Short-term food restriction followed by controlled refeeding promotes gorging behavior, enhances fat deposition, and diminishes insulin sensitivity in mice

Journal of Nutritional Biochemistry

Volumn 26, Issue 7, 2015, Pages 721-728

  Kliewer, Kara L ^a   Ke, Jia Yu ^a   Lee, Hui Young ^c   Stout, Michael B ^a   Cole, Rachel M ^a   Samuel, Varman T ^b   Shulman, Gerald I ^b   Belury, Martha A ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Gachon University   (South Korea)

Author keywords

Adiposity; Food restriction; Gorging; Insulin sensitivity; Refeeding; Weight regain

Indexed keywords

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIET RESTRICTION; FEEDING BEHAVIOR; FOOD INTAKE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GORGING BEHAVIOR; INSULIN SENSITIVITY; INTRAABDOMINAL FAT; LIPID LIVER LEVEL; LIPID STORAGE; MALE; METABOLISM; MOUSE; NONHUMAN; REFEEDING; ADVERSE EFFECTS; ANIMAL; ANIMAL BEHAVIOR; BAGG ALBINO MOUSE; BLOOD; BROWN ADIPOSE TISSUE; CALORIC RESTRICTION; CROSS BREEDING; DBA MOUSE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HYPERPHAGIA; INSULIN RESISTANCE; LIVER; OBESITY; PATHOLOGY; RANDOMIZATION; WEIGHT GAIN;

ADIPOCYTOKINE; AUTACOID;

ADIPOKINES; ADIPOSE TISSUE, BROWN; ADIPOSITY; ANIMALS; BEHAVIOR, ANIMAL; CALORIC RESTRICTION; CROSSES, GENETIC; FEEDING BEHAVIOR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HYPERPHAGIA; INFLAMMATION MEDIATORS; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; LIVER; MALE; MICE, INBRED BALB C; MICE, INBRED DBA; RANDOM ALLOCATION; WEIGHT GAIN;

EID: 84942988028     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2015.01.010     Document Type: Article

References (43)

