Patterns of cell division and interkinetic nuclear migration in the chick embryo hindbrain

Abstract

Early in its development, the chick embryo hindbrain manifests an axial series of bulges, termed rhombomeres. Rhombomeres are units of cell lineage restriction, and both they and their intervening boundaries form a series that reiterates various features of neuronal differentiation, cytoarchitecture, and molecular character. The segmented nature of hindbrain morphology and cellular development may be related to early patterns of cell division. These were explored by labeling with BrdU to reveal S-phase nuclei, and staining with basic fuchsin to visualise mitotic cells. Whereas within rhombomeres, S-phase nuclei were located predominantly toward the pial surface of the neuroepithelium, at rhombomere boundaries S-phase nuclei were significantly closer to the ventricular surface. The density of mitotic figures was greater toward the centres of rhombomeres than in boundary regions. Mitotic cells did not show any consistent bias in the orientation of division, either in the centres of rhombomeres, or near boundaries. Our results are consistent with the idea that rhombomeres are centres of cell proliferation, while boundaries contain populations of relatively static cells with reduced rates of cell division.

A New Role of Hindbrain Boundaries as Pools of Neural Stem/Progenitor Cells Regulated by Sox2

“…2 and 3; Additional file 1) [15,34,43,72,73]. Notably, DAPI-negative gaps are present in the mantle-most layer of boundaries, which reflect nuclei-free domains (Additional file 1), consistent with previously published data [14][15][16]. At st.15, Sox2 expression is detected in both rhombomeres and boundaries ( Fig.…”

“…Noticeably, the data obtained from the sections (Fig. 1B) and the confocal analysis of whole hindbrain cells (Additional file 1) shows no larger amount of cells in the boundaries compared to rhombomeres [14], ruling out the option that the enriched Sox2 expression at HBs of st.18 embryos is due to a general increase in cell density at these sites.…”

“…Individual rhombomeres are separated from their neighbors by well-defined boundaries. Contrary to rhombomeres, hindbrain boundaries (HBs) share the same molecular and cellular characteristics along the hindbrain, such as a unique fan-shaped morphology, enriched extracellular matrix (ECM), slow proliferation rate, and reduced interkinetic nuclear cell migration [5,7,[13][14][15][16][17][18][19]. Although HBs were identified decades ago, their role during hindbrain development remains largely unknown, especially in amniotes.…”

Rhombomere boundaries are Wnt signaling centers that regulate metameric patterning in the zebrafish hindbrain

“…This signaling system establishes zones of mutual exclusion and, thereby, prevents intermixing of cells between even and odd numbered rhombomeres. Successive rhombomeres are also separated by boundary regions showing distinctive cellular morphology and localized expression of boundaryspecific genes (Trevarrow et al, 1990;Guthrie et al, 1991;Heyman et al, 1993Heyman et al, , 1995Mahmood et al, 1995Mahmood et al, , 1996Moens et al, 1996;Yoshida and Colman, 2000). Although it has been argued that rhombomere boundaries serve as physical barriers to interrhombomeric cell migration, environmental factors and mutations that specifically ablate rhombomere boundaries do not lead to increased segmental intermixing (Nittenberg et al, 1997;White et al, 2000).…”

Btg1 and Btg2 gene expression during early chick development

“…Additionally, Btg2 was expressed in the inter-rhombomeric boundaries. The population of neuroepithelial cells residing in those boundaries has distinct properties and exhibit reduced rates of cell proliferation (Guthrie et al, 1991). The fact that Btg2 protein has antiploriferative functions suggests that it may be one of the molecules controlling the rate of cell proliferation in these cells.…”