An actin-mediated two-step mechanism is required for ventral enclosure of the C. elegans hypodermis

Development ◽  
1997 ◽  
Vol 124 (15) ◽  
pp. 2889-2901 ◽  
Author(s):  
E.M. Williams-Masson ◽  
A.N. Malik ◽  
J. Hardin
Keyword(s):  
Leading Edge ◽  
Ventral Surface ◽  
Dorsal Side ◽  
Cytochalasin D ◽  
Actin Ring ◽  
Purse String ◽  
Ventral Midline ◽  
C Elegans ◽  
Epithelial Sheet ◽  
Step Mechanism

The epiboly of the Caenorhabditis elegans hypodermis involves the bilateral spreading of a thin epithelial sheet from the dorsal side around the embryo to meet at the ventral midline in a process known as ventral enclosure. We present evidence that ventral enclosure occurs in two major steps. The initial migration of the hypodermis is led by a quartet of cells, which exhibit protrusive activity at their medial tips and are required to pull the hypodermis around the equator of the embryo. These cells display actin-rich filopodia and treatment with cytochalasin D immediately halts ventral enclosure, as does laser inactivation of all four cells. Once the quartet of cells has migrated around the equator of the embryo and approaches the ventral midline, the remainder of the leading edge becomes visible on the ventral surface and exhibits a localization of actin microfilaments along the free edges of the cells, forming an actin ring. Cytochalasin D and laser inactivation block ventral enclosure at this later stage as well and, based upon phalloidin staining, we propose that the second half of enclosure is dependent upon a purse string mechanism, in which the actin ring contracts and pulls together the edges of the hypodermal sheet at the ventral midline. The ventral cells then form junctions with their contralateral neighbors to complete ventral enclosure.

scholarly journals Squeezing an Egg into a Worm: C. elegans Embryonic Morphogenesis

2003 ◽  
Vol 3 ◽  
pp. 1370-1381 ◽  
Author(s):  
A. J. Piekny ◽  
P. E. Mains
Keyword(s):  
Caenorhabditis Elegans ◽  
Epidermal Cells ◽  
Ventral Midline ◽  
Single Row ◽  
C Elegans ◽  
Epithelial Sheet ◽  
Embryonic Morphogenesis ◽  
Shape Changes

We review key morphogenetic events that occur during Caenorhabditis elegans (www.wormbase.org/) embryogenesis. Morphogenesis transforms tissues from one shape into another through cell migrations and shape changes, often utilizing highly conserved actin-based contractile systems. Three major morphogenetic events occur during C. elegans embryogenesis: (1) dorsal intercalation, during which two rows of dorsal epidermal cells intercalate to form a single row; (2) ventral enclosure, where the dorsally located sheet of epidermal cells stretches to the ventral midline, encasing the embryo within a single epithelial sheet; and (3) elongation, during which actin-mediated contractions within the epithelial sheet lengthens the embryo. Here, we describe the known molecular players involved in each of these processes.

A role for regulated secretion of apical extracellular matrix during epithelial invagination in the sea urchin

Development ◽  
1993 ◽  
Vol 117 (3) ◽  
pp. 1049-1060 ◽  
Author(s):  
M.C. Lane ◽  
M.A. Koehl ◽  
F. Wilt ◽  
R. Keller
Keyword(s):  
Extracellular Matrix ◽  
Sea Urchin ◽  
Cytochalasin D ◽  
Tubular Structures ◽  
Purse String ◽  
Regulated Secretion ◽  
Optic Cup ◽  
Thermal Bending ◽  
Morphogenetic Event ◽  
Epithelial Sheet

