Limits on Information Transduction Through Amplitude and Frequency Regulation of Transcription Factor Activity

Overview

Journal Elife

Specialty Biology

Date 2015 May 19

PMID 25985085

Citations 60

Authors

Anders S Hansen

Erin K OShea

Affiliations

Soon will be listed here.

Abstract

Signaling pathways often transmit multiple signals through a single shared transcription factor (TF) and encode signal information by differentially regulating TF dynamics. However, signal information will be lost unless it can be reliably decoded by downstream genes. To understand the limits on dynamic information transduction, we apply information theory to quantify how much gene expression information the yeast TF Msn2 can transduce to target genes in the amplitude or frequency of its activation dynamics. We find that although the amount of information transmitted by Msn2 to single target genes is limited, information transduction can be increased by modulating promoter cis-elements or by integrating information from multiple genes. By correcting for extrinsic noise, we estimate an upper bound on information transduction. Overall, we find that information transduction through amplitude and frequency regulation of Msn2 is limited to error-free transduction of signal identity, but not signal intensity information.

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References

Lestas I, Vinnicombe G, Paulsson J . Fundamental limits on the suppression of molecular fluctuations. Nature. 2010; 467(7312):174-8. PMC: 2996232. DOI: 10.1038/nature09333. View

Ghaemmaghami S, Huh W, Bower K, Howson R, Belle A, Dephoure N . Global analysis of protein expression in yeast. Nature. 2003; 425(6959):737-41. DOI: 10.1038/nature02046. View

Imayoshi I, Isomura A, Harima Y, Kawaguchi K, Kori H, Miyachi H . Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science. 2013; 342(6163):1203-8. DOI: 10.1126/science.1242366. View

Zaman S, Lippman S, Schneper L, Slonim N, Broach J . Glucose regulates transcription in yeast through a network of signaling pathways. Mol Syst Biol. 2009; 5:245. PMC: 2657534. DOI: 10.1038/msb.2009.2. View

Behar M, Hoffmann A . Understanding the temporal codes of intra-cellular signals. Curr Opin Genet Dev. 2010; 20(6):684-93. PMC: 2982931. DOI: 10.1016/j.gde.2010.09.007. View

Waltermann C, Klipp E . Information theory based approaches to cellular signaling. Biochim Biophys Acta. 2011; 1810(10):924-32. DOI: 10.1016/j.bbagen.2011.07.009. View

de Nadal E, Ammerer G, Posas F . Controlling gene expression in response to stress. Nat Rev Genet. 2011; 12(12):833-45. DOI: 10.1038/nrg3055. View

Lahav G, Rosenfeld N, Sigal A, Geva-Zatorsky N, Levine A, Elowitz M . Dynamics of the p53-Mdm2 feedback loop in individual cells. Nat Genet. 2004; 36(2):147-50. DOI: 10.1038/ng1293. View

Hao N, Budnik B, Gunawardena J, OShea E . Tunable signal processing through modular control of transcription factor translocation. Science. 2013; 339(6118):460-4. PMC: 3746486. DOI: 10.1126/science.1227299. View

10.

Kremers G, Goedhart J, van Munster E, Gadella Jr T . Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Förster radius. Biochemistry. 2006; 45(21):6570-80. DOI: 10.1021/bi0516273. View

11.

Balaban N, Merrin J, Chait R, Kowalik L, Leibler S . Bacterial persistence as a phenotypic switch. Science. 2004; 305(5690):1622-5. DOI: 10.1126/science.1099390. View

12.

Tkacik G, Callan Jr C, Bialek W . Information flow and optimization in transcriptional regulation. Proc Natl Acad Sci U S A. 2008; 105(34):12265-70. PMC: 2527900. DOI: 10.1073/pnas.0806077105. View

13.

Selimkhanov J, Taylor B, Yao J, Pilko A, Albeck J, Hoffmann A . Systems biology. Accurate information transmission through dynamic biochemical signaling networks. Science. 2014; 346(6215):1370-3. PMC: 4813785. DOI: 10.1126/science.1254933. View

14.

Petrenko N, Chereji R, McClean M, Morozov A, Broach J . Noise and interlocking signaling pathways promote distinct transcription factor dynamics in response to different stresses. Mol Biol Cell. 2013; 24(12):2045-57. PMC: 3681706. DOI: 10.1091/mbc.E12-12-0870. View

15.

Mc Mahon S, Sim A, Filippi S, Johnson R, Liepe J, Smith D . Information theory and signal transduction systems: from molecular information processing to network inference. Semin Cell Dev Biol. 2014; 35:98-108. DOI: 10.1016/j.semcdb.2014.06.011. View

16.

Behar M, Dohlman H, Elston T . Kinetic insulation as an effective mechanism for achieving pathway specificity in intracellular signaling networks. Proc Natl Acad Sci U S A. 2007; 104(41):16146-51. PMC: 2042176. DOI: 10.1073/pnas.0703894104. View

17.

Uda S, Saito T, Kudo T, Kokaji T, Tsuchiya T, Kubota H . Robustness and compensation of information transmission of signaling pathways. Science. 2013; 341(6145):558-61. DOI: 10.1126/science.1234511. View

18.

Skerker J, Perchuk B, Siryaporn A, Lubin E, Ashenberg O, Goulian M . Rewiring the specificity of two-component signal transduction systems. Cell. 2008; 133(6):1043-54. PMC: 2453690. DOI: 10.1016/j.cell.2008.04.040. View

19.

Voliotis M, Perrett R, McWilliams C, McArdle C, Bowsher C . Information transfer by leaky, heterogeneous, protein kinase signaling systems. Proc Natl Acad Sci U S A. 2014; 111(3):E326-33. PMC: 3903221. DOI: 10.1073/pnas.1314446111. View

20.

Cheong R, Rhee A, Wang C, Nemenman I, Levchenko A . Information transduction capacity of noisy biochemical signaling networks. Science. 2011; 334(6054):354-8. PMC: 3895446. DOI: 10.1126/science.1204553. View