Sleep-dependent modulation of metabolic rate in drosophila

Sleep

Volumn 40, Issue 8, 2017, Pages

  Stahl, Bethany A ^a   Slocumb, Melissa E ^a,b   Chaitin, Hersh ^c   DiAngelo, Justin R ^d   Keene, Alex C ^a  

^a FLORIDA ATLANTIC UNIVERSITY   (United States)

^b Integrative Biology and Neuroscience Graduate Program   (United States)

^c Florida Atlantic University   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Calorimetry; Drosophila; Metabolism; Respirometry; Sleep

Indexed keywords

CARBON DIOXIDE; DROSOPHILA PROTEIN; TRANSLIN PROTEIN, DROSOPHILA;

ANIMAL; BASAL METABOLIC RATE; DROSOPHILA MELANOGASTER; ENERGY METABOLISM; FEMALE; FOOD DEPRIVATION; GENETICS; MALE; METABOLISM; PHYSIOLOGY; SLEEP; TIME FACTOR; WAKEFULNESS;

ANIMALS; BASAL METABOLISM; CARBON DIOXIDE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENERGY METABOLISM; FEMALE; FOOD DEPRIVATION; MALE; SLEEP; TIME FACTORS; WAKEFULNESS;

EID: 85030085182     PISSN: 01618105     EISSN: 15509109     Source Type: Journal    
DOI: 10.1093/sleep/zsx084     Document Type: Article

References (71)

