The Effect of Swimming Training on the Insulin Resistance and Expression of Adiponectin and APPL-1 Liver Genes Following Induced Polycystic Ovary Syndrome in Rats

Document Type : Original Article

Authors

1 PhD Student of Physical Education and Sports Sciences, Faculty of Literature, Humanities and Social Sciences, Science and Research Branch, Islamic Azad University, Tehran, Iran.

2 Associate Professor, Department of Physical Education and Sports Sciences, Faculty of Literature, Humanities and Social Sciences, Science and Research Branch, Islamic Azad University, Tehran, Iran.

3 Assistant Professor, Department of Obstetrics and Gynecology, Faculty of Medicine, Islamic Azad University of Medical Sciences, Tehran, Iran.

Abstract

Introduction: Polycystic ovary syndrome (PCOS) is a common endocrine disorder in women which is associated with insulin resistance (IR). Some Factors such as adiponectin and APPL-1 play a role in IR signaling that is affected by exercise. Therefore, the present study was conducted with aim to evaluate the effect of swimming training on the IR and the expression of adiponectin and APPL1 genes following induced PCOS in rats.
Methods: This experimental research was conducted in 2021 on 36 female wistar rats. The rats were divided in six groups. Swimming training was done (six and eight weeks/five days a week, 60 min each session/ flow of the water speed was increased from seven to 15 L/M). After 24hr of sacrifices the mice, the level of IR, expression of adiponectin and APPL1 genes were measured in the liver tissue. Data were analyzed using SPSS software (version 22) and two-way ANOVA. P< .05 was considered statistically significant.
Results: Six weeks of training had a significant effect on IR serum levels (P=0.001) and adiponectin gene expression (P=0.004), while it had no significant effect on APPL-1 gene expression (P=0.433). Also, eight weeks of exercises had a significant effect on the IR (P=0.001) and the expression of APPL-1 and adiponectin genes (P=0.001).
Conclusion: Swimming training can lead to significant changes in IR serum levels, expression of adiponectin and APPL-1 genes. It seems that 8 weeks if swimming training have positive effects in PCOS patients by improving the metabolic pathway.

