Advertisement

Sports Medicine

, Volume 40, Issue 1, pp 41–58 | Cite as

The Influence of Estrogen on Skeletal Muscle

Sex Matters
  • Deborah L. Enns
  • Peter M. TiidusEmail author
Review Article

Abstract

As women enter menopause, the concentration of estrogen and other female hormones declines. This hormonal decrease has been associated with a number of negative outcomes, including a greater incidence of injury as well as a delay in recovery from these injuries. Over the past two decades, our understanding of the protective effects of estrogen against various types of injury and disease states has grown immensely. In skeletal muscle, studies with animals have demonstrated that sex and estrogen may potentially influence muscle contractile properties and attenuate indices of post-exercise muscle damage, including the release of creatine kinase into the bloodstream and activity of the intramuscular lysosomal acid hydrolase, β-glucuronidase. Furthermore, numerous studies have revealed an estrogen-mediated attenuation of infiltration of inflammatory cells such as neutrophils and macrophages into the skeletal muscles of rats following exercise or injury. Estrogen has also been shown to play a significant role in stimulating muscle repair and regenerative processes, including the activation and proliferation of satellite cells. Although the mechanisms by which estrogen exerts its influence upon indices of skeletal muscle damage, inflammation and repair have not been fully elucidated, it is thought that estrogen may potentially exert its protective effects by: (i) acting as an antioxidant, thus limiting oxidative damage; (ii) acting as a membrane stabilizer by intercalating within membrane phospholipids; and (iii) binding to estrogen receptors, thus governing the regulation of a number of downstream genes and molecular targets. In contrast to animal studies, studies with humans have not as clearly delineated an effect of estrogen on muscle contractile function or on indices of post-exercise muscle damage and inflammation. These inconsistencies have been attributed to a number of factors, including age and fitness level of subjects, the type and intensity of exercise protocols, and a focus on sex differences that typically involve factors and hormones in addition to estrogen. In recent years, hormone replacement therapy (HRT) or estrogen combined with exercise have been proposed as potentially therapeutic agents for postmenopausal women, as these agents may potentially limit muscle damage and inflammation and stimulate repair in this population. While the benefits and potential health risks of long-term HRT use have been widely debated, controlled studies using short-term HRT or other estrogen agonists may provide future new and valuable insights into understanding the effects of estrogen on skeletal muscle, and greatly benefit the aging female population. Recent studies with older females have begun to demonstrate their benefits.

Keywords

Estrogen Hormone Replacement Therapy Satellite Cell Muscle Damage Muscle Injury 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

No sources of funding were used to assist in the preparation of this review. The authors have no conflicts of interest that are directly relevant to the content of this review.

References

  1. 1.
    Tiidus PM. Can estrogens diminish exercise induced muscle damage? Can J Appl Physiol 1995; 20: 26–38PubMedCrossRefGoogle Scholar
  2. 2.
    Tiidus PM. Oestrogen and sex influence on muscle damage and inflammation: evidence from animal models. Curr Opin Clin Nutr Metab Care 2001; 4: 509–13PubMedCrossRefGoogle Scholar
  3. 3.
    Kendall B, Eston R. Exercise-induced muscle damage and the potential protective role of estrogen. Sports Med 2002; 32: 103–23PubMedCrossRefGoogle Scholar
  4. 4.
    Tiidus PM. Influence of estrogen on skeletal muscle damage, inflammation, and repair. Exerc Sport Sci Rev 2003; 31: 40–4PubMedCrossRefGoogle Scholar
  5. 5.
    Tiidus PM, Enns DL, Hubal MJ, et al. Point-counterpoint: estrogen and sex do/do not influence post-exercise indices of muscle damage, inflammation and repair. J Appl Physiol 2009; 106: 110–5Google Scholar
  6. 6.
    Kahlert S, Grohe C, Karas RH, et al. Effects of estrogen on skeletal myoblast growth. Biochem Biophys Res Commun 1997; 232: 373–8PubMedCrossRefGoogle Scholar
  7. 7.
    Sipila S, Taaffe DR, Cheng S, et al. Effects of hormone replacement therapy and high-impact physical exercise on skeletal muscle in post-menopausal women: a randomized placebo-controlled study. Clin Sci (Lond) 2001; 101: 147–57CrossRefGoogle Scholar
  8. 8.
    Sorensen MB, Rosenfalck AM, Hojgaard L, et al. Obesity and sarcopenia after menopause are reversed by sex hormone replacement therapy. Obes Res 2001; 9: 622–6PubMedCrossRefGoogle Scholar
  9. 9.
    Taaffe DR, Sipila S, Cheng S, et al. The effect of hormone replacement therapy and/or exercise on skeletal muscle attenuation in postmenopausal women: a yearlong intervention. Clin Physiol Funct Imaging 2005; 25: 297–304PubMedCrossRefGoogle Scholar
  10. 10.
    Teixeira PJ, Going SB, Houtkooper LB, et al. Resistance training in postmenopausal women with and without hormone therapy. Med Sci Sports Exerc 2003; 35: 555–62PubMedCrossRefGoogle Scholar
  11. 11.
