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Juvenile Hormone Regulation of Drosophila Aging Rochele Yamamoto Brown University

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Juvenile Hormone Regulation of Drosophila Aging Rochele Yamamoto Brown University Ecology, Evolution and Organismal Biology Ecology, Evolution and Organismal Biology Publications 2013 Juvenile hormone regulation of Drosophila aging Rochele Yamamoto Brown University Hua Bai Brown University Adam G. Dolezal Iowa State University, [email protected] Gro Amdam Arizona State University Marc Tatar Brown University Follow this and additional works at: http://lib.dr.iastate.edu/eeob_ag_pubs Part of the Cell and Developmental Biology Commons, Ecology and Evolutionary Biology Commons, Entomology Commons, and the Genetics Commons The ompc lete bibliographic information for this item can be found at http://lib.dr.iastate.edu/ eeob_ag_pubs/206. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html. This Article is brought to you for free and open access by the Ecology, Evolution and Organismal Biology at Iowa State University Digital Repository. It has been accepted for inclusion in Ecology, Evolution and Organismal Biology Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Yamamoto et al. BMC Biology 2013, 11:85 http://www.biomedcentral.com/1741-7007/11/85 RESEARCH ARTICLE Open Access Juvenile hormone regulation of Drosophila aging Rochele Yamamoto1, Hua Bai1, Adam G Dolezal2,3, Gro Amdam2 and Marc Tatar1* Abstract Background: Juvenile hormone (JH) has been demonstrated to control adult lifespan in a number of non-model insects where surgical removal of the corpora allata eliminates the hormone’s source. In contrast, little is known about how juvenile hormone affects adult Drosophila melanogaster. Previous work suggests that insulin signaling may modulate Drosophila aging in part through its impact on juvenile hormone titer, but no data yet address whether reduction of juvenile hormone is sufficient to control Drosophila life span. Here we adapt a genetic approach to knock out the corpora allata in adult Drosophila melanogaster and characterize adult life history phenotypes produced by reduction of juvenile hormone. With this system we test potential explanations for how juvenile hormone modulates aging. Results: A tissue specific driver inducing an inhibitor of a protein phosphatase was used to ablate the corpora allata while permitting normal development of adult flies. Corpora allata knockout adults had greatly reduced fecundity, inhibited oogenesis, impaired adult fat body development and extended lifespan. Treating these adults with the juvenile hormone analog methoprene restored all traits toward wildtype. Knockout females remained relatively long-lived even when crossed into a genotype that blocked all egg production. Dietary restriction further extended the lifespan of knockout females. In an analysis of expression profiles of knockout females in fertile and sterile backgrounds, about 100 genes changed in response to loss of juvenile hormone independent of reproductive state. Conclusions: Reduced juvenile hormone alone is sufficient to extend the lifespan of Drosophila melanogaster. Reduced juvenile hormone limits reproduction by inhibiting the production of yolked eggs, and this may arise because juvenile hormone is required for the post-eclosion development of the vitellogenin-producing adult fat body. Our data do not support a mechanism for juvenile hormone control of longevity simply based on reducing the physiological costs of egg production. Nor does the longevity benefit appear to function through mechanisms by which dietary restriction extends longevity. We identify transcripts that change in response to juvenile hormone independent of reproductive state and suggest these represent somatically expressed genes that could modulate how juvenile hormone controls persistence and longevity. Keywords: Juvenile hormone, Drosophila, Lifespan, Fecundity, Fat body, Gene expression Background bodies [2-7]. JH in the adult also affects learning, mi- Juvenile hormone (JH) plays a central role in insect devel- gration, diapause and innate immunity [8-11]. In the opment where it interacts with ecdysone to maintain lar- monarch butterfly, some grasshoppers and the firebug val status quo between molts [1]. In adults, JH takes on Pyrrhocoris apterus, surgical allatectomy extends lifespan, different functions. From work with a variety of insects, suggesting that JH is a pro-aging hormone [12-14]. there is consensus that JH produced in adult corpora Drosophila melanogaster produces three forms of allata modulates ovarian maturation, in part through its juvenile hormone: methyl farnesoate (MF), JHIII and