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Frequency-modulated nuclear localization bursts coordinate gene regulation

Author

Listed:
  • Long Cai

    (Howard Hughes Medical Institute, California Institute of Technology, M/C 114-96, Pasadena, California 91125, USA)

  • Chiraj K. Dalal

    (Howard Hughes Medical Institute, California Institute of Technology, M/C 114-96, Pasadena, California 91125, USA)

  • Michael B. Elowitz

    (Howard Hughes Medical Institute, California Institute of Technology, M/C 114-96, Pasadena, California 91125, USA)

Abstract

In yeast, the transcription factor Crz1 is dephosphorylated and translocates into the nucleus in response to extracellular calcium. Here we show, using time-lapse microscopy, that Crz1 exhibits short bursts of nuclear localization (typically lasting 2 min) that occur stochastically in individual cells and propagate to the expression of downstream genes. Strikingly, calcium concentration controls the frequency, but not the duration, of localization bursts. Using an analytic model, we also show that this frequency modulation of bursts ensures proportional expression of multiple target genes across a wide dynamic range of expression levels, independent of promoter characteristics. We experimentally confirm this theory with natural and synthetic Crz1 target promoters. Another stress-response transcription factor, Msn2, exhibits similar, but largely uncorrelated, localization bursts under calcium stress suggesting that frequency-modulation regulation of localization bursts may be a general control strategy used by the cell to coordinate multi-gene responses to external signals.

Suggested Citation

  • Long Cai & Chiraj K. Dalal & Michael B. Elowitz, 2008. "Frequency-modulated nuclear localization bursts coordinate gene regulation," Nature, Nature, vol. 455(7212), pages 485-490, September.
    • Handle: RePEc:nat:nature:v:455:y:2008:i:7212:d:10.1038_nature07292
    DOI: 10.1038/nature07292
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    Cited by:

    1. Vera Bettenworth & Simon Vliet & Bartosz Turkowyd & Annika Bamberger & Heiko Wendt & Matthew McIntosh & Wieland Steinchen & Ulrike Endesfelder & Anke Becker, 2022. "Frequency modulation of a bacterial quorum sensing response," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. Gabriele Micali & Gerardo Aquino & David M Richards & Robert G Endres, 2015. "Accurate Encoding and Decoding by Single Cells: Amplitude Versus Frequency Modulation," PLOS Computational Biology, Public Library of Science, vol. 11(6), pages 1-21, June.
    3. Marc Weber & Javier Buceta, 2013. "Stochastic Stabilization of Phenotypic States: The Genetic Bistable Switch as a Case Study," PLOS ONE, Public Library of Science, vol. 8(9), pages 1-8, September.
    4. C Caranica & A Al-Omari & Z Deng & J Griffith & R Nilsen & L Mao & J Arnold & H-B Schüttler, 2018. "Ensemble methods for stochastic networks with special reference to the biological clock of Neurospora crassa," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-28, May.
    5. Andreas Doncic & Umut Eser & Oguzhan Atay & Jan M Skotheim, 2013. "An Algorithm to Automate Yeast Segmentation and Tracking," PLOS ONE, Public Library of Science, vol. 8(3), pages 1-11, March.
    6. Jing Kang & Bing Xu & Ye Yao & Wei Lin & Conor Hennessy & Peter Fraser & Jianfeng Feng, 2011. "A Dynamical Model Reveals Gene Co-Localizations in Nucleus," PLOS Computational Biology, Public Library of Science, vol. 7(7), pages 1-16, July.
    7. Joachim Almquist & Loubna Bendrioua & Caroline Beck Adiels & Mattias Goksör & Stefan Hohmann & Mats Jirstrand, 2015. "A Nonlinear Mixed Effects Approach for Modeling the Cell-To-Cell Variability of Mig1 Dynamics in Yeast," PLOS ONE, Public Library of Science, vol. 10(4), pages 1-32, April.
    8. Giorgos Minas & Dan J Woodcock & Louise Ashall & Claire V Harper & Michael R H White & David A Rand, 2020. "Multiplexing information flow through dynamic signalling systems," PLOS Computational Biology, Public Library of Science, vol. 16(8), pages 1-18, August.
    9. Ziya Kalay & Takahiro K Fujiwara & Akihiro Kusumi, 2012. "Confining Domains Lead to Reaction Bursts: Reaction Kinetics in the Plasma Membrane," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-8, March.

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