Dpp and Hh signaling in the Drosophila embryonic eye field

Development ◽  
2001 ◽  
Vol 128 (23) ◽  
pp. 4691-4704 ◽  
Author(s):  
Ting Chang ◽  
Julie Mazotta ◽  
Karin Dumstrei ◽  
Andra Dumitrescu ◽  
Volker Hartenstein
Keyword(s):  
Optic Lobe ◽  
Drosophila Embryo ◽  
Signal Loss ◽  
Fate Map ◽  
Dorsal Midline ◽  
Eyes Absent ◽  
Sine Oculis ◽  
Eye Field ◽  
Hh Signaling ◽  
Hypomorphic Alleles

We have analyzed the function of the Decapentaplegic (Dpp) and Hedgehog (Hh) signaling pathways in partitioning the dorsal head neurectoderm of the Drosophila embryo. This region, referred to as the anterior brain/eye anlage, gives rise to both the visual system and the protocerebrum. The anlage splits up into three main domains: the head midline ectoderm, protocerebral neurectoderm and visual primordium. Similar to their vertebrate counterparts, Hh and Dpp play an important role in the partitioning of the anterior brain/eye anlage. Dpp is secreted in the dorsal midline of the head. Lowering Dpp levels (in dpp heterozygotes or hypomorphic alleles) results in a ‘cyclops’ phenotype, where mid-dorsal head epidermis is transformed into dorsolateral structures, i.e. eye/optic lobe tissue, which causes a continuous visual primordium across the dorsal midline. Absence of Dpp results in the transformation of both dorsomedial and dorsolateral structures into brain neuroblasts. Regulatory genes that are required for eye/optic lobe fate, including sine oculis (so) and eyes absent (eya), are turned on in their respective domains by Dpp. The gene zerknuellt (zen), which is expressed in response to peak levels of Dpp in the dorsal midline, secondarily represses so and eya in the dorsomedial domain. Hh and its receptor/inhibitor, Patched (Ptc), are expressed in a transverse stripe along the posterior boundary of the eye field. As reported previously, Hh triggers the expression of determinants for larval eye (atonal) and adult eye (eyeless) in those cells of the eye field that are close to the Hh source. Eya and So, which are induced by Dpp, are epistatic to the Hh signal. Loss of Ptc, as well as overexpression of Hh, results in the ectopic induction of larval eye tissue in the dorsal midline (cyclopia). We discuss the similarities between vertebrate systems and Drosophila with regard to the fate map of the anterior brain/eye anlage, and its partitioning by Dpp and Hh signaling.

The control of cell fate in the embryonic visual system by atonal, tailless and EGFR signaling

Development ◽  
1999 ◽  
Vol 126 (13) ◽  
pp. 2945-2954 ◽  
Author(s):  
A. Daniel ◽  
K. Dumstrei ◽  
J.A. Lengyel ◽  
V. Hartenstein
Keyword(s):  
Visual System ◽  
Cell Fate ◽  
Optic Lobe ◽  
Egfr Signaling ◽  
Phenotypic Analysis ◽  
Eyes Absent ◽  
Sine Oculis ◽  
Bolwig's Organ ◽  
Encoding Genes

We describe here the role of the transcription factors encoding genes tailless (tll), atonal (ato), sine oculis (so), eyeless (ey) and eyes absent (eya), and EGFR signaling in establishing the Drosophila embryonic visual system. The embryonic visual system consists of the optic lobe primordium, which, during later larval life, develops into the prominent optic lobe neuropiles, and the larval photoreceptor (Bolwig's organ). Both structures derive from a neurectodermal placode in the embryonic head. Expression of tll is normally confined to the optic lobe primordium, whereas ato appears in a subset of Bolwig's organ cells that we call Bolwig's organ founders. Phenotypic analysis, using specific markers for Bolwig's organ and the optic lobe, of tll loss- and gain-of-function mutant embryos reveals that tll functions to drive cells to optic lobe as opposed to Bolwig's organ fate. Similar experiments indicate that ato has the opposite effect, namely driving cells to a Bolwig's organ fate. Since we can show that tll and ato do not regulate each other, we propose a model wherein tll expression restricts the ability of cells to respond to signaling arising from ato-expressing Bolwig's organ pioneers. Our data further suggest that the Bolwig's organ founder cells produce Spitz (the Drosophila TGFalpha homolog) signal, which is passed to the neighboring secondary Bolwig's organ cells where it activates the EGFR signaling cascade and maintains the fate of these secondary cells. The regulators of tll expression in the embryonic visual system remain elusive, as we were unable to find evidence for regulation by the ‘early eye genes’ so, eya and ey, or by EGFR signaling.

