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PubMed2005

The role of nutrition in creation of the eye imaginal disc and initiation of metamorphosis in Manduca sexta.

With the exception of the wing imaginal discs, the imaginal discs of Manduca sexta are not formed until early in the final larval instar. An early step in the development of these late-forming imaginal discs from the imaginal primordia appears to be an irreversible commitment to form pupal cuticle at the next molt. Similar to pupal commitment in other tissues at later stages, activation of broad expression is correlated with pupal commitment in the adult eye primordia. Feeding is required during the final larval instar for activation of broad expression in the eye primordia, and dietary sugar is the specific nutritional cue required. Dietary protein is also necessary during this time to initiate the proliferative program and growth of the eye imaginal disc. Although the hemolymph titer of juvenile hormone normally decreases to low levels early in the final larval instar, eye disc development begins even if the juvenile hormone titer is artificially maintained at high levels. Instead, creation of the late-forming imaginal discs in Manduca appears to be controlled by unidentified endocrine factors whose activation is regulated by the nutritional state of the animal.

Animal Nutritional Physiological Phenomena↗

PubMed2000

Cell-cell and cell-substrate adhesion in cultured Drosophila imaginal disc cells.

Drosophila imaginal disc cell lines were used to investigate various aspects of cellular adhesion in vitro. The distribution of PS integrins and their involvement in cell-cell and cell-substrate adhesion were assessed with the monoclonal antibody aBG-1 against the betaPS subunit, and both forms of adhesion were found to be impeded by the presence of the antibody. Adhesion to a number of extracellular matrix components was investigated, and the cells were found to adhere to human fibronectin. This adhesion was inhibited by aBG-1. The adhesion molecule fasciclin III was also found in these cells. Given that the cells are competent to perform cell-cell and cell-substrate adhesion, it was thought that apical basal polarity might be restored when other suitable conditions were provided, i.e., an artificial basement layer with feeder cells to provide nutrients basally to the cells, and some features of apical-basal morphology were seen in cells cultured under these conditions.

Animals↗

PubMed1986

Isolation of genes active during hormone-induced morphogenesis in Drosophila imaginal discs.

Mass-isolated Drosophila imaginal discs cultured in vitro undergo morphogenesis (evagination) in response to the insect steroid hormone 20-hydroxyecdysone. In vitro translation of mRNA isolated from evaginating discs shows accumulation of at least five new mRNA transcripts that are present only in membrane-bound polysomal RNA and presumably encode imaginal disc membrane or secreted proteins. Using a modified differential hybridization screen employing a competition step, six different hormone-inducible membrane protein gene sequences were isolated. These genes constitute a new set of 20-hydroxyecdysone responsive loci that may encode gene products specifically required for imaginal disc morphogenesis.

Animals↗

PubMed2005

Plasticity in central olfactory processing and pheromone blend discrimination following interspecies antennal imaginal disc transplantation.

The antennal imaginal disc was transplanted between premetamorphic male larvae of two different Lepidopteran moth species. Following adult eclosion, electrophysiological recordings were made from 33 central olfactory neurons in the antennal lobes of both Helicoverpa zea donor to Heliothis virescens recipient (Z-V) and reciprocal (V-Z) transplants. Under the influence of sensory neuron input derived from the transplanted antennal imaginal disc, most antennal lobe projection neurons (29/33) were classified as belonging to physiological categories encountered previously in donor species males. Furthermore, when stained many of these neurons had dendritic arbors restricted to donor-induced glomerular locations predicted by their physiology. However, some neurons with unexpected physiological profiles were also identified (4/33), but only in V-Z transplants. These profiles help to explain why some V-Z bilateral transplants were able to respond to both pheromone blends in flight tunnel bioassays, an unforeseen result counter to the assumption that a donor antenna develops a normal donor antennal olfactory receptor neuron complement. Stainings of several neurons in V-Z transplant males also revealed unusual morphological features including multiglomerular dendritic arbors and "incorrect" glomerular locations. These results indicate a developmental plasticity in the final dendritic arborization pattern of central olfactory neurons, including an ability to colonize and integrate inputs across topographically novel donor glomeruli, different from those found in the normal recipient antennal lobe.

