A framework for quantification and physical modeling of cell mixing applied to oscillator synchronization in vertebrate somitogenesis

Autores
Uriu, Koichiro; Bhavna, Rajasekaran; Oates, Andrew C.; Morelli, Luis Guillermo
Año de publicación
2017
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
In development and disease, cells move as they exchange signals. One example is found in vertebrate development, during which the timing of segment formation is set by a ‘segmentation clock’, in which oscillating gene expression is synchronized across a population of cells by Delta-Notch signaling. Delta-Notch signaling requires local cell-cell contact, but in the zebrafish embryonic tailbud, oscillating cells move rapidly, exchanging neighbors. Previous theoretical studies proposed that this relative movement or cell mixing might alter signaling and thereby enhance synchronization. However, it remains unclear whether the mixing timescale in the tissue is in the right range for this effect, because a framework to reliably measure the mixing timescale and compare it with signaling timescale is lacking. Here, we develop such a framework using a quantitative description of cell mixing without the need for an external reference frame and constructing a physical model of cell movement based on the data. Numerical simulations show that mixing with experimentally observed statistics enhances synchronization of coupled phase oscillators, suggesting that mixing in the tailbud is fast enough to affect the coherence of rhythmic gene expression. Our approach will find general application in analyzing the relative movements of communicating cells during development and disease.
Fil: Uriu, Koichiro. Kanazawa University; Japón
Fil: Bhavna, Rajasekaran. Max Planck Institute of Molecular Cell Biology and Genetics; Alemania. Max Planck Institute for the Physics of Complex Systems; Alemania
Fil: Oates, Andrew C.. Francis Crick Institute; Reino Unido. University College London; Reino Unido
Fil: Morelli, Luis Guillermo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigación en Biomedicina de Buenos Aires - Instituto Partner de la Sociedad Max Planck; Argentina. Max Planck Institute for Molecular Physiology; Alemania. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Física; Argentina
Materia
CELL MIXING
COUPLED OSCILLATORS
IMAGING SYNCHRONIZATION
SOMITOGENESIS
ZEBRAFISH
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/49814
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/49814
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling A framework for quantification and physical modeling of cell mixing applied to oscillator synchronization in vertebrate somitogenesisUriu, KoichiroBhavna, RajasekaranOates, Andrew C.Morelli, Luis GuillermoCELL MIXINGCOUPLED OSCILLATORSIMAGING SYNCHRONIZATIONSOMITOGENESISZEBRAFISHhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1In development and disease, cells move as they exchange signals. One example is found in vertebrate development, during which the timing of segment formation is set by a ‘segmentation clock’, in which oscillating gene expression is synchronized across a population of cells by Delta-Notch signaling. Delta-Notch signaling requires local cell-cell contact, but in the zebrafish embryonic tailbud, oscillating cells move rapidly, exchanging neighbors. Previous theoretical studies proposed that this relative movement or cell mixing might alter signaling and thereby enhance synchronization. However, it remains unclear whether the mixing timescale in the tissue is in the right range for this effect, because a framework to reliably measure the mixing timescale and compare it with signaling timescale is lacking. Here, we develop such a framework using a quantitative description of cell mixing without the need for an external reference frame and constructing a physical model of cell movement based on the data. Numerical simulations show that mixing with experimentally observed statistics enhances synchronization of coupled phase oscillators, suggesting that mixing in the tailbud is fast enough to affect the coherence of rhythmic gene expression. Our approach will find general application in analyzing the relative movements of communicating cells during development and disease.Fil: Uriu, Koichiro. Kanazawa University; JapónFil: Bhavna, Rajasekaran. Max Planck Institute of Molecular Cell Biology and Genetics; Alemania. Max Planck Institute for the Physics of Complex Systems; AlemaniaFil: Oates, Andrew C.. Francis Crick Institute; Reino Unido. University College London; Reino UnidoFil: Morelli, Luis Guillermo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigación en Biomedicina de Buenos Aires - Instituto Partner de la Sociedad Max Planck; Argentina. Max Planck Institute for Molecular Physiology; Alemania. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Física; ArgentinaCompany of Biologists2017-08info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/49814Uriu, Koichiro; Bhavna, Rajasekaran; Oates, Andrew C.; Morelli, Luis Guillermo; A framework for quantification and physical modeling of cell mixing applied to oscillator synchronization in vertebrate somitogenesis; Company of Biologists; Biology Open; 6; 8; 8-2017; 1235-12442046-6390CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/http://bio.biologists.org/content/6/8/1235info:eu-repo/semantics/altIdentifier/doi/10.1242/bio.025148info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:44:01Zoai:ri.conicet.gov.ar:11336/49814instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:44:01.33CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv A framework for quantification and physical modeling of cell mixing applied to oscillator synchronization in vertebrate somitogenesis
title A framework for quantification and physical modeling of cell mixing applied to oscillator synchronization in vertebrate somitogenesis
spellingShingle A framework for quantification and physical modeling of cell mixing applied to oscillator synchronization in vertebrate somitogenesis
Uriu, Koichiro
CELL MIXING
COUPLED OSCILLATORS
IMAGING SYNCHRONIZATION
SOMITOGENESIS
ZEBRAFISH
title_short A framework for quantification and physical modeling of cell mixing applied to oscillator synchronization in vertebrate somitogenesis
title_full A framework for quantification and physical modeling of cell mixing applied to oscillator synchronization in vertebrate somitogenesis
title_fullStr A framework for quantification and physical modeling of cell mixing applied to oscillator synchronization in vertebrate somitogenesis
title_full_unstemmed A framework for quantification and physical modeling of cell mixing applied to oscillator synchronization in vertebrate somitogenesis
title_sort A framework for quantification and physical modeling of cell mixing applied to oscillator synchronization in vertebrate somitogenesis
dc.creator.none.fl_str_mv Uriu, Koichiro
Bhavna, Rajasekaran
Oates, Andrew C.