Competition and position-dependent targeting in the development of the Drosophila R7 visual projections

Development ◽  
1994 ◽  
Vol 120 (6) ◽  
pp. 1537-1547 ◽  
Author(s):  
J.A. Ashley ◽  
F.N. Katz
Keyword(s):  
Genetic Model ◽  
Competitive Interactions ◽  
Sine Oculis ◽  
Functional Connections ◽  
Eye Field ◽  
Target Regulation ◽  
Set Up ◽  
Molecular Bases ◽  
The Brain ◽  
Retinotopic Map

The R7 photoreceptor neuron projections form a retinotopic map in the medulla of the Drosophila optic lobe. The more inner photoreceptors mutation, an allele of gap1, results in the differentiation of excess R7s in the eye, whose axons invade the brain and establish functional connections. We have used this hyperinnervation phenotype to explore the roles of photoreceptor-target regulation, competitive interactions, and chemoaffinity in map formation. We show that the extra axons are supported in a wild-type brain, with all R7s from a single ommatidium sharing a single termination site, and thus there is no evidence that the target regulates the size of the presynaptic population. In mosaic eyes, in which ommatidia containing extra R7s are surrounded by ommatidia lacking all R7 cells, R7 axons still target to appropriate retinotopic locations in a largely empty R7 terminal field. Axons at the edges of the projection, however, send collaterals into vacant areas of the field, suggesting they are normally restrained to share single termination sites by competitive interactions. In contrast, no sprouts are seen when the vacant sites are juxtaposed with singly innervated sites. In the third instar, R7 and R8 axons transiently display halos of filopodia that overlap adjacent terminals and provide a means to assess occupancy at adjacent sites. Finally, in sine oculis larvae in which only a small number of ommatidia develop, the R7/R8 axons target to predicted dorsoventral portions of the medulla despite the absence of their neighbors, suggesting that position in the eye field determines their connectivity in the brain. We suggest that the mechanisms used to set up this insect map are formally similar to strategies used by vertebrates. The availability of a genetic model for these events should facilitate studies aimed at understanding the molecular bases of retinotopic map development.

scholarly journals Identification of novel direct targets of Drosophila Sine oculis and Eyes absent by integration of genome-wide data sets

2016 ◽  
Vol 415 (1) ◽  
pp. 157-167 ◽  
Author(s):  
Meng Jin ◽  
Sara Aibar ◽  
Zhongqi Ge ◽  
Rui Chen ◽  
Stein Aerts ◽  
...  
Keyword(s):  
Data Sets ◽  
Eyes Absent ◽  
Sine Oculis ◽  
Genome Wide ◽  
Genome Wide Data

scholarly journals Order and coherence in the fate map of the zebrafish nervous system

Development ◽  
1995 ◽  
Vol 121 (8) ◽  
pp. 2595-2609 ◽  
Author(s):  
K. Woo ◽  
S.E. Fraser
Keyword(s):  
Nervous System ◽  
Neural Development ◽  
Expression Patterns ◽  
Time Lapse ◽  
Cellular Interactions ◽  
Fate Map ◽  
Dorsal Midline ◽  
Vertebrate Model ◽  
The Central Nervous System ◽  
Mutant Phenotypes