Epithelial invagination, a basic morphogenetic process reiterated throughout embryonic development, generates tubular structures such as the neural tube, or pit-like structures such as the optic cup. The ‘purse-string’ hypothesis, which proposes that circumferential bands of actin microfilaments at the apical end of epithelial cells constrict to yield a curved epithelial sheet, has been widely invoked to explain invaginations during embryogenesis. We have reevaluated this hypothesis in two species of sea urchin by examining both natural invagination of the vegetal plate at the beginning of gastrulation and invagination induced precociously by Ca2+ ionophore. Neither type of invagination is prevented by cytochalasin D. In one species, treatment with A23187 three hours before the initiation of invagination resulted in the deposition of apical extracellular matrix at the vegetal plate, rather than invagination. This apical matrix contains chondroitin sulfate, as does the lumen of the archenteron in normal gastrulae. When the expansion of this secreted matrix was resisted by an agarose gel, the vegetal plate buckled inward, creating an archenteron that appeared 3–4 hours prematurely. Pretreatment with monensin, which blocks secretion, inhibits both Ca2+ ionophore-stimulated folding and natural invagination, demonstrating that secretion is probably required for this morphogenetic event. These results indicate that alternatives to the purse-string hypothesis must be considered, and that the directed deposition of extracellular matrix may be a key Ca(2+)-regulated event in some embryonic invaginations. A bending bilayer model for matrix-driven epithelial invagination is proposed in which the deposition of hygroscopic material into a complex, stratified extra-cellular matrix results in the folding of an epithelial sheet in a manner analagous to thermal bending in a bimetallic strip.

scholarly journals Actin-ring segment switching drives nonadhesive gap closure

2020 ◽  
Vol 117 (52) ◽  
pp. 33263-33271
Author(s):  
Qiong Wei ◽  
Xuechen Shi ◽  
Tiankai Zhao ◽  
Pingqiang Cai ◽  
Tianwu Chen ◽  
...  
Keyword(s):  
Large Scale ◽  
Traction Force ◽  
Collective Cell Migration ◽  
Actin Ring ◽  
Purse String ◽  
Actin Cable ◽  
Gap Closure ◽  
Actin Fiber ◽  
Ring Segment ◽  
Cable Segment

Gap closure to eliminate physical discontinuities and restore tissue integrity is a fundamental process in normal development and repair of damaged tissues and organs. Here, we demonstrate a nonadhesive gap closure model in which collective cell migration, large-scale actin-network fusion, and purse-string contraction orchestrate to restore the gap. Proliferative pressure drives migrating cells to attach onto the gap front at which a pluricellular actin ring is already assembled. An actin-ring segment switching process then occurs by fusion of actin fibers from the newly attached cells into the actin cable and defusion from the previously lined cells, thereby narrowing the gap. Such actin-cable segment switching occurs favorably at high curvature edges of the gap, yielding size-dependent gap closure. Cellular force microscopies evidence that a persistent rise in the radial component of inward traction force signifies successful actin-cable segment switching. A kinetic model that integrates cell proliferation, actin fiber fusion, and purse-string contraction is formulated to quantitatively account for the gap-closure dynamics. Our data reveal a previously unexplored mechanism in which cells exploit multifaceted strategies in a highly cooperative manner to close nonadhesive gaps.

scholarly journals The Drosophila Shark tyrosine kinase is required for embryonic dorsal closure

2000 ◽  
Vol 14 (5) ◽  
pp. 604-614
Author(s):  
Rafael Fernandez ◽  
Fumitaka Takahashi ◽  
Zhao Liu ◽  
Ruth Steward ◽  
David Stein ◽  
...  
Keyword(s):  
Tyrosine Kinase ◽  
Leading Edge ◽  
Dorsal Closure ◽  
Kinase Gene ◽  
Dorsal Midline ◽  
Jnk Signaling ◽  
Amino Terminal ◽  
Tyrosine Kinase Gene ◽  
Epithelial Sheet ◽  
Jnk Signaling Pathway

