Int J Sports Med 2022; 43(07): 632-641
DOI: 10.1055/a-1717-1693
Training & Testing

Effect of 12-wk Training in Ovariectomised Rats on PGC-1α, NRF-1 and Energy Substrates

1   Laboratory of Endocrine Physiology and Physical Exercise, Department of Physiological Sciences, Federal University of São Carlos, São Carlos, São Paulo, Brazil
,
Vinicius Silva Faria
1   Laboratory of Endocrine Physiology and Physical Exercise, Department of Physiological Sciences, Federal University of São Carlos, São Carlos, São Paulo, Brazil
,
Claudio Alexandre Gobatto
2   Laboratory of Applied Sport Physiology, Department of Sport Sciences, School of Applied Sciences, State University of Campinas, Limeira, São Paulo, Brazil
,
2   Laboratory of Applied Sport Physiology, Department of Sport Sciences, School of Applied Sciences, State University of Campinas, Limeira, São Paulo, Brazil
,
Pedro Paulo Menezes Scariot
2   Laboratory of Applied Sport Physiology, Department of Sport Sciences, School of Applied Sciences, State University of Campinas, Limeira, São Paulo, Brazil
,
Anabelle Silva Cornachione
3   Muscle Physiology and Biophysics Laboratory, Department of Physiological Sciences, Federal University of São Carlos, São Carlos, São Paulo, Brazil
,
Wladimir Rafael Beck
3   Muscle Physiology and Biophysics Laboratory, Department of Physiological Sciences, Federal University of São Carlos, São Carlos, São Paulo, Brazil
› Author Affiliations

Abstract

Metabolic diseases are associated with hypoestrogenism owing to their lower energy expenditure and consequent imbalance. Physical training promotes energy expenditure through PGC-1α and NRF-1, which are muscle proteins of the oxidative metabolism. However, the influence of physical training on protein expression in individuals with hypoestrogenism remains uncertain. Thus, the aim of this study is to determine the effect of 12 weeks of moderate-intensity swimming training on the muscle expression of PGC-1α, NRF-1, glycogen and triglyceride in ovariectomised rats. OVX and OVX+TR rats were subjected to ovariectomy. The trained animals swam for 30 minutes, 5 days/week, at 80% of the critical load intensity. Soleus was collected to quantify PGC-1α and NRF-1 expressions, while gastrocnemius and gluteus maximus were collected to measure glycogen and triglyceride. Blood glucose was also evaluated. Whereas ovariectomy decreased PGC-1α expression (p<0.05) without altering NRF-1 (p=0.48), physical training increased PGC-1α (p<0.01) and NRF-1 (p<0.05). Ovariectomy reduced glycogen (p<0.05) and triglyceride (p<0.05), whereas physical training increased glycogen (p<0.05) but did not change triglyceride (p=0.06). Ovariectomy increased blood glucose (p<0.01), while physical training reduced it (p<0.01). In summary, 12 weeks of individualized and moderate-intensity training were capable of preventing muscle metabolic consequences caused by ovariectomy.



