The effect of exercise type and herbal supplement on the expression of mitophagic genes in obese female rats' pancreas
الموضوعات : Exercise Physiology and Performance
Faranak Amini
1
,
Mohammad Ali Azarbayjani
2
,
Shahin Riyahi Malayeri
3
,
Lida Moradi
4
1 - Department of Physical Education and Sport Sciences, NT.C., Islamic Azad University, Tehran, Iran.
2 - Department of Physical Education and Sport Sciences, CT.C., Islamic Azad University, Tehran, Iran.
3 - Department of Physical Education and Sport Sciences, ET.C., Islamic Azad University, Tehran, Iran.
4 - Department of Physical Education and Sport Sciences, NT.C., Islamic Azad University, Tehran, Iran.
الکلمات المفتاحية: Aerobic exercise, resistance exercise, herbal supplement, PINK1, Parkin,
ملخص المقالة :
Background and purpose: Physical activity and medicinal herbs can each reduce obesity's harmful effects through different mechanisms, including the effect on mitochondrial mitophagy. Since the simultaneous effect of regular physical activity and medicinal herbs on the expression of genes responsible for mitophagy is not well known, the aim of the present study was to investigate and compare the effects of aerobic and resistance training and herbal supplement consumption on the expression of genes of the mitophagy pathway in the pancreatic tissue of obese female rats. Methods: In an experimental study, 42 young female Wistar rats (12 weeks old and weighing 180-200 g) were obtained from the Pasteur Institute of Karaj, Iran and selected as subjects. One week after familiarization and adaptation to the adapted environment, the animals were randomly divided into 7 groups (6 rats per group) including: 1. Aerobic exercise-herbal supplement (AT-S), 2. Resistance exercise-herbal supplement (RT-S), 3. Aerobic exercise (AT), 4. Resistance exercise (RT), 5. Herbal supplements (S), 6. Controlled fed with a high-fat diet and 7. Control- fed with a normal diet. Forty-eight hours after the last training session, after ensuring complete anesthesia, pancreatic tissue was removed to measure the expression of PINK1 and Parkin genes and stored at -85°C until measurement.
Results: PINK1 gene expression in pancreatic tissue was significantly higher in aerobic exercise-herbal extract-high-fat diet groups (P=0.001), resistance exercise-herbal extract-high-fat diet groups (P=0.021), aerobic exercise-HFD diet groups (P=0.038), resistance exercise-HFD groups (P=0.001), and herbal supplement-HFD groups (P=0.001) than in the control group (P=0.001). PARKIN gene expression was significantly higher in aerobic exercise-herbal extract-high-fat diet groups (P=0.001), resistance exercise-herbal extract-HFD groups (P=0.035), aerobic exercise-HFD (P=0.026), and herbal supplement groups (P=0.006) than in the control-HFD group. Conclusion: The present study shows that high-fat diets can cause impaired pancreatic function by reducing the expression of mitophagy genes. Since regular physical activity, especially aerobic exercise, and herbal supplementation prevented the reduction in the expression of PINK1 and PARKIN genes, it is concluded that these two interventions have a protective effect on pancreatic tissue under conditions of a high-fat diet. Therefore, it is recommended that aerobic exercise and the herbal supplements used in the present study can be considered as a beneficial strategy to reduce the complications caused by a high-fat diet for pancreatic tissue.
1. Riyahi Malayeri S, Azadniya A, Rasaee M J. Effect of eight-week high intensity interval training and resveratrol intake on serum adiponectin and resistin in type 2 diabetic rats ijdld 2019; 18 (1) :8-1
URL: http://ijdld.tums.ac.ir/article-1-5708-en.html.
2. Heo JW, No MH, Cho J, Choi Y, Cho EJ, Park DH, et al. Moderate aerobic exercise training ameliorates impairment of mitochondrial function and dynamics in skeletal muscle of high‐fat diet‐induced obese mice. The FASEB Journal. 2021;35(2):e21340.
3. Rosa-Caldwell ME, Poole KE, Seija A, Harris MP, Greene NP, Wooten JS. Exercise during weight loss improves hepatic mitophagy. Sports medicine and health science. 2022;4(3):183-9.
