Genes expressed during imaginal discs morphogenesis: IMP-L2, a gene expressed during imaginal disc and imaginal histoblast morphogenesis

doi:10.1016/0012-1606(88)90391-0

Developmental Biology

Volume 129, Issue 2, October 1988, Pages 439-448

https://doi.org/10.1016/0012-1606(88)90391-0 Get rights and content

Abstract

We describe our analysis of IMP-L2, one of a set of six ecdysone-inducible genes in imaginal discs of Drosophila whose transcripts are associated with membrane-bound polysomes. The spatial and temporal patterns of expression of the IMP-L2 transcript were analyzed. This transcript is first expressed in imaginal discs in areas that are precursors of head and thoracic epithelium, particularly the peripodial epithelia. It is later expressed in the imaginal histoblasts, precursors of the adult abdomen. The appearance of IMP-L2 transcript in each of these tissues precedes the spreading and fusion of the separate imaginal anlagen to form the continuous adult epidermis.

References (22)

D. Fristrom et al.
The hormonal coordination of cuticulin deposition and morphogenesis in Drosophila imaginal discs in vivo and in vitro
Dev. Biol
(1986)
T. Maniatis et al.
The isolation of structural genes from libraries of eukaryotic DNA
Cell
(1978)
J.B. Nardi et al.
Cellular events within peripodial epithelia that accompany evagination of Manduca wing discs: Conversion of cuboidal epithelia into columnar epithelia
Dev. Biol
(1987)
J.E. Natzle et al.
Genes expressed during imaginal disc morphogenesis: IMP-E1, a gene implicated in epithelial cell rearrangements
Dev. Biol
(1988)
J.E. Natzle et al.
Isolation of genes active during hormone-induced morphogenesis in Drosophila imaginal discs
J. Biol. Chem
(1986)
P.W.J. Rigby et al.
Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I
J. Mol. Biol
(1977)
P.J. Bryant
Pattern formation in imaginal discs
W.D. Benton et al.
Screening lambda gt recombinant clones by hybridization to single plaques in situ
Science
(1977)
J.M. Chirgwin et al.
Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease
Biochemistry
(1979)
D. Fristrom
The cellular basis of epithelial morphogenesis
Tissue and Cell
(1988)

P.J. Gergen et al.

Segmental pattern and blastoderm cell identities

Cited by (31)

