, and A. Mondragón, “Crystal structure of the RNA component of bacterial ribonuclease P,” Nature, vol. 437, no. 7058, pp. 584–587, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. N. J. Reiter, A. Osterman, A. Torres-Larios, K. K. Swinger, T. Pan, and A. Mondragón, “Structure of a bacterial ribonuclease P holoenzyme in complex with tRNA,” Nature, vol. 468, no. 7325, pp. 784–789, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. O. Esakova and A. S. Krasilnikov, “Of proteins and RNA: the RNase P/MRP family,” RNA, vol. 16, no. 9, pp. 1725–1747, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. H. Celesnik, A. Deana, and J. G. Belasco, “Initiation of RNA decay in Escherichia coli by 5 pyrophosphate removal,” Molecular Cell, vol. 27, no. 1, pp. 79–90, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Richards, Q. Liu, O. Pellegrini et al., “An RNA pyrophosphohydrolase triggers 5-exonucleolytic degradation of mRNA in Bacillus subtilis,” Molecular Cell, vol. 43, no. 6, pp. 940–949, 2011. View at Publisher · View at Google Scholar
  60. S. H. Ling, R. Qamra, and H. Song, “Structural and functional insights into eukaryotic mRNA decapping,” Wiley Interdisciplinary Reviews, vol. 2, no. 2, pp. 193–208, 2011. View at Publisher · View at Google Scholar
  61. B. Py, H. Causton, E. A. Mudd, and C. F. Higgins, “A protein complex mediating mRNA degradation in Escherichia coli,” Molecular Microbiology, vol. 14, no. 4, pp. 717–729, 1994. View at Publisher · View at Google Scholar · View at Scopus
  62. A. J. Carpousis, G. van Houwe, C. Ehretsmann, and H. M. Krisch, “Copurification of E. coli RNAase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation,” Cell, vol. 76, no. 5, pp. 889–900, 1994. View at Publisher · View at Google Scholar · View at Scopus
  63. B. Py, C. F. Higgins, H. M. Krisch, and A. J. Carpousis, “A DEAD-box RNA helicase in the Escherichia coli RNA degradosome,” Nature, vol. 381, no. 6578, pp. 169–172, 1996. View at Publisher · View at Google Scholar · View at Scopus
  64. C. M. Roux, J. P. DeMuth, and P. M. Dunman, “Characterization of components of the Staphylococcus aureus mRNA degradosome holoenzyme-like complex,” Journal of Bacteriology, vol. 193, no. 19, pp. 5520–5526, 2011. View at Publisher · View at Google Scholar
  65. E. P. C. Rocha, “The organization of the bacterial genome,” Annual Review of Genetics, vol. 42, pp. 211–233, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. S. Yao and D. H. Bechhofer, “Initiation of decay of Bacillus subtilis rpsO mRNA by endoribonuclease RNase Y,” Journal of Bacteriology, vol. 192, no. 13, pp. 3279–3286, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. M. L. Gatewood, P. Bralley, and G. H. Jones, “Rnase III-dependent expression of the rpsO-pnp operon of Streptomyces coelicolor,” Journal of Bacteriology, vol. 193, no. 17, pp. 4371–4379, 2011. View at Publisher · View at Google Scholar
  68. P. Gao, K. L. Pinkston, S. R. Nallapareddy, A. van Hoof, B. E. Murray, and B. R. Harvey, “Enterococcus faecalis rnjB is required for pilin gene expression and biofilm formation,” Journal of Bacteriology, vol. 192, no. 20, pp. 5489–5498, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. H. Kakeshita, A. Oguro, R. Amikura, K. Nakamura, and K. Yamane, “Expression of the ftsY gene encoding a homologue of the α subunit of mammalian signal recognition particle receptor, is controlled by different promoters in vegetative and sporulating cells of Bacillus subtilis,” Microbiology, vol. 146, part 10, pp. 2595–2603, 2000. View at Scopus