    Ronkainen PH, Kovanen V, Alen M, et al. Postmenopausal hormone replacement therapy modifies skeletal muscle composition and function: a study with monozygotic twin pairs. J Appl Physiol 2009; 107: 25–33PubMedCrossRefGoogle Scholar
  12. 12.
    Taaffe DR, Newman AB, Haggerty CL, et al. Estrogen replacement, muscle composition, and physical function: the Health ABC study. Med Sci Sports Exerc 2005; 37: 1741–7PubMedCrossRefGoogle Scholar
  13. 13.
    Sciote JJ, Horton MJ, Zyman Y, et al. Differential effects of diminished oestrogen and androgen levels on development of skeletal muscle fibres in hypogonadal mice. Acta Physiol Scand 2001; 172: 179–87PubMedCrossRefGoogle Scholar
  14. 14.
    Skelton DA, Phillips SK, Bruce SA, et al. Hormone replacement therapy increases isometric muscle strength of adductor pollicis in post-menopausal women. Clin Sci (Lond) 1999; 96: 357–64CrossRefGoogle Scholar
  15. 15.
    Bemben DA, Langdon DB. Relationship between estrogen use and musculoskeletal function in postmenopausal women. Maturitas 2002; 42: 119–27PubMedCrossRefGoogle Scholar
  16. 16.
    Brown M, Birge SJ, Kohrt WM. Hormone replacement therapy does not augment gains in muscle strength or fatfree mass in response to weight-bearing exercise. J Gerontol A Biol Sci Med Sci 1997; 52: B166–70CrossRefGoogle Scholar
  17. 17.
    Bassey EJ, Mockett SP, Fentem PH. Lack of variation in muscle strength with menstrual status in healthy women aged 45-54 years: data from a national survey. Eur J Appl Physiol Occup Physiol 1996; 73: 382–6PubMedCrossRefGoogle Scholar
  18. 18.
    Taaffe DR, Luz VM, Delay R, et al. Maximal muscle strength of elderly women is not influenced by oestrogen status. Age Ageing 1995; 24: 329–33PubMedCrossRefGoogle Scholar
  19. 19.
    Maddalozzo GF, Cardinal BJ, Li F, et al. The association between hormone therapy use and changes in strength and body composition in early postmenopausal women. Menopause 2004; 11: 438–46PubMedCrossRefGoogle Scholar
  20. 20.
    McCormick KM, Burns KL, Piccone CM, et al. Effects of ovariectomy and estrogen on skeletal muscle function in growing rats. J Muscle Res Cell Motil 2004; 25: 21–7PubMedCrossRefGoogle Scholar
  21. 21.
    Schneider BS, Fine JP, Nadolski T, et al. The effects of estradiol and progesterone on plantarflexor muscle fatigue in ovariectomized mice. Biol Res Nurs 2004; 5: 265–75PubMedCrossRefGoogle Scholar
  22. 22.
    Hatae J. Effects of 17beta-estradiol on tension responses and fatigue in the skeletal twitch muscle fibers of frog. Jpn J Physiol 2001; 51: 753–9PubMedCrossRefGoogle Scholar
  23. 23.
    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: 548–59PubMedCrossRefGoogle Scholar
  24. 24.
    Wattanapermpool J, Reiser PJ. Differential effects of ovariectomy on calcium activation of cardiac and soleus myofilaments. Am J Physiol 1999; 277: H467–73Google Scholar
  25. 25.
    Warren GL, Lowe DA, Inman CL, et al. Estradiol effect on anterior crural muscles-tibial bone relationship and susceptibility to injury. J Appl Physiol 1996; 80: 1660–5PubMedGoogle Scholar
  26. 26.
    Moran AL, Nelson SA, Landisch RM, et al. Estradiol replacement reverses ovariectomy-induced muscle contractile and myosin dysfunction in mature female mice. J Appl Physiol 2007; 102: 1387–93PubMedCrossRefGoogle Scholar
  27. 27.
    Clark BC, Manini TM, The DJ, et al. Gender differences in skeletal muscle fatigability are related to contraction type and EMG spectral compression. J Appl Physiol 2003; 94: 2263–72PubMedGoogle Scholar
  28. 28.
    Fulco CS, Rock PB, Muza SR, et al. Slower fatigue and faster recovery of the adductor pollicis muscle in women matched for strength with men. Acta Physiol Scand 1999; 167: 233–9PubMedCrossRefGoogle Scholar
  29. 29.
    Hunter SK, Critchlow A, Shin IS, et al. Men are more fatigable than strength-matched women when performing intermittent submaximal contractions. J Appl Physiol 2004; 96: 2125–32PubMedCrossRefGoogle Scholar
  30. 30.
    Maughan RJ, Harmon M, Leiper JB, et al. Endurance capacity of untrained males and females in isometric and dynamic muscular contractions. Eur J Appl Physiol Occup Physiol 1986; 55: 395–400PubMedCrossRefGoogle Scholar
  31. 31.
    Petrofsky JS, Burse RL, Lind AR. Comparison of physiological responses of women and men to isometric exercise. J Appl Physiol 1975; 38: 863–8PubMedGoogle Scholar
  32. 32.
    Phillips SK, Rook KM, Siddle NC, et al. Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy. Clin Sci (Lond) 1993; 84: 95–8Google Scholar
  33. 33.
