Hostname: page-component-76fb5796d-45l2p Total loading time: 0 Render date: 2024-04-26T16:07:38.670Z Has data issue: false hasContentIssue false

Modeling Biological Rhythms in Cell Populations

Published online by Cambridge University Press:  12 December 2012

R. El Cheikh
Affiliation:
Université de Lyon, CNRS UMR 5208, Université Lyon 1, Institut Camille Jordan 43 blvd. du 11 novembre 1918, F-69622 Villeurbanne cedex, France INRIA project-team DRACULA, INRIA-antenne Lyon-La Doua, Batiment CEI-1 66 Boulevard Niels Bohr, 69603 Villeurbanne cedex France
T. Lepoutre
Affiliation:
Université de Lyon, CNRS UMR 5208, Université Lyon 1, Institut Camille Jordan 43 blvd. du 11 novembre 1918, F-69622 Villeurbanne cedex, France INRIA project-team DRACULA, INRIA-antenne Lyon-La Doua, Batiment CEI-1 66 Boulevard Niels Bohr, 69603 Villeurbanne cedex France
S. Bernard*
Affiliation:
Université de Lyon, CNRS UMR 5208, Université Lyon 1, Institut Camille Jordan 43 blvd. du 11 novembre 1918, F-69622 Villeurbanne cedex, France INRIA project-team DRACULA, INRIA-antenne Lyon-La Doua, Batiment CEI-1 66 Boulevard Niels Bohr, 69603 Villeurbanne cedex France
*
Corresponding author. E-mail: bernard@math.univ-lyon1.fr
Get access

Abstract

Biological rhythms occur at different levels in the organism. In single cells, the cell division cycle shows rhythmicity in the way its molecular regulators, the cyclin dependant kinases (CDKs), modulate their activity periodically to ensure a healthy progression. In tissues, cell proliferation is driven by the circadian clock, which modulates the progression through the cell cycle along the day. The circadian clock shows endogenous rhythmicity through a robust network of transcription-translation feedback loops that create sustained oscillations. Rhythmicity is preserved in cell populations by the coordination of the clocks among cells, through rhythmic synchronization signals. Here we discuss mechanisms for generating rhythmic activities in cell populations by reviewing some of the mathematical models that deal with them. We discuss the implication of biological rhythms for tissue growth and the possible application to chronomodulated cancer treatments.

Type
Research Article
Copyright
© EDP Sciences, 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Références

