Genetic dissection of sleep–metabolism interactions in the fruit fly

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 201, Issue 9, 2015, Pages 869-877

  Yurgel, Maria E ^a   Masek, Pavel ^a   DiAngelo, Justin ^b   Keene, Alex C ^a  

^a UNIVERSITY OF NEVADA   (United States)

^b HOFSTRA UNIVERSITY   (United States)

Author keywords

Circadian; Drosophila; Feeding; Metabolism; Sleep

Indexed keywords

HORMONE;

ANIMAL; DROSOPHILA MELANOGASTER; GENETICS; METABOLISM; PHYSIOLOGY; SLEEP;

ANIMALS; DROSOPHILA MELANOGASTER; HORMONES; METABOLISM; SLEEP;

EID: 84940702136     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-014-0936-9     Document Type: Review

References (108)

1. Agosto J, Choi JC, Parisky KM, et al. (2009) NIH Public Access. 11:354–359. doi:10.1038/nn2046.Modulation
2. Ahima RS, Lazar MA (2008) Adipokines and the peripheral and neural control of energy balance. Mol Endocrinol 22:1023–1031. doi:10.1210/me.2007-0529
3. Akalal D-BG, Yu D, Davis RL (2011) The long-term memory trace formed in the Drosophila α/β mushroom body neurons is abolished in long-term memory mutants. J Neurosci 31:5643–5647. doi:10.1523/JNEUROSCI.3190-10.2011
4. Atkinson W, Shorrocks B (1977) Breeding site specificity in the domestic species of Drosophila. Oecologia 29:223–232. doi:10.1007/BF00345697
5. Barf RP, Desprez T, Meerlo P, Scheurink AJW (2012) Increased food intake and changes in metabolic hormones in response to chronic sleep restriction alternated with short periods of sleep allowance. Am J Physiol Regul Integr Comp Physiol 302:R112–R117. doi:10.1152/ajpregu.00326.2011
6. Bharucha KN, Tarr P, Zipursky SL (2008) A glucagon-like endocrine pathway in Drosophila modulates both lipid and carbohydrate homeostasis. J Exp Biol 211:3103–3110. doi:10.1242/jeb.016451
7. Britton JS, Edgar BA (1998) Environmental control of the cell cycle in Drosophila: nutrition activates mitotic and endoreplicative cells by distinct mechanisms. Development 125:2149–2158
8. Britton JS, Lockwood WK, Li L et al (2002) Drosophila’s insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev Cell 2:239–249
9. Brogiolo W, Stocker H, Ikeya T et al (2001) An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr Biol 11:213–221
10. Broughton SJ, Piper MDW, Ikeya T et al (2005) Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci USA 102:3105–3110. doi:10.1073/pnas.0405775102
11. Broughton SJ, Slack C, Alic N et al (2010) DILP-producing median neurosecretory cells in the Drosophila brain mediate the response of lifespan to nutrition. Aging Cell 9:336–346. doi:10.1111/j.1474-9726.2010.00558.x
12. Burke CJ, Huetteroth W, Owald D et al (2012) Layered reward signalling through octopamine and dopamine in Drosophila. Nature 492:433–437. doi:10.1038/nature11614
13. Burt J, Dube L, Thibault L, Gruber R (2014) Sleep and eating in childhood: a potential behavioral mechanism underlying the relationship between poor sleep and obesity. Sleep Med 15:71–75. doi:10.1016/j.sleep.2013.07.015
14. Busch S, Selcho M, Ito K, Tanimoto H (2009) A map of octopaminergic neurons in the Drosophila brain. J Comp Neurol 513:643–667. doi:10.1002/cne.21966
15. Canavoso LE, Jouni ZE, Karnas KJ et al (2001) Fat metabolism in insects. Annu Rev Nutr 21:23–46. doi:10.1146/annurev.nutr.21.1.23
16. Carhan A, Tang K, Shirras CA et al (2011) Loss of Angiotensin-converting enzyme-related (ACER) peptidase disrupts night-time sleep in adult Drosophila melanogaster. J Exp Biol 214:680–686. doi:10.1242/jeb.049353
17. Catterson JH, Knowles-Barley S, James K et al (2010) Dietary modulation of Drosophila sleep-wake behaviour. PLoS ONE 5:e12062. doi:10.1371/journal.pone.0012062
18. Cavanaugh DJ, Geratowski JD, Wooltorton JRA et al (2014) Identification of a circadian output circuit for rest:activity rhythms in Drosophila. Cell 157:689–701. doi:10.1016/j.cell.2014.02.024
