Volume 32, Issue 4 (July 2021)
Studies in Medical Sciences 2021, 32(4): 290-302 |
Back to browse issues page
Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
Daneshyar S, OmidAli F, Feizipour S A. THE COMBINED EFFECT OF LONG-TERM FEEDING OF HIGH-FAT DIET AND REGULAR AEROBIC TRAINING ON GENE EXPRESSION OF UNCOUPLING PROTEIN 1 (UCP1) IN BROWN ADIPOSE TISSUE AND SARCOLIPIN (SLN) IN SOLEUS MUSCLE OF MICE: AN EXPERIMENTAL STUDY. Studies in Medical Sciences 2021; 32 (4) :290-302
URL: http://umj.umsu.ac.ir/article-1-5341-en.html
URL: http://umj.umsu.ac.ir/article-1-5341-en.html
Department of Physical Education, Faculty of Humanities, Ayatollah Alozma Boroujerdi University, Lorestan, Iran (Corresponding Author) , s.daneshyar@abru.ac.ir
Abstract: (1984 Views)
Background & Aims: Uncoupling protein 1 (UCP1) and Sarcolipin (SLN) are regulator proteins in non-shivering thermogenesis in brown adipose tissue and skeletal muscle (SM), respectively. This study aimed to investigate the combined effects of long-term feeding of a high-fat diet and regular aerobic training on its gene expression in mice.
Materials & Methods: 28 mice were assigned into four groups including; 1) control (n=7), 2) High Fat Diet (HFD), 3) Aerobic Training (AT) (n=7), and 4) High Fat Diet- Aerobic Training (HFD-AT) (n=7). The subjects of the HFD group were fed with a high-fat diet (fat= 45%) for 12 weeks. The mice of AT group underwent aerobic training on a treadmill for six weeks. HFD-AT group underwent the aerobic training in addition to a high fat diet. The Real-Time–PCR method was used to measure the gene expression of UCP1 and SLN.
Results: Data showed that the aerobic training did not significantly affect the expressions of UCP1 and SLN (p=0.17; p=0.87). However, a high-fat diet caused an increase (approximately three-fold) in the expression of UCP1 and SLN (p=0.0006; p=0.009). Basically, the aerobic training prevented the HFD-induced increase of UCP1 and SLN (p=0.29; p=0.49).
Conclusion: These results indicated that regular aerobic training could limit the increasing effect of the high-fat diet on thermogenic factors, i.e., UCP1 and SLN. Based on this, it seems that aerobic training could modulate diet-induced thermogenesis by these regulating mechanisms.
Materials & Methods: 28 mice were assigned into four groups including; 1) control (n=7), 2) High Fat Diet (HFD), 3) Aerobic Training (AT) (n=7), and 4) High Fat Diet- Aerobic Training (HFD-AT) (n=7). The subjects of the HFD group were fed with a high-fat diet (fat= 45%) for 12 weeks. The mice of AT group underwent aerobic training on a treadmill for six weeks. HFD-AT group underwent the aerobic training in addition to a high fat diet. The Real-Time–PCR method was used to measure the gene expression of UCP1 and SLN.
Results: Data showed that the aerobic training did not significantly affect the expressions of UCP1 and SLN (p=0.17; p=0.87). However, a high-fat diet caused an increase (approximately three-fold) in the expression of UCP1 and SLN (p=0.0006; p=0.009). Basically, the aerobic training prevented the HFD-induced increase of UCP1 and SLN (p=0.29; p=0.49).
Conclusion: These results indicated that regular aerobic training could limit the increasing effect of the high-fat diet on thermogenic factors, i.e., UCP1 and SLN. Based on this, it seems that aerobic training could modulate diet-induced thermogenesis by these regulating mechanisms.
