DOI QR코드

DOI QR Code

Small RNA biology is systems biology

  • Jost, Daniel (Department of Physics, FAS Center for Systems Biology, Harvard University) ;
  • Nowojewski, Andrzej (Department of Physics, FAS Center for Systems Biology, Harvard University) ;
  • Levine, Erel (Department of Physics, FAS Center for Systems Biology, Harvard University)
  • Received : 2011.01.12
  • Published : 2011.01.31

Abstract

During the last decade small regulatory RNA (srRNA) emerged as central players in the regulation of gene expression in all kingdoms of life. Multiple pathways for srRNA biogenesis and diverse mechanisms of gene regulation may indicate that srRNA regulation evolved independently multiple times. However, small RNA pathways share numerous properties, including the ability of a single srRNA to regulate multiple targets. Some of the mechanisms of gene regulation by srRNAs have significant effect on the abundance of free srRNAs that are ready to interact with new targets. This results in indirect interactions among seemingly unrelated genes, as well as in a crosstalk between different srRNA pathways. Here we briefly review and compare the major srRNA pathways, and argue that the impact of srRNA is always at the system level. We demonstrate how a simple mathematical model can ease the discussion of governing principles. To demonstrate these points we review a few examples from bacteria and animals.

Keywords

References

  1. Jacob, F. and Monod, J. (1961) Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 3, 318-356. https://doi.org/10.1016/S0022-2836(61)80072-7
  2. Lee, R. (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 175, 843-854.
  3. Wightman, B., Ha, I. and Ruvkun, G. (1993) Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855-862. https://doi.org/10.1016/0092-8674(93)90530-4
  4. Argaman, L., Hershberg, R., Vogel, J., Bejerano, G., Wagner, E. H., Margalit, H. and Altuvia, S. (2001) Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Current Biology. 11, 941-950. https://doi.org/10.1016/S0960-9822(01)00270-6
  5. Wassarman, K. M., Repoila, F., Rosenow, C., Storz, G. and Gottesman, S. (2001) Identification of novel small RNAs using comparative genomics and microarrays. Genes & Development 15, 1637-1651. https://doi.org/10.1101/gad.901001
  6. Rivas, E., Klein, R. J., Jones, T. A. and Eddy, S. R. (2001) Computational identification of noncoding RNAs in E. coli by comparative genomics. Current Biology 11, 1369-1373. https://doi.org/10.1016/S0960-9822(01)00401-8
  7. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E. and Mello, C. C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811. https://doi.org/10.1038/35888
  8. Reinhart, B. J., Slack, F. J., Basson, M., Pasquinelli, A. E., Bettinger, J. C., Rougvie, A. E., Horvitz, H. R. and Ruvkun, G. (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901-906. https://doi.org/10.1038/35002607
  9. Pasquinelli, A. E., Reinhart, B. J., Slack, F., Martindale, M. Q., Kuroda, M. I., Maller, B., Hayward, D. C., Ball, E. E., Degnan, B., Müller, P., Spring, J., Srinivasan, A., Fishman, M., Finnerty, J., Corbo, J., Levine, M., Leahy, P., Davidson, E. and Ruvkun, G. (2000) Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86-89. https://doi.org/10.1038/35040556
  10. Ghildiyal, M. and Zamore, P. D. (2009) Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10, 94-108. https://doi.org/10.1038/nrg2504
  11. Bartel, D. P. (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233. https://doi.org/10.1016/j.cell.2009.01.002
  12. Alvarez-Garcia, I. and Miska, E. A. (2005) MicroRNA functions in animal development and human disease. Development 132, 4653-4662. https://doi.org/10.1242/dev.02073
  13. Hagen, J. W. and Lai, E. C. (2008) microRNA control of cell-cell signaling during development and disease. Cell Cycle 7, 2327-2332. https://doi.org/10.4161/cc.6447
  14. Ivey, K. N., Muth, A., Arnold, J., King, F. W., Yeh, R., Fish, J. E., Hsiao, E. C., Schwartz, R. J., Conklin, B. R., Bernstein, H. S. and Srivastava, D. (2008) MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell 2, 219-229. https://doi.org/10.1016/j.stem.2008.01.016
  15. Khurana, J. S. and Theurkauf, W. E. (2008) piRNA function in germline development (July 30, 2008), StemBook, ed. The Stem Cell Research Community, StemBook, doi/ 10.3824/stembook.1.12.1, http://www.stembook.org.
