Coordination among multiple receptor tyrosine kinase signals controls Drosophila developmental timing and body size

Pan, Xueyang; O’Connor, Michael B.

doi:10.1016/j.celrep.2021.109644

Cited by 26 publications

(28 citation statements)

References 73 publications

(142 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Ecdysteroid biosynthesis in the PG is tightly regulated by endocrine and autocrine humoral factors. Endocrine factors include PTTH ( Kawakami et al, 1990 ; McBrayer et al, 2007 ), Drosophila insulin-like peptides (Dilps) ( Colombani et al, 2005 ), serotonin ( Shimada-Niwa and Niwa, 2014 ), Hedgehog ( Rodenfels et al, 2014 ), Decapentaplegic ( Setiawan et al, 2018 ), PDGF- and VEGF-related factors 2 and 3, and Jelly belly ( Pan and O’Connor, 2021 ). Autocrine factors include octopamine ( Ohhara et al, 2015 ) and epidermal growth factor ( Cruz et al, 2020 ).…”

Section: Future Perspectives and Remaining Questionsmentioning

confidence: 99%

Transcriptional Regulators of Ecdysteroid Biosynthetic Enzymes and Their Roles in Insect Development

Kamiyama

Niwa

2022

Front. Physiol.

View full text Add to dashboard Cite

Steroid hormones are responsible for coordinating many aspects of biological processes in most multicellular organisms, including insects. Ecdysteroid, the principal insect steroid hormone, is biosynthesized from dietary cholesterol or plant sterols. In the last 20 years, a number of ecdysteroidogenic enzymes, including Noppera-bo, Neverland, Shroud, Spook/Spookier, Cyp6t3, Phantom, Disembodied, Shadow, and Shade, have been identified and characterized in molecular genetic studies using the fruit fly Drosophila melanogaster. These enzymes are encoded by genes collectively called the Halloween genes. The transcriptional regulatory network, governed by multiple regulators of transcription, chromatin remodeling, and endoreplication, has been shown to be essential for the spatiotemporal expression control of Halloween genes in D. melanogaster. In this review, we summarize the latest information on transcriptional regulators that are crucial for controlling the expression of ecdysteroid biosynthetic enzymes and their roles in insect development.

show abstract

Section: Future Perspectives and Remaining Questionsmentioning

confidence: 99%

Transcriptional Regulators of Ecdysteroid Biosynthetic Enzymes and Their Roles in Insect Development

Kamiyama

Niwa

2022

Front. Physiol.

View full text Add to dashboard Cite

show abstract

“…Downstream of IIS, extracellular signal-regulated kinase (ERK) can also induce activity of the transcription factor Pointed, which modifies the EGF receptor signaling pathway ( O’Neill et al, 1994 ; Traverse et al, 1994 ; Morimoto et al, 1996 ). Among other functions, EGFR signaling regulates the production of ecdysone in the PG ( Cruz et al, 2020 ; Pan and O’Connor, 2021 ).…”

Section: Insulinmentioning

confidence: 99%

“…However, recent work has prompted reanalysis of the canonical ecdysone synthesis pathway ( Cruz et al, 2020 ; Pan and O’Connor, 2021 ). In both Drosophila and Bombyx mori , null mutants of PTTH or Torso will delay metamorphic transition from larvae to pupae, but will not arrest development indefinitely, implying the dispensability of PTTH for ecdysone biosynthesis in at least some insects ( Uchibori-Asano et al, 2017 ).…”

Section: Prothoracicotropic Hormonementioning

confidence: 99%

“…These results suggest Egf signaling may be the primary mode of regulation of ecdysone biosynthesis at developmental transitions. Additionally, Pan and O’Connor (2021) have identified several more candidate signaling pathways apart from PTTH to fine-tune metamorphic timing via ecdysone biosynthesis. Loss of anaplastic lymphoma kinase (Alk) and PDGF and VEGF receptor-related (Pvr) in the PG causes developmental delay in Drosophila.…”

Section: Prothoracicotropic Hormonementioning

confidence: 99%

See 1 more Smart Citation

Endocrine Regulation of Lifespan in Insect Diapause

Hutfilz

2022

Front. Physiol.

