Literature DB >> 30309963

Ultrafast epithelial contractions provide insights into contraction speed limits and tissue integrity.

Shahaf Armon1, Matthew Storm Bull2, Andres Aranda-Diaz1, Manu Prakash3,4.   

Abstract

By definition of multicellularity, all animals need to keep their cells attached and intact, despite internal and external forces. Cohesion between epithelial cells provides this key feature. To better understand fundamental limits of this cohesion, we study the epithelium mechanics of an ultrathin (∼25 μm) primitive marine animal Trichoplax adhaerens, composed essentially of two flat epithelial layers. With no known extracellular matrix and no nerves or muscles, T. adhaerens has been claimed to be the "simplest known living animal," yet is still capable of coordinated locomotion and behavior. Here we report the discovery of the fastest epithelial cellular contractions known in any metazoan, to be found in T. adhaerens dorsal epithelium (50% shrinkage of apical cell area within one second, at least an order of magnitude faster than other known examples). Live imaging reveals emergent contractile patterns that are mostly sporadic single-cell events, but also include propagating contraction waves across the tissue. We show that cell contraction speed can be explained by current models of nonmuscle actin-myosin bundles without load, while the tissue architecture and unique mechanical properties are softening the tissue, minimizing the load on a contracting cell. We propose a hypothesis, in which the physiological role of the contraction dynamics is to resist external stresses while avoiding tissue rupture ("active cohesion"), a concept that can be further applied to engineering of active materials.

Entities:  

Keywords:  biomechanics; cell contractility; epithelium; metazoan evolution; tissue integrity

Mesh:

Substances:

Year:  2018        PMID: 30309963      PMCID: PMC6217427          DOI: 10.1073/pnas.1802934115

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  43 in total

1.  Molecular signatures for sex in the Placozoa.

Authors:  Ana Y Signorovitch; Stephen L Dellaporta; Leo W Buss
Journal:  Proc Natl Acad Sci U S A       Date:  2005-10-17       Impact factor: 11.205

2.  The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing.

Authors:  Reza Farhadifar; Jens-Christian Röper; Benoit Aigouy; Suzanne Eaton; Frank Jülicher
Journal:  Curr Biol       Date:  2007-12-18       Impact factor: 10.834

3.  Novel cell types, neurosecretory cells, and body plan of the early-diverging metazoan Trichoplax adhaerens.

Authors:  Carolyn L Smith; Frédérique Varoqueaux; Maike Kittelmann; Rita N Azzam; Benjamin Cooper; Christine A Winters; Michael Eitel; Dirk Fasshauer; Thomas S Reese
Journal:  Curr Biol       Date:  2014-06-19       Impact factor: 10.834

Review 4.  Actin cortex mechanics and cellular morphogenesis.

Authors:  Guillaume Salbreux; Guillaume Charras; Ewa Paluch
Journal:  Trends Cell Biol       Date:  2012-08-04       Impact factor: 20.808

5.  Thick filament length and isoform composition determine self-organized contractile units in actomyosin bundles.

Authors:  Todd Thoresen; Martin Lenz; Margaret L Gardel
Journal:  Biophys J       Date:  2013-02-05       Impact factor: 4.033

Review 6.  Forcing cells into shape: the mechanics of actomyosin contractility.

Authors:  Michael Murrell; Patrick W Oakes; Martin Lenz; Margaret L Gardel
Journal:  Nat Rev Mol Cell Biol       Date:  2015-07-01       Impact factor: 94.444

7.  Requirements for contractility in disordered cytoskeletal bundles.

Authors:  Martin Lenz; Margaret L Gardel; Aaron R Dinner
Journal:  New J Phys       Date:  2012-03-28       Impact factor: 3.729

