Tissue-Scale Mechanical Coupling Reduces Morphogenetic Noise to Ensure Precision during Epithelial Folding.

Abstract:

:Morphological constancy is universal in developing systems. It is unclear whether precise morphogenesis stems from faithful mechanical interpretation of gene expression patterns. We investigate the formation of the cephalic furrow, an epithelial fold that is precisely positioned with a linear morphology. Fold initiation is specified by a precise genetic code with single-cell row resolution. This positional code activates and spatially confines lateral myosin contractility to induce folding. However, 20% of initiating cells are mis-specified because of fluctuating myosin intensities at the cellular level. Nevertheless, the furrow remains linearly aligned. We find that lateral myosin is planar polarized, integrating contractile membrane interfaces into supracellular "ribbons." Local reduction of mechanical coupling at the "ribbons" using optogenetics decreases furrow linearity. Furthermore, 3D vertex modeling indicates that polarized, interconnected contractility confers morphological robustness against noise. Thus, tissue-scale mechanical coupling functions as a denoising mechanism to ensure morphogenetic precision despite noisy decoding of positional information.

journal_name

Dev Cell

journal_title

Developmental cell

authors

Eritano AS,Bromley CL,Bolea Albero A,Schütz L,Wen FL,Takeda M,Fukaya T,Sami MM,Shibata T,Lemke S,Wang YC

doi

10.1016/j.devcel.2020.02.012

subject

Has Abstract

pub_date

2020-04-20 00:00:00

pages

212-228.e12

issue

2

eissn

1534-5807

issn

1878-1551

pii

S1534-5807(20)30108-8

journal_volume

53

pub_type

杂志文章
  • The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis.

    abstract::Cytokinins affect plant immunity to various pathogens; however, the mechanisms coupling plant-derived cytokinins to pathogen responses have been elusive. Here, we found that plant-derived cytokinins promote resistance of Arabidopsis to Pseudomonas syringae pv. tomato DC3000 (Pst). Modulated cytokinin levels or signali...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2010.07.011

    authors: Choi J,Huh SU,Kojima M,Sakakibara H,Paek KH,Hwang I

    更新日期:2010-08-17 00:00:00

  • HIF1α Represses Cell Stress Pathways to Allow Proliferation of Hypoxic Fetal Cardiomyocytes.

    abstract::Transcriptional mediators of cell stress pathways, including HIF1α, ATF4, and p53, are key to normal development and play critical roles in disease, including ischemia and cancer. Despite their importance, mechanisms by which pathways mediated by these transcription factors interact with one another are not fully unde...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2015.04.021

    authors: Guimarães-Camboa N,Stowe J,Aneas I,Sakabe N,Cattaneo P,Henderson L,Kilberg MS,Johnson RS,Chen J,McCulloch AD,Nobrega MA,Evans SM,Zambon AC

    更新日期:2015-06-08 00:00:00

  • Membrane Mechanics in Living Cells.

    abstract::The combination of fluid and mechanical properties exhibited by cell membranes enables a wealth of physical phenomena, many of which also have biological functions. A recent study in Cell (Shi et al., 2018) now shows that membrane tension in the cell may not be as simple as it first seemed. ...

    journal_title:Developmental cell

    pub_type: 评论,杂志文章

    doi:10.1016/j.devcel.2018.12.011

    authors: Groves JT

    更新日期:2019-01-07 00:00:00

  • SrGAP2-Dependent Integration of Membrane Geometry and Slit-Robo-Repulsive Cues Regulates Fibroblast Contact Inhibition of Locomotion.

    abstract::Migrating fibroblasts undergo contact inhibition of locomotion (CIL), a process that was discovered five decades ago and still is not fully understood at the molecular level. We identify the Slit2-Robo4-srGAP2 signaling network as a key regulator of CIL in fibroblasts. CIL involves highly dynamic contact protrusions w...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2015.09.002

    authors: Fritz RD,Menshykau D,Martin K,Reimann A,Pontelli V,Pertz O

    更新日期:2015-10-12 00:00:00

  • Germ Cells Get by with a Little Cannibalistic Help from Their Friends.

