Avian Gastrulation and Neurulation Are Not Impaired by the Removal of the Marginal Zone at the Unincubated Blastoderm Stage

Callebaut, M.; Nueten, Emmy Van; Harrisson, F.; Nassauw, Luc Van; Schrevens, A.; Bortier, Hilde

doi:10.1076/ejom.35.2.69.13065

Cited by 10 publications

(9 citation statements)

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“…In all our experimental studies, we have always observed a strong PS-inducing effect by Rauber's sickle, even in the total absence of the caudal marginal zone (Callebaut et al, 1997). After transplantation of quail caudal marginal zones or upper layer fragments taken from above Rauber's sickle on the cranial quadrants or anti-sickles of whole unincubated chicken blastoderms, we could not observe induction phenomena (Callebaut et al, 1998).…”

Section: Rauber's Sickle and Not The Caudal Marginal Zone Initiates Pmentioning

confidence: 54%

“…The latter is known to induce prosencephalon-like structures (Pera and Kessel, 1997). By interaction with sickle endoblast arising from Rauber's sickle (the early gastrulation organizer: Callebaut and Van Nueten, 1994;Callebaut et al, 1997) or from Hensen's node (a later avian organizer: Waddington, 1932), endophyll orients or re-orients the head region and the caudocranial direction of an induced miniature embryo (Callebaut et al, 1999). Chapman et al (2003) suggest that successive inductive interactions between primary hypoblast, anterior definitive endoderm and epiblast act to promote an anterior character.…”

Section: Endophyllmentioning

confidence: 99%

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Origin, fate, and function of the components of the avian germ disc region and early blastoderm: Role of ooplasmic determinants

Callebaut

2005

Developmental Dynamics

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In the avian oocytal germ disc region, at the end of oogenesis, we discerned four ooplasms (␣, ␤, ␥, ␦) presenting an onion-peel distribution (from peripheral and superficial to central and deep. Their fate was followed during early embryonic development. The most superficial and peripheral ␣ ooplasm plays a fundamental role during cleavage. The ␤ ooplasm, originally localized in the peripheral region of the blastodisc, becomes mainly concentrated in the primitive streak. At the moment of bilateral symmetrization, a spatially oblique, sickle-shaped uptake of ␥ and ␦ ooplasms occurs so that ␥ and ␦ ooplasms become incorporated into the deeper part of the avian blastoderm. These ooplasms seem to contain ooplasmic determinants that initiate either early neurulation or gastrulation events. The early neural plate-inducing structure that forms a deep part of the blastoderm is the ␦ ooplasm-containing endophyll (primary hypoblast). Together with the primordial germ cells, it is derived from the superficial centrocaudal part of the nucleus of Pander, which also contains ␦ ooplasm. The other structure (␥ ooplasm) that is incorporated into the caudolateral deep part of the blastoderm forms Rauber's sickle. It induces gastrulation in the concavity of Rauber's sickle and blood island formation exterior to Rauber's sickle. Rauber's sickle develops by ingrowth of blastodermal cells into the ␥ ooplasm, which surrounds the nucleus of Pander. Rauber's sickle constitutes the primary major organizer of the avian blastoderm and generates only extraembryonic tissues (junctional and sickle endoblast). By imparting positional information, it organizes and dominates the whole blastoderm (controlling gastrulation, neurulation, and coelom and cardiovascular system formation). Fragments of the horns of Rauber's sickle extend far cranially into the lateral quadrants of the unincubated blastoderm, so that often Rauber's sickle material forms three quarters of a circle. This finding explains the regulative capacities of isolated blastoderm parts, with the exception of the anti-sickle region and central blastoderm region, where no Rauber's sickle material is present. In avian blastoderms, there exists a competitive inhibition by Rauber's sickle on the primitive streak and neural plate-inducing effects of sickle endoblast. Avian primordial germ cells contain ␦ ooplasm derived from the superficial part of the nucleus of Pander. Their original deep and central ooplasmic localization has been confirmed by the use of a chicken vasa homologue. We conclude that the unincubated blastoderm consists of three elementary tissues: upper layer mainly containing ␤ ooplasm, endophyll containing ␦ ooplasm, and Rauber's sickle containing ␥ ooplasm). These elementary tissues form before the three classic germ layers have developed.