Morelli, Luis Guillermo
author Uriu, Koichiro
author_facet Uriu, Koichiro
Bhavna, Rajasekaran
Oates, Andrew C.
Morelli, Luis Guillermo
author_role author
author2 Bhavna, Rajasekaran
Oates, Andrew C.
Morelli, Luis Guillermo
author2_role author
author
author
dc.subject.none.fl_str_mv CELL MIXING
COUPLED OSCILLATORS
IMAGING SYNCHRONIZATION
SOMITOGENESIS
ZEBRAFISH
topic CELL MIXING
COUPLED OSCILLATORS
IMAGING SYNCHRONIZATION
SOMITOGENESIS
ZEBRAFISH
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv In development and disease, cells move as they exchange signals. One example is found in vertebrate development, during which the timing of segment formation is set by a ‘segmentation clock’, in which oscillating gene expression is synchronized across a population of cells by Delta-Notch signaling. Delta-Notch signaling requires local cell-cell contact, but in the zebrafish embryonic tailbud, oscillating cells move rapidly, exchanging neighbors. Previous theoretical studies proposed that this relative movement or cell mixing might alter signaling and thereby enhance synchronization. However, it remains unclear whether the mixing timescale in the tissue is in the right range for this effect, because a framework to reliably measure the mixing timescale and compare it with signaling timescale is lacking. Here, we develop such a framework using a quantitative description of cell mixing without the need for an external reference frame and constructing a physical model of cell movement based on the data. Numerical simulations show that mixing with experimentally observed statistics enhances synchronization of coupled phase oscillators, suggesting that mixing in the tailbud is fast enough to affect the coherence of rhythmic gene expression. Our approach will find general application in analyzing the relative movements of communicating cells during development and disease.
Fil: Uriu, Koichiro. Kanazawa University; Japón
Fil: Bhavna, Rajasekaran. Max Planck Institute of Molecular Cell Biology and Genetics; Alemania. Max Planck Institute for the Physics of Complex Systems; Alemania
Fil: Oates, Andrew C.. Francis Crick Institute; Reino Unido. University College London; Reino Unido
Fil: Morelli, Luis Guillermo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigación en Biomedicina de Buenos Aires - Instituto Partner de la Sociedad Max Planck; Argentina. Max Planck Institute for Molecular Physiology; Alemania. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Física; Argentina
description In development and disease, cells move as they exchange signals. One example is found in vertebrate development, during which the timing of segment formation is set by a ‘segmentation clock’, in which oscillating gene expression is synchronized across a population of cells by Delta-Notch signaling. Delta-Notch signaling requires local cell-cell contact, but in the zebrafish embryonic tailbud, oscillating cells move rapidly, exchanging neighbors. Previous theoretical studies proposed that this relative movement or cell mixing might alter signaling and thereby enhance synchronization. However, it remains unclear whether the mixing timescale in the tissue is in the right range for this effect, because a framework to reliably measure the mixing timescale and compare it with signaling timescale is lacking. Here, we develop such a framework using a quantitative description of cell mixing without the need for an external reference frame and constructing a physical model of cell movement based on the data. Numerical simulations show that mixing with experimentally observed statistics enhances synchronization of coupled phase oscillators, suggesting that mixing in the tailbud is fast enough to affect the coherence of rhythmic gene expression. Our approach will find general application in analyzing the relative movements of communicating cells during development and disease.
publishDate 2017
dc.date.none.fl_str_mv 2017-08
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/11336/49814
Uriu, Koichiro; Bhavna, Rajasekaran; Oates, Andrew C.; Morelli, Luis Guillermo; A framework for quantification and physical modeling of cell mixing applied to oscillator synchronization in vertebrate somitogenesis; Company of Biologists; Biology Open; 6; 8; 8-2017; 1235-1244
2046-6390
CONICET Digital
CONICET
url http://hdl.handle.net/11336/49814
identifier_str_mv Uriu, Koichiro; Bhavna, Rajasekaran; Oates, Andrew C.; Morelli, Luis Guillermo; A framework for quantification and physical modeling of cell mixing applied to oscillator synchronization in vertebrate somitogenesis; Company of Biologists; Biology Open; 6; 8; 8-2017; 1235-1244
2046-6390
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://bio.biologists.org/content/6/8/1235
info:eu-repo/semantics/altIdentifier/doi/10.1242/bio.025148
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Company of Biologists
publisher.none.fl_str_mv Company of Biologists
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
_version_ 1844613385305456640
score 13.070432

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