Synchronizing Genetic Oscillators by Signaling Molecules

The authors examine collective rhythms in a general multicell system with both linearly diffusive and nondiffusive couplings. The effect of coupling on synchronization through intercellular signaling in a population of Escherichia coli cells is studied. In particular, a synchronization solution is given through the auxiliary individual system for 2 types of couplings. The sufficient conditions for the global synchronization of such a coupled system are derived based on the Lyapunov function method. The authors show that an appropriate design of the coupling and the inner-linking matrix can ensure global synchronization of the coupled synthetic biological system. Moreover, they demonstrate that the dynamics of an individual cell with coupling and without coupling may be qualitatively different; one is oscillatory, and the other is steady state. The change from a nonoscillatory state to an oscillatory one is induced by appropriate coupling, which also entrains all cells to synchronization. These results establish not only a theoretical foundation but also a quantitative basis for understanding the essential cooperative dynamics, such as collective rhythms or synchronization, in a population of cells.

[1]  Charles S. Peskin,et al.  Mathematical aspects of heart physiology , 1975 .

[2]  J. Buck,et al.  Synchronous fireflies. , 1976, Scientific American.

[3]  A. Winfree The geometry of biological time , 1991 .

[4]  A. Goldbeter A model for circadian oscillations in the Drosophila period protein (PER) , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[5]  L. Chua,et al.  Synchronization in an array of linearly coupled dynamical systems , 1995 .

[6]  Sue Ann Campbell,et al.  Frustration, Stability, and Delay-Induced Oscillations in a Neural Network Model , 1996, SIAM J. Appl. Math..

[7]  J. Dunlap,et al.  Neurospora wc-1 and wc-2: transcription, photoresponses, and the origins of circadian rhythmicity. , 1997, Science.

[8]  Susan S. Golden,et al.  CYANOBACTERIAL CIRCADIAN RHYTHMS. , 1997, Annual review of plant physiology and plant molecular biology.

[9]  J. Dunlap Molecular Bases for Circadian Clocks , 1999, Cell.

[10]  A. Goldbeter,et al.  Limit Cycle Models for Circadian Rhythms Based on Transcriptional Regulation in Drosophila and Neurospora , 1999, Journal of biological rhythms.

[11]  T. Carroll,et al.  MASTER STABILITY FUNCTIONS FOR SYNCHRONIZED COUPLED SYSTEMS , 1999 .

[12]  J. Collins,et al.  Construction of a genetic toggle switch in Escherichia coli , 2000, Nature.

[13]  M. Elowitz,et al.  A synthetic oscillatory network of transcriptional regulators , 2000, Nature.

[14]  L. Serrano,et al.  Engineering stability in gene networks by autoregulation , 2000, Nature.

[15]  Ron Weiss,et al.  Engineered Communications for Microbial Robotics , 2000, DNA Computing.

[16]  J. Keener,et al.  A mathematical model for quorum sensing in Pseudomonas aeruginosa , 2001, Bulletin of mathematical biology.

[17]  B. Séraphin,et al.  Positive feedback in eukaryotic gene networks: cell differentiation by graded to binary response conversion , 2001, The EMBO journal.

[18]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[19]  Jürgen Kurths,et al.  Synchronization: Phase locking and frequency entrainment , 2001 .

[20]  Kenzo Hirose,et al.  Intercellular coupling mechanism for synchronized and noise-resistant circadian oscillators. , 2002, Journal of theoretical biology.

[21]  K. Aihara,et al.  A model of periodic oscillation for genetic regulatory systems , 2002 .

[22]  Ertugrul M. Ozbudak,et al.  Regulation of noise in the expression of a single gene , 2002, Nature Genetics.

[23]  J. Hasty,et al.  Synchronizing genetic relaxation oscillators by intercell signaling , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[24]  P. Swain,et al.  Stochastic Gene Expression in a Single Cell , 2002, Science.

[25]  M. Heinlein Plasmodesmata: dynamic regulation and role in macromolecular cell-to-cell signaling. , 2002, Current opinion in plant biology.

[26]  Bonnie L Bassler,et al.  Chemical communication among bacteria , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Farren J. Isaacs,et al.  Prediction and measurement of an autoregulatory genetic module , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Bernard Perbal,et al.  Communication is the key , 2003, Cell Communication and Signaling.

[29]  Peter Achermann,et al.  Simulation of circadian rhythm generation in the suprachiasmatic nucleus with locally coupled self-sustained oscillators. , 2003, Journal of theoretical biology.

[30]  Mads Kærn,et al.  Noise in eukaryotic gene expression , 2003, Nature.

[31]  A. Ninfa,et al.  Development of Genetic Circuitry Exhibiting Toggle Switch or Oscillatory Behavior in Escherichia coli , 2003, Cell.

[32]  Ruiqi Wang,et al.  Modelling periodic oscillation of biological systems with multiple timescale networks. , 2004, Systems biology.

[33]  Kazuyuki Aihara,et al.  Dynamics of gene regulatory networks with cell division cycle. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[34]  A. Klarsfeld,et al.  Circadian Synchronization and Rhythmicity in Larval Photoperception-Defective Mutants of Drosophila , 2004, Journal of biological rhythms.

[35]  J. Collins,et al.  Programmable cells: interfacing natural and engineered gene networks. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[36]  R. Weiss,et al.  Programmed population control by cell–cell communication and regulated killing , 2004, Nature.

[37]  K. Aihara,et al.  Intercellular communications induced by random fluctuations. , 2004, Genome informatics. International Conference on Genome Informatics.

[38]  Jianfeng Feng,et al.  Synchronization in stochastic coupled systems: theoretical results , 2004 .

[39]  Guanrong Chen,et al.  Global Synchronization of Coupled Delayed Neural Networks and Applications to Chaotic CNN Models , 2004, Int. J. Bifurc. Chaos.

[40]  Charles M. Gray,et al.  Synchronous oscillations in neuronal systems: Mechanisms and functions , 1994, Journal of Computational Neuroscience.

[41]  M. Elowitz,et al.  Modeling a synthetic multicellular clock: repressilators coupled by quorum sensing. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Luonan Chen,et al.  Modelling periodic oscillation in gene regulatory networks by cyclic feedback systems , 2005, Bulletin of mathematical biology.

[43]  Kazuyuki Aihara,et al.  Noise-induced cooperative behavior in a multicell system , 2005, Bioinform..

[44]  Jeffrey W. Smith,et al.  Stochastic Gene Expression in a Single Cell , 2022 .