    Sipila S, Poutamo J. Muscle performance, sex hormones and training in peri-menopausal and post-menopausal women. Scand J Med Sci Sports 2003; 13: 19–25PubMedCrossRefGoogle Scholar
  34. 34.
    Greeves JP, Cable NT, Luckas MJ, et al. Effects of acute changes in oestrogen on muscle function of the first dorsal interosseus muscle in humans. J Physiol 1997; 500 (Pt 1): 265–70PubMedGoogle Scholar
  35. 35.
    Onambele NG, Skelton DA, Bruce SA, et al. Follow-up study of the benefits of hormone replacement therapy on isometric muscle strength of adductor pollicis in postmenopausal women. Clin Sci (Lond) 2001; 100: 421–2CrossRefGoogle Scholar
  36. 36.
    Greeves JP, Cable NT, Reilly T, et al. Changes in muscle strength in women following the menopause: a longitudinal assessment of the efficacy of hormone replacement therapy. Clin Sci (Lond) 1999; 97: 79–84CrossRefGoogle Scholar
  37. 37.
    Phillips SK, Sanderson AG, Birch K, et al. Changes in maximal voluntary force of human adductor pollicis muscle during the menstrual cycle. J Physiol 1996; 496 (Pt 2): 551–7PubMedGoogle Scholar
  38. 38.
    Sarwar R, Niclos BB, Rutherford OM. Changes in muscle strength, relaxation rate and fatiguability during the human menstrual cycle. J Physiol 1996; 493 (Pt 1): 267–72PubMedGoogle Scholar
  39. 39.
    Suzuki S, Yamamuro T. Long-term effects of estrogen on rat skeletal muscle. Exp Neurol 1985; 87: 291–9PubMedCrossRefGoogle Scholar
  40. 40.
    Carville SF, Rutherford OM, Newham DJ. Power output, isometric strength and steadiness in the leg muscles of preand postmenopausal women: the effects of hormone replacement therapy. Eur J Appl Physiol 2006; 96: 292–8PubMedCrossRefGoogle Scholar
  41. 41.
    Sotiriadou S, Kyparos A, Albani M, et al. Soleus muscle force following downhill running in ovariectomized rats treated with estrogen. Appl Physiol Nutr Metab 2006; 31: 449–59PubMedCrossRefGoogle Scholar
  42. 42.
    Tiidus PM, Bestic NM, Tupling R. Estrogen and gender do not affect fatigue resistance of extensor digitorum longus muscle in rats. Physiol Res 1999; 48: 209–13PubMedGoogle Scholar
  43. 43.
    Hubal MJ, Ingalls CP, Allen MR, et al. Effects of eccentric exercise training on cortical bone and muscle strength in the estrogen-deficient mouse. J Appl Physiol 2005; 98: 1674–81PubMedCrossRefGoogle Scholar
  44. 44.
    Hubal MJ, Rubinstein SR, Clarkson PM. Muscle function in men and women during maximal eccentric exercise. J Strength Cond Res 2008; 22: 1332–8PubMedCrossRefGoogle Scholar
  45. 45.
    MacIntyre DL, Reid WD, Lyster DM, et al. Different effects of strenuous eccentric exercise on the accumulation of neutrophils in muscle in women and men. Eur J Appl Physiol 2000; 81: 47–53PubMedCrossRefGoogle Scholar
  46. 46.
    Rinard J, Clarkson PM, Smith LL, et al. Response of males and females to high-force eccentric exercise. J Sports Sci 2000; 18: 229–36PubMedCrossRefGoogle Scholar
  47. 47.
    Seeley DG, Cauley JA, Grady D, et al. Is postmenopausal estrogen therapy associated with neuromuscular function or falling in elderly women? Study of the Osteoporotic Fractures Research Group. Arch Intern Med 1995; 155: 293–9PubMedCrossRefGoogle Scholar
  48. 48.
    Uusi-Rasi K, Beck TJ, Sievanen H, et al. Associations of hormone replacement therapy with bone structure and physical performance among postmenopausal women. Bone 2003; 32: 704–10PubMedCrossRefGoogle Scholar
  49. 49.
    Ribom EL, Piehl-Aulin K, Ljunghall S, et al. Six months of hormone replacement therapy does not influence muscle strength in postmenopausal women. Maturitas 2002; 42: 225–31PubMedCrossRefGoogle Scholar
  50. 50.
    Kent-Braun JA, Ng AV. Specific strength and voluntary muscle activation in young and elderly women and men. J Appl Physiol 1999; 87: 22–9PubMedGoogle Scholar
  51. 51.
    Armstrong AL, Oborne J, Coupland CA, et al. Effects of hormone replacement therapy on muscle performance and balance in post-menopausal women. Clin Sci (Lond) 1996; 91: 685–90Google Scholar
  52. 52.
    Preisinger E, Alacamlioglu Y, Saradeth T, et al. Forearm bone density and grip strength in women after menopause, with and without estrogen replacement therapy. Maturitas 1995; 21: 57–63PubMedCrossRefGoogle Scholar
  53. 53.
    Harman SM, Blackman MR. The effects of growth hormone and sex steroid on lean body mass, fat mass, muscle strength, cardiovascular endurance and adverse events in healthy elderly women and men. Horm Res 2003; 60: 121–4PubMedCrossRefGoogle Scholar
  54. 54.
