Stereotypical Cell Division Orientation Controls Neural Rod Midline Formation in Zebrafish

Quesada-Hernández, Elena; Caneparo, Luca; Schneider, Silvia; Winkler, Sylke; Liebling, Michael; Fraser, Scott E.; Heisenberg, Carl‐Philipp

doi:10.1016/j.cub.2010.10.009

Cited by 91 publications

(109 citation statements)

References 28 publications

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“…Divisions oriented preferentially to an elongating axis have the potential to facilitate polarized extension of that tissue. This mechanism has been reported for zebrafish gastrulation, for example (Gong, Mo, & Fraser, 2004; Quesada-Hernández et al, 2010). In chick primitive streak formation, cells divide at the midline to orient primitive streak development (Wei & Mikawa, 2000).…”

Section: Introductionsupporting

confidence: 64%

New insights from a high-resolution look at gastrulation in the sea urchin, Lytechinus variegatus

Martik¹,

McClay²

2017

Mechanisms of Development

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Background Gastrulation is a complex orchestration of movements by cells that are specified early in development. Until now, classical convergent extension was considered to be the main contributor to sea urchin archenteron extension, and the relative contributions of cell divisions were unknown. Active migration of cells along the axis of extension was also not considered as a major factor in invagination. Results Cell transplantations plus live imaging were used to examine endoderm cell morphogenesis during gastrulation at high-resolution in the optically clear sea urchin embryo. The invagination sequence was imaged throughout gastrulation. One of the eight macromeres was replaced by a fluorescently labeled macromere at the 32 cell stage. At gastrulation those patches of fluorescent endoderm cell progeny initially about 4 cells wide, released a column of cells about 2 cells wide early in gastrulation and then often this column narrowed to one cell wide by the end of archenteron lengthening. The primary movement of the column of cells was in the direction of elongation of the archenteron with the narrowing (convergence) occurring as one of the two cells moved ahead of its neighbor. As the column narrowed, the labeled endoderm cells generally remained as a contiguous population of cells, rarely separated by intrusion of a lateral unlabeled cell. This longitudinal cell migration mechanism was assessed quantitatively and accounted for almost 90% of the elongation process. Much of the extension was the contribution of Veg2 endoderm with a minor contribution late in gastrulation by Veg1 endoderm cells. We also analyzed the contribution of cell divisions to elongation. Endoderm cells in Lytechinus variagatus were determined to go through approximately one cell doubling during gastrulation. That doubling occurs without a net increase in cell mass, but the question remained as to whether oriented divisions might contribute to archenteron elongation. We learned that indeed there was a biased orientation of cell divisions along the plane of archenteron elongation, but when the impact of that bias was analyzed quantitatively, it contributed a maximum 15% to the total elongation of the gut. Conclusions The major driver of archenteron elongation in the sea urchin, Lytechinus variagatus, is directed movement of Veg2 endoderm cells as a narrowing column along the plane of elongation. The narrowing occurs as cells in the column converge as they migrate, so that the combination of migration and the angular convergence provide the major component of the lengthening. A minor contributor to elongation is oriented cell divisions that contribute to the lengthening but no more than about 15%.

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Section: Introductionsupporting

confidence: 64%

New insights from a high-resolution look at gastrulation in the sea urchin, Lytechinus variegatus

Martik¹,

McClay²

2017

Mechanisms of Development

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show abstract

“…2B; perpendicular). Studies in zebrafish gastrulation have shown that cells in dorsal tissues preferentially divide along the animal-vegetal axis of the embryo (Gong et al, 2004) and may be coupled with cell rearrangements and cell shape changes to drive axis elongation (Quesada-Hernández et al, 2010). Within the chick primitive streak, oriented cell divisions play a role in streak elongation (Wei and Mikawa, 2000).…”

Section: Cranial Neural Crest Cell Proliferation Dynamicsmentioning

confidence: 99%

The neural crest cell cycle is related to phases of migration in the head

et al. 2014

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Embryonic cells that migrate long distances must critically balance cell division in order to maintain stream dynamics and population of peripheral targets. Yet details of individual cell division events and how cell cycle is related to phases of migration remain unclear. Here, we examined these questions using the chick cranial neural crest (NC). In vivo time-lapse imaging revealed that a typical migrating NC cell division event lasted ~1 hour and included four stereotypical steps. Cell tracking showed that dividing NC cells maintained position relative to non-dividing neighbors. NC cell division orientation and the time and distance to first division after neural tube exit were stochastic. To address how cell cycle is related to phases of migration, we used FACs analysis to identify significant spatiotemporal differences in NC cell cycle profiles. Two-photon photoconversion of single and small numbers of mKikGR-labeled NC cells confirmed that lead NC cells exhibited a nearly fourfold faster doubling time after populating the branchial arches. By contrast, Ki-67 staining showed that one out of every five later emerging NC cells exited the cell cycle after reaching proximal head targets. The relatively quiescent mitotic activity during NC cell migration to the branchial arches was altered when premigratory cells were reduced in number by tissue ablation. Together, our results provide the first comprehensive details of the pattern and dynamics of cell division events during cranial NC cell migration.

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“…Genetic and fatemapping studies demonstrate the existence of a population of bipotential neural/mesodermal stem cells in the mouse and zebrafish tailbud (Martin and Kimelman, 2012;Takemoto et al, 2011;Tzouanacou et al, 2009). Inhibition of cell division during gastrulation and/or the segmentation period modestly reduces body length, suggesting that cell migration primarily drives elongation (Harrington et al, 2010;Quesada-Hernández et al, 2010;Zhang et al, 2008). In zebrafish, cell-labeling and cell-tracking experiments have elucidated the spatiotemporal patterns of cell movement and cell division in the blastula, gastrula and early tailbud (Kanki and Ho, 1997;Keller et al, 2008;Olivier et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Regulated tissue fluidity steers zebrafish body elongation

et al. 2013

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SUMMARYThe tailbud is the posterior leading edge of the growing vertebrate embryo and consists of motile progenitors of the axial skeleton, musculature and spinal cord. We measure the 3D cell flow field of the zebrafish tailbud and identify changes in tissue fluidity revealed by reductions in the coherence of cell motion without alteration of cell velocities. We find a directed posterior flow wherein the polarization between individual cell motion is high, reflecting ordered collective migration. At the posterior tip of the tailbud, this flow makes sharp bilateral turns facilitated by extensive cell mixing due to increased directional variability of individual cell motions. Inhibition of Wnt or Fgf signaling or cadherin 2 function reduces the coherence of the flow but has different consequences for trunk and tail extension. Modeling and additional data analyses suggest that the balance between the coherence and rate of cell flow determines whether body elongation is linear or whether congestion forms within the flow and the body axis becomes contorted.

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Stereotypical Cell Division Orientation Controls Neural Rod Midline Formation in Zebrafish

Cited by 91 publications

References 28 publications

New insights from a high-resolution look at gastrulation in the sea urchin, Lytechinus variegatus

New insights from a high-resolution look at gastrulation in the sea urchin, Lytechinus variegatus

The neural crest cell cycle is related to phases of migration in the head

Regulated tissue fluidity steers zebrafish body elongation

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