Resistance Training and Ovariectomy: Antagonic Effects in Mitochondrial Biogenesis Markers in Rat Skeletal Muscle

M. R. Barbosa; G. E. Shiguemoto; L. M. Tomaz; F. C. Ferreira; M. F. C. Rodrigues; M. M. Domingues; M. V. C. Souza Master; G. H. R. Canevazzi; N. S. Silva-Magosso; H. S. Selistre-de-Araujo; S. EA Perez

doi:10.1055/s-0042-107247

International Journal of Sports Medicine, Inhaltsverzeichnis

Int J Sports Med 2016; 37(11): 841-848
DOI: 10.1055/s-0042-107247

Physiology & Biochemistry

Resistance Training and Ovariectomy: Antagonic Effects in Mitochondrial Biogenesis Markers in Rat Skeletal Muscle

M. R. Barbosa

¹Education in Health, Universidade Federal de Sergipe, Lagarto, Brazil

,

G. E. Shiguemoto

²Department of Physiological Sciences, Federal University of São Carlos, São Carlos, Brazil

,

L. M. Tomaz

³Physiological Sciences, Federal University of Sao Carlos, Ribeirão Preto, Brazil

,

F. C. Ferreira

⁴Physiological Sciences, Federal University of Sao Carlos, São Carlos, Brazil

,

M. F. C. Rodrigues

⁵Ciências Fisiológicas, Universidade Federal de São Carlos, São Carlos, Brazil

,

M. M. Domingues

⁵Ciências Fisiológicas, Universidade Federal de São Carlos, São Carlos, Brazil

,

M. V. C. Souza Master

⁶Department of Physiological Sciences, Laboratory of Exercise Physiology, Federal University of São Carlos, São Carlos, Brazil

,

G. H. R. Canevazzi

³Physiological Sciences, Federal University of Sao Carlos, Ribeirão Preto, Brazil

,

N. S. Silva-Magosso

⁷Physiological Sciences – Physiology of Exercise, Federal University of São Carlos, São Carlos, Brazil

,

H. S. Selistre-de-Araujo

⁵Ciências Fisiológicas, Universidade Federal de São Carlos, São Carlos, Brazil

,

S. EA Perez

⁸Department of Phsysiological Sciences, Federal University of SÃ£o Carlos (UFSCar), São Carlos, Brazil

› Institutsangaben

Abstract

Estrogen reduction is associated with a decline in skeletal muscle mitochondrial biogenesis. Molecular events associated with improvements in markers of mitochondrial biogenesis after resistance training and estradiol replacement are unknown. This study aimed to investigate the effects of ovariectomy, resistance training, and estradiol replacement on markers of mitochondrial biogenesis and protein expression related to oxidative capacity in the rat gastrocnemius pool. Estradiol replacement was performed using Silastic^® capsules. During the 12-week resistance training, animals climbed a ladder with weights attached to their tails. Gene expression was analysed by RT-PCR, and protein content was determined by western blotting. Ovariectomy decreased the gene expression of the mitochondrial biogenesis markers PGC-1α (~73%), NRF-1 (~44%), and TFAM (~53%) (p<0.05) and decreased the protein expression of phosphorylated AMPK, CREB and AKT, which are related to oxidative capacity. Resistance training increased PGC-1α (~59%) and TFAM (~48%) expression compared to the Ovariectomy-Sedentary group. The combination of resistance training and estradiol replacement was superior to the ovariectomy-sedentary and ovariectomy-resistance training treatments regarding the gastrocnemius muscle. Estrogen deficiency altered the expression of genes and proteins that favour the development of a mitochondrial dysfunction phenotype, which was improved with resistance training and was partially improved by estradiol replacement.