Animals↗

PubMed2001

Growth factors controlling imaginal disc growth in Drosophila.

In the imaginal discs of Drosophila, contact-dependent cell interactions are important both for promoting cell proliferation and for limiting it at the end of the growth period. However, recent work indicates that diffusible growth factors are also important in regulating growth and proliferation. We have identified a family of five imaginal disc growth factors (IDGFs) by purifying mitogenic proteins that accumulate in conditioned medium during culture of imaginal disc cell lines. These proteins cooperate with insulin to stimulate not only proliferation, but also polarization and motility of imaginal disc cells. They are produced by the fat body and are probably active on a variety of peripheral tissues. The IDGFs are structurally related to chitinases, but they show an amino acid substitution that is known to abrogate catalytic activity and to transform chitinases into lectins. We suggest that these proteins act as endogenous mitogenic lectins and mediate nutritional effects on tissue growth, possibly by interacting with the insulin receptor pathway. Glycoproteins similar to the IDGFs are found in mammals and may constitute a novel class of growth factors and/or inflammatory cytokines.

Animals↗

PubMed2002

Extracellular peptidases of imaginal discs of Drosophila melanogaster.

The imaginal discs of Drosophila melanogaster give rise to the adult epidermis during metamorphosis. During this developmental period several peptidase genes are expressed in disc cells, but there is a paucity of biochemical information regarding substrate specificity. We have used peptides and peptidyl 7-amino-4-methylcoumarin (AMC) substrates to detect several peptidases either positioned on the surface of wing discs or secreted by the imaginal cells. Using [Leu(5)]enkephalin as a substrate, a captopril sensitive dipeptidyl carboxypeptidase (angiotensin I-converting enzyme) and an amastatin-sensitive aminopeptidase were detected as prominent activities associated with intact discs. The formation of [Leu(5)]enkephalin-derived Phe was attributed to the concerted action of the D. melanogaster angiotensin I-converting enzyme (Ance) and a dipeptidase. The disc Ance also showed endopeptidic activity towards locust tachykinin-1 (LomTK-I) by cleaving the Gly-Val peptide bond, but this enzyme was not the sole endopeptidase activity associated with discs. Complete inhibition of the endopeptidic hydrolysis of the LomTK-1 by a disc homogenate required a combination of captopril and the neprilysin inhibitor, phosphoramidon, providing biochemical evidence for a neprilysin-like peptidase, in addition to Ance, in imaginal discs of D. melanogaster. Peptidyl AMC substrates for furin, prohormone convertase and tryptase provided evidence for trypsin-like serine endopeptidases in addition to the metalloendopeptidases. We conclude that imaginal discs are endowed with a variety of peptidases from different families that together are capable of hydrolyzing a broad range of peptides and proteins. Some of these peptidases might be responsible for the metabolic activation/inactivation of signaling peptides, as well as being involved in the production of dipeptides and free amino acids required for protein synthesis and osmotic balance during adult morphogenesis.

Animals↗

PubMed1980

The initiation of pupariation in Drosophila: dependence on growth of the imaginal discs.

Regeneration was induced in the imaginal discs in situ following lesions caused by heat-sensitive cell-lethal mutations. A clonal analysis of this event demonstrated that the subsequent delay in pupariation was correlated with the amount of extra growth that occurred during the regeneration. Pupariation of heat-treated gynandromorphs bearing the mutations was also retarded, and the duration of larval development increased with greater amounts of mutant tissue, it was therefore correlated with the extent of the lesions in the imaginal discs. Elimination of entire imaginal discs, or the presence of very small amounts of lethal tissue, did not result in prolonged larval life.

Animals↗

PubMed1991

Involvement of Sarcophaga lectin in the development of imaginal discs of Sarcophaga peregrina in an autocrine manner.