    Elliott KJ, Cable NT, Reilly T, et al. Effect of menstrual cycle phase on the concentration of bioavailable 17-beta oestradiol and testosterone and muscle strength. Clin Sci (Lond) 2003; 105: 663–9CrossRefGoogle Scholar
  55. 55.
    Stupka N, Lowther S, Chorneyko K, et al. Gender differences in muscle inflammation after eccentric exercise. J Appl Physiol 2000; 89: 2325–32PubMedGoogle Scholar
  56. 56.
    Clarkson PM, Hubal MJ. Are women less susceptible to exercise-induced muscle damage? Curr Opin Clin Nutr Metab Care 2001; 4: 527–31PubMedCrossRefGoogle Scholar
  57. 57.
    Kerksick C, Taylor L, Harvey A, et al. Gender-related differences in muscle injury, oxidative stress, and apoptosis. Med Sci Sports Exerc 2008; 40: 1772–80PubMedCrossRefGoogle Scholar
  58. 58.
    Feng X, Li GZ, Wang S. Effects of estrogen on gastrocnemius muscle strain injury and regeneration in female rats. Acta Pharmacol Sin 2004; 25: 1489–94PubMedGoogle Scholar
  59. 59.
    Amelink GJ, Bar PR. Exercise-induced muscle protein leakage in the rat: effects of hormonal manipulation. J Neurol Sci 1986; 76: 61–8PubMedCrossRefGoogle Scholar
  60. 60.
    Bar PR, Amelink GJ, Oldenburg B, et al. Prevention of exercise-induced muscle membrane damage by oestradiol. Life Sci 1988; 42: 2677–81PubMedCrossRefGoogle Scholar
  61. 61.
    Amelink GJ, Koot RW, Erich WB, et al. Sex-linked variation in creatine kinase release, and its dependence on oestradiol, can be demonstrated in an in-vitro rat skeletal muscle preparation. Acta Physiol Scand 1990; 138: 115–24PubMedCrossRefGoogle Scholar
  62. 62.
    Persky AM, Green PS, Stubley L, et al. Protective effect of estrogens against oxidative damage to heart and skeletal muscle in vivo and in vitro. Proc Soc Exp Biol Med 2000; 223: 59–66PubMedCrossRefGoogle Scholar
  63. 63.
    Tiidus PM, Holden D, Bombardier E, et al. Estrogen effect on post-exercise skeletal muscle neutrophil infiltration and calpain activity. Can J Physiol Pharmacol 2001; 79: 400–6PubMedCrossRefGoogle Scholar
  64. 64.
    Sewright KA, Hubal MJ, Kearns A, et al. Sex differences in response to maximal eccentric exercise. Med Sci Sports Exerc 2008; 40: 242–51PubMedCrossRefGoogle Scholar
  65. 65.
    Carter A, Dobridge J, Hackney AC. Influence of estrogen on markers of muscle tissue damage following eccentric exercise. Fiziol Cheloveka 2001; 27: 133–7PubMedGoogle Scholar
  66. 66.
    Dieli-Conwright CM, Spektor TM, Rice JC, et al. Hormone replacement therapy attenuates exercise-induced muscle damage in postmenopausal women. J Appl Physiol 2009; 107: 853–8PubMedCrossRefGoogle Scholar
  67. 67.
    McClung JM, Davis JM, Carson JA. Ovarian hormone status and skeletal muscle inflammation during recovery from disuse in rats. Exp Physiol 2007; 92: 219–32PubMedCrossRefGoogle Scholar
  68. 68.
    Stupka N, Tiidus PM. Effects of ovariectomy and estrogen on ischemia-reperfusion injury in hindlimbs of female rats. J Appl Physiol 2001; 91: 1828–35PubMedGoogle Scholar
  69. 69.
    Komulainen J, Koskinen SO, Kalliokoski R, et al. Gender differences in skeletal muscle fibre damage after eccentrically biased downhill running in rats. Acta Physiol Scand 1999; 165: 57–63PubMedCrossRefGoogle Scholar
  70. 70.
    Enns DL, Tiidus PM. Estrogen influences satellite cell activation and proliferation following downhill running in rats. J Appl Physiol 2008; 104: 347–53PubMedCrossRefGoogle Scholar
  71. 71.
    Enns DL, Iqbal S, Tiidus PM. Oestrogen receptors mediate oestrogen-induced increases in post-exercise rat skeletal muscle satellite cells. Acta Physiol (Oxf) 2008; 194: 81–93CrossRefGoogle Scholar
  72. 72.
    St Pierre Schneider B, Correia LA, Cannon JG. Sex differences in leukocyte invasion in injured murine skeletal muscle. Res Nurs Health 1999; 22: 243–50PubMedCrossRefGoogle Scholar
  73. 73.
    Tiidus PM, Deller M, Liu XL. Oestrogen influence on myogenic satellite cells following downhill running in male rats: a preliminary study. Acta Physiol Scand 2005; 184: 67–72PubMedCrossRefGoogle Scholar
  74. 74.
    Tiidus PM, Bombardier E. Oestrogen attenuates post-exercise myeloperoxidase activity in skeletal muscle of male rats. Acta Physiol Scand 1999; 166: 85–90PubMedCrossRefGoogle Scholar
  75. 75.
