Disruption of Adipokinetic Hormone Mediated Energy Homeostasis Has Subtle Effects on Physiology, Behavior and Lipid Status During Aging in Drosophila
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
30079029
PubMed Central
PMC6062650
DOI
10.3389/fphys.2018.00949
Knihovny.cz E-zdroje
- Klíčová slova
- AKH signaling, adipokinetic hormone, aging, energy homeostasis, lipid status, senescence,
- Publikační typ
- časopisecké články MeSH
The impact of disruption of adipokinetic hormone (AKH) signaling was studied during aging in Drosophila in a sexually dimorphic manner. A mutant (Akh1) producing a non-functional AKH peptide was compared with isogenized wild-type controls (w1118), and Akh-rescue line where AKH was ectopically expressed in the mutant background (EE-Akh). Longevity, fecundity, and locomotor activity rhythms remained unaffected by lack of AKH signaling. While the strength of rhythms declined in general with age across all fly lines tested this was more so in case of Akh1 flies. Negative geotaxis was significantly impaired in Akh1 flies. Only young Akh1 flies of both sexes and old Akh1 females showed significantly higher body weight compared to age-matched iso-control flies (except in case of EE-Akh). Expression of genes involved in energy homeostasis and aging indicated that dTOR and Akt expression were elevated in Akh1 flies compared to other genotypes, whereas AMPK and dFoxO expression levels were significantly reduced. Multivariate analysis of the distribution of lipid species revealed a significant accumulation of specific diglyceride (DG) and triglyceride (TG) lipid species, irrespective of sex, attributable in part due to lack of AKH. Moreover, irrespective of lack of AKH, older flies of all genotypes accumulated TGs. Taken together, the results strongly suggest that disruption of AKH has very subtle effects on physiology, behavior and lipid status during aging.
Biology Centre Institute of Entomology Academy of Sciences České Budějovice Czechia
Biology Centre Institute of Parasitology Academy of Sciences České Budějovice Czechia
Faculty of Science University of South Bohemia České Budějovice Czechia
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Baumbach J., Hummel P., Bickmeyer I., Kowalczyk K. M., Frank M., Knorr K., et al. (2014a). A Drosophila in vivo screen identifies store-operated calcium entry as a key regulator of adiposity. Cell Metab. 19 331–343. 10.1016/j.cmet.2013.12.004 PubMed DOI
Baumbach J., Xu Y., Hehlert P., Kühnlein R. P. (2014b). Gαq, Gγ1 and Plc21C control Drosophila body fat storage. J. Genet. Genomics 41 283–292. 10.1016/j.jgg.2014.03.005 PubMed DOI
Bednářová A. Kodrík D., Krishnan N. (2013). Unique roles of glucagon and glucagon-like peptides: parallels in understanding the functions of adipokinetic hormones in stress responses in insects. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 164 91–100. 10.1016/j.cbpa.2012.10.012 PubMed DOI
Bednářová A. Kodrík D., Krishnan N. (2015). Knockdown of adipokinetic hormone synthesis increases susceptibility to oxidative stress in Drosophila–a role for dFoxO? Comp. Biochem. Physiol. C Toxicol. Pharmacol. 171 8–14. 10.1016/j.cbpc.2015.03.006 PubMed DOI
Bharucha K. N., Tarr P., Zipursky S. L. (2008). A glucagon-like endocrine pathway in Drosophila modulates both lipid and carbohydrate homeostasis. J. Exp. Biol. 211 3103–3110. 10.1242/jeb.016451 PubMed DOI PMC
