Vertex Sliding Drives Intercalation by Radial Coupling of Adhesion and Actomyosin Networks During Germband Extension

Overview

Journal Elife

Specialty Biology

Date 2018 Jul 10

PMID 29985789

Citations 35

Authors

Timothy E Vanderleest

Celia M Smits

Yi Xie

Cayla E Jewett

J Todd Blankenship

Dinah Loerke

Affiliations

Soon will be listed here.

Abstract

Oriented cell intercalation is an essential developmental process that shapes tissue morphologies through the directional insertion of cells between their neighbors. Previous research has focused on properties of cellcell , while the function of tricellular has remained unaddressed. Here, we identify a highly novel mechanism in which vertices demonstrate independent sliding behaviors along cell peripheries to produce the topological deformations responsible for intercalation. Through systematic analysis, we find that the motion of vertices connected by contracting interfaces is not physically coupled, but instead possess strong radial coupling. E-cadherin and Myosin II exist in previously unstudied populations at cell vertices and undergo oscillatory cycles of accumulation and dispersion that are coordinated with changes in cell area. Additionally, peak enrichment of vertex E-cadherin/Myosin II coincides with interface length stabilization. Our results suggest a model in which asymmetric radial force balance directs the progressive, ratcheted motion of individual vertices to drive intercalation.

Citing Articles

Prickle2 regulates apical junction remodeling and tissue fluidity during vertebrate neurulation.

Matsuda M, Sokol S J Cell Biol. 2025; 224(4).

PMID: 39951022 PMC: 11827586. DOI: 10.1083/jcb.202407025.

Rectification of planar orientation angle switches behavior and replenishes contractile junctions.

Linvill K, Russell L, Vanderleest T, Miao H, Xie Y, Blankenship J J Cell Biol. 2025; 224(4.

PMID: 39846952 PMC: 11756375. DOI: 10.1083/jcb.202309069.

The geometric basis of epithelial convergent extension.

Brauns F, Claussen N, Lefebvre M, Wieschaus E, Shraiman B Elife. 2024; 13.

PMID: 39699945 PMC: 11658770. DOI: 10.7554/eLife.95521.

Nuclei as mechanical bumpers during epithelial remodeling.

de Leeuw N, Budhathoki R, Russell L, Loerke D, Blankenship J J Cell Biol. 2024; 223(12).

PMID: 39325019 PMC: 11450824. DOI: 10.1083/jcb.202405078.

PCP and Septins govern the polarized organization of the actin cytoskeleton during convergent extension.

Devitt C, Weng S, Bejar-Padilla V, Alvarado J, Wallingford J Curr Biol. 2024; 34(3):615-622.e4.

PMID: 38199065 PMC: 10887425. DOI: 10.1016/j.cub.2023.12.025.

References

Tudela C, Martinez T, Perez R, Aparicio M, Maestro C, Del Rio A . TGF-beta3 is required for the adhesion and intercalation of medial edge epithelial cells during palate fusion. Int J Dev Biol. 2002; 46(3):333-6. View

Tetley R, Blanchard G, Fletcher A, Adams R, Sanson B . Unipolar distributions of junctional Myosin II identify cell stripe boundaries that drive cell intercalation throughout Drosophila axis extension. Elife. 2016; 5. PMC: 4915814. DOI: 10.7554/eLife.12094. View

Wang Y, Khan Z, Wieschaus E . Distinct Rap1 activity states control the extent of epithelial invagination via α-catenin. Dev Cell. 2013; 25(3):299-309. PMC: 3741050. DOI: 10.1016/j.devcel.2013.04.002. View

Bosveld F, Markova O, Guirao B, Martin C, Wang Z, Pierre A . Epithelial tricellular junctions act as interphase cell shape sensors to orient mitosis. Nature. 2016; 530(7591):495-8. PMC: 5450930. DOI: 10.1038/nature16970. View

Resnik-Docampo M, Koehler C, Clark R, Schinaman J, Sauer V, Wong D . Tricellular junctions regulate intestinal stem cell behaviour to maintain homeostasis. Nat Cell Biol. 2016; 19(1):52-59. PMC: 6336109. DOI: 10.1038/ncb3454. View

Kasza K, Farrell D, Zallen J . Spatiotemporal control of epithelial remodeling by regulated myosin phosphorylation. Proc Natl Acad Sci U S A. 2014; 111(32):11732-7. PMC: 4136583. DOI: 10.1073/pnas.1400520111. View

Curran S, Strandkvist C, Bathmann J, de Gennes M, Kabla A, Salbreux G . Myosin II Controls Junction Fluctuations to Guide Epithelial Tissue Ordering. Dev Cell. 2017; 43(4):480-492.e6. PMC: 5703647. DOI: 10.1016/j.devcel.2017.09.018. View

Weber S, Thompson M, Moerner W, Spakowitz A, Theriot J . Analytical tools to distinguish the effects of localization error, confinement, and medium elasticity on the velocity autocorrelation function. Biophys J. 2012; 102(11):2443-50. PMC: 3368140. DOI: 10.1016/j.bpj.2012.03.062. View

Wang J, Mark S, Zhang X, Qian D, Yoo S, Radde-Gallwitz K . Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway. Nat Genet. 2005; 37(9):980-5. PMC: 1413588. DOI: 10.1038/ng1622. View

10.

Simoes S, Oh Y, Wang M, Fernandez-Gonzalez R, Tepass U . Myosin II promotes the anisotropic loss of the apical domain during neuroblast ingression. J Cell Biol. 2017; 216(5):1387-1404. PMC: 5412560. DOI: 10.1083/jcb.201608038. View

11.

Martin A, Kaschube M, Wieschaus E . Pulsed contractions of an actin-myosin network drive apical constriction. Nature. 2008; 457(7228):495-9. PMC: 2822715. DOI: 10.1038/nature07522. View

12.

Staehelin L . Further observations on the fine structure of freeze-cleaved tight junctions. J Cell Sci. 1973; 13(3):763-86. DOI: 10.1242/jcs.13.3.763. View

13.

Levayer R, Pelissier-Monier A, Lecuit T . Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis. Nat Cell Biol. 2011; 13(5):529-40. DOI: 10.1038/ncb2224. View

14.

Collinet C, Rauzi M, Lenne P, Lecuit T . Local and tissue-scale forces drive oriented junction growth during tissue extension. Nat Cell Biol. 2015; 17(10):1247-58. DOI: 10.1038/ncb3226. View

15.

Takeda M, Sami M, Wang Y . A homeostatic apical microtubule network shortens cells for epithelial folding via a basal polarity shift. Nat Cell Biol. 2017; 20(1):36-45. DOI: 10.1038/s41556-017-0001-3. View

16.

Bertet C, Sulak L, Lecuit T . Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature. 2004; 429(6992):667-71. DOI: 10.1038/nature02590. View

17.

Schulte J, Tepass U, Auld V . Gliotactin, a novel marker of tricellular junctions, is necessary for septate junction development in Drosophila. J Cell Biol. 2003; 161(5):991-1000. PMC: 2172969. DOI: 10.1083/jcb.200303192. View

18.

Munjal A, Philippe J, Munro E, Lecuit T . A self-organized biomechanical network drives shape changes during tissue morphogenesis. Nature. 2015; 524(7565):351-5. DOI: 10.1038/nature14603. View

19.

Irvine K, Wieschaus E . Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes. Development. 1994; 120(4):827-41. DOI: 10.1242/dev.120.4.827. View

20.

Rauzi M, Lenne P, Lecuit T . Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature. 2010; 468(7327):1110-4. DOI: 10.1038/nature09566. View