The HMG-box protein Lilliputian is required for Runt-dependent activation of the pair-rule gene fushi–tarazu

Transcriptional control during early Drosophila development is governed by maternal and zygotic factors. We have identified a novel maternal transcriptional regulator gene, lilliputian (lilli), which contains an HMG1 (AT-hook) motif and a domain with similarity to the human fragile X mental retardation FMR2 protein and the AF4 proto-oncoprotein. Embryos lacking maternal lilli expression show specific defects in the establishment of a functional cytoskeleton during cellularization, and exhibit a pair-rule segmentation phenotype. These mutant phenotypes correlate with markedly reduced expression of the early zygotic genes serendipity alpha, fushi tarazu and huckebein, which are essential for cellularization and embryonic patterning. In addition, loss of lilli in adult photoreceptor and bristle cells results in a significant decrease in cell size. Our results indicate that lilli represents a novel pair-rule gene that acts in cytoskeleton regulation, segmentation and morphogenesis.

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Evolution of neuroblast identity: seven-up and prospero expression reveal homologous and divergent neuroblast fates in Drosophila and Schistocerca

Development ◽

10.1242/dev.121.12.3989 ◽

1995 ◽

Vol 121 (12) ◽

pp. 3989-3996 ◽

Cited By ~ 4

Author(s):

J. Broadus ◽

C.Q. Doe

Keyword(s):

Gene Expression ◽

Central Nervous System ◽

Gene Function ◽

Fushi Tarazu ◽

Pair Rule Gene ◽

Key Features ◽

Insect Central Nervous System ◽

Or Gene ◽

Species Specific ◽

Pair Rule

In the Drosophila CNS, early neuroblast formation and fate are controlled by the pair-rule class of segmentation genes. The distantly related Schistocerca (grasshopper) embryo has a similar arrangement of neuroblasts, despite lack of known pair-rule gene function. Does divergent pair-rule gene function lead to different neuroblast identities, or can different patterning mechanisms produce homologous neuroblasts? We use four molecular markers to compare Drosophila and Schistocerca neuroblast identity: seven-up, prospero, engrailed, and fushi-tarazu/Dax. In both insects some early-forming neuroblasts share key features of neuroblast identity (position, time of formation, and temporally accurate gene expression); thus, different patterning mechanisms can generate similar neuroblast fates. In contrast, several later-forming neuroblasts show species-specific differences in position and/or gene expression; these neuroblast identities seem to have diverged, suggesting that evolution of the insect central nervous system can occur through changes in embryonic neuroblast identity.

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Ftz-F1 is a cofactor in Ftz activation of the Drosophila engrailed gene

Development ◽

10.1242/dev.124.4.839 ◽

1997 ◽

Vol 124 (4) ◽

pp. 839-847 ◽

Cited By ~ 6

Author(s):

B. Florence ◽

A. Guichet ◽

A. Ephrussi ◽

A. Laughon

Keyword(s):

Transcriptional Activation ◽

Binding Sites ◽

Direct Contact ◽

Regulatory Element ◽

Drosophila Embryo ◽

Homeodomain Protein ◽

Reporter Expression ◽

Fushi Tarazu ◽

Pair Rule Gene ◽

Pair Rule

The fushi tarazu pair-rule gene is required for the formation of alternating parasegmental boundaries in the Drosophila embryo. fushi tarazu encodes a homeodomain protein necessary for transcription of the engrailed gene in even-numbered parasegments. Here we report that, within an engrailed enhancer, adjacent and conserved binding sites for the Fushi tarazu protein and a cofactor are each necessary, and together sufficient, for transcriptional activation. Footprinting shows that the cofactor site can be bound specifically by Ftz-F1, a member of the nuclear receptor superfamily. Ftz-F1 and the Fushi tarazu homeodomain bind the sites with 4- to 8-fold cooperativity, suggesting that direct contact between the two proteins may contribute to target recognition. Even parasegmental reporter expression is dependent on Fushi tarazu and maternal Ftz-F1, suggesting that these two proteins are indeed the factors that act upon the two sites in embryos. The two adjacent binding sites are also required for continued activity of the engrailed enhancer after Fushi tarazu protein is no longer detectable, including the period when engrailed, and the enhancer, become dependent upon wingless. We also report the existence of a separate negative regulatory element that apparently responds to odd-skipped.