1. Reutrakul S, Van Cauter E. Interactions between sleep, circadian function, and glucose metabolism: Implications for risk and severity of diabetes. Ann N Y Acad Sci. 2014; 1311: 151-173.
2. Yurgel M, Masek P, DiAngelo JR, Keene A. Genetic dissection of sleep-metabolism interactions in the fruit fly. J Comp Physiol a Neuroethol Sens Neural Behav Physiol. 2015; 201(9): 869-877.
3. Schmidt MH. The energy allocation function of sleep: A unifying theory of sleep, torpor, and continuous wakefulness. Neurosci Biobehav Rev. 2014; 47: 122-153.
4. Berger RJ, Phillips NH. Energy conservation and sleep. Behav Brain Res. 1995; 69(1-2): 65-73.
5. Walker JM, Berger RJ. Sleep as an adaptation for energy conservation functionally related to hibernation and shallow torpor. Prog Brain Res. 1980; 53: 255-278.
6. Hendricks JC, Finn SM, Panckeri KA, et al. Rest in Drosophila is a sleep-like state. Neuron. 2000; 25(1): 129-138.
7. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G. Correlates of sleep and waking in Drosophila melanogaster. Science. 2000; 287(5459): 1834-1837.
8. Campbell SS, Tobler I. Animal sleep: A review of sleep duration across phylogeny. Neurosci Biobehav Rev. 1984; 8(3): 269-300.
9. Nitz DA, van Swinderen B, Tononi G, Greenspan RJ. Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr Biol. 2002; 12(22): 1934-1940.
10. van Alphen B, Yap MH, Kirszenblat L, Kottler B, van Swinderen B. A dynamic deep sleep stage in Drosophila. J Neurosci. 2013; 33(16): 6917-6927.
11. Caron AM, Stephenson R. Energy expenditure is affected by rate of accumulation of sleep deficit in rats. Sleep. 2010; 33(9): 1226-1235.
12. Valenti G, Bonomi AG, Westerterp KR. Quality sleep is associated with overnight metabolic rate in healthy older adults. J Gerontol A Biol Sci Med Sci. 2016; 72(4): 567-571.
13. Spaeth AM, Dinges DF, Goel N. Resting metabolic rate varies by race and by sleep duration. Obesity. 2015; 23(12): 2349-2356.
14. Lighton J. Measuring Metabolic Rates: A Manual for Scientists. Oxford University Press; 2008.
15. Claussen M, Koch R, Jin ZY, Suter B. Functional characterization of Drosophila Translin and Trax. Genetics. 2006; 174(3): 1337-1347.
16. Van Voorhies WA, Khazaeli AA, Curtsinger JW. Testing the "rate of living" model: Further evidence that longevity and metabolic rate are not inversely correlated in Drosophila melanogaster. J Appl Physiol (1985). 2004; 97(5): 1915-1922.
17. Pfeiffenberger C, Lear BC, Keegan KP, Allada R. Locomotor activity level monitoring using the Drosophila Activity Monitoring (DAM) system. Cold Spring Harb Protoc. 2010; 2010(11): Pdb.prot5518.
18. Keene AC, Duboué ER, McDonald DM, et al. Clock and cycle limit starvation-induced sleep loss in Drosophila. Curr Biol. 2010; 20(13): 1209-1215.
19. Dissel S, Angadi V, Kirszenblat L, et al. Sleep restores behavioral plasticity to Drosophila mutants. Curr Biol. 2015; 25(10): 1270-1281.
20. Garbe DS, Bollinger WL, Vigderman A, et al. Context-specific comparison of sleep acquisition systems in Drosophila. Biol Open. 2015; 4(11): 1558-1568.
21. Heusner AA. Energy metabolism and body size. I. Is the 0.75 mass exponent of Kleiber's equation a statistical artifact? Respir Physiol. 1982; 48(1): 1-12.
22. Schilman PE, Waters JS, Harrison JF, Lighton JR. Effects of temperature on responses to anoxia and oxygen reperfusion in Drosophila melanogaster. J Exp Biol. 2011; 214(Pt 8): 1271-1275.
23. Parisky KM, Agosto J, Pulver SR, et al. PDF cells are a GABAresponsive wake-promoting component of the Drosophila sleep circuit. Neuron. 2008; 60(4): 672-682.
24. Agosto J, Choi JC, Parisky KM, Stilwell G, Rosbash M, Griffith LC. Modulation of GABAA receptor desensitization uncouples sleep onset and maintenance in Drosophila. Nat Neurosci. 2008; 11(3): 354-359.
25. Wafford KA, Ebert B. Gaboxadol-a new awakening in sleep. Curr Opin Pharmacol. 2006; 6(1): 30-36.
26. Adamantidis A, de Lecea L. Sleep and metabolism: Shared circuits, new connections. Trends Endocrinol Metab. 2008; 19(10): 362-370.
27. Linford NJ, Chan TP, Pletcher SD. Re-patterning sleep architecture in Drosophila through gustatory perception and nutritional quality. PLoS Genet. 2012; 8(5): E1002668.
28. McDonald DM, Keene AC. The sleep-feeding conflict: Understanding behavioral integration through genetic analysis in Drosophila. Aging (Albany NY). 2010; 2(8): 519-522.
29. Murakami K, Yurgel ME, Stahl BA, et al. Translin is required for metabolic regulation of sleep. Curr Biol. 2016; 26(7): 972-980.
30. Yatsenko AS, Marrone AK, Kucherenko MM, Shcherbata HR. Measurement of metabolic rate in Drosophila using respirometry. J. Vis. Exp. 2014; (88):e51681. doi:10.3791/51681.
31. Mölich AB, Förster TD, Lighton JR. Hyperthermic overdrive: Oxygen delivery does not limit thermal tolerance in Drosophila melanogaster. J Insect Sci. 2012; 12: 109.
32. Hulbert AJ, Clancy DJ, Mair W, Braeckman BP, Gems D, Partridge L. Metabolic rate is not reduced by dietary-restriction or by lowered insulin/IGF-1 signalling and is not correlated with individual lifespan in Drosophila melanogaster. Exp Gerontol. 2004; 39(8): 1137-1143.
33. Allada R, Siegel JM. Unearthing the phylogenetic roots of sleep. Curr Biol. 2008; 18(15): R670-R679.
34. Padmanabha D, Baker KD. Drosophila gains traction as a repurposed tool to investigate metabolism. Trends Endocrinol. Metab. 2014:1-10.
35. Lee G, 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): 311-323.
36. Danguir J, Nicolaidis S. Dependence of sleep on nutrients' availability. Physiol Behav. 1979; 22(4): 735-740.
37. Elgar MA, Pagel MD, Harvey PH. Sleep in mammals. Anim. Behav. 1988; 36(5):1407-1419.
