The effect of sex hormones on skeletal muscle adaptation in females

References

• Bann, D., Wu, F. C., Keevil, B., Lashen, H., Adams, J., Hardy, R., … Ong, K. K. (2015). Changes in testosterone related to body composition in late midlife: Findings from the 1946 British birth cohort study. Obesity, 23(7), 1486–1492.
   PubMed Web of Science ®Google Scholar
• Basualto-Alarcon, C., Jorquera, G., Altamirano, F., Jaimovich, E., & Estrada, M. (2013). Testosterone signals through mTOR and androgen receptor to induce muscle hypertrophy. Medicine and Science in Sports and Exercise, 45(9), 1712–1720.
   PubMed Web of Science ®Google Scholar
• Baumgartner, R. N., Waters, D. L., Gallagher, D., Morley, J. E., & Garry, P. J. (1999). Predictors of skeletal muscle mass in elderly men and women. Mechanisms of Ageing and Development, 107(2), 123–136.
   PubMed Web of Science ®Google Scholar
• Bermon, S., & Garnier, P. Y. (2017). Serum androgen levels and their relation to performance in track and field: Mass spectrometry results from 2127 observations in male and female elite athletes. British Journal of Sports Medicine, 51(17), 1309–1314.
   PubMed Web of Science ®Google Scholar
• Bhasin, S., Storer, T. W., Berman, N., Callegari, C., Clevenger, B., Phillips, J., … Casaburi, R. (1996). The effects of supraphysiologic doses of testosterone on muscle size and strength in normal Men. New England Journal of Medicine, 335(1), 1–7.
   PubMed Web of Science ®Google Scholar
• Bhasin, S., Woodhouse, L., Casaburi, R., Singh, A. B., Bhasin, D., Berman, N., … Storer, T. W. (2001). Testosterone dose-response relationships in healthy young men. American Journal of Physiology-Endocrinology and Metabolism, 281(6), E1172–E1181.
   PubMed Web of Science ®Google Scholar
• Burger, H. G. (2002). Androgen production in women. Fertility and Sterility, 77(Suppl 4), 3–5.
   PubMed Web of Science ®Google Scholar
• Carmina, E., Guastella, E., Longo, R. A., Rini, G. B., & Lobo, R. A. (2009). Correlates of increased lean muscle mass in women with polycystic ovary syndrome. European Journal of Endocrinology, 161(4), 583–589.
   PubMed Web of Science ®Google Scholar
• Chin, K.-Y., Soelaiman, I.-N., Naina Mohamed, I., Shahar, S., Teng, N. I. M. F., Suhana Mohd Ramli, E., … Zurinah Wan Ngah, W. (2012). Testosterone is associated with age-related changes in bone health status, muscle strength and body composition in men. The Aging Male, 15(4), 240–245.
   PubMed Web of Science ®Google Scholar
• Collins, B. C., Arpke, R. W., Larson, A. A., Baumann, C. W., Xie, N., Cabelka, C. A., … Lowe, D. A. (2019). Estrogen regulates the satellite cell compartment in females. Cell Reports, 28(2), 368–381.e6.
   PubMed Web of Science ®Google Scholar
• Cui, J., Shen, Y., & Li, R. (2013). Estrogen synthesis and signaling pathways during aging: From periphery to brain. Trends in Molecular Medicine, 19(3), 197–209.
   PubMed Web of Science ®Google Scholar
• Dam, T. V., Dalgaard, L. B., Ringgaard, S., Johansen F.T., Bisgaard Bengtsen, M., Mose, M., … Hansen, M. (2021). Transdermal estrogen therapy improves gains in skeletal muscle mass after 12 weeks of resistance training in early postmenopausal women. Frontiers in Physiology, 11(1691), e596130.
   Google Scholar
• Douchi, T., Yamamoto, S., Oki, T., Maruta, K., Kuwahata, R., & Nagata, Y. (1999). Serum androgen levels and muscle mass in women with polycystic ovary syndrome. Obstetrics and Gynecology, 94(3), 337–340.