From genes to shape during metamorphosis: a history
2021, Current Opinion in Insect Science
Citation Excerpt :
Fristrom’s vision accurately predicted later breakthroughs in studying adherens junctions [41••,42••,43–45] and cell rearrangements in the Drosophila embryo [46,47••,48••,49•], and the conflicts and resolutions with Keller’s vertebrate convergent-extension model have been reviewed in detail by John Wallingford [50]. Fristrom’s subsequent work focused on identifying genes that control wing and leg evagination in Drosophila and, in collaboration with her husband James, who had characterised the role of the steroid hormone 20-hydroxyecdysone (hereafter: ecdysone) in inducing metamorphosis [51,52], she published a series of papers on target genes of ecdysone (the hormone whose peak induces metamorphosis) [53–55], Broad (a transcription factor that acts downstream of Ecdysone) [56], and Stubble (a transmembrane protease induced by ecdysone) [57•,58]. But Fristrom’s own application of confocal imaging to understand leg morphogenesis was limited to a single collaborative paper [59•] and review article [60••] identifying a circumferential stretch pattern arising at the apical surface of early larval leg discs – involving planar polarisation of Myosin-II [60••] (Figure 4b) – that dissipated during evagination through apical shape change, rather than cell rearrangement, whose possible importance to morphogenesis was surprisingly walked-back:
Metamorphosis (Greek for a state of transcending-form or change-in-shape) refers to a dramatic transformation of an animal’s body structure that occurs after development of the embryo or larva in many species. The development of a fly (or butterfly) from a crawling larva (or caterpillar) that forms a pupa (or chrysalis) before eclosing as a flying adult is a classic example of metamorphosis that captures the imagination and has been immortalized in children’s books. Powerful genetic experiments in the fruit fly Drosophila melanogaster have revealed how genes can instruct the behaviour of individual cells to control patterns of tissue growth, mechanical force, cell–cell adhesion and cell-matrix adhesion drive morphogenetic change in epithelial tissues. Together, the distribution of mass, force and resistance determines cell shape changes, cell–cell rearrangements, and/or the orientation of cell divisions to generate the final form of the tissue. In organising tissue shape, genes harness the power of self-organisation to determine the collective behaviour of molecules and cells, which can often be reproduced in computer simulations of cell polarity and/or tissue mechanics. This review highlights fundamental discoveries in epithelial morphogenesis made by pioneers who were fascinated by metamorphosis, including D’Arcy Thompson, Conrad Waddington, Dianne Fristrom and Antonio Garcia-Bellido.
MicroRNA function in Drosophila melanogaster
2017, Seminars in Cell and Developmental Biology
Citation Excerpt :
Imp-L2 protein is secreted by the fat body under starvation conditions, and it binds to and inhibits humoral ILPs [49]. Since Imp-L2 expression is induced by ecdysone [50], it is likely that ecdysone regulation of miR-8 in the fat body is one means by which ecdysone stimulates Imp-L2. In turn, this would antagonize ILP-induced body growth.
Over the last decade, microRNAs have emerged as critical regulators in the expression and function of animal genomes. This review article discusses the relationship between microRNA-mediated regulation and the biology of the fruit fly Drosophila melanogaster. We focus on the roles that microRNAs play in tissue growth, germ cell development, hormone action, and the development and activity of the central nervous system. We also discuss the ways in which microRNAs affect robustness. Many gene regulatory networks are robust; they are relatively insensitive to the precise values of reaction constants and concentrations of molecules acting within the networks. MicroRNAs involved in robustness appear to be nonessential under uniform conditions used in conventional laboratory experiments. However, the robust functions of microRNAs can be revealed when environmental or genetic variation otherwise has an impact on developmental outcomes.
Steroid hormone regulation of C. elegans and Drosophila aging and life history
2011, Experimental Gerontology
Citation Excerpt :
Similar to C. elegans, we have recently found that ablation of germline stem cell can extend lifespan and modulate IIS/dFOXO in Drosophila, suggesting that the gonadal regulation of aging might be evolutionarily conserved (Flatt et al., 2008a). Germline-less, long-lived flies also exhibit increased expression of the secreted fly insulin/IGF-binding protein IMP-L2 (Flatt et al., 2008a), and IMP-L2 is an IIS antagonist (Honegger et al., 2008) known to be induced by 20E (Natzle et al., 1986; Osterbur et al., 1988; Andres et al., 1993). It is therefore an interesting possibility that in flies germline ablation extends lifespan by interacting with IIS and 20E/EcR signaling, as is the case in the nematode.
In the last two decades it has become clear that hormones and gene mutations in endocrine signaling pathways can exert major effects on lifespan and related life history traits in worms, flies, mice, and other organisms. While most of this research has focused on insulin/insulin-like growth factor-1 signaling, a peptide hormone pathway, recent work has shown that also lipophilic hormones play an important role in modulating lifespan and other life history traits. Here we review how steroid hormones, a particular group of lipophilic hormones, affect life history traits in the nematode worm (Caenorhabditis elegans) and the fruit fly (Drosophila melanogaster), with a particular focus on longevity. Interestingly, a comparison suggests that parallel endocrine principles might be at work in worms and flies in these species and that steroid hormones interact with the gonad to affect lifespan.
Structural and biological properties of the drosophila insulin-like peptide 5 show evolutionary conservation
2011, Journal of Biological Chemistry
Citation Excerpt :
The antagonizing effect of DILP function and insulin/insulin-like growth factor-like signaling was demonstrated by overexpression of dALS and IMP-L2 in vivo in Drosophila. The importance of IMP-L2 gene has been demonstrated by genetic studies, which have shown that disruption in the IMP-L2 gene results in embryonic lethality (65, 67, 68). In the starvation resistance study of the larvae, the loss of IMP-L2 leads to a failure to decrease insulin/insulin-like growth factor-like signaling causing high metabolism when the flies need to be shutting down, resulting in starvation sensitive mutants.
We report the crystal structure of two variants of Drosophila melanogaster insulin-like peptide 5 (DILP5) at a resolution of 1.85 Å. DILP5 shares the basic fold of the insulin peptide family (T conformation) but with a disordered B-chain C terminus. DILP5 dimerizes in the crystal and in solution. The dimer interface is not similar to that observed in vertebrates, i.e. through an anti-parallel β-sheet involving the B-chain C termini but, in contrast, is formed through an anti-parallel β-sheet involving the B-chain N termini. DILP5 binds to and activates the human insulin receptor and lowers blood glucose in rats. It also lowers trehalose levels in Drosophila. Reciprocally, human insulin binds to the Drosophila insulin receptor and induces negative cooperativity as in the human receptor. DILP5 also binds to insect insulin-binding proteins. These results show high evolutionary conservation of the insulin receptor binding properties despite divergent insulin dimerization mechanisms.
A new secreted insect protein belonging to the immunoglobulin superfamily binds insulin and related peptides and inhibits their activities
2000, Journal of Biological Chemistry
Citation Excerpt :
The results of our binding studies with des-octa peptide insulin show that this part of the insulin molecule has no importance for its binding to IMP-L2. IMP-L2 has previously been studied by Fristrom and co-workers (23, 31). IMP-L2 is characterized as being induced by the molting hormone 20-hydroxyecdysone and implicated in epithelial spreading and fusion.
Insulin and related peptides are key hormones for the regulation of growth and metabolism. Here we describe a novel high affinity insulin-related peptide-binding protein (IBP) secreted from cells of the insect Spodoptera frugiperda. This IBP is composed of two Ig-like C2 domains, has a molecular mass of 27 kDa, binds human insulin with an affinity of 70 pm, and inhibits insulin signaling through the insulin receptor. The binding protein also binds insulin-like growth factors I and II, proinsulin, mini-proinsulin, and an insulin analog lacking the last 8 amino acids of the B-chain (des-octa peptide insulin) with high affinity, whereas an insulin analog with a Asp-B10 mutation bound with only 1% of the affinity of human insulin. This binding profile suggests that IBP recognizes a region that is highly conserved in the insulin superfamily but distinct from the classical insulin receptor binding site. The closest homologue of the Spodoptera frugiperda binding protein is the essential gene product IMP-L2, found inDrosophila, where it is implicated in neural and ectodermal development (Garbe, J. C., Yang, E., and Fristrom, J. W. (1993) Development 119, 1237–1250). Here we show that the IMP-L2 protein also binds insulin and related peptides, offering a possible functional explanation to the IMP-L2 null lethality.
Molecular analysis of the initiation of insect metamorphosis: A comparative study of Drosophila ecdysteroid-regulated transcription
1993, Developmental Biology
More than 50 ecdysteroid-regulated Drosophila genes have been described in the literature. These genes were identified using several different ecdysteroid-responsive systems and characterized under a variety of experimental conditions. The diversity of these approaches has made it difficult to compare results and identify common responses to the hormone. As a first step toward characterizing the temporal regulation of these genes by ecdysteroids, we have examined their transcriptional activity throughout third instar larval and prepupal development using a single collection of staged animals. We see four coordinate changes in ecdysteroid-regulated gene activity during third instar larval development, at 78-88 hr, ∼100 hr, 106-108 hr, and ∼114 hr after egg laying. A dramatic transition in gene expression occurs at puparium formation, after which the prepupal ecdysteroid pulse induces successive waves of transcription. Our results suggest that several increases in the ecdysteroid titer during third instar larval and prepupal development program a precise temporal progression of gene activity that could direct the appropriate behavioral and developmental changes at the onset of metamorphosis.

