Local and Tissue-scale Forces Drive Oriented Junction Growth During Tissue Extension

Overview

Journal Nat Cell Biol

Specialty Cell Biology

Date 2015 Sep 22

PMID 26389664

Citations 125

Authors

Claudio Collinet

Matteo Rauzi

Pierre-Francois Lenne

Thomas Lecuit

Affiliations

Soon will be listed here.

Abstract

Convergence-extension is a widespread morphogenetic process driven by polarized cell intercalation. In the Drosophila germ band, epithelial intercalation comprises loss of junctions between anterior-posterior neighbours followed by growth of new junctions between dorsal-ventral neighbours. Much is known about how active stresses drive polarized junction shrinkage. However, it is unclear how tissue convergence-extension emerges from local junction remodelling and what the specific role, if any, of junction growth is. Here we report that tissue convergence and extension correlate mostly with new junction growth. Simulations and in vivo mechanical perturbations reveal that junction growth is due to local polarized stresses driven by medial actomyosin contractions. Moreover, we find that tissue-scale pulling forces at the boundary with the invaginating posterior midgut actively participate in tissue extension by orienting junction growth. Thus, tissue extension is akin to a polarized fluid flow that requires parallel and concerted local and tissue-scale forces to drive junction growth and cell-cell displacement.

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References

Glickman N, Kimmel C, Jones M, Adams R . Shaping the zebrafish notochord. Development. 2003; 130(5):873-87. DOI: 10.1242/dev.00314. View

Thevenaz P, Ruttimann U, Unser M . A pyramid approach to subpixel registration based on intensity. IEEE Trans Image Process. 2008; 7(1):27-41. DOI: 10.1109/83.650848. View

Walck-Shannon E, Hardin J . Cell intercalation from top to bottom. Nat Rev Mol Cell Biol. 2013; 15(1):34-48. PMC: 4550482. DOI: 10.1038/nrm3723. View

Wu Y, Kanchanawong P, Zaidel-Bar R . Actin-delimited adhesion-independent clustering of E-cadherin forms the nanoscale building blocks of adherens junctions. Dev Cell. 2015; 32(2):139-54. DOI: 10.1016/j.devcel.2014.12.003. View

Hilgenfeldt S, Erisken S, Carthew R . Physical modeling of cell geometric order in an epithelial tissue. Proc Natl Acad Sci U S A. 2008; 105(3):907-11. PMC: 2242709. DOI: 10.1073/pnas.0711077105. View

Pilot F, Philippe J, Lemmers C, Chauvin J, Lecuit T . Developmental control of nuclear morphogenesis and anchoring by charleston, identified in a functional genomic screen of Drosophila cellularisation. Development. 2006; 133(4):711-23. DOI: 10.1242/dev.02251. View

Bambardekar K, Clement R, Blanc O, Chardes C, Lenne P . Direct laser manipulation reveals the mechanics of cell contacts in vivo. Proc Natl Acad Sci U S A. 2015; 112(5):1416-21. PMC: 4321260. DOI: 10.1073/pnas.1418732112. View

Farhadifar R, Roper J, Aigouy B, Eaton S, Julicher F . The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr Biol. 2007; 17(24):2095-104. DOI: 10.1016/j.cub.2007.11.049. View

Huang J, Zhou W, Dong W, Watson A, Hong Y . From the Cover: Directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering. Proc Natl Acad Sci U S A. 2009; 106(20):8284-9. PMC: 2688891. DOI: 10.1073/pnas.0900641106. View

10.

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

11.

Guillot C, Lecuit T . Adhesion disengagement uncouples intrinsic and extrinsic forces to drive cytokinesis in epithelial tissues. Dev Cell. 2013; 24(3):227-41. DOI: 10.1016/j.devcel.2013.01.010. View

12.

Bardet P, Guirao B, Paoletti C, Serman F, Leopold V, Bosveld F . PTEN controls junction lengthening and stability during cell rearrangement in epithelial tissue. Dev Cell. 2013; 25(5):534-46. DOI: 10.1016/j.devcel.2013.04.020. View

13.

Keller R, Shook D, Skoglund P . The forces that shape embryos: physical aspects of convergent extension by cell intercalation. Phys Biol. 2008; 5(1):015007. DOI: 10.1088/1478-3975/5/1/015007. View

14.

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

15.

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

16.

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

17.

Founounou N, Loyer N, Le Borgne R . Septins regulate the contractility of the actomyosin ring to enable adherens junction remodeling during cytokinesis of epithelial cells. Dev Cell. 2013; 24(3):242-55. DOI: 10.1016/j.devcel.2013.01.008. View

18.

Tada M, Heisenberg C . Convergent extension: using collective cell migration and cell intercalation to shape embryos. Development. 2012; 139(21):3897-904. DOI: 10.1242/dev.073007. View

19.

Wu S, Gomez G, Michael M, Verma S, Cox H, Lefevre J . Cortical F-actin stabilization generates apical-lateral patterns of junctional contractility that integrate cells into epithelia. Nat Cell Biol. 2014; 16(2):167-78. DOI: 10.1038/ncb2900. View

20.

Adams C, Nelson W, Smith S . Quantitative analysis of cadherin-catenin-actin reorganization during development of cell-cell adhesion. J Cell Biol. 1996; 135(6 Pt 2):1899-911. PMC: 2133977. DOI: 10.1083/jcb.135.6.1899. View