    Iqbal S, Thomas A, Bunyan K, et al. Progesterone and estrogen influence post-exercise leukocyte infiltration in ovariectomized female rats. Appl Physiol Nutr Met 2008; 33: 1207–12CrossRefGoogle Scholar
  76. 76.
    McClung JM, Davis JM, Wilson MA, et al. Estrogen status and skeletal muscle recovery from disuse atrophy. J Appl Physiol 2006; 100: 2012–23PubMedCrossRefGoogle Scholar
  77. 77.
    Salimena MC, Lagrota-Candido J, Quirico-Santos T. Gender dimorphism influences extracellular matrix expression and regeneration of muscular tissue in mdx dystrophic mice. Histochem Cell Biol 2004; 122: 435–44PubMedCrossRefGoogle Scholar
  78. 78.
    Roth SM, Martel GF, Ivey FM, et al. Skeletal muscle satellite cell characteristics in young and older men and women after heavy resistance strength training. J Gerontol A Biol Sci Med Sci 2001; 56: B240–7CrossRefGoogle Scholar
  79. 79.
    Heldring N, Pike A, Andersson S, et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev 2007; 87: 905–31PubMedCrossRefGoogle Scholar
  80. 80.
    Katzenellenbogen BS, Montano MM, Le Goff P, et al. Antiestrogens: mechanisms and actions in target cells. J Steroid Biochem Mol Biol 1995; 53: 387–93PubMedCrossRefGoogle Scholar
  81. 81.
    Gruber DM, Huber JC. Conjugated estrogens: the natural SERMs. Gynecol Endocrinol 1999; 13 Suppl. 6: 9–12Google Scholar
  82. 82.
    Harada H, Pavlick KP, Hines IN, et al. Selected contribution: effects of gender on reduced-size liver ischemia and reperfusion injury. J Appl Physiol 2001; 91: 2816–22PubMedGoogle Scholar
  83. 83.
    Sribnick EA, Ray SK, Banik NL. Estrogen as a multiactive neuroprotective agent in traumatic injuries. Neurochem Res 2004; 29: 2007–14PubMedCrossRefGoogle Scholar
  84. 84.
    Ashcroft GS, Greenwell-Wild T, Horan MA, et al. Topical estrogen accelerates cutaneous wound healing in aged humans associated with an altered inflammatory response. Am J Pathol 1999; 155: 1137–46PubMedCrossRefGoogle Scholar
  85. 85.
    Milne KJ, Noble EG. Response of the myocardium to exercise: sex-specific regulation of hsp70. Med Sci Sports Exerc 2008; 40: 655–63PubMedCrossRefGoogle Scholar
  86. 86.
    Booth EA, Flint RR, Lucas KL, et al. Estrogen protects the heart from ischemia-reperfusion injury via COX-2- derived PGI2. J Cardiovasc Pharmacol 2008; 52: 228–35PubMedCrossRefGoogle Scholar
  87. 87.
    Versi E. Oestrogen and protection against myocardial ischaemia [letter]. Lancet 1993; 342: 871PubMedCrossRefGoogle Scholar
  88. 88.
    Kolodgie FD, Farb A, Litovsky SH, et al. Myocardial protection of contractile function after global ischemia by physiologic estrogen replacement in the ovariectomized rat. J Mol Cell Cardiol 1997; 29: 2403–14PubMedCrossRefGoogle Scholar
  89. 89.
    Node K, Kitakaze M, Kosaka H, et al. Amelioration of ischemia-and reperfusion-induced myocardial injury by 17beta-estradiol. Circulation 1997; 96: 1953–63PubMedCrossRefGoogle Scholar
  90. 90.
    Delyani JA, Murohara T, Nossuli TO, et al. Protection frommyocardial reperfusion injury by acute administration of 17 beta-estradiol. J Mol Cell Cardiol 1996; 28: 1001–8PubMedCrossRefGoogle Scholar
  91. 91.
    Subbiah MT, Kessel B, Agrawal M, et al. Antioxidant potential of specific estrogens on lipid peroxidation. J Clin Endocrinol Metab 1993; 77: 1095–7PubMedCrossRefGoogle Scholar
  92. 92.
    Sugioka K, Shimosegawa Y, Nakano M. Estrogens as natural antioxidants of membrane phospholipid peroxidation. FEBS Lett 1987; 210: 37–9PubMedCrossRefGoogle Scholar
  93. 93.
    Strehlow K, Rotter S, Wassmann S, et al. Modulation of antioxidant enzyme expression and function by estrogen. Circ Res 2003; 93: 170–7PubMedCrossRefGoogle Scholar
  94. 94.
    Whiting KP, Restall CJ, Brain PF. Steroid hormoneinduced effects on membrane fluidity and their potential roles in non-genomic mechanisms. Life Sci 2000; 67: 743–57PubMedCrossRefGoogle Scholar
  95. 95.
    Patten RD, Pourati I, Aronovitz MJ, et al. 17beta-estradiol reduces cardiomyocyte apoptosis in vivo and in vitro via activation of phospho-inositide-3 kinase/Akt signaling. Circ Res 2004; 95: 692–9PubMedCrossRefGoogle Scholar
  96. 96.