Dorsal closure (DC) in the Drosophila embryo requires the coordinated interaction of two different functional domains of the epidermal cell layer—the leading edge (LE) and the lateral epidermis. In response to activation of a conserved c-Jun amino-terminal kinase (JNK) signaling module, the dorsal-most layer of cells, which constitute the LE of the stretching epithelial sheet, secrete Dpp, a member of the TGFβ superfamily. Dpp and other LE cell-derived signaling molecules stimulate the bilateral dorsal elongation of cells of the dorsolateral epidermis over the underlaying amnioserosa and the eventual fusion of their LEs along the dorsal midline. We have found that flies bearing a Shark tyrosine kinase gene mutation,shark1, exhibit a DC-defective phenotype. Dpp fails to be expressed in shark1 mutant LE cells. Consistent with these observations, epidermal-specific reconstitution ofshark function or overexpression of an activated form of c-Jun in the shark1 mutant background, rescues the DC defect. Thus, Shark regulates the JNK signaling pathway leading to Dpp expression in LE cells. Furthermore, constitutive activation of the Dpp pathway throughout the epidermis fails to rescue theshark1 DC defect, suggesting that Shark may function in additional pathways in the LE and/or lateral epithelium.

scholarly journals Wound healing and inflammation: embryos reveal the way to perfect repair

2004 ◽  
Vol 359 (1445) ◽  
pp. 777-784 ◽  
Author(s):  
Michael J. Redd ◽  
Lisa Cooper ◽  
Will Wood ◽  
Brian Stramer ◽  
Paul Martin
Keyword(s):  
Inflammatory Response ◽  
Leading Edge ◽  
Inflammatory Cells ◽  
Small Gtpase ◽  
Null Mouse ◽  
Purse String ◽  
Genetic Studies ◽  
Epithelial Migration ◽  
Naturally Occurring ◽  
Development Proceeds

Tissue repair in embryos is rapid, efficient and perfect and does not leave a scar, an ability that is lost as development proceeds. Wheras adult wound keratinocytes crawl forwards over the exposed substratum to close the gap, a wound in the embryonic epidermis is closed by contraction of a rapidly assembled actin purse string. Blocking assembly of this cable in chick and mouse embryos, by drugs or by inactivation of the small GTPase Rho, severely hinders the re–epithelialization process. Live studies of epithelial repair in GFP–actin–expressing Drosophila embryos reveal actin–rich filopodia associated with the cable, and although these protrusions from leading edge cells appear to play little role in epithelial migration, they are essential for final zippering of the wound edges together—inactivation of Cdc42 prevents their assembly and blocks the final adhesion step. This wound re–epithelialization machinery appears to recapitulate that used during naturally occurring morphogenetic episodes as typified by Drosophila dorsal closure. One key difference between embryonic and adult repair, which may explain why one heals perfectly and the other scars, is the presence of an inflammatory response at sites of adult repair where there is none in the embryo. Our studies of repair in the PU.1 null mouse, which is genetically incapable of raising an inflammatory response, show that inflammation may indeed be partly responsible for scarring, and our genetic studies of inflammation in zebrafish ( Danio rerio ) larvae suggest routes to identifying gene targets for therapeutically modulating the recruitment of inflammatory cells and thus improving adult healing.

scholarly journals Multiple Forces Contribute to Cell Sheet Morphogenesis for Dorsal Closure in Drosophila

2000 ◽  
Vol 149 (2) ◽  
pp. 471-490 ◽  
Author(s):  
Daniel P. Kiehart ◽  
Catherine G. Galbraith ◽  
Kevin A. Edwards ◽  
Wayne L. Rickoll ◽  
Ruth A. Montague
Keyword(s):  
Wound Healing ◽  
Cell Shape ◽  
Cell Sheet ◽  
Leading Edge ◽  
Drosophila Embryo ◽  
Actin Dynamics ◽  
Actin Binding ◽  
Dorsal Closure ◽  
Purse String ◽  
Ultraviolet Laser

