Re-Patterning Sleep Architecture in through Gustatory Perception and Nutritional Quality

English version České info

Organisms perceive changes in their dietary environment and enact a suite of behavioral and metabolic adaptations that can impact motivational behavior, disease resistance, and longevity. However, the precise nature and mechanism of these dietary responses is not known. We have uncovered a novel link between dietary factors and sleep behavior in Drosophila melanogaster. Dietary sugar rapidly altered sleep behavior by modulating the number of sleep episodes during both the light and dark phase of the circadian period, independent of an intact circadian rhythm and without affecting total sleep, latency to sleep, or waking activity. The effect of sugar on sleep episode number was consistent with a change in arousal threshold for waking. Dietary protein had no significant effect on sleep or wakefulness. Gustatory perception of sugar was necessary and sufficient to increase the number of sleep episodes, and this effect was blocked by activation of bitter-sensing neurons. Further addition of sugar to the diet blocked the effects of sweet gustatory perception through a gustatory-independent mechanism. However, gustatory perception was not required for diet-induced fat accumulation, indicating that sleep and energy storage are mechanistically separable. We propose a two-component model where gustatory and metabolic cues interact to regulate sleep architecture in response to the quantity of sugar available from dietary sources. Reduced arousal threshold in response to low dietary availability may have evolved to provide increased responsiveness to cues associated with alternative nutrient-dense feeding sites. These results provide evidence that gustatory perception can alter arousal thresholds for sleep behavior in response to dietary cues and provide a mechanism by which organisms tune their behavior and physiology to environmental cues.

Vyšlo v časopise: Re-Patterning Sleep Architecture in through Gustatory Perception and Nutritional Quality. PLoS Genet 8(5): e32767. doi:10.1371/journal.pgen.1002668
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002668

Souhrn

Zdroje

1. AlladaRSiegelJM 2008 Unearthing the phylogenetic roots of sleep. Curr Biol 18 R670 R679

2. KeeneACDuboueERMcDonaldDMDusMSuhGS 2010 Clock and cycle limit starvation-induced sleep loss in Drosophila. Curr Biol 20 1209 1215

3. MacFadyenUMOswaldILewisSA 1973 Starvation and human slow-wave sleep. J Appl Physiol 35 391 394

4. SkorupaDADervisefendicAZwienerJPletcherSD 2008 Dietary composition specifies consumption, obesity, and lifespan in Drosophila melanogaster. Aging Cell 7 478 490

5. AyresJSSchneiderDS 2009 The role of anorexia in resistance and tolerance to infections in Drosophila. PLoS Biol 7 e1000150 doi:10.1371/journal.pbio.1000150

6. PartridgeLPiperMDMairW 2005 Dietary restriction in Drosophila. Mech Ageing Dev 126 938 950

7. MairWPiperMDPartridgeL 2005 Calories do not explain extension of life span by dietary restriction in Drosophila. PLoS Biol 3 e223 doi:10.1371/journal.pbio.0030223

8. BeccutiGPannainS 2011 Sleep and obesity. Curr Opin Clin Nutr Metab Care 14 402 412

9. YouYJKimJRaizenDMAveryL 2008 Insulin, cGMP, and TGF-beta signals regulate food intake and quiescence in C. elegans: a model for satiety. Cell Metab 7 249 257

10. AntinJGibbsJHoltJYoungRCSmithGP 1975 Cholecystokinin elicits the complete behavioral sequence of satiety in rats. J Comp Physiol Psychol 89 784 790

11. MignotETaheriSNishinoS 2002 Sleeping with the hypothalamus: emerging therapeutic targets for sleep disorders. Nat Neurosci 5 Suppl 1071 1075

12. HendricksJCFinnSMPanckeriKAChavkinJWilliamsJA 2000 Rest in Drosophila is a sleep-like state. Neuron 25 129 138

13. ShawPJCirelliCGreenspanRJTononiG 2000 Correlates of sleep and waking in Drosophila melanogaster. Science 287 1834 1837

14. Ganguly-FitzgeraldIDonleaJShawPJ 2006 Waking experience affects sleep need in Drosophila. Science 313 1775 1781

15. PfeiffenbergerCLearBCKeeganKPAlladaR 2010 Locomotor activity level monitoring using the Drosophila Activity Monitoring (DAM) System. Cold Spring Harb Protoc 2010 pdb prot5518

16. ChiuJCLowKHPikeDHYildirimEEderyI 2010 Assaying locomotor activity to study circadian rhythms and sleep parameters in Drosophila. J Vis Exp

17. ZimmermanJERaizenDMMaycockMHMaislinGPackAI 2008 A video method to study Drosophila sleep. Sleep 31 1587 1598

18. GrandisonRCPiperMDPartridgeL 2009 Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 462 1061 1064

19. CirelliCBusheyD 2008 Sleep and wakefulness in Drosophila melanogaster. Ann N Y Acad Sci 1129 323 329

20. CirelliCBusheyDHillSHuberRKreberR 2005 Reduced sleep in Drosophila Shaker mutants. Nature 434 1087 1092

21. CrockerASehgalA 2008 Octopamine regulates sleep in drosophila through protein kinase A-dependent mechanisms. J Neurosci 28 9377 9385

22. KabilHKabilOBanerjeeRHarshmanLGPletcherSD 2011 Increased transsulfuration mediates longevity and dietary restriction in Drosophila. Proc Natl Acad Sci U S A

23. ZidBMRogersANKatewaSDVargasMAKolipinskiMC 2009 4E-BP extends lifespan upon dietary restriction by enhancing mitochondrial activity in Drosophila. Cell 139 149 160

24. WelteMACermelliSGrinerJVieraAGuoY 2005 Regulation of lipid-droplet transport by the perilipin homolog LSD2. Curr Biol 15 1266 1275

