Apical Constriction: Themes and Variations on a Cellular Mechanism Driving Morphogenesis

Overview

Journal Development

Specialty Biology

Date 2014 May 8

PMID 24803648

Citations 234

Authors

Adam C Martin

Bob Goldstein

Affiliations

Soon will be listed here.

Abstract

Apical constriction is a cell shape change that promotes tissue remodeling in a variety of homeostatic and developmental contexts, including gastrulation in many organisms and neural tube formation in vertebrates. In recent years, progress has been made towards understanding how the distinct cell biological processes that together drive apical constriction are coordinated. These processes include the contraction of actin-myosin networks, which generates force, and the attachment of actin networks to cell-cell junctions, which allows forces to be transmitted between cells. Different cell types regulate contractility and adhesion in unique ways, resulting in apical constriction with varying dynamics and subcellular organizations, as well as a variety of resulting tissue shape changes. Understanding both the common themes and the variations in apical constriction mechanisms promises to provide insight into the mechanics that underlie tissue morphogenesis.

Citing Articles

Cell signaling facilitates apical constriction by basolaterally recruiting Arp2/3 via Rac and WAVE.

Zhang P, Medwig-Kinney T, Breiner E, Perez J, Song A, Goldstein B J Cell Biol. 2025; 224(5).

PMID: 40042443 PMC: 11893165. DOI: 10.1083/jcb.202409133.

Local weakening of cell-extracellular matrix adhesion triggers basal epithelial tissue folding.

Valencia-Exposito A, Khalilgharibi N, Martinez-Abarca Millan A, Mao Y, Martin-Bermudo M EMBO J. 2025; .

PMID: 39962267 DOI: 10.1038/s44318-025-00384-6.

An actin bracket-induced elastoplastic transition determines epithelial folding irreversibility.

Teranishi A, Mori M, Ichiki R, Toda S, Shioi G, Okuda S Nat Commun. 2024; 15(1):10476.

PMID: 39668169 PMC: 11638340. DOI: 10.1038/s41467-024-54906-7.

Anillin tunes contractility and regulates barrier function during Rho flare-mediated tight junction remodeling.

Craig Z, Arnold T, Walworth K, Walkon A, Miller A bioRxiv. 2024; .

PMID: 39605712 PMC: 11601591. DOI: 10.1101/2024.11.20.624537.

Linking planar polarity signalling to actomyosin contractility during vertebrate neurulation.

Novotna S, Maia L, Radaszkiewicz K, Roudnicky P, Harnos J Open Biol. 2024; 14(11):240251.

PMID: 39561813 PMC: 11576107. DOI: 10.1098/rsob.240251.

References

Plageman Jr T, Chauhan B, Yang C, Jaudon F, Shang X, Zheng Y . A Trio-RhoA-Shroom3 pathway is required for apical constriction and epithelial invagination. Development. 2011; 138(23):5177-88. PMC: 3210497. DOI: 10.1242/dev.067868. View

Harrell J, Goldstein B . Internalization of multiple cells during C. elegans gastrulation depends on common cytoskeletal mechanisms but different cell polarity and cell fate regulators. Dev Biol. 2010; 350(1):1-12. PMC: 3022094. DOI: 10.1016/j.ydbio.2010.09.012. View

KNUDSEN K, Soler A, Johnson K, Wheelock M . Interaction of alpha-actinin with the cadherin/catenin cell-cell adhesion complex via alpha-catenin. J Cell Biol. 1995; 130(1):67-77. PMC: 2120515. DOI: 10.1083/jcb.130.1.67. View

Solon J, Kaya-Copur A, Colombelli J, Brunner D . Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell. 2009; 137(7):1331-42. DOI: 10.1016/j.cell.2009.03.050. View

Lee J, Marston D, Walston T, Hardin J, Halberstadt A, Goldstein B . Wnt/Frizzled signaling controls C. elegans gastrulation by activating actomyosin contractility. Curr Biol. 2006; 16(20):1986-97. PMC: 2989422. DOI: 10.1016/j.cub.2006.08.090. View

