AKH-FOXO pathway regulates starvation-induced sleep loss through remodeling of the small ventral lateral neuron dorsal projections


Autoři: Qiankun He aff001;  Juan Du aff001;  Liya Wei aff002;  Zhangwu Zhao aff001
Působiště autorů: Department of Entomology and MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, China aff001;  College of Life Science, Hebei University, Baoding, China aff002
Vyšlo v časopise: AKH-FOXO pathway regulates starvation-induced sleep loss through remodeling of the small ventral lateral neuron dorsal projections. PLoS Genet 16(10): e1009181. doi:10.1371/journal.pgen.1009181
Kategorie: Research Article
doi: 10.1371/journal.pgen.1009181

Souhrn

Starvation caused by adverse feeding stresses or food shortages has been reported to result in sleep loss in animals. However, how the starvation signal interacts with the central nervous system is still unknown. Here, the adipokinetic hormone (AKH)—Fork head Box-O (FOXO) pathway is shown to respond to energy change and adjust the sleep of Drosophila through remodeling of the s-LNv (small ventral lateral neurons) dorsal projections. Our results show that starvation prevents flies from going to sleep after the first light-dark transition. The LNvs are required for starvation-induced sleep loss through extension of the pigment dispersing factor (PDF)-containing s-LNv dorsal projections. Further studies reveal that loss of AKH or AKHR (akh receptor) function blocks starvation-induced extension of s-LNv dorsal projections and rescues sleep suppression during food deprivation. FOXO, which has been reported to regulate synapse plasticity of neurons, acts as starvation response factor downstream of AKH, and down regulation of FOXO level considerably alleviates the influence of starvation on s-LNv dorsal projections and sleep. Taking together, our results outline the transduction pathways between starvation signal and sleep, and reveal a novel functional site for sleep regulation.

Klíčová slova:

Analysis of variance – Behavior – Drosophila melanogaster – Fats – Food – Immunofluorescence – Neurons – Sleep


Zdroje

1. Méndez G, Wieser W. Metabolic responses to food deprivation and refeeding in juveniles of Rutilus rutilus, (Teleostei: Cyprinidae). Environmental Biology of Fishes 1993;36(1):73–81.

2. McCue MD. Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A Mol Integr Physiol. 2010;156(1):1–18. doi: 10.1016/j.cbpa.2010.01.002 20060056.

3. Wang B, Moya N, Niessen S, Hoover H, Mihaylova MM, Shaw RJ, et al. A hormone-dependent module regulating energy balance. Cell. 2011;145(4):596–606. doi: 10.1016/j.cell.2011.04.013 21565616; PubMed Central PMCID: PMC3129781.

4. Grönke S, Müller G, Hirsch J, Fellert S, Andreou A, Haase T, et al. Dual lipolytic control of body fat storage and mobilization in Drosophila. PLoS biology. 2007;5(6):e137. doi: 10.1371/journal.pbio.0050137 17488184

5. Taghert PH, Choi S, Lim D-S, Chung J. Feeding and Fasting Signals Converge on the LKB1-SIK3 Pathway to Regulate Lipid Metabolism in Drosophila. PLoS genetics. 2015;11(5):e1005263. doi: 10.1371/journal.pgen.1005263 25996931

6. Gyunghee L, Park JH. Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster. Genetics. 2004;167(1):311–23. doi: 10.1534/genetics.167.1.311 15166157

7. Keene AC, Duboue ER, McDonald DM, Dus M, Suh GS, Waddell S, et al. Clock and cycle limit starvation-induced sleep loss in Drosophila. Current biology: CB. 2010;20(13):1209–15. doi: 10.1016/j.cub.2010.05.029 20541409; PubMed Central PMCID: PMC2929698.

8. Yang Z, Yu Y, Zhang V, Tian Y, Qi W, Wang L. Octopamine mediates starvation-induced hyperactivity in adult Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(16):5219–24. doi: 10.1073/pnas.1417838112 25848004; PubMed Central PMCID: PMC4413307.

9. Yu Y, Huang R, Ye J, Zhang V, Wu C, Guo C, et al. Regulation of starvation-induced hyperactivity by insulin and glucagon signaling in adultDrosophila. eLife,5,(2016-09-08). 2016;5.

10. Murakami K, Yurgel ME, Stahl BA, Masek P, Mehta A, Heidker R, et al. translin Is Required for Metabolic Regulation of Sleep. Current biology: CB. 2016;26(7):972–80. doi: 10.1016/j.cub.2016.02.013 27020744; PubMed Central PMCID: PMC4846466.

11. Chung BY, Ro J, Hutter SA, Miller KM, Guduguntla LS, Kondo S, et al. Drosophila Neuropeptide F Signaling Independently Regulates Feeding and Sleep-Wake Behavior. Cell Reports. 2017;19(12):2441. doi: 10.1016/j.celrep.2017.05.085 28636933

12. Sonn JY, Lee J, Sung MK, Ri H, Choi JK, Lim C, et al. Serine metabolism in the brain regulates starvation-induced sleep suppression in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America. 2018;115(27):7129–34. doi: 10.1073/pnas.1719033115 29915051; PubMed Central PMCID: PMC6142195.

