Type of diet modulates the metabolic response to sleep deprivation in rats

Nutrition & Metabolism

Vânia D'Almeida¹  Sergio Tufik¹  Allan C de Oliveira¹  Leandro Fernandes¹  Paulo JF Martins¹ 

[1] Department of Psychobiology, Universidade Federal de São Paulo-UNIFESP/São Paulo - Brazil

关键词: energy intake;    sleep deprivation;    rats;    hormones;    liver glycogen;    hyperphagia;    metabolism;    liquid diet;    Body weight;   

Others  :  820222
DOI  :  10.1186/1743-7075-8-86

 received in 2011-08-19, accepted in 2011-12-12,  发布年份 2011

【 摘 要 】

Background

Evidence suggests that sleep loss is associated with an increased risk of obesity and diabetes; however, animal models have failed to produce weight gain under sleep deprivation (SD). Previous studies have suggested that this discrepancy could be due to more extreme SD conditions in experimental animals, their higher resting metabolic rate than that of humans, and the decreased opportunity for animals to ingest high-calorie foods. Thus, our objective was to determine whether diets with different textures/compositions could modify feeding behavior and affect the metabolic repercussions in SD in rats.

Methods

Three groups of male rats were used: one was designated as control, one was sleep deprived for 96 h by the platform technique (SD-96h) and one was SD-96h followed by a 24-h recovery (rebound). In the first experiment, the animals were fed chow pellets (CPs); in the second, they received high-fat diet and in the third, they were fed a liquid diet (LD).

Results

We observed that SD induces energy deficits that were related to changes in feeding behavior and affected by the type of diet consumed. Regardless of the diet consumed, SD consistently increased animals' glucagon levels and decreased their leptin and triacylglycerol levels and liver glycogen stores. However, such changes were mostly avoided in the rats on the liquid diet. SD induces a wide range of metabolic and hormonal changes that are strongly linked to the severity of weight loss.

Conclusions

The LD, but not the CP or high-fat diets, favored energy intake, consequently lessening the energy deficit induced by SD.

