Post-restriction hyperphagia and metabolic responses to short-term calorie restriction in C57BL/6 mice
Main Article Content
Abstract
Aims: To evaluate post-restriction hyperphagia (PRH) responses to short-term calorie restriction (CR) and the potential drivers of this behaviour.
Methods: Adult male C57BL/6J mice underwent 30% CR for 5 to 30 days, then refed for 12 days. Energy intake, body mass, fat mass, fat-free mass, body temperature, and physical activity were measured continuously throughout the CR and re-feeding phases and daily energy expenditure was measured over final 2 days of CR and the first 5 days of re-feeding.
Results: Following restriction, energy intake, body mass, fat free mass, body temperature and daily energy expenditure were reduced in all groups compared to controls (P<0.05). Only the 20d and 25d groups had significantly lower fat mass than controls (P=0.004). Total physical activity and dark-phase physical activity did not differ between control and CR groups (P=0.446 and 0.380 respectively); but light-phase physical activity of groups 20d, 25d and 30d increased significantly (P<0.001) due to food anticipatory activity. All CR groups displayed peak PRH on day1 of refeeding. Total energy intake over the following 2-5 days of refeeding was also greater than the controls (P=0.002). The magnitude of PRH increased with CR duration and body mass loss at the individual level (P<0.001). In a multiple regression analysis fat free mass loss was the main factor that was correlated with the level of PRH (Multiple regression R2=32.7%, fat mass P=0.036, fat free mass P=0.003).
Conclusion: Hunger (reflected by PRH) was mostly related to body mass and fat free mass loss. The effect of fat free mass loss was the opposite of that expected if fat free mass is a key driver of food intake as recently postulated. Developing restriction protocols that minimize loss of fat free mass may reduce the level of hunger that emerges when individuals are under restriction.
Keywords:
Energy Intake, Calorie Restriction, Fat mass, Fat-free mass, Post-restriction Hyperphagia
Article Details
How to Cite
UDOH, Emem P. et al.
Post-restriction hyperphagia and metabolic responses to short-term calorie restriction in C57BL/6 mice.
Medical Research Archives, [S.l.], v. 12, n. 8, aug. 2024.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/5553>. Date accessed: 06 sep. 2024.
doi: https://doi.org/10.18103/mra.v12i8.5553.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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26. Hambly C, Duncan JS, Archer ZA, Moar KM, Mercer JG, Speakman JR. Repletion of TNFα or leptin in calorically restricted mice suppresses post-restriction hyperphagia. Disease Models & Mechanisms. 2012;5(1):83-94.
27. Dulloo AG. Collateral fattening: When a deficit in lean body mass drives overeating. Obesity. 2017;25(2):277-279.
28. Dulloo AG, Jacquet J, Girardier L. Poststarvation hyperphagia and body fat overshooting in humans: A role for feedback signals from lean and fat tissues. Am J Clin Nutr. 1997;65(3):717-723.
29. Dulloo AG. Human pattern of food intake and fuel-partitioning during weight recovery after starvation: A theory of autoregulation of body composition. Proc Nutr Soc. 1997;56(1A):25-40.
30. Blundell JE, Finlayson G, Gibbons C, Caudwell P, Hopkins M. The biology of appetite control: Do resting metabolic rate and fat-free mass drive energy intake? Physiol Behav. 2015;152:473-478.
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32. Blundell JE, Gibbons C, Beaulieu K, et al. The drive to eat in homo sapiens: Energy expenditure drives energy intake. Physiol Behav. 2020;219:112846.
33. Hopkins M, Gibbons C, Blundell J. Fat-free mass and resting metabolic rate are determinants of energy intake: Implications for a theory of appetite control. Philosophical Transactions of the Royal Society B. 2023;378(1885):20220213.
34. Perry RJ, Resch JM, Douglass AM, et al. Leptin’s hunger-suppressing effects are mediated by the hypothalamic–pituitary–adrenocortical axis in rodents. Proceedings of the National Academy of Sciences. 2019;116(27):13670-13679.