  70. E. Ramirez-Peña, J. Treviño, Z. Liu, N. Perez, and P. Sumby, “The group A Streptococcus small regulatory RNA FasX enhances streptokinase activity by increasing the stability of the ska mRNA transcript,” Molecular Microbiology, vol. 78, no. 6, pp. 1332–1347, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. S. Boisset, T. Geissmann, E. Huntzinger et al., “Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism,” Genes and Development, vol. 21, no. 11, pp. 1353–1366, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. E. Huntzinger, S. Boisset, C. Saveanu et al., “Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression,” EMBO Journal, vol. 24, no. 4, pp. 824–835, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. J. M. Silvaggi, J. B. Perkins, and R. Losick, “Small untranslated RNA antitoxin in Bacillus subtilis,” Journal of Bacteriology, vol. 187, no. 19, pp. 6641–6650, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. N. J. P. ten Broeke-Smits, T. E. Pronk, I. Jongerius et al., “Operon structure of Staphylococcus aureus,” Nucleic Acids Research, vol. 38, no. 10, Article ID gkq058, pp. 3263–3274, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. P. D. Olson, L. J. Kuechenmeister, K. L. Anderson et al., “Small molecule inhibitors of staphylococcus aureus RnpA alter cellular mRNA turnover, exhibit antimicrobial activity, and attenuate pathogenesis,” PLoS Pathogens, vol. 7, no. 2, Article ID e1001287, 2011. View at Publisher · View at Google Scholar
  76. E. A. Bancroft, “Antimicrobial resistance: it's not just for hospitals,” Journal of the American Medical Association, vol. 298, no. 15, pp. 1803–1804, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. R. M. Klevens, M. A. Morrison, J. Nadle et al., “Invasive methicillin-resistant Staphylococcus aureus infections in the United States,” Journal of the American Medical Association, vol. 298, no. 15, pp. 1763–1771, 2007. View at Publisher · View at Google Scholar · View at Scopus
  78. J. V. Bugrysheva and J. R. Scott, “Regulation of virulence gene expression in Streptococcus pyogenes: determinants of differential mRNA decay,” RNA Biology, vol. 7, no. 5, pp. 569–572, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. T. C. Barnett, J. V. Bugrysheva, and J. R. Scott, “Role of mRNA stability in growth phase regulation of gene expression in the group A Streptococcus,” Journal of Bacteriology, vol. 189, no. 5, pp. 1866–1873, 2007. View at Publisher · View at Google Scholar · View at Scopus
  80. J. V. Bugrysheva and J. R. Scott, “The ribonucleases J1 and J2 are essential for growth and have independent roles in mRNA decay in Streptococcus pyogenes,” Molecular Microbiology, vol. 75, no. 3, pp. 731–743, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. C. Kaito, K. Kurokawa, Y. Matsumoto et al., “Silkworm pathogenic bacteria infection model for identification of novel virulence genes,” Molecular Microbiology, vol. 56, no. 4, pp. 934–944, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. S. O. Kang, M. G. Caparon, and K. H. Cho, “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,” Infection and Immunity, vol. 78, no. 6, pp. 2754–2767, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. M. Nagata, C. Kaito, and K. Sekimizu, “Phosphodiesterase activity of CvfA is required for virulence in Staphylococcus aureus,” Journal of Biological Chemistry, vol. 283, no. 4, pp. 2176–2184, 2008. View at Publisher · View at Google Scholar · View at Scopus
  84. K. Steiner and H. Malke, “Life in protein-rich environments: the relA-independent response of Streptococcus pyogenes to amino acid starvation,” Molecular Microbiology, vol. 38, no. 5, pp. 1004–1016, 2000. View at Publisher · View at Google Scholar · View at Scopus
  85. K. L. Anderson, C. Roberts, T. Disz et al., “Characterization of the Staphylococcus aureus heat shock, cold shock, stringent, and SOS responses and their effects on log-phase mRNA turnover,” Journal of Bacteriology, vol. 188, no. 19, pp. 6739–6756, 2006. View at Publisher · View at Google Scholar · View at Scopus
  86. K. L. Anderson, C. M. Roux, M. W. Olson et al., “Characterizing the effects of inorganic acid and alkaline shock on the Staphylococcus aureus transcriptome and messenger RNA turnover,” FEMS Immunology and Medical Microbiology, vol. 60, no. 3, pp. 208–250, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. A. Lawal, O. Jejelowo, A. K. Chopra, and J. A. Rosenzweig, “Ribonucleases and bacterial virulence,” Microbial Biotechnology, vol. 4, no. 5, pp. 558–571, 2011. View at Publisher · View at Google Scholar