13. Yurgel ME, Kakad P, Zandawala M, Nassel DR, Godenschwege TA, Keene AC. A single pair of leucokinin neurons are modulated by feeding state and regulate sleep-metabolism interactions. PLoS biology. 2019;17(2):e2006409. doi: 10.1371/journal.pbio.2006409 30759083; PubMed Central PMCID: PMC6391015.

14. Borbely AA. A two process model of sleep regulation. Human Neuuobioloqy. 1982;(1): 195–204 7185792

15. Artiushin G, Sehgal A. The Drosophila circuitry of sleep-wake regulation. Current opinion in neurobiology. 2017;44:243–50. doi: 10.1016/j.conb.2017.03.004 28366532.

16. Bringmann H. Sleep-Active Neurons: Conserved Motors of Sleep. Genetics. 2018;208(4):1279–89. doi: 10.1534/genetics.117.300521 29618588; PubMed Central PMCID: PMC5887131.

17. Xu K, Zheng X, Sehgal A. Regulation of feeding and metabolism by neuronal and peripheral clocks in Drosophila. Cell metabolism. 2008;8(4):289–300. doi: 10.1016/j.cmet.2008.09.006 18840359; PubMed Central PMCID: PMC2703740.

18. Guo F, Yu J, Jung HJ, Abruzzi KC, Luo W, Griffith LC, et al. Circadian neuron feedback controls the Drosophila sleep—activity profile. Nature. 2016;536(7616):292–7. doi: 10.1038/nature19097 27479324; PubMed Central PMCID: PMC5247284.

19. Chung BY, Kilman VL, Keath JR, Pitman JL, Allada R. The GABA(A) receptor RDL acts in peptidergic PDF neurons to promote sleep in Drosophila. Current biology: CB. 2009;19(5):386–90. doi: 10.1016/j.cub.2009.01.040 19230663; PubMed Central PMCID: PMC3209479.

20. Yao Z, Shafer OT. The Drosophila circadian clock is a variably coupled network of multiple peptidergic units. Science. 2014;343(6178):1516–20. doi: 10.1126/science.1251285 24675961; PubMed Central PMCID: PMC4259399.

21. Heekeren HR, Marrett S, Bandettini PA, Ungerleider LG. A general mechanism for perceptual decision-making in the human brain. Nature. 2004;431(7010):859–62. doi: 10.1038/nature02966 15483614.

22. Guo F, Cerullo I, Chen X, Rosbash M. PDF neuron firing phase-shifts key circadian activity neurons in Drosophila. eLife,3,(2014-06-16). 2014;3(3):e02780. doi: 10.7554/eLife.02780 24939987

23. Cavanaugh DJ, Geratowski JD, Wooltorton JR, Spaethling JM, Hector CE, Zheng X, et al. Identification of a circadian output circuit for rest:activity rhythms in Drosophila. Cell. 2014;157(3):689–701. doi: 10.1016/j.cell.2014.02.024 24766812; PubMed Central PMCID: PMC4003459.

24. Seluzicki A, Flourakis M, Kula-Eversole E, Zhang L, Kilman V, Allada R. Dual PDF signaling pathways reset clocks via TIMELESS and acutely excite target neurons to control circadian behavior. PLoS biology. 2014;12(3):e1001810. doi: 10.1371/journal.pbio.1001810 24643294; PubMed Central PMCID: PMC3958333.

25. Fernández MP, Berni J, Ceriani MF. Circadian remodeling of neuronal circuits involved in rhythmic behavior. PLoS biology. 2008;6(3):e69. doi: 10.1371/journal.pbio.0060069 18366255

26. Pirooznia SK, Kellie C, Chan MT, Zimmerman JE, Felice E. Epigenetic regulation of axonal growth of Drosophila pacemaker cells by histone acetyltransferase tip60 controls sleep. Genetics. 2012;192(4):1327–45. doi: 10.1534/genetics.112.144667 22982579

27. Sivachenko A, Li Y, Abruzzi KC, Rosbash M. The transcription factor Mef2 links the Drosophila core clock to Fas2, neuronal morphology, and circadian behavior. Neuron. 2013;79(2):281–92. doi: 10.1016/j.neuron.2013.05.015 23889933; PubMed Central PMCID: PMC3859024.

28. Chen X, Rosbash M. MicroRNA-92a is a circadian modulator of neuronal excitability in Drosophila. Nature communications. 2017;8:14707. doi: 10.1038/ncomms14707 28276426; PubMed Central PMCID: PMC5347142.

