×

Collective oscillations in coupled-cell systems. (English) Zbl 1466.92053

Summary: We investigate oscillations in coupled systems. The methodology is based on the Hopf bifurcation theorem and a condition extended from the Routh-Hurwitz criterion. Such a condition leads to locating the bifurcation values of the parameters. With such an approach, we analyze a single-cell system modeling the minimal genetic negative feedback loop and the coupled-cell system composed by these single-cell systems. We study the oscillatory properties for these systems and compare these properties between the model with Hill-type repression and the one with protein-sequestration-based repression. As the parameters move from the Hopf bifurcation value for single cells to the one for coupled cells, we compute the eigenvalues of the linearized systems to obtain the magnitude of the collective frequency when the periodic solution of the coupled-cell system is generated. Extending from this information on the parameter values, we further compute and compare the collective frequency for the coupled-cell system and the average frequency of the decoupled individual cells. To compare these scenarios with other biological oscillators, we perform parallel analysis and computations on a segmentation clock model.

MSC:

92C37 Cell biology
92B25 Biological rhythms and synchronization
34C23 Bifurcation theory for ordinary differential equations

References:

[1] An, S.; Irwin, RP; Allen, CN; Tsai, C.; Herzog, ED, Vasoactive intestinal polypeptide requires parallel changes in adenylate cyclase and phospholipase C to entrain circadian rhythms to a predictable phase, J Neurophysiol, 105, 5, 2289-2296 (2011) · doi:10.1152/jn.00966.2010
[2] Antle, MC; Silver, R., Orchestrating time: arrangements of the brain circadian clock, Trends Neurosci, 28, 3, 145-151 (2005) · doi:10.1016/j.tins.2005.01.003
[3] Aton, SJ; Colwell, CS; Harmar, AJ; Waschek, J.; Herzog, ED, Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock, Nat Neurosci, 8, 4, 476-483 (2005) · doi:10.1038/nn1419
[4] Baker, RE; Schnell, S., How can mathematics help us explore vertebrate segmentation?, HFSP, 3, 1-5 (2009) · doi:10.2976/1.3072371
[5] Bell-Pedersen, D.; Cassone, VM; Earnest, DJ; Golden, SS; Hardin, PE; Thomas, TL; Zoran, MJ, Circadian rhythms from multiple oscillators: lessons from diverse organisms, Nat Rev Genet, 6, 7, 544-556 (2015) · doi:10.1038/nrg1633
[6] Buchler, NE; Cross, FR, Protein sequestration generates a flexible ultrasensitive response in a genetic network, Mol Syst Biol, 5, 1-7 (2009) · doi:10.1038/msb.2009.30
[7] Chen, KW; Liao, KL; Shih, CW, The kinetics in mathematical models on segmentation clock genes in zebrafish, J Math Biol, 76, 1-2, 97-150 (2018) · Zbl 1383.34099 · doi:10.1007/s00285-017-1138-1
[8] Chiba, H., A proof of the Kuramoto conjecture for a bifurcation structure of the infinite dimensional Kuramoto model, Ergod Theor Dyn Syst, 35, 3, 762-834 (2015) · Zbl 1322.37036 · doi:10.1017/etds.2013.68
[9] Domijan, M.; Kirkilionis, M., Bistability and oscillations in chemical reaction networks, J Math Biol, 59, 467-501 (2009) · Zbl 1311.92088 · doi:10.1007/s00285-008-0234-7
[10] Ermentrout, GB; Kopell, N., Frequency plateaus in a chain of weakly coupled oscillators, SIAM J Math Anal, 15, 2, 215-237 (1984) · Zbl 0558.34033 · doi:10.1137/0515019
[11] Ermentrout, GB; Kopell, N., Multiple pulse interactions and averaging in systems of coupled neural oscillators, J Math Biol, 29, 3, 195-217 (1991) · Zbl 0718.92004 · doi:10.1007/BF00160535
[12] Ermentrout, GB; Park, Y.; Wilson, D., Recent advances in coupled oscillator theory, Philos Trans R Soc A, 377, 20190092 (2019) · Zbl 1462.34059 · doi:10.1098/rsta.2019.0092
