مطالعات کاربردی علوم زیستی در ورزش

مطالعات کاربردی علوم زیستی در ورزش

تأثیر هشت هفته تمرینات استقامتی، مقاومتی و تناوبی شدید بر بیان ژن‌های SLIT-2 و UCP-1 رت‌‌های نر ویستار چاق

نوع مقاله : مقاله پژوهشی

نویسندگان
1 دانشجوی دکتری،گروه تربیت بدنی و علوم ورزشی، واحد بجنورد،دانشگاه آزاد اسلامی، بجنورد، ایران.
2 استادیار، گروه تربیت بدنی و علوم ورزشی، واحد بجنورد،دانشگاه آزاد اسلامی، بجنورد، ایران.
3 دانشیار گروه تربیت بدنی و علوم ورزشی، واحد بجنورد، دانشگاه آزاد اسلامی، بجنورد، ایران.
چکیده
زمینه و هدف: اضافه وزن و چاقی یک اختلال متابولیکی است که سطوح بافت چربی در این اختلال تأثیرگذار است. هدف از پژوهش حاضر، تأثیر هشت هفته تمرینات استقامتی تداومی، مقاومتی و تناوبی شدید بر بیان لیگاند راهنمای شکاف ۲ (SLIT-2) و پروتئین جفت نشده 1 (UCP-1) رت‌‌های نر ویستار چاق بود. روش تحقیق: برای این منظور، تعداد 36 سر رت نر نژاد ویستار چاق با سن هشت هفته و وزن 40±325 گرم، به‌‌صورت تصادفی به چهار گروه؛ استقامتی تداومی (10 سر)، مقاومتی (هشت سر)، تناوبی شدید (10 سر) و کنترل (هشت سر) تقسیم شدند. رت‌های گروه‌‌های تجربی به‌‌مدت هشت هفته، هفته‌‌ای پنج جلسه تمرینات استقامتی تداومی با شدت70 تا 80 درصد سرعت بیشینه، مقاومتی با شدت 50 تا 120 درصد وزن بدن و تناوبی شدید با شدت 85 تا 90 درصد حداکثر سرعت را انجام دادند و هر هفته 5 درصد به‌‌شدت تمرینات اضافه می‌‌شد. برای اندازه‌‌گیری بیان ژن SLIT-2 و UCP-1 ازروش Real Time-PCR استفاده شد. از روش آماری تحلیل واریانس یک‌‌‌‌راهه و آزمون تعقیبی توکی جهت تعیین اختلاف بین‌‌گروه‌ها در سطح معنی‌‌داری 05/0≥p استفاده شد. یافته‌‌‌‌ها: نتایج پژوهش حاضر نشان داد هر سه مدل تمرینی استقامتی تداومی، مقاومتی و تناوبی شدید سبب افزایش معنی‌‌دار بیان ژن SLIT-2 (001/0 =p) و UCP-1 (001/0 =p) نسبت به گروه کنترل شد، اما تفاوتی بین گروه‌‌های تجربی مشاهده نشد (99/0=p ). نتیجه گیری: بنابر نتایج این پژوهش، پیشنهاد می‌‌شود از تمرینات استقامتی تداومی، مقاومتی و تناوبی شدید که با افزایش بیان ژن‌‌های SLIT-2 و UCP-1 در افزایش لیپولیز تأثیرگذارند، در جهت کاهش وزن استفاده شود.
کلیدواژه‌ها

عنوان مقاله English

The effect of eight-week of intense endurance, resistance and high intensity interval training on SLIT-2 and UCP-1 gene expression in obese male Wistar rats

نویسندگان English

Hosein Kavosi-Hasan Abad 1
Sadegh Cheragh-Birjandi 2
Najmeh Rezaeian 2
Ali Yaghoubi 3
1 Ph.D Candidate, Department of Physical Education and Sport Sciences, Bojnourd Branch, Islamic Azad University, Bojnourd, Iran.
2 Assistant Professor, Department of Physical Education and Sport Sciences, Bojnourd Branch, Islamic Azad University, Bojnourd, Iran.
3 Associate Professor at Department of Physical Education and Sport Sciences, Boj.C., Islamic Azad University, Bojnourd, Iran.
چکیده English