  16. Reynolds, S. and Ruohola-Baker, H. (2008) microRNA’s role in germline differentiation (September 15, 2008), Stem Book, ed. The Stem Cell Research Community, StemBook, doi/ 10.3824/stembook.1.17.1, http://www.stembook.org.
  17. Croce, C. M. (2009) Causes and consequences of microRNA dysregulation in cancer. Nat. Rev. Genet 10, 704-714. https://doi.org/10.1038/nrg2634
  18. Leung, A. K. L. and Sharp, P. A. (2010) MicroRNA functions in stress responses. Mol. Cell 40, 205-215. https://doi.org/10.1016/j.molcel.2010.09.027
  19. Aravin, A. A., Hannon, G. J. and Brennecke, J. (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318, 761-764. https://doi.org/10.1126/science.1146484
  20. Lee, Y., Jeon, K., Lee, J., Kim, S. and Kim, V. N. (2002) MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 21, 4663-4670. https://doi.org/10.1093/emboj/cdf476
  21. Lee, Y., Kim, M., Han, J., Yeom, K., Lee, S., Baek, S. H. and Kim, V. N. (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051-4060. https://doi.org/10.1038/sj.emboj.7600385
  22. Czech, B., Malone, C. D., Zhou, R., Stark, A., Schlingeheyde, C., Dus, M., Perrimon, N., Kellis, M., Wohlschlegel, J. A., Sachidanandam, R., Hannon, G. J. and Brennecke, J. (2008) An endogenous small interfering RNA pathway in Drosophila. Nature 453, 798-802. https://doi.org/10.1038/nature07007
  23. Okamura, K., Chung, W., Ruby, J. G., Guo, H., Bartel, D. P. and Lai, E. C. (2008) The Drosophila hairpin RNA pathway generates endogenous short interfering RNAs. Nature 453, 803-806. https://doi.org/10.1038/nature07015
  24. Kawamura, Y., Saito, K., Kin, T., Ono, Y., Asai, K., Sunohara, T., Okada, T. N., Siomi, M. C. and Siomi, H. (2008) Drosophila endogenous small RNAs bind to Argonaute(thinsp)2 in somatic cells. Nature 453, 793-797. https://doi.org/10.1038/nature06938
  25. Okamura, K., Balla, S., Martin, R., Liu, N. and Lai, E. C. (2008) Two distinct mechanisms generate endogenous siRNAs from bidirectional transcription in Drosophila melanogaster. Nat. Struct. Mol. Biol. 15, 581-590. https://doi.org/10.1038/nsmb.1438
  26. Tam, O. H., Aravin, A. A., Stein, P., Girard, A., Murchison, E. P., Cheloufi, S., Hodges, E., Anger, M., Sachidanandam, R., Schultz, R. M. and Hannon, G. J. (2008) Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453, 534-538. https://doi.org/10.1038/nature06904
  27. Watanabe, T., Totoki, Y., Toyoda, A., Kaneda, M., Kuramochi-Miyagawa, S., Obata, Y., Chiba, H., Kohara, Y., Kono, T., Nakano, T., Surani, M. A., Sakaki, Y. and Sasaki, H. (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453, 539-543. https://doi.org/10.1038/nature06908
  28. Ketting, R. F., Haverkamp, T. H. A., van Luenen, H. G. A. M. and Plasterk, R. H. A. (1999) mut-7 of C. elegans, Required for Transposon Silencing and RNA Interference, Is a Homolog of Werner Syndrome Helicase and RNaseD. Cell 99, 133-141. https://doi.org/10.1016/S0092-8674(00)81645-1
  29. Tabara, H., Sarkissian, M., Kelly, W. G., Fleenor, J., Grishok, A., Timmons, L., Fire, A. and Mello, C. C. (1999) The rde-1 Gene, RNA Interference, and Transposon Silencing in C. elegans. Cell 99, 123-132. https://doi.org/10.1016/S0092-8674(00)81644-X