Achermann, P., Kunz, H.. Modeling circadian rhythm generation in the suprachiasmatic nucleus with locally coupled self-sustained oscillators: Phase shifts and phase response curves. J Biol Rhythm, 14(6):460468, 1999. CrossRefGoogle ScholarPubMed
Becker-Weimann, S., Wolf, J., Herzel, H., Kramer, A.. Modeling feedback loops of the mammalian circadian oscillator. Biophys J, 87(5):30233034, 2004. CrossRefGoogle ScholarPubMed
Bekkal Brikci, F., Clairambault, J., Perthame, B.. Analysis of a molecular structured population model with possible polynomial growth for the cell division cycle. Math and Comp Modelling, 47(7–8): 699713, 2008. CrossRefGoogle Scholar
Bernard, S., Herzel, H.. Why do cells cycle with a 24 hour period ? Genome Inform Ser., 17(1):7279, 2006. Google Scholar
Bernard, S., Gonze, D., Cǎjavec, B., Herzel, H., Kramer, A.. Synchronization-induced rhythmicity of circadian oscillations in the suprachiasmatic nucleus. PLoS Comput Biol, 17(1):7279, 2006. Google Scholar
Bernard, S., Căjavec Bernard, B., Lévi, F., Herzel, H.. Tumor growth rate determines the timing of optimal chronomodulated treatment schedules. LoS Comput Biol, 6(3):e1000712, 2010. doi:10.1371/journal.pcbi.1000712 Google ScholarPubMed
F. Billy, J. Clairambault, O. Fercoq. Optimisation of cancer drug treatments using cell population dynamics. Math Meth and Mod in Biomed, 257–299, 2012.
Chauhan, A., Lorenzen, S., Herzel, H., Bernard, S.. Regulation of mammalian cell cycle progression in the regenerating liver. J Theor Biol, 283(1):10312, 2011. CrossRefGoogle ScholarPubMed
Clairambault, J., Gaubert, S., Lepoutre, T.. Circadian rhythm and cell population growth. Math Comput Model, 53(7-8):15581567, 2011. CrossRefGoogle Scholar
Clairambault, J., Gaubert, S., Lepoutre, T.. Comparison of Perron and Floquet eigenvalues in age structured cell division cycle models. Math Model Nat Phenom, 4(3):183209, 2009. CrossRefGoogle Scholar
Clairambault, J., Gaubert, S., Perthame, B.. An inequality for the Perron and Floquet eigenvalues of monotone differential systems and age structured equations. C R Math, 345(10):549554, 2007. CrossRefGoogle Scholar
Clairambault, J., Michel, P., Perthame, B.. Circadian rhythm and tumour growth. C R Math, 342(1):1722, 2006. CrossRefGoogle Scholar
Czeisler, C., Kronauer, R., Allan, J., Duffy, J., Jewett, M., Brown, E., Ronda, J.. Bright light induction of strong (type 0) resetting of the human circadian pacemaker. science, 244(4910):13281333, 1989. CrossRefGoogle Scholar
Davidich, M., Bornholdt, S.. Boolean network model predicts cell cycle sequence of fission yeast. PLoS One, 3(2):e1672, 2008. CrossRefGoogle Scholar
Doumic, M.. Analysis of a population Model Structured by the Cells Molecular Contents. MMNP, 3(2): 121152, 2007. Google Scholar
Ferrell, J. E., Tsai, T. Y.-c., Yang, Q.. Modeling the cell cycle: why do certain circuits oscillate ? Cell, 144(6):87485, 2011. CrossRefPubMed
da Fonseca, PC., He, J., Morris, EP.. Molecular model of the human 26S proteasome. Mol Cell, 46(1):54-66, 2012. CrossRefGoogle ScholarPubMed
Forger, D., Jewett, M., Kronauer, R.. A simpler model of the human circadian pacemaker. J Biol Rhythm, 14(6):533538, 1999. CrossRefGoogle ScholarPubMed
D. Forger, R. Kronauer. Reconciling mathematical models of biological clocks by averaging on approximate manifolds. SIAM J Appl Math., pages 1281–1296, 2002.
Forger, D. B., Peskin, C. S.. A detailed predictive model of the mammalian circadian clock. Proc Natl Acad Sci USA, 100(25):1480614811, 2003. CrossRefGoogle Scholar
Gérard, C., Goldbeter, A.. A skeleton model for the network of cyclin-dependent kinases driving the mammalian cell cycle. Interface Focus, 1(1):2435, 2011. CrossRefGoogle Scholar
Gery, S., Koeffler, HP. Circadian rhythms and cancer. Cell Cycle, 9:10971103, 2010. CrossRefGoogle Scholar
Gérard, C., Goldbeter, A.. Entrainment of the Mammalian Cell Cycle by the Circadian Clock: Modeling Two Coupled Cellular Rhythms. Plos Comp Biol, 8(5): e1002516.
A. Goldbeter, C. Ge, C. Gérard. Temporal self-organization of the Cyclin/Cdk network driving the mammalian cell cycle. Proc Natl Acad Sci USA, 1–6, 2009.
Gonze, D.. Modeling circadian clocks: From equations to oscillations. Cent Eur J Biol, 6(5):699711, 2011. Google Scholar
B.C. Goodwin. Temporal Organization in Cells. A Dynamic Theory of Cellular Control Processes. New York: Academic Press, 1963.
Goodwin, B.C.. Oscillatory behavior in enzymatic control processes. Advances in Enzyme Regulation, 3:425438, 1965. CrossRefGoogle Scholar
T. Hunt. The Life Scientific, BBC Radio 4 podcast, 13/12/2011.
Kingman, J.F.C.. A convexity property of positive matrices. Quart. J. Math. Oxford, (2)12:283284, 1961. CrossRefGoogle Scholar