Type of Study: Research |
Subject:
Exercise physiology
References
1. Joosen AM, Westerterp KR. Energy expenditure during overfeeding. Nutr Metab 2006; 3(1): 25 [DOI:10.1186/1743-7075-3-25] [PMID] [PMCID]
2. Calcagno M, Kahleova H, Alwarith J, Burgess NN, Flores RA, Busta ML, et al. The Thermic Effect of Food: A Review. J Am Coll Nutr 2011; 38(6): 547-51. [DOI:10.1080/07315724.2018.1552544] [PMID]
3. Westerterp KR. Diet induced thermogenesis. Nutr Metab (Lond) 2004; 1(1): 1-5.
https://doi.org/10.1186/1743-7075-1-5 [DOI:10.1186/1743-7075-1-1] [PMID] [PMCID]
4. Rosenbaum M,Leibel RL. Adaptive thermogenesis in humans. Int J Obes 2010; 34(1): S47-55. [DOI:10.1038/ijo.2010.184] [PMID] [PMCID]
5. Dulloo AG, Jacquet J, Montani JP, Schutz Y. Adaptive thermogenesis in human body weight regulation: more of a concept than a measurable entity? Obes Rev 2012; 13(2):105-21. [DOI:10.1111/j.1467-789X.2012.01041.x] [PMID]
6. von Essen G, Lindsund E, Cannon B, Nedergaard J. Adaptive facultative diet-induced thermogenesis in wild-type but not in UCP1-ablated mice. Am J Physiol Endocrinol Metab 2017; 313(5): E515-27. [DOI:10.1152/ajpendo.00097.2017] [PMID]
7. Saito M, Matsushita M, Yoneshiro T, Okamatsu-Ogura Y. Brown Adipose Tissue, Diet-Induced Thermogenesis, and Thermogenic Food Ingredients: From Mice to Men. Front Endocrinol 2020;11:222. [DOI:10.3389/fendo.2020.00222] [PMID] [PMCID]
8. García-Ruiz E, Reynés B, Díaz-Rúa R, Ceresi E, Oliver P, Palou A. The intake of high-fat diets induces the acquisition of brown adipocyte gene expression features in white adipose tissue. Int J Obes 2015; 39(11):1619-29. [DOI:10.1038/ijo.2015.112] [PMID]
9. Hansen IR, Jansson KM, Cannon B, Nedergaard J. Contrasting effects of cold acclimation versus obesogenic diets on chemerin gene expression in brown and brite adipose tissues. Biochim Biophys Acta Mol Cell Biol Lipids 2014; 1841(12):1691-9. [DOI:10.1016/j.bbalip.2014.09.003] [PMID]
10. Weiner J, Rohde K, Krause K, Zieger K, Klöting N, Kralisch S, et al. Brown adipose tissue (BAT) specific vaspin expression is increased after obesogenic diets and cold exposure and linked to acute changes in DNA-methylation. Mol Metab 2017; 6 (6): 482-93. [DOI:10.1016/j.molmet.2017.03.004] [PMID] [PMCID]
11. Da Eira DP. High-Fat Diet Enhances Triglyceride Recycling, Impairs UCP1-Mediated Thermogenic Activity, and Causes Insulin Resistance in Rat Brown Adipocytes. yorkspace.library.yorku.ca. 2019. [Google Scholar]
12. Wu MV, Bikopoulos G, Hung S, Ceddia RB. Thermogenic capacity is antagonistically regulated in classical brown and white subcutaneous fat depots by high fat diet and endurance training in rats impact on whole-body energy expenditure. J Biol Chem 2014; 289 (49): 34129-40. [DOI:10.1074/jbc.M114.591008] [PMID] [PMCID]
13. de Queiroz KB, Rodovalho GV, Guimaraes JB, de Lima DC, Coimbra CC, Evangelista EA, et al. Endurance training blocks uncoupling protein 1 up-regulation in brown adipose tissue while increasing uncoupling protein 3 in the muscle tissue of rats fed with a high-sugar diet. Nutr Res 2012; 32 (9): 709-717. [DOI:10.1016/j.nutres.2012.06.020] [PMID]
14. Xu X, Ying Z, Cai M, Xu Z, Li Y, Jiang SY, et al. Exercise ameliorates high-fat diet-induced metabolic and vascular dysfunction, and increases adipocyte progenitor cell population in brown adipose tissue. Am J Physiol Regul Integr Comp Physiol 2011; 300 (5): R1115-25. [DOI:10.1152/ajpregu.00806.2010] [PMID] [PMCID]