The molecular and cellular bases of cell shape change and movement during morphogenesis and wound healing are of intense interest and are only beginning to be understood. Here, we investigate the forces responsible for morphogenesis during dorsal closure with three approaches. First, we use real-time and time-lapsed laser confocal microscopy to follow actin dynamics and document cell shape changes and tissue movements in living, unperturbed embryos. We label cells with a ubiquitously expressed transgene that encodes GFP fused to an autonomously folding actin binding fragment from fly moesin. Second, we use a biomechanical approach to examine the distribution of stiffness/tension during dorsal closure by following the response of the various tissues to cutting by an ultraviolet laser. We tested our previous model (Young, P.E., A.M. Richman, A.S. Ketchum, and D.P. Kiehart. 1993. Genes Dev. 7:29–41) that the leading edge of the lateral epidermis is a contractile purse-string that provides force for dorsal closure. We show that this structure is under tension and behaves as a supracellular purse-string, however, we provide evidence that it alone cannot account for the forces responsible for dorsal closure. In addition, we show that there is isotropic stiffness/tension in the amnioserosa and anisotropic stiffness/tension in the lateral epidermis. Tension in the amnioserosa may contribute force for dorsal closure, but tension in the lateral epidermis opposes it. Third, we examine the role of various tissues in dorsal closure by repeated ablation of cells in the amnioserosa and the leading edge of the lateral epidermis. Our data provide strong evidence that both tissues appear to contribute to normal dorsal closure in living embryos, but surprisingly, neither is absolutely required for dorsal closure. Finally, we establish that the Drosophila epidermis rapidly and reproducibly heals from both mechanical and ultraviolet laser wounds, even those delivered repeatedly. During healing, actin is rapidly recruited to the margins of the wound and a newly formed, supracellular purse-string contracts during wound healing. This result establishes the Drosophila embryo as an excellent system for the investigation of wound healing. Moreover, our observations demonstrate that wound healing in this insect epidermal system parallel wound healing in vertebrate tissues in situ and vertebrate cells in culture (for review see Kiehart, D.P. 1999. Curr. Biol. 9:R602–R605).

scholarly journals An account of the devonian fish, Palæospondylus Gunni , traquair

1904 ◽  
Vol 72 (477-486) ◽  
pp. 98-99
Keyword(s):  
Ventral Surface ◽  
Dorsal Side ◽  
Serial Sections ◽  
Cranial Cavity ◽  
Larval Amphibians ◽  
Lower Jaw ◽  
Branchial Arches ◽  
Vertical Walls

This fossil, which has been variously referred to an alliance with Lampreys, Tadpoles, and Lung-fish, has been successfully studied by means of serial sections. The ventral surface of the head bears four pairs of branchial bars, with the last of which two post-branchial plates, the so-called “post-occipital” plates, are associated; in front of the branchial bars are two pairs of structures, which are regarded as representing the lower jaw and hyoid; they are supported by a suspensory apparatus, which may represent the palato-quadrate and hyo-mandibular elements. The branchial arches are wholly unlike anything seen in Marsipobranchs, but call to mind the similar structures in the Dipnoi and larval Amphibians. The dorsal side of the skull shows a large cranial cavity with thin vertical walls, but no complete roof, a pair of auditory and a pair of nasal capsules.

scholarly journals Differential Thresholds of Proteasome Activation Reveal Two Separable Mechanisms of Sensory Organ Polarization in C. elegans

2021 ◽  
Vol 9 ◽  
Author(s):  
Patricia Kunz ◽  
Christina Lehmann ◽  
Christian Pohl
Keyword(s):  
Alimentary Tract ◽  
De Novo ◽  
Mouth Opening ◽  
Leading Edge ◽  
26S Proteasome ◽  
Sensory Organ ◽  
Apical Constriction ◽  
Animal Evolution ◽  
C Elegans ◽  
Dependent Protein

Cephalization is a major innovation of animal evolution and implies a synchronization of nervous system, mouth, and foregut polarization to align alimentary tract and sensomotoric system for effective foraging. However, the underlying integration of morphogenetic programs is poorly understood. Here, we show that invagination of neuroectoderm through de novo polarization and apical constriction creates the mouth opening in the Caenorhabditis elegans embryo. Simultaneously, all 18 juxta-oral sensory organ dendritic tips become symmetrically positioned around the mouth: While the two bilaterally symmetric amphid sensilla endings are towed to the mouth opening, labial and cephalic sensilla become positioned independently. Dendrite towing is enabled by the pre-polarized sensory amphid pores intercalating into the leading edge of the anteriorly migrating epidermal sheet, while apical constriction-mediated cell–cell re-arrangements mediate positioning of all other sensory organs. These two processes can be separated by gradual inactivation of the 26S proteasome activator, RPN-6.1. Moreover, RPN-6.1 also shows a dose-dependent requirement for maintenance of coordinated apical polarization of other organs with apical lumen, the pharynx, and the intestine. Thus, our data unveil integration of morphogenetic programs during the coordination of alimentary tract and sensory organ formation and suggest that this process requires tight control of ubiquitin-dependent protein degradation.

