Literature DB >> 26880542

Persistence, period and precision of autonomous cellular oscillators from the zebrafish segmentation clock.

Alexis B Webb1,2, Iván M Lengyel3, David J Jörg4, Guillaume Valentin1,2, Frank Jülicher4, Luis G Morelli3, Andrew C Oates1,2,5.   

Abstract

In vertebrate development, the sequential and rhythmic segmentation of the body axis is regulated by a "segmentation clock". This clock is comprised of a population of coordinated oscillating cells that together produce rhythmic gene expression patterns in the embryo. Whether individual cells autonomously maintain oscillations, or whether oscillations depend on signals from neighboring cells is unknown. Using a transgenic zebrafish reporter line for the cyclic transcription factor Her1, we recorded single tailbud cells in vitro. We demonstrate that individual cells can behave as autonomous cellular oscillators. We described the observed variability in cell behavior using a theory of generic oscillators with correlated noise. Single cells have longer periods and lower precision than the tissue, highlighting the role of collective processes in the segmentation clock. Our work reveals a population of cells from the zebrafish segmentation clock that behave as self-sustained, autonomous oscillators with distinctive noisy dynamics.

Entities:  

Keywords:  biological clock; computational biology; developmental biology; gene expression noise; oscillator; somitogenesis; stem cells; systems biology; theoretical modelling; timelapse imaging; zebrafish

Mesh:

Substances:

Year:  2016        PMID: 26880542      PMCID: PMC4803185          DOI: 10.7554/eLife.08438

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  63 in total

1.  Oscillatory expression of Hes1, p53, and NF-kappaB driven by transcriptional time delays.

Authors:  Nicholas A M Monk
Journal:  Curr Biol       Date:  2003-08-19       Impact factor: 10.834

2.  Modeling a synthetic multicellular clock: repressilators coupled by quorum sensing.

Authors:  Jordi Garcia-Ojalvo; Michael B Elowitz; Steven H Strogatz
Journal:  Proc Natl Acad Sci U S A       Date:  2004-07-15       Impact factor: 11.205

3.  Emergence of traveling waves in the zebrafish segmentation clock.

Authors:  Kana Ishimatsu; Atsuko Takamatsu; Hiroyuki Takeda
Journal:  Development       Date:  2010-04-14       Impact factor: 6.868

4.  Hierarchical inductions of cell states: a model for segmentation in Drosophila.

Authors:  H Meinhardt
Journal:  J Cell Sci Suppl       Date:  1986

5.  Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms.

Authors:  D K Welsh; D E Logothetis; M Meister; S M Reppert
Journal:  Neuron       Date:  1995-04       Impact factor: 17.173

6.  Control of directed cell migration in vivo by membrane-to-cortex attachment.

Authors:  Alba Diz-Muñoz; Michael Krieg; Martin Bergert; Itziar Ibarlucea-Benitez; Daniel J Muller; Ewa Paluch; Carl-Philipp Heisenberg
Journal:  PLoS Biol       Date:  2010-11-30       Impact factor: 8.029

7.  Transcriptome-wide noise controls lineage choice in mammalian progenitor cells.

Authors:  Hannah H Chang; Martin Hemberg; Mauricio Barahona; Donald E Ingber; Sui Huang
Journal:  Nature       Date:  2008-05-22       Impact factor: 49.962

8.  Genetic oscillations. A Doppler effect in embryonic pattern formation.

Authors:  Daniele Soroldoni; David J Jörg; Luis G Morelli; David L Richmond; Johannes Schindelin; Frank Jülicher; Andrew C Oates
Journal:  Science       Date:  2014-07-11       Impact factor: 47.728

9.  Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons.

Authors:  Alexis B Webb; Nikhil Angelo; James E Huettner; Erik D Herzog
Journal:  Proc Natl Acad Sci U S A       Date:  2009-09-09       Impact factor: 11.205

10.  Cis-interactions between Notch and Delta generate mutually exclusive signalling states.

Authors:  David Sprinzak; Amit Lakhanpal; Lauren Lebon; Leah A Santat; Michelle E Fontes; Graham A Anderson; Jordi Garcia-Ojalvo; Michael B Elowitz
Journal:  Nature       Date:  2010-04-25       Impact factor: 49.962

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  34 in total

Review 1.  Communication codes in developmental signaling pathways.

Authors:  Pulin Li; Michael B Elowitz
Journal:  Development       Date:  2019-06-27       Impact factor: 6.868

2.  Light Control of Gene Expression Dynamics.

Authors:  Akihiro Isomura
Journal:  Adv Exp Med Biol       Date:  2021       Impact factor: 2.622

Review 3.  Towards a physical understanding of developmental patterning.

Authors:  Jose Negrete; Andrew C Oates
Journal:  Nat Rev Genet       Date:  2021-05-10       Impact factor: 53.242

Review 4.  Imaging and manipulating the segmentation clock.

Authors:  Kumiko Yoshioka-Kobayashi; Ryoichiro Kageyama
Journal:  Cell Mol Life Sci       Date:  2020-10-04       Impact factor: 9.261

5.  Excitable Dynamics and Yap-Dependent Mechanical Cues Drive the Segmentation Clock.

Authors:  Alexis Hubaud; Ido Regev; L Mahadevan; Olivier Pourquié
Journal:  Cell       Date:  2017-09-21       Impact factor: 41.582

6.  A segmentation clock patterns cellular differentiation in a bacterial biofilm.

Authors:  Kwang-Tao Chou; Dong-Yeon D Lee; Jian-Geng Chiou; Leticia Galera-Laporta; San Ly; Jordi Garcia-Ojalvo; Gürol M Süel
Journal:  Cell       Date:  2022-01-06       Impact factor: 41.582

7.  Diverse role of decoys on emergence and precision of oscillations in a biomolecular clock.

Authors:  Supravat Dey; Abhyudai Singh
Journal:  Biophys J       Date:  2021-11-11       Impact factor: 4.033

8.  From local resynchronization to global pattern recovery in the zebrafish segmentation clock.

Authors:  Koichiro Uriu; Bo-Kai Liao; Andrew C Oates; Luis G Morelli
Journal:  Elife       Date:  2021-02-15       Impact factor: 8.140

9.  Homology of process: developmental dynamics in comparative biology.

Authors:  James DiFrisco; Johannes Jaeger
Journal:  Interface Focus       Date:  2021-04-16       Impact factor: 3.906

10.  A dynamic, spatially periodic, micro-pattern of HES5 underlies neurogenesis in the mouse spinal cord.

Authors:  Veronica Biga; Joshua Hawley; Cerys S Manning; Nancy Papalopulu; Ximena Soto; Emma Johns; Daniel Han; Hayley Bennett; Antony D Adamson; Jochen Kursawe; Paul Glendinning
Journal:  Mol Syst Biol       Date:  2021-05       Impact factor: 13.068

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