15. Shirkhani S, Marandi SM, Kazeminasab F, Esmaeili M, Ghaedi K, Esfarjani F, et al. Comparative studies on the effects of high-fat diet, endurance training and obesity on Ucp1 expression in male C57BL/6 mice. Gene 2018; 676: 16-21. [DOI:10.1016/j.gene.2018.07.015] [PMID]
16. Bombardier E, Smith IC, Gamu D, Fajardo VA, Vigna C, Sayer RA, et al. Sarcolipin trumps β-adrenergic receptor signaling as the favored mechanism for muscle-based diet-induced thermogenesis. FASEB J 2013; 27 (9): 3871-8. [DOI:10.1096/fj.13-230631] [PMID] [PMCID]
17. Periasamy M, Herrera JL, Reis FC. Skeletal muscle thermogenesis and its role in whole body energy metabolism. Diabetes Metab J 2017; 41 (5): 327-36. [DOI:10.4093/dmj.2017.41.5.327] [PMID] [PMCID]
18. Rowland LA, Bal NC, Periasamy M. The role of skeletal‐muscle‐based thermogenic mechanisms in vertebrate endothermy. Biol Rev 2015; 90 (4): 1279-97. [DOI:10.1111/brv.12157] [PMID] [PMCID]
19. Bal NC, Maurya SK, Singh S, Wehrens XH, Periasamy M. Increased reliance on muscle-based thermogenesis upon acute minimization of brown adipose tissue function. J Biol Chem 2016; 291 (33): 17247-57. [DOI:10.1074/jbc.M116.728188] [PMID] [PMCID]
20. Rowland LA, Maurya SK, Bal NC, Kozak L, Periasamy M. Sarcolipin and uncoupling protein 1 play distinct roles in diet‐induced thermogenesis and do not compensate for one another. Obesity 2016; 24 (7): 1430-3. [DOI:10.1002/oby.21542] [PMID] [PMCID]
21. Smith IC, Bombardier E, Vigna C, Tupling AR. ATP consumption by sarcoplasmic reticulum Ca2+ pumps accounts for 40-50% of resting metabolic rate in mouse fast and slow twitch skeletal muscle. PloS one 2013; 8(7): e68924. [DOI:10.1371/journal.pone.0068924] [PMID] [PMCID]
22. Periasamy M, Maurya SK, Sahoo SK, Singh S, Reis FC, Bal NC. Role of SERCA pump in muscle thermogenesis and metabolism. Compr Physiol 2011; 7(3): 879-90. [DOI:10.1002/cphy.c160030] [PMID]
23. Pant M, Bal NC, Periasamy M. Sarcolipin: a key thermogenic and metabolic regulator in skeletal muscle. Trends Endocrinol Metab 2016; 27 (12): 881-92. [DOI:10.1016/j.tem.2016.08.006] [PMID] [PMCID]
24. Campbell KL, Dicke AA. Sarcolipin makes heat, but is it adaptive thermogenesis? Front Physiol 2018; 9: 714. [DOI:10.3389/fphys.2018.00714] [PMID] [PMCID]
25. Gamu D, Juracic ES, Hall KJ, Tupling AR. The sarcoplasmic reticulum and SERCA: a nexus for muscular adaptive thermogenesis. Appl Physiol Nutr Metab 2020;45(1):1-10. [DOI:10.1139/apnm-2019-0067] [PMID]
26. Gamu D, Bombardier E, Smith IC, Fajardo VA, Tupling AR. Sarcolipin provides a novel muscle-based mechanism for adaptive thermogenesis. Exerc Sport Sci Rev 2014; 42 (3): 136-42. [DOI:10.1249/JES.0000000000000016] [PMID]
27. Bal NC, Periasamy M. Uncoupling of sarcoendoplasmic reticulum calcium ATPase pump activity by sarcolipin as the basis for muscle non-shivering thermogenesis. Philos Trans R Soc Lond B Biol Sci 2020; 375 (1793): 20190135. [DOI:10.1098/rstb.2019.0135] [PMID] [PMCID]
28. Bal NC, Maurya SK, Sopariwala DH, Sahoo SK, Gupta SC, Shaikh SA, et al. Sarcolipin is a newly identified regulator of muscle-based thermogenesis in mammals. Nat Med 2012; 18 (10): 1575. [DOI:10.1038/nm.2897] [PMID] [PMCID]
29. Maurya SK, Bal NC, Sopariwala DH, Pant M, Rowland LA, Shaikh SA, et al. Sarcolipin is a key determinant of the basal metabolic rate, and its overexpression enhances energy expenditure and resistance against diet-induced obesity. J Biol Chem 2015; 290 (17): 10840-9. [DOI:10.1074/jbc.M115.636878] [PMID] [PMCID]
