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Int J Sports Med 2012; 33(04): 268-278
DOI: 10.1055/s-0031-1297953
Physiology & Biochemistry
© Georg Thieme Verlag KG Stuttgart · New York

Physical Inactivity is a Major Contributor to Ovariectomy-Induced Sarcopenia

H. Fonseca
1   FADEUP, Biochemistry, Porto, Portugal
,
S. K. Powers
2   Applied Physiology, University of Florida, Gainesville, United States
,
D. Gonçalves
3   Biochemistry of Sports, FADEUP, Porto, Portugal
,
A. Santos
4   Faculty of Sports, CIAFEL, Porto, Portugal
,
M. P. Mota
5   Department of Sport, University of Tras-os-Montes e Alto Douro, Vila Real, Portugal
,
J. A. Duarte
6   Sport Biology, University of Porto, Portugal
› Author Affiliations
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Publication History



accepted after revision 07 November 2011

Publication Date:
19 January 2012 (online)

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Abstract

Since the mechanism(s) underlying menopause-related sarcopenia remain unknown we aimed to investigate the role of physical inactivity in its etiology. Ovariectomized and sham-operated rats were allocated into 2 experimental groups: 1) sedentary-standard housing; and 2) exercise-housed with running wheel. After a 9-month experimental period, soleus muscle structure and biochemical properties were analyzed. No differences existed in muscle fibre size or ultrastructure between sedentary sham and ovariectomized animals housed in standard conditions. In the exercise groups, average daily running distance was 10-fold less in ovariectomized compared to sham-animals. Further, in exercised animals, soleus fibre size was smaller in ovariectomized compared to sham-animals. Nonetheless, compared to both sedentary groups, muscle fibre size was larger in the exercised ovariectomized animals. Our results indicate that ovariectomy-induced sarcopenia is not due to the loss of ovarian hormones per se, but is largely due to physical inactivity.

Key words

voluntary running - menopause - sedentary behaviour - atrophy - estrogen - skeletal muscle loss
 