35. Lee YH, Kim Y, Kim KS, et al. Lateral hypothalamic leptin receptor neurons drive hunger-gated food-seeking and consummatory behaviours in male mice. Nature Communications. 2023;14(1):1486.
36. Vaanholt LM, Magee V, Speakman JR. Factors predicting individual variability in Diet‐Induced weight loss in MF1 mice. Obesity. 2012;20(2):285-294.
37. Weir JB. New methods for calculating metabolic rate with special reference to protein metabolism. Nutrition. 1990;6:213-221.
38. Johnston SL, Peacock WL, Bell LM, Lonchampt M, Speakman JR. PIXImus DXA with different software needs individual calibration to accurately predict fat mass. Obesity. 2005;13(9):1558-1565.
39. Suchacki KJ, Thomas BJ, Ikushima YM, et al. The effects of caloric restriction on adipose tissue and metabolic health are sex-and age-dependent. Elife. 2023;12:e88080.
40. de Souza GO, Wasinski F, Donato Jr J. Characterization of the metabolic differences between male and female C57BL/6 mice. Life Sci. 2022;301:120636.
41. Xu J, Xu X, Bi Z, Shi L, Cao J, Zhao Z. The less weight loss due to modest food restriction drove more fat accumulation in striped hamsters refed with high–fat diet. Horm Behav. 2019;110:19-28.
42. Gao W, Zhu W, Ye F, Zuo M, Wang Z. Plasticity in food intake, thermogenesis and body mass in the tree shrew (tupaia belangeri) is affected by food restriction and refeeding. Animal Biology. 2016;66(2):201-217.
43. Wang H, He W, Yang G, Zhu L, Liu X. The impact of weight cycling on health and obesity. Metabolites. 2024;14(6):344.
44. Dulloo AG, Miles-Chan JL, Schutz Y. Collateral fattening in body composition autoregulation: Its determinants and significance for obesity predisposition. Eur J Clin Nutr. 2018;72(5):657-664.
45. Bond ND, Guo J, Hall KD, McPherron AC. Modeling energy dynamics in mice with skeletal muscle hypertrophy fed high calorie diets. International Journal of Biological Sciences. 2016;12(5):617.
46. Dulloo AG, Jacquet J, Montani J, Schutz Y. How dieting makes the lean fatter: From a perspective of body composition autoregulation through adipostats and proteinstats awaiting discovery. Obesity Reviews. 2015;16(S1):25-35.
47. Smith Jr DL, Yang Y, Mestre LM, et al. Impact of sustained calorie restriction and weight cycling on body composition in high‐fat diet‐fed male and female C57BL/6J mice. Obesity. 2024;32(5):959-968.
48. Fernández MAR, Vilca CMC, Batista LO, Ramos VW, Cinelli LP, de Albuquerque KT. Intermittent food restriction in female rats induces SREBP high expression in hypothalamus and immediately postfasting hyperphagia. Nutrition. 2018;48:122-126.
49. McClain AD, Otten JJ, Hekler EB, Gardner CD. Adherence to a low‐fat vs. low‐carbohydrate diet differs by insulin resistance status. Diabetes, Obesity and Metabolism. 2013;15(1):87-90.
50. Smyers ME, Bachir KZ, Britton SL, Koch LG, Novak CM. Physically active rats lose more weight during calorie restriction. Physiol Behav. 2015;139:303-313.
51. Hambly C, Speakman JR. Mice that gorged during dietary restriction increased foraging related behaviors and differed in their macronutrient preference when released from restriction. PeerJ. 2015;3:e1091.
52. Gutman R, Yosha D, Choshniak I, Kronfeld-Schor N. Two strategies for coping with food shortage in desert golden spiny mice. Physiol Behav. 2007;90(1):95-102.
53. Calonne J, Arsenijevic D, Scerri I, Miles-Chan JL, Montani J, Dulloo AG. Low 24-hour core body temperature as a thrifty metabolic trait driving catch-up fat during weight regain after caloric restriction. American Journal of Physiology-Endocrinology and Metabolism. 2019;317(4):E699-E709.
