Topology and Dynamics of the Zebrafish Segmentation Clock Core Circuit

By combining biochemical, embryological, and mathematical approaches, this work uncovers an important role for protein-protein interactions in determining the dynamics of the somite-forming segmentation clock in vertebrates.

[1]  B. Kendall.  Nonlinear Dynamics and Chaos , 2001 .

[2]  T. Emonet,et al.  network The Her7 node modulates the network topology of the zebrafish segmentation clock via sequestration of the Hes6 , 2012 .

[3]  A. Oates,et al.  Segment Number and Axial Identity in a Segmentation Clock Period Mutant , 2010, Current Biology.

[4]  Robert Geisler,et al.  beamter/deltaC and the role of Notch ligands in the zebrafish somite segmentation, hindbrain neurogenesis and hypochord differentiation. , 2005, Developmental biology.

[5]  Olivier Cinquin,et al.  Repressor Dimerization in the Zebrafish Somitogenesis Clock , 2007, PLoS Comput. Biol..

[6]  A. Bhattacharya,et al.  A Network of Broadly Expressed HLH Genes Regulates Tissue-Specific Cell Fates , 2011, Cell.

[7]  Daryl S Spinner,et al.  Interaction of the myogenic determination factor myogenin with E12 and a DNA target: mechanism and kinetics. , 2002, Journal of molecular biology.

[8]  Tomás Gedeon,et al.  Somitogenesis Clock-Wave Initiation Requires Differential Decay and Multiple Binding Sites for Clock Protein , 2010, PLoS Comput. Biol..

[9]  Olivier Pourquié,et al.  Control of segment number in vertebrate embryos , 2008, Nature.

[10]  M. Savageau,et al.  Parameter Sensitivity as a Criterion for Evaluating and Comparing the Performance of Biochemical Systems , 1971, Nature.

[11]  Stephen R Quake,et al.  An in vitro microfluidic approach to generating protein-interaction networks , 2009, Nature Methods.

[12]  Ingmar H Riedel-Kruse,et al.  Synchrony Dynamics During Initiation, Failure, and Rescue of the Segmentation Clock , 2007, Science.

[13]  A. Fischer,et al.  Delta–Notch—and then? Protein interactions and proposed modes of repression by Hes and Hey bHLH factors , 2007, Nucleic acids research.

[14]  Wolfgang Wurst,et al.  Cell-based simulation of dynamic expression patterns in the presomitic mesoderm. , 2007, Journal of theoretical biology.

[15]  S. Quake,et al.  De Novo Identification and Biophysical Characterization of Transcription Factor Binding Sites with Microfluidic Affinity Analysis , 2010, Nature Biotechnology.

[16]  S. Quake,et al.  A Systems Approach to Measuring the Binding Energy Landscapes of Transcription Factors , 2007, Science.

[17]  A. Yasui,et al.  Disruption of mCry2 restores circadian rhythmicity in mPer2 mutant mice. , 2002, Genes & development.

[18]  Ryoichiro Kageyama,et al.  Instability of Hes7 protein is crucial for the somite segmentation clock , 2004, Nature Genetics.

[19]  Ryoichiro Kageyama,et al.  Real-time imaging of the somite segmentation clock: Revelation of unstable oscillators in the individual presomitic mesoderm cells , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Hiroshi Momiji,et al.  Dissecting the dynamics of the Hes1 genetic oscillator. , 2008, Journal of theoretical biology.

[21]  Nicolas E. Buchler,et al.  Nonlinear protein degradation and the function of genetic circuits. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M. Vidal,et al.  A gateway-compatible yeast one-hybrid system. , 2004, Genome research.

[23]  Luis G. Morelli,et al.  Patterning embryos with oscillations: structure, function and dynamics of the vertebrate segmentation clock , 2012, Development.

[24]  R. Padgett,et al.  Rates of in situ transcription and splicing in large human genes , 2009, Nature Structural &Molecular Biology.

[25]  Robert Geisler,et al.  her1 and the notch pathway function within the oscillator mechanism that regulates zebrafish somitogenesis. , 2002, Development.