Extended Abstract
Background and Aim: Overweight and obesity have become major global public health concerns, largely driven by sedentary lifestyles, reduced physical activity, and unhealthy dietary habits. These conditions are strongly associated with metabolic disorders, including type 2 diabetes mellitus, dyslipidemia, and cardiovascular diseases. An imbalance between energy intake and energy expenditure is considered the primary cause of obesity, highlighting the importance of lifestyle interventions for its prevention and management. Regular physical exercise is an effective non-pharmacological strategy for weight management, glycemic control, and the improvement of lipid metabolism; however, its physiological benefits depend on the type, intensity, and duration of exercise.. Brown adipose tissue (BAT) plays a critical role in energy expenditure through adaptive thermogenesis. Slit guidance ligand 2 (SLIT-2), a protein reduced in obese individuals, and its C-terminal fragment (SLIT2-C) activate thermogenic pathways via protein kinase A (PKA) and cyclic adenosine monophosphate (cAMP), enhancing lipolysis, mitochondrial density, and uncoupling protein 1 (UCP-1) expression, which promotes browning of white fat. While studies show both resistance and endurance training may upregulate UCP-1, conflicting results exist, and the comparative efficacy of resistance training (RT), continuous endurance training (CET), and high-intensity interval training (HIIT) on SLIT-2 and UCP-1 gene expression in obese male Wistar rats remains unresolved.
Materials and Methods: This experimental laboratory study was conducted on 36 adult male Wistar rats (8 weeks old; mean body weight: 225 ± 40 g) obtained from the Razi Serum Research Institute, Mashhad, Iran. The animals were housed under controlled laboratory conditions at a temperature of 22 ± 5 °C, relative humidity of approximately 45%, and a 12:12-hour light–dark cycle, with free access to standard chow and water. Obesity, defined as a body weight exceeding 300 g at the time of group allocation, was used as the inclusion criterion. Following a one-week familiarization period on a motorized treadmill and a 36-rung rat climbing ladder, the animals were randomly assigned to four groups (n=9 per group): continuous endurance training (CET), resistance training (RT), high-intensity interval training (HIIT), and control. Maximal running speed was determined using an incremental exercise test before the intervention and repeated after four weeks to adjust the training intensity. The CET protocol consisted of a warm-up followed by 30 minutes of continuous running at progressively increasing intensities (60%–70% of maximal running speed) over the eight-week intervention, followed by a cool-down period. The RT protocol involved climbing a weighted ladder for three sets of five repetitions per session, with the load progressively increased from 50% to 120% of body weight throughout the intervention. The HIIT protocol consisted of repeated two-minute running bouts performed at 85%–90% of maximal running speed, interspersed with active recovery intervals, with the number of bouts gradually increasing from six to twelve over the eight-week training period.
Total ribonucleic acid (RNA) was extracted from tissue samples and reverse-transcribed into complementary DNA (cDNA) using a thermocycler-based polymerase chain reaction (PCR) system, with gene expression quantified via real-time PCR using SYBR Green dye and the threshold cycle (Ct) recorded for each sample. After confirming normal data distribution, one-way analysis of variance (ANOVA) was used to examine between-group differences in SLIT-2 and UCP-1 gene expression, followed by Tukey’s post hoc test for pairwise comparisons, with all statistical analyses performed using the Statistical Package for the Social Sciences (SPSS), version 22, at a significance level of p≤0.05.