Braco J. T., Gillespie E. L., Alberto G. E., Brenman J. E., Johnson E. C. (2012). Energy-dependent modulation of glucagon-like signaling in Drosophila via the AMP-activated protein kinase. Genetics 192 457–466. 10.1534/genetics.112.143610 PubMed DOI PMC
Broughton S. J., Piper M. D., Ikeya T., Bass T. M., Jacobson J., Driege Y., et al. (2005). Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc. Natl. Acad. Sci. U.S.A. 102 3105–3110. 10.1073/pnas.0405775102 PubMed DOI PMC
Brunet A., Sweeney L. B., Sturgill J. F., Chua K. F., Greer P. L., Lin Y., et al. (2004). Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303 2011–2015. 10.1126/science.1094637 PubMed DOI
Caers J., Peeters L., Janssen T., De Haes W., Gade G., Schoofs L. (2012). Structure-activity studies of Drosophila adipokinetic hormone (AKH) by a cellular expression system of dipteran AKH receptors. Gen. Comp. Endocrinol. 177 332–337. 10.1016/j.ygcen.2012.04.025 PubMed DOI
Carlisle J., Loughton B. G. (1986). The inhibition of protein synthesis in Locusta migratoria by adipokinetic hormone. J. Insect Physiol. 32 573–578. 10.1016/0022-1910(86)90074-0 DOI
Carter M. E., Brunet A. (2007). FOXO transcription factors. Curr. Biol. 17 R113–R114. 10.1016/j.cub.2007.01.008 PubMed DOI
Demontis F., Perrimon N. (2010). FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 143 813–825. 10.1016/j.cell.2010.10.007 PubMed DOI PMC
Folch J., Lees M., Stanley G. H. S. (1957). A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226 497–509. PubMed
Fuentes E. N., Safian D., Einarsdottir I. E., Valdés J. A., Elorza A. A., Molina A., et al. (2013). Nutritional status modulates plasma leptin, AMPK and TOR activation, and mitochondrial biogenesis: implications for cell metabolism and growth in skeletal muscle of the fine flounder. Gen. Comp. Endocrinol. 186 172–180. 10.1016/j.ygcen.2013.02.009 PubMed DOI
Furukawa-Hibi Y., Kobayashi Y., Chen C., Motoyama N. (2005). FOXO transcription factors in cell-cycle regulation and the response to oxidative stress. Antioxid. Redox Signal. 7 752–760. 10.1089/ars.2005.7.752 PubMed DOI
Gäde G., Hoffmann K. H., Spring J. H. (1997). Hormonal regulation in insects: facts, gaps, and future directions. Physiol. Rev. 77 963–1032. 10.1152/physrev.1997.77.4.963 PubMed DOI
Gáliková M., Diesner M., Klepsatel P., Hehlert P., Xu Y., Bickmeyer I., et al. (2015). Energy homeostasis control in Drosophila adipokinetic hormone mutants. Genetics 201 665–683. 10.1534/genetics.115.178897 PubMed DOI PMC
Gáliková M., Klepsatel P., Xu Y., Kuhnlein R. P. (2017). The obesity related adipokinetic hormone controls feeding and expression of neuropeptide regulators of Drosophila metabolism. Eur. J. Lipid Sci. Technol. 119:1600138 10.1002/ejlt.201600138 DOI
Gargano J. W., Martin I., Bhandari P., Grotewiel M. S. (2005). Rapid iterative negative geotaxis (RING): a new method for assessing age-related locomotor decline in Drosophila. Exp. Gerontol. 40 386–395. 10.1016/j.exger.2005.02.005 PubMed DOI
Giannakou M. E., Goss M., Partridge L. (2008). Role of dFOXO in lifespan extension by dietary restriction in Drosophila melanogaster: not required, but its activity modulates the response. Aging Cell 7 187–198. 10.1111/j.1474-9726.2007.00362.x PubMed DOI
Glauser D. A., Schlegel W. (2007). The emerging role of FOXO transcription factors in pancreatic beta cells. J. Endocrinol. 193 195–207. 10.1677/JOE-06-0191 PubMed DOI
Greer E. L., Brunet A. (2008). FOXO transcription factors in ageing and cancer. Acta Physiol. 192 19–28. 10.1111/j.1748-1716.2007.01780.x PubMed DOI
