Morphogenetic pattern formation during ascidian notochord formation is regulative and highly robust

Development ◽  
2002 ◽  
Vol 129 (1) ◽  
pp. 1-12 ◽  
Author(s):  
Edwin M. Munro ◽  
Garrett Odell
Keyword(s):  
Confocal Microscopy ◽  
Cell Shape ◽  
Shape Change ◽  
Time Lapse ◽  
Neural Plate ◽  
Convergent Extension ◽  
Complex Interplay ◽  
Cell Stage ◽  
Cell Shape Change ◽  
Global Patterns

The ascidian notochord forms through simultaneous invagination and convergent extension of a monolayer epithelial plate. Here we combine micromanipulation with time lapse and confocal microscopy to examine how notochord-intrinsic morphogenetic behaviors and interactions with surrounding tissues, determine these global patterns of movement. We show that notochord rudiments isolated at the 64-cell stage divide and become motile with normal timing; but, in the absence of interactions with non-notochordal tissues, they neither invaginate nor converge and extend. We find that notochord formation is robust in the sense that no particular neighboring tissue is required for notochord formation. Basal contact with either neural plate or anterior endoderm/lateral mesenchyme or posterior mesoderm are each alone sufficient to ensure that the notochord plate forms and extends a cylindrical rod. Surprisingly, the axis of convergent extension depends on the specific tissues that contact the notochord, as do other patterns of cell shape change, movement and tissue deformation that accompany notochord formation. We characterize one case in detail, namely, embryos lacking neural plates, in which a normal notochord forms but by an entirely different trajectory. Our results show ascidian notochord formation to be regulative in a fashion and to a degree never before appreciated. They suggest this regulative behavior depends on a complex interplay between morphogenetic tendencies intrinsic to the notochord plate and instructive and permissive interactions with surrounding tissues. We discuss mechanisms that could account for these data and what they imply about notochord morphogenesis and its evolution within the chordate phylum.

scholarly journals Apical Accumulation of Rho in the Neural Plate Is Important for Neural Plate Cell Shape Change and Neural Tube Formation

2008 ◽  
Vol 19 (5) ◽  
pp. 2289-2299 ◽  
Author(s):  
Nagatoki Kinoshita ◽  
Noriaki Sasai ◽  
Kazuyo Misaki ◽  
Shigenobu Yonemura
Keyword(s):  
Neural Tube ◽  
Rho Gtpases ◽  
Cell Shape ◽  
Shape Change ◽  
Myosin Ii ◽  
Tube Formation ◽  
Neural Plate ◽  
Cell Shape Change ◽  
Neural Tube Formation

Although Rho-GTPases are well-known regulators of cytoskeletal reorganization, their in vivo distribution and physiological functions have remained elusive. In this study, we found marked apical accumulation of Rho in developing chick embryos undergoing folding of the neural plate during neural tube formation, with similar accumulation of activated myosin II. The timing of accumulation and biochemical activation of both Rho and myosin II was coincident with the dynamics of neural tube formation. Inhibition of Rho disrupted its apical accumulation and led to defects in neural tube formation, with abnormal morphology of the neural plate. Continuous activation of Rho also altered neural tube formation. These results indicate that correct spatiotemporal regulation of Rho is essential for neural tube morphogenesis. Furthermore, we found that a key morphogenetic signaling pathway, the Wnt/PCP pathway, was implicated in the apical accumulation of Rho and regulation of cell shape in the neural plate, suggesting that this signal may be the spatiotemporal regulator of Rho in neural tube formation.

scholarly journals A contractile actomyosin network linked to adherens junctions by Canoe/afadin helps drive convergent extension

2011 ◽  
Vol 22 (14) ◽  
pp. 2491-2508 ◽  
Author(s):  
Jessica K. Sawyer ◽  
Wangsun Choi ◽  
Kuo-Chen Jung ◽  
Li He ◽  
Nathan J. Harris ◽  
...  
Keyword(s):  
Cell Shape ◽  
Shape Change ◽  
Adherens Junction ◽  
Tissue Level ◽  
The Body ◽  
Convergent Extension ◽  
Planar Polarity ◽  
Cell Shape Change ◽  
Apical Polarity ◽  
Polarity Proteins

Integrating individual cell movements to create tissue-level shape change is essential to building an animal. We explored mechanisms of adherens junction (AJ):cytoskeleton linkage and roles of the linkage regulator Canoe/afadin during Drosophila germband extension (GBE), a convergent-extension process elongating the body axis. We found surprising parallels between GBE and a quite different morphogenetic movement, mesoderm apical constriction. Germband cells have an apical actomyosin network undergoing cyclical contractions. These coincide with a novel cell shape change—cell extension along the anterior–posterior (AP) axis. In Canoe's absence, GBE is disrupted. The apical actomyosin network detaches from AJs at AP cell borders, reducing coordination of actomyosin contractility and cell shape change. Normal GBE requires planar polarization of AJs and the cytoskeleton. Canoe loss subtly enhances AJ planar polarity and dramatically increases planar polarity of the apical polarity proteins Bazooka/Par3 and atypical protein kinase C. Changes in Bazooka localization parallel retraction of the actomyosin network. Globally reducing AJ function does not mimic Canoe loss, but many effects are replicated by global actin disruption. Strong dose-sensitive genetic interactions between canoe and bazooka are consistent with them affecting a common process. We propose a model in which an actomyosin network linked at AP AJs by Canoe and coupled to apical polarity proteins regulates convergent extension.