The zebrafish is an excellent vertebrate model for the study of the cellular interactions underlying the patterning and the morphogenesis of the nervous system. Here, we report regional fate maps of the zebrafish anterior nervous system at two key stages of neural development: the beginning (6 hours) and the end (10 hours) of gastrulation. Early in gastrulation, we find that the presumptive neurectoderm displays a predictable organization that reflects the future anteroposterior and dorsoventral order of the central nervous system. The precursors of the major brain subdivisions (forebrain, midbrain, hindbrain, neural retina) occupy discernible, though overlapping, domains within the dorsal blastoderm at 6 hours. As gastrulation proceeds, these domains are rearranged such that the basic order of the neural tube is evident at 10 hours. Furthermore, the anteroposterior and dorsoventral order of the progenitors is refined and becomes aligned with the primary axes of the embryo. Time-lapse video microscopy shows that the rearrangement of blastoderm cells during gastrulation is highly ordered. Cells near the dorsal midline at 6 hours, primarily forebrain progenitors, display anterior-directed migration. Cells more laterally positioned, corresponding to midbrain and hindbrain progenitors, converge at the midline prior to anteriorward migration. These results demonstrate a predictable order in the presumptive neurectoderm, suggesting that patterning interactions may be well underway by early gastrulation. The fate maps provide the basis for further analyses of the specification, induction and patterning of the anterior nervous system, as well as for the interpretation of mutant phenotypes and gene-expression patterns.

scholarly journals Transcriptional regulation of atonal required for Drosophila larval eye development by concerted action of eyes absent, sine oculis and hedgehog signaling independent of fused kinase and cubitus interruptus

Development ◽  
2000 ◽  
Vol 127 (7) ◽  
pp. 1531-1540 ◽  
Author(s):  
T. Suzuki ◽  
K. Saigo
Keyword(s):  
Hedgehog Signaling ◽  
Specific Antigen ◽  
Photoreceptor Cells ◽  
Organ Development ◽  
Cubitus Interruptus ◽  
Eyes Absent ◽  
Organ Formation ◽  
Sine Oculis ◽  
Founder Cells ◽  
Bolwig's Organ

Bolwig's organ is the larval light-sensing system consisting of 12 photoreceptors and its development requires atonal activity. Here, we showed that Bolwig's organ formation and atonal expression are controlled by the concerted function of hedgehog, eyes absent and sine oculis. Bolwig's organ primordium was first detected as a cluster of about 14 Atonal-positive cells at the posterior edge of the ocular segment in embryos and hence, atonal expression may define the region from which a few Atonal-positive founder cells (future primary photoreceptor cells) are generated by lateral specification. In Bolwig's organ development, neural differentiation precedes photoreceptor specification, since Elav, a neuron-specific antigen, whose expression is under the control of atonal, is expressed in virtually all early-Atonal-positive cells prior to the establishment of founder cells. Neither Atonal expression nor Bolwig's organ formation occurred in the absence of hedgehog, eyes absent or sine oculis activity. Genetic and histochemical analyses indicated that (1) responsible Hedgehog signals derive from the ocular segment, (2) Eyes absent and Sine oculis act downstream of or in parallel with Hedgehog signaling and (3) the Hedgehog signaling pathway required for Bolwig's organ development is a new type and lacks Fused kinase and Cubitus interruptus as downstream components.

scholarly journals Expression of wingless in the Drosophila embryo: a conserved cis-acting element lacking conserved Ci-binding sites is required for patched-mediated repression

Development ◽  
1998 ◽  
Vol 125 (8) ◽  
pp. 1469-1476 ◽  
Author(s):  
D. Lessing ◽  
R. Nusse
Keyword(s):  
Binding Sites ◽  
Transmembrane Protein ◽  
Cell Communication ◽  
Signal Transduction Pathway ◽  
Transcription Unit ◽  
Drosophila Virilis ◽  
Negative Regulator ◽  
Drosophila Embryo ◽  
Cis Acting ◽  
Hh Signaling

