Intercellular coupling regulates the period of the segmentation clock

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Background: 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 set...

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Autores principales: Herrgen, L., Ares, S., Morelli, L.G., Schröter, C., Jülicher, F., Oates, A.C.
Formato: JOUR
Lenguaje:English
Materias:
DEVBIO
Danio rerio
Ixodida
Vertebrata
Acceso en línea:http://hdl.handle.net/20.500.12110/paper_09609822_v20_n14_p1254_Herrgen
Aporte de:
Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA) de Universidad de Buenos Aires
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spelling todo:paper_09609822_v20_n14_p1254_Herrgen2023-10-03T15:54:05Z Intercellular coupling regulates the period of the segmentation clock Herrgen, L. Ares, S. Morelli, L.G. Schröter, C. Jülicher, F. Oates, A.C. DEVBIO Danio rerio Ixodida Vertebrata Background: 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. Results: 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 role of coupling delays in the clock, we predict and experimentally confirm an instability resulting from decreased coupling delay time. Conclusions: Synchronization of cells by Delta-Notch coupling regulates the collective period of the segmentation clock. Our identification of the first segmentation clock period mutants is a critical step toward a molecular understanding of temporal control in this system. We propose that collective control of period via delayed coupling may be a general feature of biological clocks. © 2010 Elsevier Ltd. JOUR English info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/2.5/ar http://hdl.handle.net/20.500.12110/paper_09609822_v20_n14_p1254_Herrgen
institution Universidad de Buenos Aires
institution_str I-28
repository_str R-134
collection Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA)
language English
orig_language_str_mv English
topic DEVBIO
Danio rerio
Ixodida
Vertebrata
spellingShingle DEVBIO
Danio rerio
Ixodida
Vertebrata
Herrgen, L.
Ares, S.
Morelli, L.G.
Schröter, C.
Jülicher, F.
Oates, A.C.
Intercellular coupling regulates the period of the segmentation clock
topic_facet DEVBIO
Danio rerio
Ixodida
Vertebrata
description Background: 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. Results: 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 role of coupling delays in the clock, we predict and experimentally confirm an instability resulting from decreased coupling delay time. Conclusions: Synchronization of cells by Delta-Notch coupling regulates the collective period of the segmentation clock. Our identification of the first segmentation clock period mutants is a critical step toward a molecular understanding of temporal control in this system. We propose that collective control of period via delayed coupling may be a general feature of biological clocks. © 2010 Elsevier Ltd.
format JOUR
author Herrgen, L.
Ares, S.
Morelli, L.G.
Schröter, C.
Jülicher, F.
Oates, A.C.
author_facet Herrgen, L.
Ares, S.
Morelli, L.G.
Schröter, C.
Jülicher, F.
Oates, A.C.
author_sort Herrgen, L.
title Intercellular coupling regulates the period of the segmentation clock
title_short Intercellular coupling regulates the period of the segmentation clock
title_full Intercellular coupling regulates the period of the segmentation clock
title_fullStr Intercellular coupling regulates the period of the segmentation clock
title_full_unstemmed Intercellular coupling regulates the period of the segmentation clock
title_sort intercellular coupling regulates the period of the segmentation clock
url http://hdl.handle.net/20.500.12110/paper_09609822_v20_n14_p1254_Herrgen
work_keys_str_mv AT herrgenl intercellularcouplingregulatestheperiodofthesegmentationclock
AT aress intercellularcouplingregulatestheperiodofthesegmentationclock
AT morellilg intercellularcouplingregulatestheperiodofthesegmentationclock
AT schroterc intercellularcouplingregulatestheperiodofthesegmentationclock
AT julicherf intercellularcouplingregulatestheperiodofthesegmentationclock
AT oatesac intercellularcouplingregulatestheperiodofthesegmentationclock
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