Polarized basolateral cell motility underlies invagination and convergent extension of the ascidian notochord

Development ◽  
2002 ◽  
Vol 129 (1) ◽  
pp. 13-24 ◽  
Author(s):  
Edwin M. Munro ◽  
Garrett M. Odell
Keyword(s):  
Cell Motility ◽  
Laser Scanning ◽  
Shape Change ◽  
Three Dimensional ◽  
Leading Edge ◽  
Time Lapse ◽  
Convergent Extension ◽  
Cellular Mechanisms ◽  
Cell Shape Change ◽  
Edge Extension

We use 3D time-lapse analysis of living embryos and laser scanning confocal reconstructions of fixed, staged, whole-mounted embryos to describe three-dimensional patterns of cell motility, cell shape change, cell rearrangement and tissue deformation that accompany formation of the ascidian notochord. We show that notochord formation involves two simultaneous processes occurring within an initially monolayer epithelial plate: The first is invagination of the notochord plate about the axial midline to form a solid cylindrical rod. The second is mediolaterally directed intercalation of cells within the plane of the epithelial plate, and then later about the circumference of the cylindrical rod, that accompanies its extension along the anterior/posterior (AP) axis. We provide evidence that these shape changes and rearrangements are driven by active extension of interior basolateral notochord cell edges directly across the faces of their adjacent notochord neighbors in a manner analogous to leading edge extension of lamellapodia by motile cells in culture. We show further that local edge extension is polarized with respect to both the AP axis of the embryo and the apicobasal axis of the notochord plate. Our observations suggest a novel view of how active basolateral motility could drive both invagination and convergent extension of a monolayer epithelium. They further reveal deep similarities between modes of notochord morphogenesis exhibited by ascidians and other chordate embryos, suggesting that cellular mechanisms of ascidian notochord formation may operate across the chordate phylum.

Formation of the notochord in living ascidian embryos

Development ◽  
1985 ◽  
Vol 86 (1) ◽  
pp. 1-17
Author(s):  
David M. Miyamoto
Keyword(s):  
Cell Growth ◽  
Cell Shape ◽  
Dynamic Behaviour ◽  
Shape Change ◽  
Time Lapse ◽  
Differential Interference Contrast ◽  
Cell Shape Change ◽  
A Cell ◽  
Ascidian Embryos ◽  
Dic Microscopy

The dynamic behaviour of cells during formation of the notochord in the ascidian, Ciona intestinalis, was examined by means of Differential Interference Contrast (DIC) microscopy and time-lapse videorecording. The initial rudiment is formed in part as a consequence of the pattern of mitotic divisions as the blastopore shifts posteriorly. Vertical and horizontal rearrangements produce an elongate rod of disc-shaped cells stacked end to end. Further elongation is accompanied by a cell shape change. Some cell growth or swelling is indicated to occur later in development, but this growth appears to contribute mostly to an increase in the diameter, and only insignificantly to the length of the notochord. Intracellular vacuoles that appear around 13 h after fertilization increase in size and fuse at about 16 h to form intercellular ones. These in turn merge to form the central matrix core of the notochord at around 18 to 20 h. As the notochord elongates and cells change in shape, the basal surfaces bleb actively. This surface activity may be related to formation of the perinotochordal sheath.

The role of microtubules in chick blastoderm expansion—a quantitative study using colchicine

Development ◽  
1975 ◽  
Vol 34 (1) ◽  
pp. 265-277
Author(s):  
J. R. Downie
Keyword(s):  
Cell Division ◽  
Cell Shape ◽  
Shape Change ◽  
Cell Sheet ◽  
Cell Movement ◽  
Vitelline Membrane ◽  
General Context ◽  
Chick Blastoderm ◽  
Cell Shape Change ◽  
Cytoplasmic Microtubules

