The DOI matches its Crossref record; 42 of the 42 references it cites were found in a registry or an index.
Effect of the ovarian hormones on GLUT4 expression and contraction-stimulated glucose uptake
Abstract
This study examined the roles of the female sex steroids, 17β-estradiol (E 2) and progesterone (Prog), on glucose uptake and GLUT4 protein expression. Female Sprague-Dawley rats were either sham operated (C) or ovariectomized and treated with placebo (O), E 2(E), Prog (P), or both hormones at physiological doses (P + E) or the same dose of Prog with a high dose of E 2(P + HiE) via timed-release pellets inserted at the time of surgery, 15 days before metabolic testing. On the morning of day 15, animals received a 300-μCi injection (ip) of 2-deoxy-[14 C]glucose and then either exercised on a motorized treadmill for 30 min at 0.35 m/s or remained sedentary in their cages for the same period. Basal glucose uptake was not different between the treatment groups in either the red or white quadriceps. However, glucose uptake was decreased ( P < 0.05) in O, P, and P + E rats during exercise in the red quadriceps compared with C rats, whereas E and P + HiE treatment restored glucose uptake. Glycogen content in skeletal muscle followed similar trends, with no differences seen in resting animals. Postexercise red quadriceps glycogen levels were higher ( P < 0.05) in the E and P + HiE rats compared with O and P. Treatment of ovariectomized rats with progesterone (P rats) decreased ( P < 0.05) GLUT4 content in the red quadriceps by 21% compared with C rats. These data demonstrate that estrogen-deficient animals have a decreased ability for contraction-stimulated glucose uptake and increased glycogen use during aerobic exercise. However, changes in contraction-stimulated glucose uptake could not be explained by altered transporter protein content, since the absence of E 2 had no effect on GLUT4 protein.
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“functions catabolically to increase amino acid oxidation and decreases muscle protein synthesis [78–81]”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [81]
In the citing paper
“Progesterone also exerts influence over protein metabolism, specifically during the luteal phase, which corresponds with the previously observed increases in protein oxidation at rest and during exercise at this time in the menstrual cycle [81,164].”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [81]
In the citing paper
“In eumenorrheic women, evidence suggests protein catabolism is higher at rest and following aerobic endurance exercise in the luteal phase, when estrogen and progesterone are elevated, compared to the early follicular phase when estrogen and progesterone concentrations are low [81,164,223,224].”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [81]
In the citing paper
“females require more lysine during the luteal phase than the follicular phase [81] with a lower ability to uptake and utilize amino acids for protein synthesis.”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [81]
Citations
Cites
Induction of calcium-dependent nitric oxide synthases by sex hormones.
Weiner, C. P., Lizasoaín, I., Baylis, S. A., Knowles, R. G., Charles, I. G., & Moncada, S. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.11.5212 · Cited by 1,066
Zisman, A., Peroni, O. D., Abel, E. D., Michael, M. D., Mauvais-Jarvis, F., Lowell, B. B., Wojtaszewski, J. F. P., Hirshman, M. F., Virkamaki, A., Goodyear, L. J., et al. (2000) · Nature Medicine · doi:10.1038/78693 · Cited by 743
A comparison of three methods of glycogen measurement in tissues
Passonneau, J. V., & Lauderdale, V. R. (1974) · Analytical Biochemistry · doi:10.1016/0003-2697(74)90248-6 · Cited by 735
Glucose transporter protein content and glucose transport capacity in rat skeletal muscles
Henriksen, E. J., Bourey, R. E., Rodnick, K. J., Koranyi, L. I., Permutt, M. A., & Holloszy, J. O. (1990) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1990.259.4.e593 · Cited by 432
Role of Gestational Hormones in the Induction of Insulin Resistance*
Ryan, E. A., & Enns, L. (1988) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-67-2-341 · Cited by 401
Gonadal hormones and behavioral regulation of body weight
