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Transcriptional Regulation Is a Major Controller of Cell Cycle Transition Dynamics

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  • Alessandro Romanel
  • Lars Juhl Jensen
  • Luca Cardelli
  • Attila Csikász-Nagy

Abstract

DNA replication, mitosis and mitotic exit are critical transitions of the cell cycle which normally occur only once per cycle. A universal control mechanism was proposed for the regulation of mitotic entry in which Cdk helps its own activation through two positive feedback loops. Recent discoveries in various organisms showed the importance of positive feedbacks in other transitions as well. Here we investigate if a universal control system with transcriptional regulation(s) and post-translational positive feedback(s) can be proposed for the regulation of all cell cycle transitions. Through computational modeling, we analyze the transition dynamics in all possible combinations of transcriptional and post-translational regulations. We find that some combinations lead to ‘sloppy’ transitions, while others give very precise control. The periodic transcriptional regulation through the activator or the inhibitor leads to radically different dynamics. Experimental evidence shows that in cell cycle transitions of organisms investigated for cell cycle dependent periodic transcription, only the inhibitor OR the activator is under cyclic control and never both of them. Based on these observations, we propose two transcriptional control modes of cell cycle regulation that either STOP or let the cycle GO in case of a transcriptional failure. We discuss the biological relevance of such differences.

Suggested Citation

  • Alessandro Romanel & Lars Juhl Jensen & Luca Cardelli & Attila Csikász-Nagy, 2012. "Transcriptional Regulation Is a Major Controller of Cell Cycle Transition Dynamics," PLOS ONE, Public Library of Science, vol. 7(1), pages 1-9, January.
  • Handle: RePEc:plo:pone00:0029716
    DOI: 10.1371/journal.pone.0029716
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    References listed on IDEAS

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    1. Jan M. Skotheim & Stefano Di Talia & Eric D. Siggia & Frederick R. Cross, 2008. "Positive feedback of G1 cyclins ensures coherent cell cycle entry," Nature, Nature, vol. 454(7202), pages 291-296, July.
    2. David A. Orlando & Charles Y. Lin & Allister Bernard & Jean Y. Wang & Joshua E. S. Socolar & Edwin S. Iversen & Alexander J. Hartemink & Steven B. Haase, 2008. "Global control of cell-cycle transcription by coupled CDK and network oscillators," Nature, Nature, vol. 453(7197), pages 944-947, June.
    3. Sandra López-Avilés & Orsolya Kapuy & Béla Novák & Frank Uhlmann, 2009. "Irreversibility of mitotic exit is the consequence of systems-level feedback," Nature, Nature, vol. 459(7246), pages 592-595, May.
    4. N. Barkai & S. Leibler, 1997. "Robustness in simple biochemical networks," Nature, Nature, vol. 387(6636), pages 913-917, June.
    5. Damien Coudreuse & Paul Nurse, 2010. "Driving the cell cycle with a minimal CDK control network," Nature, Nature, vol. 468(7327), pages 1074-1079, December.
    6. Erez Dekel & Uri Alon, 2005. "Optimality and evolutionary tuning of the expression level of a protein," Nature, Nature, vol. 436(7050), pages 588-592, July.
    7. Liam J. Holt & Andrew N. Krutchinsky & David O. Morgan, 2008. "Positive feedback sharpens the anaphase switch," Nature, Nature, vol. 454(7202), pages 353-357, July.
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