Since their discovery, cytoplasmic microtubules have been much studied in the context of cell movement and cell shape change. Much of the work has used drugs, particularly colchicine and its relatives, which break down microtubules — the so-called anti-tubulins. Colchicine inhibits the orientated movements of many cell types in vitro, and disrupts cell shape change in several morphogenetic situations. The investigation reported here used chick blastoderm expansion in New culture in an attempt to quantify the colchicine effect on orientated cell movement. However, although colchicine could halt blastoderm expansion entirely, a simple interpretation was not possible. (1) Colchicine at concentrations capable of blocking mitosis, and of disrupting all or most of the cytoplasmic microtubules of the cells studied, inhibited blastoderm expansion, often resulting in an overall retraction of the cell sheet. (2) Though blastoderm expansion does normally involve considerable cell proliferation, the colchicine effect could not be ascribed to a block on cell division since aminopterin, which stops cell division without affecting microtubules, did not inhibit expansion. (3) Blastoderm expansion is effected by the locomotion of a specialized band of edge cells at the blastoderm periphery. These are the only cells normally attached to the vitelline membrane — the substrate for expansion. When most of the blastoderm was excised, leaving the band of edge cells, and the cultures then treated with colchicine, expansion occurred normally. The colchicine effect on blastoderm expansion could not therefore be ascribed to a direct effect on the edge cells. (4) An alternative site of action of the drug is the remaining cells of the blastoderm. These normally become progressively flatter as expansion proceeds. If flattening in these cells is even partially dependent on their cytoplasmic microtubules, disruption of these microtubules might result in the inherent contractility of the cells resisting and eventually halting edge cell migration. That cell shape in these cells is dependent on microtubules was demonstrated by treating flat blastoderm fragments with colchicine. On incubation, the area occupied by these fragments decreased by 25–30 % more than controls. The significance of these results in the general context of orientated cell movements and cell shape determination is discussed, with particular emphasis on the analogous system of Fundulus epiboly.

Autonomy and non-autonomy in Drosophila mesoderm determination and morphogenesis

Development ◽  
1994 ◽  
Vol 120 (4) ◽  
pp. 853-859 ◽  
Author(s):  
M. Leptin ◽  
S. Roth
Keyword(s):  
Cell Shape ◽  
Shape Change ◽  
Developmental Program ◽  
Cell Shape Change ◽  
Ventral Furrow ◽  
Large Numbers ◽  
The Individual ◽  
Mutant Cells ◽  
Transplantation Experiments ◽  
Shape Changes

The mesoderm in Drosophila invaginates by a series of characteristic cell shape changes. Mosaics of wild-type cells in an environment of mutant cells incapable of making mesodermal invaginations show that this morphogenetic behaviour does not require interactions between large numbers of cells but that small patches of cells can invaginate independent of their neighbours' behaviour. While the initiation of cell shape change is locally autonomous, the shapes the cells assume are partly determined by the individual cell's environment. Cytoplasmic transplantation experiments show that areas of cells expressing mesodermal genes ectopically at any position in the egg form an invagination. We propose that ventral furrow formation is the consequence of all prospective mesodermal cells independently following their developmental program. Gene expression at the border of the mesoderm is induced by the apposition of mesodermal and non-mesodermal cells.

scholarly journals Tissue tectonics: morphogenetic strain rates, cell shape change and intercalation

2009 ◽  
Vol 6 (6) ◽  
pp. 458-464 ◽  
Author(s):  
Guy B Blanchard ◽  
Alexandre J Kabla ◽  
Nora L Schultz ◽  
Lucy C Butler ◽  
Benedicte Sanson ◽  
...  
Keyword(s):  
Cell Shape ◽  
Shape Change ◽  
Strain Rates ◽  
Cell Shape Change

A dominant inhibitory version of the small GTP-binding protein Rac disrupts cytoskeletal structures and inhibits developmental cell shape changes in Drosophila

Development ◽  
1995 ◽  
Vol 121 (3) ◽  
pp. 903-914 ◽  
Author(s):  
N. Harden ◽  
H.Y. Loh ◽  
W. Chia ◽  
L. Lim
Keyword(s):  
Epidermal Cell ◽  
Cell Shape ◽  
Shape Change ◽  
Yeast Cells ◽  
Cell Shape Change ◽  
Gtp Binding ◽  
Wide Range ◽  
Cell Shape Changes ◽  
Germband Retraction ◽  
Shape Changes

The Rho subfamily of Ras-related small GTP-binding proteins is involved in regulation of the cytoskeleton. The cytoskeletal changes induced by two members of this subfamily, Rho and Rac, in response to growth factor stimulation, have dramatic effects on cell morphology. We are interested in using Drosophila as a system for studying how such effects participate in development. We have identified two Drosophila genes, DRacA and DRacB, encoding proteins with homology to mammalian Rac1 and Rac2. We have made transgenic flies bearing dominant inhibitory (N17DRacA), and wild-type versions of the DRacA cDNA under control of an Hsp70 promoter. Expression of the N17DRacA transgene during embryonic development causes a high frequency of defects in dorsal closure which are due to disruption of cell shape changes in the lateral epidermis. Embryonic expression of N17DRacA also affects germband retraction and head involution. The epidermal cell shape defects caused by expression of N17DRacA are accompanied by disruption of a localized accumulation of actin and myosin thought to be driving epidermal cell shape change. Thus the Rho subfamily may be generating localized changes in the cytoskeleton during Drosophila development in a similar fashion to that seen in mammalian and yeast cells. The Rho subfamily is likely to be participating in a wide range of developmental processes in Drosophila through its regulation of the cytoskeleton.

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