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Pair-rule expression of the Drosophila fushi tarazu gene: a nuclear receptor response element mediates the opposing regulatory effects of runt and hairy

Development ◽

10.1242/dev.121.2.453 ◽

1995 ◽

Vol 121 (2) ◽

pp. 453-462 ◽

Cited By ~ 2

Author(s):

C. Tsai ◽

P. Gergen

Keyword(s):

Nuclear Receptor ◽

Transcriptional Activation ◽

Reporter Genes ◽

Orphan Nuclear Receptor ◽

Fushi Tarazu ◽

Pair Rule Gene ◽

Dna Elements ◽

Regulatory Effects ◽

Opposing Effects ◽

Pair Rule

The segmentation genes runt and hairy are required for the proper transcriptional regulation of the pair-rule gene fushi tarazu during the blastoderm stage of Drosophila embryogenesis. The expression of different fushi tarazu reporter genes was examined in runt and hairy mutant embryos, as well as in runt over-expressing embryos in order to identify DNA elements responsible for mediating these regulatory effects. The results indicated that runt and hairy act through a common 32 base-pair element. This element, designated as fDE1, contains a binding site for a small family of orphan nuclear receptor proteins that are uniformly expressed in blastoderm embryos. The pair-rule expression of reporter gene constructs containing multimerized fDE1 elements depends on activation by runt and repression by hairy. Examination of reporter genes with mutated fDE1 elements provided further evidence that this element mediates both transcriptional activation and repression. Genetic experiments indicated that the opposing effects of runt and hairy were not due solely to cross-regulatory interactions between these two genes and that fDE1-dependent expression is regulated by factors in addition to runt and hairy.

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Faculty Opinions recommendation of Odd-paired controls frequency doubling in Drosophila segmentation by altering the pair-rule gene regulatory network.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.726638482.793522390 ◽

2016 ◽

Author(s):

Siegfried Roth

Keyword(s):

Gene Regulatory Network ◽

Regulatory Network ◽

Frequency Doubling ◽

Pair Rule Gene ◽

Gene Regulatory ◽

Pair Rule

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odd Oz: A novel Drosophila pair rule gene

Cell ◽

10.1016/0092-8674(94)90220-8 ◽

1994 ◽

Vol 77 (4) ◽

pp. 587-598 ◽

Cited By ~ 105

Author(s):

Anna Levine ◽

Ayelet Bashan-Ahrend ◽

Ofra Budai-Hadrian ◽

Devorah Gartenberg ◽

Sophia Menasherow ◽

...

Keyword(s):

Pair Rule Gene ◽

Pair Rule

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Teneurin-1, a vertebrate homologue of the Drosophila pair-rule gene ten-m, is a neuronal protein with a novel type of heparin-binding domain

Journal of Cell Science ◽

10.1242/jcs.112.12.2019 ◽

1999 ◽

Vol 112 (12) ◽

pp. 2019-2032 ◽

Cited By ~ 7

Author(s):

A.D. Minet ◽

B.P. Rubin ◽

R.P. Tucker ◽

S. Baumgartner ◽

R. Chiquet-Ehrismann

Keyword(s):

Sequence Motifs ◽

Heparin Binding ◽

Terminal Part ◽

Phylogenetic Conservation ◽

Neuronal Protein ◽

Repeat Proteins ◽

Heparin Binding Domain ◽

Pair Rule Gene ◽

Pair Rule

The Drosophila gene ten-m is the first pair-rule gene not encoding a transcription factor, but an extracellular protein. We have characterized a highly conserved chicken homologue that we call teneurin-1. The C-terminal part harbors 26 repetitive sequence motifs termed YD-repeats. The YD-repeats are most similar to the core of the rhs elements of Escherichia coli. Related repeats in toxin A of Clostridium difficile are known to bind specific carbohydrates. We show that recombinantly expressed proteins containing the YD-repeats of teneurin-1 bind to heparin. Furthermore, heparin lyase treatment of extracts of cells expressing recombinant YD-repeat protein releases this protein from high molecular mass aggregates. In situ hybridization and immunostaining reveals teneurin-1 expression in neurons of the developing visual system of chicken and Drosophila. This phylogenetic conservation of neuronal expression from flies to birds implies fundamental roles for teneurin-1 in neurogenesis. This is supported by the neurite outgrowth occurring on substrates made of recombinant YD-repeat proteins, which can be inhibited by heparin. Database searches resulted in the identification of ESTs encoding at least three further members of the teneurin family of proteins. Furthermore, the human teneurin-1 gene could be identified on chromosome Xq24/25, a region implied in an X-linked mental retardation syndrome.