25. AmreinHThorneN 2005 Gustatory perception and behavior in Drosophila melanogaster. Curr Biol 15 R673 684

26. SloneJDanielsJAmreinH 2007 Sugar receptors in Drosophila. Curr Biol 17 1809 1816

27. JiaoYMoonSJMontellC 2007 A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging. Proc Natl Acad Sci U S A 104 14110 14115

28. DahanukarAFosterKvan der Goes van NatersWMCarlsonJR 2001 A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nat Neurosci 4 1182 1186

29. MarellaSFischlerWKongPAsgarianSRueckertE 2006 Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49 285 295

30. WuQZhaoZShenP 2005 Regulation of aversion to noxious food by Drosophila neuropeptide Y -⁠ and insulin-like systems. Nat Neurosci 8 1350 1355

31. MasekPScottK 2010 Limited taste discrimination in Drosophila. Proc Natl Acad Sci U S A 107 14833 14838

32. LarssonMCDomingosAIJonesWDChiappeMEAmreinH 2004 Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43 703 714

33. LibertSZwienerJChuXVanvoorhiesWRomanG 2007 Regulation of Drosophila life span by olfaction and food-derived odors. Science 315 1133 1137

34. KwonJYDahanukarAWeissLACarlsonJR 2007 The molecular basis of CO2 reception in Drosophila. Proc Natl Acad Sci U S A 104 3574 3578

35. PoonPCKuoTHLinfordNJRomanGPletcherSD 2010 Carbon dioxide sensing modulates lifespan and physiology in Drosophila. PLoS Biol 8 e1000356 doi:10.1371/journal.pbio.1000356

36. DethierVG 1976 The hungry fly: a physiological study of the behavior associated with feeding Harvard University Press

37. FujitaMTanimuraT 2011 Drosophila evaluates and learns the nutritional value of sugars. Curr Biol 21 751 755

38. BurkeCJWaddellS 2011 Remembering nutrient quality of sugar in Drosophila. Curr Biol 21 746 750

39. DusMMinSKeeneACLeeGYSuhGS 2011 Taste-independent detection of the caloric content of sugar in Drosophila. Proc Natl Acad Sci U S A 108 11644 11649

40. TempelBLBoniniNDawsonDRQuinnWG 1983 Reward learning in normal and mutant Drosophila. Proc Natl Acad Sci U S A 80 1482 1486

41. Ben ArousJLaffontSChatenayD 2009 Molecular and sensory basis of a food related two-state behavior in C. elegans. PLoS ONE 4 e7584 doi:10.1371/journal.pone.0007584

42. WuQWenTLeeGParkJHCaiHN 2003 Developmental control of foraging and social behavior by the Drosophila neuropeptide Y-like system. Neuron 39 147 161

43. KumeKKumeSParkSKHirshJJacksonFR 2005 Dopamine is a regulator of arousal in the fruit fly. J Neurosci 25 7377 7384

44. CrockerAShahidullahMLevitanIBSehgalA 2010 Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behavior. Neuron 65 670 681

45. XuKZhengXSehgalA 2008 Regulation of feeding and metabolism by neuronal and peripheral clocks in Drosophila. Cell Metab 8 289 300

46. ChatterjeeATanoueSHoulJHHardinPE 2010 Regulation of gustatory physiology and appetitive behavior by the Drosophila circadian clock. Curr Biol 20 300 309

47. KrishnanBDryerSEHardinPE 1999 Circadian rhythms in olfactory responses of Drosophila melanogaster. Nature 400 375 378

48. SeugnetLSuzukiYThimganMDonleaJGimbelSI 2009 Identifying sleep regulatory genes using a Drosophila model of insomnia. J Neurosci 29 7148 7157

49. McDonaldDMKeeneAC 2010 The sleep-feeding conflict: Understanding behavioral integration through genetic analysis in Drosophila. Aging (Albany NY) 2 519 522

50. KohKEvansJMHendricksJCSehgalA 2006 A Drosophila model for age-associated changes in sleep:wake cycles. Proc Natl Acad Sci USA 103 13843 13847

51. BusheyDHuberRTononiGCirelliC 2007 Drosophila Hyperkinetic mutants have reduced sleep and impaired memory. J Neurosci 27 5384 5393

52. KohKJoinerWJWuMNYueZSmithCJ 2008 Identification of SLEEPLESS, a sleep-promoting factor. Science 321 372 376

53. BusheyDHughesKATononiGCirelliC 2010 Sleep, aging, and lifespan in Drosophila. BMC Neurosci 11 56

54. RiemenspergerTIsabelGCoulomHNeuserKSeugnetL 2010 Behavioral consequences of dopamine deficiency in the Drosophila central nervous system. Proc Natl Acad Sci U S A 108 834 839

55. SumiyoshiMSakanakaMKimuraY 2006 Chronic intake of high-fat and high-sucrose diets differentially affects glucose intolerance in mice. J Nutr 136 582 587

56. MusselmanLPFinkJLNarzinskiKRamachandranPVHathiramaniSS 2011 A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Dis Model Mech 4 842 849

57. ZadehSSBegumK 2011 Comparison of nutrient intake by sleep status in selected adults in Mysore, India. Nutr Res Pract 5 230 235

58. GronkeSBellerMFellertSRamakrishnanHJackleH 2003 Control of fat storage by a Drosophila PAT domain protein. Curr Biol 13 603 606

59. GentlemanRCIhakaR 1996 R: A Language for Data Analysis and Graphics. Journal of Graphical and Computational Statistics 5 299 314

60. ChenQMaEBeharKLXuTHaddadGG 2002 Role of trehalose phosphate synthase in anoxia tolerance and development in Drosophila melanogaster. J Biol Chem 277 3274 3279