38. Lesku JA, Roth TC 2nd, Amlaner CJ, Lima SL. A phylogenetic analysis of sleep architecture in mammals: The integration of anatomy, physiology, and ecology. Am Nat. 2006; 168(4): 441-453.
39. Capellini I, Nunn CL, McNamara P, Preston BT, Barton RA. Energetic constraints, not predation, influence the evolution of sleep patterning in mammals. Funct Ecol. 2008; 22(5): 847-853.
40. Shapiro CM, Goll CC, Cohen GR, Oswald I. Heat production during sleep. J Appl Physiol Respir Environ Exerc Physiol. 1984; 56(3): 671-677.
41. Garby L, Kurzer MS, Lammert O, Nielsen E. Energy expenditure during sleep in men and women: Evaporative and sensible heat losses. Hum Nutr Clin Nutr. 1987; 41(3): 225-233.
42. Goldberg GR, Prentice AM, Davies HL, Murgatroyd PR. Overnight and basal metabolic rates in men and women. Eur. J. Clin. Nutr. 1988; 42(2):137-144.
43. Kume K, Kume S, Park SK, Hirsh J, Jackson FR. Dopamine is a regulator of arousal in the fruit fly. J Neurosci. 2005; 25(32): 7377-7384.
44. Ueno T, Tomita J, Kume S, Kume K. Dopamine modulates metabolic rate and temperature sensitivity in Drosophila melanogaster. PLoS One 2012; 7(2). doi:10.1371/journal.pone.0031513.
45. Stephenson R, Chu KM, Lee J. Prolonged deprivation of sleep-like rest raises metabolic rate in the Pacific beetle cockroach, Diploptera punctata (Eschscholtz). J Exp Biol. 2007; 210(Pt 14): 2540-2547.
46. Yurgel ME, Masek P, DiAngelo J, Keene AC. Genetic dissection of sleep-metabolism interactions in the fruit fly. J Comp Physiol a Neuroethol Sens Neural Behav Physiol. 2015; 201(9): 869-877.
47. Griffith LC. Neuromodulatory control of sleep in Drosophila melanogaster: Integration of competing and complementary behaviors. Curr Opin Neurobiol. 2013; 23(5): 819-823.
48. Schwasinger-Schmidt TE, Kachman SD, Harshman LG. Evolution of starvation resistance in Drosophila melanogaster: Measurement of direct and correlated responses to artificial selection. J Evol Biol. 2012; 25(2): 378-387.
49. Masek P, Reynolds LA, Bollinger WL, et al. Altered regulation of sleep and feeding contributes to starvation resistance in Drosophila melanogaster. J Exp Biol. 2014; 217(Pt 17): 3122-3132.
50. Slocumb ME, Regalado JM, Yoshizawa M, et al. Enhanced sleep is an evolutionarily adaptive response to starvation stress in Drosophila. PLoS One. 2015; 10(7): E0131275.
51. Harshman LG, Hoffmann AA, Clark AG. Selection for starvation resistance in Drosophila melanogaster: Physiological correlates, enzyme activities and multiple stress responses. J. Evol. Biol. 1999; 12:370-379.
52. Masek P, Reynolds L a, Bollinger WL, et al. Altered regulation of sleep and feeding contributes to starvation resistance in Drosophila melanogaster. J Exp Biol. 2014; 217(Pt 17): 3122-3132.
53. Newman SM, Paletz EM, Rattenborg NC, Obermeyer WH, Benca RM. Sleep deprivation in the pigeon using the Disk-Over-Water method. Physiol Behav. 2008; 93(1-2): 50-58.
54. Siegel JM. Clues to the functions of mammalian sleep. Nature. 2005; 437(7063): 1264-1271.
55. Faville R, Kottler B, Goodhill GJ, Shaw PJ, van Swinderen B. How deeply does your mutant sleep? Probing arousal to better understand sleep defects in Drosophila. Sci Rep. 2015; 5: 8454.
56. Crocker A, Shahidullah M, Levitan IB, Sehgal A. Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behavior. Neuron. 2010; 65(5): 670-681.
57. Keene AC, Duboué ER, McDonald DM, et al. Clock and cycle limit starvation-induced sleep loss in Drosophila. Curr Biol. 2010; 20(13): 1209-1215.
58. Joiner WJ, Crocker A, White BH, Sehgal A. Sleep in Drosophila is regulated by adult mushroom bodies. Nature. 2006; 441(7094): 757-760.
59. Pitman JL, McGill JJ, Keegan KP, Allada R. A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature. 2006; 441(7094): 753-756.
60. Donlea JM, Thimgan MS, Suzuki Y, Gottschalk L, Shaw PJ. Inducing sleep by remote control facilitates memory consolidation in Drosophila. Science. 2011; 332(6037): 1571-1576.
61. Guo F, Yu J, Jung HJ, et al. Circadian neuron feedback controls the Drosophila sleep-activity profile. Nature. 2016; 536(7616): 292-297.
62. Liu S, Liu Q, Tabuchi M, Wu MN. Sleep drive is encoded by neural plastic changes in a dedicated circuit. Cell. 2016; 165(6): 1347-1360.
63. Seidner G, Robinson JE, Wu M, et al. Identification of neurons with a privileged role in sleep homeostasis in Drosophila melanogaster. Curr Biol. 2015; 25(22): 2928-2938.
64. Donlea JM, Pimentel D, Miesenböck G. Neuronal machinery of sleep homeostasis in Drosophila. Neuron. 2014; 81(4): 860-872.
65. Xu K, DiAngelo JR, Hughes ME, Hogenesch JB, Sehgal A. The circadian clock interacts with metabolic physiology to influence reproductive fitness. Cell Metab. 2011; 13(6): 639-654.
66. Lin JD, Liu C, Li S. Integration of energy metabolism and the mammalian clock. Cell Cycle. 2008; 7(4): 453-457.
67. Arrese E, Soulages J. Insect fat body: Energy, metabolism, and regulation. Annu. Rev. Entomol. 2010; 55: 207-225.
68. Marron MT, Markow TA, Kain KJ, Gibbs AG. Effects of starvation and desiccation on energy metabolism in desert and mesic Drosophila. J Insect Physiol. 2003; 49(3): 261-270.
69. Melanson EL, Ingebrigtsen JP, Bergouignan A, Ohkawara K, Kohrt WM, Lighton JR. A new approach for flow-through respirometry measurements in humans. Am J Physiol Regul Integr Comp Physiol. 2010; 298(6): R1571-R1579.
70. Sinitskaya N, Gourmelen S, Schuster-Klein C, Guardiola-Lemaitre B, Pévet P, Challet E. Increasing the fat-to-carbohydrate ratio in a high-fat diet prevents the development of obesity but not a prediabetic state in rats. Clin Sci (Lond). 2007; 113(10): 417-425.
71. Liu C, Haynes PR, Donelson NC, Aharon S, Griffith LC. Sleep in populations of Drosophila melanogaster. eNeuro 2015; 2(4): Doi:10.1523/ENEURO.0071-15.2015.