8.  The Trichoplax genome and the nature of placozoans.

Authors:  Mansi Srivastava; Emina Begovic; Jarrod Chapman; Nicholas H Putnam; Uffe Hellsten; Takeshi Kawashima; Alan Kuo; Therese Mitros; Asaf Salamov; Meredith L Carpenter; Ana Y Signorovitch; Maria A Moreno; Kai Kamm; Jane Grimwood; Jeremy Schmutz; Harris Shapiro; Igor V Grigoriev; Leo W Buss; Bernd Schierwater; Stephen L Dellaporta; Daniel S Rokhsar
Journal:  Nature       Date:  2008-08-21       Impact factor: 49.962

9.  A positional Toll receptor code directs convergent extension in Drosophila.

Authors:  Adam C Paré; Athea Vichas; Christopher T Fincher; Zachary Mirman; Dene L Farrell; Avantika Mainieri; Jennifer A Zallen
Journal:  Nature       Date:  2014-11-02       Impact factor: 49.962

10.  Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses.

Authors:  Adriano Senatore; Thomas S Reese; Carolyn L Smith
Journal:  J Exp Biol       Date:  2017-09-15       Impact factor: 3.312

View more
  16 in total

1.  Sodium action potentials in placozoa: Insights into behavioral integration and evolution of nerveless animals.

Authors:  Daria Y Romanova; Ivan V Smirnov; Mikhail A Nikitin; Andrea B Kohn; Alisa I Borman; Alexey Y Malyshev; Pavel M Balaban; Leonid L Moroz
Journal:  Biochem Biophys Res Commun       Date:  2020-08-20       Impact factor: 3.575

Review 2.  Neural versus alternative integrative systems: molecular insights into origins of neurotransmitters.

Authors:  Leonid L Moroz; Daria Y Romanova; Andrea B Kohn
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2021-02-08       Impact factor: 6.237

3.  Sensitive detection of cell-derived force and collagen matrix tension in microtissues undergoing large-scale densification.

Authors:  Xiang Wang; Qiang Gao; Xiaoning Han; Bing Bu; Longfei Wang; Aoqi Li; Linhong Deng
Journal:  Proc Natl Acad Sci U S A       Date:  2021-09-07       Impact factor: 11.205

4.  Hidden cell diversity in Placozoa: ultrastructural insights from Hoilungia hongkongensis.

Authors:  Daria Y Romanova; Frédérique Varoqueaux; Dirk Fasshauer; Leonid L Moroz; Jean Daraspe; Mikhail A Nikitin; Michael Eitel
Journal:  Cell Tissue Res       Date:  2021-04-19       Impact factor: 4.051

5.  Coherent directed movement toward food modeled in Trichoplax, a ciliated animal lacking a nervous system.

Authors:  Carolyn L Smith; Thomas S Reese; Tzipe Govezensky; Rafael A Barrio
Journal:  Proc Natl Acad Sci U S A       Date:  2019-04-12       Impact factor: 11.205

Review 6.  Early animal evolution: a morphologist's view.

Authors:  Claus Nielsen
Journal:  R Soc Open Sci       Date:  2019-07-31       Impact factor: 2.963

7.  The chemical brain hypothesis for the origin of nervous systems.

Authors:  Gáspár Jékely
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2021-02-08       Impact factor: 6.237

Review 8.  Evolution of glutamatergic signaling and synapses.

Authors:  Leonid L Moroz; Mikhail A Nikitin; Pavlin G Poličar; Andrea B Kohn; Daria Y Romanova
Journal:  Neuropharmacology       Date:  2021-07-31       Impact factor: 5.273

9.  Neuronal coordination of motile cilia in locomotion and feeding.

Authors:  Milena Marinković; Jürgen Berger; Gáspár Jékely
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2019-12-30       Impact factor: 6.237

10.  The diversification and lineage-specific expansion of nitric oxide signaling in Placozoa: insights in the evolution of gaseous transmission.

Authors:  Leonid L Moroz; Daria Y Romanova; Mikhail A Nikitin; Dosung Sohn; Andrea B Kohn; Emilie Neveu; Frederique Varoqueaux; Dirk Fasshauer
Journal:  Sci Rep       Date:  2020-08-03       Impact factor: 4.379

View more

北京卡尤迪生物科技股份有限公司 © 2022-2023.