  30. Chung, W., Okamura, K., Martin, R. and Lai, E. C. (2008) Endogenous RNA Interference Provides a Somatic Defense against Drosophila Transposons. Current Biology 18, 795-802. https://doi.org/10.1016/j.cub.2008.05.006
  31. Ghildiyal, M., Seitz, H., Horwich, M. D., Li, C., Du, T., Lee, S., Xu, J., Kittler, E. L. W., Zapp, M. L., Weng, Z. and Zamore, P. D. (2008) Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 320, 1077-1081. https://doi.org/10.1126/science.1157396
  32. Hammond, S. M., Bernstein, E., Beach, D. and Hannon, G. J. (2000) An RNA-directed nuclease mediates posttranscriptional gene silencing in Drosophila cells. Nature 404, 293-296. https://doi.org/10.1038/35005107
  33. Zamore, P. D., Tuschl, T., Sharp, P. A. and Bartel, D. P. (2000) RNAi: Double-Stranded RNA Directs the ATPDependent Cleavage of mRNA at 21 to 23 Nucleotide Intervals. Cell 101, 25-33. https://doi.org/10.1016/S0092-8674(00)80620-0
  34. Pak, J. and Fire, A. (2007) Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 315, 241-244. https://doi.org/10.1126/science.1132839
  35. Sijen, T., Steiner, F. A., Thijssen, K. L. and Plasterk, R. H. A. (2007) Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science 2007, 315, 244-247. https://doi.org/10.1126/science.1136699
  36. Sijen, T., Fleenor, J., Simmer, F., Thijssen, K. L., Parrish, S., Timmons, L., Plasterk, R. H. and Fire, A. (2001) On the Role of RNA Amplification in dsRNA-Triggered Gene Silencing. Cell 107, 465-476. https://doi.org/10.1016/S0092-8674(01)00576-1
  37. Brennecke, J., Aravin, A. A., Stark, A., Dus, M., Kellis, M., Sachidanandam, R. and Hannon, G. J. (2007) Discrete Small RNA-Generating Loci as Master Regulators of Transposon Activity in Drosophila. Cell 128, 1089-1103. https://doi.org/10.1016/j.cell.2007.01.043
  38. Hunter, C. P., Winston, W. M., Molodowitch, C., Feinberg, E. H., Shih, J., Sutherlin, M., Wright, A. J. and Fitzgerald, M. C. (2006) Systemic RNAi in Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 71, 95-100. https://doi.org/10.1101/sqb.2006.71.060
  39. Gottesman, S. (2005) Micros for microbes: non-coding regulatory RNAs in bacteria. Trends in Genetics 21, 399-404. https://doi.org/10.1016/j.tig.2005.05.008
  40. Aiba, H. (2007) Mechanism of RNA silencing by Hfq-binding small RNAs. Current Opinion in Microbiology 10, 134-139. https://doi.org/10.1016/j.mib.2007.03.010
  41. Gottesman, S., McCullen, C. A., Guillier, M., Vanderpool, C. K., Majdalani, N., Benhammou, J., Thompson, K. M., FitzGerald, P. C., Sowa, N. A. and FitzGerald, D. J. (2006) Small RNA regulators and the bacterial response to stress. Cold Spring Harb. Symp. Quant. Biol. 71, 1-11. https://doi.org/10.1101/sqb.2006.71.016
  42. Geissmann, T., Possedko, M., Huntzinger, E., Fechter, P., Ehresmann, C. and Romby, P. (2006) Regulatory RNAs as mediators of virulence gene expression in bacteria. Handb Exp. Pharmacol. 173, 9-43. https://doi.org/10.1007/3-540-27262-3_2
  43. Murphy, E. R. and Payne, S. M. (2007) RyhB, an iron-responsive small RNA molecule, regulates Shigella dysenteriae virulence. Infect. Immun. 75, 3470-3477. https://doi.org/10.1128/IAI.00112-07
  44. Padalon-Brauch, G., Hershberg, R., Elgrably-Weiss, M., Baruch, K., Rosenshine, I., Margalit, H. and Altuvia, S. (2008) Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic. Acids. Res. 36, 1913-1927. https://doi.org/10.1093/nar/gkn050
  45. Schiano, C. A., Bellows, L. E. and Lathem, W. W. (2010) The small RNA chaperone Hfq is required for the virulence of Yersinia pseudotuberculosis. Infect. Immun. 78, 2034-2044. https://doi.org/10.1128/IAI.01046-09
  46. Chabelskaya, S., Gaillot, O. and Felden, B. (2010) A Staphylococcus aureus small RNA is required for bacterial virulence and regulates the expression of an immune-evasion molecule. PLoS Pathog. 6, e1000927. https://doi.org/10.1371/journal.ppat.1000927
  47. Podkaminski, D. and Vogel, J. (2010) Small RNAs promote mRNA stability to activate the synthesis of virulence factors. Mol. Microbiol. 78, 1327-1331. https://doi.org/10.1111/j.1365-2958.2010.07428.x
  48. Hammond, S. M., Bernstein, E., Beach, D. and Hannon, G. J. (2000) An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404, 293-296. https://doi.org/10.1038/35005107
  49. Hutvagner, G. and Zamore, P. D. (2002) A microRNA in a multiple-turnover RNAi enzyme complex. Science 297, 2056-2060. https://doi.org/10.1126/science.1073827
  50. Liu, J., Carmell, M. A., Rivas, F. V., Marsden, C. G, Thomson, J. M., Song, J., Hammond, S. M., Joshua-Tor, L. and Hannon, G. J. (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305, 1437-1441. https://doi.org/10.1126/science.1102513
  51. Haley, B. and Zamore, P. D. (2004) Kinetic analysis of the RNAi enzyme complex. Nat. Struct. Mol. Biol. 11, 599-606. https://doi.org/10.1038/nsmb780
  52. Arvey, A., Larsson, E., Sander, C., Leslie, C. S. and Marks, D. S. (2010) Target mRNA abundance dilutes microRNA and siRNA activity. Mol. Syst. Biol. 6, 363.
  53. Masse, E., Escorcia, F. E. and Gottesman, S. (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev. 17, 2374-2383. https://doi.org/10.1101/gad.1127103
  54. Figueroa-Bossi, N., Valentini, M., Malleret, L. and Bossi, L. (2009) Caught at its own game: regulatory small RNA inactivated by an inducible transcript mimicking its target. Genes & Development 23, 2004 -2015. https://doi.org/10.1101/gad.541609
  55. Levine, E., Zhang, Z., Kuhlman, T. and Hwa, T. (2007) Quantitative characteristics of gene regulation by small RNA. PLoS Biol. 5, e229. https://doi.org/10.1371/journal.pbio.0050229
  56. Mitarai, N., Andersson, A. M., Krishna, S., Semsey, S. and Sneppen, K. (2007) Efficient degradation and expression prioritization with small RNAs. Phys. Biol. 4, 164-171. https://doi.org/10.1088/1478-3975/4/3/003
  57. Shimoni, Y., Friedlander, G., Hetzroni, G., Niv, G., Altuvia, S., Biham, O. and Margalit, H. (2007) Regulation of gene expression by small non-coding RNAs: a quantitative view. Mol. Syst. Biol. 3, 138.
  58. Mehta, P., Goyal, S. and Wingreen, N. S. (2008) A quantitative comparison of sRNA-based and protein-based gene regulation. Mol. Syst. Biol. 4, 221.
  59. Levine, E., Huang, M., Huang, Y., Kuhlman, T., Zhang, Z. and Hwa, T. On noise and silence in gene regulation by small RNA. In submission.
