Intercellular coupling regulates the period of the segmentation clock

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...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Herrgen, L., Ares, S., Morelli, L.G., Schröter, C., Jülicher, F., Oates, A.C.
Formato: Artículo publishedVersion
Lenguaje:Inglés
Publicado: 2010
Materias:
Acceso en línea:http://hdl.handle.net/20.500.12110/paper_09609822_v20_n14_p1244_Herrgen
Aporte de:
id paperaa:paper_09609822_v20_n14_p1244_Herrgen
record_format dspace
spelling paperaa:paper_09609822_v20_n14_p1244_Herrgen2023-06-12T16:48:46Z Intercellular coupling regulates the period of the segmentation clock Curr. Biol. 2010;20(14):1244-1253 Herrgen, L. Ares, S. Morelli, L.G. Schröter, C. Jülicher, F. Oates, A.C. DEVBIO membrane protein Notch receptor protein signal peptide animal article biological model biological rhythm computer simulation fluorescence microscopy gene expression regulation metabolism morphogenesis physiology prenatal development signal transduction somite time zebra fish Animals Biological Clocks Body Patterning Computer Simulation Gene Expression Regulation, Developmental Intracellular Signaling Peptides and Proteins Membrane Proteins Microscopy, Fluorescence Models, Biological Receptors, Notch Signal Transduction Somites Time Factors Zebrafish Danio rerio Ixodida Vertebrata 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. All rights reserved. 2010 info:eu-repo/semantics/article info:ar-repo/semantics/artículo info:eu-repo/semantics/publishedVersion application/pdf eng info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/2.5/ar http://hdl.handle.net/20.500.12110/paper_09609822_v20_n14_p1244_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 Inglés
orig_language_str_mv eng
topic DEVBIO
membrane protein
Notch receptor
protein
signal peptide
animal
article
biological model
biological rhythm
computer simulation
fluorescence microscopy
gene expression regulation
metabolism
morphogenesis
physiology
prenatal development
signal transduction
somite
time
zebra fish
Animals
Biological Clocks
Body Patterning
Computer Simulation
Gene Expression Regulation, Developmental
Intracellular Signaling Peptides and Proteins
Membrane Proteins
Microscopy, Fluorescence
Models, Biological
Receptors, Notch
Signal Transduction
Somites
Time Factors
Zebrafish
Danio rerio
Ixodida
Vertebrata
Danio rerio
Ixodida
Vertebrata
spellingShingle DEVBIO
membrane protein
Notch receptor
protein
signal peptide
animal
article
biological model
biological rhythm
computer simulation
fluorescence microscopy
gene expression regulation
metabolism
morphogenesis
physiology
prenatal development
signal transduction
somite
time
zebra fish
Animals
Biological Clocks
Body Patterning
Computer Simulation
Gene Expression Regulation, Developmental
Intracellular Signaling Peptides and Proteins
Membrane Proteins
Microscopy, Fluorescence
Models, Biological
Receptors, Notch
Signal Transduction
Somites
Time Factors
Zebrafish
Danio rerio
Ixodida
Vertebrata
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
membrane protein
Notch receptor
protein
signal peptide
animal
article
biological model
biological rhythm
computer simulation
fluorescence microscopy
gene expression regulation
metabolism
morphogenesis
physiology
prenatal development
signal transduction
somite
time
zebra fish
Animals
Biological Clocks
Body Patterning
Computer Simulation
Gene Expression Regulation, Developmental
Intracellular Signaling Peptides and Proteins
Membrane Proteins
Microscopy, Fluorescence
Models, Biological
Receptors, Notch
Signal Transduction
Somites
Time Factors
Zebrafish
Danio rerio
Ixodida
Vertebrata
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. All rights reserved.
format Artículo
Artículo
publishedVersion
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
publishDate 2010
url http://hdl.handle.net/20.500.12110/paper_09609822_v20_n14_p1244_Herrgen
work_keys_str_mv AT herrgenl intercellularcouplingregulatestheperiodofthesegmentationclock
AT aress intercellularcouplingregulatestheperiodofthesegmentationclock
AT morellilg intercellularcouplingregulatestheperiodofthesegmentationclock
AT schroterc intercellularcouplingregulatestheperiodofthesegmentationclock
AT julicherf intercellularcouplingregulatestheperiodofthesegmentationclock
AT oatesac intercellularcouplingregulatestheperiodofthesegmentationclock
_version_ 1769810126983659520