    Kadi F, Karlsson C, Larsson B, et al. The effects of physical activity and estrogen treatment on rat fast and slow skeletal muscles following ovariectomy. J Muscle Res Cell Motil 2002; 23: 335–9PubMedCrossRefGoogle Scholar
  97. 97.
    Dieli-Conwright CM, Spektor TM, Rice JC, et al. Influence of hormone replacement therapy on eccentric exercise induced myogenic gene expression in postmenopausal women. J Appl Physiol 2009; 107: 1381–8PubMedCrossRefGoogle Scholar
  98. 98.
    Onambele-Pearson, GL. HRT affects skeletal muscle contractile characteristics: a definitive answer? J Appl Physiol 2009; 107: 4–5PubMedCrossRefGoogle Scholar
  99. 99.
    Friden J, Sjostrom M, Ekblom B. A morphological study of delayed muscle soreness. Experientia 1981; 37: 506–7PubMedCrossRefGoogle Scholar
  100. 100.
    Jones DA, Newham DJ, Round JM, et al. Experimental human muscle damage:morphological changes in relation to other indices of damage. J Physiol 1986; 375: 435–48PubMedGoogle Scholar
  101. 101.
    Newham DJ, McPhail G, Mills KR, et al. Ultrastructural changes after concentric and eccentric contractions of human muscle. J Neurol Sci 1983; 61: 109–22PubMedCrossRefGoogle Scholar
  102. 102.
    Clarkson PM, Nosaka K, Braun B. Muscle function after exercise-induced muscle damage and rapid adaptation. Med Sci Sports Exerc 1992; 24: 512–20PubMedGoogle Scholar
  103. 103.
    Armstrong RB, Warren GL, Warren JA. Mechanisms of exercise-induced muscle fibre injury. Sports Med 1991; 12: 184–207PubMedCrossRefGoogle Scholar
  104. 104.
    Vierck J, O’Reilly B, Hossner K, et al. Satellite cell regulation following myotrauma caused by resistance exercise. Cell Biol Int 2000; 24: 263–72PubMedCrossRefGoogle Scholar
  105. 105.
    Warren GL, O’farrell L, Rogers KR, et al. CK-MM autoantibodies: prevalence, immune complexes, and effect on CK clearance. Muscle Nerve 2006; 34: 335–46PubMedCrossRefGoogle Scholar
  106. 106.
    Hyatt JP, Clarkson PM. Creatine kinase release and clearance using MM variants following repeated bouts of eccentric exercise.Med Sci Sports Exerc 1998; 30: 1059–65PubMedCrossRefGoogle Scholar
  107. 107.
    Kasperek GJ, Snider RD. The susceptibility to exerciseinduced muscle damage increases as rats grow larger. Experientia 1985; 41: 616–7PubMedCrossRefGoogle Scholar
  108. 108.
    Lightfoot JT. Sex hormones’ regulation of rodent physical activity: a review. Int J Biol Sci 2008; 4: 126–32PubMedCrossRefGoogle Scholar
  109. 109.
    Paroo Z, Dipchand ES, Noble EG. Estrogen attenuates postexercise HSP70 expression in skeletal muscle. Am J Physiol Cell Physiol 2002; 282: C245–51Google Scholar
  110. 110.
    Tiidus PM, Bombardier E, Hidiroglou N, et al. Estrogen administration, postexercise tissue oxidative stress and vitamin C status in male rats. Can J Physiol Pharmacol 1998; 76: 952–60PubMedCrossRefGoogle Scholar
  111. 111.
    Tiidus PM, Bombardier E, Seaman C, et al. Vitamin C and vitamin E status in guinea pig tissues following estrogen administration. Nutr Res 1999; 19: 773–82CrossRefGoogle Scholar
  112. 112.
    Dernbach AR, Sherman WM, Simonsen JC, et al. No evidence of oxidant stress during high-intensity rowing training. J Appl Physiol 1993; 74: 2140–5PubMedCrossRefGoogle Scholar
  113. 113.
    Ayres S, Baer J, Subbiah MT. Exercised-induced increase in lipid peroxidation parameters in amenorrheic female athletes. Fertil Steril 1998; 69: 73–7PubMedCrossRefGoogle Scholar
  114. 114.
    Chung SC, Goldfarb AH, Jamurtas AZ, et al. Effect of exercise during the follicular and luteal phases on indices of oxidative stress in healthy women. Med Sci Sports Exerc 1999; 31: 409–13PubMedCrossRefGoogle Scholar
  115. 115.
    Willoughby DS, Wilborn CD. Estradiol in females may negate skeletal muscle myostatin mRNA expression and serum myostatin mRNA propeptide levels after eccentric muscle contractions. J Sports Sci Med 2006; 5: 672–81Google Scholar
  116. 116.
    Paroo Z, Tiidus PM, Noble EG. Estrogen attenuates HSP 72 expression in acutely exercised male rodents. Eur J Appl Physiol Occup Physiol 1999; 80: 180–4PubMedCrossRefGoogle Scholar
  117. 117.
    Bombardier E, Vigna C, Iqbal S, et al. Effects of ovarian sex hormones and downhill running on fibre-type-specific HSP70 expression in rat soleus. J Appl Physiol 2009; 106: 2009–15PubMedCrossRefGoogle Scholar
  118. 118.