   PubMed Web of Science ®Google Scholar
• Ekenros, L., Papoutsi, Z., Friden, C., Dahlman Wright, K., & Linden Hirschberg, A. (2017). Expression of sex steroid hormone receptors in human skeletal muscle during the menstrual cycle. Acta Physiologica, 219(2), 486–493.
   PubMed Web of Science ®Google Scholar
• Gower, B. A., & Nyman, L. (2000). Associations among oral estrogen use, free testosterone concentration, and lean body mass among postmenopausal women. Journal of Clinical Endocrinology and Metabolism, 85(12), 4476–4480.
   PubMed Web of Science ®Google Scholar
• Greising, S. M., Baltgalvis, K. A., Lowe, D. A., & Warren, G. L. (2009). Hormone therapy and skeletal muscle strength: A meta-analysis. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 64A(10), 1071–1081.
   Google Scholar
• Grundberg, E., Ribom, E. L., Brändström, H., Ljunggren, Ö, Mallmin, H., & Kindmark, A. (2005). A TA-repeat polymorphism in the gene for the estrogen receptor alpha does not correlate with muscle strength or body composition in young adult Swedish women. Maturitas, 50(3), 153–160.
   PubMed Web of Science ®Google Scholar
• Häkkinen, K., & Pakarinen, A. (1993). Muscle strength and serum testosterone, cortisol and SHBG concentrations in middle-aged and elderly men and women. Acta Physiologica Scandinavica, 148(2), 199–207.
   PubMedGoogle Scholar
• Häkkinen, K., Pakarinen, A., & Kallinen, M. (1992). Neuromuscular adaptations and serum hormones in women during short-term intensive strength training. European Journal of Applied Physiology and Occupational Physiology, 64(2), 106–111.
   PubMed Web of Science ®Google Scholar
• Häkkinen, K., Pakarinen, A., Kraemer, W. J., Häkkinen, A., Valkeinen, H., & Alen, M. (2001). Selective muscle hypertrophy, changes in EMG and force, and serum hormones during strength training in older women. Journal of Applied Physiology, 91(2), 569–580.
   PubMed Web of Science ®Google Scholar
• Hammes, A., Andreassen, T. K., Spoelgen, R., Raila, J., Hubner, N., Schulz, H., … Willnow, T.E. (2005). Role of endocytosis in cellular uptake of sex steroids. Cell. 122(5), 751–762.
   Google Scholar
• Hansen, M., Skovgaard, D., Reitelseder, S., Holm, L., Langbjerg, H., & Kjaer, M. (2012). Effects of estrogen replacement and lower androgen status on skeletal muscle collagen and myofibrillar protein synthesis in postmenopausal women. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 67(10), 1005–1013.
   PubMed Web of Science ®Google Scholar
• Herbst, K. L., & Bhasin, S. (2004). Testosterone action on skeletal muscle. Current Opinion in Clinical Nutrition and Metabolic Care, 7(3), 271–277.
   PubMed Web of Science ®Google Scholar
• Hirschberg, A. L., Elings Knutsson, J., Helge, T., Godhe, M., Ekblom, M., Bermon, S., & Ekblom, B. (2020). Effects of moderately increased testosterone concentration on physical performance in young women: A double blind, randomised, placebo controlled study. British Journal of Sports Medicine, 54(10), 599–604.
   PubMed Web of Science ®Google Scholar
• Ho, C. K., Stoddart, M., Walton, M., Anderson, R. A., & Beckett, G. J. (2006). Calculated free testosterone in men: Comparison of four equations and with free androgen index. Annals of Clinical Biochemistry, 43(Pt 5), 389–397.
   PubMedGoogle Scholar
• Huang, G., Basaria, S., Travison, T. G., Ho, M. H., Davda, M., Mazer, N. A., … Bhasin, S. (2014). Testosterone dose-response relationships in hysterectomized women with or without oophorectomy: Effects on sexual function, body composition, muscle performance and physical function in a randomized trial. Menopause (New York, N. Y.), 21(6), 612–623.