Key words

mitochondrial biogenesis - ovariectomy - resistance training - skeletal muscle

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References
1 Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, Rosenberg PB, Williams RS, Yan Z. Exercise stimulates PGC-1α transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem 2005; 280: 19587-19593
2 Baltgalvis KA, Greising SM, Warren GL, Lowe DA. Estrogen regulates estrogen receptors and antioxidant gene expression in mouse skeletal muscle. PLoS One 2010; 5: 10164
3 Berchtold MW, Brinkmeier H, Muntener M. Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol Rev 2000; 80: 1215-1265
4 Bo H, Zhang Y, Ji LL. Redefining the role of mitochondria in exercise: a dynamic remodeling. Ann N Y Acad Sci 2012; 1201: 121-128
5 Brault JJ, Jespersen JG, Goldberg AL. Peroxisome proliferator-activated receptor gamma coactivator 1alpha or 1beta overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy. J Biol Chem 2010; 285: 19460-19471
6 Brinton RD. Minireview: translational animal models of human menopause: challenges and emerging opportunities. Endocrinology 2012; 153: 3571-3578
7 Brinton RD. The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications. Trends Neurosci 2008; 31: 529-537
8 Brown M, Ferreira JA, Foley AM, Hemmann KM. A rehabilitation exercise program to remediate skeletal muscle atrophy in an estrogen-deficient organism may be ineffective. Eur J Appl Physiol 2012; 112: 91-104
9 Caffin F, Prola A, Piquereau J, Novotova M, David DJ, Garnier A, Fortin D, Alavi MV, Veksler V, Ventura-Clapier R, Joubert F. Altered skeletal muscle mitochondrial biogenesis but improved endurance capacity in trained OPA1-deficient mice. J Physiol 2013; 591: 6017-6037
10 Calvo JA, Daniels TG, Wang X, Paul A, Lin J, Spiegelman BM, Stevenson SC, Rangwala SM. Muscle-specific expression of PPARgamma coactivator-1alpha improves exercise performance and increases peak oxygen uptake. J Appl Physiol 2008; 104: 1304-1312
11 Chen JQ, Cammarata PR, Baines CP, Yager JD. Regulation of mitochondrial respiratory chain biogenesis by estrogens/estrogen receptors and physiological, pathological and pharmacological implications. Biochim Biophys Acta 2009; 1793: 1540-1570
12 Corton JC, Apte U, Anderson SP, Limaye P, Yoon L, Latendresse J, Dunn C, Everitt JI, Voss KA, Swanson C, Kimbrough C, Wong JS, Gill SS, Chandraratna RA, Kwak MK, Kensler TW, Stulnig TM, Steffensen KR, Gustafsson JA, Mehendale HM. Mimetics of caloric restriction include agonists of lipid-activated nuclear receptors. J Biol Chem 2004; 279: 46204-46212
13 Ding H, Jiang N, Liu H, Liu X, Liu D, Zhao F, Wen L, Liu S, Ji LL, Zhang Y. Response of mitochondrial fusion and fission protein gene expression to exercise in rat skeletal muscle. Biochim Biophys Acta 2010; 1800: 250-256
14 Domingos MM, Rodrigues MF, Stotzer US, Bertucci DR, Souza MV, Marine DA, Gatto C, do V, de Araujo HS, de Andrade Perez SE. Resistance training restores the gene expression of molecules related to fat oxidation and lipogenesis in the liver of ovariectomized rats. Eur J Appl Physiol 2012; 112: 1437-1444
15 Gigli I, Bussmann LE. Exercise and ovarian steroid hormones: their effects on mitochondrial respiration. Life Sci 2001; 68: 1505-1514
16 Gorzek JF, Hendrickson KC, Forstner JP, Rixen JL, Moran AL, Lowe DA. Estradiol and tamoxifen reverse ovariectomy-induced physical inactivity in mice. Med Sci Sports Exerc 2007; 39: 248-256