54. Schubert KA, Boerema AS, Vaanholt LM, de Boer SF, Strijkstra AM, Daan S. Daily torpor in mice: High foraging costs trigger energy-saving hypothermia. Biol Lett. 2010;6(1):132-135.
55. Canale CI, Perret M, Thery M, Henry PY. Physiological flexibility and acclimation to food shortage in a heterothermic primate. J Exp Biol. 2011;214(Pt 4):551-560.
56. Minderis P, Fokin A, Povilonis T, Kvedaras M, Ratkevicius A. Effects of diet macronutrient composition on weight loss during caloric restriction and subsequent weight regain during refeeding in aging mice. Nutrients. 2023;15(22):4836.
57. Zhong W, Wang H, Yang Y, et al. High-protein diet prevents fat mass increase after dieting by counteracting lactobacillus-enhanced lipid absorption. Nature Metabolism. 2022;4(12):1713-1731.
58. Huo D, Bao M, Cao J, Zhao Z. Cold exposure prevents fat accumulation in striped hamsters refed a high-fat diet following food restriction. BMC zoology. 2022;7(1):19.
59. Zhao Z, Derous D, Gerrard A, et al. Limits to sustained energy intake. XXX. constraint or restraint? manipulations of food supply show peak food intake in lactation is constrained. J Exp Biol. 2020;223(8):jeb208314.
60. Mitchell SE, Delville C, Konstantopedos P, et al. The effects of graded levels of calorie restriction: V. impact of short term calorie and protein restriction on physical activity in the C57BL/6 mouse. Oncotarget. 2016;7:19147-19170.
61. Froy O. The relationship between nutrition and circadian rhythms in mammals. Front Neuroendocrinol. 2007;28(2-3):61-71.
62. Hsu JL, Yu L, Sullivan E, Bowman M, Mistlberger RE, Tecott LH. Enhanced food anticipatory activity associated with enhanced activation of extrahypothalamic neural pathways in serotonin2C receptor null mutant mice. PLoS ONE. 2010;5(7):e11802.
63. Gallardo CM, Hsu CT, Gunapala KM, et al. Behavioral and neural correlates of acute and scheduled hunger in C57BL/6 mice. PloS one. 2014;9(5):e95990.
64. Norren K, Rusli F, Dijk M, et al. Behavioural changes are a major contributing factor in the reduction of sarcopenia in caloric‐restricted ageing mice. Journal of Cachexia, Sarcopenia and Muscle. 2015;6(3):253-268.
2. Speakman JR, Mitchell SE. Caloric restriction. Mol Aspects Med. 2011;32(3):159-221.
3. Green CL, Lamming DW, Fontana L. Molecular mechanisms of dietary restriction promoting health and longevity. Nature Reviews Molecular Cell Biology. 2021:1-18.
4. Hofer SJ, Carmona‐Gutierrez D, Mueller MI, Madeo F. The ups and downs of caloric restriction and fasting: From molecular effects to clinical application. EMBO Molecular Medicine. 2022;14(1):e14418.
5. Mockett RJ, Cooper TM, Orr WC, Sohal RS. Effects of caloric restriction are species-specific. Biogerontology. 2006;7:157-160.
6. Speakman JR, Mitchell SE, Mazidi M. Calories or protein? the effect of dietary restriction on lifespan in rodents is explained by calories alone. Exp Gerontol. 2016;86:28-38.
7. Mitchell SE, Togo J, Green CL, Derous D, Hambly C, Speakman JR. The effects of graded levels of calorie restriction: XX. impact of long term graded calorie restriction on survival and body mass dynamics in male C57BL/6J mice. The Journals of Gerontology: Series A. 2023;78:1953-1963. doi: rg/10.1093/gerona/glad152.
8. Mitchell SJ, Madrigal-Matute J, Scheibye-Knudsen M, et al. Effects of sex, strain, and energy intake on hallmarks of aging in mice. Cell metabolism. 2016;23(6):1093-1112.
