DOI: 10.1242/dev.113.4.1133. Establishment of rostrocaudal polarity in tectal primordium: <i>engrailed</i> expression and subsequent tectal polarity

Establishment of rostrocaudal polarity in tectal primordium: engrailed expression and subsequent tectal polarity

10.1242/dev.113.4.1133

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT In the E4 (embryonic day 4) chick tectal primordium, engrailed expression is strong at the caudal end and gradually weakens toward the rostral end. We used quail-chick chimeric tecta to investigate how the caudorostral gradient of engrailed expression is established and whether it is correlated with the subsequent rostrocaudal polarity of tectal development. To examine the positional value of the tectal primordium, we produced ectopic tecta in the diencephalon by transplanting a part of the mesencephalic alar plate heterotopically. In the ectopic tectum, the gradient of the engrailed expression reversed and the strength of the expression was dependent on the distance from the mes-diencephalon junction; the nearer the ectopic tectum was to the junction, the weaker the expression was. Consequently, the pattern of the engrailed expression in the host and ectopic tecta was nearly a mirror image, suggesting the existence of a repressive influence around the mes-diencephalon junction on the engrailed expression. We examined cytoarchitectonie development in the ectopic tecta, which normally proceeds in a gradient along the rostrocaudal axis; the rostral shows more advanced lamination than the caudal. In contrast, the caudal part of the ectopic tecta (near to the mesdiencephalon junction) showed more advanced lamination than the rostral. In both the host and ectopic tecta, advanced lamination was observed where the engrailed expression was repressed, and vice versa. Next we studied the correlation between engrailed expression and retinotectal projection from a view of plasticity and rigidity of rostrocaudal polarity in the tectum. We produced ectopic tecta by anisochronal transplantations between E3 host and E2 donor, and showed that there is little repressive influence at E3 around the mes-diencephalon junction. We then made chimeric double-rostral tectum (caudal half of it was replaced by rostral half of the donor tectum) or double-caudal tectum at E3. The transplants kept their original staining pattern in hosts. Consequently, the chimeric tecta showed wholly negative or positive staining of engrailed protein on the grafted side. In such tecta retinotectal projection pattern was disturbed as if the transplants retained their original position-specific characters. We propose from these heterotopic and anisochronal experiments that the engrailed expression can be a marker for subsequent rostrocaudal polarity in the tectum, both as regards cytoarchitectonie development and retinotectal projection.

Bibliography

Itasaki, N., Ichijo, H., Hama, C., Matsuno, T., & Nakamura, H. (1991). Establishment of rostrocaudal polarity in tectal primordium: engrailed expression and subsequent tectal polarity. Development, 113(4), 1133â1144.

Authors 5

Nobue Itasaki (first)
Hiroyuki Ichijo (additional)
Chihiro Hama (additional)
Toru Matsuno (additional)
Harukazu Nakamura (additional)