  • References

  • 1 Anantharaman-Barr HG, Decombaz J. The effect of wheel running and the estrous cycle on energy expenditure in female rats. Physiol Behav 1989; 46: 259-263
    CrossrefPubMedGoogle Scholar
  • 2 Angstwurm MW, Gartner R, Ziegler-Heitbrock HW. Cyclic plasma IL-6 levels during normal menstrual cycle. Cytokine 1997; 9: 370-374
    CrossrefPubMedGoogle Scholar
  • 3 Baltgalvis KA, Greising SM, Warren GL, Lowe DA. Estrogen regulates estrogen receptors and antioxidant gene expression in mouse skeletal muscle. PLoS One 2010; 5: e10164
    CrossrefPubMedGoogle Scholar
  • 4 Boland R, Vasconsuelo A, Milanesi L, Ronda AC, de Boland AR. 17beta-estradiol signaling in skeletal muscle cells and its relationship to apoptosis. Steroids 2008; 73: 859-863
    CrossrefPubMedGoogle Scholar
  • 5 Chen JQ, Delannoy M, Cooke C, Yager JD. Mitochondrial localization of ERalpha and ERbeta in human MCF7 cells. Am J Physiol 2004; 286: E1011-E1022
    CrossrefPubMedGoogle Scholar
  • 6 Chen JQ, Eshete M, Alworth WL, Yager JD. Binding of MCF-7 cell mitochondrial proteins and recombinant human estrogen receptors alpha and beta to human mitochondrial DNA estrogen response elements. J Cell Biochem 2004; 93: 358-373
    CrossrefPubMedGoogle Scholar
  • 7 Coore HG, Denton RM, Martin BR, Randle PJ. Regulation of adipose tissue pyruvate dehydrogenase by insulin and other hormones. Biochem J 1971; 125: 115-127
    PubMedGoogle Scholar
  • 8 Cushing BS, Marhenke S, McClure PA. Estradiol concentration and the regulation of locomotor activity. Physiol Behav 1995; 58: 953-957
    CrossrefPubMedGoogle Scholar
  • 9 Dionne IJ, Kinaman KA, Poehlman ET. Sarcopenia and muscle function during menopause and hormone-replacement therapy. J Nutr Health Aging 2000; 4: 156-161
    PubMedGoogle Scholar
  • 10 Giles ED, Jackman MR, Johnson GC, Schedin PJ, Houser JL, MacLean PS. Effect of the estrous cycle and surgical ovariectomy on energy balance, fuel utilization, and physical activity in lean and obese female rats. Am J Physiol 2010; 299: R1634-R1642
    CrossrefPubMedGoogle Scholar
  • 11 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
    CrossrefPubMedGoogle Scholar
  • 12 Guccione M, Silbiger S, Lei J, Neugarten J. Estradiol upregulates mesangial cell MMP-2 activity via the transcription factor AP-2. Am J Physiol 2002; 282: F164-F169
    PubMedGoogle Scholar
  • 13 Harriss DJ, Atkinson G. Update – Ethical Standards in Sport and Exercise Science Research. Int J Sports Med 2011; 32: 819-821
    Article in Thieme ConnectPubMedGoogle Scholar
  • 14 Johansson C, Lunde PK, Gothe S, Lannergren J, Westerblad H. Isometric force and endurance in skeletal muscle of mice devoid of all known thyroid hormone receptors. J Physiol 2003; 547: 789-796
    CrossrefPubMedGoogle Scholar
  • 15 Jozsa L, Kannus P, Thoring J, Reffy A, Jarvinen M, Kvist M. The effect of tenotomy and immobilisation on intramuscular connective tissue. A morphometric and microscopic study in rat calf muscles. J Bone Joint Surg Br 1990; 72: 293-297
    PubMedGoogle Scholar
  • 16 Kadi F, Karlsson C, Larsson B, Eriksson J, Larval M, Billig H, Jonsdottir IH. The effects of physical activity and estrogen treatment on rat fast and slow skeletal muscles following ovariectomy. J Muscle Res Cell Motil 2002; 23: 335-339
    CrossrefPubMedGoogle Scholar
  • 17 Lemoine S, Granier P, Tiffoche C, Rannou-Bekono F, Thieulant ML, Delamarche P. Estrogen receptor alpha mRNA in human skeletal muscles. Med Sci Sports Exerc 2003; 35: 439-443
    CrossrefPubMedGoogle Scholar
  • 18 McClung JM, Davis JM, Wilson MA, Goldsmith EC, Carson JA. Estrogen status and skeletal muscle recovery from disuse atrophy. J Appl Physiol 2006; 100: 2012-2023
    CrossrefPubMedGoogle Scholar
  • 19 McCormick KM, Burns KL, Piccone CM, Gosselin LE, Brazeau GA. Effects of ovariectomy and estrogen on skeletal muscle function in growing rats. J Muscle Res Cell Motil 2004; 25: 21-27
    CrossrefPubMedGoogle Scholar