    Melling CW, Thorp DB, Noble EG. Regulation of myocardial heat shock protein 70 gene expression following exercise. J Mol Cell Cardiol 2004; 37: 847–55PubMedCrossRefGoogle Scholar
  119. 119.
    Belcastro AN, Shewchuk LD, Raj DA. Exercise-induced muscle injury: a calpain hypothesis. Mol Cell Biochem 1998; 179: 135–45PubMedCrossRefGoogle Scholar
  120. 120.
    Belcastro AN. Skeletal muscle calcium-activated neutral protease (calpain) with exercise. J Appl Physiol 1993; 74: 1381–6PubMedGoogle Scholar
  121. 121.
    McNulty PH, Jagasia D, Whiting JM, et al. Effect of 6-wk estrogen withdrawal or replacement on myocardial ischemic tolerance in rats. Am J Physiol Heart Circ Physiol 2000; 278: H1030–4Google Scholar
  122. 122.
    Raj DA, Booker TS, Belcastro AN. Striated muscle calcium-stimulated cysteine protease (calpain-like) activity promotes myeloperoxidase activity with exercise. Pflugers Arch 1998; 435: 804–9PubMedCrossRefGoogle Scholar
  123. 123.
    Belcastro AN, Arthur GD, Albisser TA, et al. Heart, liver, and skeletal muscle myeloperoxidase activity during exercise. J Appl Physiol 1996; 80: 1331–5PubMedGoogle Scholar
  124. 124.
    McCord JM. Superoxide radical: controversies, contradictions, and paradoxes. Proc Soc Exp Biol Med 1995; 209: 112–7PubMedGoogle Scholar
  125. 125.
    Clarkson PM, Sayers SP. Etiology of exercise-induced muscle damage. Can J Appl Physiol 1999; 24: 234–48PubMedCrossRefGoogle Scholar
  126. 126.
    Tidball JG. Inflammatory cell response to acute muscle injury. Med Sci Sports Exerc 1995; 27: 1022–32PubMedCrossRefGoogle Scholar
  127. 127.
    Merly F, Lescaudron L, Rouaud T, et al. Macrophages enhance muscle satellite cell proliferation and delay their differentiation. Muscle Nerve 1999; 22: 724–32PubMedCrossRefGoogle Scholar
  128. 128.
    Wise PM, Dubal DB, Wilson ME, et al. Neuroprotective effects of estrogen-new insights into mechanisms of action. Endocrinology 2001; 142: 969–73PubMedCrossRefGoogle Scholar
  129. 129.
    Xing D, Miller A, Novak L, et al. Estradiol and progestins differentially modulate leukocyte infiltration after vascular injury. Circulation 2004; 109: 234–41PubMedCrossRefGoogle Scholar
  130. 130.
    Prorock AJ, Hafezi-Moghadam A, Laubach VE, et al. Vascular protection by estrogen in ischemia-reperfusion injury requires endothelial nitric oxide synthase. Am J Physiol Heart Circ Physiol 2003; 284: H133–40Google Scholar
  131. 131.
    Simoncini T, Fornari L, Mannella P, et al. Novel nontranscriptionalmechanisms for estrogen receptor signaling in the cardiovascular system: interaction of estrogen receptor alpha with phosphatidylinositol 3-OH kinase. Steroids 2002; 67: 935–9PubMedCrossRefGoogle Scholar
  132. 132.
    Reid MB. Role of nitric oxide in skeletal muscle: synthesis, distribution and functional importance. Acta Physiol Scand 1998; 162: 401–9PubMedCrossRefGoogle Scholar
  133. 133.
    Kalbe C, Mau M, Wollenhaupt K, et al. Evidence for estrogen receptor alpha and beta expression in skeletal muscle of pigs. Histochem Cell Biol 2007; 127: 95–107PubMedCrossRefGoogle Scholar
  134. 134.
    Lemoine S, Granier P, Tiffoche C, et al. Effect of endurance training on oestrogen receptor alpha transcripts in rat skeletal muscle. Acta Physiol Scand 2002; 174: 283–9PubMedCrossRefGoogle Scholar
  135. 135.
    Wiik A, Glenmark B, Ekman M, et al. Oestrogen receptor beta is expressed in adult human skeletal muscle both at the mRNA and protein level. Acta Physiol Scand 2003; 179: 381–7PubMedCrossRefGoogle Scholar
  136. 136.
    Sitnick M, Foley AM, Brown M, et al. Ovariectomy prevents the recovery of atrophied gastrocnemius skeletal muscle mass. J Appl Physiol 2006; 100: 286–93PubMedCrossRefGoogle Scholar
  137. 137.
    Wakeling AE, Dukes M, Bowler J. A potent specific pure antiestrogen with clinical potential. Cancer Res 1991; 51: 3867–73PubMedGoogle Scholar
  138. 138.
    Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 2001; 91: 534–51PubMedGoogle Scholar
  139. 139.
    Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 1961; 9: 493–5PubMedCrossRefGoogle Scholar
  140. 140.
    Hurme T, Kalimo H. Activation of myogenic precursor cells after muscle injury. Med Sci Sports Exerc 1992; 24: 197–205PubMedGoogle Scholar
  141. 141.
