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

Development ◽  
1995 ◽  
Vol 121 (7) ◽  
pp. 2005-2018 ◽  
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.

scholarly journals Hyperactivation of the folded gastrulation pathway induces specific cell shape changes

Development ◽  
1998 ◽  
Vol 125 (4) ◽  
pp. 589-597 ◽  
Author(s):  
P. Morize ◽  
A.E. Christiansen ◽  
M. Costa ◽  
S. Parks ◽  
E. Wieschaus
Keyword(s):  
Cell Shape ◽  
Inducible Promoter ◽  
Specific Cell ◽  
Apical Surface ◽  
Apical Constriction ◽  
Cellular Effects ◽  
Ventral Furrow ◽  
Cell Shape Changes ◽  
Shape Changes

During Drosophila gastrulation, mesodermal precursors are brought into the interior of the embryo by formation of the ventral furrow. The first steps of ventral furrow formation involve a flattening of the apical surface of the presumptive mesodermal cells and a constriction of their apical diameters. In embryos mutant for folded gastrulation (fog), these cell shape changes occur but the timing and synchrony of the constrictions are abnormal. A similar phenotype is seen in a maternal effect mutant, concertina (cta). fog encodes a putative secreted protein whereas cta encodes an (alpha)-subunit of a heterotrimeric G protein. We have proposed that localized expression of the fog signaling protein induces apical constriction by interacting with a receptor whose downstream cellular effects are mediated by the cta G(alpha)protein. <P> In order to test this model, we have ectopically expressed fog at the blastoderm stage using an inducible promoter. In addition, we have examined the constitutive activation of cta protein by blocking GTP hydrolysis using both in vitro synthesized mutant alleles and cholera toxin treatment. Activation of the fog/cta pathway by any of these procedures results in ectopic cell shape changes in the gastrula. Uniform fog expression rescues the gastrulation defects of fog null embryos but not cta mutant embryos, arguing that cta functions downstream of fog expression. The normal location of the ventral furrow in embryos with uniformly expressed fog suggests the existence of a fog-independent pathway determining mesoderm-specific cell behaviors and invagination. Epistasis experiments indicate that this pathway requires snail but not twist expression.

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

2019 ◽  
Author(s):  
Clint S. Ko ◽  
Prateek Kalakuntla ◽  
Adam C. Martin
Keyword(s):  
Cell Division ◽  
Cell Shape ◽  
Mitotic Cell ◽  
Signal Interference ◽  
Apical Constriction ◽  
Mitotic Entry ◽  
Cell Divisions ◽  
Cell Shape Changes ◽  
Shape Changes ◽  
Mitotic Cells

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.

scholarly journals Integrin binding and cell spreading on extracellular matrix act at different points in the cell cycle to promote hepatocyte growth.

1994 ◽  
Vol 5 (9) ◽  
pp. 967-975 ◽  
Author(s):  
L K Hansen ◽  
D J Mooney ◽  
J P Vacanti ◽  
D E Ingber
Keyword(s):  
Cell Cycle ◽  
Extracellular Matrix ◽  
Cell Shape ◽  
Time Course ◽  
Cell Spreading ◽  
S Phase ◽  
Similar Time ◽  
Cell Shape Changes ◽  
Hepatocyte Growth ◽  
Shape Changes

This study was undertaken to determine the importance of integrin binding and cell shape changes in the control of cell-cycle progression by extracellular matrix (ECM). Primary rat hepatocytes were cultured on ECM-coated dishes in serum-free medium with saturating amounts of growth factors (epidermal growth factor and insulin). Integrin binding and cell spreading were promoted in parallel by plating cells on dishes coated with fibronectin (FN). Integrin binding was separated from cell shape changes by culturing cells on dishes coated with a synthetic arg-gly-asp (RGD)-peptide that acts as an integrin ligand but does not support hepatocyte extension. Expression of early (junB) and late (ras) growth response genes and DNA synthesis were measured to determine whether these substrata induce G0-synchronized hepatocytes to reenter the growth cycle. Cells plated on FN exhibited transient increases in junB and ras gene expression (within 2 and 8 h after plating, respectively) and synchronous entry into S phase. Induction of junB and ras was observed over a similar time course in cells on RGD-coated dishes, however, these round cells did not enter S phase. The possibility that round cells on RGD were blocked in mid to late G1 was confirmed by the finding that when trypsinized and replated onto FN-coated dishes after 30 h of culture, they required a similar time (12-15 h) to reenter S phase as cells that had been spread and allowed to progress through G1 on FN. We have previously shown that hepatocytes remain viable and maintain high levels of liver-specific functions when cultured on these RGD-coated dishes. Thus, these results suggest that ECM acts at two different points in the cell cycle to regulate hepatocyte growth: first, by activating the G0/G1 transition via integrin binding and second, by promoting the G1/S phase transition and switching off the default differentiation program through mechanisms related to cell spreading.

