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The ECM Moves during Primitive Streak Formation—Computation of ECM Versus Cellular Motion

Galileo described the concept of motion relativity—motion with respect to a reference frame—in 1632. He noted that a person below deck would be unable to discern whether the boat was moving. Embryologists, while recognizing that embryonic tissues undergo large-scale deformations, have failed to acco...

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Detalles Bibliográficos
Autores principales: Zamir, Evan A, Rongish, Brenda J, Little, Charles D
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2008
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2567004/
https://www.ncbi.nlm.nih.gov/pubmed/18922043
http://dx.doi.org/10.1371/journal.pbio.0060247
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author Zamir, Evan A
Rongish, Brenda J
Little, Charles D
author_facet Zamir, Evan A
Rongish, Brenda J
Little, Charles D
author_sort Zamir, Evan A
collection PubMed
description Galileo described the concept of motion relativity—motion with respect to a reference frame—in 1632. He noted that a person below deck would be unable to discern whether the boat was moving. Embryologists, while recognizing that embryonic tissues undergo large-scale deformations, have failed to account for relative motion when analyzing cell motility data. A century of scientific articles has advanced the concept that embryonic cells move (“migrate”) in an autonomous fashion such that, as time progresses, the cells and their progeny assemble an embryo. In sharp contrast, the motion of the surrounding extracellular matrix scaffold has been largely ignored/overlooked. We developed computational/optical methods that measure the extent embryonic cells move relative to the extracellular matrix. Our time-lapse data show that epiblastic cells largely move in concert with a sub-epiblastic extracellular matrix during stages 2 and 3 in primitive streak quail embryos. In other words, there is little cellular motion relative to the extracellular matrix scaffold—both components move together as a tissue. The extracellular matrix displacements exhibit bilateral vortical motion, convergence to the midline, and extension along the presumptive vertebral axis—all patterns previously attributed solely to cellular “migration.” Our time-resolved data pose new challenges for understanding how extracellular chemical (morphogen) gradients, widely hypothesized to guide cellular trajectories at early gastrulation stages, are maintained in this dynamic extracellular environment. We conclude that models describing primitive streak cellular guidance mechanisms must be able to account for sub-epiblastic extracellular matrix displacements.
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spelling pubmed-25670042008-10-28 The ECM Moves during Primitive Streak Formation—Computation of ECM Versus Cellular Motion Zamir, Evan A Rongish, Brenda J Little, Charles D PLoS Biol Research Article Galileo described the concept of motion relativity—motion with respect to a reference frame—in 1632. He noted that a person below deck would be unable to discern whether the boat was moving. Embryologists, while recognizing that embryonic tissues undergo large-scale deformations, have failed to account for relative motion when analyzing cell motility data. A century of scientific articles has advanced the concept that embryonic cells move (“migrate”) in an autonomous fashion such that, as time progresses, the cells and their progeny assemble an embryo. In sharp contrast, the motion of the surrounding extracellular matrix scaffold has been largely ignored/overlooked. We developed computational/optical methods that measure the extent embryonic cells move relative to the extracellular matrix. Our time-lapse data show that epiblastic cells largely move in concert with a sub-epiblastic extracellular matrix during stages 2 and 3 in primitive streak quail embryos. In other words, there is little cellular motion relative to the extracellular matrix scaffold—both components move together as a tissue. The extracellular matrix displacements exhibit bilateral vortical motion, convergence to the midline, and extension along the presumptive vertebral axis—all patterns previously attributed solely to cellular “migration.” Our time-resolved data pose new challenges for understanding how extracellular chemical (morphogen) gradients, widely hypothesized to guide cellular trajectories at early gastrulation stages, are maintained in this dynamic extracellular environment. We conclude that models describing primitive streak cellular guidance mechanisms must be able to account for sub-epiblastic extracellular matrix displacements. Public Library of Science 2008-10 2008-10-14 /pmc/articles/PMC2567004/ /pubmed/18922043 http://dx.doi.org/10.1371/journal.pbio.0060247 Text en © 2008 Zamir et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Zamir, Evan A
Rongish, Brenda J
Little, Charles D
The ECM Moves during Primitive Streak Formation—Computation of ECM Versus Cellular Motion
title The ECM Moves during Primitive Streak Formation—Computation of ECM Versus Cellular Motion
title_full The ECM Moves during Primitive Streak Formation—Computation of ECM Versus Cellular Motion
title_fullStr The ECM Moves during Primitive Streak Formation—Computation of ECM Versus Cellular Motion
title_full_unstemmed The ECM Moves during Primitive Streak Formation—Computation of ECM Versus Cellular Motion
title_short The ECM Moves during Primitive Streak Formation—Computation of ECM Versus Cellular Motion
title_sort ecm moves during primitive streak formation—computation of ecm versus cellular motion
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2567004/
https://www.ncbi.nlm.nih.gov/pubmed/18922043
http://dx.doi.org/10.1371/journal.pbio.0060247
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