[13] Fall, CP; Marland, ES; Wagner, JM; Tyson, JJ, Computational cell biology (2002), New York: Springer, New York · Zbl 1010.92019
[14] Forger, DB; Peskin, CS, A detailed predictive model of the mammalian circadian clock, Proc Natl Acad Sci USA, 100, 25, 14806-14811 (2003) · doi:10.1073/pnas.2036281100
[15] François, P.; Despierre, N.; Siggia, E., Adaptive temperature compensation in circadian oscillations, PLoS Comput Biol, 8, 7, e1002585 (2012) · doi:10.1371/journal.pcbi.1002585
[16] Gantmacher, FR, The theory of matrices (1959), Providence: American Mathematical Society, Providence · Zbl 0085.01001
[17] Golubitsky, M.; Schaeffer, DG, Singularities and groups in bifurcation theory (1985), New York: Springer-Verlag, New York · Zbl 0607.35004 · doi:10.1007/978-1-4612-5034-0
[18] Gonze, D., Modeling circadian clocks: from equations to oscillations, Cent Eur J Biol, 6, 5, 699-711 (2011)
[19] Gonze, D.; Abou-Jaoudé, W., The Goodwin model: behind the Hill function, PLoS ONE, 8, e69573 (2013) · doi:10.1371/journal.pone.0069573
[20] Gonze, D.; Bernard, S.; Waltermann, C.; Kramer, A.; Herzel, H., Spontaneous synchronization of coupled circadian oscillators, Biophys J, 89, 120-129 (2005) · doi:10.1529/biophysj.104.058388
[21] Goodwin, BC, Oscillatory behavior in enzymatic control process, Adv Enzyme Regul, 3, 425-438 (1965) · doi:10.1016/0065-2571(65)90067-1
[22] Griffith, JS, Mathematics of cellular control process. I. Negative feedback to one gene, J Theor Biol, 20, 202-208 (1968) · doi:10.1016/0022-5193(68)90189-6
[23] Ha, SL; Noh, SE; Park, J., Synchronization of Kuramoto oscillators with adaptive couplings, SIAM J Appl Dyn Syst, 15, 1, 162-194 (2016) · Zbl 1393.34052 · doi:10.1137/15M101484X
[24] Hassard, BD; Kazarinoff, ND; Wan, YH, Theory and applications of Hopf bifurcation (1981), Cambridge, New York: Cambridge University, Cambridge, New York · Zbl 0474.34002
[25] Herrgen, L.; Ares, S.; Morelli, LG; Schröter, C.; Jülicher, F.; Oates, AC, Intercellular coupling regulates the period of the segmentation clock, Curr Biol, 20, 14, 1244-1253 (2010) · doi:10.1016/j.cub.2010.06.034
[26] Herzog, ED; Aton, SJ; Numano, R.; Sakaki, Y.; Tei, H., Temporal precision in the mammalian circadian systems: a reliable clock from less reliable neurons, J Biol Rhythms, 19, 1, 35-46 (2004) · doi:10.1177/0748730403260776
[27] Honma, S.; Ono, D.; Suzuki, Y.; Inagaki, N.; Yoshikawa, T.; Nakamura, W.; Honma, K., Suprachiasmatic nucleus: cellular clocks and networks, Prog Brain Res, 199, 129-141 (2012) · doi:10.1016/B978-0-444-59427-3.00029-0
[28] Hurwitz, A., Ueber die Bedingungen, unter welchen eine Gleichung nut Wurzeln mit negativen reellen Teilen besitzt, Math Ann, 46, 273-284 (1895) · JFM 26.0119.03 · doi:10.1007/BF01446812
[29] Keller, AD, Model genetic circuits encoding autoregulatory transcription factors, J Theor Biol, 172, 2, 169-185 (1995) · doi:10.1006/jtbi.1995.0014
[30] Kemperman, JHB, A Hurwitz matrix is totally positive, SIAM J Math Anal, 13, 2, 331-341 (1982) · Zbl 0484.30006 · doi:10.1137/0513025
[31] Kim, JK, Protein sequestration versus hill-type repression in circadian clock models, IET Syst Biol, 10, 4, 125-135 (2016) · doi:10.1049/iet-syb.2015.0090
[32] Kim, JK; Forger, DB, A mechanism for robust circadian timekeeping via stoichiometric balance, Mol Syst Biol, 8, 630 (2012) · doi:10.1038/msb.2012.62
[33] Kim, JK; Kilpatrick, ZP; Bennett, MR; Josić, K., Molecular mechanisms that regulate the coupled period of the mammalian circadian clocks, Biophys J, 106, 9, 2071-2081 (2014) · doi:10.1016/j.bpj.2014.02.039
[34] Kuramoto, Y., Chemical oscillations, waves and turbulence (1984), Berlin: Springer-Verlag, Berlin · Zbl 0558.76051 · doi:10.1007/978-3-642-69689-3