[26]  Frank Jülicher,et al.  Delayed coupling theory of vertebrate segmentation , 2008, HFSP journal.

[27]  James A. Glazier,et al.  A Multi-cell, Multi-scale Model of Vertebrate Segmentation and Somite Formation , 2011, PLoS Comput. Biol..

[28]  M A Savageau,et al.  Concepts relating the behavior of biochemical systems to their underlying molecular properties. , 1971, Archives of biochemistry and biophysics.

[29]  Olivier Tassy,et al.  Evolutionary plasticity of segmentation clock networks , 2011, Development.

[30]  C. Kimmel,et al.  Two linked hairy/Enhancer of split-related zebrafish genes, her1 and her7, function together to refine alternating somite boundaries. , 2002, Development.

[31]  A. Ciechanover,et al.  Ubiquitin-Proteasome-mediated Degradation of Id1 Is Modulated by MyoD* , 2004, Journal of Biological Chemistry.

[32]  B. Thisse,et al.  Loss of selenoprotein N function causes disruption of muscle architecture in the zebrafish embryo. , 2007, Experimental Cell Research.

[33]  T. Emonet,et al.  The Her7 node modulates the network topology of the zebrafish segmentation clock via sequestration of the Hes6 hub , 2012, Development.

[34]  Yoshihiro Morishita,et al.  Traveling wave formation in vertebrate segmentation. , 2009, Journal of theoretical biology.

[35]  D. Tautz,et al.  her11 is involved in the somitogenesis clock in zebrafish , 2004, Development Genes and Evolution.

[36]  J. Campos-Ortega,et al.  Expression domains of a zebrafish homologue of the Drosophila pair-rule gene hairy correspond to primordia of alternating somites. , 1996, Development.

[37]  M. Allende,et al.  Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. , 1996, Development.

[38]  Michael C Mackey,et al.  The segmentation clock in mice: interaction between the Wnt and Notch signalling pathways. , 2007, Journal of theoretical biology.

[39]  Y. Bessho,et al.  The bHLH gene Hes6, an inhibitor of Hes1, promotes neuronal differentiation. , 2000, Development.

[40]  R. Shigemoto,et al.  Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. , 1992, Genes & development.

[41]  A. Oates,et al.  Multiple embryo time-lapse imaging of zebrafish development. , 2009, Methods in molecular biology.

[42]  M. Caudy,et al.  Hairy function as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. , 1994, Genes & development.

[43]  Stephen R Quake,et al.  Experimental determination of the evolvability of a transcription factor , 2009, Proceedings of the National Academy of Sciences.

[44]  N. Monk.  Oscillatory Expression of Hes1, p53, and NF-κB Driven by Transcriptional Time Delays , 2003, Current Biology.

[45]  Andrew C Oates,et al.  Cooperative function of deltaC and her7 in anterior segment formation. , 2005, Developmental biology.

[46]  Jianwei Shen,et al.  Effects of nonlinear degradation of protein on the oscillatory dynamics in a simple gene regulatory network , 2010 .

[47]  Stefan Hans,et al.  Anterior and posterior waves of cyclic her1 gene expression are differentially regulated in the presomitic mesoderm of zebrafish , 2003, Development.

[48]  F Radtke,et al.  Oscillating expression of c-Hey2 in the presomitic mesoderm suggests that the segmentation clock may use combinatorial signaling through multiple interacting bHLH factors. , 2000, Developmental biology.

[49]  Bart Deplancke,et al.  Automated protein-DNA interaction screening of Drosophila regulatory elements , 2011, Nature Methods.

[50]  T. Ohtsuka,et al.  Hes1 and Hes5 as Notch effectors in mammalian neuronal differentiation , 1999, The EMBO journal.

[51]  C. Murre,et al.  Helix-Loop-Helix Proteins: Regulators of Transcription in Eucaryotic Organisms , 2000, Molecular and Cellular Biology.

[52]  A. Ciechanover,et al.  E12 and E47 modulate cellular localization and proteasome-mediated degradation of MyoD and Id1 , 2005, Oncogene.

