Anisotropy of cell division and epithelial sheet bending via apical constriction shape the complex folding pattern of beetle horn primordia

AbstractDuring development, coordinated cell shape changes and cell divisions sculpt tissues. While these individual cell behaviors have been extensively studied, how cell shape changes and cell divisions that occur concurrently in epithelia influence tissue shape is less understood. We addressed this question in two contexts of the early Drosophila embryo: premature cell division during mesoderm invagination, and native ectodermal cell divisions with ectopic activation of apical contractility. Using quantitative live-cell imaging, we demonstrated that mitotic entry reverses apical contractility by interfering with medioapical RhoA signaling. While premature mitotic entry inhibits mesoderm invagination, which relies on apical constriction, mitotic entry in an artificially contractile ectoderm induced ectopic tissue invaginations. Ectopic invaginations resulted from medioapical myosin loss in neighboring mitotic cells. This myosin loss enabled non-mitotic cells to apically constrict through mitotic cell stretching. Thus, the spatial pattern of mitotic entry can differentially regulate tissue shape through signal interference between apical contractility and mitosis.

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A Nodal/Eph signalling relay drives the transition from apical constriction to apico-basal shortening in ascidian endoderm invagination

Development ◽

10.1242/dev.186965 ◽

2020 ◽

Vol 147 (15) ◽

pp. dev186965

Author(s):

Ulla-Maj Fiuza ◽

Takefumi Negishi ◽

Alice Rouan ◽

Hitoyoshi Yasuo ◽

Patrick Lemaire

Keyword(s):

Cell Cycle ◽

Cell Division ◽

Ciona Intestinalis ◽

Precursor Cells ◽

Endodermal Cell ◽

Apical Constriction ◽

Fate Specification ◽

Endoderm Cell ◽

Ascidian Species ◽

Morphogenetic Event

ABSTRACTGastrulation is the first major morphogenetic event during animal embryogenesis. Ascidian gastrulation starts with the invagination of 10 endodermal precursor cells between the 64- and late 112-cell stages. This process occurs in the absence of endodermal cell division and in two steps, driven by myosin-dependent contractions of the acto-myosin network. First, endoderm precursors constrict their apex. Second, they shorten apico-basally, while retaining small apical surfaces, thereby causing invagination. The mechanisms that prevent endoderm cell division, trigger the transition between step 1 and step 2, and drive apico-basal shortening have remained elusive. Here, we demonstrate a conserved role for Nodal and Eph signalling during invagination in two distantly related ascidian species, Phallusia mammillata and Ciona intestinalis. Specifically, we show that the transition to step 2 is triggered by Nodal relayed by Eph signalling. In addition, our results indicate that Eph signalling lengthens the endodermal cell cycle, independently of Nodal. Finally, we find that both Nodal and Eph signals are dispensable for endoderm fate specification. These results illustrate commonalities as well as differences in the action of Nodal during ascidian and vertebrate gastrulation.

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Apical Constriction Reversal upon Mitotic Entry Underlies Different Morphogenetic Outcomes of Cell Division

Molecular Biology of the Cell ◽

10.1091/mbc.e19-12-0673 ◽

2020 ◽

Vol 31 (16) ◽

pp. 1663-1674 ◽

Cited By ~ 1

Author(s):

Clint S. Ko ◽

Prateek Kalakuntla ◽

Adam C. Martin

Keyword(s):

Cell Division ◽

Tissue Level ◽

Spatiotemporal Patterns ◽

Force Generation ◽

Tissue Morphogenesis ◽

Apical Constriction ◽

Mitotic Entry ◽

Cell Divisions

Cell divisions can either promote or inhibit tissue morphogenesis. In contractile epithelia, mitotic entry disrupts medioapical myosin activation and reverses apical constriction. We found that different spatiotemporal patterns of mitotic entry and the resultant changes in force generation at the tissue level dictate distinct tissue shape outcomes.

