Comparison of eight weeks of resistance training and high-intensity intermittent aerobic training on the expression of microRNAs associated with adipose tissue angiogenesis and antiangiogenesis in rats fed a high-fat diet

Document Type : original article

Authors

1 Department of Sports Science, Faculty of Education and Psychology, University of Mohaghegh Ardabili, Ardabil, Iran

2 Department of Sports Science, Faculty of Literature and Humanities, University of Qom, Qom, Iran

Abstract

Background and Purpose: Exercise and obesity alter angiogenesis in adipose tissue, resulting in large changes in metabolic processes. The aim of this study was to compare the effect of eight weeks of resistance training and high-intensity intermittent aerobic training (HIIAT) on the expression of microRNAs associated with adipose tissue angiogenesis and antiangiogenesis in rats fed a high-fat diet.
Materials and Methods: In the experimental study, 60 six-week-old male wistar rats (mean body weight = 192.40 ± 11.35) were obtained from Pasteur Institute of Iran. The animals were randomly divided into six equal groups after transfer to the laboratory environment and one week of exposure to the new environment: 1. Normal diet (CO), 2. Normal diet + Resistance training (NRT), 3. Normal diet + HIIAT (NHT), 4. High-fat diet (HF), 5. High-fat diet + Resistance training (HFRT), 6. High-fat diet + HIIAT (HFHT) (n = 10 per group). The training groups performed their training protocol for eight weeks and five sessions per week. Resistance training included climbing a 1-meter ladder with a 90-degree slope and 46 steps. Initially, the weight attached to the rats' tails was 30% of their body weight and gradually reached about 180% of their body weight in the final week. The exercises were performed in five sets of four repetitions. High-intensity intermittent aerobic training was started on the treadmill at an initial speed of 15 meters per minute, and in each session, one to two meters per minute was added to the treadmill speed, depending on the ability of the rats. During the Pabani week, the exercise reached six stages of three minutes of running at a speed of 40 meters per minute with a slope of 15 degrees. To evaluate the effect of resistance training and high-intensity intermittent aerobic training and high-fat diet (58% of calories in the form of fat) on miR-221, miR-222, miR-329 and VEGF variables, subjects in each group were killed 48 hours after the last training session. Sampling of mesenteric adipose tissue was performed immediately after killing the animals. Data analysis was performed using independent t-test, one-way and two-way ANOVA at the significant level (P ≥ 0.05). Scheffe post hoc test was used to compare the pairwise .
Results: The miR-221, miR-222 and VEGF in the Normal diet + Resistance training, Normal diet + HIIT and High-fat diet + Resistance training groups a significant increase was observed compared to the control group (P ≥ 0.01). However, miR-329 was significantly higher only in the high-fat diet group than in the normal diet + HIIAT group (P = 0.022).
Conclusion: The results showed that resistance training and HIIAT by increasing miR-221, miR-222, and decreasing miR329 led to the activation of pathways that increased VEGF protein and ultimately increased angiogenesis in rats with a high-fat and normal diets. Therefore, these exercises are an important factor in angiogenesis and mechanism in adipose tissue, which may be able to cause significant changes in adipose tissue during this process. However, in order to confirm this point and generalize it to humans, more research is needed, especially on human specimens. Also, since the effect of resistance training on miRNAs was greater than HIIAT, these exercises can be a good alternative to HIIAT.