19. Chapman T, Partridge L (1996) Female fitness in Drosophila melanogaster: an interaction between the effect of nutrition and of encounter rate with males. Proc Biol Sci 263:755–759. doi:10.1098/rspb.1996.0113
20. Chaput J-P, Després J-P, Bouchard C, Tremblay A (2007) Association of sleep duration with type 2 diabetes and impaired glucose tolerance. Diabetologia 50:2298–2304. doi:10.1007/s00125-007-0786-x
21. Claridge-Chang A, Roorda RD, Vrontou E et al (2009) Writing memories with light-addressable reinforcement circuitry. Cell 139:405–415. doi:10.1016/j.cell.2009.08.034
22. Crocker A, Sehgal A (2008) Octopamine regulates sleep in drosophila through protein kinase A-dependent mechanisms. J Neurosci 28:9377–9385. doi:10.1523/JNEUROSCI.3072-08a.2008
23. Crocker A, Shahidullah M, Levitan IB, Sehgal A (2010) Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behavior. Neuron 65:670–681. doi:10.1016/j.neuron.2010.01.032
24. Dahanukar A, Lei Y-T, Kwon JY, Carlson JR (2007) Two Gr genes underlie sugar reception in Drosophila. Neuron 56:503–516. doi:10.1016/j.neuron.2007.10.024
25. Danguir J, Nicolaidis S (1979) Dependence of sleep on nutrients’ availability. Physiol Behav 22:735–740
26. Davis RL (2011) Traces of Drosophila memory. Neuron 70:8–19. doi:10.1016/j.neuron.2011.03.012
27. DiAngelo JR, Birnbaum MJ (2009) Regulation of fat cell mass by insulin in Drosophila melanogaster. Mol Cell Biol 29:6341–6352. doi:10.1128/MCB.00675-09
28. Donelson NC, Donelson N, Kim EZ et al (2012) High-resolution positional tracking for long-term analysis of Drosophila sleep and locomotion using the “tracker” program. PLoS ONE 7:e37250. doi:10.1371/journal.pone.0037250
29. Donlea JM, Thimgan MS, Suzuki Y et al (2011) Inducing sleep by remote control facilitates memory consolidation in Drosophila. Science 332:1571–1576. doi:10.1126/science.1202249
30. Donlea J, Leahy A, Thimgan MS et al (2012) Foraging alters resilience/vulnerability to sleep disruption and starvation in Drosophila. Proc Natl Acad Sci USA 109:2613–2618. doi:10.1073/pnas.1112623109
31. Donlea JM, Pimentel D, Miesenböck G (2014) Neuronal machinery of sleep homeostasis in Drosophila. Neuron 81:860–872. doi:10.1016/j.neuron.2013.12.013
32. Dus M, Min S, Keene AC, et al. (2011) Taste-independent detection of the caloric content of sugar in Drosophila. 2–7. doi: 10.1073/pnas.1017096108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1017096108
33. Edgar BA (2006) How flies get their size: genetics meets physiology. Nat Rev Genet 7:907–916. doi:10.1038/nrg1989
34. Erion R, DiAngelo JR, Crocker A, Sehgal A (2012) Interaction between sleep and metabolism in Drosophila with altered octopamine signaling. J Biol Chem 287:32406–32414. doi:10.1074/jbc.M112.360875
35. Fernandez R, Tabarini D, Azpiazu N et al (1995) The Drosophila insulin receptor homolog: a gene essential for embryonic development encodes two receptor isoforms with different signaling potential. EMBO J 14:3373–3384
36. Foltenyi K, Greenspan RJ, Newport JW (2007) Activation of EGFR and ERK by rhomboid signaling regulates the consolidation and maintenance of sleep in Drosophila. Nat Neurosci 10:1160–1167. doi:10.1038/nn1957
37. Froy O, Miskin R (2010) Effect of feeding regimens on circadian rhythms: implications for aging and longevity. Aging (Albany NY) 2:7–27
38. Gilestro GF (2012) Video tracking and analysis of sleep in Drosophila melanogaster. Nat Protoc 7:995–1007. doi:10.1038/nprot.2012.041
39. Good TP, Tatar M (2001) Age-specific mortality and reproduction respond to adult dietary restriction in Drosophila melanogaster. J Insect Physiol 47:1467–1473
40. Grandison RC, Piper MDW, Partridge L (2009) Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 462:1061–1064. doi:10.1038/nature08619