4. Wang X-L, Feng S-T, Wang Y-T, Yuan Y-H, Li Z-P, Chen N-H, et al. Mitophagy, a form of selective autophagy, plays an essential role in mitochondrial dynamics of parkinson’s disease. Cellular and Molecular Neurobiology. 2021:1-19.
5. Chen W, Xu Z, You W, Zhou Y, Wang L, Huang Y, et al. Cold exposure alters lipid metabolism of skeletal muscle through HIF-1α-induced mitophagy. BMC biology. 2023;21(1):27.
6. Wang C-H, Wei Y-H. Roles of mitochondrial sirtuins in mitochondrial function, redox homeostasis, insulin resistance and type 2 diabetes. International journal of molecular sciences. 2020;21(15):5266.
7. Slavin MB, Memme JM, Oliveira AN, Moradi N, Hood DA. Regulatory networks coordinating mitochondrial quality control in skeletal muscle. American Journal of Physiology-Cell Physiology. 2022;322(5):C913-C26.
8. Takhti M, Riyahi Malayeri S, Behdari R. Comparison of two methods of concurrent training and ginger intake on visfatin and metabolic syndrome in overweight women. RJMS 2020; 27 (9) :98-111.
9. Riyahi Malayeri S, Hoseini M. The effect of acute exercise on vaspin and chemerin levels in obese men. jbrms 2021; 8 (1) :58-66.URL: http://jbrms.medilam.ac.ir/article-1-528-en.html.
10. Bouviere J, Fortunato RS, Dupuy C, Werneck-de-Castro JP, Carvalho DP, Louzada RA. Exercise-stimulated ROS sensitive signaling pathways in skeletal muscle. Antioxidants. 2021;10(4):537.
11. Kavazis AN, Smuder AJ, Powers SK. Effects of short-term endurance exercise training on acute doxorubicin-induced FoxO transcription in cardiac and skeletal muscle. Journal of applied physiology. 2014;117(3):223-30.
12. Porter C, Reidy PT, Bhattarai N, Sidossis LS, Rasmussen BB. Resistance exercise training alters mitochondrial function in human skeletal muscle. Medicine and science in sports and exercise. 2015;47(9):1922.
13. Jee S-C, Cheong H. Autophagy/Mitophagy Regulated by Ubiquitination: A Promising Pathway in Cancer Therapeutics. Cancers. 2023;15(4):1112.
14. Mosaddeghi P, Eslami M, Farahmandnejad M, Akhavein M, Ranjbarfarrokhi R, Khorraminejad-Shirazi M, et al. A systems pharmacology approach to identify the autophagy-inducing effects of Traditional Persian medicinal plants. Scientific reports. 2021;11(1):336.
15. Vermaak I, Viljoen AM, Hamman JH. Natural products in anti-obesity therapy. Natural product reports. 2011;28(9):1493-533.
16. Sarkar A, Alam M, Roy P, Biswas R, Haque MI. Physicochemical, antioxidant and antimicrobial activities of green teas manufactured from common tea clones of different gardens in Bangladesh. Journal of Agriculture and Food Research. 2022;10:100407.
17. Ghorbanpour A, Salari S, Baluchnejadmojarad T, Roghani M. Capsaicin protects against septic acute liver injury by attenuation of apoptosis and mitochondrial dysfunction. Heliyon. 2023;9(3).
18. Picos-Salas MA, Cabanillas-Bojórquez LÁ, Elizalde-Romero CA, Leyva-López N, Montoya-Inzunza LA, Heredia JB, et al. Naringenin as a Natural Agent Against Oxidative Stress and Inflammation, and Its Bioavailability. Food Reviews International. 2022:1-39.
19. Tong M, Saito T, Zhai P, Oka S-i, Mizushima W, Nakamura M, et al. Mitophagy Is Essential for Maintaining Cardiac Function During High Fat Diet-Induced Diabetic Cardiomyopathy. Circulation Research. 2019;124(9):1360-71.