    abstract::During development, primordial germ cells (PGCs) navigate a complex journey to generate the germline. In a recent paper in Nature Cell Biology, Nance and colleagues (Abdu et al., 2016) have discovered an unexpected step along the way: PGCs get cut in half by endodermal cells. ...

    journal_title:Developmental cell

    pub_type: 评论,杂志文章

    doi:10.1016/j.devcel.2016.12.003

    authors: Krishna S,Overholtzer M

    更新日期:2016-12-19 00:00:00

  • miRNA in embryonic development: the taming of Nodal signaling.

    abstract::The TGF-beta family member Nodal is one of the most potent molecules known to an embryo. Studies on Nodal regulation thus far have focused on its transcription, maturation, and interaction with antagonists. Two recent studies on the role of microRNAs (miRNAs) in Nodal signaling now reveal that something important was ...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2007.09.012

    authors: Collignon J

    更新日期:2007-10-01 00:00:00

  • Opposing Action of Hedgehog and Insulin Signaling Balances Proliferation and Autophagy to Determine Follicle Stem Cell Lifespan.

    abstract::Egg production declines with age in many species, a process linked with stem cell loss. Diet-dependent signaling has emerged as critical for stem cell maintenance during aging. Follicle stem cells (FSCs) in the Drosophila ovary are exquisitely responsive to diet-induced signals including Hedgehog (Hh) and insulin-IGF ...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2018.08.008

    authors: Singh T,Lee EH,Hartman TR,Ruiz-Whalen DM,O'Reilly AM

    更新日期:2018-09-24 00:00:00

  • The Shh Topological Domain Facilitates the Action of Remote Enhancers by Reducing the Effects of Genomic Distances.

    abstract::Gene expression often requires interaction between promoters and distant enhancers, which occur within the context of highly organized topologically associating domains (TADs). Using a series of engineered chromosomal rearrangements at the Shh locus, we carried out an extensive fine-scale characterization of the facto...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2016.10.015

    authors: Symmons O,Pan L,Remeseiro S,Aktas T,Klein F,Huber W,Spitz F

    更新日期:2016-12-05 00:00:00

  • External mechanical cues trigger the establishment of the anterior-posterior axis in early mouse embryos.

    abstract::Mouse anterior-posterior axis polarization is preceded by formation of the distal visceral endoderm (DVE) by unknown mechanisms. Here, we show by in vitro culturing of embryos immediately after implantation in microfabricated cavities that the external mechanical cues exerted on the embryo are crucial for DVE formatio...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2013.09.026

    authors: Hiramatsu R,Matsuoka T,Kimura-Yoshida C,Han SW,Mochida K,Adachi T,Takayama S,Matsuo I

    更新日期:2013-10-28 00:00:00

  • C. elegans CED-12 acts in the conserved crkII/DOCK180/Rac pathway to control cell migration and cell corpse engulfment.

    abstract::We have identified and characterized a novel C. elegans gene, ced-12, that functions in the conserved GTPase signaling pathway mediated by CED-2/Crkll, CED-5/DOCK180, and CED-10/Rac to control cell migration and phagocytosis of apoptotic cells. We provide evidence that ced-12 likely acts upstream of ced-10 during cell...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/s1534-5807(01)00056-9

    authors: Wu YC,Tsai MC,Cheng LC,Chou CJ,Weng NY

    更新日期:2001-10-01 00:00:00

  • Memorizing Shape to Orient Cell Division.

    abstract::A century ago, Oscar Hertwig discovered that cells orient their cleavage plane orthogonal to their long axis. Reporting recently in Nature, Bosveld et al. (2016) shed light on how, showing that NuMA/Mud localization at tricellular junctions provides mitotic cells with the memory of interphase shape used to orient clea...

