Developmental function and state transitions of a gene expression oscillator in Caenorhabditis elegans.

Molecular Systems Biology
Milou Wm MeeuseHelge Großhans

Abstract

Gene expression oscillators can structure biological events temporally and spatially. Different biological functions benefit from distinct oscillator properties. Thus, finite developmental processes rely on oscillators that start and stop at specific times, a poorly understood behavior. Here, we have characterized a massive gene expression oscillator comprising > 3,700 genes in Caenorhabditis elegans larvae. We report that oscillations initiate in embryos, arrest transiently after hatching and in response to perturbation, and cease in adults. Experimental observation of the transitions between oscillatory and non-oscillatory states at high temporal resolution reveals an oscillator operating near a Saddle Node on Invariant Cycle (SNIC) bifurcation. These findings constrain the architecture and mathematical models that can represent this oscillator. They also reveal that oscillator arrests occur reproducibly in a specific phase. Since we find oscillations to be coupled to developmental processes, including molting, this characteristic of SNIC bifurcations endows the oscillator with the potential to halt larval development at defined intervals, and thereby execute a developmental checkpoint function.

References

Nov 1, 1983·Developmental Biology·J E SulstonJ N Thomson
Jul 28, 2001·Chronobiology International·L RensingP Ruoff
Dec 6, 2001·Nature Reviews. Molecular Cell Biology·J J TysonB Novak
Dec 26, 2001·Nucleic Acids Research·Ron EdgarAlex E Lash
May 17, 2002·Nature·Satchidananda PandaSteve A Kay
Nov 26, 2002·BioEssays : News and Reviews in Molecular, Cellular and Developmental Biology·John J TysonBela Novak
Dec 4, 2003·Biophysical Journal·Zhilin QuJames N Weiss
Aug 27, 2005·PLoS Biology·Alison R FrandGary Ruvkun
Apr 4, 2006·Biophysical Journal·Attila Csikász-NagyJohn J Tyson
Apr 11, 2006·PLoS Computational Biology·Raúl Guantes, Juan F Poyatos
May 5, 2006·Development·Anne-Françoise Ruaud, Jean-Louis Bessereau
Aug 19, 2007·Science·Ingmar H Riedel-KruseAndrew C Oates
Apr 23, 2008·Journal of the Royal Society, Interface·Emery ConradDaniel B Forger
Oct 28, 2008·Nature Genetics·Christian Frøkjaer-JensenErik M Jorgensen
Apr 14, 2009·Nature Methods·Daniel G GibsonHamilton O Smith
Mar 23, 2010·Biophysical Journal·Peter B JensenMogens H Jensen
Apr 8, 2010·Nucleic Acids Research·Kin Fai AuWing Hung Wong
Jul 2, 2010·Journal of the Royal Society, Interface·Oliver PurcellMario di Bernardo
Jul 6, 2010·BMC Bioinformatics·Renaud Gaujoux, Cathal Seoighe
Sep 11, 2010·Science·Miguel A Moreno-RisuenoPhilip N Benfey
Feb 1, 2012·Nature Methods·Christian Frøkjær-JensenErik M Jorgensen
Sep 17, 2013·Nature Genetics·Dong hyun KimAlexander van Oudenaarden
Jan 21, 2014·Molecular Cell·Gert-Jan HendriksHelge Großhans
Jan 28, 2014·Cell Reports·Dominic GrünNikolaus Rajewsky
Apr 20, 2014·PLoS Computational Biology·Bharath AnanthasubramaniamHanspeter Herzel
Jul 12, 2014·Science·Daniele SoroldoniAndrew C Oates
Oct 29, 2014·Proceedings of the National Academy of Sciences of the United States of America·Ray ZhangJohn B Hogenesch
Nov 25, 2014·Bioinformatics·Dimos GaidatzisMichael B Stadler
Jul 2, 2015·Journal of Visualized Experiments : JoVE·Michal TurekHenrik Bringmann
Jan 13, 2016·Development, Growth & Differentiation·Koichiro Uriu
Oct 30, 2016·Bioinformatics·Gang WuJohn B Hogenesch
Aug 26, 2016·Nature Communications·Nicola GrittiJeroen Sebastiaan van Zon
Aug 26, 2016·Biophysical Journal·Joshua D SalviA J Hudspeth
Feb 10, 2017·ELife·Thanh Thi Kim Vuong-BrenderMichel Labouesse
Jul 14, 2017·Worm·Vladimir Lažetić, David S Fay
Jul 27, 2017·Journal of Mathematical Neuroscience·Maria Luisa SaggioViktor K Jirsa

❮ Previous
Next ❯

Datasets Mentioned

BETA
WBCel215
WS230
GSM4448413

Methods Mentioned

BETA
transgenic
environmental stress
dissection
single cell sequencing

Software Mentioned

QuasR package
Scargle
Ilastik
pandas
_ CYCLE
seewave
JTK
QuasR
MetaCycle
STAR

Related Concepts

Related Feeds

Cell Checkpoints & Regulators

Cell cycle checkpoints are a series of complex checkpoint mechanisms that detect DNA abnormalities and ensure that DNA replication and repair are complete before cell division. They are primarily regulated by cyclins, cyclin-dependent kinases, and the anaphase-promoting complex/cyclosome. Here is the latest research.

Related Papers

The Review of Scientific Instruments
J C MOUZON
ELife
Bas J H M Rosier, Tom F A de Greef
Advances in Biological and Medical Physics
S R Caplan, A Naparstek
© 2021 Meta ULC. All rights reserved