Intercellular coupling regulates the period of the segmentation clock

Autores
Herrgen, L.; Ares, S.; Morelli, L.G.; Schröter, C.; Jülicher, F.; Oates, A.C.
Año de publicación
2010
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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.
Fuente
Curr. Biol. 2010;20(14):1244-1253
Materia
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
Nivel de accesibilidad
acceso abierto
Condiciones de uso
http://creativecommons.org/licenses/by/2.5/ar
Repositorio
Biblioteca Digital (UBA-FCEN)
Institución
Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
OAI Identificador
paperaa:paper_09609822_v20_n14_p1244_Herrgen

id BDUBAFCEN_41e0f991cfef8ce16529f6aef00fb968
oai_identifier_str paperaa:paper_09609822_v20_n14_p1244_Herrgen
network_acronym_str BDUBAFCEN
repository_id_str 1896
network_name_str Biblioteca Digital (UBA-FCEN)
spelling Intercellular coupling regulates the period of the segmentation clockHerrgen, L.Ares, S.Morelli, L.G.Schröter, C.Jülicher, F.Oates, A.C.DEVBIOmembrane proteinNotch receptorproteinsignal peptideanimalarticlebiological modelbiological rhythmcomputer simulationfluorescence microscopygene expression regulationmetabolismmorphogenesisphysiologyprenatal developmentsignal transductionsomitetimezebra fishAnimalsBiological ClocksBody PatterningComputer SimulationGene Expression Regulation, DevelopmentalIntracellular Signaling Peptides and ProteinsMembrane ProteinsMicroscopy, FluorescenceModels, BiologicalReceptors, NotchSignal TransductionSomitesTime FactorsZebrafishDanio rerioIxodidaVertebrataDanio rerioIxodidaVertebrataBackground: 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.2010info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12110/paper_09609822_v20_n14_p1244_HerrgenCurr. Biol. 2010;20(14):1244-1253reponame:Biblioteca Digital (UBA-FCEN)instname:Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturalesinstacron:UBA-FCENenginfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by/2.5/ar2025-09-29T13:42:52Zpaperaa:paper_09609822_v20_n14_p1244_HerrgenInstitucionalhttps://digital.bl.fcen.uba.ar/Universidad públicaNo correspondehttps://digital.bl.fcen.uba.ar/cgi-bin/oaiserver.cgiana@bl.fcen.uba.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:18962025-09-29 13:42:53.651Biblioteca Digital (UBA-FCEN) - Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturalesfalse
dc.title.none.fl_str_mv Intercellular coupling regulates the period of the segmentation clock
title Intercellular coupling regulates the period of the segmentation clock
spellingShingle Intercellular coupling regulates the period of the segmentation clock
Herrgen, L.
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
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
dc.creator.none.fl_str_mv Herrgen, L.
Ares, S.
Morelli, L.G.
Schröter, C.
Jülicher, F.
Oates, A.C.
author Herrgen, L.
author_facet Herrgen, L.
Ares, S.
Morelli, L.G.
Schröter, C.
Jülicher, F.
Oates, A.C.
author_role author
author2 Ares, S.
Morelli, L.G.
Schröter, C.
Jülicher, F.
Oates, A.C.
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv 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
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
dc.description.none.fl_txt_mv 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.
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.
publishDate 2010
dc.date.none.fl_str_mv 2010
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12110/paper_09609822_v20_n14_p1244_Herrgen
url http://hdl.handle.net/20.500.12110/paper_09609822_v20_n14_p1244_Herrgen
dc.language.none.fl_str_mv eng
language eng
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
http://creativecommons.org/licenses/by/2.5/ar
eu_rights_str_mv openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/2.5/ar
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv Curr. Biol. 2010;20(14):1244-1253
reponame:Biblioteca Digital (UBA-FCEN)
instname:Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
instacron:UBA-FCEN
reponame_str Biblioteca Digital (UBA-FCEN)
collection Biblioteca Digital (UBA-FCEN)
instname_str Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
instacron_str UBA-FCEN
institution UBA-FCEN
repository.name.fl_str_mv Biblioteca Digital (UBA-FCEN) - Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
repository.mail.fl_str_mv ana@bl.fcen.uba.ar
_version_ 1844618734541471744
score 13.070432