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Estrogen Regulates Estrogen Receptors and Antioxidant Gene Expression in Mouse Skeletal Muscle
Open accessAbstract
BACKGROUND: Estrogens are associated with the loss of skeletal muscle strength in women with age. Ovarian hormone removal by ovariectomy in mice leads to a loss of muscle strength, which is reversed with 17beta-estradiol replacement. Aging is also associated with an increase in antioxidant stress, and estrogens can improve antioxidant status via their interaction with estrogen receptors (ER) to regulate antioxidant gene expression. The purpose of this study was to determine if ER and antioxidant gene expression in skeletal muscle are responsive to changes in circulating estradiol, and if ERs regulate antioxidant gene expression in this tissue. METHODOLOGY/PRINCIPAL FINDINGS: Adult C57BL/6 mice underwent ovariectomies or sham surgeries to remove circulating estrogens. These mice were implanted with placebo or 17beta-estradiol pellets acutely or chronically. A separate experiment examined mice that received weekly injections of Faslodex to chronically block ERs. Skeletal muscles were analyzed for expression of ER genes and proteins and antioxidant genes. ERalpha was the most abundant, followed by Gper and ERbeta in both soleus and EDL muscles. The loss of estrogens through ovariectomy induced ERalpha gene and protein expression in the soleus, EDL, and TA muscles at both the acute and chronic time points. Gpx3 mRNA was also induced both acutely and chronically in all 3 muscles in mice receiving 17beta-estradiol. When ERs were blocked using Faslodex, Gpx3 mRNA was downregulated in the soleus muscle, but not the EDL and TA muscles. CONCLUSIONS/SIGNIFICANCE: These data suggest that Gpx3 and ERalpha gene expression are sensitive to circulating estrogens in skeletal muscle. ERs may regulate Gpx3 gene expression in the soleus muscle, but skeletal muscle regulation of Gpx3 via ERs is dependent upon muscle type. Further work is needed to determine the indirect effects of estrogen and ERalpha on Gpx3 expression in skeletal muscle, and their importance in the aging process.
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“Skeletal muscle is an estrogen-responsive tissue such that estrogen receptor (ER) mRNA and protein levels change with circulating estrogen levels (7).”
From Sex-Based Differences in Skeletal Muscle Kinetics and Fiber-Type Composition (2015) · cites this paper as [7]
In the citing paper
“OVX leads to an increase in overall body weight and muscle weight (68), and a 70% increase in ERα mRNA with no change in ERβ mRNA (7).”
From Sex-Based Differences in Skeletal Muscle Kinetics and Fiber-Type Composition (2015) · cites this paper as [7]
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Cites
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860
Couse, J. F., Lindzey, J., Grandien, K., Gustafsson, J.-A., & Korach, K. S. (1997) · Endocrinology · doi:10.1210/endo.138.11.5496 · Cited by 978
Carmeci, C., Thompson, D. A., Ring, H. Z., Francke, U., & Weigel, R. J. (1997) · Genomics · doi:10.1006/geno.1997.4972 · Cited by 590
Modulation of Antioxidant Enzyme Expression and Function by Estrogen
Strehlow, K., Rotter, S., Wassmann, S., Adam, O., Grohé, C., Laufs, K., Böhm, M., & Nickenig, G. (2003) · Circulation Research · doi:10.1161/01.res.0000082334.17947.11 · Cited by 483 · cited 1×
“Ovariectomized mice have lower levels of many antioxidant enzymes in the heart, including glutathione peroxidase, catalase, and superoxide dismutase [21,22].”