[53]  Ruth E Baker,et al.  The clock and wavefront model revisited. , 2011, Journal of theoretical biology.

[54]  Michael C. Mackey,et al.  A Proposed Mechanism for the Interaction of the Segmentation Clock and the Determination Front in Somitogenesis , 2008, PloS one.

[55]  Scott A Holley,et al.  Expression of the oscillating gene her1 is directly regulated by hairy/enhancer of split, T‐box, and suppressor of hairless proteins in the zebrafish segmentation clock , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[56]  Jie Chen,et al.  A Complex Oscillating Network of Signaling Genes Underlies the Mouse Segmentation Clock , 2006, Science.

[57]  S. Quake,et al.  Microfluidic Large-Scale Integration , 2002, Science.

[58]  Scott A Holley,et al.  The genetics and embryology of zebrafish metamerism , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[59]  Julian Lewis.  Autoinhibition with Transcriptional Delay A Simple Mechanism for the Zebrafish Somitogenesis Oscillator , 2003, Current Biology.

[60]  M. Vidal,et al.  High-throughput yeast two-hybrid assays for large-scale protein interaction mapping. , 2001, Methods.

[61]  L. Joly,et al.  Zebrafish hox genes: genomic organization and modified colinear expression patterns in the trunk. , 1998, Development.

[62]  Albert Cardona,et al.  Dynamics of zebrafish somitogenesis , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[63]  Stefan Zeiser,et al.  Number of active transcription factor binding sites is essential for the Hes7 oscillator , 2006, Theoretical Biology and Medical Modelling.

[64]  Olivier Pourquié,et al.  Segmental patterning of the vertebrate embryonic axis , 2008, Nature Reviews Genetics.

[65]  Frank Jülicher,et al.  Intercellular Coupling Regulates the Period of the Segmentation Clock , 2010, Current Biology.

[66]  Hisato Kondoh,et al.  Zebrafish hairy/enhancer of split protein links FGF signaling to cyclic gene expression in the periodic segmentation of somites. , 2005, Genes & development.

[67]  Julian Lewis,et al.  Setting the Tempo in Development: An Investigation of the Zebrafish Somite Clock Mechanism , 2007, PLoS biology.

[68]  E. C. Zeeman,et al.  A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. , 1976, Journal of theoretical biology.

[69]  O. Pourquié,et al.  Avian hairy Gene Expression Identifies a Molecular Clock Linked to Vertebrate Segmentation and Somitogenesis , 1997, Cell.

[70]  J. Tyson,et al.  Design principles of biochemical oscillators , 2008, Nature Reviews Molecular Cell Biology.

[71]  Andrew C Oates,et al.  Hairy/E(spl)-related (Her) genes are central components of the segmentation oscillator and display redundancy with the Delta/Notch signaling pathway in the formation of anterior segmental boundaries in the zebrafish , 2002 .

[72]  Yoshihiro Morishita,et al.  Random cell movement promotes synchronization of the segmentation clock , 2010, Proceedings of the National Academy of Sciences.

[73]  Nicolas E. Buchler,et al.  Molecular titration and ultrasensitivity in regulatory networks. , 2008, Journal of molecular biology.

[74]  Y. Bessho,et al.  Dynamic expression and essential functions of Hes7 in somite segmentation. , 2001, Genes & development.

[75]  Ryoichiro Kageyama,et al.  Periodic repression by the bHLH factor Hes7 is an essential mechanism for the somite segmentation clock. , 2003, Genes & development.

[76]  Christoph Winkler,et al.  her1 and her13.2 are jointly required for somitic border specification along the entire axis of the fish embryo. , 2006, Developmental biology.

[77]  Edwin Cuppen,et al.  Efficient target-selected mutagenesis in zebrafish. , 2003, Genome research.

[78]  A. Oates,et al.  Completing the set of h/E(spl) cyclic genes in zebrafish: her12 and her15 reveal novel modes of expression and contribute to the segmentation clock. , 2007, Developmental biology.

[79]  Johannes Müller,et al.  Modeling the Hes1 Oscillator , 2007, J. Comput. Biol..