View full text Add to dashboard Cite

Diapause is a physiological adaptation to conditions that are unfavorable for growth or reproduction. During diapause, animals become long-lived, stress-resistant, developmentally static, and non-reproductive, in the case of diapausing adults. Diapause has been observed at all developmental stages in both vertebrates and invertebrates. In adults, diapause traits weaken into adaptations such as hibernation, estivation, dormancy, or torpor, which represent evolutionarily diverse versions of the traditional diapause traits. These traits are regulated through modifications of the endocrine program guiding development. In insects, this typically includes changes in molting hormones, as well as metabolic signals that limit growth while skewing the organism’s energetic demands toward conservation. While much work has been done to characterize these modifications, the interactions between hormones and their downstream consequences are incompletely understood. The current state of diapause endocrinology is reviewed here to highlight the relevance of diapause beyond its use as a model to study seasonality and development. Specifically, insect diapause is an emerging model to study mechanisms that determine lifespan. The induction of diapause represents a dramatic change in the normal progression of age. Hormones such as juvenile hormone, 20-hydroxyecdysone, and prothoracicotropic hormone are well-known to modulate this plasticity. The induction of diapause—and by extension, the cessation of normal aging—is coordinated by interactions between these pathways. However, research directly connecting diapause endocrinology to the biology of aging is lacking. This review explores connections between diapause and aging through the perspective of endocrine signaling. The current state of research in both fields suggests appreciable overlap that will greatly contribute to our understanding of diapause and lifespan determination.

show abstract

“…Our findings show that JAK/STAT signaling is active in the PG at basal levels during normal development. Another study examined JAK/STAT activity in the PG and found expression of the same 10xSTAT-GFP reporter we used ( Pan and O'Connor, 2021 ). We found, in addition, that pupation is slightly advanced and the size of the ring gland is smaller in multiple conditions of JAK/STAT signaling reduction, including knockdown in PG cells of upd3 , which a GAL4 expression reporter and quantitative reverse transcription PCR (qRT-PCR) show is intrinsically expressed in the ring gland.…”

Section: Discussionmentioning

confidence: 99%

Intrinsic and damage-induced JAK/STAT signaling regulate developmental timing by the Drosophila prothoracic gland

Cao

Rojas

Pastor-Pareja

2022

Disease Models &Amp; Mechanisms

View full text Add to dashboard Cite

Development involves tightly paced, reproducible sequences of events, yet it must adjust to conditions external to it, such as resource availability and organismal damage. A major mediator of damage-induced immune responses in vertebrates and insects is JAK/STAT signaling. At the same time, JAK/STAT activation by the Drosophila Upd cytokines is pleiotropically involved in normal development of multiple organs. Whether inflammatory and developmental roles of JAK/STAT intersect is unknown. Here, we show that JAK/STAT is active during development of the prothoracic gland (PG), the organ that controls metamorphosis onset through ecdysone production. Reducing JAK/STAT signaling decreased PG size and slightly advanced metamorphosis. Conversely, JAK/STAT hyperactivation, achieved through overexpression of pathway components or SUMOylation loss, caused PG hypertrophy and metamorphosis delay. Interestingly, tissue damage and tumors, known to secrete Upd cytokines, also activated JAK/STAT in the PG and delayed metamorphosis. Finally, we show that expression of transcription factor Apontic, a JAK/STAT target in the PG, recapitulates PG hypertrophy and metamorphosis delay. JAK/STAT damage signaling, therefore, regulates metamorphosis onset at least in part by coopting its developmental role in the PG.

show abstract

Coordination among multiple receptor tyrosine kinase signals controls Drosophila developmental timing and body size

Abstract: Highlights d Juxtacrine Jeb/Alk and autocrine Pvf/Pvr signals control timing of ecdysone production d Jeb/Alk and Pvf/Pvr augment PTTH/Torso and EGFR signaling, respectively, via Ras/Erk d Jeb/Alk signaling also regulates starvation-induced autophagy within the PG

Cited by 26 publications

References 73 publications

Transcriptional Regulators of Ecdysteroid Biosynthetic Enzymes and Their Roles in Insect Development

Transcriptional Regulators of Ecdysteroid Biosynthetic Enzymes and Their Roles in Insect Development

Endocrine Regulation of Lifespan in Insect Diapause

Intrinsic and damage-induced JAK/STAT signaling regulate developmental timing by the Drosophila prothoracic gland

Contact Info

Product

Resources

About