Luo W, Yu C, Lieu Z, Allard J, Mogilner A, Sheetz M . Analysis of the local organization and dynamics of cellular actin networks. J Cell Biol. 2013; 202(7):1057-73. PMC: 3787384. DOI: 10.1083/jcb.201210123. View

Wang Y, Khan Z, Kaschube M, Wieschaus E . Differential positioning of adherens junctions is associated with initiation of epithelial folding. Nature. 2012; 484(7394):390-3. PMC: 3597240. DOI: 10.1038/nature10938. View

Sherrard K, Robin F, Lemaire P, Munro E . Sequential activation of apical and basolateral contractility drives ascidian endoderm invagination. Curr Biol. 2010; 20(17):1499-510. PMC: 4088275. DOI: 10.1016/j.cub.2010.06.075. View

Parks S, Wieschaus E . The Drosophila gastrulation gene concertina encodes a G alpha-like protein. Cell. 1991; 64(2):447-58. DOI: 10.1016/0092-8674(91)90652-f. View

10.

Soares E Silva M, Depken M, Stuhrmann B, Korsten M, MacKintosh F, Koenderink G . Active multistage coarsening of actin networks driven by myosin motors. Proc Natl Acad Sci U S A. 2011; 108(23):9408-13. PMC: 3111259. DOI: 10.1073/pnas.1016616108. View

11.

Fanning A, Van Itallie C, Anderson J . Zonula occludens-1 and -2 regulate apical cell structure and the zonula adherens cytoskeleton in polarized epithelia. Mol Biol Cell. 2011; 23(4):577-90. PMC: 3279387. DOI: 10.1091/mbc.E11-09-0791. View

12.

Quintin S, Gally C, Labouesse M . Epithelial morphogenesis in embryos: asymmetries, motors and brakes. Trends Genet. 2008; 24(5):221-30. DOI: 10.1016/j.tig.2008.02.005. View

13.

Roh-Johnson M, Shemer G, Higgins C, McClellan J, Werts A, Tulu U . Triggering a cell shape change by exploiting preexisting actomyosin contractions. Science. 2012; 335(6073):1232-5. PMC: 3298882. DOI: 10.1126/science.1217869. View

14.

Anstrom J . Microfilaments, cell shape changes, and the formation of primary mesenchyme in sea urchin embryos. J Exp Zool. 1992; 264(3):312-22. DOI: 10.1002/jez.1402640310. View

15.

Williams M, Burdsal C, Periasamy A, Lewandoski M, Sutherland A . Mouse primitive streak forms in situ by initiation of epithelial to mesenchymal transition without migration of a cell population. Dev Dyn. 2011; 241(2):270-83. PMC: 3266444. DOI: 10.1002/dvdy.23711. View

16.

Murrell M, Gardel M . F-actin buckling coordinates contractility and severing in a biomimetic actomyosin cortex. Proc Natl Acad Sci U S A. 2012; 109(51):20820-5. PMC: 3529094. DOI: 10.1073/pnas.1214753109. View

17.

Rogers S, Wiedemann U, Hacker U, Turck C, Vale R . Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner. Curr Biol. 2004; 14(20):1827-33. DOI: 10.1016/j.cub.2004.09.078. View

18.

Hildebrand J, Soriano P . Shroom, a PDZ domain-containing actin-binding protein, is required for neural tube morphogenesis in mice. Cell. 1999; 99(5):485-97. DOI: 10.1016/s0092-8674(00)81537-8. View

19.

Toyama Y, Peralta X, Wells A, Kiehart D, Edwards G . Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science. 2008; 321(5896):1683-6. PMC: 2757114. DOI: 10.1126/science.1157052. View

20.

Lee J, Harland R . Endocytosis is required for efficient apical constriction during Xenopus gastrulation. Curr Biol. 2010; 20(3):253-8. PMC: 3310928. DOI: 10.1016/j.cub.2009.12.021. View