Myosin II Controls Junction Fluctuations to Guide Epithelial Tissue Ordering

Overview

Journal Dev Cell

Publisher Cell Press

Specialties Cell Biology
Reproductive Medicine

Date 2017 Nov 7

PMID 29107560

Citations 59

Authors

Scott Curran

Charlotte Strandkvist

Jasper Bathmann

Marc de Gennes

Alexandre Kabla

Guillaume Salbreux

Buzz Baum

Affiliations

Soon will be listed here.

Abstract

Under conditions of homeostasis, dynamic changes in the length of individual adherens junctions (AJs) provide epithelia with the fluidity required to maintain tissue integrity in the face of intrinsic and extrinsic forces. While the contribution of AJ remodeling to developmental morphogenesis has been intensively studied, less is known about AJ dynamics in other circumstances. Here, we study AJ dynamics in an epithelium that undergoes a gradual increase in packing order, without concomitant large-scale changes in tissue size or shape. We find that neighbor exchange events are driven by stochastic fluctuations in junction length, regulated in part by junctional actomyosin. In this context, the developmental increase of isotropic junctional actomyosin reduces the rate of neighbor exchange, contributing to tissue order. We propose a model in which the local variance in tension between junctions determines whether actomyosin-based forces will inhibit or drive the topological transitions that either refine or deform a tissue.

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References

Nakayama M, Goto T, Sugimoto M, Nishimura T, Shinagawa T, Ohno S . Rho-kinase phosphorylates PAR-3 and disrupts PAR complex formation. Dev Cell. 2008; 14(2):205-15. DOI: 10.1016/j.devcel.2007.11.021. View

Georgiou M, Marinari E, Burden J, Baum B . Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Curr Biol. 2008; 18(21):1631-8. DOI: 10.1016/j.cub.2008.09.029. View

Brand A, Perrimon N . Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993; 118(2):401-15. DOI: 10.1242/dev.118.2.401. View

Busson D, Pret A . GAL4/UAS targeted gene expression for studying Drosophila Hedgehog signaling. Methods Mol Biol. 2007; 397:161-201. DOI: 10.1007/978-1-59745-516-9_13. View

Pare A, Vichas A, Fincher C, Mirman Z, Farrell D, Mainieri A . A positional Toll receptor code directs convergent extension in Drosophila. Nature. 2014; 515(7528):523-7. PMC: 4943584. DOI: 10.1038/nature13953. 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

Desai R, Sarpal R, Ishiyama N, Pellikka M, Ikura M, Tepass U . Monomeric α-catenin links cadherin to the actin cytoskeleton. Nat Cell Biol. 2013; 15(3):261-73. DOI: 10.1038/ncb2685. View

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

10.

Harris T, Tepass U . Adherens junctions: from molecules to morphogenesis. Nat Rev Mol Cell Biol. 2010; 11(7):502-14. DOI: 10.1038/nrm2927. View

11.

Verdier V, Guang-Chao-Chen , Settleman J . Rho-kinase regulates tissue morphogenesis via non-muscle myosin and LIM-kinase during Drosophila development. BMC Dev Biol. 2006; 6:38. PMC: 1552057. DOI: 10.1186/1471-213X-6-38. View

12.

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

13.

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

14.

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

15.

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

16.

Marinari E, Mehonic A, Curran S, Gale J, Duke T, Baum B . Live-cell delamination counterbalances epithelial growth to limit tissue overcrowding. Nature. 2012; 484(7395):542-5. DOI: 10.1038/nature10984. View

17.

Blankenship J, Backovic S, Sanny J, Weitz O, Zallen J . Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev Cell. 2006; 11(4):459-70. DOI: 10.1016/j.devcel.2006.09.007. View

18.

Gibson M, Patel A, Nagpal R, Perrimon N . The emergence of geometric order in proliferating metazoan epithelia. Nature. 2006; 442(7106):1038-41. DOI: 10.1038/nature05014. View

19.

Heisenberg C, Bellaiche Y . Forces in tissue morphogenesis and patterning. Cell. 2013; 153(5):948-62. DOI: 10.1016/j.cell.2013.05.008. View

20.

Mao Y, Tournier A, Hoppe A, Kester L, Thompson B, Tapon N . Differential proliferation rates generate patterns of mechanical tension that orient tissue growth. EMBO J. 2013; 32(21):2790-803. PMC: 3817460. DOI: 10.1038/emboj.2013.197. View