    journal_title:Developmental cell

    pub_type: 评论,杂志文章

    doi:10.1016/j.devcel.2016.03.005

    authors: Michel M,Dahmann C

    更新日期:2016-03-21 00:00:00

  • A molecular base for cell sorting at embryonic boundaries: contact inhibition of cadherin adhesion by ephrin/ Eph-dependent contractility.

    abstract::The mechanism responsible for subdividing the embryo into individual tissues is a fundamental, yet still poorly understood, question in developmental biology. Various general hypotheses have been proposed, involving differences in cell adhesion, contractility, or contact-mediated repulsion. However, the key parameter ...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2013.09.004

    authors: Fagotto F,Rohani N,Touret AS,Li R

    更新日期:2013-10-14 00:00:00

  • Kinetochore-dependent microtubule rescue ensures their efficient and sustained interactions in early mitosis.

    abstract::How kinetochores regulate microtubule dynamics to ensure proper kinetochore-microtubule interactions is unknown. Here, we studied this during early mitosis in Saccharomyces cerevisiae. When a microtubule shrinks and its plus end reaches a kinetochore bound to its lateral surface, the microtubule end attempts to tether...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2011.09.006

    authors: Gandhi SR,Gierliński M,Mino A,Tanaka K,Kitamura E,Clayton L,Tanaka TU

    更新日期:2011-11-15 00:00:00

  • Crosstalk between a nuclear receptor and beta-catenin signaling decides cell fates in the C. elegans somatic gonad.

    abstract::beta-Catenin signaling determines the proximal-distal axis of the C. elegans gonad by promoting distal fate in asymmetrically dividing somatic gonad precursor cells (SGPs). Impaired function of the Wnt effector POP-1/TCF, its coactivator SYS-1/beta-catenin, and of upstream components including beta-catenin WRM-1 cause...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2006.06.003

    authors: Asahina M,Valenta T,Silhankova M,Korinek V,Jindra M

    更新日期:2006-08-01 00:00:00

  • Reconsidering the Passive Diffusion Model of Steroid Hormone Cellular Entry.

    abstract::Steroid hormones have long been thought to enter target cells via passive diffusion through the plasma membrane. Now, reporting in Developmental Cell, Okamoto et al. (2018) demonstrate that, at least for Drosophila, steroid hormones require a protein transporter for cellular entry. ...

    journal_title:Developmental cell

    pub_type: 评论,杂志文章

    doi:10.1016/j.devcel.2018.10.022

    authors: Neuman SD,Bashirullah A

    更新日期:2018-11-05 00:00:00

  • CNS myelin wrapping is driven by actin disassembly.

    abstract::Myelin is essential in vertebrates for the rapid propagation of action potentials, but the molecular mechanisms driving its formation remain largely unknown. Here we show that the initial stage of process extension and axon ensheathment by oligodendrocytes requires dynamic actin filament assembly by the Arp2/3 complex...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2015.06.011

    authors: Zuchero JB,Fu MM,Sloan SA,Ibrahim A,Olson A,Zaremba A,Dugas JC,Wienbar S,Caprariello AV,Kantor C,Leonoudakis D,Lariosa-Willingham K,Kronenberg G,Gertz K,Soderling SH,Miller RH,Barres BA

    更新日期:2015-07-27 00:00:00

  • Oligodendrocyte Neurofascin Independently Regulates Both Myelin Targeting and Sheath Growth in the CNS.

    abstract::Selection of the correct targets for myelination and regulation of myelin sheath growth are essential for central nervous system (CNS) formation and function. Through a genetic screen in zebrafish and complementary analyses in mice, we find that loss of oligodendrocyte Neurofascin leads to mistargeting of myelin to ce...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2019.10.016

    authors: Klingseisen A,Ristoiu AM,Kegel L,Sherman DL,Rubio-Brotons M,Almeida RG,Koudelka S,Benito-Kwiecinski SK,Poole RJ,Brophy PJ,Lyons DA

    更新日期:2019-12-16 00:00:00

  • Live free or die: cell-cell adhesion regulates sensitivity to trail-induced apoptosis.