Kubo, T., Ozasa, K., Mikami, K., Wakai, K., Fujino, Y., Watanabe, Y., Miki, T., Nakao, M., Hayashi, K., Suzuki, K., et al. Prospective cohort study of the risk of prostate cancer among rotating-shift workers: findings from the japan collaborative cohort study. Am J Epidemiol, 164(6):549555, 2006. CrossRefGoogle ScholarPubMed
Kunz, H., Achermann, P.. Simulation of circadian rhythm generation in the suprachiasmatic nucleus with locally coupled self-sustained oscillators. J Theor Biol, 224(1):6378, 2003. CrossRefGoogle Scholar
Leloup, J.-C., Goldbeter, A.. Toward a detailed computational model for the mammalian circadian clock. Proc Natl Acad Sci USA, 100(12):70517056, 2003. CrossRefGoogle Scholar
T. Lepoutre. Analysis and modelling of growth and motion phenomenon from biology. PHD in applied mathematics. Université Pierre et Marie Curie Paris (France), 2007–2009.
Lévi, F., Circadian chronotherapy for human cancers. The Lancet Oncology, 2(5), 307315, 2001, doi:10.1016/S1470-2045(00)00326-0 CrossRefGoogle ScholarPubMed
Lévi, F.. Cancer chronotherapy. J of Pharmacy and Pharmacol, 51(8), 891898, 1999. CrossRefGoogle ScholarPubMed
Maywood, E.S., Reddy, A.B., Wong, G.K.Y., O’Neill, J.S., O’Brien, J.A., McMahon, D.G., Harmar, A.J., Okamura, H., Hastings, M.H.. Synchronisation and maintenance of timekeeping in suprachiasmatic circadian clock cells by neuropeptidergic signaling. Curr Biol, 16:599605, 2006. CrossRefGoogle Scholar
Mackey, M.C.. Unified hypothesis for the origin of aplastic anemia and periodic hematopoiesis. Blood, 51(5):94156, 1978. Google Scholar
Mirsky, H., Liu, A., Welsh, D., Kay, S., Doyle, F.. A model of the cell-autonomous mammalian circadian clock. Proc Natl Acad Sci USA, 106(27):1110711112, 2009. CrossRefGoogle Scholar
Novak, B., Pataki, Z., Ciliberto, A., Tyson, J.J.. Mathematical model of the cell division cycle of fission yeast. Chaos, 11(1):277286, 2001. CrossRefGoogle Scholar
Novak, B., Tyson, J.J.. A model for restriction point control of the mammalian cell cycle. J Theor Biol, 230(4):563579, 2004. CrossRefGoogle ScholarPubMed
Pando, B.F., van Oudenaarden, A.. Coupling cellular oscillators-circadian and cell division cycles in cyanobacterial cells. Curr Opin Genet Dev, 20:16, 2010. CrossRefGoogle Scholar
B. Perthame. Transport equations in biology. Birkhauser, 2007.
Pomerening, J. R., Sontag, E. D., Ferrell, J. E.. Building a cell cycle oscillator: hysteresis and bistability in the activation of Cdc2. Nat Cell Biol, 5(4):34651, 2003. CrossRefGoogle Scholar
Rompala, K., Rand, R., Howland, H.. Dynamics of three coupled van der Pol oscillators with application to circadian rhythms. Commun Nonlinear Sci, 12(5):794803, 2007. CrossRefGoogle Scholar
Ruoff, P., M Vindjevik, C.M., Rensing, L.. The Goodwin model simulating the effect of light pulses on the circadian sporulation rhythm of Neurospora crassa. J. Theor. Biol., 209:2942, 2001. CrossRefGoogle Scholar
S. Sahar, P. Sassone-Corsi. Circadian rhythms and memory formation: regulation by chromatin remodeling. Front Mol Neurosci, 5–37, 2006. Published online 2012 March 26. doi: 10.3389/fnmol.2012.00037.
Swat, M., Kel, A., Herzel, H.. Bifurcation analysis of the regulatory modules of the mammalian G1/S transition. Bioinformatics, 20(10):15061511, 2004. CrossRefGoogle ScholarPubMed
J.J. Tyson, B. Novak. Temporal organization of the cell cycle. Curr Biol 18, R759-R768, 2008.
Tyson, J.J., Chen, K.C., Novak, B.. Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. Curr Op in Cell Biol, 15:221231, 2003. CrossRefGoogle Scholar
Van der Pol, B., Van der Mark, J.. Frequency demultiplication. Nature, 120:363364, 1927. CrossRefGoogle Scholar
Webb, A.B., Angelo, N., Huettner, J.E., Herzog, E.D.. Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons. Proc Natl Acad Sci USA, 106(38):1649316498, 2009. CrossRefGoogle Scholar
Welsh, D., Takahashi, J., Kay, S.. Suprachiasmatic nucleus: cell autonomy and network properties. Ann Rev Physiol, 72:551577, 2010. CrossRefGoogle ScholarPubMed
Westermark, P.O., Welsh, D.K., Okamura, H., Herzel, H.. Quantification of Circadian Rhythms in Single Cells. PLoS Comput Biol, 5(11):e1000580, 2009. CrossRefGoogle ScholarPubMed
Wever, R.. Zum Mechanismus der Biologischen 24-Stunden-Periodik. Biol Cybern, 1(4):139154, 1962. Google Scholar
Wever, R.. Zum Mechanismus der Biologischen 24-Stunden-Periodik II. Biol Cybern, 1(6):213231, 1963. Google Scholar
Yamaguchi, S., Isejima, H., Matsuo, T., Okura, R., Yagita, K., Kobayashi, M., Okamura, H, H. Synchronization of cellular clocks in the suprachiasmatic nucleus. Science, 302:14081412, 2003. CrossRefGoogle Scholar
Zhang, E. E., Kay, S. A.. Clocks not winding down: unravelling circadian networks. Nat Rev Mol Cell Biol, 11(11):764776, 2010. CrossRefGoogle Scholar