[35] Kuramoto, Y.; Nakao, H., On the concept of dynamical reduction: the case of coupled oscillators, Philos Trans R Soc A, 377, 20190041 (2019) · Zbl 1462.34062 · doi:10.1098/rsta.2019.0041
[36] Kurosawa, G.; Iwasa, Y., Saturation of enzyme kinetics in circadian clock models, J Biol Rhythm, 17, 6, 568-577 (2002) · doi:10.1177/0748730402238239
[37] Kurosawa, G.; Iwasa, Y., Temperature compensation in circadian clock models, J Theor Biol, 233, 4, 453-468 (2005) · Zbl 1443.92051 · doi:10.1016/j.jtbi.2004.10.012
[38] Kurosawa, G.; Mochizuki, A.; Iwasa, Y., Comparative study of circadian clock models, in search of processes promoting oscillation, J Theor Biol, 216, 2, 193-208 (2002) · doi:10.1006/jtbi.2002.2546
[39] Liao, KL; Shih, CW, A lattice model on somitogenesis of zebrafish, Discrete Contin Dyn Syst B, 17, 8, 2789-2814 (2012) · Zbl 1395.92021 · doi:10.3934/dcdsb.2012.17.2789
[40] Liao, KL; Shih, CW; Tseng, JP, Synchronized oscillations in mathematical model of segmentation in zebrafish, Nonlinearity, 25, 869-904 (2012) · Zbl 1237.37065 · doi:10.1088/0951-7715/25/4/869
[41] Liu, WM, Criterion of Hopf bifurcation without using eigenvalues, J Math Anal Appl, 182, 250-256 (1994) · Zbl 0794.34033 · doi:10.1006/jmaa.1994.1079
[42] Liu, WM, Nonlinear oscillations in models of immune responses to persistent viruses, Theor Popul Biol, 52, 224-230 (1997) · Zbl 0890.92015 · doi:10.1006/tpbi.1997.1334
[43] Liu, C.; Weaver, DR; Strogatz, SH; Reppert, SM, Cellular construction of a circadian clock: period determination in the suprachiasmatic nuclei, Cell, 91, 855-860 (1997) · doi:10.1016/S0092-8674(00)80473-0
[44] Obatake, N.; Shiu, A.; Tang, X.; Torres, A., Oscillations and bistability in a model of ERK regulation, J Math Biol, 79, 1515-1549 (2019) · Zbl 1425.92097 · doi:10.1007/s00285-019-01402-y
[45] Ruoff, P.; Vinsjevik, M.; Monnerjahn, C.; Rensing, L., The Goodwin oscillator: on the importance of degradation reactions in the circadian clock, J Biol Rhythm, 14, 6, 469-479 (1999) · doi:10.1177/074873099129001037
[46] Ruoff, P.; Vinsjevik, M.; Monnerjahn, C.; Rensing, L., The Goodwin model: simulating the effect of light pulses on the circadian sporulation rhythm on Neurospora crassa, J Theor Biol, 209, 1, 29-42 (2001) · doi:10.1006/jtbi.2000.2239
[47] Schwemmer MA, Lewis TJ (2012) The theory of weakly coupled oscillators. Phase response curves in neuroscience: theory, experiment and analysis pp. 3-31
[48] Shih CW, Yang JZ (2021) Hopf bifurcation analysis on the Goodwin’s model. Preprint
[49] Strogatz, SH, Nonlinear dynamics and chaos (1994), Boston: Addison-Wesley, Boston
[50] Taylor, SR, How to get oscillators in a multicellular clock to agree on the right period, Biophys J, 106, 9, 1839-1840 (2014) · doi:10.1016/j.bpj.2014.03.036
[51] To, TL; Henson, MA; Herzog, ED; Doyle, FJ III, A molecular model for intercellular synchronization in the mammalian circadian clock, Biophys J, 92, 11, 3792-3803 (2007) · doi:10.1529/biophysj.106.094086
[52] Uriu, K.; Morishita, Y.; Iwasa, Y., Traveling wave formation in vertebrate segmentation, J Theor Biol, 257, 3, 385-396 (2009) · Zbl 1400.92067 · doi:10.1016/j.jtbi.2009.01.003
[53] Uriu, K.; Morishita, Y.; Iwasa, Y., Synchronized oscillation of the segmentation clock gene in vertebrate development, J Math Biol, 61, 2, 207-229 (2010) · Zbl 1203.92001 · doi:10.1007/s00285-009-0296-1
[54] Uspensky, JV, Theory of equations (1948), Chennai: McGraw-Hill Book Company, Chennai
[55] Winfree, AT, The geometry of biological time (1980), New York: Springer-Verlag, New York · Zbl 0464.92001 · doi:10.1007/978-3-662-22492-2
[56] Woller, A.; Gonze, D.; Erneux, T., The Goodwin model revisited: Hopf bifurcation, limit cycle, and periodic entrainment, Phys Biol, 11, 4, 045002 (2014) · doi:10.1088/1478-3975/11/4/045002
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.