  88. T. Geissmann, C. Chevalier, M. Cros et al., “A search for small noncoding RNAs in Staphylococcus aureus reveals a conserved sequence motif for regulation,” Nucleic Acids Research, vol. 37, no. 21, Article ID gkp668, pp. 7239–7257, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. K. Ohtani, H. Hirakawa, K. Tashiro, S. Yoshizawa, S. Kuhara, and T. Shimizu, “Identification of a two-component VirR/VirS regulon in Clostridium perfringens,” Anaerobe, vol. 16, no. 3, pp. 258–264, 2010. View at Publisher · View at Google Scholar · View at Scopus
  90. N. Obana, Y. Shirahama, K. Abe, and K. Nakamura, “Stabilization of Clostridium perfringens collagenase mRNA by VR-RNA-dependent cleavage in 5 leader sequence,” Molecular Microbiology, vol. 77, no. 6, pp. 1416–1428, 2010. View at Publisher · View at Google Scholar · View at Scopus
  91. A. I. Hidron, J. R. Edwards, J. Patel et al., “NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007,” Infection Control and Hospital Epidemiology, vol. 29, no. 11, pp. 996–1011, 2008. View at Publisher · View at Google Scholar
  92. T. Proft and E. N. Baker, “Pili in Gram-negative and Gram-positive bacteria—structure, assembly and their role in disease,” Cellular and Molecular Life Sciences, vol. 66, no. 4, pp. 613–635, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. R. P. Novick and E. Geisinger, “Quorum sensing in staphylococci,” Annual Review of Genetics, vol. 42, pp. 541–564, 2008. View at Publisher · View at Google Scholar · View at Scopus
  94. C. Bohn, C. Rigoulay, S. Chabelskaya et al., “Experimental discovery of small RNAs in Staphylococcus aureus reveals a riboregulator of central metabolism,” Nucleic Acids Research, vol. 38, no. 19, Article ID gkq462, pp. 6620–6636, 2010. View at Publisher · View at Google Scholar · View at Scopus
  95. B. Felden, F. Vandenesch, P. Bouloc, and P. Romby, “The Staphylococcus aureus RNome and its commitment to virulence,” PLoS Pathogens, vol. 7, no. 3, Article ID e1002006, 2011. View at Publisher · View at Google Scholar
  96. C. Pichon and B. Felden, “Small RNA genes expressed from Staphylococcus aureus genomic and pathogenicity islands with specific expression among pathogenic strains,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 40, pp. 14249–14254, 2005. View at Publisher · View at Google Scholar · View at Scopus
  97. Y. Liu, J. Dong, N. Wu et al., “The production of extracellular proteins is regulated by ribonuclease III via two different pathways in Staphylococcus aureus,” PLoS ONE, vol. 6, no. 5, Article ID e20554, 2011. View at Publisher · View at Google Scholar
  98. H. Aiba, “Mechanism of RNA silencing by Hfq-binding small RNAs,” Current Opinion in Microbiology, vol. 10, no. 2, pp. 134–139, 2007. View at Publisher · View at Google Scholar · View at Scopus
  99. P. Romby and E. Charpentier, “An overview of RNAs with regulatory functions in gram-positive bacteria,” Cellular and Molecular Life Sciences, vol. 67, no. 2, pp. 217–237, 2010. View at Publisher · View at Google Scholar · View at Scopus
  100. J. S. Nielsen, L. K. Lei, T. Ebersbach et al., “Defining a role for Hfq in Gram-positive bacteria: evidence for Hfq-dependent antisense regulation in Listeria monocytogenes,” Nucleic Acids Research, vol. 38, no. 3, Article ID gkp1081, pp. 907–919, 2009. View at Publisher · View at Google Scholar · View at Scopus
  101. J. S. Nielsen, M. H. Larsen, E. M. S. Lillebæk et al., “A small RNA controls expression of the chitinase ChiA in listeria monocytogenes,” PLoS ONE, vol. 6, no. 4, Article ID e19019, 2011. View at Publisher · View at Google Scholar
