A Fat Body-Derived IGF-like Peptide Regulates Postfeeding Growth in Drosophila

Okamoto, Naoki; Yamanaka, Naoaki; Yagi, Yuki; Nishida, Yasuyoshi; Kataoka, Hiroshi; O’Connor, Michael B.; Mizoguchi, Akira

doi:10.1016/j.devcel.2009.10.008

Cited by 239 publications

(270 citation statements)

References 33 publications

(49 reference statements)

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“…The role of oenocytes in metabolic adaptation resembles the function of the mammalian liver, as has been predicted from studies in larvae (14). The various insulin-like peptides of flies influence growth and stress responses in different contexts, providing a complex, spatiotemporally defined regulatory system to sustain local cell growth, proliferation, cell survival, and metabolism (10,11,(21)(22)(23)(24)(25)(26)(27)(28)(29)(30). So far, the molecular codes that ensure specificity in this signaling network remain unclear.…”

Section: Discussionmentioning

confidence: 96%

“…DILP6 is one such ligand. It is expressed in the fat body both in larvae and adults (10,11,24), and is induced after starvation (11). Because the fat body and oenocytes are closely associated in the adult abdomen, the induction of dILP6 after starvation suggested that it might serve as a paracrine signal that coordinates the fasting response between fat body and oenocytes.…”

Section: Dilp6 In Fat Body Is Required To Accumulate Lipid Droplets Inmentioning

confidence: 99%

“…growth in nonfeeding states, and its transcription in the fat body is induced under starvation conditions (10,11,24). DILP6 is likely to be an endocrine mediator of lifespan extension by Foxo activity in the fat body (11).…”

mentioning

confidence: 99%

“…In Drosophila, IIS activity is stimulated by a number of different insulin-like peptides (ILPs) that are independently regulated and can act in endocrine as well as local, paracrine fashion. A major source of dILPs are the median neurosecretory cells (mNSCs, also known as insulin-producing cells, IPCs) in the pars intercerebralis of the head, but expression of individual dILPs has also been reported in the gut, the ovary, glial cells, fat body, and abnormally growing imaginal discs (10,11,(21)(22)(23)(24)(25)(26)(27)(28)(29)(30). Whereas secretion of dILP2, -3, and -5 from mNSCs is regulated by nutritional cues, transcriptional regulation of these peptides depends on the stimulus (9,21).…”

mentioning

confidence: 99%

“…The central function of the liver in metabolic adaptation of flies is shared by the fat body and oenocytes. Whereas the fat body is an important glycogen and fat storage organ in flies, it also serves as an endocrine organ to coordinate metabolic homeostasis (9)(10)(11)(12). Oenocytes have a critical role in lipid mobilization and turnover in larvae, accumulating lipids during starvation similar to mammalian hepatocytes and expressing genes with homology to liver-specific enzymes in mammals (13,14).…”

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confidence: 99%

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Control of metabolic adaptation to fasting by dILP6-induced insulin signaling in Drosophila oenocytes

Chatterjee

Katewa

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Metabolic adaptation to changing dietary conditions is critical to maintain homeostasis of the internal milieu. In metazoans, this adaptation is achieved by a combination of tissue-autonomous metabolic adjustments and endocrine signals that coordinate the mobilization, turnover, and storage of nutrients across tissues. To understand metabolic adaptation comprehensively, detailed insight into these tissue interactions is necessary. Here we characterize the tissue-specific response to fasting in adult flies and identify an endocrine interaction between the fat body and liverlike oenocytes that regulates the mobilization of lipid stores. Using tissue-specific expression profiling, we confirm that oenocytes in adult flies play a central role in the metabolic adaptation to fasting. Furthermore, we find that fat body-derived Drosophila insulinlike peptide 6 (dILP6) induces lipid uptake in oenocytes, promoting lipid turnover during fasting and increasing starvation tolerance of the animal. Selective activation of insulin/IGF signaling in oenocytes by a fat body-derived peptide represents a previously unidentified regulatory principle in the control of metabolic adaptation and starvation tolerance.T o maintain metabolic homeostasis during fasting periods, metazoans have to coordinate the mobilization of glycogen, lipids, and protein, ensuring an adequate energy supply across tissues. In addition to tissue-autonomous metabolic adjustments, endocrine signals are therefore critical components of the fasting response (1, 2). In mammals, the liver is central to adjusting intermediary metabolism during fasting. Starvation stimulates lipid accumulation in hepatocytes, which oxidize these lipids to provide energy in the form of ketone bodies for other tissues. Hepatocytes also respond to glucagon and insulin signals to control the expression of enzymes involved in glycogenolysis and gluconeogenesis, lipolysis, fatty acid oxidation, and ketogenesis, all regulated by a battery of transcription factors that include forkhead box O (Foxo), cAMP-response element binding (CREB), peroxisome proliferator-activated receptor gamma, coactivator 1 alpha (PGC1a), and hepatocyte nuclear factor 4a (HNF4a) (3-5). At the same time, the liver integrates a suite of endocrine signals derived from major energy storing and consuming tissues, such as the brain, the adipose tissue, and the muscle (1). Deregulation of these processes can lead to hepatic steatosis and is a major cause of metabolic diseases, including diabetes and metabolic syndrome (1,3,6).Drosophila has emerged as a productive model organism in which to characterize the endocrine regulation of metabolic adaptation (7,8). The central function of the liver in metabolic adaptation of flies is shared by the fat body and oenocytes. Whereas the fat body is an important glycogen and fat storage organ in flies, it also serves as an endocrine organ to coordinate metabolic homeostasis (9-12). Oenocytes have a critical role in lipid mobilization and turnover in larvae, accumulating lipids during s...