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Section: Rauber's Sickle and Not The Caudal Marginal Zone Initiates Pmentioning

confidence: 54%

Section: Endophyllmentioning

confidence: 99%

Origin, fate, and function of the components of the avian germ disc region and early blastoderm: Role of ooplasmic determinants

Callebaut

2005

Developmental Dynamics

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“…This inductive capacity exists broadly in the posterior marginal zone at stage X but becomes more restricted to the posterior-most marginal zone by stage XII (Eyal-Giladi and Khaner, 1989;Khaner, 1995). Detailed studies of the posterior marginal zone have mapped its inductive activity to nonepiblast midline cells immediately posterior to Koller's sickle (Bachvarova et al, 1998) rather than cells of the Koller's sickle itself or hypoblast cells as previously thought (Azar and Eyal-Giladi, 1979;Eyal-Giladi et al, 1992Callebaut et al, 1997). These studies indicate that all epiblast cells are competent to respond to the inductive cues provided by the posterior midline cells and can undergo primitive streak formation.…”

Section: Induction Of the Initial Primitive Streakmentioning

confidence: 95%

“…When a segment of the posterior marginal zone of the blastodisc is implanted into an anterolateral marginal zone, an ectopic primitive streak is induced ( Fig. 3A-C; Khaner and Eyal-Giladi, 1986;Izpisua-Belmonte et al, 1993;Callebaut and van Nueten, 1994;Callebaut et al, 1997). This inductive capacity exists broadly in the posterior marginal zone at stage X but becomes more restricted to the posterior-most marginal zone by stage XII (Eyal-Giladi and Khaner, 1989;Khaner, 1995).…”

Section: Induction Of the Initial Primitive Streakmentioning

confidence: 99%

“…The data suggest a potential role of the hypoblast in inhibiting formation of supernumerary streaks. However, the hypoblast-derived inhibitory activity alone may not be sufficient to account for the lateral inhibition, because the posterior marginal zone can induce an ectopic primitive streak where the hypoblast still exists (Khaner and EyalGiladi, 1986;Izpisua-Belmonte et al, 1993;Callebaut and van Nueten, 1994;Callebaut et al, 1997).…”

Section: Induction Of the Initial Primitive Streakmentioning

confidence: 99%

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Induction and patterning of the primitive streak, an organizing center of gastrulation in the amniote

Matsukawa

Poh

Kelly

et al. 2004

Developmental Dynamics

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The primitive streak is the organizing center for amniote gastrulation. It defines the future embryonic midline and serves as a conduit of cell migration for germ layer formation. The migration patterns of endodermal and mesodermal precursors through the streak have been studied in great detail. Additional new breakthroughs recently have revealed the cell biological and molecular mechanisms that govern streak induction and patterning. These findings include (1) identification of the ontogeny and inductive signals of streak precursors, (2) the potential cellular mechanism of streak extension, and (3) the molecular and functional diversification along the anterior-posterior and mediolateral axes within the primitive streak. These findings indicate that amniote embryos initiate gastrulation by using both evolutionarily conserved and divergent mechanisms. The data also provide a foundation for understanding how the midline axis is defined and maintained during gastrulation of the amniotes. Developmental Dynamics 229:422-432, 2004.

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Positional information by rauber's sickle and a new look at the mechanisms of primitive streak initiation in avian blastoderms

Callebaut¹,

Nueten²,

Bortier³

et al. 2003

Journal of Morphology

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The present experimental in vitro study suggests that a primitive streak (PS) in avian blastoderms is induced by diffusion of morphogenetic substances emanating from Rauber's sickle. Indeed, even without direct contact between a quail Rauber's sickle and the reacting upper layer (by interposition of a vitelline membrane), a PS can be induced in the isolated area centralis or antisickle region of unincubated chicken blastoderms. The so-formed PSs are localized below the vitelline membrane in the immediate neighborhood of the apposed Rauber's sickle material. This seems to indicate that Rauber's sickle organizes the formation of the avian PS according to the basic concept of "positional information." The morphogenetic substances seem to have an effect only on the formation of a PS. Each part of Rauber's sickle seems to have, point by point, the same thickening and PS-inducing effect on each corresponding part of the underlying upper layer (UL). By a mechanism of sliding over the basement membrane and fusion, this finally results in the formation of one single median PS. Our study shows that a PS can be induced in the total absence of hypoblast (sickle endoblast) or caudal marginal zone, by only the presence of Rauber's sickle material. In contrast, the differentiation of mesoblast into blood islands under the influence of Rauber's sickle and neural tissue development are impaired by the interposition of a vitelline membrane. The latter could be due to the absence of a normal interaction of Rauber's sickle-derived sickle endoblast with endophyll and/or upper layer and the absence of cranial migration of the mesoblast. Thus, earlier studies and the present study indicate the existence of a temporospatially bound cascade of gastrulation and neurulation phenomena and blood island formation in the avian blastoderm, starting from Rauber's sickle, the primary major organizer with inducing, inhibiting, and dominating potencies. The latter not only plays a role by secretion of signaling molecules, but also influences development by its cell lineages (junctional endoblast and sickle endoblast).

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Avian Gastrulation and Neurulation Are Not Impaired by the Removal of the Marginal Zone at the Unincubated Blastoderm Stage

Cited by 10 publications

References 0 publications

Origin, fate, and function of the components of the avian germ disc region and early blastoderm: Role of ooplasmic determinants

Origin, fate, and function of the components of the avian germ disc region and early blastoderm: Role of ooplasmic determinants

Induction and patterning of the primitive streak, an organizing center of gastrulation in the amniote

Positional information by rauber's sickle and a new look at the mechanisms of primitive streak initiation in avian blastoderms

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