The imaginal discs of Sarcophaga were found not to develop normally in the presence of galactose, a hapten sugar of Sarcophaga lectin, or anti-Sarcophaga lectin antibody. Wing and leg discs cultured with these substances became morphologically abnormal and no imaginal discs reached the stage of terminal differentiation, even in the presence of 20-hydroxyecdysone. The development of the imaginal discs was shown to be autonomously regulated in an autocrine manner by Sarcophaga lectin; namely Sarcophaga lectin was secreted by the imaginal discs in the presence of 20-hydroxyecdysone, and the stimulus of self-induced Sarcophaga lectin seemed to be indispensable for further development of the imaginal discs. Sarcophaga lectin was originally found as a defense protein, but these results show that it plays independent roles in both defense and development.

Animals↗

PubMed2005

Role of Jun N-terminal Kinase (JNK) signaling in the wound healing and regeneration of a Drosophila melanogaster wing imaginal disc.

When a fragment of a Drosophila imaginal disc is cultured in growth permissive conditions, it either regenerates the missing structures or duplicates the pattern present in the fragment. This kind of pattern regulation is known to be epimorphic, i.e. the new pattern is generated by proliferation in a specialized tissue called the blastema. Pattern regulation is accompanied by the healing of the cut surfaces restoring the continuous epithelia. Wound healing has been considered to be the inductive signal to commence regenerative cell divisions. Although the general outlines of the proliferation dynamics in a regenerating imaginal disc blastema have been well studied, little is known about the mechanisms driving cells into the regenerative cell cycles. In this study, we have investigated the role of Jun N-terminal Kinase (JNK) signaling in the wound healing and regeneration of a Drosophila wing imaginal disc. By utilizing in vivo and in vitro culturing of incised and fragmented discs, we have been able to visualize the dynamics in cellular architecture and gene expression involved in the healing and regeneration process. Our results directly show that homotypic wound healing is not a prerequisite for regenerative cell divisions. We also show that JNK signaling participates in imaginal disc wound healing and is regulated by the physical dynamics of the process, as well as in recruiting cells into the regenerative cell cycles. A model describing the determination of blastema size is discussed.

Animals↗

PubMed1993

A wingless-dependent polar coordinate system in Drosophila imaginal discs.

The patterning of the imaginal discs in Drosophila melanogaster is a progressive process that, like the patterning of the larval epidermis during embryogenesis, requires the activity of segment polarity genes. One segment polarity gene, wingless, encodes a homolog of the mouse proto-oncogene Wnt-1 and plays a prominent role in the patterning of the larval epidermis and the imaginal discs. However, whereas the function of wingless in the embryo is initially associated with a pattern of stripes along the anteroposterior axis that are part of a Cartesian coordinate system, it is shown here that during imaginal development wingless is associated with a pattern of sectors that provide references for a polar coordinate system homologous to that postulated in a well-known model for the regeneration of insect and vertebrate limbs.

Animals↗

PubMed1985

Cell-free translation of Drosophila imaginal disc mRNA.

Total RNA derived from the imaginal discs of Drosophila melanogaster was translated in vitro, and the polypeptide products electrophoresed on two-dimensional gels. In agreement with previously published examinations of imaginal disc protein synthesis and content, we can detect no reproducible differences in abundant mRNA populations between different disc types (foreleg and wing). Differences can be found, however, between imaginal discs and other tissues. We also present evidence for a nonuniformly distributed wing disc mRNA.

Animals↗

PubMed1992

Genetic, cytogenetic and developmental analysis of the Drosophila melanogaster tumor suppressor gene lethal(2)tumorous imaginal discs (1(2)tid).