Patterning of the Drosophila embryo depends on the accurate expression of wingless (wg), which encodes a secreted signal required for segmentation and many other processes. Early expression of wg is regulated by the nuclear proteins of the gap and pair-rule gene classes but, after gastrulation, wg transcription is also dependent on cell-cell communication. Signaling to the Wg-producing cells is mediated by the secreted protein, Hedgehog (Hh), and by Cubitus interruptus (Ci), a transcriptional effector of the Hh signal transduction pathway. The transmembrane protein Patched (Ptc) acts as a negative regulator of wg expression; ptc- embryos have ectopic wg expression. According to the current models, Ptc is a receptor for Hh. The default activity of Ptc is to inhibit Ci function; when Ptc binds Hh, this inhibition is released and Ci can control wg transcription. We have investigated cis-acting sequences that regulate wg during the time that wg expression depends on Hh signaling. We show that approximately 4.5 kb immediately upstream of the wg transcription unit can direct expression of the reporter gene lacZ in domains similar to the normal wg pattern in the embryonic ectoderm. Expression of this reporter construct expands in ptc mutants and responds to hh activity. Within this 4.5 kb, a 150 bp element, highly conserved between D. melanogaster and Drosophila virilis, is required to spatially restrict wg transcription. Activity of this element depends on ptc, but it contains no consensus Ci-binding sites. The discovery of an element that is likely to bind a transcriptional repressor was unexpected, since the prevailing model suggests that wg expression is principally controlled by Hh signaling acting through the Ci activator. We show that wg regulatory DNA can drive lacZ in a proper wg-like pattern without any conserved Ci-binding sites and suggest that Ci can not be the sole endpoint of the Hh pathway.

Spatial and temporal expression pattern during sea urchin embryogenesis of a gene coding for a protease homologous to the human protein BMP-1 and to the product of the Drosophila dorsal-ventral patterning gene tolloid

Development ◽  
1992 ◽  
Vol 114 (1) ◽  
pp. 147-163 ◽  
Author(s):  
T. Lepage ◽  
C. Ghiglione ◽  
C. Gache
Keyword(s):  
Sea Urchin ◽  
Catalytic Domain ◽  
Intracellular Localization ◽  
Regulation Of Gene Expression ◽  
Drosophila Embryo ◽  
Limited Area ◽  
Fate Map ◽  
Blastula Stage ◽  
Cell Stage ◽  
Short Period

A cDNA clone coding for a sea urchin embryonic protein was isolated from a prehatching blastula lambda gt11 library. The predicted translation product is a secreted 64 × 10(3) Mr enzyme designated as BP10. The protein contains several domains: a signal peptide, a putative propeptide, a catalytic domain with an active center typical of a Zn(2+)-metalloprotease, an EGF-like domain and two internal repeats similar to repeated domains found in the C1s and C1r serine proteases of the complement cascade. The BP10 protease is constructed with the same domains as the human bone morphogenetic protein BMP-1, a protease described as a factor involved in bone formation, and as the recently characterized product of the tolloid gene which is required for correct dorsal-ventral patterning of the Drosophila embryo. The transcription of the BP10 gene is transiently activated around the 16- to 32-cell stage and the accumulation of BP10 transcripts is limited to a short period at the blastula stage. By in situ hybridization with digoxygenin-labelled RNA probes, the BP10 transcripts were only detected in a limited area of the blastula, showing that the transcription of the BP10 gene is also spatially controlled. Antibodies directed against a fusion protein were used to detect the BP10 protein in embryonic extracts. The protein is first detected in early blastula stages, its level peaks in late cleavage, declines abruptly before ingression of primary mesenchyme cells and remains constant in late development. The distribution of the BP10 protein during its synthesis and secretion was analysed by immunostaining blastula-stage embryos. The intracellular localization of the BP10 staining varies with time. The protein is first detected in a perinuclear region, then in an apical and submembranous position just before its secretion into the perivitelline space. The protein is synthesized in a sharply delimited continuous territory spanning about 70% of the blastula. Comparison of the size and orientation of the labelled territory in the late blastula with the fate map of the blastula stage embryo shows that the domain in which the BP10 gene is expressed corresponds to the presumptive ectoderm. Developing embryos treated with purified antibodies against the BP10 protein and with synthetic peptides derived from the EGF-like domain displayed perturbations in morphogenesis and were radialized to various degrees. These results are consistent with a role for BP10 in the differentiation of ectodermal lineages and subsequent patterning of the embryo. On the basis of these results, we speculate that the role of BP10 in the sea urchin embryo might be similar to that of tolloid in Drosophila. We discuss the idea that the processes of spatial regulation of gene expression along the animal-vegetal in sea urchin and dorsal-ventral axes in Drosophila might have some similarities and might use common elements.