scholarly journals broad controls leg imaginal disc morphogenesis in Drosophila via regulation of cell shape changes and remodeling of extracellular matrix

2019 ◽  
Author(s):  
Clinton Rice ◽  
Stuart Macdonald ◽  
Xiaochen Wang ◽  
Robert E Ward
Keyword(s):  
Extracellular Matrix ◽  
Transcription Factor ◽  
Drosophila Melanogaster ◽  
Cell Shape ◽  
Imaginal Disc ◽  
Molecular Mechanisms ◽  
Matrix Remodeling ◽  
Ecm Remodeling ◽  
Cell Shape Changes ◽  
Shape Changes

AbstractImaginal disc morphogenesis during metamorphosis in Drosophila melanogaster provides an excellent model to uncover molecular mechanisms by which hormonal signals effect physical changes during development. The broad (br) Z2 isoform encodes a transcription factor required for disc morphogenesis in response to 20-hydroxyecdysone, yet how it accomplishes this remains largely unknown. Here, we show that amorphic br5 mutant discs fail to remodel their basal extracellular matrix (ECM) after puparium formation and do not undergo necessary cell shape changes. RNA sequencing of wild type and mutant leg discs identified 717 genes differentially regulated by br; functional studies reveal that several are required for adult leg formation, particularly those involved in remodeling the ECM. Additionally, br Z2 expression is abruptly shut down at the onset of metamorphosis, and expressing it beyond this time results in failure of leg development during the late prepupal and pupal stages. Taken together, our results suggest that br Z2 is required to drive ECM remodeling, change cell shape, and maintain metabolic activity through the mid prepupal stage, but must be switched off to allow expression of pupation genes.Summary StatementThe Drosophila melanogaster ecdysone-responding transcription factor broad controls morphogenetic processes in leg imaginal discs during metamorphosis through regulation of genes involved in extracellular matrix remodeling, metabolism, and cell shape changes and rearrangements.

Real-time imaging of cell-cell adherens junctions reveals that Drosophila mesoderm invagination begins with two phases of apical constriction of cells

2001 ◽  
Vol 114 (3) ◽  
pp. 493-501 ◽  
Author(s):  
H. Oda ◽  
S. Tsukita
Keyword(s):  
Real Time ◽  
Cell Shape ◽  
Adherens Junctions ◽  
Cell Sheet ◽  
Apical Surface ◽  
Apical Constriction ◽  
Real Time Imaging ◽  
Cell Shape Changes ◽  
Shape Changes ◽  
Cell Cell

Invagination of the epithelial cell sheet of the prospective mesoderm in Drosophila gastrulation is a well-studied, relatively simple morphogenetic event that results from dynamic cell shape changes and cell movements. However, these cell behaviors have not been followed at a sufficiently short time resolution. We examined mesoderm invagination in living wild-type embryos by real-time imaging of fluorescently labeled cell-cell adherens junctions, which are located at the apical zones of cell-cell contact. Low-light fluorescence video microscopy directly visualized the onset and progression of invagination. In an initial period of approximately 2 minutes, cells around the ventral midline reduced their apical surface areas slowly in a rather synchronous manner. Next, the central and more lateral cells stochastically accelerated or initiated their apical constriction, giving rise to random arrangements of cells with small and relatively large apices. Thus, we found that mesoderm invagination began with slow synchronous and subsequent fast stochastic phases of cell apex constriction. Furthermore, we showed that the mesoderm invagination of folded gastrulation mutant embryos lacked the normal two constriction phases, and instead began with asynchronous, feeble cell shape changes. Our observations suggested that Folded gastrulation-mediated signaling enabled synchronous activation of the contractile cortex, causing competition among the individual mesodermal cells for apical constriction. Movies available on-line: http://www.biologists.com/JCS/movies/jcs2073.html

scholarly journals Crosstalk between basal extracellular matrix adhesion and building of apical architecture during morphogenesis