Findings: One-way ANOVA revealed that eight weeks of CET, RT, and HIIT significantly increased SLIT-2 and UCP-1 gene expression in male Wistar rats compared with control (p≤0.05). Given this significant overall effect, Tukey’s post hoc test was subsequently performed to identify the specific source of between-group differences. For SLIT-2 gene expression, Tukey’s test showed that the CET, RT, and HIIT groups each differed significantly from the control group (p=0.001 for all three comparisons); in contrast, no significant differences were observed among the three exercise groups themselves, whether comparing RT with CET (p=0.82), RT with HIIT (p=0.99), or CET with HIIT (p=0.99).
A similar pattern was observed for UCP-1 gene expression: the CET, RT, and HIIT groups again differed significantly from control (p=0.001 for each comparison), while pairwise comparisons among the exercise groups showed no significant differences (RT vs. CET, p=0.99; RT vs. HIIT, p=0.99; CET vs. HIIT, p=0.99). Both SLIT-2 and UCP-1 gene expression increased markedly following CET, RT, and HIIT relative to the control group, with mean fold-change values ranging from approximately 3.1 to 3.3 across all three exercise groups for both genes, compared with a baseline value of roughly 1.0 in the control group, corresponding to an approximately three-fold increase in relative expression of both genes following each of the three training protocols. Moreover, these findings demonstrate a consistent and statistically robust effect of exercise training on the expression of both genes, regardless of training modality. Therefore, all three training protocols produced comparable increases in SLIT-2 and UCP-1 expression, none of the exercise groups differed significantly from one another in either gene, and this pattern, observed identically across both target genes, suggests that CET, RT, and HIIT were equally effective in upregulating SLIT-2 and UCP-1 expression in this model, with no evidence that any single training modality conferred superior efficacy over the others. The magnitude and direction of change were highly consistent between the two genes, further supporting the reliability of the observed training-induced upregulation across all three exercise protocols in this obese Wistar rat model.
Conclusion: Based on the results, it clear that the mechanisms underlying these adaptations remain incompletely understood, particularly for SLIT-2, whose exercise-related signaling pathways have not previously been characterized. The SLIT-2 is implicated in angiogenesis, anti-inflammatory processes, and lipolysis, and its C-terminal fragment promotes thermogenesis via the protein kinase A (PKA)/cyclic adenosine monophosphate (cAMP) pathway. In this way, the SLIT-2 expression appears to be driven by PRDM16, whose downstream activation may explain the training-induced increases observed here, consistent with prior reports demonstrating that PRDM16 induces SLIT-2 expression. Furthermore, SLIT-2 enhances lipolysis, mitochondrial biogenesis, and PI3K-mediated immune regulation, thereby potentially mitigating obesity-related metabolic dysfunction.
For UCP-1, exercise-induced upregulation is thought to be mediated through multiple mechanisms, including irisin release and MAPK/p38 signaling, PGC-1α-dependent mitochondrial biogenesis, sympathetic activation via β3-adrenergic receptors, and thyroid hormone–dependent deiodinase activity. UCP-1 facilitates proton leakage across the inner mitochondrial membrane, thereby uncoupling oxidative phosphorylation from ATP synthesis and dissipating energy as heat. The discrepancies observed among previous studies regarding UCP-1 responsiveness may be attributable to differences in training duration, dietary conditions, and the anatomical site of adipose tissue sampling.
Compliance with Ethical Guidelines: All experimental procedures were conducted in accordance with ethical guidelines for animal research and were approved by the Ethics Committee of Bojnourd Azad University (Approval Code: IR.IAU.BOJNOURD.REC.1402.017). All procedures were performed minimizing pain and distress to the animals.
Funding: This research is based on a doctoral dissertation from a student at the Islamic Azad University, Bojnourd Branch, and was conducted without any financial support.
Conflicts of interest: There are no conflicts of interest regarding this article.

