Reuse & Permissions

It is not necessary to obtain permission to reuse this article or its components as it is available under the terms of the Creative Commons Attribution 4.0 International license. This license permits unrestricted use, distribution, and reproduction in any medium, provided attribution to the author(s) and the published article's title, journal citation, and DOI are maintained. Please note that some figures may have been included with permission from other third parties. It is your responsibility to obtain the proper permission from the rights holder directly for these figures.

Export citation

Export citation

Choose format for download:

Download Citation
  • Letter
  • Open Access

Buffering variability in cell regulation motifs close to criticality

Daniele Proverbio1,2,*, Arthur N. Montanari1, Alexander Skupin1,3,4, and Jorge Gonçalves1,5

  • 1Luxembourg Centre for Systems Biomedicine, University of Luxembourg, 6 Avenue du Swing, 4367, Belvaux, Luxembourg
  • 2College of Engineering, Mathematics and Physical Sciences, University of Exeter, EX4 4QL, Exeter, United Kingdom
  • 3Department of Physics and Material Science, University of Luxembourg, 162a Avenue de la Faiencerie, 1511 Luxembourg, Luxembourg
  • 4Department of Neuroscience, University of California San Diego, 9500 Gilman Drive, La Jolla, California, United States
  • 5Department of Plant Sciences, University of Cambridge, CB2 3EA, Cambridge, United Kingdom

  • *daniele.proverbio@uni.lu

Phys. Rev. E 106, L032402 – Published 12 September, 2022

DOI: https://doi.org/10.1103/PhysRevE.106.L032402

Abstract

Bistable biological regulatory systems need to cope with stochastic noise to fine tune their function close to bifurcation points. Here, we study stability properties of this regime in generic systems to demonstrate that cooperative interactions buffer system variability, hampering noise-induced regime shifts. Our analysis also shows that, in the considered cooperativity range, impending regime shifts can be generically detected by statistical early warning signals from distributional data. Our generic framework, based on minimal models, can be used to extract robustness and variability properties of more complex models and empirical data close to criticality.

View figure in article

Physics Subject Headings (PhySH)

Article Text

Supplemental Material

References (50)