    abstract::The ability of the death ligand TRAIL to induce tumor cell apoptosis has led to the development of TRAIL-based cancer therapies. Reporting recently in Molecular Cell, Lu et al. (2014) show that the basis for differential TRAIL responses involves clustering of death receptor complexes by E-cadherin and the actin cytosk...

    journal_title:Developmental cell

    pub_type: 评论,杂志文章

    doi:10.1016/j.devcel.2014.06.031

    authors: Gallegos LL,Brugge JS

    更新日期:2014-07-14 00:00:00

  • The centrosome-specific phosphorylation of Cnn by Polo/Plk1 drives Cnn scaffold assembly and centrosome maturation.

    abstract::Centrosomes are important cell organizers. They consist of a pair of centrioles surrounded by pericentriolar material (PCM) that expands dramatically during mitosis-a process termed centrosome maturation. How centrosomes mature remains mysterious. Here, we identify a domain in Drosophila Cnn that appears to be phospho...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2014.02.013

    authors: Conduit PT,Feng Z,Richens JH,Baumbach J,Wainman A,Bakshi SD,Dobbelaere J,Johnson S,Lea SM,Raff JW

    更新日期:2014-03-31 00:00:00

  • Integrinalpha5-dependent fibronectin accumulation for maintenance of somite boundaries in zebrafish embryos.

    abstract::Boundary formation and epithelialization are crucial processes in the morphological segmentation of vertebrate somites. By a genetic screening procedure with zebrafish, we identified two genes, integrinalpha5 (itga5) and fibronectin (fn), required for these processes. Fibronectin proteins accumulate at somite boundari...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2005.03.006

    authors: Koshida S,Kishimoto Y,Ustumi H,Shimizu T,Furutani-Seiki M,Kondoh H,Takada S

    更新日期:2005-04-01 00:00:00

  • (Re)inventing the circadian feedback loop.

    abstract::For 20 years, researchers have thought that circadian clocks are defined by feedback loops of transcription and translation. The rediscovery of posttranslational circadian oscillators in diverse organisms forces us to rethink this paradigm. Meanwhile, the original "basic" feedback loops of canonical circadian clocks h...

    journal_title:Developmental cell

    pub_type: 杂志文章,评审

    doi:10.1016/j.devcel.2012.02.007

    authors: Brown SA,Kowalska E,Dallmann R

    更新日期:2012-03-13 00:00:00

  • Sensory-neuron subtype-specific transcriptional programs controlling dendrite morphogenesis: genome-wide analysis of Abrupt and Knot/Collier.

    abstract::The transcription factors Abrupt (Ab) and Knot (Kn) act as selectors of distinct dendritic arbor morphologies in two classes of Drosophila sensory neurons, termed class I and class IV, respectively. We performed binding-site mapping and transcriptional profiling of these isolated neurons. Their profiles were similarly...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2013.10.024

    authors: Hattori Y,Usui T,Satoh D,Moriyama S,Shimono K,Itoh T,Shirahige K,Uemura T

    更新日期:2013-12-09 00:00:00

  • S6K1 plays a critical role in early adipocyte differentiation.

    abstract::Earlier, we reported that S6K1(-/-) mice have reduced body fat mass, have elevated rates of lipolysis, have severely decreased adipocyte size, and are resistant to high fat diet (HFD)-induced obesity. Here we report that adipocytes of S6K1(-/-) mice on a HFD have the capacity to increase in size to a degree comparable...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2010.02.018

    authors: Carnevalli LS,Masuda K,Frigerio F,Le Bacquer O,Um SH,Gandin V,Topisirovic I,Sonenberg N,Thomas G,Kozma SC

    更新日期:2010-05-18 00:00:00

  • Tugging organs into place.

    abstract::In this issue of Developmental Cell, Weavers and Skaer (2013) show that interplay between two opposing forces generated by tip cell attachment to muscles and migration of kink cells allows for the formation of the looped shape and positioning of renal tubules within the body of a fly larva. ...

