PTK7 is essential for polarized cell motility and convergent extension during mouse gastrulation (original) (raw)
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Current Biology, 2004
veloppement des Verté bré s Institut Jacques Monod dynamic patterning events still poorly characterized at the molecular and cellular levels. One day after implanta-UMR 7592 CNRS Université Paris 6 et 7 tion, molecular patterning is evident along the proximaldistal (PD) axis of the conceptus [2-4]. Around E5.0, a 2 place Jussieu 75251 Paris subset of visceral endoderm cells at the distal tip of the embryo responds to signaling by the TGF superfamily France 2 Laboratoire de Morphomé trie et Modé lisation member Nodal by expressing a specific repertoire of genes [5]. At the same time, genes later involved in Molé culaire Institut Jacques Monod primitive streak formation such as Nodal and Wnt3 are expressed in a ring of proximal epiblast cells abutting UMR 7592 CNRS Université Paris 6 et 7 the extraembryonic ectoderm [3]. The first symmetrybreaking event in the establishment of AP polarity is the 2 place Jussieu 75251 Paris asymmetric movement of distal visceral endoderm cells to a more proximal position close to the extraembryonic France 3 Laboratoire d'Optique Physique boundary. Once this cell population has reached its new position (E5.75), which defines the anterior side of the É cole Supé rieure de Physique et Chimie Industrielles (ESPCI) embryo, it is called anterior visceral endoderm (AVE) [2, 6-8]. Concomitantly, the Nodal and Wnt3 expression CNRS UPR A0005 10 rue Vauquelin domains become restricted to the opposite, i.e., posterior, side of the embryo [3]. This restriction is thought 75231 Paris France to reflect either a regulation of gene expression in the proximal epiblast or a displacement of proximal epiblast cells toward the posterior side before the onset of gastrulation [2]. Genetic and embryological experiments indicate that AVE cells, which secrete Nodal and Wnt Summary antagonists such as Cer-l, Lefty1, and Dkk1, impart anterior identity on the underlying epiblast by protecting it Background: It is generally assumed that the migration of anterior visceral endoderm (AVE) cells from a distal from the signals that promote the formation of the primitive streak in the posterior epiblast [9-11]. to a proximal position at embryonic day (E)5.5 breaks the radial symmetry of the mouse embryo, marks ante-This model, where a proximal-distal polarity is converted into an anterior-posterior polarity, gives a promi-rior, and conditions the formation of the primitive streak on the opposite side at E6.5. Transverse sections of a nent role to the migration of AVE cells in determining the position where the primitive streak will form. Al-gastrulating mouse embryo fit within the outline of an ellipse, with the primitive streak positioned at one end though there is currently little information on the morphology of the embryos at these stages, the model of its long axis. How the establishment of anterior-posterior (AP) polarity relates to the morphology of the postim-seems to rely on the assumption that at the egg-cylinder stage (E5.0), the mouse embryo is radially symmetrical plantation embryo is, however, unclear. Results: Transverse sections of prestreak E6.0 em-and the migration of AVE cells toward the anterior pole initiates changes in the embryo's shape leading up to bryos also reveal an elliptical outline, but the AP axis, bilateral symmetry. Understanding these events in reladefined by molecular markers, tends to be perpendicular tion to prestreak embryo morphology will be important to the long axis of the ellipse. Subsequently, the relative to address a number of issues such as why or how AVE orientations of the AP axis and of the long axis change cells migrate in a particular direction, whether posterior so that when gastrulation begins, they are closer to is specified before AVE migration, and how the primitive being parallel, albeit not exactly aligned. As a result, streak actually forms. most embryos briefly lose their bilateral symmetry when In contrast to prestreak embryos, the morphology of the primitive streak starts forming in the epiblast. the midgastrula embryo is well known [1]. It can be Conclusions: The change in the orientation of the AP described as a flattened cylinder, where the AP axis runs axis is only apparent and results from a dramatic remodalong the medial part of the embryonic region (Figure 1). eling of the whole epiblast, in which cell migrations take Transverse sections of midstreak-stage embryos reveal no part. These results reveal a level of regulation and an elliptical outline with two geometrical axes, desigplasticity so far unsuspected in the mouse gastrula. nated long and short. At this stage, the AP axis, marked by the primitive streak at the posterior pole, is aligned with the long axis.
