Novel insights into palatal shelf elevation dynamics in normal mouse embryos

Development of the embryonic palate requires that the palatal shelves (PS), which extend from maxillary processes, to grow bilaterally and vertically alongside the tongue. This growth continues until embryonic day (E) 13.5, after which the PS elevate above the tongue and adhere, completing the proce...

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Main Authors: Jeremy P. Goering, Michael Moedritzer, Marta Stetsiv, Dona Greta Isai, Brittany M. Hufft-Martinez, An J. Tran, Zaid Umar, Madison K. Rickabaugh, Paul Keselman, Munish Chauhan, Pamela V. Tran, William M. Brooks, Kenneth J. Fischer, Andras Czirok, Irfan Saadi
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-02-01
Series:Frontiers in Cell and Developmental Biology
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Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2025.1532448/full
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author Jeremy P. Goering
Michael Moedritzer
Marta Stetsiv
Dona Greta Isai
Brittany M. Hufft-Martinez
An J. Tran
Zaid Umar
Madison K. Rickabaugh
Paul Keselman
Munish Chauhan
Pamela V. Tran
William M. Brooks
William M. Brooks
Kenneth J. Fischer
Andras Czirok
Andras Czirok
Irfan Saadi
Irfan Saadi
author_facet Jeremy P. Goering
Michael Moedritzer
Marta Stetsiv
Dona Greta Isai
Brittany M. Hufft-Martinez
An J. Tran
Zaid Umar
Madison K. Rickabaugh
Paul Keselman
Munish Chauhan
Pamela V. Tran
William M. Brooks
William M. Brooks
Kenneth J. Fischer
Andras Czirok
Andras Czirok
Irfan Saadi
Irfan Saadi
author_sort Jeremy P. Goering
collection DOAJ
description Development of the embryonic palate requires that the palatal shelves (PS), which extend from maxillary processes, to grow bilaterally and vertically alongside the tongue. This growth continues until embryonic day (E) 13.5, after which the PS elevate above the tongue and adhere, completing the process by E14.5. Current models indicate that this elevation process involves a complex vertical-to-horizontal PS reorientation. While earlier studies have implied that reorientation occurs rapidly, the precise timing has not been resolved. Time-restricted pregnancies with a 1-h resolution showed that in 97% of C57BL/6J embryos, the PS were unelevated at E14.0. However, 6 h later, at E14.25, the PS had completed elevation in 80% of embryos, indicating that the PS elevate in a rapid and constrained timeframe. Interestingly, all E14.25 embryos with unelevated PS (20%) were female, suggesting sex differences in C57BL/6J PS elevation. In FVB/NJ embryos, the elevation window started earlier (E13.875-E14.25), and without any sex differences. An intermediate stage with unilateral PS elevation was frequently observed. Magnetic resonance imaging (MRI) of various stages showed that PS elevation began with posterior bilateral bulges, which then progressed laterally and anteriorly over time. During elevation, we observed increased cell proliferation in the PS lingual region. Within the bulge, cell orientation was tilted towards the tongue, and actomyosin activity was increased, which together may participate in horizontal projection of the bulge. Thus, our data reveal novel insights into rapid dynamic changes during PS elevation, and lay the foundation for future studies of normal and abnormal palatogenesis.