کلیدواژه‌ها English

Continuous endurance training
Resistance training
High intensity interval training
Slit guidance ligand 2
Uncoupling protein 1
Obesity
1. Loos RJ, Yeo GS. The genetics of obesity: from discovery to biology. Nature Reviews Genetics. 2022;23(2):120-33. https://doi.org/10.1038/s41576-021-00414-z
2. Li VL, He Y, Contrepois K, Liu H, Kim JT, Wiggenhorn AL, et al. An exercise-inducible metabolite that suppresses feeding and obesity. Nature. 2022;606(7915):785-90. https://doi.org/10.1038/s41586-022-04828-5
3. Herz CT, Kulterer OC, Prager M, Schmöltzer C, Langer FB, Prager G, et al. Active brown adipose tissue is associated with a healthier metabolic phenotype in obesity. Diabetes. 2022;71(1):93-103. https://doi.org/10.2337/db21-0475
4. Liao W-x, Wing DA, Geng J-G, Chen D-b. Perspectives of SLIT/ROBO signaling in placental angiogenesis. Histology and histopathology. 2010;25(9):1181. https://doi.org/10.14670/HH-25.1181
5. Chen H, Zhang M, Tang S, London NR, Li DY, Zhang K. Slit-Robo signaling in ocular angiogenesis.  Retinal Degenerative Diseases: Laboratory and Therapeutic Investigations: Springer; 2009. p. 457-63. https://doi.org/10.1007/978-1-4419-1399-9_52
6. Svensson KJ, Long JZ, Jedrychowski MP, Cohen P, Lo JC, Serag S, et al. A secreted Slit2 fragment regulates adipose tissue thermogenesis and metabolic function. Cell metabolism. 2016;23(3):454-66. https://doi.org/10.1016/j.cmet.2016.01.008
7. Hirschenson J, Melgar-Bermudez E, Mailloux RJ. The uncoupling proteins: a systematic review on the mechanism used in the prevention of oxidative stress. Antioxidants. 2022;11(2):322. https://doi.org/10.3390/antiox11020322
8. Chaudhary R, Gupta S, Chauhan S. Protein Uncoupling as an Innovative Practice in Diabetes Mellitus Treatment: A Metabolic Disorder. Endocrine, Metabolic & Immune Disorders Drug Targets. 2022. https://doi.org/10.2174/1871530322666220902143401
9. Kim YJ, Kim HJ, Lee SG, Jang SI, Go HS, Lee WJ, et al. Aerobic exercise for eight weeks provides protective effects towards liver and cardiometabolic health and adipose tissue remodeling under metabolic stress for one week: A study in mice. Metabolism. 2022;130:155178. https://doi.org/10.1016/j.metabol.2022.155178
10. Liu Y, Guo C, Liu S, Zhang S, Mao Y, Fang L. Eight weeks of high-intensity interval static strength training improves skeletal muscle atrophy and motor function in aged rats via the PGC-1α/FNDC5/UCP1 pathway. Clinical Interventions in Aging. 2021;16:811. https://doi.org/10.2147/CIA.S308893
11. Daneshyar S, OmidAli F, Feizipour SA. 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. [In Persian]. https://www.magiran.com/p2305491
12. Shaker M, Khamisipour G, Sadeghipour H, Zar A, Naeimi B, Akbarzadeh S. Effect of resistance training and garlic extract on insulin sensitivity/resistance and biochemical parameters in diabetic rats. Comparative Exercise Physiology. 2022;18(2):163-70. https://doi.org/10.3920/CEP210031
13. Bonfante ILP, Monfort-Pires M, Duft RG, da Silva Mateus KC, de Lima Júnior JC, dos Santos Trombeta JC, et al. Combined training increases thermogenic fat activity in patients with overweight and type 2 diabetes. International Journal of Obesity. 2022;46(6):1145-54. https://doi.org/10.1038/s41366-022-01086-3
14. Afshari S, Kordi MR, Mohammad-Amoli M, Daneshyar S. The Effect of High Intensity Interval Training (HIIT) on Gene Expression of Uncoupling Protein 1 (UCP-1) in Subcutaneous White Adipose Tissue of Wistar Rats. Sport Physiology. 2018;10(39):17-32. [In Persian]. https://doi.org/10.22089/spj.2018.1101
15. Nakhuda A, Josse AR, Gburcik V, Crossland H, Raymond F, Metairon S, et al. Biomarkers of browning of white adipose tissue and their regulation during exercise-and diet-induced weight loss. The American journal of clinical nutrition. 2016;104(3):557-65. https://doi.org/10.3945/ajcn.116.132563
16. Leandro CG, Levada AC, Hirabara SM, MANHAS-DE-CASTRO R, De-Castro CB, Curi R, et al. Aprogram of moderate physical training for wistar rats based on maximal oxygen consumption. The Journal of Strength & Conditioning Research. 2007;21(3):751-6. https://doi.org/10.1519/R-20155.1
