Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein

DiNardo, Stephen

doi:10.1016/0092-8674(85)90012-1

Cited by 396 publications

(196 citation statements)

References 43 publications

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“…But in embryos homozygous for en CXI , striped expression in the ectoderm stops during full germ-band extension (Fig. 2d), a time when en is easily detectable in wild-type embryos 7,14 (Fig. 2b).…”

Section: Requirement For Enmentioning

confidence: 99%

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Multiple modes of engrailed regulation in the progression towards cell fate determination

Heemskerk

DiNardo

Kostriken³

et al. 1991

Nature

246

147

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The engrailed gene product of Drosophila specifies the fate of a subset of cells in each segment. Our studies of engrailed regulation suggest that fate determination is an elaborate, multistep process. At the time in embryogenesis when the engrailed-dependent cell fate is probably determined, four modes of control act in an overlapping progression to govern engrailed expression. After activation by pairrule genes, both an extracellular signal, wingless, and autoregulation are required for engrailed expression. Autoregulation graduates to wingless independence, but is transient, and is superseded by an engrailed-independent mode of maintenance.Two levels of commitment have been defined for the choice of cell fate 1 . Early in development, fate can be instructed by environmental cues. This fate specification is flexible and allows fate to change in response to extracellular signals. But cells can undergo a transition from this type of specification to one which is determined and therefore irreversible. Because a determined cell maintains a particular fate independent of its environment, the transition to a determined state requires that development comes under cell-intrinsic, rather than cell-extrinsic control. The identification of selector genes in Drosophila provides an opportunity to study the basis of both types of cell-fate control. Selector genes encode regulators whose function defines the fate of a cell, and whose continued expression stably maintains cell fate 2,3 . Where the choice of cell fate is initially dependent on the environment, selector gene expression must be sensitive to extracellular signals. By contrast, once cell fate is determined, expression of these genes must be governed exclusively by cell-intrinsic factors.The engrailed (en) gene is a selector gene that distinguishes two populations of cells in each developing embryonic segment, the progenitors of the anterior and posterior compartments 3,4 . This distinction can be seen as a lineage restriction when individual embryonic cells are marked by mitotic recombination 5,6 . These give rise to clonal patches in the adult that never span the boundary between the anterior and posterior compartments, demonstrating that, from the time of marking, the progeny of a given cell only contribute to one compartment. This restriction requires expression of en by posterior cells 3,4,7 . But it seems that the onset of localized en expression in early embryos is not sufficient to irreversibly determine posterior compartment identity because en requires at least one cell-extrinsic input at this time.This input is provided by the wingless (wg) gene, expressed in segmentally repeated stripes of cells that lie next to en-expressing cells 8,9 . The wg protein, which is homologous to the product of the proto-oncogene Wnt-1 ( ref. 10 ), is secreted and appears to be taken up by en-expressing cells 9 . In wg mutant embryos, en expression is initiated in a normal striped pattern but soon stops, indicating that continued en expression in wild-type embryos r...

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Section: Requirement For Enmentioning

confidence: 99%

“…Expression of en becomes wg-independent after 5 h. Embryos are stained with an anti-en antibody 14 . Magnification 140×, anterior is left and ventral is down in all figures except when noted.…”

Section: Figmentioning

confidence: 99%

Multiple modes of engrailed regulation in the progression towards cell fate determination

Heemskerk

DiNardo

Kostriken³

et al. 1991

Nature

246

147

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“…2d, e). As endogenous en expression is established, the odd-numbered stripes initially lag behind the development of even-numbered stripes 10,22 . However, en is equivalently expressed in the oddand even-numbered stripes by the time the germband is elongating (compare panels d and b, Fig.…”

Section: Early Expressionmentioning

confidence: 99%

“…Methods. Preparation of embryos for immunocytochemistry was as in refs 10,12 . Rabbit anti-β-gal was from Cappel, rabbit anti-en, (ref.…”

Section: Separate Regulatory Programmesmentioning

confidence: 99%

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Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis

DiNardo

Sher

Heemskerk-Jongens

et al. 1988

Nature

381

189

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A regulatory cascade, initiated during the syncytial stage of embryogenesis, culminates in the striped pattern of engrailed gene expression at the cellular blastoderm stage. The early regulatory genes, for example the pair-rule genes, are expressed transiently and as their products decay a distinct regulatory programme involving segment polarity genes takes over. This late programme maintains and perhaps modifies the striped pattern of engrailed expression through interactions that may involve cell communication.An early step in the generation of the Drosophila body pattern is the determination of the segmental subdivisions of the embryo. This occurs quite rapidly. By the cellular blastoderm stage (2-2.5 h after fertilization) the segmental outlines of the embryo, although not morphologically visible, are represented by the precise expression patterns of the segmentation (or segment polarity) genes, such as engrailed 1,2 and wingless 3 . The subsequent activity of genes such as these directs the morphological events leading to segmentation 4,5 .The segmentation genes are expressed in their localized patterns as a consequence of an early regulatory cascade. Three gene classes (maternal genes 6 , and the zygotically acting gap and pair-rule genes 4 ) act in sequence, each establishing the more refined spatial expression pattern of the next 7-9 . This takes place in a syncytial cytoplasm and is thought to rely on the diffusion and interaction of regulatory products encoded by these genes. The subdivision of the embryonic field by this cascade is rapid, occurring during the first thirteen nuclear divisions. After the thirteenth division, the nuclei are cellularized and the cellular blastoderm is formed.One outcome of this regulatory hierarchy is the establishment of engrailed (en) expression at the cellular blastoderm stage in 14 single-cell-wide stripes transecting the antero-posterior axis of the embryo 1,2,10,22 . Previous work has shown that the activity of separate sets of pair-rule genes controls establishment of en expression in even-and in odd-numbered stripes 11,12 . The data presented here suggests further that the separate control of even-and odd-numbered stripes is reflected in the organization of the cis-regulatory sequences at en.During the post-cellular blastoderm phase of development the expression pattern of en is maintained and modified 1,10 . It is unlikely that the pair-rule genes are involved in the postblastoderm regulation of en, since the pair-rule genes characterized to date are only expressed transiently in their pair-rule blastoderm patterns [13][14][15][16]31 . Here we address the mechanism by which the en gene is regulated in later embryonic development.

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Engrailed protein is expressed in interneurons but not motor neurons of the dorsal unpaired median group in the adult grasshopper

Siegler

Pankhaniya

1997

J. Comp. Neurol.

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We report that the homeodomain protein Engrailed (En) is differentially expressed by neuronal type. Expression was examined within identified midline neurons in T3, A1, and A2 neuromeres of the adult grasshopper by using immunohistochemistry. All save a few neurons in the adult dorsal unpaired median (DUM) group arise embryonically from a single precursor, the median neuroblast. DUM neurons are efferent neurons, local interneurons, or intersegmental interneurons, recognizable as such by their distinct morphologies and neurotransmitter phenotypes. We show that interneurons are En-positive, whereas efferents are En-negative. In the T3 DUM group, the 70 or so interneurons contained cytoplasmic immunoreactivity for gamma-aminobutyric acid (GABA) and glutamate decarboxylase. In double-labeling experiments, all GABA-immunoreactive neurons were also En-positive, and all En-positive neurons contained GABA immunoreactivity. In complementary experiments, the 20 or so efferents in the T3 DUM group, which are octopaminergic, were selectively labeled with a histological marker and then processed to reveal En immunoreactivity. No efferents in the group were En-positive. The abdominal DUM groups contain fewer neurons, but the same dichotomy of labeling was found. The En pattern is established during embryogenesis, with the type-specific pattern apparent by stage 90% of development, the earliest stage examined here. The differential expression of En in the embryo and its continued expression in the adult nervous system suggest a role in the development and maintenance of neuronal phenotype. Morphological differences between efferents and interneurons are discussed in light of a hypothesis that En mediates differential expression of cell adhesion or cell-affinity molecules.

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Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein

Cited by 396 publications

References 43 publications

Multiple modes of engrailed regulation in the progression towards cell fate determination

Multiple modes of engrailed regulation in the progression towards cell fate determination

Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis

Engrailed protein is expressed in interneurons but not motor neurons of the dorsal unpaired median group in the adult grasshopper

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