Distributed and dynamic intracellular organization of extracellular information

Alejandro Granados Castro, Julian M.J. Pietsch, Sarah A. Cepeda-Humerez, Iseabail Farquhar, Gašper Tkačik, Peter Swain

Research output: Contribution to journalArticlepeer-review

Abstract

Although cells respond specifically to environments, how environmental identity is encoded intracellularly is not understood. Here we study this organization of information in budding yeast by estimating the mutual information between environmental transitions and the dynamics of nuclear translocation for ten transcription factors. Our method of estimation is general, scalable, and based on decoding from single cells. The dynamics of the transcription factors are necessary to encode the highest amounts of extracellular information, and we show that information is transduced through two channels: generalists (Msn2/4, Tod6 and Dot6, Maf1, and Sfp1) can encode the nature of multiple stresses but only if stress is high; specialists (Hog1, Yap1, and Mig1/2) encode one particular stress, but do so more quickly and for a wider range of magnitudes. In particular, Dot6 encodes almost as much information as Msn2, the master regulator of the environmental stress response. Each transcription factor reports differently, and it is only their collective behavior that distinguishes between multiple environmental states. Changes in the dynamics of the localization of transcription factors thus constitute a precise, distributed internal representation of extracellular change. We predict that such multi-dimensional representations are common in cellular decision-making.
Original languageEnglish
Pages (from-to)6088-6093
Number of pages6
JournalProceedings of the National Academy of Sciences
Volume115
Issue number23
Early online date21 May 2018
DOIs
Publication statusPublished - 5 Jun 2018

Keywords

  • cell signaling
  • mutual information
  • time series
  • transcription factors
  • stress

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