17 Harriss DJ, Atkinson G. Ethical standards in sports and exercise science research: 2016 update. Int J Sports Med. 2015 36. 1121-1124
18 Holloszy JO. Regulation by exercise of skeletal muscle content of mitochondria and Glut4. J Physiol Pharmacol 2008; 59: 5-18
19 Hood DA, Irrcher I, Ljubicic V, Joseph AM. Coordination of metabolic plasticity in skeletal muscle. J Exp Biol 2006; 209: 2265-2275
20 Hoppeler H, Fluck M. Plasticity of skeletal muscle mitochondria: structure and function. Med Sci Sports Exer 2003; 35: 95-104
21 Hornberger Jr TA, Farrar RP. Physiological hypertrophy of the FHL muscle following 8 weeks of progressive resistance exercise in the rat. Can J Appl Physiol 2004; 29: 16-31
22 Hsieh YC, Yang S, Choudhry MA, Yu HP, Rue LW, Bland KI, Chaudry IH. PGC-1 upregulation via estrogen receptors: a common mechanism of salutary effects of estrogen and flutamide on heart function after trauma hemorrhage. Am J Physiol Heart Circ Physiol 2005; 289: 2665-2672
23 Irwin RW, Yao J, To J, Hamilton RT, Cadenas E, Brinton RD. Selective oestrogen receptor modulators differentially potentiate brain mitochondrial function. J Neuroendocrinology 2002; 24: 236-248
24 Jager S, Handschin C, St-Pierre J, Spiegelman BM. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci USA 2007; 104: 12017-12022
25 Kalu DN. The ovariectomized rat model of postmenopausal bone loss. Bone Miner 1991; 15: 175-191
26 Kang C, Ji LL. Role of PGC-1 signaling in skeletal muscle health and disease. Ann NY Acad Sci 2012; 1271: 110-117
27 Leone TC, Lehman JJ, Finck BN, Schaeffer PJ, Wende AR, Boudina S, Courtois M, Wozniak DF, Sambandam N, Bernal-Mizrachi C, Chen Z, Holloszy JO, Medeiros DM, Schmidt RE, Saffitz JE, Abel ED, Semenkovich CF, Kelly DP. PGC-1a Deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol 2005; 672-687
28 Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 2005; 1: 361-370
29 Lobo RA, Davis SR, De Villiers TJ, Gompel A, Henderson VW, Hodis HN, Lumsden MA, Mack WJ, Shapiro S, Baber RJ. Prevention of diseases after menopause. Climacteric 2014; 17: 540-556
30 Mannella P, Brinton RD. Estrogen receptor protein interaction with phosphatidylinositol 3-kinase leads to activation of phosphorylated Akt and extracellular signal-regulated kinase 1/2 in the same population of cortical neurons: a unified mechanism of estrogen action. J Neurosci 2009; 26: 9439-9447
31 Mitterling KL, Spencer JL, Dziedzic N, Shenoy S, McCarthy K, Waters EM, McEwen BS, Teresa A, Milner TA. Cellular and subcellular localization of estrogen and progestin receptor immunoreactivities in the mouse hippocampus. J Comp Neurol 2010; 518: 2729-2743
32 Musatov S, Chen W, Pfaff DW, Mobbs CV, Yang XJ, Clegg DJ, Kaplitt MG, Ogawa S. Silencing of estrogen receptor α in the ventromedial nucleus of hypothalamus leads to metabolic syndrome. Proc Natl Acad Sci USA 2007; 104: 2501-2506
33 Nedrow A, Miller J, Walker M, Nygren P, Huffman LH, Nelson HD. Complementary and alternative therapies for the management of menopause-related symptoms: a systematic evidence review. Arch Intern Med 2006; 166: 1453-1465
34 Nigro M, Santos AT, Barthem CS, Louzada RAN, Fortunato RS, Ketzer LA, Carvalho DP, Meis L. A change in liver metabolism but not in brown adipose tissue thermogenesis is an early event in ovariectomy-induced obesity in rats. Endocrinology 2014; 155: 2881-2891