20. Shao D, Kolwicz SC, Wang P, Roe ND, Villet O, Nishi K, et al. Increasing Fatty Acid Oxidation Prevents High-Fat Diet–Induced Cardiomyopathy Through Regulating Parkin-Mediated Mitophagy. Circulation. 2020;142(10):983-97.
21. Rabinovich-Nikitin I, Dhingra R, Kirshenbaum LA. Activation of Mitophagy in High-Fat Diet–Induced Diabetic Cardiomyopathy. Circulation Research. 2019;124(9):1288-90.
22. Seabright AP, Fine NH, Barlow JP, Lord SO, Musa I, Gray A, et al. AMPK activation induces mitophagy and promotes mitochondrial fission while activating TBK1 in a PINK11‐Parkin independent manner. The FASEB Journal. 2020;34(5):6284.
23. McWilliams TG, Prescott AR, Montava-Garriga L, Ball G, Singh F, Barini E, et al. Basal mitophagy occurs independently of PINK11 in mouse tissues of high metabolic demand. Cell metabolism. 2018;27(2):439-49. e5.
24. Roberts FL, Markby GR. New Insights into Molecular Mechanisms Mediating Adaptation to Exercise; A Review Focusing on Mitochondrial Biogenesis, Mitochondrial Function, Mitophagy and Autophagy. Cells [Internet]. 2021; 10(10).
25. Chen CCW, Erlich AT, Hood DA. Role of Parkin and endurance training on mitochondrial turnover in skeletal muscle. Skeletal muscle. 2018;8:1-14.
26. Saleem A, Carter HN, Hood DA. p53 is necessary for the adaptive changes in cellular milieu subsequent to an acute bout of endurance exercise. American Journal of Physiology-Cell Physiology. 2014;306(3):C241-C9.
27. James DI, Parone PA, Mattenberger Y, Martinou J-C. hFis1, a novel component of the mammalian mitochondrial fission machinery. Journal of Biological Chemistry. 2003;278(38):36373-9.
28. Sanchez AM, Csibi A, Raibon A, Cornille K, Gay S, Bernardi H, et al. AMPK promotes skeletal muscle autophagy through activation of forkhead FoxO3a and interaction with Ulk1. Journal of cellular biochemistry. 2012;113(2):695-710.
29. Laker RC, Drake JC, Wilson RJ, Lira VA, Lewellen BM, Ryall KA, et al. Ampk phosphorylation of Ulk1 is required for targeting of mitochondria to lysosomes in exercise-induced mitophagy. Nature communications. 2017;8(1):548.
30. Corsa CA, Pearson GL, Renberg A, Askar MM, Vozheiko T, MacDougald OA, et al. The E3 ubiquitin ligase parkin is dispensable for metabolic homeostasis in murine pancreatic β cells and adipocytes. Journal of Biological Chemistry. 2019;294(18):7296-307.
31. Deas E, Piipari K, Machhada A, Li A, Gutierrez-del-Arroyo A, Withers DJ, et al. PINK11 deficiency in β-cells increases basal insulin secretion and improves glucose tolerance in mice. Open biology. 2014;4(5):140051.
32. Park K, Lim H, Kim J, Hwang Y, Lee YS, Bae SH, et al. Lysosomal Ca2+-mediated TFEB activation modulates mitophagy and functional adaptation of pancreatic β-cells to metabolic stress. Nature Communications. 2022;13(1):1300.
33. Jin H-S, Kim J, Lee S-J, Kim K, Go MJ, Lee J-Y, et al. The PARK2 gene is involved in the maintenance of pancreatic β-cell functions related to insulin production and secretion. Molecular and cellular endocrinology. 2014;382(1):178-89.
34. Park GH, Park JH, Chung KC. Precise control of mitophagy through ubiquitin proteasome system and deubiquitin proteases and their dysfunction in Parkinson’s disease. BMB reports. 2021;54(12):592.
35. Gan Z, Fu T, Kelly DP, Vega RB. Skeletal muscle mitochondrial remodeling in exercise and diseases. Cell Research. 2018;28(10):969-80.
36. Zhang T, Liu Q, Gao W, Sehgal SA, Wu H. The multifaceted regulation of mitophagy by endogenous metabolites. Autophagy. 2022;18(6):1216-39.
