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