Multi-target regulation by small RNAs synchronizes gene expression thresholds and may enhance ultrasensitive behavior

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Schmiedel, Jörn Matthias ^a   Axmann, Ilka Maria ^a   Legewie, Stefan ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b INSTITUTE OF MOLECULAR BIOLOGY   (Armenia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; MESSENGER RNA; RNA; SMALL RNA; UNCLASSIFIED DRUG;

ARTICLE; GENE EXPRESSION; GENE FUNCTION; GENETIC LINKAGE; MATHEMATICAL ANALYSIS; MATHEMATICAL MODEL; MOLECULAR MECHANICS; REGULATORY MECHANISM; SINGLE INPUT MODULE; TRANSCRIPTION REGULATION; UNCERTAINTY;

FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; MODELS, GENETIC; RNA, MESSENGER; RNA, UNTRANSLATED; TRANSCRIPTION, GENETIC;

EID: 84865199642     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042296     Document Type: Article

References (57)

1. Aiba H, (2007) Mechanism of RNA silencing by Hfq-binding small RNAs. Curr Opin Microbiol 10: 134-139.
2. Gottesman S, (2005) Micros for microbes: non-coding regulatory RNAs in bacteria. Trends Genet 21: 399-404.
3. Masse E, Escorcia FE, Gottesman S, (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev 17: 2374-2383.
4. Hutvagner G, Zamore PD, (2002) A microRNA in a multiple-turnover RNAi enzyme complex. Science 297: 2056-2060.
5. Babitzke P, Baker CS, Romeo T, (2009) Regulation of translation initiation by RNA binding proteins. Annu Rev Microbiol 63: 27-44.
6. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W, (2006) Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125: 1111-1124.
7. Legewie S, Dienst D, Wilde A, Herzel H, Axmann IM, (2008) Small RNAs establish delays and temporal thresholds in gene expression. Biophys J 95: 3232-3238.
8. Levine E, Hwa T, (2008) Small RNAs establish gene expression thresholds. Curr Opin Microbiol 11: 574-579.
9. Levine E, Zhang Z, Kuhlman T, Hwa T, (2007) Quantitative characteristics of gene regulation by small RNA. PLoS Biol 5: e229.
10. Mehta P, Goyal S, Wingreen NS, (2008) A quantitative comparison of sRNA-based and protein-based gene regulation. Mol Syst Biol 4: 221.
11. Mitarai N, Andersson AM, Krishna S, Semsey S, Sneppen K, (2007) Efficient degradation and expression prioritization with small RNAs. Phys Biol 4: 164-171.
12. Mitarai N, Benjamin JA, Krishna S, Semsey S, Csiszovszki Z, et al. (2009) Dynamic features of gene expression control by small regulatory RNAs. Proc Natl Acad Sci U S A 106: 10655-10659.
13. Shimoni Y, Friedlander G, Hetzroni G, Niv G, Altuvia S, et al. (2007) Regulation of gene expression by small non-coding RNAs: a quantitative view. Mol Syst Biol 3: 138.
14. Zhdanov VP, (2011) Kinetic models of the interference of gene transcription to ncRNA and mRNA. Chaos 21: 023135.
15. Mukherji S, Ebert MS, Zheng GX, Tsang JS, Sharp PA, et al. (2011) MicroRNAs can generate thresholds in target gene expression. Nature Genetics 43: 854-859.
16. Beisel CL, Storz G, (2010) Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev 34: 866-882.
17. Maki K, Uno K, Morita T, Aiba H, (2008) RNA, but not protein partners, is directly responsible for translational silencing by a bacterial Hfq-binding small RNA. Proc Natl Acad Sci U S A 105: 10332-10337.
18. Morita T, Mochizuki Y, Aiba H, (2006) Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruction. Proc Natl Acad Sci U S A 103: 4858-4863.
19. Kawamoto H, Koide Y, Morita T, Aiba H, (2006) Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol Microbiol 61: 1013-1022.
20. Argaman L, Altuvia S, (2000) fhlA repression by OxyS RNA: kissing complex formation at two sites results in a stable antisense-target RNA complex. J Mol Biol 300: 1101-1112.
21. Brantl S, (2007) Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr Opin Microbiol 10: 102-109.
22. Waters LS, Storz G, (2009) Regulatory RNAs in bacteria. Cell 136: 615-628.
23. Soper TJ, Woodson SA, (2008) The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 14: 1907-1917.
24. Fender A, Elf J, Hampel K, Zimmermann B, Wagner EG, (2010) RNAs actively cycle on the Sm-like protein Hfq. Genes Dev 24: 2621-2626.
25. Dühring U, Axmann IM, Hess WR, Wilde A, (2006) An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc Natl Acad Sci U S A 103: 7054-7058.
26. Papenfort K, Vogel J, (2009) Multiple target regulation by small noncoding RNAs rewires gene expression at the post-transcriptional level. Res Microbiol 160: 278-287.
27. Lease RA, Cusick ME, Belfort M, (1998) Riboregulation in Escherichia coli: DsrA RNA acts by RNA:RNA interactions at multiple loci. Proc Natl Acad Sci U S A 95: 12456-12461.
28. Masse E, Vanderpool CK, Gottesman S, (2005) Effect of RyhB small RNA on global iron use in Escherichia coli. J Bacteriol 187: 6962-6971.