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How do sea urchins invaginate? Using biomechanics to distinguish between mechanisms of primary invagination

Development ◽

10.1242/dev.121.7.2005 ◽

1995 ◽

Vol 121 (7) ◽

pp. 2005-2018 ◽

Cited By ~ 7

Author(s):

L.A. Davidson ◽

M.A. Koehl ◽

R. Keller ◽

G.F. Oster

Keyword(s):

Mechanical Properties ◽

Extracellular Matrix ◽

Finite Element ◽

Cell Shape ◽

Sea Urchins ◽

Specific Cell ◽

Apical Constriction ◽

Epithelial Sheet ◽

Shape Changes ◽

Design Experiments

The forces that drive sea urchin primary invagination remain mysterious. To solve this mystery we have developed a set of finite element simulations that test five hypothesized mechanisms. Our models show that each of these mechanisms can generate an invagination; however, the mechanical properties of an epithelial sheet required for proper invagination are different for each mechanism. For example, we find that the gel swelling hypothesis of Lane et al. (Lane, M. C., Koehl, M. A. R., Wilt, F. and Keller, R. (1993) Development 117, 1049–1060) requires the embryo to possess a mechanically stiff apical extracellular matrix and highly deformable cells, whereas a hypothesis based on apical constriction of the epithelial cells requires a more compliant extracellular matrix. For each mechanism, we have mapped out a range of embryo designs that work. Additionally, the simulations predict specific cell shape changes accompanying each mechanism. This allows us to design experiments that can distinguish between different mechanisms, all of which can, in principle, drive primary invagination.

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Computational analyses decipher the primordial folding coding the 3D structure of the beetle horn

Scientific Reports ◽

10.1038/s41598-020-79757-2 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Keisuke Matsuda ◽

Hiroki Gotoh ◽

Haruhiko Adachi ◽

Yasuhiro Inoue ◽

Shigeru Kondo

Keyword(s):

Computational Methods ◽

Morphological Study ◽

Morphological Changes ◽

3D Structure ◽

Larval Cuticle ◽

3D Shape ◽

Folding Pattern ◽

Angular Change ◽

Epithelial Sheet ◽

Computational Analyses

AbstractThe beetle horn primordium is a complex and compactly folded epithelial sheet located beneath the larval cuticle. Only by unfolding the primordium can the complete 3D shape of the horn appear, suggesting that the morphology of beetle horns is encoded in the primordial folding pattern. To decipher the folding pattern, we developed a method to manipulate the primordial local folding on a computer and clarified the contribution of the folding of each primordium region to transformation. We found that the three major morphological changes (branching of distal tips, proximodistal elongation, and angular change) were caused by the folding of different regions, and that the folding mechanism also differs according to the region. The computational methods we used are applicable to the morphological study of other exoskeletal animals.

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Apical Constriction Reversal upon Mitotic Entry Underlies Different Morphogenetic Outcomes of Cell Division

10.1242/prelights.15746 ◽

2019 ◽

Author(s):

Grace Lim

Keyword(s):

Cell Division ◽

Apical Constriction ◽

Mitotic Entry

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MAGIs regulate aPKC to enable balanced distribution of intercellular tension for epithelial sheet homeostasis

Communications Biology ◽

10.1038/s42003-021-01874-z ◽

2021 ◽

Vol 4 (1) ◽

Author(s):

Kenji Matsuzawa ◽

Hayato Ohga ◽

Kenta Shigetomi ◽

Tomohiro Shiiya ◽

Masanori Hirashima ◽

...

Keyword(s):