30. Maurya SK, Herrera JL, Sahoo SK, Reis FC, Vega RB, Kelly DP, et al. Sarcolipin signaling promotes mitochondrial biogenesis and oxidative metabolism in skeletal muscle. Cell Rep 2018; 24 (11): 2919-31. [DOI:10.1016/j.celrep.2018.08.036] [PMID] [PMCID]
31. Swift DL, Johannsen NM, Lavie CJ, Earnest CP, Church TS. The role of exercise and physical activity in weight loss and maintenance. Prog Cardiovasc Dis 2014; 56 (4): 441-7. [DOI:10.1016/j.pcad.2013.09.012] [PMID] [PMCID]
32. Aldiss P, Lewis JE, Lupini I, Bloor I, Chavoshinejad R, Boocock DJ, et al. Exercise training in obese rats does not induce browning at thermoneutrality and induces a muscle-like signature in brown adipose tissue. Front Endocrinol 2020; 11: 97. [DOI:10.3389/fendo.2020.00097] [PMID] [PMCID]
33. de Snoo M, Responses of mouse skeletal muscle to endurance exercise. Functional, metabolic, and genomic adaptations. (dissertation). Utrecht University; 2009. [Google Scholar]
34. Hariri N, Thibault L. High-fat diet-induced obesity in animal models. Nutr Res Rev 2010; 23 (2): 270-99. [DOI:10.1017/S0954422410000168] [PMID]
35. Benoit B, Plaisancie P, Awada M, Géloën A, Estienne M, Capel F, et al. High-fat diet action on adiposity, inflammation, and insulin sensitivity depends on the control low-fat diet. Nutr Res 2013; 33 (11): 952-60. [DOI:10.1016/j.nutres.2013.07.017] [PMID]
36. Høydal MA, Wisløff U, Kemi OJ, Ellingsen Ø. Running speed and maximal oxygen uptake in rats and mice: practical implications for exercise training. Eur Heart J 2007; 14 (6): 753-60. [DOI:10.1097/HJR.0b013e3281eacef1] [PMID]
37. Wang Y, Wisloff U, Kemi OJ. Animal models in the study of exercise-induced cardiac hypertrophy. Physiol Res 2010; 59 (5): 633. [DOI:10.33549/physiolres.931928] [PMID]
38. David JM, Chatziioannou AF, Taschereau R, Wang H, Stout DB. The hidden cost of housing practices: using noninvasive imaging to quantify the metabolic demands of chronic cold stress of laboratory mice. Comp Med 2013; 63 (5): 386-91. [Google Scholar]
39. Fischer AW, Cannon B, Nedergaard J. Optimal housing temperatures for mice to mimic the thermal environment of humans: An experimental study. Mol Metab 2018; 7 161-70. [DOI:10.1016/j.molmet.2017.10.009] [PMID] [PMCID]
40. Bastías-Pérez M, Zagmutt S, Soler-Vázquez MC, Serra D, Mera P, Herrero L. Impact of adaptive thermogenesis in mice on the treatment of obesity. Cells 2020; 9 (2): 316. [DOI:10.3390/cells9020316] [PMID] [PMCID]
41. Arras M, Autenried P, Rettich A, Spaeni D, Rülicke T. Optimization of intraperitoneal injection anesthesia in mice: drugs, dosages, adverse effects, and anesthesia depth. Comp Med 2001; 51(5):443-56 [Google Scholar]
42. Pant M, Bal NC, Periasamy M. Cold adaptation overrides developmental regulation of sarcolipin expression in mice skeletal muscle: SOS for muscle-based thermogenesis? J Exp Bio 2015; 218 (15): 2321-5. [DOI:10.1242/jeb.119164] [PMID] [PMCID]
43. Kalinovich AV, de Jong JM, Cannon B, Nedergaard J. UCP1 in adipose tissues: two steps to full browning. Biochimie 2017; 134 127-37. [DOI:10.1016/j.biochi.2017.01.007] [PMID]
44. Parousis A, Carter HN, Tran C, Erlich AT, Mesbah Moosavi ZS, Pauly M, et al. Contractile activity attenuates autophagy suppression and reverses mitochondrial defects in skeletal muscle cells. Autophagy 2018; 14 (11): 1886-97. [DOI:10.1080/15548627.2018.1491488] [PMID] [PMCID]