BackgroundGlutathione peroxidases and redox-regulated transcription factors
Brigelius‐Flohé, R. (2006) · Biological Chemistry · doi:10.1515/bc.2006.166 · Cited by 361
Mechanisms of estrogen signaling and gene expression via GPR30
Prossnitz, E. R., & Maggiolini, M. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.03.026 · Cited by 346
Ogawa, S., Chan, J., Gustafsson, J.-A., Korach, K. S., & Pfaff, D. W. (2003) · Endocrinology · doi:10.1210/en.2002-220519 · Cited by 275
Hormone Therapy and Skeletal Muscle Strength: A Meta-Analysis
Greising, S. M., Baltgalvis, K. A., Lowe, D. A., & Warren, G. L. (2009) · The Journals of Gerontology Series A · doi:10.1093/gerona/glp082 · Cited by 252
Self-citationAge-related muscle dysfunction
Thompson, L. V. (2009) · Experimental Gerontology · doi:10.1016/j.exger.2008.05.003 · Cited by 226
Owman, C., Blay, P., Nilsson, C., & Lolait, S. J. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.1654 · Cited by 224
Pellegrino, M. A., Canepari, M., Rossi, R., D’Antona, G., Reggiani, C., & Bottinelli, R. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.027375 · Cited by 214
Moran, A. L., Nelson, S. A., Landisch, R. M., Warren, G. L., & Lowe, D. A. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01305.2006 · Cited by 208
Self-citationEstrogen Receptor Alpha mRNA in Human Skeletal Muscles
LEMOINE, S., GRANIER, P., TIFFOCHE, C., RANNOU-BEKONO, F., THIEULANT, M.-L., & DELAMARCHE, P. (2003) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000053654.14410.78 · Cited by 201
Expression of Both Oestrogen Receptor Alpha and Beta in Human Skeletal Muscle Tissue
Wiik, A., Ekman, M., Johansson, O., Jansson, E., & Esbjörnsson, M. (2009) · Histochemistry and Cell Biology · doi:10.1007/s00418-008-0512-x · Cited by 190
Expression Pattern of G Protein-Coupled Receptor 30 in LacZ Reporter Mice
Isensee, J., Meoli, L., Zazzu, V., Nabzdyk, C. S., Witt, H., Soewarto, D., Effertz, K., Fuchs, H., Gailus‐Durner, V., Busch, D. H., et al. (2008) · Endocrinology · doi:10.1210/en.2008-1488 · Cited by 189
Lee, Y. S., Kim, A., Choi, J. W., Kim, M., Yasue, S., Son, H. J., Masuzaki, H., Park, K. S., & Kim, J. B. (2008) · Molecular Endocrinology · doi:10.1210/me.2008-0023 · Cited by 184
Ronkainen, P. H. A., Kovanen, V., Alén, M., Pöllänen, E., Palonen, E.-M., Ankarberg-Lindgren, C., Hämäläinen, E., Turpeinen, U., Kujala, U. M., Puolakka, J., et al. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91518.2008 · Cited by 168
Why Females Live Longer Than Males: Control of Longevity by Sex Hormones
Viña, J., Borrás, C., Gambini, J., Sastre, J., & Pallardó, F. V. (2005) · Science of Aging Knowledge Environment · doi:10.1126/sageke.2005.23.pe17 · Cited by 151
Estrogen status and skeletal muscle recovery from disuse atrophy
McClung, J. M., Davis, J. M., Wilson, M. A., Goldsmith, E. C., & Carson, J. A. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01583.2005 · Cited by 151
Glutathione homeostasis in response to exercise training and nutritional supplements
Sen, C. K. (1999) · Molecular and Cellular Biochemistry · doi:10.1023/a:1006910011048 · Cited by 137
Ovariectomy prevents the recovery of atrophied gastrocnemius skeletal muscle mass
Sitnick, M., Foley, A. M., Brown, M., & Spangenburg, E. E. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00869.2005 · Cited by 131
Mohamed, M., & Abdel-Rahman, A. (2000) · European Journal of Endocrinology · doi:10.1530/eje.0.1420307 · Cited by 127
Rogers, N. H., Witczak, C. A., Hirshman, M. F., Goodyear, L. J., & Greenberg, A. S. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.02.154 · Cited by 124
Moran, A. L., Warren, G. L., & Lowe, D. A. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01029.2005 · Cited by 123
Self-citationOestrogen receptor β is expressed in adult human skeletal muscle both at the mRNA and protein level
