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 ac...
Saved in:
| Main Authors: | , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2008-10-01
|
| Series: | PLoS Biology |
| Online Access: | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.0060247&type=printable |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849686713970982912 |
|---|---|
| author | Evan A Zamir Brenda J Rongish Charles D Little |
| author_facet | Evan A Zamir Brenda J Rongish Charles D Little |
| author_sort | Evan A Zamir |
| collection | DOAJ |
| 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. |
| format | Article |
| id | doaj-art-fce6777a65464df9b9bc1319c1947df7 |
| institution | DOAJ |
| issn | 1544-9173 1545-7885 |
| language | English |
| publishDate | 2008-10-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj-art-fce6777a65464df9b9bc1319c1947df72025-08-20T03:22:35ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852008-10-01610e24710.1371/journal.pbio.0060247The ECM moves during primitive streak formation--computation of ECM versus cellular motion.Evan A ZamirBrenda J RongishCharles D LittleGalileo 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.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.0060247&type=printable |
| spellingShingle | Evan A Zamir Brenda J Rongish Charles D Little The ECM moves during primitive streak formation--computation of ECM versus cellular motion. PLoS Biology |
| 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 |
| url | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.0060247&type=printable |
| work_keys_str_mv | AT evanazamir theecmmovesduringprimitivestreakformationcomputationofecmversuscellularmotion AT brendajrongish theecmmovesduringprimitivestreakformationcomputationofecmversuscellularmotion AT charlesdlittle theecmmovesduringprimitivestreakformationcomputationofecmversuscellularmotion AT evanazamir ecmmovesduringprimitivestreakformationcomputationofecmversuscellularmotion AT brendajrongish ecmmovesduringprimitivestreakformationcomputationofecmversuscellularmotion AT charlesdlittle ecmmovesduringprimitivestreakformationcomputationofecmversuscellularmotion |