  102. E. Deltcheva, K. Chylinski, C. M. Sharma et al., “CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III,” Nature, vol. 471, no. 7340, pp. 602–607, 2011. View at Publisher · View at Google Scholar
  103. L. A. Marraffini and E. J. Sontheimer, “CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA,” Science, vol. 322, no. 5909, pp. 1843–1845, 2008. View at Publisher · View at Google Scholar · View at Scopus
  104. L. A. Marraffini and E. J. Sontheimer, “Self versus non-self discrimination during CRISPR RNA-directed immunity,” Nature, vol. 463, no. 7280, pp. 568–571, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. R. Barrangou, C. Fremaux, H. Deveau et al., “CRISPR provides acquired resistance against viruses in prokaryotes,” Science, vol. 315, no. 5819, pp. 1709–1712, 2007. View at Publisher · View at Google Scholar · View at Scopus
  106. P. Horvath and R. Barrangou, “CRISPR/Cas, the immune system of Bacteria and archaea,” Science, vol. 327, no. 5962, pp. 167–170, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. T. Sinkunas, G. Gasiunas, C. Fremaux, R. Barrangou, P. Horvath, and V. Siksnys, “Cas3 is a single-stranded DNA nuclease and ATP-dependent helicase in the CRISPR/Cas immune system,” EMBO Journal, vol. 30, no. 7, pp. 1335–1342, 2011. View at Publisher · View at Google Scholar
  108. R. R. Breaker, “Riboswitches: from ancient gene-control systems to modern drug targets,” Future Microbiology, vol. 4, no. 7, pp. 771–773, 2009. View at Publisher · View at Google Scholar · View at Scopus
  109. E. R. Lee, J. L. Baker, Z. Weinberg, N. Sudarsan, and R. R. Breaker, “An allosteric self-splicing ribozyme triggered by a bacterial second messenger,” Science, vol. 329, no. 5993, pp. 845–848, 2010. View at Publisher · View at Google Scholar · View at Scopus
  110. A. G. Y. Chen, N. Sudarsan, and R. R. Breaker, “Mechanism for gene control by a natural allosteric group I ribozyme,” RNA, vol. 17, no. 11, pp. 1967–1972, 2011. View at Publisher · View at Google Scholar
  111. J. A. Collins, I. Irnov, S. Baker, and W. C. Winkler, “Mechanism of mRNA destabilization by the glmS ribozyme,” Genes and Development, vol. 21, no. 24, pp. 3356–3368, 2007. View at Publisher · View at Google Scholar · View at Scopus
  112. H. Engelberg-Kulka, S. Amitai, I. Kolodkin-Gal, and R. Hazan, “Bacterial programmed cell death and multicellular behavior in bacteria,” PLoS Genetics, vol. 2, no. 10, article e135, 2006. View at Publisher · View at Google Scholar · View at Scopus
  113. Y. Yamaguchi and M. Inouye, “mRNA interferases, sequence-specific endoribonucleases from the toxin-antitoxin systems,” Progress in Molecular Biology and Translational Science, vol. 85, pp. 467–500, 2009. View at Publisher · View at Google Scholar · View at Scopus
  114. K. Gerdes, S. K. Christensen, and A. Løbner-Olesen, “Prokaryotic toxin-antitoxin stress response loci,” Nature Reviews Microbiology, vol. 3, no. 5, pp. 371–382, 2005. View at Publisher · View at Google Scholar · View at Scopus
  115. T. R. Blower, G. P. C. Salmond, and B. F. Luisi, “Balancing at survival's edge: the structure and adaptive benefits of prokaryotic toxin-antitoxin partners,” Current Opinion in Structural Biology, vol. 21, no. 1, pp. 109–118, 2011. View at Publisher · View at Google Scholar
  116. E. M. Fozo, M. R. Hemm, and G. Storz, “Small toxic proteins and the antisense RNAs that repress them,” Microbiology and Molecular Biology Reviews, vol. 72, no. 4, pp. 579–589, 2008, Table of Contents. View at Publisher · View at Google Scholar
  117. D. P. Pandey and K. Gerdes, “Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes,” Nucleic Acids Research, vol. 33, no. 3, pp. 966–976, 2005. View at Publisher · View at Google Scholar · View at Scopus
  118. K. Gerdes and E. G. H. Wagner, “RNA antitoxins,” Current Opinion in Microbiology, vol. 10, no. 2, pp. 117–124, 2007. View at Publisher · View at Google Scholar · View at Scopus