References 28 Referenced 102

10.1016/0012-1606(90)90280-V / Devl Biol / Pluripotentiality of the 2-day-old avian germinative neuroepithelium by Alvarado-Mallart (1990)
10.1016/0012-1606(84)90326-9 / Devl Biol / Homotopic and heterotopic transplantations of quail tectal primordia in chick embryos: Organization of the retinotectal projections in the chimeric embryos by Alvarado-Mallart (1984)
10.1038/258126a0 / Nature / Polarity of structure and of ordered nerve connections in the developing amphibian brain by Chung (1975)
{'key': '2023050315324706500_DEVELOP_113_4_1133C4', 'first-page': '389', 'article-title': 'The development of the retinotectal projection: An overview', 'volume-title': 'Molecular Bases of Neural Development', 'author': 'Cowan', 'year': '1985'} / Molecular Bases of Neural Development / The development of the retinotectal projection: An overview by Cowan (1985)
{'key': '2023050315324706500_DEVELOP_113_4_1133C5', 'first-page': '604', 'article-title': 'Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis', 'volume-title': 'Nature', 'author': 'Dinardo', 'year': '1988'} / Nature / Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis by Dinardo (1988)
{'key': '2023050315324706500_DEVELOP_113_4_1133C6', 'first-page': '426', 'article-title': 'Expression of an engrailed-Mse gene during development of the early embryonic chick nervous system', 'volume-title': 'J. Neurosci. Res', 'author': 'Gardner'} / J. Neurosci. Res / Expression of an engrailed-Mse gene during development of the early embryonic chick nervous system by Gardner
10.1002/jmor.1050880104 / J. Morph / A series of normal stages in the development of the chick embryo by Hamburger (1951)
10.1242/dev.110.2.331 / Development / Rotation of the tectal primordium reveals plasticity of target recognition in retinotectal projection by Ichuo (1990)
10.1126/science.1672471 / Science / Subtle cerebellar phenotype in mice homozygous for a targeted deletion of the En-2 homeobox by Joyner (1991)
10.1016/0006-8993(71)90053-9 / Brain Res / The development of the chick optic tectum. I. Normal morphology and cytoarchitectonie development by LaVail (1971)
10.1016/0012-1606(73)90061-4 / Devl Biol / A biological cell labeling technique and its use in experimental embryology by Le Douarin (1973)
10.1016/0012-1606(90)90312-7 / Devl Biol / Expression of the homeobox chick-en gene in chick/quail chimeras with inverted mes-metencephalic grafts by Martinez (1990)
10.1016/0896-6273(91)90237-T / Neuron / Induction of a mesencephalic phenotype in the 2-day-old chick prosencephalon is preceded by the early expression of the homeobox gene en by Martinez (1991)
10.1242/dev.103.1.157 / Development / Role of segment polarity genes in the definition and maintenance of cel states in the Drosophila embryo by Martinez Arias (1988)
10.1016/0165-3806(91)90014-A / Devl Brain Res / Regulation of the rostrocaudal axis of the optic tectum: histological study after rostrocaudal rotation in quail-chick chimeras by Matsuno (1991)
10.1016/0092-8674(90)90385-R / Cell / The Wnt-1 (inr-1) proto-oncogene is required for development of a large region of the mouse brain by McMahon (1990)
10.1016/0006-8993(90)90231-Y / Brain Res / Do CNS anlagen have plasticity in differentiation? Analysis in quail-chick chimera by Nakamura (1990)
10.1523/JNEUROSCI.09-11-03776.1989 / J. Neurosci / Inaccuracies in initial growth and arborization of chick retinotectal axons followed by course corrections and axon remodeling to develop topographic order by Nakamura (1989)
10.1016/0092-8674(89)90947-1 / Cell / Expression of engrailed proteins in arthropods, annelids, and chordates by Patel (1989)
{'key': '2023050315324706500_DEVELOP_113_4_1133C20', 'first-page': '2723', 'article-title': 'Secreted int-1 protein is associated with the cell surface', 'volume': '10', 'author': 'Papkoff', 'year': '1990', 'journal-title': 'Molec. cell. Biol'} / Molec. cell. Biol / Secreted int-1 protein is associated with the cell surface by Papkoff (1990)
10.1016/0092-8674(87)90038-9 / Cell / The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless by Rusewuk (1987)
10.1016/0165-3806(86)90088-X / Devl Brain Res / Development of the retinotectal system in normal quail embryos: Cytoarchitectonie development and optic fiber innervation by Senut (1986)
10.1016/0165-3806(87)90100-3 / Devl Brain Res / Cytodifferentiation of quail tectal primordium transplanted homotopically into the chick embryo by Senut (1987)
10.1016/0896-6273(90)90227-7 / Neuron / Biochemical characterization of a putative axonal guidance molecule of the chick visual system by Stahl (1990)
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10.1242/dev.101.4.909 / Development / Avoidance of posterior tectal membranes by temporal retinal axons by Walter (1987)
10.1242/dev.101.4.685 / Development / Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro by Walter (1987)
10.1016/0092-8674(87)90664-7 / Cell / Expression of the proto-oncogene int-1 is restricted to specific neural cells in the developing mouse embryo by Wilkinson (1987)

Dates

Type	When
Created	4 years, 4 months ago (April 23, 2021, 2:26 p.m.)
Deposited	2 years, 3 months ago (May 3, 2023, 11:37 a.m.)
Indexed	3 months, 2 weeks ago (May 16, 2025, 7:03 p.m.)
Issued	33 years, 9 months ago (Dec. 1, 1991)
Published	33 years, 9 months ago (Dec. 1, 1991)
Published Online	33 years, 9 months ago (Dec. 1, 1991)
Published Print	33 years, 9 months ago (Dec. 1, 1991)

Funders 0

None

BibTeX

@article{Itasaki_1991, title={Establishment of rostrocaudal polarity in tectal primordium: engrailed expression and subsequent tectal polarity}, volume={113}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.113.4.1133}, DOI={10.1242/dev.113.4.1133}, number={4}, journal={Development}, publisher={The Company of Biologists}, author={Itasaki, Nobue and Ichijo, Hiroyuki and Hama, Chihiro and Matsuno, Toru and Nakamura, Harukazu}, year={1991}, month=dec, pages={1133–1144} }

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