Wiik, A., Glenmark, B., Ekman, M., Esbjörnsson‐Liljedahl, M., Johansson, O., Bodin, K., Enmark, E., & Jansson, E. (2003) · Acta Physiologica Scandinavica · doi:10.1046/j.0001-6772.2003.01186.x · Cited by 122
Plasma glutathione peroxidase in healthy young adults: influence of gender and physical activity
Rush, J. W. E., & Sandiford, S. (2003) · Clinical Biochemistry · doi:10.1016/s0009-9120(03)00039-0 · Cited by 117
Enns, D. L., Iqbal, S., & Tiidus, P. M. (2008) · Acta Physiologica · doi:10.1111/j.1748-1716.2008.01861.x · Cited by 116
Papaconstantinou, A. D. (2000) · Toxicological Sciences · doi:10.1093/toxsci/56.2.332 · Cited by 113
Estradiol and Tamoxifen Reverse Ovariectomy-Induced Physical Inactivity in Mice
Gorzek, J. F., Hendrickson, K. C., Forstner, J. P., Rixen, J. L., MORAN, A. L., & Lowe, D. A. (2007) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000241649.15006.b8 · Cited by 111
Self-citationPróchniewicz, E., Lowe, D. A., Spakowicz, D. J., Higgins, L., O'Conor, K., Thompson, L. V., Ferrington, D. A., & Thomas, D. D. (2007) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00232.2007 · Cited by 107
Self-citationWade, G. N., Blaustein, J. D., Gray, J., & Meredith, J. M. (1993) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1993.265.6.r1392 · Cited by 105
Vasconsuelo, A., Milanesi, L. M., & Boland, R. (2007) · Journal of Endocrinology · doi:10.1677/joe-07-0250 · Cited by 103
Galluzzo, P., Rastelli, C., Bulzomi, P., Acconcia, F., Pallottini, V., & Marino, M. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00188.2009 · Cited by 79
Estradiol Regulates the Thioredoxin Antioxidant System in the Mouse Uterus
Deroo, B. J., Hewitt, S. C., Peddada, S. D., & Korach, K. S. (2004) · Endocrinology · doi:10.1210/en.2004-0471 · Cited by 77
Expression and localization of estrogen receptor α in the C2C12 murine skeletal muscle cell line
Milanesi, L., de Boland, A. R., & Boland, R. (2008) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21706 · Cited by 64
Lemoine, S., Granier, P., Tiffoche, C., Berthon, P. M., Thieulant, M.-L., Carré, F., & Delamarche, P. (2002) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2002.00992.x · Cited by 61
Oestrogen receptor‐alpha activation augments post‐exercise myoblast proliferation
Thomas, A., Bunyan, K., & Tiidus, P. M. (2009) · Acta Physiologica · doi:10.1111/j.1748-1716.2009.02033.x · Cited by 60
Brown, M., Ning, J., Ferreira, J. A., Bogener, J. L., & Lubahn, D. B. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90696.2008 · Cited by 60
17β-Estradiol signaling in skeletal muscle cells and its relationship to apoptosis
Boland, R., Vasconsuelo, A., Milanesi, L. M., Ronda, A. C., & Deboland, A. R. (2008) · Steroids · doi:10.1016/j.steroids.2007.12.027 · Cited by 59
Steroid Receptors in Two Types of Rabbit Skeletal Muscle*
Saartok, T. (1984) · International Journal of Sports Medicine · doi:10.1055/s-2008-1025894 · Cited by 59
Estradiol effect on anterior crural muscles-tibial bone relationship and susceptibility to injury
Warren, G. L., Lowe, D. A., Inman, C. L., Orr, O. M., Hogan, H. A., Bloomfield, S. A., & Armstrong, R. B. (1996) · Journal of Applied Physiology · doi:10.1152/jappl.1996.80.5.1660 · Cited by 56
Self-citationEffects of ovariectomy and exercise training on muscle GLUT-4 content and glucose metabolism in rats
Hansen, P. A., McCarthy, T. J., Pasia, E. N., Spina, R. J., & Gulve, E. A. (1996) · Journal of Applied Physiology · doi:10.1152/jappl.1996.80.5.1605 · Cited by 56
Wiik, A., Ekman, M., Morgan, G., Johansson, O., Jansson, E., & Esbjörnsson, M. (2005) · Histochemistry and Cell Biology · doi:10.1007/s00418-005-0030-z · Cited by 52
Milanesi, L., Vasconsuelo, A., de Boland, A. R., & Boland, R. (2009) · Steroids · doi:10.1016/j.steroids.2009.01.005 · Cited by 47 · cited 1×
“Both ERa and ERb have been carefully characterized for their localization in C2C12 cells [13,14].”