  60. Lease, R. A. and Belfort, M. (2000) A trans-acting RNA as a control switch in Escherichia coli: DsrA modulates function by forming alternative structures. Proc. Natl. Acad. Sci. U.S.A. 97, 9919-9924. https://doi.org/10.1073/pnas.170281497
  61. Fang, F. C. and Rimsky, S. (2008) New insights into transcriptional regulation by H-NS. Current Opinion in Microbiology. 11, 113-120. https://doi.org/10.1016/j.mib.2008.02.011
  62. Amit, R., Oppenheim, A. B. and Stavans, J. (2003) Increased Bending Rigidity of Single DNA Molecules by H-NS, a Temperature and Osmolarity Sensor. Biophysical Journal 84, 2467-2473. https://doi.org/10.1016/S0006-3495(03)75051-6
  63. Dorman, C. J. (2007) H-NS, the genome sentinel. Nat. Rev. Micro. 5, 157-161. https://doi.org/10.1038/nrmicro1598
  64. Majdalani, N., Cunning, C., Sledjeski, D., Elliott, T. and Gottesman, S. (1998) DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proc. Natl. Acad. Sci. U.S.A. 95, 12462-12467. https://doi.org/10.1073/pnas.95.21.12462
  65. Zhang, A., Altuvia, S., Tiwari, A., Argaman, L., Hengge-Aronis, R. and Storz, G. (1998) The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J. 17, 6061-6068. https://doi.org/10.1093/emboj/17.20.6061
  66. Basineni, S. R., Madhugiri, R., Kolmsee, T., Hengge, R. and Klug, G. (2009) The influence of Hfq and ribonucleases on the stability of the small non-coding RNA OxyS and its target rpoS in E. coli is growth phase dependent. RNA Biol. 6, 584-594. https://doi.org/10.4161/rna.6.5.10082
  67. Repoila, F., Majdalani, N. and Gottesman, S. (2003) Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm. Mol. Microbiol 48, 855-861. https://doi.org/10.1046/j.1365-2958.2003.03454.x
  68. Madhugiri, R., Basineni, S. R. and Klug, G. (2010) Turnover of the small non-coding RNA RprA in E. coli is influenced by osmolarity. Mol. Genet. Genomics. 284, 307-318. https://doi.org/10.1007/s00438-010-0568-x
  69. Repoila, F. and Gottesman, S. (2001) Signal Transduction Cascade for Regulation of RpoS: Temperature Regulation of DsrA. J. Bacteriol. 183, 4012-4023. https://doi.org/10.1128/JB.183.13.4012-4023.2001
  70. Repoila, F. and Gottesman, S. (2003) Temperature Sensing by the dsrA Promoter. J. Bacteriol. 185, 6609-6614. https://doi.org/10.1128/JB.185.22.6609-6614.2003
  71. Lenz, D., Mok, K., Lilley, B., Kulkarni, R., Wingreen, N. and Bassler, B. (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118, 69-82. https://doi.org/10.1016/j.cell.2004.06.009
  72. Tu, K. C. and Bassler, B. L. (2007) Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi. Genes Dev. 21, 221-233. https://doi.org/10.1101/gad.1502407
  73. Svenningsen, S. L., Tu, K. C. and Bassler, B. L. (2009) Gene dosage compensation calibrates four regulatory RNAs to control Vibrio cholerae quorum sensing. EMBO J. 28, 429-439. https://doi.org/10.1038/emboj.2008.300
  74. Long, T., Tu, K. C., Wang, Y., Mehta, P., Ong, N. P., Bassler, B. L. and Wingreen, N. S. (2009) Quantifying the integration of quorum-sensing signals with single-cell resolution. PLoS Biol. 7, e68. https://doi.org/10.1371/journal.pbio.1000068
  75. Thomas, M., Lieberman, J. and Lal, A. (2010) Desperately seeking microRNA targets. Nat. Struct. Mol. Biol. 17, 1169-1174. https://doi.org/10.1038/nsmb.1921
  76. Baek, D., Villén, J., Shin, C., Camargo, F. D., Gygi, S. P. and Bartel, D. P. (2008) The impact of microRNAs on protein output. Nature 455, 64-71. https://doi.org/10.1038/nature07242
  77. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R. and Rajewsky, N. (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58-63. https://doi.org/10.1038/nature07228
  78. Stark, A., Brennecke, J., Bushati, N., Russell, R. B. and Cohen, S. M. (2005) Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3'UTR evolution. Cell 123, 1133-1146. https://doi.org/10.1016/j.cell.2005.11.023
  79. Jan, C. H., Friedman, R. C., Ruby, J. G. and Bartel, D. P. (2010) Formation, regulation and evolution of Caenorhabditis elegans 3'UTRs. Nature doi:10.1038/nature09616.
