Intercellular coupling regulates the period of the segmentation clock

Current Biology : CB
Leah HerrgenAndrew C Oates

Abstract

Coupled biological oscillators can tick with the same period. How this collective period is established is a key question in understanding biological clocks. We explore this question in the segmentation clock, a population of coupled cellular oscillators in the vertebrate embryo that sets the rhythm of somitogenesis, the morphological segmentation of the body axis. The oscillating cells of the zebrafish segmentation clock are thought to possess noisy autonomous periods, which are synchronized by intercellular coupling through the Delta-Notch pathway. Here we ask whether Delta-Notch coupling additionally influences the collective period of the segmentation clock. Using multiple-embryo time-lapse microscopy, we show that disruption of Delta-Notch intercellular coupling increases the period of zebrafish somitogenesis. Embryonic segment length and the spatial wavelength of oscillating gene expression also increase correspondingly, indicating an increase in the segmentation clock's period. Using a theory based on phase oscillators in which the collective period self-organizes because of time delays in coupling, we estimate the cell-autonomous period, the coupling strength, and the coupling delay from our data. Further supporting the...Continue Reading

References

Sep 1, 1988·The Quarterly Review of Biology·J Buck
Dec 1, 1973·Genetics·J F Feldman, M N Hoyle
Dec 1, 1972·Proceedings of the National Academy of Sciences of the United States of America·L Mets, L Bogorad
Sep 1, 1971·Proceedings of the National Academy of Sciences of the United States of America·R J Konopka, S Benzer
Jul 1, 1967·Journal of Theoretical Biology·A T Winfree
Oct 7, 1981·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·J Cooke
Dec 1, 1996·Development·M Furutani-SeikiC Nüsslein-Volhard
Apr 20, 2000·The Journal of Biological Chemistry·I ZieglerT McDonaldo
Nov 30, 2000·Journal of Theoretical Biology·M KaernA Hunding
Jun 29, 2001·Mechanisms of Development·V E PrinceT F Vogt
Mar 16, 2002·Journal of Theoretical Biology·J Jaeger, B C Goodwin
Mar 16, 2005·Developmental Biology·Andrew C OatesRobert K Ho
Apr 6, 2005·Developmental Cell·Dörthe JülichUNKNOWN Tübingen 2000 Screen Consortium
May 21, 2005·Physical Review Letters·H-J WünscheI Fischer
Aug 30, 2005·Developmental Biology·Dörthe JülichUNKNOWN Tübingen 2000 Screen Consortium
Jan 25, 2006·Proceedings of the National Academy of Sciences of the United States of America·Yoshito MasamizuRyoichiro Kageyama
Jun 9, 2006·Nature·Kazuki HorikawaHiroyuki Takeda
Feb 20, 2007·PLoS Computational Biology·Olivier Cinquin
Jun 20, 2007·Journal of Theoretical Biology·Hendrik B TiedemannMartin Hrabé de Angelis
Aug 19, 2007·Science·Ingmar H Riedel-KruseAndrew C Oates
Dec 21, 2007·The Journal of Investigative Dermatology·Maksim V Plikus, Cheng-Ming Chuong
Feb 12, 2008·Developmental Dynamics : an Official Publication of the American Association of Anatomists·Christian SchröterAndrew C Oates
Mar 1, 2008·Journal of Theoretical Biology·Albert Goldbeter, Olivier Pourquié
Apr 11, 2008·Neuron·Hiromi ShimojoRyoichiro Kageyama
Apr 17, 2008·Nature Reviews. Genetics·Mary-Lee Dequéant, Olivier Pourquié
Jun 3, 2008·The Journal of Chemical Physics·André LeierKevin Burrage
Jun 20, 2008·Nature·Céline GomezOlivier Pourquié
Aug 5, 2008·Proceedings of the National Academy of Sciences of the United States of America·Sara Farrah HeussFrédérique Logeat
Jan 29, 2009·Journal of Theoretical Biology·Koichiro UriuYoh Iwasa
Feb 25, 2009·Journal of Theoretical Biology·Aitor González, Ryoichiro Kageyama

❮ Previous
Next ❯

Citations

Jul 19, 2013·Studies in History and Philosophy of Biological and Biomedical Sciences·Ingo Brigandt
Jul 29, 2011·Molecular Biology of the Cell·Woong KimYasumasa Bessho
Apr 14, 2012·Science·Luis G MorelliAndrew C Oates
Jun 28, 2012·Development·Miguel MarotoJ Kim Dale
Aug 23, 2012·PLoS Biology·Christian SchröterAndrew C Oates
Mar 27, 2013·Annual Review of Biophysics·Pau Rué, Jordi Garcia-Ojalvo
Apr 23, 2013·Theoretical Biology & Medical Modelling·Hong-yan WangYu-xin Li
Feb 13, 2016·Cell·Charisios D Tsiairis, Alexander Aulehla
Jan 13, 2016·Development, Growth & Differentiation·Koichiro Uriu
Jan 26, 2016·Seminars in Cell & Developmental Biology·Caroline J SheebaIsabel Palmeirim
Mar 8, 2013·Current Opinion in Genetics & Development·Yukiko Harima, Ryoichiro Kageyama
Jun 4, 2011·Journal of Theoretical Biology·Philip J MurrayRuth E Baker
Mar 9, 2011·Journal of Theoretical Biology·Rebecca H ChisholmPaul M Whitington
Jul 17, 2014·Biophysical Journal·Koichiro Uriu, Luis G Morelli
Jun 14, 2012·Birth Defects Research. Part C, Embryo Today : Reviews·Christian Tendeng
Jun 27, 2013·Wiley Interdisciplinary Reviews. Developmental Biology·Ryoichiro KageyamaYukiko Harima
Oct 28, 2014·IEEE Transactions on Automatic Control·Yongqiang WangFrancis J Doyle
Nov 15, 2012·Current Opinion in Genetics & Development·David L Richmond, Andrew C Oates
Jun 5, 2014·BioMed Research International·Tatiana P ResendeIsabel Palmeirim
May 9, 2014·Biophysical Journal·Jae Kyoung KimKrešimir Josić
Jul 6, 2014·Seminars in Cell & Developmental Biology·Anna L Keyte, Kathleen K Smith
Oct 23, 2012·Developmental Biology·Philip J MurrayRuth E Baker
Dec 9, 2014·Seminars in Cell & Developmental Biology·Kanu WahiSusan E Cole
Jun 16, 2016·Nature Communications·Bo-Kai LiaoAndrew C Oates
Nov 27, 2016·Arthropod Structure & Development·Bo-Kai Liao, Andrew C Oates
Feb 18, 2017·IEEE Transactions on Nanobioscience·Guang LingYonghong Wu
Jun 20, 2017·Development, Growth & Differentiation·Koichiro Uriu, Luis G Morelli
Dec 3, 2017·Nature Communications·Sandra RichterAndrew C Oates
Jan 20, 2018·Physical Review. E·Gabriela PetrungaroLuis G Morelli
Oct 23, 2014·Nature Reviews. Molecular Cell Biology·Alexis Hubaud, Olivier Pourquié
Jul 7, 2011·Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics·Víctor M EguíluzAlex Arenas
Sep 26, 2012·Physical Review Letters·Saúl AresFrank Jülicher

❮ Previous
Next ❯

Related Concepts

Related Feeds

Advanced Imaging of Cellular Signaling

Cell signaling is a vital mechanism for communication within cells and outside with the environment. Several different signaling pathways have been found and advanced imaging techniques are being developed to visualize the molecules involved in these signaling pathways. Find the latest research in advanced imaging of cellular signaling here.