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Effect of estradiol on tissue glycogen metabolism and lipid availability in exercised male rats
Abstract
The effect of 17 beta-estradiol 3-benzoate (10 micrograms.0.1 ml sunflower oil-1.100 g body wt-1) on exercise performance, tissue glycogen utilization, and lipid availability was determined in male rats. In experiment 1, estradiol or oil was administered 1 h or 1–6 days before a treadmill run to exhaustion. No differences in body weight between oil- and estradiol-administered animals were observed during the 6-day treatment. Animals receiving estradiol for 3–6 days ran significantly longer and completed more work than oil-administered animals. Significant degradation of red and white vastus muscle, myocardial, and liver glycogen was observed in all animals run to exhaustion. In experiment 2, animals were administered estradiol for 5 days and then run for 2 h. The submaximal run for 2 h significantly reduced tissue glycogen content in red and white vastus muscle, heart, and liver of oil-administered animals. The latter effect was attenuated in both vastus muscles, liver, and myocardial tissues in the estradiol-administered animals. Estradiol administration significantly increased plasma fatty acids and lowered plasma lactate during the submaximal run. These data indicate that when body weight remained constant between groups of male rats, estradiol administration for 3–6 days increased exercise performance. Furthermore, estradiol administration for 5 days resulted in greater lipid availability and less tissue glycogen utilization during submaximal running for 2 h.
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“Animal studies demonstrate that estrogens (and perhaps progesterone) enhance the activity of lipoprotein lipase, increase circulating growth hormone-cortisol levels, and decreases circulating insulin levels [2, 1517].”
From The Effect of Sex Steroid Hormones on Substrate Oxidation during Prolonged Submaximal Exercise in Women. (2000) · cites this paper as [2]
In the citing paper
“Animal studies demonstrate that estrogens (and perhaps progesterone) enhance the activity of lipoprotein lipase, increase circulating growth hormone-cortisol levels, and decreases circulating insulin levels [2, 1517].”
From The Effect of Sex Steroid Hormones on Substrate Oxidation during Prolonged Submaximal Exercise in Women. (2000) · cites this paper as [2]
In the citing paper
“Animal studies demonstrate that estrogens (and perhaps progesterone) enhance the activity of lipoprotein lipase, increase circulating growth hormone-cortisol levels, and decreases circulating insulin levels [2, 1517].”
From The Effect of Sex Steroid Hormones on Substrate Oxidation during Prolonged Submaximal Exercise in Women. (2000) · cites this paper as [2]
In the citing paper
“Rodent studies indicate estrogens increase muscle glycogen storage at rest and reduce glycogen utilization during prolonged submaximal exercise, primarily due to the increased oxidation of free-fatty acids as an energy source, which results in a glycogen sparing effect [2].”
From The Effect of Sex Steroid Hormones on Substrate Oxidation during Prolonged Submaximal Exercise in Women. (2000) · cites this paper as [2]
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BackgroundSex-Based Differences in Skeletal Muscle Kinetics and Fiber-Type Composition
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“Alternatively, the reduced increase in MAP in the women may have been the result of an attenuated sympathetic neural outflow (7, 31), possibly due to estrogen (8, 22, 23, 33), that reduced vasoconstriction, maintained muscle perfusion, and prolonged endurance time.”
BackgroundSubstrate utilization during endurance exercise in men and women after endurance training
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“These observations are similar to animal data demonstrating muscle and hepatic glycogen sparing (23, 24) and increased lipid oxidation (18) in 17b-estradiolsupplemented male or oophorectomized female rats.”
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“Accordingly, treatment of male rats with estradiol (E2) significantly increased lipid availability during submaximal exercise (19).”
BackgroundRegulation of exercise carbohydrate metabolism by estrogen and progesterone in women
D'Eon, T. M., Sharoff, C., Chipkin, S. R., Grow, D., Ruby, B. C., & Braun, B. (2002) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00271.2002 · Cited by 166
“There are consistent data from animal studies that estrogen spares endogenous carbohydrate use in both liver and muscle (23, 31, 32, 37, 38).”
BackgroundCampbell, S. E., Angus, D. J., & Febbraio, M. A. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.281.4.e817 · Cited by 165
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“Animal data suggest that the female sex hormone 17-b-estradiol may mediate these metabolic differences (5, 12, 13, 18).”
BackgroundEffects of the ovarian cycle on sympathetic neural outflow during static exercise
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“Additionally, this glycogen-‘‘sparing’’ effect was associated with an increase in the oxidation of fatty acids (11, 20, 26, 27).”
The Influence of Oral Contraceptives on Athletic Performance in Female Athletes
Burrows, M., & Peters, C. E. (2007) · Sports Medicine · doi:10.2165/00007256-200737070-00001 · Cited by 122
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“Possible mechanisms include differences in nutrient mobilization (7–9), role of the sex steroid hormones (10, 22, 30, 31), or differences in muscle fiber-type and enzymatic profiles (17, 32, 34).”
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Charkoudian, N., & Joyner, M. J. (2004) · Clinics in Chest Medicine · doi:10.1016/j.ccm.2004.01.001 · Cited by 120
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“Adding to this finding, biopsy samples from skeletal muscle, heart, and liver in estradiol treated rats demonstrated reduced glycogen metabolism compared to non-treated male rats (53, 54).”
Dietary carbohydrate, muscle glycogen content, and endurance performance in well-trained women
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“Rodent data suggest that the reproductive hormones may augment glycogen synthesis and resting muscle glycogen contents (10, 22, 37).”
