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Molecular Basis of Juvenile Hormone Signaling

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Molecular Basis of Juvenile Hormone Signaling Available online at www.sciencedirect.com ScienceDirect Molecular basis of juvenile hormone signaling 1 2 3 Marek Jindra , Xavier Belle´ s and Tetsuro Shinoda Despite important roles played by juvenile hormone (JH) in of the recently characterized JH receptor, and the role JH insects, the mechanisms underlying its action were until signaling plays during insect development. recently unknown. A breakthrough has been the demonstration that the bHLH-PAS protein Met is an intracellular receptor for Establishing Met as a JH receptor JH. Binding of JH to Met triggers dimerization of Met with its Sesquiterpenoids in structure, JHs differ from other ani- partner protein Tai, and the resulting complex induces mal non-peptide lipophilic hormones, which all activate transcription of target genes. In addition, JH can potentiate this proteins of the nuclear receptor family [1,2]. In contrast, response by phosphorylating Met and Tai via cell membrane, the intracellular JH receptor, Methoprene-tolerant (Met), second-messenger signaling. An important gene induced by belongs to an ancient family of basic helix–loop–helix the JH–Met–Tai complex is Kr-h1, which inhibits Per/Arnt/Sim (bHLH-PAS) transcription factors [3,4,5 ] metamorphosis. Kr-h1 represses an ‘adult specifier’ gene (reviewed in [6,7]). E93. The action of this JH-activated pathway in maintaining the juvenile status is dispensable during early postembryonic Met was discovered in 1986 through a mutagenesis screen development when larvae/nymphs lack competence to in Drosophila melanogaster as a genetic lesion that caused metamorphose. resistance to the JH mimic methoprene, but permitted Addresses the flies to survive [8]. Lethality resulted when loss of Met 1 Biology Center, Czech Academy of Sciences, Branisovska 31, Ceske was combined with a deletion in a paralogous D. melano- Budejovice 37005, Czech Republic gaster gene, germ cell-expressed (gce) [9]. However, no de- 2 Institute of Evolutionary Biology, CSIC-Universitat Pompeu Fabra, velopmental defect obviously linked to disrupted JH Passeig Marı´tim 37, 08003 Barcelona, Spain 3 signaling (i.e. precocious metamorphosis), could be dis- National Institute of Agrobiological Sciences, Ohwashi 1-2, Tsukuba, cerned in the mutants. The expected phenotype was Ibaraki 305-8634, Japan revealed through RNAi knockdown of a single Met/gce Corresponding author: Jindra, Marek ([email protected]) ortholog in the red flour beetle, Tribolium castaneum, which triggered precocious pupation of larvae [10]. This phenotype matched the effect of JH depletion [11], thus Current Opinion in Insect Science 2015, 11:39–46 establishing Met as a mediator of the capacity of JH to This review comes from a themed issue on Molecular physiology prevent metamorphosis. Edited by Naoki Yamanaka and Alexander Raikhel Met/Gce proteins from several insect species have been shown to bind the natural JH (JH III) at physiological (nanomolar) range [4,5 ,12,13 ]. Synthetic JH mimics, http://dx.doi.org/10.1016/j.cois.2015.08.004 including methoprene or pyriproxyfen, are also true ago- 2214-5745/# 2015 Elsevier Inc. All rights reserved. nists of T. castaneum Met and D. melanogaster Gce, as they compete with JH III for binding to the same receptor domain [4,5 ]. Interestingly, Gce can bind the non- epoxidated JH precursor, methyl farnesoate (MF), albeit with an affinity nearly fivefold lower than that for JH III [5 ]. Consistently, MF is less potent than epoxidated JHs Introduction in inducing transcription of Met/Gce-dependent genes JH was originally known for its capacity to maintain [5 ,14,15]. MF prevails over JH III and is considered a juvenile character of insect larvae and thus ensure proper genuine circulating hormone in D. melanogaster larvae timing of metamorphosis. However, JHs govern many [15,16], but in live silkworms (Bombyx mori) MF cannot aspects of development and reproduction, not only in compensate for loss of epoxidated JH [17]. insects but also in related crustaceans. Being essential to arthropods and absent from vertebrates, JH signaling Although the crystal structure of the JH receptor is yet to offers a target to control insect pests and disease vectors. be resolved, a model of the JH-binding domain of Met/ Insecticides that mimic the effect of JH on development Gce has been developed based on homology to related have been employed for decades. Detailed knowledge of bHLH-PAS proteins of known structures [4,7,13 ]. When the mode of JH action is therefore of major interest, both individual amino acids forming the presumed ligand- from the biological and the practical perspectives. The binding pocket of T. castaneum Met were replaced with purpose of this review is to highlight important new residues possessing bulkier side chains, binding of JH III findings en route to understanding the molecular action was abolished or reduced [4]. These results have been www.sciencedirect.com