Juvenile Hormone Is Required to Couple Imaginal Disc Formation with Nutrition in Insects

Faculty of Agriculture and Life Sciences, Hirosaki University, Khirosaki, Aomori, Japan
Science (Impact Factor: 33.61). 07/2006; 312(5778):1385-8. DOI: 10.1126/science.1123652
Source: PubMed


In starved larvae of the tobacco hornworm moth Manduca sexta, larval and imaginal tissues stop growing, the former because they lack nutrient-dependent signals but the latter because
of suppression by juvenile hormone. Without juvenile hormone, imaginal discs form and grow despite severe starvation. This
hormone inhibits the intrinsic signaling needed for disc morphogenesis and does so independently of ecdysteroid action. Starvation
and juvenile hormone treatments allowed the separation of intrinsic and nutrient-dependent aspects of disc growth and showed
that both aspects must occur during the early phases of disc morphogenesis to ensure normal growth leading to typical-sized

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    • "Starvation represses the growth of the wing discs, and eye and leg primordia (Macwhinnie et al., 2005; Truman et al., 2006). Eliminating JH by removing the CA partially restores disc growth even in starved larvae (Truman et al., 2006). The effects of JH on tissue growth are overridden by insulin; wing discs cultured in the presence of JH alone show reduced growth whereas when they are cultured with JH and insulin, growth rates are restored (Koyama et al., 2008). "
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    ABSTRACT: Nutrition, via the insulin/insulin-like growth factor (IIS)/Target of Rapamycin (TOR) signaling pathway, can provide a strong molding force for determining animal size and shape. For instance, nutrition induces a disproportionate increase in the size of male horns in dung and rhinoceros beetles, or mandibles in staghorn or horned flour beetles, relative to body size. In these species, well-fed male larvae produce adults with greatly enlarged horns or mandibles, whereas males that are starved or poorly fed as larvae bear much more modest appendages. Changes in IIS/TOR signaling plays a key role in appendage development by regulating growth in the horn and mandible primordia. In contrast, changes in the IIS/TOR pathway produce minimal effects on the size of other adult structures, such as the male genitalia in fruit flies and dung beetles. The horn, mandible and genitalia illustrate that although all tissues are exposed to the same hormonal environment within the larval body, the extent to which insulin can induce growth is organ specific. In addition, the IIS/TOR pathway affects body size and shape by controlling production of metamorphic hormones important for regulating developmental timing, like the steroid molting hormone ecdysone and sesquiterpenoid hormone juvenile hormone. In this review, we discuss recent results from Drosophila and other insects that highlight mechanisms allowing tissues to differ in their sensitivity to IIS/TOR and the potential consequences of these differences on body size and shape.
    Frontiers in Physiology 09/2013; 4:263. DOI:10.3389/fphys.2013.00263 · 3.53 Impact Factor
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    • "At the beginning of the final larval instar, wing discs are committed to initiate larval-pupal development. Juvenile hormone (JH) prevents this commitment in earlier instars and in starved final instar larvae, but nutrient intake overcomes this effect of JH in the latter (Truman et al., 2006). "
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    ABSTRACT: A quarter of a century has passed since bombyxin, the first insulin-like peptide identified in insects, was discovered in the silkmoth Bombyx mori. During these years, bombyxin has been studied for its structure, genes, distribution, hemolymph titers, secretion control, as well as physiological functions, thereby stimulating a wide range of studies on insulin-like peptides in other insects. Moreover, recent studies have identified a new class of insulin family peptides, IGF-like peptides, in B. mori and Drosophila melanogaster, broadening the base of the research area of the insulin-related peptides in insects. In this review, we describe the achievements of the studies on insulin-like and IGF-like peptides mainly in B. mori with short histories of their discovery. Our emphasis is that bombyxins, secreted by the brain neurosecretory cells, regulate nutrient-dependent growth and metabolism, whereas the IGF-like peptides, secreted by the fat body and other peripheral tissues, regulate stage-dependent growth of tissues.
    Frontiers in Physiology 08/2013; 4:217. DOI:10.3389/fphys.2013.00217 · 3.53 Impact Factor
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    • "These sex differences in locomotor activity are dependent on insulin and juvenile hormone signaling [98,99]. As these hormones that have been implicated in the internal representation of feeding status in insects [100-102], these observations raise the possibility that sex differences in spontaneous motor activity may reflect a sex difference in appetitive or motivational state in Drosophila. It is thought that sexual modification of a small set of approximately ten neurons in the pars intercerebralis (PI) determines the sex-specific structure of locomotor bouts. "
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    ABSTRACT: Animals prioritize behaviors according to their physiological needs and reproductive goals, selecting a single behavioral strategy from a repertoire of possible responses to any given stimulus. Biological sex influences this decision-making process in significant ways, differentiating the responses animals choose when faced with stimuli ranging from food to conspecifics. We review here recent work in invertebrate models, including C. elegans, Drosophila, and a variety of insects, mollusks and crustaceans, that has begun to offer intriguing insights into the neural mechanisms underlying the sexual modulation of behavioral decision-making. These findings show that an animal's sex can modulate neural function in surprisingly diverse ways, much like internal physiological variables such as hunger or thirst. In the context of homeostatic behaviors such as feeding, an animal's sex and nutritional status may converge on a common physiological mechanism, the functional modulation of shared sensory circuitry, to influence decision-making. Similarly, considerable evidence suggests that decisions on whether to mate or fight with conspecifics are also mediated through sex-specific neuromodulatory control of nominally shared neural circuits. This work offers a new perspective on how sex differences in behavior emerge, in which the regulated function of shared neural circuitry plays a crucial role. Emerging evidence from vertebrates indicates that this paradigm is likely to extend to more complex nervous systems as well. As men and women differ in their susceptibility to a variety of neuropsychiatric disorders affecting shared behaviors, these findings may ultimately have important implications for human health.
    Biology of Sex Differences 03/2012; 3(1):8. DOI:10.1186/2042-6410-3-8 · 4.84 Impact Factor
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