Exercise-induced muscle protein leakage in the rat: Effects of hormonal manipulation

doi:10.1016/0022-510X(86)90142-5

Journal of the Neurological Sciences

Volume 76, Issue 1, November 1986, Pages 61-68

https://doi.org/10.1016/0022-510X(86)90142-5 Get rights and content

Abstract

Differences in exercise-induced muscle damage between males and females were studied in an animal model by measuring the serum activities of specific muscle enzymes (creatine kinase and aspartate aminotransferase). It was found that rats showed muscle damage, comparable to that observed in humans after long-term exercise: males were much more affected than females. For example, the CK activity in male rats immediately after exercise was 335% of the resting value, but remained unchanged in females. To test the hypothesis that oestrogens may protect the female muscle membrane, female rats were ovariectomized at different stages of sexual maturity and exercised. A clear effect of this hormonal manipulation was observed: operated animals showed post-exercise CK elevations, depending of the age at the time of ovariectomy. Rats, ovariectomized before reaching sexual maturity, showed more damage than those ovariectomized after reaching sexual maturity.

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Muscle protein synthesis is driven by a damage/repair process that occurs after 1–2 weeks of resistance training [39]. Estrogen presence in skeletal muscle has been associated with damage/repair process in this tissue [40,41] by decreasing neutrophil invasion into damaged muscle fibers [40]. In fact, 17β-estradiol and the estrogen receptors beta (ERβ) are associated with an attenuation of protein degradation in skeletal muscle [42–45] promoting regenerative and anti-apoptotic effects in this tissue through a mechanism that involves satellite cells [46].
This study aimed to examine the evidence regarding the regulatory role of exercise in circulating levels of sex hormones in overweight and obese postmenopausal women.
Exercise has shown to be an effective non-pharmacological tool in obesity and breast cancer prevention. Sex hormones have been proposed as a potential link by which exercise may modulate obesity and breast cancer after menopause, however, the response of sex hormones as a metabolic pathway responsible for the connection between both pathologies are not entirely understood. An extensive search was performed using PubMed, Medline, Scopus and SPORTDiscus databases for the period from inception of each database to May 2018. A total of 778 studies were found in the search. Of these, 9 met the inclusion criteria and were further analyzed. Despite the different exercise protocols performed, most studies found a decrease in circulating levels of estrone and estradiol, and an increase in sex hormone-binding globulin (SHBG). However, when the effect of exercise on these sex hormones was compared to an unexercised control group, conflicting results were obtained. A reduction in body mass was reported in those studies in which exercise caused a significant effect on estrone, estradiol and SHBG compared to a control group.
These results suggest that exercise-induced weight loss and the type of exercise performed may to be critical factors in the modification of the circulation expression of some sex hormones. Further studies are required to elucidate the most effective exercise dose to restore sex hormones homeostasis as potential obesity-breast cancer nexus in the postmenopausal woman.
L’objectif de cette étude était de faire le point de la littérature scientifique sur l’influence de l’exercice sur les taux circulants d’hormones sexuelles chez les femmes ménopausées en surcharge pondérale.
L’exercice s’est avéré être un outil non pharmacologique efficace pour la prévention de l’obésité et le cancer du sein. Il a été suggéré que les hormones sexuelles étaient impliquées dans ce mécanisme, mais ces interactions entre obésité, activité physique et cancer restent incomplètement comprises. Une recherche approfondie a été effectuée en utilisant les bases de données PubMed, Medline, Scopus et SPORTDiscus pour la période allant de la création de chaque base de données à mai 2018. Un total de 778 études ont été trouvées lors de cette recherche. Parmi ceux-ci, 9 répondaient aux critères d’inclusion et ont été analysées en plus en détail. Malgré les différents protocoles d’exercice, la plupart des études ont montré une diminution des taux circulants d’estrone et d’estradiol ainsi qu’une augmentation de la SHBG (protéine porteuse des hormones sexuelles). Cependant, lorsque l’effet de l’exercice sur ces hormones sexuelles a été comparé à un groupe contrôle, des résultats contradictoires ont été obtenus. Une réduction de la masse corporelle a été rapportée dans les études où l’exercice a eu un effet significatif sur l’estrone, l’estradiol et la SHBG en comparaison à un groupe contrôle.
Les résultats suggèrent que la perte de poids induite par l’exercice et le type d’exercice effectué peuvent être des facteurs critiques dans la modification de l’expression des hormones sexuelles circulantes. D’autres études sont nécessaires pour élucider la dose d’exercice qui serait la plus efficace pour restaurer l’homéostasie des hormones sexuelles en tant que lien potentiel entre l’obésité et le cancer du sein chez la femme ménopausée.
Functions of estrogen and estrogen receptor signaling on skeletal muscle
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Satellite cells are skeletal muscle stem cells required for the growth, maintenance and regeneration of skeletal muscle [102–104]. It has been known that satellite cells show gender differences in the response to myofiber injury and hypertrophic signals [105–109], suggesting that sex steroids can regulate satellite cells. Proliferation of satellite cells is stimulated by cytokines and growth factors produced by macrophages during the inflammation after muscle-damaging exercise [55] or ischemia/reperfusion injury [110].