35 Palmer K, Gray J. Central vs. peripheral effects of estrogen on food intake and lipoprotein lipase activity in ovariectomized rats. Physiol Behav 1986; 37: 187-189
36 Pantaleão TU, Mousovich F, Rosenthal D, Padron AS, Carvalho DP, da Costa VM. Effect of serum estradiol and leptin levels on thyroid function, food intake and body weight gain in female Wistar rats. Steroids 2010; 75: 638-642
37 Pighon A, Gutkowska J, Jankowski M, Rabasa-Lhoret R, Lavoie JM. Exercise training in ovariectomized rats stimulates estrogenic – like effects on expression of genes involved in lipid accumulation and subclinical inflammation in liver. Metabolism 2011; 60: 629-639
38 Prestes J, De Cassia Marqueti R, Shiguemoto GE, Leite RD, Pereira GB, Selistrede-Araujo HS, Baldissera V, de Andrade Perez SE. Effects of ovariectomy and resistance training on MMP-2 activity in skeletal muscle. Appl Physiol Nutr Metab 2009; 34: 700-706
39 Puigserver P, Spiegelman BM. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev 2003; 24: 78-90
40 Rogers NH, Perfield JW, Strissel KJ, Obin MS, Greenberg AS. Reduced energy expenditure and increased inflammation are early events in the development of ovariectomy-induced obesity. Endocrinology 2009; 150: 2161-2168
41 Santen RJ, Allred DC, Ardoin SP, Archer DF, Boyd N, Braunstein GD, Burger HG, Colditz GA, Davis SR, Gambacciani M, Gower BA, Henderson VW, Jarjour WN, Karas RH, Kleerekoper M, Lobo RA, Manson JE, Marsden J, Martin KA, Martin L, Pinkerton JV, Rubinow DR, Teede H, Thiboutot DM, Utian WH. Postmenopausal hormone therapy: an Endocrine Society scientific statement. J Clin Endocrinol Metab 2010; 1-66
42 Scarpulla RC. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim Biophys Acta 2011; 1813: 1269-1278
43 Shiguemoto GE, Prestes J, Leite RD, Pereira GB, Pontes CL, D’Avila FV, Botero JP, Baldissera V, Nonaka KO, Selistre-de-Araujo HS, Perez SE. Effects of resistance training on matrix metalloproteinase-2 activity and biomechanical and physical properties of bone in ovariectomized and intact rats. Scand J Med Sci Sports 2012; 22: 607-617
44 Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. Measurement of protein using bicinchoninic acid. Anal Biochem 1985; 150: 76-85
45 Strom JO, Theodorsson E, Theodorsson A. Order of magnitude differences between methods for maintaining physiological 17β-estradiol concentrations in ovariectomized rats. Scand J Clin Lab Invest 2008; 68: 814-822
46 Taaffe DR. Sarcopenia – Exercise as a treatment strategy. Aust Fam Physician 2006; 35: 130-134
47 Terada S, Goto M, Kato M, Pantaleão TU, Mousovich F, Rosenthal D, Padrón AS, Carvalho DP, da Costa VM. Effects of low-intensity prolonged exercise on PGC-1 mRNA expression in rat epitrochlearis muscle. Biochem Biophys Res Commun 2002; 296: 350-354
48 Wright DC, Han DH, Garcia-Roves PM, Geiger PC, Jones TE, Holloszy JO. Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1 alpha expression. J Biol Chem 2007; 282: 194-199
49 Xu Y, Lin J, Wang S, Xiong J, Zhu Q. Combined estrogen replacement therapy on metabolic control in postmenopausal women with diabetes mellitus. Kaohsiung J Med Sci 2014; 30: 350-361
50 Zierau O, Zheng KY, Papke A, Dong TT, Tsim KW, Vollmer G. Functions of Danggui Buxue Tang, a Chinese herbal decoction containing Astragali radix and Angelicae sinensis radix, in uterus and liver are both estrogen receptor-dependent and independent. Evid Based Complement Alternat Med 2014; 438531