41. Green CB, Takahashi JS, Bass J (2008) The meter of metabolism. Cell 134:728–742. doi:10.1016/j.cell.2008.08.022
42. Griffith LC (2013) Neuromodulatory control of sleep in Drosophila melanogaster: integration of competing and complementary behaviors. Curr Opin Neurobiol 23:819–823. doi:10.1016/j.conb.2013.05.003
43. Grönke S, Mildner A, Fellert S et al (2005) Brummer lipase is an evolutionary conserved fat storage regulator in Drosophila. Cell Metab 1:323–330. doi:10.1016/j.cmet.2005.04.003
44. Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266–275. doi:10.1038/nrn1074
45. Hendricks JC, Finn SM, Panckeri KA et al (2000) Rest in Drosophila is a sleep-like state. Neuron 25:129–138
46. Hendricks JC, Kirk D, Panckeri K et al (2003) Modafinil maintains waking in the fruit fly drosophila melanogaster. Sleep 26:139–146
47. Horne J (2009) REM sleep, energy balance and “optimal foraging”. Neurosci Biobehav Rev 33:466–474. doi:10.1016/j.neubiorev.2008.12.002
48. Ikeya T, Galic M, Belawat P et al (2002) Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr Biol 12:1293–1300
49. Inutsuka A, Yamanaka A (2013) The physiological role of orexin/hypocretin neurons in the regulation of sleep/wakefulness and neuroendocrine functions. Front Endocrinol (Lausanne) 4:18. doi:10.3389/fendo.2013.00018
50. Isabel G, Martin J-R, Chidami S et al (2005) AKH-producing neuroendocrine cell ablation decreases trehalose and induces behavioral changes in Drosophila. Am J Physiol Regul Integr Comp Physiol 288:R531–R538. doi:10.1152/ajpregu.00158.2004
51. Joiner WJ, Crocker A, White BH, Sehgal A (2006) Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441:757–760. doi:10.1038/nature04811
52. Kaneko M, Hall JC (2000) Neuroanatomy of cells expressing clock genes in Drosophila: transgenic manipulation of the period and timeless genes to mark the perikarya of circadian pacemaker neurons and their projections. J Comp Neurol 422(1):66–94
53. Kayser MS, Yue Z, Sehgal A (2014) A critical period of sleep for development of courtship circuitry and behavior in Drosophila. Science 344:269–274. doi:10.1126/science.1250553
54. Keene AC, Stratmann M, Keller A et al (2004) Diverse odor-conditioned memories require uniquely timed dorsal paired medial neuron output. Neuron 44:521–533. doi:10.1016/j.neuron.2004.10.006
55. Keene AC, Duboué ER, McDonald DM et al (2010) Clock and cycle limit starvation-induced sleep loss in Drosophila. Curr Biol 20:1209–1215. doi:10.1016/j.cub.2010.05.029
56. Kim SK, Rulifson EJ (2004) Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. 431:316–320. doi:10.1038/nature02913.1
57. Knutson KL, Van Cauter E (2008) Associations between sleep loss and increased risk of obesity and diabetes. Ann NY Acad Sci 1129:287–304. doi:10.1196/annals.1417.033
58. Laposky AD, Shelton J, Bass J et al (2006) Altered sleep regulation in leptin-deficient mice. Am J Physiol Regul Integr Comp Physiol 290:R894–R903. doi:10.1152/ajpregu.00304.2005
59. Laposky AD, Bass J, Kohsaka A, Turek FW (2008) Sleep and circadian rhythms: key components in the regulation of energy metabolism. FEBS Lett 582:142–151. doi:10.1016/j.febslet.2007.06.079
60. Lazareva Aa, Roman G, Mattox W et al (2007) A role for the adult fat body in Drosophila male courtship behavior. PLoS Genet 3:e16. doi:10.1371/journal.pgen.0030016
61. Lebestky T, Chang J-SC, Dankert H et al (2009) Two different forms of arousal in Drosophila are oppositely regulated by the dopamine D1 receptor ortholog DopR via distinct neural circuits. Neuron 64:522–536. doi:10.1016/j.neuron.2009.09.031
62. Lee W-C, Micchelli CA (2013) Development and characterization of a chemically defined food for Drosophila. PLoS ONE 8:e67308. doi:10.1371/journal.pone.0067308
63. Lee G, Park JH (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