View all citing articles on Scopus

^☆: This work was supported by USPHS Grant GM-19937 to J.W.F.

¹: Current address: Department of Biology, Indiana University, Bloomington, IN 47405.

²: Osterbur was supported for part of this work on USPHS Training Grant GM-07127.

²: Current address: Department of Zoology, University of California, Davis, CA 95616.

View full text

Article preview

Developmental Biology

Abstract

References (22)

The hormonal coordination of cuticulin deposition and morphogenesis in Drosophila imaginal discs in vivo and in vitro

Dev. Biol

The isolation of structural genes from libraries of eukaryotic DNA

Cell

Cellular events within peripodial epithelia that accompany evagination of Manduca wing discs: Conversion of cuboidal epithelia into columnar epithelia

Dev. Biol

Genes expressed during imaginal disc morphogenesis: IMP-E1, a gene implicated in epithelial cell rearrangements

Dev. Biol

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

J. Biol. Chem

Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I

J. Mol. Biol

Pattern formation in imaginal discs

Screening lambda gt recombinant clones by hybridization to single plaques in situ

Science

Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease

Biochemistry

The cellular basis of epithelial morphogenesis

Tissue and Cell

Segmental pattern and blastoderm cell identities

Cited by (31)

From genes to shape during metamorphosis: a history

MicroRNA function in Drosophila melanogaster

Steroid hormone regulation of C. elegans and Drosophila aging and life history

Structural and biological properties of the drosophila insulin-like peptide 5 show evolutionary conservation

A new secreted insect protein belonging to the immunoglobulin superfamily binds insulin and related peptides and inhibits their activities

Molecular analysis of the initiation of insect metamorphosis: A comparative study of Drosophila ecdysteroid-regulated transcription

Full paperGenes expressed during imaginal discs morphogenesis: IMP-L2, a gene expressed during imaginal disc and imaginal histoblast morphogenesis☆

Abstract

Dev. Biol

Cell

Dev. Biol

Dev. Biol

J. Biol. Chem

J. Mol. Biol

Pattern formation in imaginal discs

Screening lambda gt recombinant clones by hybridization to single plaques in situ

Science

Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease

Biochemistry

The cellular basis of epithelial morphogenesis

Tissue and Cell

Segmental pattern and blastoderm cell identities

Full paper
Genes expressed during imaginal discs morphogenesis: IMP-L2, a gene expressed during imaginal disc and imaginal histoblast morphogenesis☆