17. Steki A, Valipour V, Ghahramanlo E, Kargarfard M. The effect of endurance training in air pollution on the expression of brain cortex PGC-1α and Atf2 genes in Wistar male rats. KAUMS Journal (FEYZ). 2019;23(6):615-26. [In Persian]. https://www.magiran.com/p2091481
18. Lee S, Farrar RP. Resistance training induces muscle-specific changes in muscle mass and function in rat. Journal of Exercise Physiology Online. 2003;6(2).
19. Karbasi S, Zaeemi M, Mohri M, Rashidlamir A, Moosavi Z. Effects of testosterone enanthate and resistance training on myocardium in Wistar rats; clinical and anatomical pathology. Andrologia. 2018;50(3):e12908. https://doi.org/10.1111/and.12908
20. Norozi M, Sadeghi A, Faal Pakdehi M, Torabi G. The effect of eight-week high intensity interval training (HIIT) and caffeine consumption on glycogen synthase expression and hepatic glycogen levels in diabetic rats. Daneshvar Medicine. 2021;29(5):41-55. [In Persian]. https://doi.org/10.22070/daneshmed.2021.14819.1101
21. Wang Y, Zhao S, Peng W, Chen Y, Chi J, Che K, et al. The Role of Slit-2 in Gestational Diabetes Mellitus and Its Effect on Pregnancy Outcome. Frontiers in Endocrinology. 2022;13. https://doi.org/10.3389/fendo.2022.889505
22. Kaisanlahti A, Glumoff T. Browning of white fat: agents and implications for beige adipose tissue to type 2 diabetes. Journal of Physiology and Biochemistry. 2019;75(1):1-10. https://doi.org/10.1007/s13105-018-0658-5
23. Yazdi AB, Homaee HM, Peeri M. The Effect of Endurance Exercise and Adenosine Consumption on UCP-1 Gene Expression in the Visceral Adipose Tissue of Obese Male Rats. Iranian Journal of Diabetes and Obesity. 2018;10(2):80-7. [In Persian]. https://www.magiran.com/p1882802
24. Hejazi K, Attarzadeh Hosseini SR, Fathi M, Mosaferi Ziaaldini M, Zaeemi M. Comparison the effect of eight weeks aerobic training with moderate and high intensities on serum levels of Irisin and Uncoupling Protein 1 (UCP-1) in white adipose tissue in obese male rats. Journal of Gorgan University of Medical Sciences. 2018;20(3):31-9. [In Persian]. http://goums.ac.ir/journal/article-1-3453-en.html
25. Ringholm S, Grunnet Knudsen J, Leick L, Lundgaard A, Munk Nielsen M, Pilegaard H. PGC-1α is required for exercise-and exercise training-induced UCP1 up-regulation in mouse white adipose tissue. PloS One. 2013;8(5):e64123. https://doi.org/10.1371/journal.pone.0064123
26. Chouchani ET, Kazak L, Spiegelman BM. New advances in adaptive thermogenesis: UCP1 and beyond. Cell Metabolism. 2019;29(1):27-37. https://doi.org/10.1016/j.cmet.2018.11.002
27. Ikeda K, Yamada T. UCP1 dependent and independent thermogenesis in brown and beige adipocytes. Frontiers in Endocrinology. 2020;11:498. https://doi.org/10.3389/fendo.2020.00498
28. Nourshahi M, Mir Khalafzadeh F, Khodagholi F, Abuzari N. Effect of eight weeks of continuous and high intensity interval training on UCP1 in visceral and subcutaneous white adipose tissue of obese rats. Sport Biosciences. 2021;13(4):427-38. [In Persian]. https://doi.org/10.22059/jsb.2020.301401.1394
29. Reisi J, Ghaedi K, Rajabi H, Marandi SM. Can resistance exercise alter irisin levels and expression profiles of FNDC5 and UCP1 in rats? Asian Journal of Sports Medicine. 2016;7(4). https://doi.org/10.5812/asjsm.35205
30. Kraemer WJ, Rogol AD. The endocrine system in sports and exercise: John Wiley & Sons; 2008.
31. Dieckmann S, Strohmeyer A, Willershäuser M, Maurer SF, Wurst W, Marschall S, et al. Susceptibility to diet-induced obesity at thermoneutral conditions is independent of UCP1. American Journal of Physiology-Endocrinology and Metabolism. 2022;322(2):E85-E100. https://doi.org/10.1152/ajpendo.00278.2021
32. Martinez-deMena R, Anedda A, Cadenas S, Obregon M-J. TSH effects on thermogenesis in rat brown adipocytes. Molecular and Cellular Endocrinology. 2015;404:151-8. https://doi.org/10.1016/j.mce.2015.01.028