Wade, G. N. (1972) · Physiology & Behavior · doi:10.1016/0031-9384(72)90340-x · Cited by 377
Pedersen, O., Bak, J. F., Andersen, P. H., Lund, S., Moller, D. E., Flier, J. S., & Kahn, B. B. (1990) · Diabetes · doi:10.2337/diab.39.7.865 · Cited by 329
Garvey, W. T., Maianu, L., Huecksteadt, T. P., Birnbaum, M. J., Molina, J. M., & Ciaraldi, T. P. (1991) · Journal of Clinical Investigation · doi:10.1172/jci115068 · Cited by 324
Decreased expression of the insulin-responsive glucose transporter in diabetes and fasting
Berger, J., Biswas, C., Vicario, P. P., Strout, H. V., Saperstein, R., & Pilch, P. F. (1989) · Nature · doi:10.1038/340070a0 · Cited by 299
Garvey, W. T., Maianu, L., Hancock, J. A., Golichowski, A. M., & Baron, A. (1992) · Diabetes · doi:10.2337/diab.41.4.465 · Cited by 289
Flagged first, then by citations
Research works printed but not linked: 2
- Cagnacci A, 1992, J Clin Endocrinol Metab, 74, 1396
- Elkind Hirsch KE, 1993, J Clin Endocrinol Metab, 76, 472
Cited by
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Items 101–142 of 142
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Masson, S. W. C., Dissanayake, W. C., Broome, S. C., Hedges, C. P., Peeters, W., Gram, M., ROWLANDS, D. S., Shepherd, P. R., & Merry, T. L. (2023) · Physiological Reports · doi:10.14814/phy2.15536 · Cited by 5
Oxfeldt, M., FREDERIKSEN, L. K., GUNNARSON, T., & Hansen, M. (2024) · The Journal of Sports Medicine and Physical Fitness · doi:10.23736/s0022-4707.23.15458-2 · Cited by 5
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Sasaki, S., Yasuda, T., Kaneto, H., Kuroda, A., Fujita, Y., Fujisawa, K., Tabuchi, Y., Kasami, R., Matsuoka, T., Matsuhisa, M., et al. (2013) · Internal Medicine · doi:10.2169/internalmedicine.52.8675 · Cited by 5
Siqueira, R., Colombo, R., Conzatti, A., de Castro, A. L., Carraro, C. C., Tavares, Â. M. V., Fernandes, T. R. G., Araújo, A. S. D. R., & Belló‐Klein, A. (2017) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2016-0445 · Cited by 5
Effects of oral contraceptives on glucoregulatory responses to exercise
Jankowski, C. M., Ben‐Ezra, V., Gozansky, W. S., & Sheaffer, S. E. (2004) · Metabolism · doi:10.1016/j.metabol.2003.10.024 · Cited by 5
Exogenous progesterone as a factor for the development of gestational diabetes mellitus
Kapustin, R. V., Arzhanova, O. N., & Bespalova, O. N. (2019) · Russian Bulletin of Obstetrician-Gynecologist · doi:10.17116/rosakush20191901138 · Cited by 5
Acharya, K. D., Nettles, S. A., Lichti, C. F., Warre-Cornish, K. M., Polit, L. D., Srivastava, D. P., Denner, L. A., & Tetel, M. J. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12904 · Cited by 4
Li, J., Zhang, S., Sun, Y., Li, J. H., Feng, Z., Li, H., Zhang, M., Yan, T., Han, J., & Duan, Y. (2024) · EMBO Reports · doi:10.1038/s44319-024-00121-w · Cited by 3
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Sex Hormones and Substrate Metabolism During Endurance Exercise
Isacco, L., & Boisseau, N. (2023) · Springer eBooks · doi:10.1007/978-3-031-21881-1_2 · Cited by 3
Dole, A., Sims, S. T., Gan, H., Gill, N., & Beaven, C. M. (2024) · International Journal of Sports Physiology and Performance · doi:10.1123/ijspp.2024-0068 · Cited by 2
Estrogen deficiency induces pelvic floor muscle atrophy via ERα/GLUT4 pathway
Huang, X., Zhou, M., Wang, Y., Chen, M., Xiao, Y., Li, L., Zhu, F., Chen, L., Tian, X., Wu, S., et al. (2026) · PLoS ONE · doi:10.1371/journal.pone.0349371 · Cited by 2
Köşüş, A., Köşüş, N., Haktankaçmaz, S. A., Ak, D., & Turhan, N. Ö. (2011) · Fetal Diagnosis and Therapy · doi:10.1159/000334054 · Cited by 2
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Hevener, A. L., & Drew, B. G. (2013) · Springer eBooks · doi:10.1007/978-1-4614-8630-5_6 · Cited by 2
Braun, B., Friedlander, A. L., Pollack, M., Butterfield, G. E., Marcus, R., & Hoffman, A. R. (2003) · Metabolism · doi:10.1016/s0026-0495(03)00166-5 · Cited by 2
Muscle Physiology in Healthy Men and Women and Those with Metabolic Myopathies
Devries, M. C., & Tarnopolsky, M. A. (2008) · Physical Medicine and Rehabilitation Clinics of North America · doi:10.1016/j.pmr.2008.10.011 · Cited by 2
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Sugumar, D., Rymbai, E., Vasu, S., & Selvaraj, D. (2023) · Journal of Applied Pharmaceutical Science · doi:10.7324/japs.2023.132467 · Cited by 3