Hierarchy of the genetic interactions that specify the anteroposterior segmentation pattern of the Drosophila embryo as monitored by caudal protein expression

Development ◽  
1987 ◽  
Vol 101 (3) ◽  
pp. 421-435 ◽  
Author(s):  
M. Mlodzik ◽  
W.J. Gehring
Keyword(s):  
Protein Product ◽  
The Body ◽  
Drosophila Embryo ◽  
Fate Map ◽  
Gradient Distribution ◽  
Segmentation Genes ◽  
Anteroposterior Axis ◽  
Segmentation Pattern ◽  
Maternal Determinants ◽  
Homeotic Selector

The establishment of the body pattern of Drosophila along the anteroposterior axis requires the coordinated functions of at least three classes of genes. First, the maternally active coordinate genes define the polarity of the embryo and act as primary determinants; second, the segmentation genes divide the developing embryo into the correct number of segments and third, the segments become specified by the homeotic selector genes. We have examined the effects of mutations in the genes of the first two classes on the spatial distribution of the protein product(s) of the caudal (cad) gene, which in wild type shows a graded distribution along the anteroposterior axis during the syncytial blastoderm stage, whereas its persistent zygotic expression is confined to the telson region (the posterior terminal structures). Mutations in maternal genes that specify the spatial coordinates of the egg and the future embryo change the gradient distribution of cad according to the alterations of the fate map which they produce. A second group of maternally expressed genes, the gap genes of the ‘grandchildless-knirps’ group, which are considered to represent posterior activities, do not have any effect on the cad gradient. The same is true for the zygotic segmentation genes that are active after fertilization. However, the same class of zygotic genes partly affects the zygotic cad expression in the telson. Therefore, the two phases of cad expression represent different levels within the genetic hierarchy. The cad protein gradient seems to form in response to the primary maternal determinants independent of the segmentation genes, whereas the latter influence zygotic cad expression in the telson region which corresponds to a homeotic selector gene function.

Signaling by the TGF-beta homolog decapentaplegic functions reiteratively within the network of genes controlling retinal cell fate determination in Drosophila

Development ◽  
1999 ◽  
Vol 126 (5) ◽  
pp. 935-943 ◽  
Author(s):  
R. Chen ◽  
G. Halder ◽  
Z. Zhang ◽  
G. Mardon
Keyword(s):  
Cell Fate ◽  
Retinal Cell ◽  
Cell Fate Determination ◽  
Tgf Beta ◽  
Eyes Absent ◽  
Fate Determination ◽  
Sine Oculis ◽  
Retinal Determination ◽  
Interactive Network ◽  
Distinct Cell

Retinal cell fate determination in Drosophila is controlled by an interactive network of genes, including eyeless, eyes absent, sine oculis and dachshund. We have investigated the role of the TGF-beta homolog decapentaplegic in this pathway. We demonstrate that, during eye development, while eyeless transcription does not depend on decapentaplegic activity, the expression of eyes absent, sine oculis and dachshund are greatly reduced in a decapentaplegic mutant background. We also show that decapentaplegic signaling acts synergistically with and at multiple levels of the retinal determination network to induce eyes absent, sine oculis and dachshund expression and ectopic eye formation. These results suggest a mechanism by which a general patterning signal such as Decapentaplegic cooperates reiteratively with tissue-specific factors to determine distinct cell fates during development.

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