Journal of Cell Biology, 2008
During vertebrate gastrulation, convergence and extension (C&E) movements narrow and lengthen the embryonic tissues, respectively. In zebrafish, regional differences of C&E movements have been observed; however, the underlying cell behaviors are poorly understood. Using time-lapse analyses and computational modeling, we demonstrate that C&E of the medial presomitic mesoderm is achieved by cooperation of planar and radial cell intercalations. Radial intercalations preferentially separate anterior and posterior neighbors to promote extension. In knypek;trilobite noncanonical Wnt mutants, the frequencies of cell intercalations are altered and the anteroposterior bias of radial intercalations is lost. This provides evidence for noncanonical Wnt signaling polarizing cell movements between different mesodermal cell layers. We further show using fluorescent fusion proteins that during dorsal mesoderm C&E, the noncanonical Wnt component Prickle localizes at the anterior cell edge, whereas D...
During gastrulation in the mouse embryo, dynamic cell movements including epiblast invagination and mesodermal layer expansion lead to the establishment of the three-layered body plan. The precise details of these movements, however, are sometimes elusive, because of the limitations in live imaging. To overcome this problem, we developed techniques to enable observation of living mouse embryos with digital scanned light sheet microscope (DSLM). The achieved deep and high time-resolution images of GFP-expressing nuclei and following 3D tracking analysis revealed the following findings: (i) Interkinetic nuclear migration (INM) occurs in the epiblast at embryonic day (E)6 and 6.5. (ii) INM-like migration occurs in the E5.5 embryo, when the epiblast is a monolayer and not yet pseudostratified. (iii) Primary driving force for INM at E6.5 is not pressure from neighboring nuclei. (iv) Mesodermal cells migrate not as a sheet but as individual cells without coordination.
Planar Cell Movements and Axial Patterning During Early Gastrulation of the Rabbit Embryo
2014
Animal gastrulation specifies the embryonic axes and induces the first major change in cell shape after fertilisation. The ‘milieu intérieur’ is thus created in disparate topographical arrangements such as the circular blastopore of amphibia or the straight primitive streak of amniotes (birds and mammals). We modified mammalian gastrulation topography by interfering selectively with pre-gastrulation planar cell movements using rabbit blastocyst cultures. Time-lapse videomicroscopy, ultrastructural analysis and gene expression after Rho kinase inhibition show a dose-dependent molding of the prospective primitive streak into regularly patterned circular or arch-like forms, as known in amphibia, fish or reptiles. The mammalian embryo reveals that temporal shift and consecutive adjustment of planar cell movements can be instrumental to the evolution of gastrulation forms.
Development, 2011
During vertebrate gastrulation, convergence and extension cell movements are coordinated with the anteroposterior and mediolateral embryonic axes. Wnt planar cell polarity (Wnt/PCP) signaling polarizes the motile behaviors of cells with respect to the anteroposterior embryonic axis. Understanding how Wnt/PCP signaling mediates convergence and extension (C&E) movements requires analysis of the mechanisms employed to alter cell morphology and behavior with respect to embryonic polarity. Here, we examine the interactions between the microtubule cytoskeleton and Wnt/PCP signaling during zebrafish gastrulation. First, we assessed the location of the centrosome/microtubule organizing center (MTOC) relative to the cell nucleus and the body axes, as a marker of cell polarity. The intracellular position of MTOCs was polarized, perpendicular to the plane of the germ layers, independently of Wnt/PCP signaling. In addition, this position became biased posteriorly and medially within the plane o...
Coordination of Cell Polarity during Xenopus Gastrulation
PLoS ONE, 2008
Cell polarity is an essential feature of animal cells contributing to morphogenesis. During Xenopus gastrulation, it is known that chordamesoderm cells are polarized and intercalate each other allowing anterior-posterior elongation of the embryo proper by convergent extension (CE). Although it is well known that the cellular protrusions at both ends of polarized cells exert tractive force for intercalation and that PCP pathway is known to be essential for the cell polarity, little is known about what triggers the cell polarization and what the polarization causes to control intracellular events enabling the intercalation that leads to the CE. In our research, we used EB3 (end-binding 3), a member of +TIPs that bind to the plus end of microtubule (MT), to visualize the intracellular polarity of chordamesoderm cells during CE to investigate the trigger of the establishment of cell polarity. We found that EB3 movement is polarized in chordamesoderm cells and that the notochordsomite tissue boundary plays an essential role in generating the cell polarity. This polarity was generated before the change of cell morphology and the polarized movement of EB3 in chordamesoderm cells was also observed near the boundary between the chordamesoderm tissue and naïve ectoderm tissue or lateral mesoderm tissues induced by a low concentration of nodal mRNA. These suggest that definitive tissue separation established by the distinct levels of nodal signaling is essential for the chordamesodermal cells to acquire mediolateral cell polarity.