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spelling doaj-art-5f585132947d4f2889483017017cb96e2025-02-11T06:59:59ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2025-02-011310.3389/fcell.2025.15324481532448Novel insights into palatal shelf elevation dynamics in normal mouse embryosJeremy P. Goering0Michael Moedritzer1Marta Stetsiv2Dona Greta Isai3Brittany M. Hufft-Martinez4An J. Tran5Zaid Umar6Madison K. Rickabaugh7Paul Keselman8Munish Chauhan9Pamela V. Tran10William M. Brooks11William M. Brooks12Kenneth J. Fischer13Andras Czirok14Andras Czirok15Irfan Saadi16Irfan Saadi17Department of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS, United StatesDepartment of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS, United StatesDepartment of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS, United StatesDepartment of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS, United StatesDepartment of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS, United StatesDepartment of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS, United StatesDepartment of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS, United StatesDepartment of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS, United StatesHoglund Biomedical Imaging Center, University of Kansas Medical Center, Kansas City, KS, United StatesHoglund Biomedical Imaging Center, University of Kansas Medical Center, Kansas City, KS, United StatesDepartment of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS, United StatesHoglund Biomedical Imaging Center, University of Kansas Medical Center, Kansas City, KS, United StatesDepartment of Neurology, University of Kansas Medical Center, Kansas City, KS, United StatesDepartment of Mechanical Engineering, University of Kansas, Lawrence, KS, United StatesDepartment of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS, United StatesDepartment of Biological Physics, Eotvos University, Budapest, HungaryDepartment of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS, United StatesInstitute for Reproductive and Developmental Sciences, University of Kansas Medical Center, Kansas City, KS, United StatesDevelopment of the embryonic palate requires that the palatal shelves (PS), which extend from maxillary processes, to grow bilaterally and vertically alongside the tongue. This growth continues until embryonic day (E) 13.5, after which the PS elevate above the tongue and adhere, completing the process by E14.5. Current models indicate that this elevation process involves a complex vertical-to-horizontal PS reorientation. While earlier studies have implied that reorientation occurs rapidly, the precise timing has not been resolved. Time-restricted pregnancies with a 1-h resolution showed that in 97% of C57BL/6J embryos, the PS were unelevated at E14.0. However, 6 h later, at E14.25, the PS had completed elevation in 80% of embryos, indicating that the PS elevate in a rapid and constrained timeframe. Interestingly, all E14.25 embryos with unelevated PS (20%) were female, suggesting sex differences in C57BL/6J PS elevation. In FVB/NJ embryos, the elevation window started earlier (E13.875-E14.25), and without any sex differences. An intermediate stage with unilateral PS elevation was frequently observed. Magnetic resonance imaging (MRI) of various stages showed that PS elevation began with posterior bilateral bulges, which then progressed laterally and anteriorly over time. During elevation, we observed increased cell proliferation in the PS lingual region. Within the bulge, cell orientation was tilted towards the tongue, and actomyosin activity was increased, which together may participate in horizontal projection of the bulge. Thus, our data reveal novel insights into rapid dynamic changes during PS elevation, and lay the foundation for future studies of normal and abnormal palatogenesis.https://www.frontiersin.org/articles/10.3389/fcell.2025.1532448/fullembryonic developmentpalatogenesispalatal shelf elevationcleft palateembryonic sex difference
spellingShingle Jeremy P. Goering
Michael Moedritzer
Marta Stetsiv
Dona Greta Isai
Brittany M. Hufft-Martinez
An J. Tran
Zaid Umar
Madison K. Rickabaugh
Paul Keselman
Munish Chauhan
Pamela V. Tran
William M. Brooks
William M. Brooks
Kenneth J. Fischer
Andras Czirok
Andras Czirok
Irfan Saadi
Irfan Saadi
Novel insights into palatal shelf elevation dynamics in normal mouse embryos
Frontiers in Cell and Developmental Biology
embryonic development
palatogenesis
palatal shelf elevation
cleft palate
embryonic sex difference
title Novel insights into palatal shelf elevation dynamics in normal mouse embryos
title_full Novel insights into palatal shelf elevation dynamics in normal mouse embryos
title_fullStr Novel insights into palatal shelf elevation dynamics in normal mouse embryos
title_full_unstemmed Novel insights into palatal shelf elevation dynamics in normal mouse embryos
title_short Novel insights into palatal shelf elevation dynamics in normal mouse embryos
title_sort novel insights into palatal shelf elevation dynamics in normal mouse embryos
topic embryonic development
palatogenesis
palatal shelf elevation
cleft palate
embryonic sex difference
url https://www.frontiersin.org/articles/10.3389/fcell.2025.1532448/full
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