  119. T. R. Blower, X. Y. Pei, F. L. Short et al., “A processed noncoding RNA regulates an altruistic bacterial antiviral system,” Nature Structural and Molecular Biology, vol. 18, no. 2, pp. 185–191, 2011. View at Publisher · View at Google Scholar
  120. P. C. Fineran, T. R. Blower, I. J. Foulds, D. P. Humphreys, K. S. Lilley, and G. P. C. Salmond, “The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 3, pp. 894–899, 2009. View at Publisher · View at Google Scholar · View at Scopus
  121. J. H. Park, Y. Yamaguchi, and M. Inouye, “Bacillus subtilis MazF-bs (EndoA) is a UACAU-specific mRNA interferase,” FEBS Letters, vol. 585, no. 15, pp. 2526–2532, 2011. View at Publisher · View at Google Scholar
  122. O. Pellegrini, N. Mathy, A. Gogos, L. Shapiro, and C. Condon, “The Bacillus subtilis ydcDE operon encodes an endoribonuclease of the MazF/PemK family and its inhibitor,” Molecular Microbiology, vol. 56, no. 5, pp. 1139–1148, 2005. View at Publisher · View at Google Scholar · View at Scopus
  123. X. Wu, X. Wang, K. Drlica, and X. Zhao, “A toxin-antitoxin module in Bacillus subtilis can both mitigate and amplify effects of lethal stress,” PLoS ONE, vol. 6, no. 8, Article ID e23909, 2011. View at Publisher · View at Google Scholar
  124. S. Agarwal, N. K. Mishra, S. Bhatnagar, and R. Bhatnagar, “PemK toxin of Bacillus anthracis is a ribonuclease: an insight into its active site, structure, and function,” Journal of Biological Chemistry, vol. 285, no. 10, pp. 7254–7270, 2010. View at Publisher · View at Google Scholar · View at Scopus
  125. E. M. Moritz and P. J. Hergenrother, “Toxin-antitoxin systems are ubiquitous and plasmid-encoded in vancomycin-resistant enterococci,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 1, pp. 311–316, 2007. View at Publisher · View at Google Scholar · View at Scopus
  126. E. M. Halvorsen, J. J. Williams, A. J. Bhimani, E. A. Billings, and P. J. Hergenrother, “Txe, an endoribonuclease of the enterococcal Axe-Txe toxin-antitoxin system, cleaves mRNA and inhibits protein synthesis,” Microbiology, vol. 157, part 2, pp. 387–397, 2011. View at Publisher · View at Google Scholar
  127. L. M. Weigel, D. B. Clewell, S. R. Gill et al., “Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus,” Science, vol. 302, no. 5650, pp. 1569–1571, 2003. View at Publisher · View at Google Scholar · View at Scopus
  128. Z. Fu, N. P. Donegan, G. Memmi, and A. L. Cheung, “Characterization of mazFSa, an endoribonuclease from Staphylococcus aureus,” Journal of Bacteriology, vol. 189, no. 24, pp. 8871–8879, 2007. View at Publisher · View at Google Scholar
  129. L. Zhu, K. Inoue, S. Yoshizumi et al., “Staphylococcus aureus MazF specifically cleaves a pentad sequence, UACAU, which is unusually abundant in the mRNA for pathogenic adhesive factor SraP,” Journal of Bacteriology, vol. 191, no. 10, pp. 3248–3255, 2009. View at Publisher · View at Google Scholar · View at Scopus
  130. Z. Fu, S. Tamber, G. Memmi, N. P. Donegan, and A. L. Cheung, “Overexpression of mazFSa in Staphylococcus aureus induces bacteriostasis by selectively targeting mRNAs for cleavage,” Journal of Bacteriology, vol. 191, no. 7, pp. 2051–2059, 2009. View at Publisher · View at Google Scholar
  131. N. P. Donegan and A. L. Cheung, “Regulation of the mazEF toxin-antitoxin module in Staphylococcus aureus and its impact on sigB expression,” Journal of Bacteriology, vol. 191, no. 8, pp. 2795–2805, 2009. View at Publisher · View at Google Scholar · View at Scopus
  132. M. Bischoff, P. Dunman, J. Kormanec et al., “Microarray-based analysis of the Staphylococcus aureus σB regulon,” Journal of Bacteriology, vol. 186, no. 13, pp. 4085–4099, 2004. View at Publisher · View at Google Scholar
  133. J. J. Williams, E. M. Halvorsen, E. M. Dwyer, R. M. Difazio, and P. J. Hergenrother, “Toxin-antitoxin (TA) systems are prevalent and transcribed in clinical isolates of Pseudomonas aeruginosa and methicillin-resistant Staphylococcus aureus,” FEMS Microbiology Letters, vol. 322, no. 1, pp. 41–50, 2011. View at Publisher · View at Google Scholar