Plasma Membrane ◽

Epithelial Cells ◽

Cell Sheet ◽

Apical Plasma Membrane ◽

Apical Constriction ◽

Tissue Integrity ◽

Balanced Distribution ◽

Junctional Complexes ◽

Epithelial Sheet ◽

Polarity Proteins

AbstractConstriction of the apical plasma membrane is a hallmark of epithelial cells that underlies cell shape changes in tissue morphogenesis and maintenance of tissue integrity in homeostasis. Contractile force is exerted by a cortical actomyosin network that is anchored to the plasma membrane by the apical junctional complexes (AJC). In this study, we present evidence that MAGI proteins, structural components of AJC whose function remained unclear, regulate apical constriction of epithelial cells through the Par polarity proteins. We reveal that MAGIs are required to uniformly distribute Partitioning defective-3 (Par-3) at AJC of cells throughout the epithelial monolayer. MAGIs recruit ankyrin-repeat-, SH3-domain- and proline-rich-region-containing protein 2 (ASPP2) to AJC, which modulates Par-3-aPKC to antagonize ROCK-driven contractility. By coupling the adhesion machinery to the polarity proteins to regulate cellular contractility, we propose that MAGIs play essential and central roles in maintaining steady state intercellular tension throughout the epithelial cell sheet.

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Computational analyses decipher the primordial folding coding the 3D structure of the beetle horn

10.21203/rs.3.rs-49595/v1 ◽

2020 ◽

Author(s):

Keisuke Matsuda ◽

Hiroki Gotoh ◽

Haruhiko Adachi ◽

Yasuhiro Inoue ◽

Shigeru Kondo

Keyword(s):

Computational Methods ◽

Morphological Study ◽

Morphological Changes ◽

3D Structure ◽

Larval Cuticle ◽

3D Shape ◽

Folding Pattern ◽

Angular Change ◽

Epithelial Sheet ◽

Computational Analyses

Abstract The beetle horn primordium is a complex and compactly folded epithelial sheet located beneath the larval cuticle. Only by unfolding the primordium the complete 3D shape of the horn appears, suggesting that the morphology of beetle horns is coded in the primordial folding pattern. To decipher the folding pattern, we have developed a method to manipulate the primordial local folding, reproduced it on a computer, and clarified the contribution of the folding of each primordium region to transformation. We found that the three major morphological changes (branching of distal tips, proximodistal elongation, and angular change) were caused by the folding of different regions, and that the folding mechanism was also different depending on the region. The computational methods we used are applicable to the morphological study of other exoskeletal animals.

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The Ultrastructure of the Nuclear Events of Binary Fission in Paramecium bursaria and the Effects of Colchicine on Cell Division

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100051396 ◽

1974 ◽

Vol 32 ◽

pp. 276-277

Author(s):

L. M. Lewis

Keyword(s):

Cell Division ◽

Nuclear Envelope ◽

Condensed Chromatin ◽

Binary Fission ◽

Paramecium Bursaria ◽

Nuclear Events ◽

Division Axis

The effects of colchicine on extranuclear microtubules associated with the macronucleus of Paramecium bursaria were studied to determine the possible role that these microtubules play in controlling the shape of the macronucleus. In the course of this study, the ultrastructure of the nuclear events of binary fission in control cells was also studied.During interphase in control cells, the micronucleus contains randomly distributed clumps of condensed chromatin and microtubular fragments. Throughout mitosis the nuclear envelope remains intact. During micronuclear prophase, cup-shaped microfilamentous structures appear that are filled with condensing chromatin. Microtubules are also present and are parallel to the division axis.

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Stimulated Virus Production in Vinblastine and Cytochalasin-Induced Multinucleate Cells

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100067923 ◽

1970 ◽

Vol 28 ◽

pp. 186-187

Author(s):

Krishan Awtar

Keyword(s):

Cell Division ◽

Normal Cell ◽

Virus Production ◽

Multinucleate Cells ◽

Daughter Cells ◽

Cell Divisions ◽

Nuclear Membranes ◽

Division 2 ◽

Vinblastine Sulfate

Exposure of cells to low sublethal but mitosis-arresting doses of vinblastine sulfate (Velban) results in the initial arrest of cells in mitosis followed by their subsequent return to an “interphase“-like stage. A large number of these cells reform their nuclear membranes and form large multimicronucleated cells, some containing as many as 25 or more micronuclei (1). Formation of large multinucleate cells is also caused by cytochalasin, by causing the fusion of daughter cells at the end of an otherwise .normal cell division (2). By the repetition of this process through subsequent cell divisions, large cells with 6 or more nuclei are formed.

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