1. Kraschnewski JL, Boan J, Esposito J, Sherwood NE, Lehman EB, Kephart DK, et al. Long-term weight loss maintenance in the United States. Int J Obes (Lond) 2010; 34:1644-54.
2. Maclean PS, Bergouignan A, Cornier MA, Jackman MR. Biology's response to dieting: the impetus for weight regain. Am J Physiol Regul Integr Comp Physiol 2011;301:R581-600.
3. Beavers KM, Lyles MF, Davis CC, Wang X, Beavers DP, Nicklas BJ. Is lost lean mass from intentional weight loss recovered during weight regain in postmenopausal women? Am J Clin Nutr 2011;94:767-74.
4. Lee JS, Visser M, Tylavsky FA, Kritchevsky SB, Schwartz AV, Sahyoun N, et al. Weight loss and regain and effects on body composition: the Health, Aging, and Body Composition Study. J Gerontol A Biol Sci Med Sci 2010;65:78-83.
5. Ibanez L, Ong K, Dunger DB, de Zegher F. Early development of adiposity and insulin resistance after catch-up weight gain in small-for-gestational-age children. J Clin Endocrinol Metab 2006;91:2153-8.
6. Dulloo AG, Jacquet J, Montani JP. Pathways from weight fluctuations to metabolic diseases: focus on maladaptive thermogenesis during catch-up fat. Int J Obes Relat Metab Disord 2002;26(Suppl. 2):S46-57.
7. Ozelci A, Romsos DR, Leveille GA. Influence of initial food restriction on subsequent body weight gain and body fat accumulation in rats. J Nutr 1978; 108:1724-32.
8. Brownell KD, Greenwood MR, Stellar E, Shrager EE. The effects of repeated cycles of weight loss and regain in rats. Physiol Behav 1986;38:459-64.
9. Fried SK, Hill JO, Nickel M, DiGirolamo M. Novel regulation of lipoprotein lipase activity in rat brown adipose tissue: effects of fasting and caloric restriction during refeeding. J Nutr 1983;113:1870-4.
10. MacLean PS, Higgins JA, Johnson GC, Fleming-Elder BK, Donahoo WT, Melanson EL, et al. Enhanced metabolic efficiency contributes to weight regain after weight loss in obesity-prone rats. Am J Physiol Regul Integr Comp Physiol 2004;287: R1306-15.
11. MacLean PS, Higgins JA, Jackman MR, Johnson GC, Fleming-Elder BK, Wyatt HR, et al. Peripheral metabolic responses to prolonged weight reduction that promote rapid, efficient regain in obesity-prone rats. Am J Physiol Regul Integr Comp Physiol 2006;290:R1577-88.
12. Dulloo AG, Girardier L. Adaptive changes in energy expenditure during refeeding following low-calorie intake: evidence for a specific metabolic component favoring fat storage. Am J Clin Nutr 1990;52:415-20.
13. Dulloo AG, Calokatisa R. Adaptation to low calorie intake in obese mice: contribution of a metabolic component to diminished energy expenditures during and after weight loss. Int J Obes 1991;15:7-16.
14. Cettour-Rose P, Samec S, Russell AP, Summermatter S, Mainieri D, CarrilloTheander C, et al. Redistribution of glucose from skeletal muscle to adipose tissue during catch-up fat: a link between catch-up growth and later metabolic syndrome. Diabetes 2005;54:751-6.
15. Summermatter S, Marcelino H, Arsenijevic D, Buchala A, Aprikian O, Assimacopoulos-Jeannet F, et al. Adipose tissue plasticity during catch-up fat driven by thrifty metabolism: relevance for muscle-adipose glucose redistribution during catch-up growth. Diabetes 2009;58:2228-37.
16. Crescenzo R, Samec S, Antic V, Rohner-Jeanrenaud F, Seydoux J, Montani JP, et al. A role for suppressed thermogenesis favoring catch-up fat in the pathophysiology of catch-up growth. Diabetes 2003;52:1090-7.
17. Isganaitis E, Jimenez-Chillaron J, Woo M, Chow A, DeCoste J, Vokes M, et al. Accelerated postnatal growth increases lipogenic gene expression and adipocyte size in low-birth weight mice. Diabetes 2009;58:1192-200.
18. Ellacott KL, Morton GJ, Woods SC, Tso P, Schwartz MW. Assessment of feeding behavior in laboratory mice. Cell Metab 2010;12:10-7.
19. Russell JC, Proctor SD, Kelly SE, Brindley DN. Pair feeding-mediated changes in metabolism: stress response and pathophysiology in insulin-resistant, atherosclerosis-prone JCR:LA-cp rats. Am J Physiol Endocrinol Metab 2008;294: E1078-87.
20. Hambly C, Simpson CA, McIntosh S, Duncan JS, Dalgleish GD, Speakman JR. Calorie-restricted mice that gorge show less ability to compensate for reduced energy intake. Physiol Behav 2007;92:985-92.
21. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-8.
22. Tian M, Kliewer KL, Asp ML, Stout MB, Belury MA. c9t11-Conjugated linoleic acidrich oil fails to attenuate wasting in colon-26 tumor-induced late-stage cancer cachexia in male CD2F1 mice. Mol Nutr Food Res 2011;55:268-77.
23. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 1957;226:497-509.
24. Ayala JE, Samuel VT, Morton GJ, Obici S, Croniger CM, Shulman GI, et al. Standard operating procedures for describing and performing metabolic tests of glucose homeostasis in mice. Dis Model Mech 2010;3:525-34.
25. Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care 1999;22:1462-70.
26. Youn JH, Buchanan TA. Fasting does not impair insulin-stimulated glucose uptake but alters intracellular glucose metabolism in conscious rats. Diabetes 1993;42: 757-63.
27. Guan HP, Goldstein JL, Brown MS, Liang G. Accelerated fatty acid oxidation in muscle averts fasting-induced hepatic steatosis in SJL/J mice. J Biol Chem 2009; 284:24644-52.
28. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 2004;84:277-359.
29. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A coldinducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998;92:829-39.
30. Zechner R, Zimmermann R, Eichmann TO, Kohlwein SD, Haemmerle G, Lass A, et al. FAT SIGNALS-lipases and lipolysis in lipid metabolism and signaling. Cell Metab 2012;15:279-91.
31. Deng Y, Scherer PE. Adipokines as novel biomarkers and regulators of the metabolic syndrome. Ann N Y Acad Sci 2010;1212:E1-19. [32] Grinspoon S, Thomas L, Miller K, Pitts S, Herzog D, Klibanski A. Changes in regional fat redistribution and the effects of estrogen during spontaneous weight gain in women with anorexia nervosa. Am J Clin Nutr 2001;73:865-9.
32. Grinspoon S, Thomas L, Miller K, Pitts S, Herzog D, Klibanski A. Changes in regional fat redistribution and the effects of estrogen during spontaneous weight gain in women with anorexia nervosa. Am J Clin Nutr 2001;73:865-9
33. Mayer L, Walsh BT, Pierson RN, Heymsfield SB, Gallagher D, Wang J, et al. Body fat redistribution after weight gain in women with anorexia nervosa. Am J Clin Nutr 2005;81:1286-91.
34. Dulloo AG, Seydoux J, Jacquet J. Adaptive thermogenesis and uncoupling proteins: a reappraisal of their roles in fat metabolism and energy balance. Physiol Behav 2004;83:587-602.
35. Richard D, Picard F. Brown fat biology and thermogenesis. Front Biosci (Landmark Ed) 2011;16:1233-60.
36. Einstein FH, Atzmon G, Yang XM, Ma XH, Rincon M, Rudin E, et al. Differential responses of visceral and subcutaneous fat depots to nutrients. Diabetes 2005;54: 672-8.
37. Lee MJ, Fried SK. Integration of hormonal and nutrient signals that regulate leptin synthesis and secretion. Am J Physiol Endocrinol Metab 2009;296:E1230-8.
38. DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, Felber JP. The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 1981;30:1000-7.
39. Birkenfeld AL, Shulman GI. Nonalcoholic fatty liver disease, hepatic insulin resistance, and type 2 diabetes. Hepatology 2014;59:713-23.
40. Lebovitz HE, Banerji MA. Point: visceral adiposity is causally related to insulin resistance. Diabetes Care 2005;28:2322-5.
41. Miles JM, Jensen MD. Counterpoint: visceral adiposity is not causally related to insulin resistance. Diabetes Care 2005;28:2326-8.
42. Arble DM, Ramsey KM, Bass J, Turek FW. Circadian disruption and metabolic disease: findings from animal models. Best Pract Res Clin Endocrinol Metab 2010; 24:785-800.
43. Arble DM, Bass J, Laposky AD, Vitaterna MH, Turek FW. Circadian timing of food intake contributes to weight gain. Obesity (Silver Spring) 2009;17:2100-2.