  80. Overgaard, M., Johansen, J., Moller-Jensen, J. and Valentin-Hansen, P. (2009) Switching off small RNA regulation with trap-mRNA. Mol. Microbiol. 73, 790-800. https://doi.org/10.1111/j.1365-2958.2009.06807.x
  81. Plumbridge, J. and Pellegrini, O. (2004) Expression of the chitobiose operon of Escherichia coli is regulated by three transcription factors: NagC, ChbR and CAP. Mol. Microbiol. 52, 437-449. https://doi.org/10.1111/j.1365-2958.2004.03986.x
  82. Nowojewski, A. and Levine, E. Manuscript in preparation.
  83. Masse, E. and Gottesman, S. (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 99, 4620-4625. https://doi.org/10.1073/pnas.032066599
  84. Mey, A. R., Craig, S. A. and Payne, S. M. (2005) Characterization of Vibrio cholerae RyhB: the RyhB regulon and role of RyhB in biofilm formation. Infect. Immun. 73, 5706-5719. https://doi.org/10.1128/IAI.73.9.5706-5719.2005
  85. Masse, E., Vanderpool, C. K. and Gottesman, S. (2005) Effect of RyhB small RNA on global iron use in Escherichia coli. J. Bacteriol. 187, 6962-6971. https://doi.org/10.1128/JB.187.20.6962-6971.2005
  86. Jacques, J., Jang, S., Prevost, K., Desnoyers, G., Desmarais, M., Imlay, J. and Masse, E. (2006) RyhB small RNA modulates the free intracellular iron pool and is essential for normal growth during iron limitation in Escherichia coli. Mol. Microbiol. 62, 1181-1190. https://doi.org/10.1111/j.1365-2958.2006.05439.x
  87. Wyckoff, E. E., Mey, A. R. and Payne, S. M. (2007) Iron acquisition in Vibrio cholerae. Biometals 20, 405-416. https://doi.org/10.1007/s10534-006-9073-4
  88. Prevost, K., Salvail, H., Desnoyers, G., Jacques, J., Phaneuf, E. and Masse, E. (2007) The small RNA RyhB activates the translation of shiA mRNA encoding a permease of shikimate, a compound involved in siderophore synthesis. Mol. Microbiol. 64, 1260-1273. https://doi.org/10.1111/j.1365-2958.2007.05733.x
  89. Vecerek, B., Moll, I. and Blasi, U. (2007) Control of Fur synthesis by the non-coding RNA RyhB and iron-responsive decoding. EMBO J. 26, 965-975. https://doi.org/10.1038/sj.emboj.7601553
  90. Semsey, S., Andersson, A. M. C., Krishna, S., Jensen, M. H., Masse, E. and Sneppen, K. (2006) Genetic regulation of fluxes: iron homeostasis of Escherichia coli. Nucleic. Acids. Res. 34, 4960-4967. https://doi.org/10.1093/nar/gkl627
  91. Andrews, S. C., Robinson, A. K. and Rodriguez-Quinones, F. (2003) Bacterial iron homeostasis. FEMS Microbiol. Rev. 27, 215-237. https://doi.org/10.1016/S0168-6445(03)00055-X
  92. Ambros, V. (1989) A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans. Cell 57, 49-57. https://doi.org/10.1016/0092-8674(89)90171-2
  93. Slack, F. J., Basson, M., Liu, Z., Ambros, V., Horvitz, H. R. and Ruvkun, G. (2000) The lin-41 RBCC gene acts in the C. elegans heterochronic pathway between the let-7 regulatory RNA and the LIN-29 transcription factor. Mol. Cell 5, 659-669. https://doi.org/10.1016/S1097-2765(00)80245-2
  94. Ketting, R. F., Fischer, S. E., Bernstein, E., Sijen, T., Hannon, G. J. and Plasterk, R. H. (2001) Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes & Development 15, 2654-2659. https://doi.org/10.1101/gad.927801