   PubMed Web of Science ®Google Scholar
• Hwang, A. C., Liu, L. K., Lee, W. J., Chen, L.-Y., Lin, M.-H., Peng, L.-N., … Chen, L.-K. (2013). Association of androgen with skeletal muscle mass and muscle function among men and women aged 50 years and older in Taiwan: Results from the I-Lan longitudinal aging study. Rejuvenation Research, 16(6), 453–459.
   PubMed Web of Science ®Google Scholar
• Javed, A. A., Mayhew, A. J., Shea, A. K., & Raina, P. (2019). Association between hormone therapy and muscle mass in postmenopausal women. JAMA Network Open, 2(8), e1910154.
   Web of Science ®Google Scholar
• Kahlert, S., Grohé, C., Karas, R. H., Löbbert, K., Neyses, L., & Vetter, H. (1997). Effects of estrogen on skeletal myoblast growth. Biochemical and Biophysical Research Communications, 232(2), 373–378.
   PubMed Web of Science ®Google Scholar
• Kirchengast, S., & Huber, J. (2001). Body composition characteristics and body fat distribution in lean women with polycystic ovary syndrome. Human Reproduction, 16(6), 1255–1260.
   PubMed Web of Science ®Google Scholar
• Knowles, O. E., Aisbett, B., Main, L. C., Drinkwater, E. J., Orellana, L., & Lamon, S. (2019). Resistance training and skeletal muscle protein metabolism in eumenorrheic females: Implications for researchers and practitioners. Sports Medicine. 49(11), 1637–1650.
   PubMed Web of Science ®Google Scholar
• Kogure, G. S., Silva, R. C., Picchi Ramos, F. K., Miranda-Furtado, C. L., da Silva Lara, L. A., Ferriani, R. A., & dos Reis, R. M. (2015). Women with polycystic ovary syndrome have greater muscle strength irrespective of body composition. Gynecological Endocrinology, 31(3), 237–242.
   PubMed Web of Science ®Google Scholar
• Kong, S. H., Kim, J. H., Lee, J. H., Hong, A. R., Shin, C. S., & Cho, N. H. (2019). Dehydroepiandrosterone sulfate and free testosterone but not estradiol are related to muscle strength and bone microarchitecture in older adults. Calcified Tissue International, 105(3), 285–293.
   PubMed Web of Science ®Google Scholar
• Korenman, S. G., Sherman, B. M., & Korenman, J. C. (1978). Reproductive hormone function: The perimenopausal period and beyond. Clinics in Endocrinology and Metabolism, 7(3), 625–643.
   PubMedGoogle Scholar
• MacLean, H. E., Chiu, W. S. M., Notini, A. J., Axell, A.-M., Davey, R. A., McManus, J. F., … Zajac, J. D. (2008). Impaired skeletal muscle development and function in male, but not female, genomic androgen receptor knockout mice. The FASEB Journal, 22(8), 2676–2689.
   PubMed Web of Science ®Google Scholar
• Moran, A. L., Nelson, S. A., Landisch, R. M., Warren, G. L., & Lowe, D. A. (2007). Estradiol replacement reverses ovariectomy-induced muscle contractile and myosin dysfunction in mature female mice. Journal of Applied Physiology, 102(4), 1387–1393.
   PubMed Web of Science ®Google Scholar
• Nilsson, E., Benrick, A., Kokosar, M., Krook, A., Lindgren, E., Källman, T., … Stener-Victorin, E. (2018). Transcriptional and epigenetic changes influencing skeletal muscle Metabolism in women With polycystic ovary syndrome. The Journal of Clinical Endocrinology & Metabolism, 103(12), 4465–4477.
   PubMed Web of Science ®Google Scholar
• Oliva, M., Munoz-Aguirre, M., Kim-Hellmuth, S., Gewirtz, A.D.H., Cotter, D.J., Parsana, P., … Stranger, B.E. (2020). The impact of sex on gene expression across human tissues. Science, 369(6509), eaba3066.