9. Forster M, Morris P, Sohal R. Genotype of age influence the effect of caloric intake on mortality in mice. FASEB J. 2003;17:690-692.
10. Liao C, Rikke BA, Johnson TE, Diaz V, Nelson JF. Genetic variation in the murine lifespan response to dietary restriction: From life extension to life shortening. Aging Cell. 2010;9(1):92-95.
11. Burnett C, Valentini S, Cabreiro F, et al. Absence of effects of Sir2 overexpression on lifespan in C. elegans and drosophila. Nature. 2011;477(7365):482-485.
12. Redman LM, Ravussin E. Caloric restriction in humans: Impact on physiological, psychological, and behavioral outcomes. Antioxidants & Redox Signaling. 2010;14(2):275-287.
13. Most J, Tosti V, Redman LM, Fontana L. Calorie restriction in humans: An update. Ageing research reviews. 2017;39:36-45.
14. Flanagan EW, Most J, Mey JT, Redman LM. Calorie restriction and aging in humans. Annu Rev Nutr. 2020;40:105-133.
15. Speakman JR, Hambly C. Starving for life: What animal studies can and cannot tell us about the use of caloric restriction to prolong human lifespan. J Nutr. 2007;137(4):1078-1086.
16. Hambly C, Mercer JG, Speakman JR. Hunger does not diminish over time in mice under protracted caloric restriction. Rejuvenation Res. 2007;10(4):533-542.
17. Derous D, Mitchell SE, Green CL, et al. The effects of graded levels of calorie restriction: VI. impact of short-term graded calorie restriction on transcriptomic responses of the hypothalamic hunger and circadian signaling pathways. Aging (Albany NY). 2016;8(4):642-663.
18. Mann T, Tomiyama AJ, Westling E, Lew A, Samuels B, Chatman J. Medicare's search for effective obesity treatments: Diets are not the answer. Am Psychol. 2007;62(3):220-233.
19. Keim NL, Stern JS, Havel PJ. Relation between circulating leptin concentrations and appetite during a prolonged, moderate energy deficit in women. Am J Clin Nutr. 1998;68(4):794-801.
20. Adam TC, Westerterp-Plantenga MS. Glucagon-like peptide-1 release and satiety after a nutrient challenge in normal-weight and obese subjects. Br J Nutr. 2005;93(6):845-851.
21. Pasman WJ, Saris WH, Westerterp‐Plantenga MS. Predictors of weight maintenance. Obes Res. 1999;7(1):43-50.
22. McGuire MT, Wing RR, Klem ML, Lang W, Hill JO. What predicts weight regain in a group of successful weight losers? J Consult Clin Psychol. 1999;67(2):177-185.
23. Anton SD, Han H, York E, Martin CK, Ravussin E, Williamson DA. Effect of calorie restriction on subjective ratings of appetite. J Hum Nutr Diet . 2009;22(2):141-147.
24. Mitchell SE, Tang ZH, Kerbois C, et al. The effects of graded levels of calorie restriction: I. impact of short term calorie and protein restriction on body composition in the C57BL/6 mouse. Oncotarget. 2015;6(18):15902-15930.
25. Hambly C, Speakman JR. Contribution of different mechanisms to compensation for energy restriction in the mouse. Obes Res. 2005;13(9):1548-1557.
26. Hambly C, Duncan JS, Archer ZA, Moar KM, Mercer JG, Speakman JR. Repletion of TNFα or leptin in calorically restricted mice suppresses post-restriction hyperphagia. Disease Models & Mechanisms. 2012;5(1):83-94.
27. Dulloo AG. Collateral fattening: When a deficit in lean body mass drives overeating. Obesity. 2017;25(2):277-279.
28. Dulloo AG, Jacquet J, Girardier L. Poststarvation hyperphagia and body fat overshooting in humans: A role for feedback signals from lean and fat tissues. Am J Clin Nutr. 1997;65(3):717-723.