【 授权许可】

   
2011 Martins et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Spiegel K, Tasali E, Penev P, Van Cauter E: Brief communication: Sleep curtailment in healthy young men is associated with decreased leptin levels, elevated ghrelin levels, and increased hunger and appetite. Ann Intern Med 2004, 141:846-850.
• [2]Taheri S, Lin L, Austin D, Young T, Mignot E: Short sleep duration is associated with reduced leptin, elevated ghrelin, and increased body mass index. PLoS Med 2004, 1:e62.
• [3]Leproult R, Van Cauter E: Role of sleep and sleep loss in hormonal release and metabolism. Endocr Dev 2010, 17:11-21.
• [4]Nordin M, Kaplan RM: Sleep discontinuity and impaired sleep continuity affect transition to and from obesity over time: results from the Alameda county study. Scand J Public Health 2010, 38:200-207.
• [5]Theorell-Haglow J, Berne C, Janson C, Sahlin C, Lindberg E: Associations between short sleep duration and central obesity in women. Sleep 2010, 33:593-598.
• [6]Mendelson WB, Guthrie RD, Frederick G, Wyatt RJ: The flower pot technique of rapid eye movement (REM) sleep deprivation. Pharmacol Biochem Behav 1974, 2:553-556.
• [7]Everson CA, Bergmann BM, Rechtschaffen A: Sleep deprivation in the rat: III. Total sleep deprivation. Sleep 1989, 12:13-21.
• [8]Kushida CA, Bergmann BM, Rechtschaffen A: Sleep deprivation in the rat: IV. Paradoxical sleep deprivation. Sleep 1989, 12:22-30.
• [9]Koban M, Swinson KL: Chronic REM-sleep deprivation of rats elevates metabolic rate and increases UCP1 gene expression in brown adipose tissue. Am J Physiol Endocrinol Metab 2005, 289:E68-74.
• [10]Everson CA, Crowley WR: Reductions in circulating anabolic hormones induced by sustained sleep deprivation in rats. Am J Physiol Endocrinol Metab 2004, 286:E1060-1070.
• [11]Suchecki D, Tufik S: Social stability attenuates the stress in the modified multiple platform method for paradoxical sleep deprivation in the rat. Physiol Behav 2000, 68:309-316.
• [12]Koban M, Le WW, Hoffman GE: Changes in hypothalamic corticotropin-releasing hormone, neuropeptide Y, and proopiomelanocortin gene expression during chronic rapid eye movement sleep deprivation of rats. Endocrinology 2006, 147:421-431.
• [13]Martins PJ, Marques MS, Tufik S, D'Almeida V: Orexin activation precedes increased NPY expression, hyperphagia, and metabolic changes in response to sleep deprivation. Am J Physiol Endocrinol Metab 2010, 298:E726-734.
• [14]Andersen ML, Martins PJ, D'Almeida V, Bignotto M, Tufik S: Endocrinological and catecholaminergic alterations during sleep deprivation and recovery in male rats. J Sleep Res 2005, 14:83-90.
• [15]Bergmann BM, Everson CA, Kushida CA, Fang VS, Leitch CA, Schoeller DA, Refetoff S, Rechtschaffen A: Sleep deprivation in the rat: V. Energy use and mediation. Sleep 1989, 12:31-41.
• [16]Hipolide DC, Suchecki D, Pimentel de Carvalho Pinto A, Chiconelli Faria E, Tufik S, Luz J: Paradoxical sleep deprivation and sleep recovery: effects on the hypothalamic-pituitary-adrenal axis activity, energy balance and body composition of rats. J Neuroendocrinol 2006, 18:231-238.
• [17]Meerlo P, Koehl M, van der Borght K, Turek FW: Sleep restriction alters the hypothalamic-pituitary-adrenal response to stress. J Neuroendocrinol 2002, 14:397-402.
• [18]Bhanot JL, Chhina GS, Singh B, Sachdeva U, Kumar VM: REM sleep deprivation and food intake. Indian J Physiol Pharmacol 1989, 33:139-145.
• [19]Martins PJF, D'Almeida V, Nobrega JN, Tufik S: A reassessment of the hyperphagia/weight-loss paradox during sleep deprivation. Sleep 2006, 29:1233-1238.
• [20]Martins PJ, Nobrega JN, Tufik S, D'Almeida V: Sleep deprivation-induced gnawing-relationship to changes in feeding behavior in rats. Physiol Behav 2008, 93:229-234.
• [21]Dallman MF, Pecoraro N, Akana SF, La Fleur SE, Gomez F, Houshyar H, Bell ME, Bhatnagar S, Laugero KD, Manalo S: Chronic stress and obesity: a new view of "comfort food". Proc Natl Acad Sci USA 2003, 100:11696-11701.
• [22]Hanlon EC, Andrzejewski ME, Harder BK, Kelley AE, Benca RM: The effect of REM sleep deprivation on motivation for food reward. Behav Brain Res 2005, 163:58-69.
• [23]Johnson PM, Kenny PJ: Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 2010, 13:635-641.
• [24]Machado RB, Hipolide DC, Benedito-Silva AA, Tufik S: Sleep deprivation induced by the modified multiple platform technique: quantification of sleep loss and recovery. Brain Res 2004, 1004:45-51.
• [25]Martins PJF, Nobrega JN, Tufik S, D'Almeida V: Sleep deprivation-induced gnawing-relationship to changes in feeding behavior in rats. Physiol Behav 2008, 93:229-234.
• [26]Giavarotti L, D'Almeida V, Giavarotti KA, Azzalis LA, Rodrigues L, Cravero AA, Videla LA, Koch OR, Junqueira VB: Liver necrosis induced by acute intraperitoneal ethanol administration in aged rats. Free Radic Res 2002, 36:269-275.
• [27]Roversi FM, Galdieri LC, Grego BH, Souza FG, Micheletti C, Martins AM, D'Almeida V: Blood oxidative stress markers in Gaucher disease patients. Clin Chim Acta 2006, 364:316-320.
• [28]Papakonstantinou E, Ryan DH, Harris RB: Dietary fish oil does not protect rats exposed to restraint or sleep deprivation stress. Physiol Behav 2003, 78:759-765.
• [29]Jones KL, Russo A, Berry MK, Stevens JE, Wishart JM, Horowitz M: A longitudinal study of gastric emptying and upper gastrointestinal symptoms in patients with diabetes mellitus. Am J Med 2002, 113:449-455.
• [30]Nemeth S, Hepa J: Liver glycogen content and activity of several hepatic enzymes in repeatedly immobilized rats. Acta Physiol Pol 1978, 29:55-60.
• [31]Ilan Y, Martinowitz G, Abramsky O, Glazer G, Lavie P: Prolonged sleep-deprivation induced disturbed liver functions serum lipid levels, and hyperphosphatemia. Eur J Clin Invest 1992, 22:740-743.
• [32]Ricart-Jane D, Rodriguez-Sureda V, Benavides A, Peinado-Onsurbe J, Lopez-Tejero MD, Llobera M: Immobilization stress alters intermediate metabolism and circulating lipoproteins in the rat. Metabolism 2002, 51:925-931.
• [33]van der Wal AM, Bakker O, Wiersinga WM: The decrease of liver LDL receptor mRNA during fasting is related to the decrease in serum T3. Int J Biochem Cell Biol 1998, 30:209-215.
• [34]Andersen ML, Martins PJF, D'Almeida V, Bignotto M, Tufik S: Endocrinological and catecholaminergic alterations during sleep deprivation and recovery in male rats. J Sleep Res 2005, 14:83-90.
• [35]Nicolaidis S: Metabolic mechanism of wakefulness (and hunger) and sleep (and satiety): Role of adenosine triphosphate and hypocretin and other peptides. Metabolism 2006, 55:S24-29.
• [36]Everson CA, Wehr TA: Nutritional and metabolic adaptations to prolonged sleep deprivation in the rat. Am J Physiol 1993, 264:R376-387.
• [37]Laboure H, Saux S, Nicolaidis S: Effects of food texture change on metabolic parameters: short- and long-term feeding patterns and body weight. Am J Physiol Regul Integr Comp Physiol 2001, 280:R780-789.
• [38]Laboure H, Van Wymelbeke V, Fantino M, Nicolaidis S: Behavioral, plasma, and calorimetric changes related to food texture modification in men. Am J Physiol Regul Integr Comp Physiol 2002, 282:R1501-1511.