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Section: Discussionmentioning

confidence: 96%

Section: Dilp6 In Fat Body Is Required To Accumulate Lipid Droplets Inmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Control of metabolic adaptation to fasting by dILP6-induced insulin signaling in Drosophila oenocytes

Chatterjee

Katewa

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The big and small of it: How body size evolves

Bernstein

2010

Am. J. Phys. Anthropol.

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Body size is a biological variable of fundamental importance and plays a central role in analyses of life history, sexual dimorphism, allometry, and natural and sexual selection. Yet, there remains a sizeable gulf in our understanding that lies between what we hypothesize influences change in size, from the point of view of ultimate causation, and what we know about how shifts in body size are regulated from a proximate perspective. I seek here to tie these two perspectives together, and specifically to argue that an understanding of the hormonal regulation of body size is necessary for constructing hypotheses regarding how body size evolves. Recent work using model organisms points to the insulin/insulin-like growth factor pathway as playing a key role in the regulation of growth, size, reproduction, and senescence. I review the role of various components of this pathway in regulating growth and size and illustrate the evidence for different ways in which these might work to generate differences in size in various organisms. Of particular interest are the tradeoffs between size and other life history traits produced by experimental alterations in this pathway. Recent work emphasizing the ways in which body size can be altered based on extrinsic factors provides the opportunity to link advances in uncovering the proximate bases of growth and size and offers an opportunity to frame new hypotheses regarding how variation in size evolves. Yrbk Phys Anthropol 53:46-62,

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Insulin‐like peptides of the legume pod borer, Maruca vitrata, and their mediation effects on hemolymph trehalose level, larval development, and adult reproduction

Baki

Lee

Jung

et al. 2018

Arch Insect Biochem Physiol

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Insulin-like peptides (ILPs) of insects mediate various physiological processes including hemolymph sugar level, immature growth, female reproduction, and lifespan. In target cells of ILPs, insulin/insulin-like growth factor signaling (IIS) is highly conserved in animals. IIS in the legume pod borer, Maruca vitrata (Lepidoptera: Crambidae), is known to be involved in maintaining hemolymph trehalose levels and promoting larval growth. However, ILPs in M. vitrata have not been reported yet. This study predicted two ILP genes of Mv-ILP1 and Mv-ILP2 from transcriptome of M. vitrata. Mv-ILP1 and Mv-ILP2 shared high sequence homologies and domain architecture with Drosophila ILPs. Both ILPs exhibited similar expression patterns in most developmental stages, showing high expression levels in adult stage. In the larval stage, Mv-ILP1 and Mv-IlP2 were expressed mostly in the brain and fat body. However, in the adult stage, both ILP genes were expressed more in the abdomen than those in the head containing the brain. RNA interference (RNAi) of either Mv-ILP1 or Mv-ILP2 during larval stage resulted in significant malfunctioning in regulating hemolymph trehalose titers. RNAi-treated larvae also exhibited significant retardation of larval growth. RNAi treatment in adult stage interfered with the ovarian development of females. These results suggest that Mv-ILP1 and Mv-ILP2 play crucial roles in mediating larval growth and adult reproduction.

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A Fat Body-Derived IGF-like Peptide Regulates Postfeeding Growth in Drosophila

Cited by 239 publications

References 33 publications

Control of metabolic adaptation to fasting by dILP6-induced insulin signaling in Drosophila oenocytes

Control of metabolic adaptation to fasting by dILP6-induced insulin signaling in Drosophila oenocytes

The big and small of it: How body size evolves

Insulin‐like peptides of the legume pod borer, Maruca vitrata, and their mediation effects on hemolymph trehalose level, larval development, and adult reproduction

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