Activity of estrogen, a sex steroid hormone, is not only limited to the reproductive organs but also involves other organs and tissues, including skeletal muscle. In postmenopausal women, estrogen decline causes endocrine and metabolic dysfunction, leading to a predisposition to osteoporosis, metabolic syndrome, and decreased muscle mass and strength. The decline in skeletal muscle mass often associates with sarcopenia, a popular condition observed in fragile elder people. In addition, varying estrogen levels associated with the menstrual phases may modulate exercise performance in women. Estrogen is thus considered to play a crucial role in skeletal muscle homeostasis and exercise capacity, although its precise mechanisms remain to be elucidated. In this article, we review the role of estrogen in the skeletal muscle, outlining the proposed molecular mechanisms. We especially focus on the current understanding of estrogen actions on mitochondria metabolism in skeletal muscle.
Sexual Dimorphism in Stem Cell–Based Therapies for the Musculoskeletal System
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Citation Excerpt :
For example, Amelink et al found lower levels of circulating CK in male animals when estrogen was administered following exercise. Furthermore, the investigators also found that pre-exercise estrogen therapy may help prevent the accumulation of excessive muscle damage in ovariectomized female rats.23 Current studies are being conducted that explore the potential protective role of estrogen and its ability to minimize inflammation and leukocyte infiltration at the site of muscle injury.
Musculoskeletal health is one of the areas of medicine in which the differences between males and females are most striking. Differences in disease prevalence, pain sensation, drug handling, and healing responses between individuals have known biologic bases; however, the impact of sex on these biologic processes is unclear. In skeletal muscle tissues, stem cells and progenitor cells are known to persist throughout life and contribute to the ongoing process of repair and regeneration. However, currently, there is a paucity of literature that describes the sex-related differences in satellite cells and other muscle stem cell populations that may have an influence on future stem cell applications. Therefore, an in-depth understanding of the sex-related differences in the biology of skeletal muscle and its resident stem cell populations would greatly enhance our ability to devise new individualized treatment strategies for tissue regeneration in many pathologic and non-pathologic conditions involving the musculoskeletal system.
17β-Estradiol and testosterone in sarcopenia: Role of satellite cells
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The understanding of the influence of estrogens and androgens on satellite cells has significantly grown over the last decade. Of relevance, it has been shown that there are gender differences in those responses (Amelink and Bar, 1986; Amelink et al., 1990; Bar et al., 1995; Bar and Amelink, 1997; Reisz-Porszasz et al., 2003), suggesting that satellite cells could be regulated by sex steroids. In fact, several muscle genes detailed in Table 1 are affected by these hormones; e.g., Pax-7, MyoD, myogenin, among others (Braga et al., 2012; Cleveland and Weber, 2015; McFarland et al., 2013; Rana et al., 2014).
The loss of muscle mass and strength with aging, referred to as sarcopenia, is a prevalent condition among the elderly. Although the molecular mechanisms underlying sarcopenia are unclear, evidence suggests that an age-related acceleration of myocyte loss via apoptosis might be responsible for muscle perfomance decline. Interestingly, sarcopenia has been associated to a deficit of sex hormones which decrease upon aging. The skeletal muscle ability to repair and regenerate itself would not be possible without satellite cells, a subpopulation of cells that remain quiescent throughout life. They are activated in response to stress, enabling them to guide skeletal muscle regeneration. Thus, these cells could be a key factor to overcome sarcopenia. Of importance, satellite cells are 17β-estradiol (E2) and testosterone (T) targets. In this review, we summarize potential mechanisms through which these hormones regulate satellite cells activation during skeletal muscle regeneration in the elderly. The advance in its understanding will help to the development of potential therapeutic agents to alleviate and treat sarcopenia and other related myophaties.
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Exercise-induced muscle protein leakage in the rat: Effects of hormonal manipulation

Abstract

Clin. Chim. Acta

Physiol. Behav.

Clin. Chim. Acta

Effects of exercise on serum enzyme values and tissues of rats

Amer. J. Physiol.

Eccentric excercise-induced injury to rat skeletal muscle

J. Appl. Physiol. Resp. Environm. Exc. Physiol.

Muscle protein leakage after strenous excercise — Sex and chronological differences

Neurosci. Lett.

Changes in serum creatine kinase and hexose phosphate isomerase activity with excercise duration

Europ. J. Appl. Physiol.

Körperbelastung und Serumenzyme

D. Z. Sportmed.

Physiological and metabolic responses of female athletes during laboratory and field excercise

Medicine Sport

Effects of excercise on the serum concentrations of FSH, LH, progesteron and estradiol

Europ. J. Appl. Physiol.

Cellular Uptake of Steroids

Diethylstilbestrol effects on serum enzymes and isozymes in muscular dystrophy

Arch. Neurol. (Chic.)