    Smith HK, Maxwell L, Rodgers CD, et al. Exerciseenhanced satellite cell proliferation and new myonuclear accretion in rat skeletal muscle. J Appl Physiol 2001; 90: 1407–14PubMedCrossRefGoogle Scholar
  142. 142.
    Kadi F, Charifi N, Denis C, et al. The behaviour of satellite cells in response to exercise: what have we learned from human studies? Pflugers Arch 2005; 451: 319–27PubMedCrossRefGoogle Scholar
  143. 143.
    Seale P, Asakura A, Rudnicki MA. The potential of muscle stem cells. Dev Cell 2001; 1: 333–42PubMedCrossRefGoogle Scholar
  144. 144.
    Machida S, Booth FW. Insulin-like growth factor 1 and muscle growth: implication for satellite cell proliferation. Proc Nutr Soc 2004; 63: 337–40PubMedCrossRefGoogle Scholar
  145. 145.
    Kamanga-Sollo E, Pampusch MS, Xi G, et al. IGF-I mRNA levels in bovine satellite cell cultures: effects of fusion and anabolic steroid treatment. J Cell Physiol 2004; 201: 181–9PubMedCrossRefGoogle Scholar
  146. 146.
    Thomas A, Bunyan K, Tiidus PM. Oestrogen receptoralpha activation augments post-exercise myoblast proliferation. Acta Physiol 2010; 198: 81–9CrossRefGoogle Scholar
  147. 147.
    Caulin-Glaser T, Garcia-Cardena G, Sarrel P, et al. 17-Beta-estradiol regulation of human endothelial cell basal nitric oxide release, independent of cytosolic Ca2+ mobilization. Circ Res 1997; 81: 885–92PubMedCrossRefGoogle Scholar
  148. 148.
    Anderson JE. A role for nitric oxide in muscle repair: nitric oxide-mediated activation of muscle satellite cells. Mol Biol Cell 2000; 11: 1859–74PubMedGoogle Scholar
  149. 149.
    Tatsumi R, Anderson JE, Nevoret CJ, et al. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol 1998; 194: 114–28PubMedCrossRefGoogle Scholar
  150. 150.
    Tatsumi R, Hattori A, Ikeuchi Y, et al. Release of hepatocyte growth factor from mechanically stretched skeletal muscle satellite cells and role of pH and nitric oxide. Mol Biol Cell 2002; 13: 2909–18PubMedCrossRefGoogle Scholar
  151. 151.
    Tidball JG, Wehling-Henricks M. Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo. J Physiol 2007; 578: 327–36PubMedCrossRefGoogle Scholar
  152. 152.
    Massimino ML, Rapizzi E, Cantini M, et al. ED2+ macrophages increase selectively myoblast proliferation in muscle cultures. Biochem Biophys Res Commun 1997; 235: 754–9PubMedCrossRefGoogle Scholar
  153. 153.
    Frazier-Jessen MR, Kovacs EJ. Estrogen modulation of JE/monocyte chemoattractant protein-1 mRNA expression in murine macrophages. J Immunol 1995; 154: 1838–45PubMedGoogle Scholar
  154. 154.
    Gulshan S, McCruden AB, Stimson WH. Oestrogen receptors in macrophages. Scand J Immunol 1990; 31: 691–7PubMedCrossRefGoogle Scholar
  155. 155.
    Miller L, Hunt JS. Sex steroid hormones and macrophage function. Life Sci 1996; 59: 1–14PubMedCrossRefGoogle Scholar
  156. 156.
    Calippe B, Douin-Echinard V, Laffargue M, et al. Chronic estradiol administration in vivo promotes the proinflammatory response of macrophages to TLR4 activation: involvement of the phosphatidylinositol 3-kinase pathway. J Immunol 2008; 180: 7980–8PubMedGoogle Scholar
  157. 157.
    Sugiura T, Ito N, Goto K, et al. Estrogen administration attenuates immobilization-induced skeletal muscle atrophy in male rats. J Physiol Sci 2006; 56: 393–9PubMedCrossRefGoogle Scholar
  158. 158.
    Fisher JS, Hasser EM, Brown M. Effects of ovariectomy and hindlimb unloading on skeletal muscle. J Appl Physiol 1998; 85: 1316–21PubMedGoogle Scholar
  159. 159.
    Meeuwsen IB, Samson MM, Verhaar HJ. Evaluation of the applicability of HRT as a preservative of muscle strength in women. Maturitas 2000; 36: 49–61PubMedCrossRefGoogle Scholar
  160. 160.
    Yager JD, Davidson NE. Estrogen carcinogenesis in breast cancer. N Engl J Med 2006; 354: 270–82PubMedCrossRefGoogle Scholar
  161. 161.
    Hulley S, Furberg C, Barrett-Connor E, et al. Noncardiovascular disease outcomes during 6.8 years of hormone therapy: Heart and Estrogen/progestin Replacement Study follow-up (HERS II). JAMA 2002; 288: 58–66PubMedCrossRefGoogle Scholar
  162. 162.
    Stauffer SR, Coletta CJ, Tedesco R, et al. Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. J Med Chem 2000; 43: 4934–47PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2010

Authors and Affiliations

  1. 1.Department of Kinesiology and Physical Education, Faculty of ScienceWilfrid Laurier UniversityWaterlooCanada

Personalised recommendations