Biology Open ◽  
2021 ◽  
Vol 10 (11) ◽  
Author(s):  
Mariana Barrera-Velázquez ◽  
Luis Daniel Ríos-Barrera
Keyword(s):  
Extracellular Matrix ◽  
Plasma Membrane ◽  
Cell Shape ◽  
Plasma Membranes ◽  
Tube Formation ◽  
Apical Plasma Membrane ◽  
Complex Structures ◽  
Apicobasal Polarity ◽  
Basal Plasma ◽  
Shape Changes

ABSTRACT Tissues build complex structures like lumens and microvilli to carry out their functions. Most of the mechanisms used to build these structures rely on cells remodelling their apical plasma membranes, which ultimately constitute the specialised compartments. In addition to apical remodelling, these shape changes also depend on the proper attachment of the basal plasma membrane to the extracellular matrix (ECM). The ECM provides cues to establish apicobasal polarity, and it also transduces forces that allow apical remodelling. However, physical crosstalk mechanisms between basal ECM attachment and the apical plasma membrane remain understudied, and the ones described so far are very diverse, which highlights the importance of identifying the general principles. Here, we review apicobasal crosstalk of two well-established models of membrane remodelling taking place during Drosophila melanogaster embryogenesis: amnioserosa cell shape oscillations during dorsal closure and subcellular tube formation in tracheal cells. We discuss how anchoring to the basal ECM affects apical architecture and the mechanisms that mediate these interactions. We analyse this knowledge under the scope of other morphogenetic processes and discuss what aspects of apicobasal crosstalk may represent widespread phenomena and which ones are used to build subsets of specialised compartments.

scholarly journals Abl suppresses cell extrusion and intercalation during epithelium folding

2016 ◽  
Vol 27 (18) ◽  
pp. 2822-2832 ◽  
Author(s):  
Jeanne N. Jodoin ◽  
Adam C. Martin
Keyword(s):  
Cell Shape ◽  
Epithelial To Mesenchymal Transition ◽  
Adherens Junction ◽  
Apical Constriction ◽  
Mesenchymal Transition ◽  
Abl Tyrosine Kinase ◽  
Cell Intercalation ◽  
Shape Changes ◽  
Insight Into ◽  
Cell Extrusion

Tissue morphogenesis requires control over cell shape changes and rearrangements. In the Drosophila mesoderm, linked epithelial cells apically constrict, without cell extrusion or intercalation, to fold the epithelium into a tube that will then undergo epithelial-to-mesenchymal transition (EMT). Apical constriction drives tissue folding or cell extrusion in different contexts, but the mechanisms that dictate the specific outcomes are poorly understood. Using live imaging, we found that Abelson (Abl) tyrosine kinase depletion causes apically constricting cells to undergo aberrant basal cell extrusion and cell intercalation. abl depletion disrupted apical–basal polarity and adherens junction organization in mesoderm cells, suggesting that extruding cells undergo premature EMT. The polarity loss was associated with abnormal basolateral contractile actomyosin and Enabled (Ena) accumulation. Depletion of the Abl effector Enabled (Ena) in abl-depleted embryos suppressed the abl phenotype, consistent with cell extrusion resulting from misregulated ena. Our work provides new insight into how Abl loss and Ena misregulation promote cell extrusion and EMT.

scholarly journals Orchestrating morphogenesis: building the body plan by cell shape changes and movements

Development ◽  
2020 ◽  
Vol 147 (17) ◽  
pp. dev191049 ◽  
Author(s):  
Kia Z. Perez-Vale ◽  
Mark Peifer
Keyword(s):  
Cell Shape ◽  
Molecular Mechanisms ◽  
Fruit Fly ◽  
Body Plan ◽  
The Body ◽  
Collective Cell Migration ◽  
Convergent Extension ◽  
Apical Constriction ◽  
Cell Shape Changes ◽  
Shape Changes

ABSTRACTDuring embryonic development, a simple ball of cells re-shapes itself into the elaborate body plan of an animal. This requires dramatic cell shape changes and cell movements, powered by the contractile force generated by actin and myosin linked to the plasma membrane at cell-cell and cell-matrix junctions. Here, we review three morphogenetic events common to most animals: apical constriction, convergent extension and collective cell migration. Using the fruit fly Drosophila as an example, we discuss recent work that has revealed exciting new insights into the molecular mechanisms that allow cells to change shape and move without tearing tissues apart. We also point out parallel events at work in other animals, which suggest that the mechanisms underlying these morphogenetic processes are conserved.

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