Publication History

Received: 18 June 2021

Accepted: 15 November 2021

Article published online:
18 February 2022

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Edwards DP. Regulation of signal transduction pathways by estrogen and progesterone. Annu Rev Physiol 2005; 67: 335-376
  • 2 Cavalcanti-de-Albuquerque JPA, Salvador IC, Martins EL. et al. Role of estrogen on skeletal muscle mitochondrial function in ovariectomized rats: a time course study in different fiber types. J Appl Physiol (1985) 2014; 116: 779-789
  • 3 Hamilton DJ, Minze LJ, Kumar T. et al. Estrogen receptor alpha activation enhances mitochondrial function and systemic metabolism in high-fat-fed ovariectomized mice. Physiol Rep 2016; 4: e12913
  • 4 Zheng W, Rogoschin J, Niehoff A. et al. Combinatory effects of phytoestrogens and exercise on body fat mass and lipid metabolism in ovariectomized female rats. J Steroid Biochem Mol Biol 2018; 178: 73-81
  • 5 Seong-Hee Ko, Hyun-Sook Kim. Menopause-associated lipid metabolic disorders and foods beneficial for postmenopausal women. Nutrients 2020; 12: 202–226
  • 6 Medina-Contreras JML, Villalobos-Molina R, Zarain-Herzberg A. et al. Ovariectomized rodents as a menopausal metabolic syndrome model. A minireview. Mol Cell Biochem 2020; 475: 261-276
  • 7 Ventura-Clapier R, Piquereau J, Veksler V, Garnier A. Estrogens, estrogen receptors effects on cardiac and skeletal muscle mitochondria. Front Endocrinol (Lausanne) 2019; 10: 557
  • 8 Barbosa MR, Shiguemoto GE, Tomaz LM. et al. Resistance training and ovariectomy: Antagonic effects in mitochondrial biogenesis markers in rat skeletal muscle. Int J Sports Med 2016; 37: 841-848
  • 9 Ching-Feng Cheng, Hui-Chen Ku, Lin H. PGC-1α as a pivotal factor in lipid and metabolic regulation. Int J Mol Sci 2018; 19: 3447
  • 10 Yang Q, Wang C, Jin Y. et al. Disocin prevents postmenopausal atherosclerosis in ovariectomized LDLR-/-mice through a PGC-1α/ERα pathway leading to promotion of autophagy and inhibition of oxidative stress, inflammation and apoptosis. Pharmacol Res 2019; 148: 104414
  • 11 Ji LL, Kang C. Role of PGC-1α in sarcopenia: etiology and potential intervention-a mini-review. Gerontology 2015; 61: 139-148
  • 12 Huang TY, Zheng D, Houmard JA. et al. Overexpression of PGC-1α increases peroxisomal activity and mitochondrial fatty acid oxidation in human primary myotubes. Am J Physiol Endocrinol Metab 2017; 312: E253-E263
  • 13 Klinge CM. Estrogenic control of mitochondrial function. Redox Biol 2020; 31: 101435
  • 14 Park YM. Time since menopause and skeletal muscle estrogen receptors, PGC-1α, and AMPK. Menopause 2017; 24: 815–823
  • 15 Ikeda K, Horie-Inoue K, Inoue S. Functions of estrogen and estrogen receptor signaling on skeletal muscle. J Steroid Biochem Mol Biol 2019; 191: 105375
  • 16 Stacchiotti A, Favero G, Rodella LF. Impact of melatonin on skeletal muscle and exercise. Cells 2020; 9: 288–310
  • 17 Gan Z, Fu T, Kelly DP. et al. Skeletal muscle mitochondrial remodeling in exercise and diseases. Cell Res 2018; 28: 969-980
  • 18 Jin-Ho Koh, Hancock CR, Han Dong-Ho. et al. AMPK and PPARβ positive feedback loop regulates endurance exercise training-mediated GLUT4 expression in skeletal muscle. Am J Physiol Endocrinol Metab 2019; 316: E931-E939
  • 19 Holloszy JO. Regulation of mitochondrial biogenesis and GLUT4 expression by exercise. Compr Physiol 2011; 1: 921-940
  • 20 Kim HJ, Yoon HM, Kwon O, Lee WJ. The effect of pueraria lobata/rehmannia glutinosa and exercise on fatty acid transporters expression in ovariectomized rats skeletal muscles. J Exerc Nutrition Biochem 2016; 20: 32-38
  • 21 Harriss DJ, MacSween A, Atkinson G. Ethical standards in sport and exercise science research: 2020 update. Int J Sports Med 2019; 40: 813-817
  • 22 Zarrow MX, Yochim JM, McCarthy JL. Experimental Endocrinology: Sourcebook of Basic Techniques. New York: Academic Press; 1964: 39-40
  • 23 Gobatto CA, Scariot PPM, Ribeiro LFP. et al. Critical load estimation in young swimming rats using hyperbolic and linear models. Comp Exerc Physiol 2013; 9: 85-91
  • 24 De Lima AA, Gobatto CA, Messias LHD. et al. Two water environment adaptation models enhance motor behavior and improve the success of the lactate minimum test in swimming rats. Motriz: Rev Ed Fis 2017; 23: e101607
  • 25 American Physiological Society.. Resource Book for the Design of Animal Exercise Protocols. 2006: 35-41
  • 26 De Araujo GG, Papoti M, Dos Reis IGM, De Mello MAR, Gobatto CA. Physiological responses during linear periodized training in rats. Eur J Appl Physiol 2012; 112: 839-852
  • 27 Beck WR, Gobatto CA. Effects of maximum intensity aerobic swimming exercise until exhaustion at different times of day on the hematological parameters in rats. Acta Physiol Hung 2013; 100: 427-434
  • 28 Beck WR, Scariot PPM, Gobatto CA. Melatonin is an ergogenic aid for exhaustive aerobic exercise only during the wakefulness period. Int J Sports Med 2016; 37: 71-76