29. Nian X, Chen W, Bai W, Zhao Z, Zhang Y. miR-263b Controls Circadian Behavior and the Structural Plasticity of Pacemaker Neurons by Regulating the LIM-Only Protein Beadex. Cells. 2019;8(8). doi: 10.3390/cells8080923 31426557; PubMed Central PMCID: PMC6721658.

30. Sajwan S, Sidorov R, Staskova T, Zaloudikova A, Takasu Y, Kodrik D, et al. Targeted mutagenesis and functional analysis of adipokinetic hormone-encoding gene in Drosophila. Insect biochemistry and molecular biology. 2015;61:79–86. doi: 10.1016/j.ibmb.2015.01.011 25641265.

31. Martina G, Max D, Peter K, Philip H, Yanjun X, Iris B, et al. Energy Homeostasis Control in Drosophila Adipokinetic Hormone Mutants. Genetics. 2015;201(2):665–83. doi: 10.1534/genetics.115.178897 26275422

32. Bednarova A, Kodrik D, Krishnan N. Knockdown of adipokinetic hormone synthesis increases susceptibility to oxidative stress in Drosophila—a role for dFoxO? Comp Biochem Physiol C Toxicol Pharmacol. 2015;171:8–14. doi: 10.1016/j.cbpc.2015.03.006 25814322.

33. Collins B, Kane EA, Reeves DC, Akabas MH, Blau J. Balance of activity between LN(v)s and glutamatergic dorsal clock neurons promotes robust circadian rhythms in Drosophila. Neuron. 2012;74(4):706–18. doi: 10.1016/j.neuron.2012.02.034 22632728; PubMed Central PMCID: PMC3361687.

34. Fujii S, Emery P, Amrein H. SIK3-HDAC4 signaling regulates Drosophila circadian male sex drive rhythm via modulating the DN1 clock neurons. Proceedings of the National Academy of Sciences of the United States of America. 2017;114(32):E6669. doi: 10.1073/pnas.1620483114 28743754

35. Hong SH, Lee KS, Kwak SJ, Kim AK, Bai H, Jung MS, et al. Minibrain/Dyrk1a regulates food intake through the Sir2-FOXO-sNPF/NPY pathway in Drosophila and mammals. PLoS genetics. 2012;8(8):e1002857. doi: 10.1371/journal.pgen.1002857 22876196; PubMed Central PMCID: PMC3410862.

36. McLaughlin CN, Nechipurenko IV, Liu N, Broihier HT. A Toll receptor-FoxO pathway represses Pavarotti/MKLP1 to promote microtubule dynamics in motoneurons. The Journal of cell biology. 2016;214(4):459–74. doi: 10.1083/jcb.201601014 27502486; PubMed Central PMCID: PMC4987293.

37. Nechipurenko IV, Broihier HT. FoxO limits microtubule stability and is itself negatively regulated by microtubule disruption. The Journal of cell biology. 2012;196(3):345–62. doi: 10.1083/jcb.201105154 22312004; PubMed Central PMCID: PMC3275378.

38. Mahoney RE, Azpurua J, Eaton B. Insulin signaling controls neurotransmission via the 4eBP-dependent modification of the exocytotic machinery. eLife,5,(2016-08-14). 2016;5. doi: 10.7554/eLife.16807 27525480

39. Depetris-Chauvin A, Fernandez-Gamba A, Gorostiza EA, Herrero A, Castano EM, Ceriani MF. Mmp1 processing of the PDF neuropeptide regulates circadian structural plasticity of pacemaker neurons. PLoS genetics. 2014;10(10):e1004700. doi: 10.1371/journal.pgen.1004700 25356918; PubMed Central PMCID: PMC4214601.

40. Koh H, Kim H, Kim MJ, Park J, Lee HJ, Chung J. Silent information regulator 2 (Sir2) and Forkhead box O (FOXO) complement mitochondrial dysfunction and dopaminergic neuron loss in Drosophila PTEN-induced kinase 1 (PINK1) null mutant. The Journal of biological chemistry. 2012;287(16):12750–8. doi: 10.1074/jbc.M111.337907 22378780; PubMed Central PMCID: PMC3339960.

41. Clocchiatti A, Di Giorgio E, Demarchi F, Brancolini C. Beside the MEF2 axis: unconventional functions of HDAC4. Cellular signalling. 2013;25(1):269–76. doi: 10.1016/j.cellsig.2012.10.002 23063464.


Článek vyšel v časopise

PLOS Genetics


2020 Číslo 10

Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Antiseptika a prevence ve stomatologii
nový kurz
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Diagnostika a léčba deprese pro ambulantní praxi
Autoři: MUDr. Jan Hubeňák, Ph.D

Snímatelné zubní náhrady a fixační krémy
Autoři: doc. MUDr. Hana Hubálková, Ph.D.

Nová éra v léčbě migrény
Autoři: MUDr. Eva Medová, MUDr. Tomáš Nežádal, Ph.D.

Význam nutraceutik u kardiovaskulárních onemocnění
Autoři:

Všechny kurzy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se