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...
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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 |
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_version_ |
1769810126983659520 |