  • 29 Beck WR, Scariot PPM, Carmo SS. et al. Metabolic profile and spontaneous physical activity modulation under short-term food restriction in young rats. Motriz: Rev Ed Fis 2017; 23: e101606
  • 30 Scariot PP, Manchado-Gobatto FB, Torsoni AS. et al. Continuous aerobic training in individualized intensity avoids spontaneous physical activity decline and improves MCT1 expression in oxidative muscle of swimming rats. Front Physiol 2016; 7: 132
  • 31 Scariot PPM, Manchado-Gobatto FB, Prolla TA. et al. Housing conditions modulate spontaneous physical activity, feeding behavior, aerobic running capacity and adiposity in C57BL/6J mice. Horm Behav 2019; 115: 104556
  • 32 Biesiadecki BJ, Brand PH, Koch LG, Britton SL. A gravimetric method for the measurement of total spontaneous activity in rats. Proc Soc Exp Biol Med 1999; 222: 65-69
  • 33 American Veterinary Medical Association. AVMA Guidelines for the Euthanasia of Animals: 2013 Edition; 2013: 44–45
  • 34 Bradley H, Shaw CS, Worthington PL. et al. Quantitative immunofluorescence microscopy of subcellular GLUT 4 distribution in human skeletal muscle: Effects of endurance and sprint interval training. Physiol Rep 2014; 2: e12085
  • 35 Da Rocha AL, Pereira BC, Teixeira GR. et al. Treadmill slope modulates inflammation, fiber type composition, androgen, and glucocorticoid receptors in the skeletal muscle of overtrained mice. Front Immunol 2017; 8: 1378
  • 36 Dubois M, Gilles KA, Hamilton JK. et al. Colorimetric method for determination of sugars and related substances. Anal Chem 1956; 28: 350-356
  • 37 Cohen J. Statistical Power Analysis for the Behavioral Sciences. Abingdon. England: Routledge; 1988
  • 38 Glatz JFC, Luiken JJFP. Dynamic role of the transmembrane glycoprotein CD36 (SR-B2) in cellular fatty acid uptake and utilization. J Lipid Res 2018; 59: 1084-1093
  • 39 Saengsirisuwan V, Pongseeda S, Prasannarong M. et al. Modulation of insulin resistance in ovariectomized rats by endurance exercise training and estrogen replacement. Metabolism 2009; 58: 38-47
  • 40 Michael LF, Wu Z, Cheatham RB. et al. Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc Nat Acad Sci U S A 2001; 98: 3820-3825
  • 41 Davis SR, Lambrinoudaki I, Lumsden M. et al. Menopause. Nat Rev Dis Primers 2015; 1: 15004
  • 42 Inada A, Fujii NL, Inada O. et al. Effects of 17β-estradiol and androgen on glucose metabolism in skeletal muscle. Endocrinology 2016; 157: 4691-4705
  • 43 Baxi D, Singh PK, Vachhrajani K. et al. Melatonin supplementation therapy as a potent alternative to ERT in ovariectomized rats. Climacteric 2012; 15: 382-392
  • 44 Bian C, Bai B, Gao Q. et al. 17β-estradiol regulates glucose metabolism and insulin secretion in rat islet β cells through GPER and Akt/mTOR/GLUT2 pathway. Front Endocrinol (Lausanne) 2019; 10: 531
  • 45 Capllonch-Amer G, Sbert-Roig M, Galmés-Pascual BM. et al. Estradiol stimulates mitochondrial biogenesis and adiponectin expression in skeletal muscle. J Endocrinol 2014; 221: 391-403
  • 46 Faude O, Kindermann W, Meyer T. Lactate threshold concepts. Sports Med 2009; 39: 469-490
  • 47 Booth FW, Ruegsegger GN, Toedebusch RG. et al. Endurance exercise and the regulation of skeletal muscle metabolism. Prog Mol Biol Transl Sci 2015; 135: 129-151
  • 48 Goto M, Terada S, Kato M. et al. cDNA cloning and mRNA analysis of PGC-1 in epitrochlearis muscle in swimming-exercised rats. Biochem Biophys Res Commun 2000; 274: 350-354
  • 49 Islam H, Hood DA, Gurd BJ. The impact of acute and chronic exercise on Nrf2 expression in relation to markers of mitochondrial biogenesis in human skeletal muscle. Eur J Appl Physiol 2020; 120: 149-160
  • 50 Huss JM, Torra IP, Staels B. et al. Estrogen-related receptor α directs peroxisome proliferator-activated receptor α signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol Cell Biol 2004; 24: 9079-9091
  • 51 Baar K, Wende AR, Jones TE. et al. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J 2002; 16: 1879-1886
  • 52 Wende AR, Schaeffer PJ, Parker GJ, Zechner C, Han Dong-Ho, Chen MM. et al. A role for the transcriptional coactivator PGC-1α in muscle refueling. J Biol Chem 2007; 282: 36642-36651
  • 53 Hue L, Taegtmeyer H. The Randle cycle revisited: a new head for an old hat. Am J Physiol Endocrinol Metab 2009; 297: E578-E591
  • 54 Lehnig AC, Stanford KI. Exercise-induced adaptations to white and brown adipose tissue. J Exp Biol 2018; 221: jeb161570
  • 55 Garland T, Schutz H, Chappell MA. et al. The biological control of voluntary exercise, spontaneous physical activity and daily energy expenditure in relation to obesity: human and rodent perspectives. J Exp Biol 2011; 14: 206-229
  • 56 Kotz CM. et al. Spontaneous physical activity defends against obesity. Curr Obes Rep 2017; 6: 362-370
  • 57 Thompson D, Karpe F, Lafontan M, Frayan K. Physical activity and exercise in the regulation of human adipose tissue physiology. Physiol Rev 2012; 92: 157-191
  • 58 Koebele SV, Bimonte-Nelson HA. Modeling menopause: the utility of rodents in translational behavioral endocrinology research. Maturitas 2016; 87: 5-17