Three of the twenty recessive-lethal tumor suppressor genes of Drosophila cause imaginal disc tumors in the homozygously mutated state. One of these is the lethal(2)tumorous imaginal discs (l(2)tid) gene. Histological preparations show the tumorous imaginal disc epithelium to consist of a mosaic of cells in monolayer and cells in clumped arrangement. In contrast, the wild-type imaginal disc epithelium is comprised exclusively of cells in monolayer arrangement. Mutant imaginal disc tissue pieces implanted into ready-to-pupariate wild-type larvae fail to differentiate. Implantation of l(2)tid imaginal disc tissue pieces in vivo into wild-type adult flies revealed a lethal, tumorous growth comparable to that in situ, thus characterizing the l(2)tid imaginal discs as truly malignant. The phenotypes of double mutants between two l(2)tid alleles and tumor suppressor genes, such as lethal(2)giant larvae and lethal(2)brain tumor, and the epithelial overgrowth mutant lethal(2)fat are described and discussed. Finally, we present the genetic, cytogenetic and molecular localization of the l(2)tid gene to the giant chromosome bands 59F4-6.

Alleles↗

PubMed1999

Ectopic expression of human p53 inhibits entry into S phase and induces apoptosis in the Drosophila eye imaginal disc.

Transgenic flies in which ectopic expression of human p53 was targeted to the Drosophila eye imaginal disc were established. On sectioning of adult fly eyes which displayed a severe rough eye phenotype, most ommatidia were found to be fused and irregular shapes of rabdomeres were observed. In addition, many pigment cells were lost. In the developing eye imaginal disc, photoreceptor cell differentiation was initiated normally despite the ectopic expression of p53. However, expression of p53 inhibited cell cycle progression in eye imaginal disc cells and the S phase zone (the second mitotic wave) behind the morphogenetic furrow was almost completely abolished. Furthermore, expression of p53 induced extensive apoptosis of eye imaginal disc cells, and co-expression of baculovirus P35 in the eye imaginal disc suppressed the p53-induced rough eye phenotype. These results are consistent with the known functions of human p53 and indicate the existence of signaling systems with elements corresponding to human p53 in Drosophila eye imaginal disc cells. Genetic crosses of transgenic flies expressing p53 to a collection of Drosophila deficiency stocks allowed us to identify several genomic regions, deletions of which caused enhancement or suppression of the p53-induced rough eye phenotype. The transgenic flies established in this study should be useful to identify novel targets of p53 and its positive or negative regulators in Drosophila.

Animals↗

PubMed1993

Gene expression during imaginal disc regeneration detected using enhancer-sensitive P-elements.

When imaginal disc fragments from Drosophila are cultured in adult female hosts, they either duplicate the part of the pattern specified by the fate map, or regenerate to replace the missing part. The new tissue is added by proliferation of a small number of cells from the cut edge, brought together when the wound heals to form a regeneration blastema. Specification of the new pattern has been explained by assuming interactions among cells of different positional value in the regeneration blastema. In order to identify genes which might mediate these events, we screened over eight hundred independently isolated autosomal insertions of an enhancer-sensitive P-element, for altered lac-z expression in regenerating discs following cell death induced by a temperature-sensitive cell-lethal mutation. Two further screens divided the positive lines into four groups based on appropriate timing of the lac-z response in the cell-lethal mutant background and the expected response to an alternate source of cell death. Expression in wing disc fragments cultured in vivo was most frequent in the target class defined by the screens. In this direct test, lac-z expression was found in 23 lines and in most cases was spatially and temporally correlated with the formation of the regeneration blastema. Our results suggest a very substantial transcriptional response during the early stages of imaginal disc regeneration. lac-z expression in control imaginal discs, embryos and adult ovaries of the positive lines was also assayed. The selected insertions included: a small class expressed only in discs undergoing regeneration and apparently not at any other stage, possibly representing genes active exclusively in regeneration; a larger class expressed in the embryo or during oogenesis, but not normally in imaginal discs, as expected for functions recruited from earlier stages of the developmental program; and finally a class with spatially patterned expression in normal discs. This class included several insertions with expression associated with compartment boundaries, including one at the decapentaplegic (dpp), and one at the crumbs (crb) locus, a growth factor homologue, and an EGF-repeat gene respectively. Some of the expression patterns observed in cultured disc fragments provide evidence for cell communication in the regeneration blastema.