  1. D. Angeli Jr., J. E. Ferrell, and E. D. Sontag, Proc. Natl. Acad. Sci. USA 101, 1822 (2004).
  2. M. Kheir Gouda, M. Manhart, and G. Balázsi, Proc. Natl. Acad. Sci. 116, 25162 (2019).
  3. J. B. Deris, M. Kim, Z. Zhang, H. Okano, R. Hermsen, A. Groisman, and T. Hwa, Science 342, 1237435 (2013).
  4. L. De Mot, D. Gonze, S. Bessonnard, C. Chazaud, A. Goldbeter, and G. Dupont, Biophys. J. 110, 710 (2016).
  5. M. Acar, A. Becskei, and A. Van Oudenaarden, Nature (London) 435, 228 (2005).
  6. M. T. Guinn, Y. Wan, S. Levovitz, D. Yang, M. R. Rosner, and G. Balázsi, Front. Genet. 11, 586726 (2020).
  7. S. Huang, Y.-P. Guo, G. May, and T. Enver, Dev. Biol. 305, 695 (2007).
  8. J. Fiorentino, M.-E. Torres-Padilla, and A. Scialdone, Annu. Rev. Genet. 54, 167 (2020).
  9. U. Alon, An Introduction to Systems Biology: Design Principles of Biological Circuits (Chapman and Hall/CRC, New York, 2019).
  10. S. Tripathi, D. A. Kessler, and H. Levine, Phys. Rev. Lett. 125, 088101 (2020).
  11. N. Komin and A. Skupin, Curr. Opin. Syst. Biol. 3, 154 (2017).
  12. M. Kærn, T. C. Elston, W. J. Blake, and J. J. Collins, Nat. Rev. Gen. 6, 451 (2005).
  13. M. Weber and J. Buceta, PLoS One 8, e73487 (2013).
  14. P. Thomas, N. Popović, and R. Grima, Proc. Natl. Acad. Sci. USA 111, 6994 (2014).
  15. R. Milo, S. Shen-Orr, S. Itzkovitz, N. Kashtan, D. Chklovskii, and U. Alon, Science 298, 824 (2002).
  16. E. M. Ozbudak, M. Thattai, H. N. Lim, B. I. Shraiman, and A. Van Oudenaarden, Nature (London) 427, 737 (2004).
  17. P. Ashwin, S. Wieczorek, R. Vitolo, and P. Cox, Philos. Trans. R. Soc., A 370, 1166 (2012).
  18. M. Scheffer, J. Bascompte, W. A. Brock, V. Brovkin, and S. R. e. a. Carpenter, Nature (London) 461, 53 (2009).
  19. T. Mora and W. Bialek, J. Stat. Phys. 144, 268 (2011).
  20. M. Mojtahedi, A. Skupin, J. Zhou, I. G. Castaño, R. Y. Leong-Quong, H. Chang, K. Trachana, A. Giuliani, and S. Huang, PLoS Biol. 14, e2000640 (2016).
  21. Y. Sharma, P. S. Dutta, and A. Gupta, Phys. Rev. E 93, 032404 (2016).
  22. J. Scholz, J. Kelso, and G. Schöner, Phys. Lett. A 123, 390 (1987).
  23. T. A. Byrd, A. Erez, R. M. Vogel, C. Peterson, M. Vennettilli, G. Altan-Bonnet, and A. Mugler, Phys. Rev. E 100, 022415 (2019).
  24. L. Dai, K. S. Korolev, and J. Gore, Proc. Natl. Acad. Sci. USA 112, 10056 (2015).
  25. V. Siciliano, I. Garzilli, C. Fracassi, S. Criscuolo, S. Ventre, and D. Di Bernardo, Nat. Commun. 4, 2364 (2013).
  26. I. Lestas, G. Vinnicombe, and J. Paulsson, Nature (London) 467, 174 (2010).
  27. D. Del Vecchio, A. J. Dy, and Y. Qian, J. R. Soc., Interface 13, 20160380 (2016).
  28. M. Santillán, Math. Model. Nat. Phenom. 3, 85 (2008).
  29. S. H. Strogatz, Nonlinear Dynamics and Chaos: With Applications to Physics, Biology, Chemistry, and Engineering (CRC Press, Boca Raton, 2018).
  30. D. Frigola, L. Casanellas, J. M. Sancho, and M. Ibañes, PLoS One 7, e31407 (2012).
  31. See Supplementary Material at http://link.aps.org/supplemental/10.1103/PhysRevE.106.L032402 for supplemental background, calculations and figures.
  32. P. Smolen, D. A. Baxter, and J. H. Byrne, Am. J. Physiol.: Cell Physiol. 274, C531 (1998).
  33. J. Hasty, J. Pradines, M. Dolnik, and J. J. Collins, Proc. Natl. Acad. Sci. USA 97, 2075 (2000).
  34. N. Berglund and B. Gentz, Noise-Induced Phenomena in Slow-Fast Dynamical Systems: A Sample-Paths Approach (Science & Business Media, Springer, 2006).
  35. N. Friedman, L. Cai, and X. S. Xie, Phys. Rev. Lett. 97, 168302 (2006).
  36. N. Kumar, T. Platini, and R. V. Kulkarni, Phys. Rev. Lett. 113, 268105 (2014).
  37. C. W. Gardiner, Handbook of Stochastic Methods (Springer, Boca Raton, 1985).
  38. C. Kuehn and C. Bick, Sci. Adv. 7, eabe3824 (2021).
  39. Y. A. Kuznetsov, Elements of Applied Bifurcation Theory, Vol. 112 (Springer Science & Business Media, Springer, 2004).
  40. C. Kuehn, Physica D 240, 1020 (2011).
  41. C. Trefois, P. M. Antony, J. Goncalves, A. Skupin, and R. Balling, Curr. Opin. Biotechnol. 34, 48 (2015).
  42. J. R. Taylor, An Introduction to Error Analysis (University Science Books, Mill Valley, California, 1997).
  43. D. Proverbio, F. Kemp, S. Magni, and J. Gonçalves, PLoS Comput. Biol. 18, e1009958 (2022).
  44. C. Boettiger and A. Hastings, Proc. R. Soc. B 279, 4734 (2012).
  45. C. Andrade, Indian J. Psychol. Med. 41, 210 (2019).
  46. F. J. Bruggeman and B. Teusink, Curr. Opin. Syst. Biol. 8, 144 (2018).
  47. W. Pan, Z. Wanf, H. Gao, Y. Li, and M. Du, Int. J. Robust Nonlinear Control 18, 557 (2010).
  48. M. Zahri, J. Taibah Univ. Sci. 8, 186 (2014).
  49. B. Yang, M. Li, W. Tang, W. Liu, S. Zhang, L. Chen, and J. Xia, Nat. Commun. 9, 1 (2018).
  50. K. Aihara, R. Liu, K. Koizumi, X. Liu, and L. Chen, Gene 808, 145997 (2022).

Outline

Information

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation