{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,31]],"date-time":"2025-12-31T10:07:35Z","timestamp":1767175655747,"version":"build-2238731810"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1005298","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2017,1,11]],"date-time":"2017-01-11T00:00:00Z","timestamp":1484092800000}}],"reference-count":69,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2016,12,27]],"date-time":"2016-12-27T00:00:00Z","timestamp":1482796800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"DOI":"10.1371\/journal.pcbi.1005298","type":"journal-article","created":{"date-parts":[[2017,1,9]],"date-time":"2017-01-09T14:56:29Z","timestamp":1483973789000},"page":"e1005298","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":17,"title":["Feedback, Mass Conservation and Reaction Kinetics Impact the Robustness of Cellular Oscillations"],"prefix":"10.1371","volume":"12","author":[{"given":"Katharina","family":"Baum","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4788-0933","authenticated-orcid":true,"given":"Antonio Z.","family":"Politi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bente","family":"Kofahl","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ralf","family":"Steuer","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jana","family":"Wolf","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2016,12,27]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"2955","DOI":"10.1016\/j.febslet.2012.07.041","article-title":"Systems biology of cellular rhythms","volume":"586","author":"A Goldbeter","year":"2012","journal-title":"FEBS Lett"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1016\/j.gde.2010.08.006","article-title":"Frequency control of cell cycle oscillators","volume":"20","author":"C Oikonomou","year":"2010","journal-title":"Curr Opin Genet Dev"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"945","DOI":"10.1016\/j.cell.2013.02.005","article-title":"Encoding and decoding cellular information through signaling dynamics","volume":"152","author":"JE Purvis","year":"2013","journal-title":"Cell"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1146\/annurev-biochem-060713-035623","article-title":"Metabolic and nontranscriptional circadian clocks: eukaryotes","volume":"83","author":"AB Reddy","year":"2014","journal-title":"Annu Rev Biochem"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1038\/msb4100179","article-title":"Towards a theory of biological robustness","volume":"3","author":"H Kitano","year":"2007","journal-title":"Mol Syst Biol"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1016\/j.cell.2004.09.008","article-title":"Robustness of cellular functions","volume":"118","author":"J Stelling","year":"2004","journal-title":"Cell"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"e104761","DOI":"10.1371\/journal.pone.0104761","article-title":"Positive feedback promotes oscillations in negative feedback loops","volume":"9","author":"B Ananthasubramaniam","year":"2014","journal-title":"PLoS One"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"e9865","DOI":"10.1371\/journal.pone.0009865","article-title":"Efficient estimation of the robustness region of biological models with oscillatory behavior","volume":"5","author":"M Apri","year":"2010","journal-title":"PLoS One"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1186\/1471-2105-3-38","article-title":"Quantifying robustness of biochemical network models","volume":"3","author":"L Ma","year":"2002","journal-title":"BMC Bioinformatics"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"11775","DOI":"10.1073\/pnas.0501094102","article-title":"Circuit topology and the evolution of robustness in two-gene circadian oscillators","volume":"102","author":"A Wagner","year":"2005","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"1018","DOI":"10.1073\/pnas.40.10.1018","article-title":"On Temperature Independence in the Clock System Controlling Emergence Time in Drosophila","volume":"40","author":"CS Pittendrigh","year":"1954","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"2697","DOI":"10.1073\/pnas.70.9.2697","article-title":"General homeostasis of the frequency of circadian oscillations","volume":"70","author":"CS Pittendrigh","year":"1973","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"8630","DOI":"10.1523\/JNEUROSCI.19-19-08630.1999","article-title":"Circadian rhythms in the suprachiasmatic nucleus are temperature-compensated and phase-shifted by heat pulses in vitro","volume":"19","author":"NF Ruby","year":"1999","journal-title":"J Neurosci"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1081\/CBI-100102109","article-title":"pH homeostasis of the circadian sporulation rhythm in clock mutants of Neurospora crassa","volume":"17","author":"P Ruoff","year":"2000","journal-title":"Chronobiol Int"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1126\/science.279.5348.227","article-title":"Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations","volume":"279","author":"P De Koninck","year":"1998","journal-title":"Science"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/j.ceca.2007.06.002","article-title":"Temperature and nitric oxide control spontaneous calcium transients in astrocytes","volume":"43","author":"CG Schipke","year":"2008","journal-title":"Cell Calcium"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1038\/nature07292","article-title":"Frequency-modulated nuclear localization bursts coordinate gene regulation","volume":"455","author":"L Cai","year":"2008","journal-title":"Nature"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"933","DOI":"10.1038\/31960","article-title":"Calcium oscillations increase the efficiency and specificity of gene expression","volume":"392","author":"RE Dolmetsch","year":"1998","journal-title":"Nature"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1016\/j.cell.2010.03.021","article-title":"Periodic cyclin-Cdk activity entrains an autonomous Cdc14 release oscillator","volume":"141","author":"Y Lu","year":"2010","journal-title":"Cell"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"e1000534","DOI":"10.1371\/journal.pcbi.1000534","article-title":"&apos;Glocal&apos; robustness analysis and model discrimination for circadian oscillators","volume":"5","author":"M Hafner","year":"2009","journal-title":"PLoS Comput Biol"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1186\/1752-0509-5-142","article-title":"Efficient characterization of high-dimensional parameter spaces for systems biology","volume":"5","author":"E Zamora-Sillero","year":"2011","journal-title":"BMC Syst Biol"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"1998","DOI":"10.1098\/rsif.2012.0028","article-title":"Regulation of oscillation dynamics in biochemical systems with dual negative feedback loops","volume":"9","author":"LK Nguyen","year":"2012","journal-title":"J R Soc Interface"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1038\/nature07389","article-title":"A fast, robust and tunable synthetic gene oscillator","volume":"456","author":"J Stricker","year":"2008","journal-title":"Nature"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1126\/science.1156951","article-title":"Robust, tunable biological oscillations from interlinked positive and negative feedback loops","volume":"321","author":"TYC Tsai","year":"2008","journal-title":"Science"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1093\/bioinformatics\/btl627","article-title":"Quantitative performance metrics for robustness in circadian rhythms","volume":"23","author":"N Bagheri","year":"2007","journal-title":"Bioinformatics"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"13161","DOI":"10.1038\/srep13161","article-title":"Robustness and period sensitivity analysis of minimal models for biochemical oscillators","volume":"5","author":"A Caicedo-Casso","year":"2015","journal-title":"Sci Rep"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"13210","DOI":"10.1073\/pnas.0401463101","article-title":"Robustness properties of circadian clock architectures","volume":"101","author":"J Stelling","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1049\/sb:20045009","article-title":"Sensitivity analysis of parameters controlling oscillatory signalling in the NF-kappaB pathway: the roles of IKK and IkappaBalpha","volume":"1","author":"AE Ihekwaba","year":"2004","journal-title":"Syst Biol (Stevenage)"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1049\/sb:20045035","article-title":"Analysing the robustness of cellular rhythms","volume":"2","author":"J Wolf","year":"2005","journal-title":"Syst Biol (Stevenage)"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/S0955-0674(03)00017-6","article-title":"Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell","volume":"15","author":"JJ Tyson","year":"2003","journal-title":"Curr Opin Cell Biol"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1016\/0065-2571(65)90067-1","article-title":"Oscillatory behavior in enzymatic control processes","volume":"3","author":"BC Goodwin","year":"1965","journal-title":"Adv Enzyme Regul"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"2778","DOI":"10.1016\/j.febslet.2013.07.031","article-title":"Oscillatory enzyme reactions and Michaelis-Menten kinetics","volume":"587","author":"A Goldbeter","year":"2013","journal-title":"FEBS letters"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.jtbi.2013.02.001","article-title":"Modeling the effect of cell division on genetic oscillators","volume":"325","author":"D Gonze","year":"2013","journal-title":"J Theor Biol"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"e34616","DOI":"10.1371\/journal.pone.0034616","article-title":"Roles of protein ubiquitination and degradation kinetics in biological oscillations","volume":"7","author":"L Xu","year":"2012","journal-title":"PLoS One"},{"key":"ref35","first-page":"138","article-title":"Model reduction and analysis of robustness for the Wnt\/beta-catenin signal transduction pathway","volume":"15","author":"R Kr\u00fcger","year":"2004","journal-title":"Genome Inform"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"E10","DOI":"10.1371\/journal.pbio.0000010","article-title":"The roles of APC and Axin derived from experimental and theoretical analysis of the Wnt pathway","volume":"1","author":"E Lee","year":"2003","journal-title":"PLoS Biol"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"3023","DOI":"10.1529\/biophysj.104.040824","article-title":"Modeling feedback loops of the Mammalian circadian oscillator","volume":"87","author":"S Becker-Weimann","year":"2004","journal-title":"Biophys J"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"1461","DOI":"10.1073\/pnas.87.4.1461","article-title":"Minimal model for signal-induced Ca2+ oscillations and for their frequency encoding through protein phosphorylation","volume":"87","author":"A Goldbeter","year":"1990","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref39","first-page":"436","volume":"XXIII","author":"G Dupont","year":"2016"},{"key":"ref40","first-page":"712","article-title":"Modeling circadian clocks: Roles, advantages, and limitations","volume":"6","author":"D Gonze","year":"2011","journal-title":"Cent Eur J Biol"},{"key":"ref41","first-page":"183","author":"J-C Leloup","year":"2014"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.pbiomolbio.2004.11.001","article-title":"Models of the inositol trisphosphate receptor","volume":"89","author":"J Sneyd","year":"2005","journal-title":"Prog Biophys Mol Biol"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"6840","DOI":"10.1073\/pnas.78.11.6840","article-title":"An amplified sensitivity arising from covalent modification in biological systems","volume":"78","author":"A Goldbeter","year":"1981","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"568","DOI":"10.1177\/0748730402238239","article-title":"Saturation of enzyme kinetics in circadian clock models","volume":"17","author":"G Kurosawa","year":"2002","journal-title":"J Biol Rhythms"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1016\/0022-5193(68)90189-6","article-title":"Mathematics of Cellular Control Processes. I. Negative Feedback to 1 Gene","volume":"20","author":"JS Griffith","year":"1968","journal-title":"J Theor Biol"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1098\/rspb.1995.0153","article-title":"A model for circadian oscillations in the Drosophila period protein (PER)","volume":"261","author":"A Goldbeter","year":"1995","journal-title":"Proc Biol Sci"},{"key":"ref47","article-title":"Extension of a genetic network model by iterative experimentation and mathematical analysis","volume":"1","author":"JCW Locke","year":"2005","journal-title":"Mol Syst Biol"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"1392","DOI":"10.1073\/pnas.0303472101","article-title":"Control of calcium oscillations by membrane fluxes","volume":"101","author":"J Sneyd","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"9895","DOI":"10.1073\/pnas.89.20.9895","article-title":"A single-pool inositol 1,4,5-trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca2+ concentration","volume":"89","author":"GW De Young","year":"1992","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1038\/35002125","article-title":"A synthetic oscillatory network of transcriptional regulators","volume":"403","author":"MB Elowitz","year":"2000","journal-title":"Nature"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"1583","DOI":"10.1046\/j.1432-1327.2000.01197.x","article-title":"Negative feedback and ultrasensitivity can bring about oscillations in the mitogen-activated protein kinase cascades","volume":"267","author":"BN Kholodenko","year":"2000","journal-title":"Eur J Biochem"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1111\/j.1432-1033.1968.tb00175.x","article-title":"Self-oscillations in glycolysis. 1. A simple kinetic model","volume":"4","author":"EE Sel'kov","year":"1968","journal-title":"Eur J Biochem"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0303-2647(97)01688-2","article-title":"Dynamics of two-component biochemical systems in interacting cells; synchronization and desynchronization of oscillations and multiple steady states","volume":"43","author":"J Wolf","year":"1997","journal-title":"Biosystems"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"7328","DOI":"10.1073\/pnas.88.16.7328","article-title":"Modeling the cell division cycle: cdc2 and cyclin interactions","volume":"88","author":"JJ Tyson","year":"1991","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1038\/nrg2102","article-title":"Network motifs: theory and experimental approaches","volume":"8","author":"U Alon","year":"2007","journal-title":"Nat Rev Genet"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1126\/science.1074560","article-title":"Oscillatory expression of the bHLH factor Hes1 regulated by a negative feedback loop","volume":"298","author":"H Hirata","year":"2002","journal-title":"Science"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1186\/s12918-016-0325-9","article-title":"How time delay and network design shape response patterns in biochemical negative feedback systems","volume":"10","author":"A B\u00f6rsch","year":"2016","journal-title":"BMC Syst Biol"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/j.mbs.2006.08.010","article-title":"Intracellular delay limits cyclic changes in gene expression","volume":"205","author":"K Rateitschak","year":"2007","journal-title":"Math Biosci"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.mbs.2008.05.004","article-title":"Genetic oscillation deduced from Hopf bifurcation in a genetic regulatory network with delays","volume":"215","author":"M Xiao","year":"2008","journal-title":"Math Biosci"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/S0006-3495(61)86902-6","article-title":"Impulses and Physiological States in Theoretical Models of Nerve Membrane","volume":"1","author":"R FitzHugh","year":"1961","journal-title":"Biophys J"},{"key":"ref61","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-662-22492-2","article-title":"The Geometry of Biological Time","author":"AT Winfree","year":"1980"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1016\/j.physleta.2003.08.006","article-title":"Noise enhances robustness of intracellular Ca2+ oscillations","volume":"316","author":"M Perc","year":"2003","journal-title":"Phys Lett A"},{"key":"ref63","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1073\/pnas.022628299","article-title":"Robustness of circadian rhythms with respect to molecular noise","volume":"99","author":"D Gonze","year":"2002","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref64","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1016\/j.cell.2015.01.013","article-title":"Noise facilitates transcriptional control under dynamic inputs","volume":"160","author":"RA Kellogg","year":"2015","journal-title":"Cell"},{"key":"ref65","doi-asserted-by":"crossref","first-page":"5988","DOI":"10.1073\/pnas.092133899","article-title":"Mechanisms of noise-resistance in genetic oscillators","volume":"99","author":"JM Vilar","year":"2002","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref66","doi-asserted-by":"crossref","first-page":"2139","DOI":"10.1016\/j.phytochem.2007.04.041","article-title":"Computational approaches to the topology, stability and dynamics of metabolic networks","volume":"68","author":"R Steuer","year":"2007","journal-title":"Phytochemistry"},{"key":"ref67","doi-asserted-by":"crossref","first-page":"1262","DOI":"10.1016\/j.cell.2010.06.019","article-title":"SnapShot: key numbers in biology","volume":"141","author":"U Moran","year":"2010","journal-title":"Cell"},{"key":"ref68","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1214\/aoms\/1177732502","article-title":"On confidence ranges for the median and other expectation distributions for populations of unknown distribution form","volume":"7","author":"WR Thompson","year":"1936","journal-title":"Ann Math Statist"},{"key":"ref69","author":"B Ermentrout","year":"2002"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1005298","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2017,1,11]],"date-time":"2017-01-11T00:00:00Z","timestamp":1484092800000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pcbi.1005298","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,5,8]],"date-time":"2020-05-08T19:06:17Z","timestamp":1588964777000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1005298"}},"subtitle":[],"editor":[{"given":"Jeffrey J.","family":"Saucerman","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2016,12,27]]},"references-count":69,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2016,12,27]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1005298","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,12,27]]}}}