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Analysis of function of the pair-rule genes hairy, even-skipped and fushi tarazu in mosaic Drosophila embryos

Development ◽

10.1242/dev.107.4.847 ◽

1989 ◽

Vol 107 (4) ◽

pp. 847-853 ◽

Cited By ~ 1

Author(s):

P.A. Lawrence ◽

P. Johnston

Keyword(s):

Genetic Interactions ◽

Nuclear Transplantation ◽

Fushi Tarazu ◽

Segmentation Gene ◽

Hairy Cells ◽

Analysis Of Function ◽

Mutant Cells ◽

Pair Rule ◽

Drosophila Embryos

We report the first attempt of its kind to study genetic interactions using young Drosophila embryos that are mosaic for wildtype and mutant cells. Using nuclear transplantation we make mosaic embryos in which a patch of cells lacks a particular segmentation gene, A. With antibodies, we than look at the expression of another gene that is known to be downstream of gene A, with respect to the cells in the patch. We have examples of patches of hairy cells (where we monitor the effect on fushi tarazu (ftz) expression), even-skipped (monitoring ftz) and ftz (monitoring engrailed and Ultrabithorax). Our main finding is that the dependence of engrailed expression on the ftz gene is strictly cell-autonomous. This result goes some way towards explaining the dependence of Ultrabithorax expression on ftz, a dependence we show to be locally cell-autonomous within parts of parasegments 6 and 8 but non autonomous within parasegment 7.

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Tc-knirps plays different roles in the specification of antennal and mandibular parasegment boundaries and is regulated by a pair-rule gene in the beetle Tribolium castaneum

BMC Developmental Biology ◽

10.1186/1471-213x-13-25 ◽

2013 ◽

Vol 13 (1) ◽

pp. 25 ◽

Cited By ~ 7

Author(s):

Andrew D Peel ◽

Julia Schanda ◽

Daniela Grossmann ◽

Frank Ruge ◽

Georg Oberhofer ◽

...

Keyword(s):

Tribolium Castaneum ◽

Pair Rule Gene ◽

Pair Rule

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Unipolar distributions of junctional Myosin II identify cell stripe boundaries that drive cell intercalation throughout Drosophila axis extension

eLife ◽

10.7554/elife.12094 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 55

Author(s):

Robert J Tetley ◽

Guy B Blanchard ◽

Alexander G Fletcher ◽

Richard J Adams ◽

Bénédicte Sanson

Keyword(s):

Myosin Ii ◽

Interaction Model ◽

Cell Interaction ◽

Cell Number ◽

Cell Polarization ◽

Convergence And Extension ◽

Pair Rule Gene ◽

Cell Intercalation ◽

Pair Rule ◽

Cell Cell

Convergence and extension movements elongate tissues during development. Drosophila germ-band extension (GBE) is one example, which requires active cell rearrangements driven by Myosin II planar polarisation. Here, we develop novel computational methods to analyse the spatiotemporal dynamics of Myosin II during GBE, at the scale of the tissue. We show that initial Myosin II bipolar cell polarization gives way to unipolar enrichment at parasegmental boundaries and two further boundaries within each parasegment, concomitant with a doubling of cell number as the tissue elongates. These boundaries are the primary sites of cell intercalation, behaving as mechanical barriers and providing a mechanism for how cells remain ordered during GBE. Enrichment at parasegment boundaries during GBE is independent of Wingless signaling, suggesting pair-rule gene control. Our results are consistent with recent work showing that a combinatorial code of Toll-like receptors downstream of pair-rule genes contributes to Myosin II polarization via local cell-cell interactions. We propose an updated cell-cell interaction model for Myosin II polarization that we tested in a vertex-based simulation.

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