regulation of yolk protein uptake while ecdysone derived bisepoxide JHIII (JHBIII) [15]. JHBIII is unique to dip- from the follicle cells induces yolk protein synthesis in fat terans and is the most abundant JH in flies. In other in- sects, exogenous JH or juvenile hormone analogs (JHA), * Correspondence: [email protected] such as methoprene, induce supernumerary juvenile or 1Department of Ecology and Evolutionary Biology, Brown University, pupal stages and block metamorphosis, but Drosophila Providence, RI, USA larvae treated with JH analogs still initiate metamorphosis Full list of author information is available at the end of the article © 2013 Yamamoto et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Yamamoto et al. BMC Biology 2013, 11:85 Page 2 of 14 http://www.biomedcentral.com/1741-7007/11/85 [16,17], although high doses of JHA produce a mosaic Allatectomy reduced egg production as expected, and fe- adult where the abdomen is covered with pupal cuticle cundity was partially restored by treating adults with ex- [18]. The high dosage required to induce this phenotype, ogenous JHA. Reduced JH extended lifespan in fertile flies and an artifact produced by a common genetic marker and, importantly, it also did so in adults made sterile by (rosy encoding xanthine dehydrogenase), have complicated the dominant OvoD1 mutation, which inhibits egg matur- our ability to study the roles of JH in Drosophila develop- ation [35]. These data suggest that reduced JH extends life- ment [19,20]. Even less is known about the role of JH in span by mechanisms independent of direct physiological the Drosophila adult, in part because treating wildtype trade-offs with egg production. Allatectomy extended life- adults with JH analogs produces few obvious phenotypes span robustly in flies fed different concentrations of yeast, and because surgical allatectomy is not practical. eliminating a potential explanation based on mechanisms One potential role for JH in adult Drosophila became of dietary restriction. Finally, we analyzed gene expression apparent in studies of fly insulin-like receptor mutants. profiles from allatectomized adults when fertile and when Drosophila insulin-like receptor (InR) mutants have OvoD1 sterile, and from the intersection of these data iden- ovaries similar to those seen in wildtype flies during re- tified soma-related genes through which JH may poten- productive diapause [21]. Drosophila reproductive dia- tially modulate longevity. pause is maintained in part by reduced JH [22,23], and insulin-like signaling mutants were found to be JH defi- Results and discussion cient [21]. InR mutants are long-lived, and JHA treat- Corpora allata knockout (CAKO) ment restores lifespan toward that of wildtype flies. JH is normally abundant in females, at least up to age 10 Together these observations motivated the question of days [36]. Here, the genotype Aug21-Gal4, UAS-GFP > our current study: Is JH deficiency sufficient to extend UAS-NIPP1 (CAKO: Corpora Allata Knock Out) pro- lifespan in Drosophila, and if so, by what mechanism? duced adults within 12 to 24 hours post-eclosion with JH production in Drosophila might be experimentally small to non-existent corpora allata and limited levels of reduced in several ways. A classic genetic approach used JH as measured by gas chromatography–mass spectrom- the apterous mutant, which regulates development in etry. Females of wildtype and parental genotypes contained wing, muscle and axons, and neuroendocrine control of between 700 and 850 pg JH per gram body mass while juvenile hormone as well as other neuropeptides [24-28]. CAKO females had less than 50 pg/g (Figure 1). More recently, the P{Gal4} insertion (Aug21) was found to be expressed in larval corpora allata [29] and Riddiford CAKO reduces fecundity and impedes adult fat body et al. [30] used Aug21 to drive UAS-grim to induce apop- development tosis in larval corpora allata (CA). Allatectomized larvae CAKO strongly reduced egg production. When measured produced small pupae that died at head eversion and from caged cohorts, average daily fecundity of control ge- showed many photoreceptor development defects. Liu notypes peaked at 50 to 60 eggs per female, while CAKO et al. [31] used this genotype to reveal how the JH- females laid less than 20 eggs per day (Figure 2A). Fecund- interacting proteins MET (methoprene-tolerant) and GCE ity was also measured from individually maintained fe- (Germ-cell expressed bHLH-PAS) regulate larval fat body males (Figure 2C). From eclosion to age 10 days, wildtype programmed cell death. To study adult traits, Gruntenko females produced two-fold more eggs than CAKO. Not- et al. [32] drove CA apoptosis
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