64. Linford NJ, Chan TP, Pletcher SD (2012) Re-patterning sleep architecture in Drosophila through gustatory perception and nutritional quality. PLoS Genet 8:e1002668. doi:10.1371/journal.pgen.1002668
65. Liu G, Seiler H, Wen A et al (2006) Distinct memory traces for two visual features in the Drosophila brain. Nature 439:551–556. doi:10.1038/nature04381
66. Liu W, Guo F, Lu B, Guo A (2008) Amnesiac regulates sleep onset and maintenance in Drosophila melanogaster. Biochem Biophys Res Commun 372:798–803. doi:10.1016/j.bbrc.2008.05.119
67. Liu Q, Liu S, Kodama L et al (2012) Two dopaminergic neurons signal to the dorsal fan-shaped body to promote wakefulness in Drosophila. Curr Biol 22:2114–2123. doi:10.1016/j.cub.2012.09.008
68. Mair W, Piper MDW, Partridge L (2005) Calories do not explain extension of life span by dietary restriction in Drosophila. PLoS Biol 3:e223. doi:10.1371/journal.pbio.0030223
69. Mattaliano MD, Montana ES, Parisky KM et al (2007) The Drosophila ARC homolog regulates behavioral responses to starvation. Mol Cell Neurosci 36:211–221. doi:10.1016/j.mcn.2007.06.008
70. McDonald DM, Keene AC (2010) The sleep-feeding conflict: understanding behavioral integration through genetic analysis in Drosophila. Aging (Albany NY) 2:519–522
71. Metaxakis A, Tain LS, Grönke S et al (2014) Lowered insulin signalling ameliorates age-related sleep fragmentation in Drosophila. PLoS Biol 12:e1001824. doi:10.1371/journal.pbio.1001824
72. Morton GJ, Schwartz MW (2011) Leptin and the central nervous system control of glucose metabolism. Physiol Rev 91:389–411. doi:10.1152/physrev.00007.2010
73. Nitz DA, van Swinderen B, Tononi G, Greenspan RJ (2002) Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr Biol 12:1934–1940
74. Okamoto N, Yamanaka N, Yagi Y et al (2009) A fat body-derived IGF-like peptide regulates postfeeding growth in Drosophila. Dev Cell 17:885–891. doi:10.1016/j.devcel.2009.10.008
75. Osborne KA, Robichon A, Burgess E, Butland S, Shaw RA, Coulthard A, Pereira HS, Greenspan RJ, Sokolowski MB (1997) Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277:834–836
76. Parisky KM, Agosto J, Pulver SR et al (2008) PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60:672–682. doi:10.1016/j.neuron.2008.10.042
77. Park D, Veenstra Ja, Park JH, Taghert PH (2008) Mapping peptidergic cells in Drosophila: where DIMM fits in. PLoS ONE 3:e1896. doi:10.1371/journal.pone.0001896
78. Pfeiffenberger C, Lear BC, Keegan KP, Allada R (2010) Locomotor activity level monitoring using the Drosophila Activity Monitoring (DAM) System. Cold Spring Harb Protoc:pdb.prot5518
79. Piper MDW, Blanc E, Leitão-Gonçalves R et al (2014) A holidic medium for Drosophila melanogaster. Nat Methods 11:100–105. doi:10.1038/nmeth.2731
80. Pitman JL, McGill JJ, Keegan KP, Allada R (2006) A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 441:753–756. doi:10.1038/nature04739
81. Poeck B, Triphan T, Neuser K, Strauss R (2008) Locomotor control by the central complex in Drosophila—an analysis of the tay bridge mutant. Dev Neurobiol 68:1046–1058. doi:10.1002/dneu.20643
82. Rajan A, Perrimon N (2012) Drosophila cytokine unpaired 2 regulates physiological homeostasis by remotely controlling insulin secretion. Cell 151:123–137. doi:10.1016/j.cell.2012.08.019
83. Renn SC, Park JH, Rosbash M et al (1999) A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99:791–802. doi:10.1016/S0092-8674(00)81676-1
84. Root CM, Masuyama K, Green DS et al (2008) A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59:311–321. doi:10.1016/j.neuron.2008.07.003
85. Rulifson EJ, Kim SK, Nusse R (2002) Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296:1118–1120. doi:10.1126/science.1070058
86. Saltiel AR, Kahn CR (2001) Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414:799–806. doi:10.1038/414799a