  134. O. Vesper, S. Amitai, M. Belitsky et al., “Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli,” Cell, vol. 147, no. 1, pp. 147–157, 2011. View at Publisher · View at Google Scholar
  135. H. R. Ramage, L. E. Connolly, and J. S. Cox, “Comprehensive functional analysis of Mycobacterium tuberculosis toxin-antitoxin systems: implications for pathogenesis, stress responses, and evolution,” PLoS Genetics, vol. 5, no. 12, Article ID e1000767, 2009. View at Publisher · View at Google Scholar · View at Scopus
  136. B. A. Ahidjo, D. Kuhnert, J. L. McKenzie et al., “VapC toxins from Mycobacterium tuberculosis are ribonucleases that differentially inhibit growth and are neutralized by cognate vapB antitoxins,” PLoS ONE, vol. 6, no. 6, Article ID e21738, 2011. View at Publisher · View at Google Scholar
  137. K. S. Winther and K. Gerdes, “Enteric virulence associated protein VapC inhibits translation by cleavage of initiator tRNA,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 18, pp. 7403–7407, 2011. View at Publisher · View at Google Scholar
  138. L. Aussel, W. Zhao, M. Hébrard et al., “Salmonella detoxifying enzymes are sufficient to cope with the host oxidative burst,” Molecular Microbiology, vol. 80, no. 3, pp. 628–640, 2011. View at Publisher · View at Google Scholar
  139. K. Lewis, “Persister cells,” Annual Review of Microbiology, vol. 64, pp. 357–372, 2010. View at Publisher · View at Google Scholar · View at Scopus
  140. E. Maisonneuve, L. J. Shakespeare, M. G. Jørgensen, and K. Gerdes, “Bacterial persistence by RNA endonucleases,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 32, pp. 13206–13211, 2011. View at Publisher · View at Google Scholar
  141. I. Keren, S. Minami, E. Rubin, and K. Lewis, “Characterization and transcriptome analysis of mycobacterium tuberculosis persisters,” mBio, vol. 2, no. 3, pp. e00100–e00111, 2011. View at Publisher · View at Google Scholar
  142. M. C. Chopin, A. Chopin, and E. Bidnenko, “Phage abortive infection in lactococci: variations on a theme,” Current Opinion in Microbiology, vol. 8, no. 4, pp. 473–479, 2005. View at Publisher · View at Google Scholar · View at Scopus
  143. J. M. Andrade and C. M. Arraiano, “PNPase is a key player in the regulation of small RNAs that control the expression of outer membrane proteins,” RNA, vol. 14, no. 3, pp. 543–551, 2008. View at Publisher · View at Google Scholar · View at Scopus
  144. N. de Lay and S. Gottesman, “Role of polynucleotide phosphorylase in sRNA function in Escherichia coli,” RNA, vol. 17, no. 6, pp. 1172–1189, 2011. View at Publisher · View at Google Scholar
  145. S. C. Viegas, I. J. Silva, M. Saramago, S. Domingues, and C. M. Arraiano, “Regulation of the small regulatory RNA MicA by ribonuclease III: a target-dependent pathway,” Nucleic Acids Research, vol. 39, no. 7, pp. 2918–2930, 2011. View at Publisher · View at Google Scholar
  146. S. C. Viegas and C. M. Arraiano, “Regulating the regulators: how ribonucleases dictate the rules in the control of small non-coding RNAs,” RNA Biology, vol. 5, no. 4, pp. 230–243, 2008. View at Scopus
  147. K. Prévost, G. Desnoyers, J. F. Jacques, F. Lavoie, and E. Massé, “Small RNA-induced mRNA degradation achieved through both translation block and activated cleavage,” Genes and Development, vol. 25, no. 4, pp. 385–396, 2011. View at Publisher · View at Google Scholar
  148. S. P. Pandey, B. K. Minesinger, J. Kumar, and G. C. Walker, “A highly conserved protein of unknown function in Sinorhizobium meliloti affects sRNA regulation similar to Hfq,” Nucleic Acids Research, vol. 39, no. 11, pp. 4691–4708, 2011. View at Publisher · View at Google Scholar
  149. A. Gaballa, H. Antelmann, C. Aguilar et al., “The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 33, pp. 11927–11932, 2008. View at Publisher · View at Google Scholar · View at Scopus