Animals↗

PubMed1999

A new family of growth factors produced by the fat body and active on Drosophila imaginal disc cells.

By fractionating conditioned medium (CM) from Drosophila imaginal disc cell cultures, we have identified a family of Imaginal Disc Growth Factors (IDGFs), which are the first polypeptide growth factors to be reported from invertebrates. The active fraction from CM, as well as recombinant IDGFs, cooperate with insulin to stimulate the proliferation, polarization and motility of imaginal disc cells. The IDGF family in Drosophila includes at least five members, three of which are encoded by three genes in a tight cluster. The proteins are structurally related to chitinases, but they show an amino acid substitution that is known to abrogate catalytic activity. It therefore seems likely that they have evolved from chitinases but acquired a new growth-promoting function. The IDGF genes are expressed most strongly in the embryonic yolk cells and in the fat body of the embryo and larva. The predicted molecular structure, expression patterns, and mitogenic activity of these proteins suggest that they are secreted and transported to target tissues via the hemolymph. However, the genes are also expressed in embryonic epithelia in association with invagination movements, so the proteins may have local as well as systemic functions. Similar proteins are found in mammals and may constitute a novel class of growth factors.

Amino Acid Sequence↗

PubMed1983

The effects of 20-hydroxyecdysone on the metabolic labeling of membrane proteins in Drosophila imaginal discs.

20-Hydroxyecdysone induces evagination of imaginal discs of Drosophila melanogaster cultured in vitro. The possible involvement of cell-surface proteins in this process has prompted us to study the synthesis of membrane proteins in imaginal discs. A procedure is reported for the isolation of membrane vesicle fractions from discs that are enriched for the plasma membrane enzyme, Na+/K+-ATPase, and that label with the surface-labeling reagent [125I]iodosulfanilic acid. 20-Hydroxyecdysone alters the pattern of [35S]methionine incorporation into polypeptides in these membrane vesicle fractions. Increased and decreased incorporation as well as changes in migration on two-dimensional gels of specific polypeptides are caused by the hormone. These changes parallel in time the onset and the continuation of evagination.

Animals↗

PubMed2001

The sex determination gene doublesex regulates the A/P organizer to direct sex-specific patterns of growth in the Drosophila genital imaginal disc.

Each Drosophila genital imaginal disc contains primordia for both male and female genitalia and analia. The sexually dimorphic development of this disc is governed by the sex-specific expression of doublesex (dsx). We present data that substantially revises our understanding of how dsx controls growth and differentiation in the genital disc. The classical view of genital disc development is that in each sex, dsx autonomously "represses" the development of the inappropriate genital primordium while allowing the development of the appropriate primordium. Instead, we show that dsx regulates the A/P organizer to control growth of each genital primordium, and then directs each genital primordium to differentiate defined adult structures in both sexes.

Animals↗

PubMed1999

Hedgehog is required for activation of engrailed during regeneration of fragmented Drosophila imaginal discs.

Surgically fragmented Drosophila appendage primordia (imaginal discs) engage in wound healing and pattern regulation during short periods of in vivo culture. Prothoracic leg disc fragments possess exceptional regulative capacity, highlighted by the ability of anterior cells to convert to posterior identity and establish a novel posterior compartment. This anterior/posterior conversion violates developmental lineage restrictions essential for normal growth and patterning of the disc, and thus provides an ideal model for understanding how cells change fate during epimorphic pattern regulation. Here we present evidence that the secreted signal encoded by hedgehog directs anterior/posterior conversion by activating the posterior-specific transcription factor engrailed in regulating anterior cells. In the absence of hedgehog activity, prothoracic leg disc fragments fail to undergo anterior/posterior conversion, but can still regenerate missing anterior pattern elements. We suggest that hedgehog-independent regeneration within the anterior compartment (termed integration) is mediated by the positional cues encoded by wingless and decapentaplegic. Taken together, our results provide a novel mechanistic interpretation of imaginal disc pattern regulation and permit speculation that similar mechanisms could govern appendage regeneration in other organisms.

Animals↗