    journal_title:Developmental cell

    pub_type: 评论,杂志文章

    doi:10.1016/j.devcel.2013.10.021

    authors: Lenard A,Affolter M

    更新日期:2013-11-11 00:00:00

  • Mechanical Forces Program the Orientation of Cell Division during Airway Tube Morphogenesis.

    abstract::Oriented cell division plays a key role in controlling organogenesis. The mechanisms for regulating division orientation at the whole-organ level are only starting to become understood. By combining 3D time-lapse imaging, mouse genetics, and mathematical modeling, we find that global orientation of cell division is th...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2017.12.013

    authors: Tang Z,Hu Y,Wang Z,Jiang K,Zhan C,Marshall WF,Tang N

    更新日期:2018-02-05 00:00:00

  • Functional Coordination of WAVE and WASP in C. elegans Neuroblast Migration.

    abstract::Directional cell migration is critical for metazoan development. We define two molecular pathways that activate the Arp2/3 complex during neuroblast migration in Caenorhabditis elegans. The transmembrane protein MIG-13/Lrp12 is linked to the Arp2/3 nucleation-promoting factors WAVE or WASP through direct interactions ...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2016.09.029

    authors: Zhu Z,Chai Y,Jiang Y,Li W,Hu H,Li W,Wu JW,Wang ZX,Huang S,Ou G

    更新日期:2016-10-24 00:00:00

  • Linking Matrix Rigidity with EMT and Cancer Invasion.

    abstract::The extracellular matrix (ECM) plays a major role in cancer progression through its increased deposition and alignment. In this issue of Developmental Cell, Fattet et al. reveal a pathway in which ECM stiffness promotes EPHA2/LYN complex activation, leading to TWIST1 nuclear localization and triggering EMT in breast c...

    journal_title:Developmental cell

    pub_type: 评论,杂志文章

    doi:10.1016/j.devcel.2020.06.032

    authors: Ros M,Sala M,Saltel F

    更新日期:2020-08-10 00:00:00

  • Drosophila rasiRNA pathway mutations disrupt embryonic axis specification through activation of an ATR/Chk2 DNA damage response.

    abstract::Small repeat-associated siRNAs (rasiRNAs) mediate silencing of retrotransposons and the Stellate locus. Mutations in the Drosophila rasiRNA pathway genes armitage and aubergine disrupt embryonic axis specification, triggering defects in microtubule polarization as well as asymmetric localization of mRNA and protein de...

    journal_title:Developmental cell

    pub_type: 杂志文章

    doi:10.1016/j.devcel.2006.12.001

    authors: Klattenhoff C,Bratu DP,McGinnis-Schultz N,Koppetsch BS,Cook HA,Theurkauf WE

    更新日期:2007-01-01 00:00:00

  • Epithelial Morphogenesis: Size Matters.

    abstract::In this issue of Developmental Cell, Gibson and colleagues (Ramanathan et al., 2019) investigate the relationship between size and shape in epithelial cells. They find that cell size impacts cell shape, with unexpected consequences for epithelial growth and morphogenesis, particularly the clonal dynamics of epithelial...

    journal_title:Developmental cell

    pub_type: 评论,杂志文章

    doi:10.1016/j.devcel.2019.09.015

    authors: Thompson BJ

    更新日期:2019-10-07 00:00:00

  • Fat2 and Lar Dance a Pas de Deux during Collective Cell Migration.

    abstract::What coordinates the internal leading and trailing edges in collectively migrating cells is largely unknown. In this issue of Developmental Cell, Barlan et al. (2017) delineate a Fat2/Lar planar signaling pathway at the basal, motile cell-cell contacts of Drosophila egg chamber follicle cells. ...

    journal_title:Developmental cell

    pub_type: 评论,杂志文章

    doi:10.1016/j.devcel.2017.02.025

    authors: Mao Q,Lavalou J,Lecuit T

    更新日期:2017-03-13 00:00:00