  • 20 Moran AL, Nelson SA, Landisch RM, Warren GL, Lowe DA. Estradiol replacement reverses ovariectomy-induced muscle contractile and myosin dysfunction in mature female mice. J Appl Physiol 2007; 102: 1387-1393
    PubMedGoogle Scholar
  • 21 Moran AL, Warren GL, Lowe DA. Removal of ovarian hormones from mature mice detrimentally affects muscle contractile function and myosin structural distribution. J Appl Physiol 2006; 100: 548-559
    CrossrefPubMedGoogle Scholar
  • 22 Musatov S, Chen W, Pfaff DW, Mobbs CV, Yang XJ, Clegg DJ, Kaplitt MG, Ogawa S. Silencing of estrogen receptor alpha in the ventromedial nucleus of hypothalamus leads to metabolic syndrome. Proc Natl Acad Sci USA 2007; 104: 2501-2506
    CrossrefPubMedGoogle Scholar
  • 23 Ogawa S, Chan J, Gustafsson JA, Korach KS, Pfaff DW. Estrogen increases locomotor activity in mice through estrogen receptor alpha: specificity for the type of activity. Endocrinology 2003; 144: 230-239
    CrossrefPubMedGoogle Scholar
  • 24 Olson ME, Bruce J. Ovariectomy, ovariohysterectomy and orchidectomy in rodents and rabbits. Can Vet J 1986; 27: 523-527
    PubMedGoogle Scholar
  • 25 Pedram A, Razandi M, Levin ER. Nature of functional estrogen receptors at the plasma membrane. Mol Endocrinol 2006; 20: 1996-2009
    CrossrefPubMedGoogle Scholar
  • 26 Persky AM, Green PS, Stubley L, Howell CO, Zaulyanov L, Brazeau GA, Simpkins JW. Protective effect of estrogens against oxidative damage to heart and skeletal muscle in vivo and in vitro. Proc Soc Exp Biol Med 2000; 223: 59-66
    CrossrefPubMedGoogle Scholar
  • 27 Roubenoff R, Hughes VA. Sarcopenia: current concepts. J Gerontol A Biol Sci Med Sci 2000; 55: M716-M724
    CrossrefPubMedGoogle Scholar
  • 28 Sartori MG, Girao MJ, de Jesus Simoes M, Sartori JP, Baracat EC, Rodrigues de Lima G. Quantitative evaluation of collagen and muscle fibers in the lower urinary tract of castrated and under-hormone replacement female rats. Clin Exp Obstet Gynecol 2001; 28: 92-96
    PubMedGoogle Scholar
  • 29 Schaible TF, Malhotra A, Ciambrone G, Scheuer J. The effects of gonadectomy on left ventricular function and cardiac contractile proteins in male and female rats. Circ Res 1984; 54: 38-49
    CrossrefPubMedGoogle Scholar
  • 30 Scheuer J, Malhotra A, Schaible TF, Capasso J. Effects of gonadectomy and hormonal replacement on rat hearts. Circ Res 1987; 61: 12-19
    CrossrefPubMedGoogle Scholar
  • 31 Sorensen MB, Rosenfalck AM, Hojgaard L, Ottesen B. Obesity and sarcopenia after menopause are reversed by sex hormone replacement therapy. Obes Res 2001; 9: 622-626
    CrossrefPubMedGoogle Scholar
  • 32 Stenn PG, Klinge V. Relationship between the menstrual cycle and bodily activity in humans. Horm Behav 1972; 3: 297-305
    CrossrefPubMedGoogle Scholar
  • 33 Stirone C, Duckles SP, Krause DN, Procaccio V. Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol Pharmacol 2005; 68: 959-965
    CrossrefPubMedGoogle Scholar
  • 34 Sweat F, Puchtler H, Rosenthal SI. Sirius Red F3ba as a stain for connective tissue. Arch Pathol 1964; 78: 69-72
    PubMedGoogle Scholar
  • 35 Thomas DK, Storlien LH, Bellingham WP, Gillette K. Ovarian hormone effects on activity, glucoregulation and thyroid hormones in the rat. Physiol Behav 1986; 36: 567-573
    CrossrefPubMedGoogle Scholar
  • 36 Vasconsuelo A, Milanesi L, Boland R. 17Beta-estradiol abrogates apoptosis in murine skeletal muscle cells through estrogen receptors: role of the phosphatidylinositol 3-kinase/Akt pathway. J Endocrinol 2008; 196: 385-397
    CrossrefPubMedGoogle Scholar
  • 37 Velick S. Glyceraldehyde-3-Phosphate Dehydrogenase from Yeast. In: Colowick SP, Kaplan NO. (eds.). Methods in Enzymology. New York: Academic Press; 1955: 401
    CrossrefGoogle Scholar
  • 38 Weitzmann MN, Pacifici R. Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest 2006; 116: 1186-1194
    CrossrefPubMedGoogle Scholar
  • 39 Xu Y, Arenas IA, Armstrong SJ, Davidge ST. Estrogen modulation of left ventricular remodeling in the aged heart. Cardiovasc Res 2003; 57: 388-394
    CrossrefPubMedGoogle Scholar