   Web of Science ®Google Scholar
• Park, Y. M., Keller, A. C., Runchey, S. S., Miller, B. F., Kohrt, W. M., Van Pelt, R. E., … Moreau, K. L. (2019). Acute estradiol treatment reduces skeletal muscle protein breakdown markers in early- but not late-postmenopausal women. Steroids, 146, 43–49.
   PubMed Web of Science ®Google Scholar
• Peters, C., & Burrows, M. (2006). Androgenicity of the progestin in oral contraceptives does not affect maximal leg strength. Contraception, 74(6), 487–491.
   PubMed Web of Science ®Google Scholar
• Pielke, R., Tucker, R., & Boye, E. (2019). Scientific integrity and the IAAF testosterone regulations. The International Sports Law Journal, 19(1), 18–26.
   Web of Science ®Google Scholar
• Pöllänen, E., Kangas, R., Horttanainen, M., Niskala, P., Kaprio, J., Butler-Browne, G., … Kovanen, V. (2015). Intramuscular sex steroid hormones are associated with skeletal muscle strength and power in women with different hormonal status. Aging Cell, 14(2), 236–248.
   PubMed Web of Science ®Google Scholar
• Pöllänen, E., Ronkainen, P. H., Suominen, H., Takala, T., Koskinen, S., Puolakka, J., … Kovanen, V. (2007). Muscular transcriptome in postmenopausal women with or without hormone replacement. Rejuvenation Research, 10(4), 485–500E.
   PubMed Web of Science ®Google Scholar
• Pöllänen, E., Sipilä, S., Alen, M., Ronkainen, P. H. A., Ankarberg-Lindgren, C., Puolakka, J., … Kovanen, V. (2011). Differential influence of peripheral and systemic sex steroids on skeletal muscle quality in pre- and postmenopausal women. Aging Cell, 10(4), 650–660.
   PubMed Web of Science ®Google Scholar
• Rariy, C. M., Ratcliffe, S. J., Weinstein, R., Bhasin, S., Blackman, M. R., Cauley, J. A., … Cappola, A. R. (2011). Higher serum free testosterone concentration in older women is associated with greater bone mineral density, lean body mass, and total fat mass: The cardiovascular health study. The Journal of Clinical Endocrinology & Metabolism, 96(4), 989–996.
   PubMed Web of Science ®Google Scholar
• Rolland, Y. M., Perry, H. M., Patrick, P., Banks, W. A., & Morley, J. E. (2007). Loss of appendicular muscle mass and loss of muscle strength in young postmenopausal women. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 62(3), 330–335.
   PubMed Web of Science ®Google Scholar
• Rosner, W., Hryb, D. J., Kahn, S. M., Nakhla, A. M., & Romas, N. A. (2010). Interactions of sex hormone-binding globulin with target cells. Molecular and Cellular Endocrinology, 316(1), 79–85.
   PubMed Web of Science ®Google Scholar
• Roy, T. A., Blackman, M. R., Harman, S. M., Tobin, J. D., Schrager, M., & Metter, E. J. (2002). Interrelationships of serum testosterone and free testosterone index with FFM and strength in aging men. American Journal of Physiology-Endocrinology and Metabolism, 283(2), E284–E294.
   PubMed Web of Science ®Google Scholar
• Sallinen, J., Pakarinen, A., Fogelholm, M., Sillanpää, E., Alen, M., Volek, J. S., … Häkkinen, K. (2006). Serum basal hormone concentrations and muscle mass in aging women: Effects of strength training and diet. International Journal of Sport Nutrition and Exercise Metabolism, 16(3), 316–331.
   PubMed Web of Science ®Google Scholar
• Schaap, L. A., Pluijm, S. M., Smit, J. H., van Schoor, N. M., Visser, M., Gooren, L. J. G., & Lips, P. (2005). The association of sex hormone levels with poor mobility, low muscle strength and incidence of falls among older men and women. Clinical Endocrinology, 63(2), 152–160.