87. Sassu ED, McDermott JE, Keys BJ et al (2012) Mio/dChREBP coordinately increases fat mass by regulating lipid synthesis and feeding behavior in Drosophila. Biochem Biophys Res Commun 426:43–48. doi:10.1016/j.bbrc.2012.08.028
88. Seelig JD, Jayaraman V (2013) Feature detection and orientation tuning in the Drosophila central complex. Nature 503:262–266. doi:10.1038/nature12601
89. Sehgal A, Mignot E (2011) Genetics of sleep and sleep disorders. Cell 146:194–207. doi:10.1016/j.cell.2011.07.004
90. Seugnet L, Suzuki Y, Donlea JM et al (2011) Sleep deprivation during early-adult development results in long-lasting learning deficits in adult Drosophila. Sleep 34:137–146
91. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287:1834–1837
92. Sinakevitch I, Strausfeld NJ (2006) Comparison of octopamine-like immunoreactivity in the brains of the fruit fly and blow fly. J Comp Neurol 494:460–475. doi:10.1002/cne.20799
93. Skorupa Da, Dervisefendic A, Zwiener J, Pletcher SD (2008) Dietary composition specifies consumption, obesity, and lifespan in Drosophila melanogaster. Aging Cell 7:478–490. doi:10.1111/j.1474-9726.2008.00400.x
94. Taheri S, Lin L, Austin D et al (2004) Short sleep duration is associated with reduced leptin, elevated ghrelin, and increased body mass index. PLoS Med 1:e62. doi:10.1371/journal.pmed.0010062
95. Tanaka NK, Tanimoto H, Ito K (2008) Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508:711–755. doi:10.1002/cne.21692
96. Thimgan MS, Suzuki Y, Seugnet L et al (2010) The perilipin homologue, lipid storage droplet 2, regulates sleep homeostasis and prevents learning impairments following sleep loss. PLoS Biol. doi:10.1371/journal.pbio.1000466
97. Ueno T, Tomita J, Tanimoto H et al (2012) Identification of a dopamine pathway that regulates sleep and arousal in Drosophila. Nat Neurosci 15:1516–1523. doi:10.1038/nn.3238
98. Unger RH, Cherrington AD (2012) Glucagonocentric restructuring of diabetes: a pathophysiologic and therapeutic makeover. J Clin Invest 122:4–12. doi:10.1172/JCI60016
99. Van Alphen B, Yap MHW, Kirszenblat L et al (2013) A dynamic deep sleep stage in Drosophila. J Neurosci 33:6917–6927. doi:10.1523/JNEUROSCI.0061-13.2013
100. Van der Horst DJ (2003) Insect adipokinetic hormones: release and integration of flight energy metabolism. Comp Biochem Physiol B Biochem Mol Biol 136:217–226
101. Winther AME, Acebes A, Ferrús A (2006) Tachykinin-related peptides modulate odor perception and locomotor activity in Drosophila. Mol Cell Neurosci 31:399–406. doi:10.1016/j.mcn.2005.10.010
102. Wu Q, Zhao Z, Shen P (2005) Regulation of aversion to noxious food by Drosophila neuropeptide Y- and insulin-like systems. Nat Neurosci 8:1350–1355. doi:10.1038/nn1540
103. Wu MN, Ho K, Crocker A et al (2009) The effects of caffeine on sleep in Drosophila require PKA activity, but not the adenosine receptor. J Neurosci 29:11029–11037. doi:10.1523/JNEUROSCI.1653-09.2009
104. Xu K, Zheng X, Sehgal A (2008) Regulation of feeding and metabolism by neuronal and peripheral clocks in Drosophila. Cell Metab 8:289–300. doi:10.1016/j.cmet.2008.09.006
105. Xu K, DiAngelo JR, Hughes ME et al (2011) The circadian clock interacts with metabolic physiology to influence reproductive fitness. Cell Metab 13:639–654. doi:10.1016/j.cmet.2011.05.001
106. Yu D, Keene AC, Srivatsan A et al (2005) Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning. Cell 123:945–957. doi:10.1016/j.cell.2005.09.037
107. Zheng X, Yang Z, Yue Z et al (2007) FOXO and insulin signaling regulate sensitivity of the circadian clock to oxidative stress. Proc Natl Acad Sci USA 104:15899–15904. doi:10.1073/pnas.0701599104
108. Zimmerman JE, Raizen DM, Maycock MH et al (2008) A video method to study Drosophila sleep. Sleep 31:1587–1598