29. Dulloo AG. Human pattern of food intake and fuel-partitioning during weight recovery after starvation: A theory of autoregulation of body composition. Proc Nutr Soc. 1997;56(1A):25-40.
30. Blundell JE, Finlayson G, Gibbons C, Caudwell P, Hopkins M. The biology of appetite control: Do resting metabolic rate and fat-free mass drive energy intake? Physiol Behav. 2015;152:473-478.
31. Stubbs RJ, Hopkins M, Finlayson GS, Duarte C, Gibbons C, Blundell JE. Potential effects of fat mass and fat-free mass on energy intake in different states of energy balance. Eur J Clin Nutr. 2018;72(5):698-709.
32. Blundell JE, Gibbons C, Beaulieu K, et al. The drive to eat in homo sapiens: Energy expenditure drives energy intake. Physiol Behav. 2020;219:112846.
33. Hopkins M, Gibbons C, Blundell J. Fat-free mass and resting metabolic rate are determinants of energy intake: Implications for a theory of appetite control. Philosophical Transactions of the Royal Society B. 2023;378(1885):20220213.
34. Perry RJ, Resch JM, Douglass AM, et al. Leptin’s hunger-suppressing effects are mediated by the hypothalamic–pituitary–adrenocortical axis in rodents. Proceedings of the National Academy of Sciences. 2019;116(27):13670-13679.
35. Lee YH, Kim Y, Kim KS, et al. Lateral hypothalamic leptin receptor neurons drive hunger-gated food-seeking and consummatory behaviours in male mice. Nature Communications. 2023;14(1):1486.
36. Vaanholt LM, Magee V, Speakman JR. Factors predicting individual variability in Diet‐Induced weight loss in MF1 mice. Obesity. 2012;20(2):285-294.
37. Weir JB. New methods for calculating metabolic rate with special reference to protein metabolism. Nutrition. 1990;6:213-221.
38. Johnston SL, Peacock WL, Bell LM, Lonchampt M, Speakman JR. PIXImus DXA with different software needs individual calibration to accurately predict fat mass. Obesity. 2005;13(9):1558-1565.
39. Suchacki KJ, Thomas BJ, Ikushima YM, et al. The effects of caloric restriction on adipose tissue and metabolic health are sex-and age-dependent. Elife. 2023;12:e88080.
40. de Souza GO, Wasinski F, Donato Jr J. Characterization of the metabolic differences between male and female C57BL/6 mice. Life Sci. 2022;301:120636.
41. Xu J, Xu X, Bi Z, Shi L, Cao J, Zhao Z. The less weight loss due to modest food restriction drove more fat accumulation in striped hamsters refed with high–fat diet. Horm Behav. 2019;110:19-28.
42. Gao W, Zhu W, Ye F, Zuo M, Wang Z. Plasticity in food intake, thermogenesis and body mass in the tree shrew (tupaia belangeri) is affected by food restriction and refeeding. Animal Biology. 2016;66(2):201-217.
43. Wang H, He W, Yang G, Zhu L, Liu X. The impact of weight cycling on health and obesity. Metabolites. 2024;14(6):344.
44. Dulloo AG, Miles-Chan JL, Schutz Y. Collateral fattening in body composition autoregulation: Its determinants and significance for obesity predisposition. Eur J Clin Nutr. 2018;72(5):657-664.
45. Bond ND, Guo J, Hall KD, McPherron AC. Modeling energy dynamics in mice with skeletal muscle hypertrophy fed high calorie diets. International Journal of Biological Sciences. 2016;12(5):617.
46. Dulloo AG, Jacquet J, Montani J, Schutz Y. How dieting makes the lean fatter: From a perspective of body composition autoregulation through adipostats and proteinstats awaiting discovery. Obesity Reviews. 2015;16(S1):25-35.
47. Smith Jr DL, Yang Y, Mestre LM, et al. Impact of sustained calorie restriction and weight cycling on body composition in high‐fat diet‐fed male and female C57BL/6J mice. Obesity. 2024;32(5):959-968.