Developmental Cell, 2001
cells employ unipolar, protrusive activity to intercalate between lateral neighbors, driving convergence and si-1 Department of Biological Sciences Vanderbilt University multaneous tissue extension (Keller et al., 2000). In contrast, in embryos of teleost fish, lateral cells initially mi-VU Station B 351634 Nashville, Tennessee 37235 grate dorsally with increasing speed as individuals or groups, effecting narrowing and thickening of the tissue, 2 Institute of Neuroscience 1254 University of Oregon but not extension (Sepich et al., 2000; Trinkaus et al., 1992). CE driven by medio-lateral intercalation is thought Eugene, Oregon 97403 3 Max-Planck Institut fü r Immunbiologie to be confined to the dorsal region of the gastrula (Kimmel et al., 1994). Stü beweg 51 D-79108 Freiburg Several lines of evidence implicate Wnt signaling in regulation of polarized cell morphology and medio-lat-Germany eral cell intercalation underlying CE. Zebrafish silberblick (slb, wnt11) and pipetail (ppt, wnt5) mutants exhibit
Initiation of convergence and extension movements of lateral mesoderm during zebrafish gastrulation
Developmental Dynamics, 2005
Embryonic morphogenesis is accomplished by cellular movements, rearrangements, and cell fate inductions. Vertebrate gastrulation entails morphogenetic processes that generate three germ layers, endoderm, mesoderm, and ectoderm, shaped into head, trunk, and tail. To understand how cell migration mechanistically contributes to tissue shaping during gastrulation, we examined migration of lateral mesoderm in the zebrafish. Our results illustrate that cell behaviors, different from mediolaterally oriented cell intercalation, also promote convergence and extension (C&E). During early gastrulation, upon internalization, individually migrating mesendodermal cells contribute to the elongation of the mesoderm by moving animally, without dorsal movement. Convergence toward dorsal starts later, by 70% epiboly (7.7 hpf). Depending on location along the Animal-Vegetal axis, an animal or vegetal bias is added to the dorsalward movement, so that paths fan out and the lateral mesoderm both converges and extends. Onset of convergence is independent of noncanonical Wnt signaling but is delayed when Stat3 signaling is compromised. To understand which aspects of motility are controlled by guidance cues, we measured turning behavior of lateral mesodermal cells. We show that cells exhibit directional preference, directionally-regulated speed, and turn toward dorsal when off-course. We estimate that ectoderm could supply from a fraction to all the dorsalward displacement seen in mesoderm cells. Using mathematical modeling, we demonstrate that directional preference is sufficient to account for mesoderm convergence and extension, and that, at minimum, two sources of guidance cues could orient cell paths realistically if located in the dorsal midline. Developmental Dynamics 234: 279 -292, 2005.
Convergent extension in mammalian morphogenesis
Seminars in Cell & Developmental Biology, 2019
Convergent extension is a fundamental morphogenetic process that underlies not only the generation of the elongated vertebrate body plan from the initially radially symmetrical embryo, but also the specific shape changes characteristic of many individual tissues. These tissue shape changes are the result of specific cell behaviors, coordinated in time and space, and affected by the physical properties of the tissue. While mediolateral cell intercalation is the classic cellular mechanism for producing tissue convergence and extension, other cell behaviors can also provide similar tissue-scale distortions or can modulate the effects of mediolateral cell intercalation to sculpt a specific shape. Regulation of regional tissue morphogenesis through planar polarization of the variety of underlying cell behaviors is well-recognized, but as yet is not well understood at the molecular level. Here, we review recent advances in understanding the cellular basis for convergence and extension and its regulation. 2.1. General mechanisms of mesenchymal convergent extension Mesenchymal (non-epithelial) cells provided the initial paradigm