  150. S. Altuvia, H. Locker-Giladi, S. Koby, O. Ben-Nun, and A. B. Oppenheim, “RNase III stimulates the translation of the cIII gene of bacteriophage lambda,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 18, pp. 6511–6515, 1987. View at Scopus
  151. A. Prud'homme-Géńreux, R. K. Beran, I. Iost, C. S. Ramey, G. A. Mackie, and R. W. Simons, “Physical and functional interactions among RNase E, polynucleotide phosphorylase and the cold-shock protein, CsdA: evidence for a ‘cold shock degradosome’,” Molecular Microbiology, vol. 54, no. 5, pp. 1409–1421, 2004. View at Publisher · View at Google Scholar · View at Scopus
  152. S. W. Hardwick, V. S.Y. Chan, R. W. Broadhurst, and B. F. Luisi, “An RNA degradosome assembly in Caulobacter crescentus,” Nucleic Acids Research, vol. 39, no. 4, pp. 1449–1459, 2011. View at Publisher · View at Google Scholar
  153. S. Nurmohamed, H. A. Vincent, C. M. Titman et al., “Polynucleotide phosphorylase activity may be modulated by metabolites in Escherichia coli,” Journal of Biological Chemistry, vol. 286, no. 16, pp. 14315–14323, 2011. View at Publisher · View at Google Scholar
  154. J. R. Tuckerman, G. Gonzalez, and M. A. Gilles-Gonzalez, “Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing,” Journal of Molecular Biology, vol. 407, no. 5, pp. 633–639, 2011. View at Publisher · View at Google Scholar
  155. A. C. Jarrige, N. Mathy, and C. Portier, “PNPase autocontrols its expression by degrading a double-stranded structure in the pnp mRNA leader,” EMBO Journal, vol. 20, no. 23, pp. 6845–6855, 2001. View at Publisher · View at Google Scholar · View at Scopus
  156. W. Xu, J. Huang, and S. N. Cohen, “Autoregulation of absB (RNase III) expression in Streptomyces coelicolor by endoribonucleolytic cleavage of absB operon transcripts,” Journal of Bacteriology, vol. 190, no. 15, pp. 5526–5530, 2008. View at Publisher · View at Google Scholar · View at Scopus
  157. J. C. A. Bardwell, P. Regnier, S. M. Chen, Y. Nakamura, M. Grunberg-Manago, and D. L. Court, “Autoregulation of RNase III operon by mRNA processing,” EMBO Journal, vol. 8, no. 11, pp. 3401–3407, 1989. View at Scopus
  158. C. Jain and J. G. Belasco, “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 and Development, vol. 9, no. 1, pp. 84–96, 1995. View at Scopus
  159. K. S. Kim, R. Manasherob, and S. N. Cohen, “YmdB: a stress-responsive ribonuclease-binding regulator of E. coli RNase III activity,” Genes and Development, vol. 22, no. 24, pp. 3497–3508, 2008. View at Publisher · View at Google Scholar · View at Scopus
  160. D. D. Licatalosi, A. Mele, J. J. Fak et al., “HITS-CLIP yields genome-wide insights into brain alternative RNA processing,” Nature, vol. 456, no. 7221, pp. 464–469, 2008. View at Publisher · View at Google Scholar · View at Scopus
  161. S. W. Chi, J. B. Zang, A. Mele, and R. B. Darnell, “Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps,” Nature, vol. 460, no. 7254, pp. 479–486, 2009. View at Publisher · View at Google Scholar · View at Scopus
  162. K. F. Blount and R. R. Breaker, “Riboswitches as antibacterial drug targets,” Nature Biotechnology, vol. 24, no. 12, pp. 1558–1564, 2006. View at Publisher · View at Google Scholar · View at Scopus
  163. J. Mulhbacher, P. St-Pierre, and D. A. Lafontaine, “Therapeutic applications of ribozymes and riboswitches,” Current Opinion in Pharmacology, vol. 10, no. 5, pp. 551–556, 2010. View at Publisher · View at Google Scholar · View at Scopus
  164. J. J. Williams and P. J. Hergenrother, “Exposing plasmids as the Achilles' heel of drug-resistant bacteria,” Current Opinion in Chemical Biology, vol. 12, no. 4, pp. 389–399, 2008. View at Publisher · View at Google Scholar · View at Scopus
  165. I. Lasa, A. Toledo-Arana, A. Dobin et al., “Genome-wide antisense transcription drives mRNA processing in bacteria,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 50, pp. 20172–20177, 2011. View at Publisher · View at Google Scholar