Martin, D., Bargh, M., & Pennington, K. (2024) · European Journal of Applied Physiology · doi:10.1007/s00421-025-05733-1 · Cited by 2
Xue, P., Meth, E. M. S., Noory, S. F. M., Rossi, V., Motoshaleh, D., Pacheco, A. P., Vogel, H., Nôga, D. A., & Benedict, C. (2026) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgag038 · Cited by 1
Nishikawa, M., Ohara, N., Naito, Y., Saito, Y., Amma, C., Tatematsu, K., Baoyindugurong, J., Miyazawa, D., Hashimoto, Y., & Okuyama, H. (2022) · Toxicology Reports · doi:10.1016/j.toxrep.2022.01.011 · Cited by 1
Exercise Metabolism and Menstrual Cycle
Fernández-del-Valle, M. (2023) · Springer eBooks · doi:10.1007/978-3-031-15485-0_7 · Cited by 1
Nutritional Strategies and Sex Hormone Interactions in Women
Rehrer, N. J., McLay-Cooke, R. T., & Sims, S. T. (2023) · Springer eBooks · doi:10.1007/978-3-031-21881-1_12 · Cited by 1
Comparative morphometric study of adipose tissue in ovariectomized mice of different ages
Ivanishchev, V., Ustymenko, A., Kyryk, V. M., & Butenko, G. M. (2020) · Cell and Organ Transplantology · doi:10.22494/cot.v8i1.108 · Cited by 1
Purwanto, B. T., Herawati, L., & Jm, H. (2006) · Folia Medica Indonesiana
EFEITO DO TRATAMENTO COM ESTRADIOL SOBRE O CONTROLE DA PRESSÃO ARTERIAL E O ESTRESSE OXIDATIVO
Carraro, C. C. (2012) · Americanae (AECID Library)
Dresseno, L. P. (2012) · Americanae (AECID Library)
Demeda, C. F. (2012) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Smith, J. L. (2019) · Scholarship@Western (Western University)
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Archer, A. E. (2018) · KU ScholarWorks (The University of Kansas)
Faria, I. D. S. (2022) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/d.5.2022.tde-28042022-085734
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(2022) · MDPI eBooks · doi:10.3390/books978-3-0365-3132-8 · Cited by 2
The effect of menstrual cycle phase on exercise capacity measured by treadmill exercise test
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Lee, S. J. L., van Rens, F. E. C. A., & Peiffer, J. J. (2024) · International Journal of Sports Physiology and Performance · doi:10.1123/ijspp.2023-0143
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Aragão, J. M. D. A., Heimfarth, L., Neres, W. D. S., Félix, F. B., dos Santos, P. R., de Abreu, F. F., Cercato, L. M., Nascimento, A. C. S., Vasconcelos, A. B. S., Soares, R. C., et al. (2024) · Research Square · doi:10.21203/rs.3.rs-5188359/v1
Tamaki, T., Muramatsu, K., & Ikutomo, M. (2025) · Cureus · doi:10.7759/cureus.87793
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Wu, X., Miura, T., Zhou, T., & Ebihara, S. (2026) · JCSM Communications · doi:10.1002/rco2.70029
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Tarnopolsky, M. A. (2004) · Principles of Gender-Specific Medicine · doi:10.1016/b978-012440905-7/50338-8
Metadata
- Authors
- Campbell, S. E., & Febbraio, M. A.
- Affiliations
- The University of Melbourne (AU)
- ORCID
- Febbraio, M. A.
- Venue
- American Journal of Physiology-Endocrinology and Metabolism
- Publisher
- American Physiological Society
- Published
- 2002-05-01
- Volume
- 282
- Issue
- 5
- Pages
- E1139-E1146
- ISSN
- 0193-1849 (ISSN-L)
- 1522-1555
- OpenAlex
- W2112665865
- Semantic Scholar
- 8786fa5da249859947f5bc875ed89357abc9e2b1
- Cited by
- 142
- References
- 42
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 12 · 2023: 10 · 2022: 11 · 2021: 6 · 2020: 8 · 2019: 6 · 2018: 7 · 2017: 8 · 2016: 4 · 2015: 5 · 2014: 4 · 2013: 7 · 2012: 4
- FWCI
- 2.28
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Endocrinology and Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Keywords
- estradiol, progesterone, ovarian hormones, GLUT4, glucose uptake, skeletal muscle, physical activity, ovariectomy, glycogen, female sex hormones, skeletal muscle glucose transport
- MeSH terms
- Animals, Deoxyglucose, Estradiol, Physical Exertion, Female, Glucose, Glycogen, Insulin, Monosaccharide Transport Proteins, Muscle Contraction, Muscle Proteins, Ovariectomy, Progesterone, Rats, Sprague-Dawley, Muscle, Skeletal, Lactic Acid, Glucose Transporter Type 4, Rats
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