Keywords

References

  1. Woodward A, Broom D, Dalton C, Metwally M, Klonizakis M. Supervised exercise training and increased physical activity to reduce cardiovascular disease risk in women with polycystic ovary syndrome: study protocol for a randomized controlled feasibility trial. Trials 2020; 21:1-8.
  2. Aye MM, Butler AE, Kilpatrick ES, Kirk R, Vince R, Rigby AS, et al. Dynamic change in insulin resistance induced by free fatty acids is unchanged though insulin sensitivity improves following endurance exercise in PCOS. Frontiers in Endocrinology 2018; 9:592.
  3. Hansen SL, Svendsen PF, Jeppesen JF, Hoeg LD, Andersen NR, Kristensen JM, et al. Molecular mechanisms in skeletal muscle underlying insulin resistance in women who are lean with polycystic ovary syndrome. The Journal of Clinical Endocrinology & Metabolism 2019; 104(5):1841-54.
  4. Freeman AM, Pennings N. Insulin Resistance. [Updated 2022 Jul 4]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2022. Available from: https://www.ncbi.nlm.nih.gov/books/NBK507839/
  5. Anwar AA, Abdullah N, Padjalangi AN, Hamid F, Mappeware NA, Lukas E. Serum leptin concentration is correlated to insulin resistance in polycystic ovary syndrome (PCOS) patients. Molecular and Cellular Biomedical Sciences 2021; 5(2):93-7.
  6. da Silva Rosa SC, Nayak N, Caymo AM, Gordon JW. Mechanisms of muscle insulin resistance and the cross‐talk with liver and adipose tissue. Physiological Reports 2020; 8(19):e14607.
  7. Artimani T, Najafi R. APPL1 as an important regulator of insulin and adiponectin‐signaling pathways in the PCOS: A narrative review. Cell Biology International 2020; 44(8):1577-87.
  8. Dobrzyn K, Smolinska N, Kiezun M, Szeszko K, Rytelewska E, Kisielewska K, et al. Adiponectin: a new regulator of female reproductive system. International journal of endocrinology 2018; 2018.
  9. Pahlavan F, Tork Tatari F, Fazeli S, Razavinia F, Tehranian N. Role of Adiponectin Hormone in Fertility and Sterility: A Systematic Review. Iran J Obstet Gynecol Infertil 2018; 21(5):97-107.
  10. Salva-Pastor N, Chavez-Tapia NC, Uribe M, Nuno-Lambarri N. Understanding the association of polycystic ovary syndrome and non-alcoholic fatty liver disease. The Journal of Steroid Biochemistry and Molecular Biology 2019; 194:105445.
  11. Combs TP, Marliss EB. Adiponectin signaling in the liver. Reviews in Endocrine and Metabolic Disorders 2014; 15:137-47.
  12. Iwabu M, Okada-Iwabu M, Yamauchi T, Kadowaki T. Adiponectin/AdipoR research and its implications for lifestyle-related diseases. Frontiers in Cardiovascular Medicine 2019; 6:116.
  13. Gamberi T, Magherini F, Modesti A, Fiaschi T. Adiponectin signaling pathways in liver diseases. Biomedicines 2018; 6(2):52.
  14. Minuzzi LG, Kuga GK, Breda L, Gaspar RC, Muñoz VR, Pereira RM, et al. Short-term Resistance Training Increases APPL1 Content in the Liver and the Insulin Sensitivity of Mice Fed a Long-term High-fat Diet. Exp Clin Endocrinol Diabetes 2020; 128(1):30-37.
  15. Wright PJ, Corbett CF, Pinto BM, Dawson RM, Wirth M. Resistance Training as Therapeutic Management in Women with PCOS: What is the Evidence? International Journal of Exercise Science 2021; 14(3):840-54.
  16. Amiri M, Ramezani Tehrani P, Ramezani Tehrani F. Effect of interventions based on lifestyle modification on clinical, hormonal and metabolic findings in the patients with polycystic ovary syndrome: a systematic review. Iranian Journal of Endocrinology and Metabolism 2016; 17(6):489-500.
  17. Bruce CR, Thrush AB, Mertz VA, Bezaire V, Chabowski A, Heigenhauser GJ, et al. Endurance training in obese humans improves glucose tolerance and mitochondrial fatty acid oxidation and alters muscle lipid content. American journal of physiology-endocrinology and metabolism 2006; 291(1):E99-107.
  18. Mirdar S, Arab A, Hedayati M, Hajizade A. The effect of pregnant rat swimming on hypoxia-inducible factor-1α levels of neonatal lung. Tehran University Medical Journal 2012; 69(12).
  19. Bijeh N, Delpasand A, Hejazi K. The effect of different intensities of aerobic exercise on insulin levels and insulin resistance in rats with polycystic ovary syndrome. Journal of Sabzevar University of Medical Sciences 2014; 21(6):1163-72.
  20. Pandit U, Singh M, Ranjan R, Gupta V. The Effect of Exercise Training on Body Composition, Insulin Resistance and High Sensitivity C-reactive Protein (Hs-CRP) in Women With Polycystic Ovary Syndrome: A Pilot Study From North India. Cureus 2022; 14(4).
  21. Stepto NK, Hiam D, Gibson-Helm M, Cassar S, Harrison CL, Hutchison SK, et al. Exercise and insulin resistance in PCOS: muscle insulin signalling and fibrosis. Endocrine connections 2020; 9(4):346-59.
  22. Jafari S, Taghian F. The effect of aerobic exercise training on biochemical and inflammatory markers among young females suffering from polycystic ovary syndrome. Journal of Midwifery and Reproductive Health 2020; 8(2):2194-202.
  23. Lim AJ, Huang Z, Chua SE, Kramer MS, Yong EL. Sleep duration, exercise, shift work and polycystic ovarian syndrome-related outcomes in a healthy population: a cross-sectional study. PloS one 2016; 11(11):e0167048.