   PubMed Web of Science ®Google Scholar
• Sipilä, S., Heikkinen, E., Cheng, S., Suominen, H., Saari, P., Kovanen, V., … Rantanen, T. (2006). Endogenous hormones, muscle strength, and risk of fall-related fractures in older women. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 61(1), 92–96.
   PubMed Web of Science ®Google Scholar
• Smith, G. I., Yoshino, J., Reeds, D. N., Bradley, D., Burrows, R. E., Heisey, H. D., … Mittendorfer, B. (2014). Testosterone and progesterone, but not estradiol, stimulate muscle protein synthesis in postmenopausal women. The Journal of Clinical Endocrinology & Metabolism, 99(1), 256–265.
   PubMed Web of Science ®Google Scholar
• Södergard, R., Bäckström, T., Shanbhag, V., & Carstensen, H. (1982). Calculation of free and bound fractions of testosterone and estradiol-17β to human plasma proteins at body temperature. Journal of Steroid Biochemistry, 16(6), 801–810.
   PubMedGoogle Scholar
• Stricker, R., Eberhart, R., Chevailler, M. C., Quinn, F. A., Bischof, P., & Stricker, R. (2006). Establishment of detailed reference values for luteinizing hormone, follicle stimulating hormone, estradiol, and progesterone during different phases of the menstrual cycle on the Abbott ARCHITECT analyzer. Clinical Chemistry and Laboratory Medicine (CCLM), 44(7), 883–887.
   Google Scholar
• Suuronen, J., Sjöblom, S., Tuppurainen, M., Honkanen, R., Rikkonen, T., Kröger, H., & Sirola, J. (2019). Effects of ethinyl estradiol-containing oral contraception and other factors on body composition and muscle strength among young healthy females in Finland—A cross-sectional study. European Journal of Obstetrics & Gynecology and Reproductive Biology, 232, 75–81.
   PubMed Web of Science ®Google Scholar
• Taraborrelli, S. (2015). Physiology, production and action of progesterone. Acta obstetricia et gynecologica Scandinavica, 94(Suppl 161), 8–16.
   PubMedGoogle Scholar
• Tchernof, A., Brochu, D., Maltais-Payette, I., Mansour, M. F., Marchand, G.B., Carreau, A-M., Kapeluto, J. (2018). Androgens and the regulation of adiposity and body fat distribution in humans. Comprehensive Physiology, 8(4), 1253–1290.
   Web of Science ®Google Scholar
• Thompson, B., Almarjawi, A., Sculley, D., & de Jonge X, J. (2020). The effect of the menstrual cycle and oral contraceptives on Acute responses and chronic adaptations to resistance training: A systematic review of the literature. Sports Medicine, 50(1), 171–185.
   PubMed Web of Science ®Google Scholar
• van den Beld, A. W., de Jong, F. H., Grobbee, D. E., Pols, H. A. P., & Lamberts, S. W. J. (2000). Measures of bioavailable serum testosterone and estradiol and their relationships with muscle strength, bone density, and body composition in elderly men*. The Journal of Clinical Endocrinology & Metabolism, 85(9), 3276–3282.
   PubMed Web of Science ®Google Scholar
• van Geel, T. A., Geusens, P. P., Winkens, B., Sels, J. P., & Dinant, G. J. (2009). Measures of bioavailable serum testosterone and estradiol and their relationships with muscle mass, muscle strength and bone mineral density in postmenopausal women: A cross-sectional study. European Journal of Endocrinology, 160(4), 681–687.
   PubMed Web of Science ®Google Scholar
• Widmaier, E. P., Raff, H., & Strang, K. T. (2014). Vander’s human physiology (13th ed.). McGraw-Hill. New York, USA.
   Google Scholar
• Yee, M. L., Hau, R., Taylor, A., Guerra, M., Guerra, P., Darzins, P., & Gilfillan, C. (2020). Sarcopenia in women with hip fracture: A comparison of hormonal biomarkers and their relationship to skeletal muscle mass and function. Osteoporosis and Sarcopenia, 6(3), 139–145.
   PubMedGoogle Scholar