Grönke S., Clarke D.-F., Broughton S., Andrews T. D., Partridge L. (2010). Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet. 6:e1000857. 10.1371/journal.pgen.1000857 PubMed DOI PMC
Grönke S., Mildner A., Fellert S., Tennagels N., Petry S., Müller G., et al. (2005). Brummer lipase is an evolutionary conserved fat storage regulator in Drosophila. Cell Metab. 1 323–330. 10.1016/j.cmet.2005.04.003 PubMed DOI
Grönke S., Müller G., Hirsch J., Fellert S., Andreou A., Haase T., et al. (2007). Dual lipolytic control of body fat storage and mobilization in Drosophila. PLoS Biol. 5:e137. 10.1371/journal.pbio.0050137 PubMed DOI PMC
Isabel G., Martin J.-R., Chidami S., Veenstra J. A., Rosay P. (2005). AKH-producing neuroendocrine cell ablation decreases trehalose and induces behavioral changes in Drosophila. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288 R531–R538. 10.1152/ajpregu.00158.2004 PubMed DOI
Jones B. J., Tan T., Bloom S. R. (2012). Minireview: glucagon in stress and energy homeostasis glucagon as a stress hormone. Endocrinology 153 1049–1054. 10.1210/en.2011-1979 PubMed DOI PMC
Kahn B. B., Alquier T., Carling D., Hardie D. G. (2005). AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 1 15–25. 10.1016/j.cmet.2004.12.003 PubMed DOI
Kim J., Neufeld T. P. (2015). Dietary sugar promotes systemic TOR activation in Drosophila through AKH-dependent selective secretion of Dilp3. Nat. Commun. 6:6846. 10.1038/ncomms7846 PubMed DOI PMC
Kim S. K., Rulifson E. J. (2004). Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 431 316–320. 10.1038/nature02897 PubMed DOI
Kodrík D. Bednářová A. Zemanová M., Krishnan N. (2015). Hormonal regulation of response to oxidative stress in insects - an update. Int. J. Mol. Sci. 16 25788–25816. 10.3390/ijms161025788 PubMed DOI PMC
Koštál V., Šimek P. (1998). Changes in fatty acid composition of phospholipids and triacylglycerols after cold-acclimation of an aestivating insect prepupa. J. Comp. Physiol. B 168 453–460. 10.1007/s003600050165 DOI
Krishnan N., Kretzchmar D., Rakshit K., Chow E., Giebultowicz J. M. (2009). The circadian clock gene period extends healthspan in aging Drosophila melanogaster. Aging 1 937–948. 10.18632/aging.100103 PubMed DOI PMC
Lee G., Park J. H. (2004). Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster. Genetics 167 311–323. 10.1534/genetics.167.1.311 PubMed DOI PMC
Lin L., Hron J. D., Peng S. L. (2004). Regulation of NF-κB, Th activation, and autoinflammation by the forkhead transcription factor Foxo3a. Immunity 21 203–213. 10.1016/j.immuni.2004.06.016 PubMed DOI
Lindemans M., Liu F., Janssen T., Husson S. J., Mertens I., Gäde G., et al. (2009). Adipokinetic hormone signaling through the gonadotropin-releasing hormone receptor modulates egg-laying in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 106 1642–1647. 10.1073/pnas.0809881106 PubMed DOI PMC
Livak K. J., Schmittgen T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25 402–408. 10.1006/meth.2001.1262 PubMed DOI
López-Otín C., Blasco M. A., Partridge L., Serrano M., Kroemer G. (2013). The hallmarks of aging. Cell 153 1194–1217. 10.1016/j.cell.2013.05.039 PubMed DOI PMC
Lorenz M. W., Anand A. N. (2004). Changes in the biochemical composition of fat body stores during adult development of female crickets, Gryllus bimaculatus. Arch. Insect Biochem. Physiol. 56 110–119. 10.1002/arch.20002 PubMed DOI
Lorenz M. W., Gäde G. (2009). Hormonal regulation of energy metabolism in insects as a driving force for performance. Integr. Comp. Biol. 49 380–392. 10.1093/icb/icp019 PubMed DOI