Keywords


  1. Thamotharan S, Chu A, Kempf K, Janzen C, Grogan T, Elashoff DA, et al. Differential microRNA expression in human placentas of term intra-uterine growth restriction that regulates target genes mediating angiogenesis and amino acid transport. Plos one. 2017;12(5):e0176493.
  2. Witwer KW. Circulating microRNA biomarker studies: pitfalls and potential solutions. Clinical chemistry. 2015;61(1):56-63.
  3. Lowy D, Wolff L. Articles and brief reports. Haematologica. 2012;97(6):818-26.
  4. Celic T, Metzinger-Le Meuth V, Six I, A Massy Z, Metzinger L. The mir-221/222 cluster is a key player in vascular biology via the fine-tuning of endothelial cell physiology. Current vascular pharmacology. 2017;15(1):40-6.
  5. Dentelli P, Rosso A, Orso F, Olgasi C, Taverna D, Brizzi MF. microRNA-222 controls neovascularization by regulating signal transducer and activator of transcription 5A expression. Arteriosclerosis, thrombosis, and vascular biology. 2010;30(8):1562-8.
  6. Wang P, Luo Y, Duan H, Xing S, Zhang J, Lu D, et al. MicroRNA 329 suppresses angiogenesis by targeting CD146. Molecular and cellular biology. 2013;33(18):3689-99.
  7. Monzemi AH, Etemad Z, Nazari A, Mohammadi M. The effect of eight weeks of endurance training along with cinnamon extract consumption on expression of angiogenic markers in endothelial dysfunction of the coronary arteries in streptozotocin-diabetic male rats. Journal of Sport and Exercise Physiology. 2022:11-20. (In Persian).
  8. Faber D, De Groot PG, Visseren F. Role of adipose tissue in haemostasis, coagulation and fibrinolysis. Obesity reviews. 2009;10(5):554-63.
  9. Sadegh Ghomi M, Kashef M, Salehpour M. The effect of eight weeks resistance and endurance training on some angiogenesis factors of hippocampus tissue in male wistar rats. Journal of Sport and Exercise Physiology. 2021;14(2):45-54. (In Persian).
  10. Sun K, Asterholm IW, Kusminski CM, Bueno AC, Wang ZV, Pollard JW, et al. Dichotomous effects of VEGF-A on adipose tissue dysfunction. Proceedings of the national academy of sciences. 2012;109(15):5874-9.
  11. Fu P, Zhu R, Jia J, Hu Y, Wu C, Cieszczyk P, et al. Aerobic exercise promotes the functions of brown adipose tissue in obese mice via a mechanism involving COX2 in the VEGF signaling pathway. Nutrition & Metabolism. 2021;18(1):1-14.
  12. Yeo H-S, Lim J-Y. Effects of different types of exercise training on angiogenic responses in the left ventricular muscle of aged rats. Experimental gerontology. 2022;158:111650.
  13. Van Pelt DW, Guth LM, Horowitz JF. Aerobic exercise elevates markers of angiogenesis and macrophage IL-6 gene expression in the subcutaneous adipose tissue of overweight-to-obese adults. Journal of applied physiology. 2017;123(5):1150-9.
  14. Sun LL, Li WD, Lei FR, Li XQ. The regulatory role of micro RNA s in angiogenesis‐related diseases. Journal Of Cellular And Molecular Medicine. 2018;22(10):4568-87.
  15. Fathi R, Ebrahimi M, Khenar Sanami S. Effects of High Fat Diet and High Intensity Aerobic Training on Interleukin 6 Plasma Levels in Rats. Pathobiology research. 2015;18(3):109-16. (In Persian).
  16. Council NR. Guide for the care and use of laboratory animals2010.
  17. Kolahdouzi S, Talebi Garakani E, Hamidian G, Safarzade A. The Effects of High-Intensity Intermittent Aerobic Training on Adipose Tissue Angiogenesis in Rats Fed a High Fat Diet. Sport physiology. 2018;10(38):143-62. (In Persian).
  18. Moreira JB, Bechara LR, Bozi LH, Jannig PR, Monteiro AW, Dourado PM, et al. High-versus moderate-intensity aerobic exercise training effects on skeletal muscle of infarcted rats. Journal of applied physiology. 2013;114(8):1029-41.
  19. Linden MA, Fletcher JA, Morris EM, Meers GM, Laughlin MH, Booth FW, et al. Treating NAFLD in OLETF rats with vigorous-intensity interval exercise training. Medicine and science in sports and exercise. 2015;47(3):556.
  20. Borujeny AK, Marandi M, Javanmard SH, Rajabi H, Burojeny ZK, Behzadi MK. Effect of Eight Weeks of Resistance Training on Some Signaling Factors Affecting on the Satellite Cells in Wistar Rats. Journal of isfahan medical school. 2012;30(207).
  21. Banitalebi E, Gharakhanlou R, Ghatreh Samani K, Amoli M, Teimori H. The effect of resistance training on plasma and skeletal muscles sphingosine-1-phosphate levels of male Wistar rat. Journal of shahrekord uuniversity of medical sciences. 2012;14. (In Persian).
  22. Bao F, Slusher AL, Whitehurst M, Huang C-J. Circulating microRNAs are upregulated following acute aerobic exercise in obese individuals. Physiology & behavior. 2018;197:15-21.
  23. Schmitz B, Rolfes F, Schelleckes K, Mewes M, Thorwesten L, Krüger M, et al. Longer work/rest intervals during high-intensity interval training (HIIT) lead to elevated levels of miR-222 and miR-29c. Frontiers in physiology. 2018;9:395.
  24. Liu X, Xiao J, Zhu H, Wei X, Platt C, Damilano F, et al. miR-222 is necessary for exercise-induced cardiac growth and protects against pathological cardiac remodeling. Cell metabolism. 2015;21(4):584-95.
  25. Lijnen HR. Angiogenesis and obesity. Cardiovascular research. 2008;78(2):286-93.
  26. Nourshahi M, Babaei A, Bigdeli MR, Ghasemi Beyrami M. The effect of six weeks of resistance training on tumor tissue VEGF and endostatin in mice with breast cancer. Journal of Sport Biosciences. 2013;5(2):27-46. (In Persian).
  27. Logsdon EA, Finley SD, Popel AS, Gabhann FM. A systems biology view of blood vessel growth and remodelling. Journal of cellular and molecular medicine. 2014;18(8):1491-508.
  28. Li Y, Yao M, Zhou Q, Cheng Y, Che L, Xu J. Dynamic Regulation of Circulating microRNAs During Acute Exercise and Long-Term Exercise Training in Basketball Athletes. Front Physiol. 2018; 9: 282. doi: 10.3389/fphys. 2018.00282.». 2018.
  29. Akbarpour M, Fathollahi SF, Moradpoorian M, Hamidi M. Investigation of Some MicroRNAs Related to Cell Death to Eight-Week Resistance Training in Women with Breast Cancer. Journal of fasa university of medical sciences, . 2020(10(1)):2043-52. (In Persian).
  30. Zaccagnini G, Maimone B, Di Stefano V, Fasanaro P, Greco S, Perfetti A, et al. Hypoxia-induced miR-210 modulates tissue response to acute peripheral ischemia. Antioxidants & redox signaling. 2014;21(8):1177-88.
  31. Alaiti MA, Ishikawa M, Masuda H, Simon DI, Jain MK, Asahara T, et al. Up‐regulation of miR‐210 by vascular endothelial growth factor in ex vivo expanded CD 34+ cells enhances cell‐mediated angiogenesis. Journal of cellular and molecular medicine. 2012;16(10):2413-21.                                                                                                                            
Volume 15, Issue 4 - Serial Number 31
September 2022
Pages 42-53
  • Receive Date: 14 April 2022
  • Revise Date: 26 May 2022
  • Accept Date: 09 July 2022
  • First Publish Date: 10 August 2022
  • Publish Date: 23 August 2022