45. Wong ML, Medrano JF. Real-time PCR for mRNA quantitation. BioTechniques 2005; 39 (1): 75-85. [DOI:10.2144/05391RV01] [PMID]
46. Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 2007; 293 (2): E444-52. [DOI:10.1152/ajpendo.00691.2006] [PMID]
47. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med 2009; 360 (15): 1509-17. [DOI:10.1056/NEJMoa0810780] [PMID] [PMCID]
48. Moura EdOCd, Tanaka K, Gomes MFP, Nogueira E, Gomes R, Estadella D, et al. Comparison between the effects of swimming and treadmill-based aerobic training protocols in diabetic rats. Int J Cardiovasc Sci 2018; 31 (6): 610-8. [DOI:10.5935/2359-4802.20180058]
49. Baptista S, Piloto N, Reis F, Teixeira-de-Lemos E, Garrido A, Dias A, et al. Treadmill running and swimming imposes distinct cardiovascular physiological adaptations in the rat: focus on serotonergic and sympathetic nervous systems modulation. Acta Physiol Hung 2008; 95 (4): 365-81. [DOI:10.1556/APhysiol.2008.0002] [PMID]
50. Wankhade UD, Shen M, Yadav H, Thakali KM. Novel Browning Agents, Mechanisms, and Therapeutic Potentials of Brown Adipose Tissue. Biomed Res Int 2016; 2016: 2365609. [DOI:10.1155/2016/2365609] [PMID] [PMCID]
51. Bachman ES, Dhillon H, Zhang C-Y, Cinti S, Bianco AC, Kobilka BK, et al. βAR signaling required for diet-induced thermogenesis and obesity resistance. Science 2002; 297 (5582): 843-5. [DOI:10.1126/science.1073160] [PMID]
52. Lowell BB, Bachman ES. β-Adrenergic receptors, diet-induced thermogenesis, and obesity. J Biol Chem 2003; 278 (32): 29385-8. [DOI:10.1074/jbc.R300011200] [PMID]
53. Fuller-Jackson J-P, Henry BA. Adipose and skeletal muscle thermogenesis: studies from large animals. Endocrinology 2018; 237 (3): R99-115. [DOI:10.1530/JOE-18-0090] [PMID]
54. Raun SH, Henriquez-Olguín C, Karavaeva I, Ali M, Møller LLV, Kot W, et al. Housing temperature influences exercise training adaptations in mice. Nat Commun 2020; 11 (1): 1560. [DOI:10.1038/s41467-020-15311-y] [PMID] [PMCID]
55. Riedl I, Osler ME, Björnholm M, Egan B, Nader GA, Chibalin AV, et al. AMPKγ3 is dispensable for skeletal muscle hypertrophy induced by functional overload. Am J Physiol Endocrinol Metab 2016; 310 (6): E461-72. [DOI:10.1152/ajpendo.00387.2015] [PMID] [PMCID]
56. Fajardo VA, Rietze BA, Chambers PJ, Bellissimo C, Bombardier E, Quadrilatero J, et al. Effects of sarcolipin deletion on skeletal muscle adaptive responses to functional overload and unload. Am J Physiol Cell Physiol 2017; 313 (2): C154-61. [DOI:10.1152/ajpcell.00291.2016] [PMID]
57. Hughes DC, Ellefsen S, Baar K. Adaptations to Endurance and Strength Training. Cold Spring Harb Perspect Med 2018; 8 (6): a029769. [DOI:10.1101/cshperspect.a029769] [PMID] [PMCID]
58. Ukropec J, Anunciado RV, Ravussin Y, Kozak LP. Leptin is required for uncoupling protein-1-independent thermogenesis during cold stress. Endocrinology 2006; 147 (5): 2468-80. [DOI:10.1210/en.2005-1216] [PMID]
59. Minamisawa S, Uemura N, Sato Y, Yokoyama U, Yamaguchi T, Inoue K, et al. Post‐transcriptional downregulation of sarcolipin mRNA by triiodothyronine in the atrial myocardium. FEBS letters 2006; 580 (9): 2247-52. [DOI:10.1016/j.febslet.2006.03.032] [PMID]
Send email to the article author
| Rights and permissions | |
 |
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