48. Fernández MAR, Vilca CMC, Batista LO, Ramos VW, Cinelli LP, de Albuquerque KT. Intermittent food restriction in female rats induces SREBP high expression in hypothalamus and immediately postfasting hyperphagia. Nutrition. 2018;48:122-126.
49. McClain AD, Otten JJ, Hekler EB, Gardner CD. Adherence to a low‐fat vs. low‐carbohydrate diet differs by insulin resistance status. Diabetes, Obesity and Metabolism. 2013;15(1):87-90.
50. Smyers ME, Bachir KZ, Britton SL, Koch LG, Novak CM. Physically active rats lose more weight during calorie restriction. Physiol Behav. 2015;139:303-313.
51. Hambly C, Speakman JR. Mice that gorged during dietary restriction increased foraging related behaviors and differed in their macronutrient preference when released from restriction. PeerJ. 2015;3:e1091.
52. Gutman R, Yosha D, Choshniak I, Kronfeld-Schor N. Two strategies for coping with food shortage in desert golden spiny mice. Physiol Behav. 2007;90(1):95-102.
53. Calonne J, Arsenijevic D, Scerri I, Miles-Chan JL, Montani J, Dulloo AG. Low 24-hour core body temperature as a thrifty metabolic trait driving catch-up fat during weight regain after caloric restriction. American Journal of Physiology-Endocrinology and Metabolism. 2019;317(4):E699-E709.
54. Schubert KA, Boerema AS, Vaanholt LM, de Boer SF, Strijkstra AM, Daan S. Daily torpor in mice: High foraging costs trigger energy-saving hypothermia. Biol Lett. 2010;6(1):132-135.
55. Canale CI, Perret M, Thery M, Henry PY. Physiological flexibility and acclimation to food shortage in a heterothermic primate. J Exp Biol. 2011;214(Pt 4):551-560.
56. Minderis P, Fokin A, Povilonis T, Kvedaras M, Ratkevicius A. Effects of diet macronutrient composition on weight loss during caloric restriction and subsequent weight regain during refeeding in aging mice. Nutrients. 2023;15(22):4836.
57. Zhong W, Wang H, Yang Y, et al. High-protein diet prevents fat mass increase after dieting by counteracting lactobacillus-enhanced lipid absorption. Nature Metabolism. 2022;4(12):1713-1731.
58. Huo D, Bao M, Cao J, Zhao Z. Cold exposure prevents fat accumulation in striped hamsters refed a high-fat diet following food restriction. BMC zoology. 2022;7(1):19.
59. Zhao Z, Derous D, Gerrard A, et al. Limits to sustained energy intake. XXX. constraint or restraint? manipulations of food supply show peak food intake in lactation is constrained. J Exp Biol. 2020;223(8):jeb208314.
60. Mitchell SE, Delville C, Konstantopedos P, et al. The effects of graded levels of calorie restriction: V. impact of short term calorie and protein restriction on physical activity in the C57BL/6 mouse. Oncotarget. 2016;7:19147-19170.
61. Froy O. The relationship between nutrition and circadian rhythms in mammals. Front Neuroendocrinol. 2007;28(2-3):61-71.
62. Hsu JL, Yu L, Sullivan E, Bowman M, Mistlberger RE, Tecott LH. Enhanced food anticipatory activity associated with enhanced activation of extrahypothalamic neural pathways in serotonin2C receptor null mutant mice. PLoS ONE. 2010;5(7):e11802.
63. Gallardo CM, Hsu CT, Gunapala KM, et al. Behavioral and neural correlates of acute and scheduled hunger in C57BL/6 mice. PloS one. 2014;9(5):e95990.
64. Norren K, Rusli F, Dijk M, et al. Behavioural changes are a major contributing factor in the reduction of sarcopenia in caloric‐restricted ageing mice. Journal of Cachexia, Sarcopenia and Muscle. 2015;6(3):253-268.