  24. Joseph A, Parvathy S, Varma KK, Nandakumar A. Four weeks exercise training enhanced the hepatic insulin sensitivity in high fat-and high carbohydrate-diet fed hyperinsulinemic rats. Journal of Diabetes & Metabolic Disorders 2020; 19:1583-92.
  25. Fakhri F, Fakhri S, Shakeryan S, Alizadeh A. Effect of six weeks of high intensity interval training on under-Carboxylated Osteocalcin serum levels, insulin resistance, and lipid profile in overweight girls: randomized clinical trial. Iran J Obstet Gynecol Infertil 2021; 23(12)57-66.
  26. Khoshkam F, Taghian F, Jalali Dehkordi K. Effect of eight weeks of supplementation of omega-3 supplementation and TRX training on visfatin and insulin resistance in women with polycystic ovary syndrome. Iran J Obstet Gynecol Infertil 2018; 21(9):58-70.
  27. Ramanjaneya M, Abdalhakam I, Bettahi I, Bensila M, Jerobin J, Aye MM, et al. Effect of moderate aerobic exercise on complement activation pathways in polycystic ovary syndrome women. Frontiers in Endocrinology 2022; 12:1933.
  28. Santos IK, Nunes FA, Queiros VS, Cobucci RN, Dantas PB, Soares GM, et al. Effect of high-intensity interval training on metabolic parameters in women with polycystic ovary syndrome: A systematic review and meta-analysis of randomized controlled trials. Plos one 2021; 16(1):e0245023.
  29. Asl Dehghan R. Investigation of APPL adiponectin gene expression and its relationship with insulin and adiponectin receptors in granulosa cells of patients with polycystic ovary syndrome. [Master's degree, medical biotechnology] Iran. University of Medical Sciences of Hamadan Faculty of Medicine, 2015.(Persian)
  30. Sun L, Lv Y, Tian J, Yu T, Niu F, Zhang X, et al. Regular swimming exercise attenuated neuroma pain in rats: involvement of leptin and adiponectin. The Journal of Pain 2019; 20(9):1112-24.
  31. Martinez-Huenchullan SF, Tam CS, Ban LA, Ehrenfeld-Slater P, Mclennan SV, Twigg SM. Skeletal muscle adiponectin induction in obesity and exercise. Metabolism 2020; 102:154008.
  32. Kido K, Ato S, Yokokawa T, Sato K, Fujita S. Resistance training recovers attenuated APPL1 expression and improves insulin-induced Akt signal activation in skeletal muscle of type 2 diabetic rats. American Journal of Physiology-Endocrinology and Metabolism 2018; 314(6):E564-71.
  33. Gaspar RC, Muñoz VR, Kuga GK, Nakandakari SCBR, Crisol BM, Lenhare L, et al. Acute physical exercise increases APPL1/PI3K signaling in the hypothalamus of lean mice. Eur J Neurosci 2019; 50(7):3181-3190.
  34. Farias JM, Maggi RM, Tromm CB, Silva LA, Luciano TF, Marques SO, et al. Exercise training performed simultaneously to a high-fat diet reduces the degree of insulin resistance and improves adipoR1-2/APPL1 protein levels in mice. Lipids in health and disease 2012; 11:1-9.
  35. Zaidi H, Byrkjeland R, Njerve IU, Åkra S, Solheim S, Arnesen H, et al. Adiponectin in relation to exercise and physical performance in patients with type 2 diabetes and coronary artery disease. Adipocyte 2021; 10(1):612-20.
  36. Shokri E, Heidarianpour A, Razavi Z. Positive effect of combined exercise on adipokines levels and pubertal signs in overweight and obese girls with central precocious puberty. Lipids in Health and Disease 2021; 20(1):1-4.
  37. Kao HH, Hsu HS, Wu TH, Chiang HF, Huang HY, Wang HJ, et al. Effects of a single bout of short-duration high-intensity and long-duration low-intensity exercise on insulin resistance and adiponectin/leptin ratio. Obesity research & clinical practice 2021; 15(1):58-63.
  38. Shele G, Genkil J, Speelman D. A systematic review of the effects of exercise on hormones in women with polycystic ovary syndrome. Journal of Functional Morphology and Kinesiology 2020; 5(2):35.
  39. Guo Q, Chang B, Yu QL, Xu ST, Yi XJ, Cao SC. Adiponectin treatment improves insulin resistance in mice by regulating the expression of the mitochondrial-derived peptide MOTS-c and its response to exercise via APPL1–SIRT1–PGC-1α. Diabetologia 2020; 63:2675-88.
  40. Dallak MA, Bin-Jaliah I, Albawardi A, Haidara MA, Sakr HF, Eid RA, et al. Swim exercise training ameliorates hepatocyte ultrastructural alterations in rats fed on a high fat and sugar diet. Ultrastructural pathology 2018; 42(2):155-61.
  41. Hasanheyvadi N, Razavinia F, Yahyavi Koochaksaraei F, Rezaei Chamani S. Role of adiponectin and nsafatin_1 hormones in polycystic ovary syndrome: systematic review. Iran J Obstet Gynecol Infertil 2020; 23(4):75-88.
  42. Orio F, Muscogiuri G, Giallauria F, Savastano S, Bottiglieri P, Tafuri D, et al. Oral contraceptives versus physical exercise on cardiovascular and metabolic risk factors in women with polycystic ovary syndrome: a randomized controlled trial. Clinical Endocrinology 2016; 85(5):764-71.
  43. Bahrami H, Mohseni M, Amini L, Karimian Z. The effect of six weeks yoga exercises on quality of life in infertile women with polycystic ovary syndrome (PCOS). Iran J Obstet Gynecol Infertil 2019; 22(5):18-26.
The Iranian Journal of Obstetrics, Gynecology and Infertility
Volume 26, Issue 1
March 2023
Pages 40-53

Files

Share

How to cite

Statistics