29. Beisel CL, Storz G, (2011) The base-pairing RNA spot 42 participates in a multioutput feedforward loop to help enact catabolite repression in Escherichia coli. Mol Cell 41: 286-297.
30. Papenfort K, Bouvier M, Mika F, Sharma CM, Vogel J, (2010) Evidence for an autonomous 5′ target recognition domain in an Hfq-associated small RNA. Proc Natl Acad Sci U S A 107: 20435-20440.
31. Sharma CM, Darfeuille F, Plantinga TH, Vogel J, (2007) A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites. Genes Dev 21: 2804-2817.
32. Gogol EB, Rhodius VA, Papenfort K, Vogel J, Gross CA, (2011) Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon. Proc Natl Acad Sci U S A 108: 12875-12880.
33. Zhdanov VP, (2011) Kinetic models of gene expression including non-coding RNAs. Physics Reports-Review Section of Physics Letters 500: 1-42.
34. Zhdanov VP, (2009) Conditions of appreciable influence of microRNA on a large number of target mRNAs. Molecular bioSystems 5: 638-643.
35. Niehrs C, Pollet N, (1999) Synexpression groups in eukaryotes. Nature 402: 483-487.
36. Gurdon JB, Dyson S, St Johnston D, (1998) Cells' perception of position in a concentration gradient. Cell 95: 159-162.
37. Hogan DJ, Riordan DP, Gerber AP, Herschlag D, Brown PO, (2008) Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol 6: e255.
38. Kollmann M, Lovdok L, Bartholome K, Timmer J, Sourjik V, (2005) Design principles of a bacterial signalling network. Nature 438: 504-507.
39. Lovdok L, Bentele K, Vladimirov N, Muller A, Pop FS, et al. (2009) Role of translational coupling in robustness of bacterial chemotaxis pathway. PLoS Biol 7: e1000171.
40. Zaslaver A, Mayo AE, Rosenberg R, Bashkin P, Sberro H, et al. (2004) Just-in-time transcription program in metabolic pathways. Nat Genet 36: 486-491.
41. Legewie S, Herzel H, Westerhoff HV, Bluthgen N, (2008) Recurrent design patterns in the feedback regulation of the mammalian signalling network. Mol Syst Biol 4: 190.
42. Alon U, (2007) Network motifs: theory and experimental approaches. Nature reviews Genetics 8: 450-461.
43. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP, (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146: 353-358.
44. Hao Y, Zhang ZJ, Erickson DW, Huang M, Huang Y, et al. (2011) Quantifying the sequence-function relation in gene silencing by bacterial small RNAs. Proceedings of the National Academy of Sciences of the United States of America 108: 12473-12478.
45. Mather WH, Cookson NA, Hasty J, Tsimring LS, Williams RJ, (2010) Correlation resonance generated by coupled enzymatic processing. Biophysical journal 99: 3172-3181.
46. Santos SD, Ferrell JE, (2008) Systems biology: On the cell cycle and its switches. Nature 454: 288-289.
47. Bluthgen N, Bruggeman FJ, Legewie S, Herzel H, Westerhoff HV, et al. (2006) Effects of sequestration on signal transduction cascades. The FEBS journal 273: 895-906.
48. Legewie S, Bluthgen N, Herzel H, (2006) Mathematical modeling identifies inhibitors of apoptosis as mediators of positive feedback and bistability. PLoS computational biology 2: e120.
49. Legewie S, Schoeberl B, Bluthgen N, Herzel H, (2007) Competing docking interactions can bring about bistability in the MAPK cascade. Biophysical journal 93: 2279-2288.
50. Ventura AC, Jiang P, Van Wassenhove L, Del Vecchio D, Merajver SD, et al. (2010) Signaling properties of a covalent modification cycle are altered by a downstream target. Proceedings of the National Academy of Sciences of the United States of America 107: 10032-10037.
51. Salazar C, Hofer T, (2009) Multisite protein phosphorylation-from molecular mechanisms to kinetic models. The FEBS journal 276: 3177-3198.
52. Markevich NI, Hoek JB, Kholodenko BN, (2004) Signaling switches and bistability arising from multisite phosphorylation in protein kinase cascades. The Journal of cell biology 164: 353-359.
53. Becskei A, Serrano L, (2000) Engineering stability in gene networks by autoregulation. Nature 405: 590-593.
54. Fritsche-Guenther R, Witzel F, Sieber A, Herr R, Schmidt N, et al. (2011) Strong negative feedback from Erk to Raf confers robustness to MAPK signalling. Molecular systems biology 7: 489.
55. Paulsen M, Legewie S, Eils R, Karaulanov E, Niehrs C, (2011) Negative feedback in the bone morphogenetic protein 4 (BMP4) synexpression group governs its dynamic signaling range and canalizes development. Proceedings of the National Academy of Sciences of the United States of America 108: 10202-10207.
56. Li X, Cassidy JJ, Reinke CA, Fischboeck S, Carthew RW, (2009) A microRNA imparts robustness against environmental fluctuation during development. Cell 137: 273-282.
57. Staton AA, Knaut H, Giraldez AJ, (2011) miRNA regulation of Sdf1 chemokine signaling provides genetic robustness to germ cell migration. Nature genetics 43: 204-211.