  95. Grishok, A., Pasquinelli, A. E., Conte, D., Li, N., Parrish, S., Ha, I., Baillie, D. L., Fire, A., Ruvkun, G. and Mello, C. C. (2001) Genes and Mechanisms Related to RNA Interference Regulate Expression of the Small Temporal RNAs that Control C. elegans Developmental Timing. Cell 106, 23-34. https://doi.org/10.1016/S0092-8674(01)00431-7
  96. Lee, Y. S., Nakahara, K., Pham, J. W., Kim, K., He, Z., Sontheimer, E. J. and Carthew, R. W. (2004) Distinct Roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA Silencing Pathways. Cell 117, 69-81. https://doi.org/10.1016/S0092-8674(04)00261-2
  97. Tolia, N. H. and Joshua-Tor, L. (2007) Slicer and the Argonautes. Nat. Chem. Biol. 3, 36-43. https://doi.org/10.1038/nchembio848
  98. Jackson, A. L. and Linsley, P. S. (2010) Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application. Nat. Rev. Drug Discov. 9, 57-67. https://doi.org/10.1038/nrd3010
  99. Jackson, A. L., Bartz, S. R., Schelter, J., Kobayashi, S. V., Burchard, J., Mao, M., Li, B., Cavet, G. and Linsley, P. S. (2003) Expression profiling reveals off-target gene regulation by RNAi. Nat. Biotechnol 21, 635-637. https://doi.org/10.1038/nbt831
  100. Yi, R., Doehle, B. P., Qin, Y., Macara, I. G. and Cullen, B. R. (2005) Overexpression of Exportin 5 enhances RNA interference mediated by short hairpin RNAs and microRNAs. RNA 11, 220-226. https://doi.org/10.1261/rna.7233305
  101. Grimm, D., Streetz, K. L., Jopling, C. L., Storm, T. A., Pandey, K., Davis, C. R., Marion, P., Salazar, F. and Kay, M. A. (2006) Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441, 537-541. https://doi.org/10.1038/nature04791
  102. Khan, A. A., Betel, D., Miller, M. L., Sander, C., Leslie, C. S. and Marks, D. S. (2009) Transfection of small RNAs globally perturbs gene regulation by endogenous microRNAs. Nat. Biotech. 27, 549-555. https://doi.org/10.1038/nbt.1543
  103. Larsson, E., Sander, C. and Marks, D. (2010) mRNA turnover rate limits siRNA and microRNA efficacy. Mol. Syst. Biol. 6, 433.
  104. Sittka, A., Lucchini, S., Papenfort, K., Sharma, C. M., Rolle, K., Binnewies, T. T., Hinton, J. C. D. and Vogel, J. (2008) Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet. 4, e1000163. https://doi.org/10.1371/journal.pgen.1000163
  105. Jousselin, A., Metzinger, L. and Felden, B. (2009) On the facultative requirement of the bacterial RNA chaperone, Hfq. Trends. Microbiol. 17, 399-405. https://doi.org/10.1016/j.tim.2009.06.003
  106. Le Derout, J., Boni, I. V., Regnier, P. and Hajnsdorf, E. (2010) Hfq affects mRNA levels independently of degradation. BMC Mol. Biol. 11, 17. https://doi.org/10.1186/1471-2199-11-17
  107. Valentin-Hansen, P., Eriksen, M. and Udesen, C. (2004) The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol. Microbiol. 51, 1525-1533. https://doi.org/10.1111/j.1365-2958.2003.03935.x
  108. Taniguchi, Y., Choi, P. J., Li, G., Chen, H., Babu, M., Hearn, J., Emili, A. and Xie, X. S. (2010) Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329, 533-538. https://doi.org/10.1126/science.1188308
  109. Hussein, R. and Lim, H. N. (2010) Disruption of small RNA signaling caused by competition for Hfq. Proc. Natl. Acad. Sci. U.S.A. doi:10.1073/pnas.1010082108.