The C. elegans septin genes, unc-59 and unc-61, are required for normal postembryonic cytokineses and morphogenesis but have no essential function in embryogenesis

2000 ◽  
Vol 113 (21) ◽  
pp. 3825-3837 ◽  
Author(s):  
T.Q. Nguyen ◽  
H. Sawa ◽  
H. Okano ◽  
J.G. White
Keyword(s):  
Caenorhabditis Elegans ◽  
Embryonic Development ◽  
Sensory Neurons ◽  
Leading Edge ◽  
The Other ◽  
Male Tail ◽  
Genomic Database ◽  
C Elegans ◽  
Essential Function ◽  
Normal Embryonic Development

Septins have been shown to play important roles in cytokinesis in diverse organisms ranging from yeast to mammals. In this study, we show that both the unc-59 and unc-61 loci encode Caenorhabditis elegans septins. Genomic database searches indicate that unc-59 and unc-61 are probably the only septin genes in the C. elegans genome. UNC-59 and UNC-61 localize to the leading edge of cleavage furrows and eventually reside at the midbody. Analysis of unc-59 and unc-61 mutants revealed that each septin requires the presence of the other for localization to the cytokinetic furrow. Surprisingly, unc-59 and unc-61 mutants generally have normal embryonic development; however, defects were observed in post-embryonic development affecting the morphogenesis of the vulva, male tail, gonad, and sensory neurons. These defects can be at least partially attributed to failures in post-embryonic cytokineses although our data also suggest other possible roles for septins. unc-59 and unc-61 double mutants show similar defects to each of the single mutants.

scholarly journals Regional rheological differences in locomoting neutrophils

2004 ◽  
Vol 287 (3) ◽  
pp. C603-C611 ◽  
Author(s):  
M. Yanai ◽  
J. P. Butler ◽  
T. Suzuki ◽  
H. Sasaki ◽  
H. Higuchi
Keyword(s):  
Power Law ◽  
Leading Edge ◽  
Cell Types ◽  
Cytochalasin D ◽  
Human Neutrophils ◽  
Cell Cortex ◽  
Structural Damping ◽  
Integrin Receptors ◽  
Storage And Loss Moduli ◽  
Power Law Exponent

Intracellular rheology is a useful probe of the mechanisms underlying spontaneous or chemotactic locomotion and transcellular migration of leukocytes. We characterized regional rheological differences between the leading, body, and trailing regions of isolated, adherent, and spontaneously locomoting human neutrophils. We optically trapped intracellular granules and measured their displacement for 500 ms after a 100-nm step change in the trap position. Results were analyzed in terms of simple viscoelasticity and with the use of structural damping (stress relaxation follows a power law in time). Structural damping fit the data better than did viscoelasticity. Regional viscoelastic stiffness and viscosity or structural damping storage and loss moduli were all significantly lower in leading regions than in pooled body and/or trailing regions (the latter were not significantly different). Structural damping showed similar levels of elastic and dissipative stresses in body and/or trailing regions; leading regions were significantly more fluidlike (increased power law exponent). Cytoskeletal disruption with cytochalasin D or nocodazole made body and/or trailing regions ∼50% less elastic and less viscous. Cytochalasin D completely suppressed pseudopodial formation and locomotion; nocodazole had no effect on leading regions. Neither drug changed the dissipation-storage energy ratio. These results differ from those of studies of neutrophils and other cell types probed at the cell membrane via β2-integrin receptors, which suggests a distinct role for the cell cortex or focal adhesion complexes. We conclude that 1) structural damping well describes intracellular rheology, and 2) while not conclusive, the significantly more fluidlike behavior of the leading edge supports the idea that intracellular pressure may be the origin of motive force in neutrophil locomotion.

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