Ma Q. (2010). Transcriptional responses to oxidative stress: pathological and toxicological implications. Pharmacol. Ther. 125 376–393. 10.1016/j.pharmthera.2009.11.004 PubMed DOI
Min K. J., Yamamoto R., Buch S., Pankratz M., Tatar M. (2008). Drosophila lifespan control by dietary restriction independent of insulin-like signaling. Aging Cell 7 199–206. 10.1111/j.1474-9726.2008.00373.x PubMed DOI PMC
Moshitzky P., Applebaum S. W. (1990). The role of adipokinetic hormone in the control of vitellogenins in locusts. Insect Biochem. 20 319–323. 10.1016/0020-1790(90)90050-5 DOI
Murphy M. P., Partridge L. (2008). Toward a control theory analysis of aging. Annu. Rev. Biochem. 77 777–798. 10.1146/annurev.biochem.77.070606.101605 PubMed DOI PMC
Nakae J., Oki M., Cao Y. (2008). The FoxO transcription factors and metabolic regulation. FEBS Lett. 582 54–67. 10.1016/j.febslet.2007.11.025 PubMed DOI
Noyes B. E., Katz F. N., Schaffer M. H. (1995). Identification and expression of the Drosophila adipokinetic hormone gene. Mol. Cell. Endocrinol. 109 133–141. 10.1016/0303-7207(95)03492-P PubMed DOI
Peng S. (2008). Foxo in the immune system. Oncogene 27 2337–2344. 10.1038/onc.2008.26 PubMed DOI
Pfeiffenberger C., Lear B. C., Keegan K. P., Allada R. (2010). Locomotor activity level monitoring using the Drosophila activity monitoring (DAM) System. Cold Spring Harb. Protoc. 2010:db.rot5518. 10.1101/pdb.prot5518 PubMed DOI
Rajan A., Perrimon N. (2011). Drosophila as a model for interorgan communication: lessons from studies on energy homeostasis. Dev. Cell 21 29–31. 10.1016/j.devcel.2011.06.034 PubMed DOI PMC
Rando T. A., Chang H. Y. (2012). Aging, rejuvenation, and epigenetic reprogramming: resetting the aging clock. Cell 148 46–57. 10.1016/j.cell.2012.01.003 PubMed DOI PMC
Rulifson E. J. (2002). Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296 1118–1120. 10.1126/science.1070058 PubMed DOI
Sajwan S., Sidorov R., Stašková T., Žaloudíková A., Takasu Y., Kodrík D., et al. (2015). Targeted mutagenesis and functional analysis of adipokinetic hormone-encoding gene in Drosophila. Insect Biochem. Mol. Biol. 61 79–86. 10.1016/j.ibmb.2015.01.011 PubMed DOI
Schaffer M. H., Noyes B. E., Slaughter C. A., Thorne G. C., Gaskell S. J. (1990). The fruitfly Drosophila melanogaster contains a novel charged adipokinetic-hormone-family peptide. Biochem. J. 269 315–320. 10.1042/bj2690315 PubMed DOI PMC
Tatar M., Bartke A., Antebi A. (2003). The endocrine regulation of aging by insulin-like signals. Science 299 1346–1351. 10.1126/science.1081447 PubMed DOI
Tomčala A., Kyselová V., Schneedorferová I., Opekarová I., Moos M., Urajová P., et al. (2017). Separation and identification of lipids in the photosynthetic cousins of Apicomplexa Chromera velia and Vitrella brassicaformis. J. Sep. Sci. 40 3402–3413. 10.1002/jssc.201700171 PubMed DOI
Umezaki Y., Yoshii T., Kawaguchi T., Helfrich-Förster C., Tomioka K. (2012). Pigment-dispersing factor is involved in age-dependent rhythm changes in Drosophila melanogaster. J. Biol. Rhythms 27 423–432. 10.1177/0748730412462206 PubMed DOI
Wang L., Karpac J., Jasper H. (2014). Promoting longevity by maintaining metabolic and proliferative homeostasis. J. Exp. Biol. 217 109–118. 10.1242/jeb.089920 PubMed DOI PMC
Zemanová M., Stašková T., Kodrík D. (2016). Role of adipokinetic hormone and adenosine in the anti-stress response in Drosophila melanogaster. J. Insect Physiol. 91 39–47. 10.1016/j.jinsphys.2016.06.010 PubMed DOI