  110. Ebert, M. S. and Sharp, P. A. (2010) MicroRNA sponges: Progress and possibilities. RNA 16, 2043-2050. https://doi.org/10.1261/rna.2414110

Cited by

  1. HrpA, a DEAH-Box RNA Helicase, Is Involved in Global Gene Regulation in the Lyme Disease Spirochete vol.6, pp.7, 2011, https://doi.org/10.1371/journal.pone.0022168
  2. Chemically controlled unfolding of a RNA-like polymer model vol.86, pp.4, 2012, https://doi.org/10.1103/PhysRevE.86.041913
  3. Large-scale mapping of sequence-function relations in small regulatory RNAs reveals plasticity and modularity vol.42, pp.19, 2014, https://doi.org/10.1093/nar/gku863
  4. Quantification of the gene silencing performances of rationally-designed synthetic small RNAs vol.9, pp.3, 2015, https://doi.org/10.1007/s11693-015-9177-7
  5. Competing endogenous RNAs: a target-centric view of small RNA regulation in bacteria vol.14, pp.12, 2016, https://doi.org/10.1038/nrmicro.2016.129
  6. Identification and analysis of microRNAs in the left ventricular myocardium of two-kidney one-clip hypertensive rats vol.8, pp.2, 2013, https://doi.org/10.3892/mmr.2013.1549
  7. HDAC3 acts as a negative regulator of angiogenesis vol.47, pp.4, 2014, https://doi.org/10.5483/BMBRep.2014.47.4.128
  8. miR-15b induced by platelet-derived growth factor signaling is required for vascular smooth muscle cell proliferation vol.46, pp.11, 2013, https://doi.org/10.5483/BMBRep.2013.46.11.057
  9. Experimental measurements and mathematical modeling of biological noise arising from transcriptional and translational regulation of basic synthetic gene circuits vol.395, 2016, https://doi.org/10.1016/j.jtbi.2016.02.004
  10. Sub-cellular mRNA localization modulates the regulation of gene expression by small RNAs in bacteria vol.14, pp.5, 2017, https://doi.org/10.1088/1478-3975/aa69ac
  11. Body fluid identification in forensics vol.45, pp.10, 2012, https://doi.org/10.5483/BMBRep.2012.45.10.206
  12. A systems view of the protein expression process vol.5, pp.3-4, 2011, https://doi.org/10.1007/s11693-011-9088-1
  13. Transcript degradation and noise of small RNA-controlled genes in a switch activated network inEscherichia coli vol.44, pp.14, 2016, https://doi.org/10.1093/nar/gkw273
  14. mRNA and miRNA expression patterns associated to pathways linked to metal mixture health effects vol.533, pp.2, 2014, https://doi.org/10.1016/j.gene.2013.09.049
  15. Regulating the Many to Benefit the Few: Role of Weak Small RNA Targets vol.104, pp.8, 2013, https://doi.org/10.1016/j.bpj.2013.02.020
  16. Quantitative effect of target translation on small RNA efficacy reveals a novel mode of interaction vol.42, pp.19, 2014, https://doi.org/10.1093/nar/gku889
  17. CSM Murray Award Lecture — Functional studies of the Lyme disease spirochete — from molecules to mice11This article is based on a presentation by Dr. George Chaconas at the 61st Annual Meeting of the Canadian Society of Microbiologists in St. John’s, Newfoundland, on 20 June 2011. Dr. Chaconas was the recipient of the CSM Murray Award for Career Achievement. vol.58, pp.3, 2012, https://doi.org/10.1139/w11-143
  18. Misfolded human tRNA isodecoder binds and neutralizes a 3' UTR-embedded Alu element vol.108, pp.40, 2011, https://doi.org/10.1073/pnas.1103698108
  19. Stochastic modeling of regulation of gene expression by multiple small RNAs vol.85, pp.6, 2012, https://doi.org/10.1103/PhysRevE.85.061915
  20. RNA pseudo-knots simulated with a one-bead coarse-grained model vol.140, pp.11, 2014, https://doi.org/10.1063/1.4868650
  21. Metatranscriptomic Analysis of Microbes in an Oceanfront Deep-Subsurface Hot Spring Reveals Novel Small RNAs and Type-Specific tRNA Degradation vol.78, pp.4, 2011, https://doi.org/10.1128/AEM.06811-11
  22. QsRNA-seq: a method for high-throughput profiling and quantifying small RNAs vol.19, pp.1, 2018, https://doi.org/10.1186/s13059-018-1495-0