Current Opinion in Insect Science 2015, 11:39–46 40 Molecular physiology corroborated with Met/Gce from D. melanogaster and the JH-dependent growth [25]. Lipid accumulation for milk mosquito Aedes aegypti [5 ,13 ]. A recent demonstration synthesis in the tsetse fly females also relies on Met rather that Gce and Met indeed require the JH-binding capacity than Gce [36 ]. Conversely, Gce rather than Met seems to in vivo to sustain the normal development in D. melano- mediate JH effect on enterocyte proliferation in the gut of gaster provides unequivocal genetic evidence for the JH mated D. melanogaster females [37 ]. Thus, while Met and receptor function of the two proteins [5 ]. Gce can mutually substitute for each other under experi- mental conditions, they are not fully redundant during Biological roles and their partition between normal development. duplicated JH receptor genes Although Met/Gce may not be the single universal JH Met and gce arose via gene duplication during dipteran receptor, it seems versatile enough to execute several evolution, as both paralogs are present in Drosophila major functions of JH in insects. A model in which JH- species and in the tsetse fly, but not in less modified activated Met represses metamorphosis via regulating dipterans such as mosquitoes [36 ,40,41]. gce is more downstream genes has been validated across distant similar than Met to the single orthologs of other insects. orders [18–22,23 ] (for recent reviews see [6,24 ]). A Conserved positions of 10 introns in gce and presence of growth-promoting effect of JH in D. melanogaster larvae only two introns in Met suggest that gce is the ancestral also relies on Met [25]. Recently, Met has been implicat- gene. Two paralogs of Met/gce, called Met1 and Met2, are ed in soldier caste formation in termites [26], where also found in B. mori [14,42], and phylogenetic analyses development of specific body parts into ‘weapons’ is a show that the gene duplication occurred independently striking example of polyphenism induced by JH. after the divergence of Diptera and Lepidoptera [43]. Similarly to gce in D. melanogaster, Met2 contains 9 introns; In addition to the roles JH plays in juveniles, Met is Met1 is intronless. required for JH-dependent reproductive maturation in adult females across distant insect orders [8,27–34]. Met B. mori Met2 and Met1 both mediate JH signaling, albeit has been shown to act autonomously in the fat body to the latter was less potent in a cell-based assay [14,44]. It induce expression of yolk precursor proteins, vitellogen- was initially reported that RNAi knockdown of either ins, in response to JH [29,31,33]. While this induction Met1 or Met2 prevented pupation or adult emergence and appears to be indirect, a mechanism involving JH- that both proteins were essential for normal transcription- dependent and Met-dependent polyploidization of fat al activation by the steroid hormone 20-hydroxyecdysone body cells has been proposed [33]. Other adult roles of (20E) in B. mori [42]. However, in another lepidopteran, Met include stimulation of mating behavior [35] or Helicoverpa armigera, Met1 RNAi shortened the final larval termination of seasonal reproductive diapause [34]. In instar but neither inhibited pupation nor affected the the viviparous tsetse fly, Glossina morsitans, knockdown response to 20E [45]. These inconsistencies might be due of Met reduced lipid accumulation, which is required for to off-target effects or efficiency of RNAi, which varies sufficient lactation and hence for successful pregnancy greatly in lepidopterans [46]. The transcription activator- [36 ]. Finally, a recent study reveals that in preparation like effector nuclease (TALEN) technique that has been for the increased food intake that is needed for oogene- adapted for B. mori [47,48] is much more robust as it sis, JH acts through Met and Gce to induce proliferation produces genetic mutants. TALEN-based knockout has of gut progenitor cells in mated D. melanogaster females recently revealed that loss of Met1 in B. mori causes [37 ]. lethality at the second-to-third larval instar molt, with patches of prematurely forming pupal cuticle. In contrast, One reason explaining why D. melanogaster Met-null Met2 knockout silkworms develop normally to adults and mutants do not die is that the function of Met is partly lay eggs [23 ]. Thus, Met1 mediates the anti-metamor- redundant with gce [9]. gce-null flies are viable and tolerate phic action of JH in B. mori larvae, whereas the role of high levels of JH mimics. Only loss of both Met and gce Met2 remains unclear. causes lethality at the onset of pupation, similarly to genetic elimination of the JH-producing gland, the corpus The intracellular JH receptor complex allatum [9,38]. Like Met, Gce is capable of binding JH Like other bHLH-PAS proteins, Met dimerizes with [5 ] and mediating its effect on target gene expression other members of the bHLH-PAS family to form a [5 ,9,39 ]. When expressed from transgenic constructs in functional transcription factor.
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