Wnt/PCP signaling controls intracellular position of MTOCs during gastrulation convergence and extension movements

Sepich, Diane S.; Usmani, Mohsinah; Pawlicki, Staci; Solnica‐Krezel, Lila

doi:10.1242/dev.053959

Cited by 74 publications

(87 citation statements)

References 82 publications

(123 reference statements)

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“…However, there are several features of lateral mesendoderm progenitors that distinguish them from cells undergoing either collective migration or intercalation alone. First, the microtubule-organizing center (MTOC) is positioned in posterior-medial regions of these cells, and not along the axis of cell migration as described for other cell types undergoing directed migration (Sepich et al, 2011). Second, the localization of core Wnt/PCP components at the anterior and posterior sides of these cells does not correlate with their ML elongation and polarization (Yin et al, 2008).…”

Section: Coordinating Collective Cell Migration and Cell Intercalationmentioning

confidence: 92%

Convergent extension: using collective cell migration and cell intercalation to shape embryos

2012

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SummaryBody axis elongation represents a common and fundamental morphogenetic process in development. A key mechanism triggering body axis elongation without additional growth is convergent extension (CE), whereby a tissue undergoes simultaneous narrowing and extension. Both collective cell migration and cell intercalation are thought to drive CE and are used to different degrees in various species as they elongate their body axis. Here, we provide an overview of CE as a general strategy for body axis elongation and discuss conserved and divergent mechanisms underlying CE among different species. Key words: Convergent extension, Collective cell migration, Cell intercalation, Planar cell polarity IntroductionConvergent extension (CE) is a key process by which tissues undergo narrowing along one axis and concomitant extension along another axis. The first identified and best-studied example of CE in development is body axis elongation during gastrulation (reviewed by Keller et al., 2000). Generally, CE in body axis elongation is characterized by the collective movement of germ layer progenitor cells towards the dorsal side of the gastrula, where the embryonic body axis will form, accompanied or followed by cell intercalations along their axis of movement. This combination of collective cell movement and cell intercalations triggers narrowing of the body axis along its medial-lateral (ML) axis (i.e. the convergence) and elongation along its anterior-posterior (AP) axis (i.e. the extension). CE thus includes two fundamentally different types of cell movement ( Fig. 1): collective cell migration (see Glossary, Box 1), which commonly describes the coordinated movement of a highly cohesive sheet of cells; and cell intercalations (see Glossary, Box 1), whereby oriented exchanges of neighboring cells alter tissue geometry.In this Primer (see Box, Development: the big picture), we review how cells intermittently use collective migration and cell intercalation in CE-driven body axis elongation during gastrulation in various species. We also discuss the cell-intrinsic and extrinsic factors that determine the contribution of these different movement types to CE. Finally, we highlight the key molecular and genetic pathways involved in CE, but refer the reader to recent reviews of this topic (Gray et al., 2011;Skoglund and Keller, 2010) for further details on these pathways. CE during zebrafish gastrulation: a case for collective cell migrationAt the onset of gastrulation in zebrafish, mesoderm and endoderm (mesendoderm) progenitor cells internalize at the germ ring margin (see Glossary, Box 1) and subsequently migrate away from the margin towards the animal pole ( Fig. 2A). Progenitors that internalize in the region of the embryonic organizer (the shield) and give rise to the anterior axial mesendoderm (the prechordal plate) migrate as a highly cohesive cluster of cells, typical of collective migration (reviewed by Friedl and Gilmour, 2009). Once all of the prechordal plate progenitor cells have internalized, the prechordal p...

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Section: Coordinating Collective Cell Migration and Cell Intercalationmentioning

confidence: 92%

Convergent extension: using collective cell migration and cell intercalation to shape embryos

2012

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“…The lengthening and narrowing of a field of cells, termed convergent extension, contributes to a variety of morphogenetic processes including gastrulation. During zebrafish gastrulation, the centrosome position is highly polarized along the anteroposterior and mediolateral embryonic axes (Sepich et al, 2011). Centrosomes first polarize along a superficial-deep axis through the ectoderm and mesoderm, and later become polarized within the planes of the ectoderm and mesoderm between mid and late gastrulation.…”

Section: Convergent Extensionmentioning

confidence: 99%

Centrosome positioning in vertebrate development

Tang

Marshall

2012

Journal of Cell Science

115

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SummaryThe centrosome, a major organizer of microtubules, has important functions in regulating cell shape, polarity, cilia formation and intracellular transport as well as the position of cellular structures, including the mitotic spindle. By means of these activities, centrosomes have important roles during animal development by regulating polarized cell behaviors, such as cell migration or neurite outgrowth, as well as mitotic spindle orientation. In recent years, the pace of discovery regarding the structure and composition of centrosomes has continuously accelerated. At the same time, functional studies have revealed the importance of centrosomes in controlling both morphogenesis and cell fate decision during tissue and organ development. Here, we review examples of centrosome and centriole positioning with a particular emphasis on vertebrate developmental systems, and discuss the roles of centrosome positioning, the cues that determine positioning and the mechanisms by which centrosomes respond to these cues. The studies reviewed here suggest that centrosome functions extend to the development of tissues and organs in vertebrates.

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“…MTs are also required for the convergent extension movements of gastrulation (Lane and Keller, 1997;Sepich et al, 2011;Shindo et al, 2008), although it is unknown whether JNK signaling influences MT architecture in this context. Nonetheless, JNK plays pivotal roles in MT organization and stability in other cell types.…”

Section: Jnk Regulates Microtubule Architecture During Endoderm Rearrmentioning

confidence: 99%

Jun N-terminal kinase maintains tissue integrity during cell rearrangement in the gut

Dush

Nascone-Yoder

2013

Development

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SUMMARYTissue elongation is a fundamental morphogenetic process that generates the proper anatomical topology of the body plan and vital organs. In many elongating embryonic structures, tissue lengthening is driven by Rho family GTPase-mediated cell rearrangement. During this dynamic process, the mechanisms that modulate intercellular adhesion to allow individual cells to change position without compromising structural integrity are not well understood. In vertebrates, Jun N-terminal kinase (JNK) is also required for tissue elongation, but the precise cellular role of JNK in this context has remained elusive. Here, we show that JNK activity is indispensable for the rearrangement of endoderm cells that underlies the elongation of the Xenopus gut tube. Whereas Rho kinase is necessary to induce cell intercalation and remodel adhesive contacts, we have found that JNK is required to maintain cell-cell adhesion and establish parallel microtubule arrays; without JNK activity, the reorganizing endoderm dissociates. Depleting polymerized microtubules phenocopies this effect of JNK inhibition on endoderm morphogenesis, consistent with a model in which JNK regulates microtubule architecture to preserve adhesive contacts between rearranging gut cells. Thus, in contrast to Rho kinase, which generates actomyosinbased tension and cell movement, JNK signaling is required to establish microtubule stability and maintain tissue cohesion; both factors are required to achieve proper cell rearrangement and gut extension. This model of gut elongation has implications not only for the etiology of digestive tract defects, but sheds new light on the means by which intra-and intercellular forces are balanced to promote topological change, while preserving structural integrity, in numerous morphogenetic contexts.

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Wnt/PCP signaling controls intracellular position of MTOCs during gastrulation convergence and extension movements

Cited by 74 publications

References 82 publications

Convergent extension: using collective cell migration and cell intercalation to shape embryos

Convergent extension: using collective cell migration and cell intercalation to shape embryos

Centrosome positioning in vertebrate development

Jun N-terminal kinase maintains tissue integrity during cell rearrangement in the gut

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