BackgroundHertrampf, T., Seibel, J., Laudenbach, U., Fritzemeier, K. H., & Diel, P. (2008) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707664 · Cited by 46
Kamanga‐Sollo, E., White, M. E., Chung, K. Y., Johnson, B. J., & Dayton, W. R. (2008) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2008.06.001 · Cited by 44
Dieli-Conwright, C. M., Spektor, T. M., Rice, J. C., & Schroeder, E. T. (2009) · Acta Physiologica · doi:10.1111/j.1748-1716.2009.01997.x · Cited by 39
Lundholm, L., Putnik, M., Otsuki, M., Andersson, S., Ohlsson, C., Gustafsson, J., & Dahlman‐Wright, K. (2007) · Journal of Endocrinology · doi:10.1677/joe-07-0277 · Cited by 37
Rogers, N. H., Perfield, J. W., Strissel, K. J., Obin, M. S., & Greenberg, A. S. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.10.072 · Cited by 30
Muñoz-Castañeda, J., Montilla, P., Muñoz, M., Bujalance, I., Muntané, J., & Túnez, I. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.08.056 · Cited by 27
Gustafsson, J.-Α., Saartok, T., Dahlberg, E., Snochowski, M., Häggmark, T., & Eriksson, E. (1984) · PubMed · Cited by 27
Glutathione homeostasis in response to exercise training and nutritional supplements
Sen, C. K. (1999) · Springer eBooks · doi:10.1007/978-1-4615-5097-6_4 · Cited by 23
Estrogen receptor regulates MyoD gene expression by preventing AP-1-mediated repression
Pedraza‐Alva, G., Zingg, J.-M., Donda, A., & Pérez‐Martínez, L. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.08.153 · Cited by 17
ESTRADIOL EFFECT ON ANTERIOR CRURAL MUSCLES: TIBIAL BONE RELATIONSHIP AND SUSCEPTIBILITY TO INJURY.
Warren, G. L., Lowe, D. A., Inman, C. L., Orr, O. M., Hogan, H. A., Bloomfield, S. A., & Armstrong, R. B. (1995) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199505001-00896 · Cited by 6
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Mauvais-Jarvis, F., Clegg, D. J., & Hevener, A. L. (2013) · Endocrine Reviews · doi:10.1210/er.2012-1055 · Cited by 1,329
Lonardo, A., Nascimbeni, F., Ballestri, S., Fairweather, D., Win, S., Than, T. A., Abdelmalek, M. F., & Suzuki, A. (2019) · Hepatology · doi:10.1002/hep.30626 · Cited by 1,095
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Metadata
- Authors
- Baltgalvis, K. A., Greising, S. M., Warren, G. L., & Lowe, D. A.
- Affiliations
- University of Minnesota (US)
- Georgia State University (US)
- Corresponding author
- Baltgalvis, Kristen A.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2010-04-13
- Volume
- 5
- Issue
- 4
- Pages
- e10164
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2854140
- OpenAlex
- W2083315142
- Cited by
- 192
- References
- 54
- Citations by year
- 2026: 9 · 2025: 13 · 2024: 16 · 2023: 11 · 2022: 18 · 2021: 11 · 2020: 10 · 2019: 15 · 2018: 12 · 2017: 7 · 2016: 15 · 2015: 13 · 2014: 8 · 2013: 12 · 2012: 11
- FWCI
- 6.11
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Archive @ GSU (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Counseling And Psychological Services Dissertations (Georgia State University) (submittedVersion, cc-by)
- Funders
- National Institutes of Health
- National Institute on Aging (K02AG036827, R01AG031743)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology (medical) › Exercise and Physiological Responses
- Keywords
- estrogen, estrogen receptor, estrogen receptor alpha, estrogen receptor beta, G protein-coupled estrogen receptor, antioxidant gene expression, glutathione peroxidase 3, skeletal muscle, ovariectomy, estradiol, fulvestrant, muscle aging, soleus muscle, muscle fiber type, oxidative stress
- MeSH terms
- Aging, Animals, Antioxidants, Estradiol, Estrogens, Female, Gene Expression Regulation, Glutathione Peroxidase, Mice, Inbred C57BL, Receptors, Estrogen, Muscle, Skeletal, Estrogen Receptor alpha, Mice
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