BackgroundGender differences in metabolism; nutrition and supplements
Tarnopolsky, M. A. (2000) · Journal of science and medicine in sport · doi:10.1016/s1440-2440(00)80038-9 · Cited by 105
Sex Differences in Global mRNA Content of Human Skeletal Muscle
Maher, A. C., Fu, M., Isfort, R. J., Varbanov, A. R., Qu, X. A., & Tarnopolsky, M. A. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006335 · Cited by 108
“Similar studies in rats have also found gender differences in lipid metabolism, specifically that female rats have greater lipid oxidation and muscle lipoprotein lipase (LPL) activity, as compared with male rats [12,13].”
BackgroundSex Steroid Metabolism and Menstrual Irregularities in the Exercising Female
Crée, C. D. (1998) · Sports Medicine · doi:10.2165/00007256-199825060-00003 · Cited by 104
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“Indeed, the administration of 17-b-estradiol to male subjects results in significant muscle and liver glycogen sparing during exercise (17, 30).”
BackgroundIsselée, H., Laat, A. D., Bogaerts, K., & Lysens, R. (2001) · European Journal of Pain · doi:10.1053/eujp.2000.0213 · Cited by 92
“…be the result of the local properties of the muscle itself as it has been shown that oestrogen could favour the local metabolism and endothelial wall tissues, suggesting a better tissue compliance (Amelink et al., 1990; Kendrick and Ellis, 1991; Ramamani et al., 1999a; 1999b; Inoue et al., 1999).”
BackgroundMen supplemented with 17β-estradiol have increased β-oxidation capacity in skeletal muscle
Maher, A. C., Akhtar, M., & Tarnopolsky, M. A. (2010) · Physiological Genomics · doi:10.1152/physiolgenomics.00016.2010 · Cited by 87
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“In fact, estrogen supplementation studies in animals and humans have supported the aforementioned findings of higher fat oxidation for women during endurance exercise (7, 13, 23, 24, 30, 31, 45, 46).”
BackgroundGender differences in glucoregulatory responses to intense exercise
Marliss, E. B., Kreisman, S. H., Manzon, A., Halter, J. B., Vranić, M., & Nessim, S. J. (2000) · Journal of Applied Physiology · doi:10.1152/jappl.2000.88.2.457 · Cited by 89
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BackgroundInfluence of oestrogen on muscle glycogen utilization during exercise
Hackney (1999) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.1999.00605.x · Cited by 88
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“An increase in skeletal muscle glycogen utilization is opposite to the conclusions based on direct muscle glycogen measurements in humans (33, 36) and rats (17, 18, 29).”
BackgroundResultInfluentialSex differences in myocardial oxygen and glucose metabolism
Peterson, L. R., Soto, P. F., Herrero, P., Schechtman, K. B., Dence, C. S., & Gropler, R. J. (2007) · Journal of Nuclear Cardiology · doi:10.1016/j.nuclcard.2007.03.001 · Cited by 80
Impact of sex on the heart's metabolic and functional responses to diabetic therapies
Lyons, M. R., Peterson, L. R., McGill, J. B., Herrero, P., Coggan, A. R., Saeed, I. M., Recklein, C. L., Schechtman, K. B., & Gropler, R. J. (2013) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00420.2013 · Cited by 77
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Kushwaha, P., Wolfgang, M. J., & Riddle, R. C. (2017) · Bone · doi:10.1016/j.bone.2017.08.024 · Cited by 79
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“In both liver and skeletal muscle, estrogen decreases glucose oxidation and increases FA oxidation (28,29).”
BackgroundWomen Have Higher Protein Content of β-Oxidation Enzymes in Skeletal Muscle than Men
Maher, A. C., Akhtar, M., Vockley, J., & Tarnopolsky, M. A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012025 · Cited by 72
“Research using rodents [58–60] and humans [35–36,61–62] has suggested that estrogen may play a role in regulating substrate utilization.”
BackgroundFatty acid reesterification but not oxidation is increased by oral contraceptive use in women
Jacobs, K. A., Casazza, G. A., Suh, S., Horning, M. A., & Brooks, G. A. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00685.2004 · Cited by 68
“Those studies have found that, compared with treatments containing placebo or progesterone, estrogen treatment alone stimulates adipose lipolysis (31) and increases plasma FFA availability (41) and Rox during prolonged exercise (32).”
BackgroundThe Effects of Exercise on the Storage and Oxidation of Dietary Fat
Hansen, K. C., Shriver, T. C., & Schoeller, D. A. (2005) · Sports Medicine · doi:10.2165/00007256-200535050-00001 · Cited by 67
Measuring Performance during the Menstrual Cycle: A Model Using Oral Contraceptives
Redman, L. M., & Weatherby, R. P. (2004) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000106181.52102.99 · Cited by 64
Ruby, B. C., Coggan, A. R., & Zderic, T. W. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00296.2001 · Cited by 62
D'Eon, T. M., & Braun, B. (2002) · Journal of Women s Health & Gender-Based Medicine · doi:10.1089/152460902753668439 · Cited by 60
“They speculated, as did others, 19,23,24 that E 2 may increase the oxidation of FFA in exercising muscle, leading to carbohydrate sparing and increased glycogen levels after exercise.”
Gender Differences in Carbohydrate Metabolism and Carbohydrate Loading
Wismann, J., & Willoughby, D. (2006) · Journal of the International Society of Sports Nutrition · doi:10.1186/1550-2783-3-1-28 · Cited by 58
The Physiology of the Highly Trained Female Endurance Runner
Burrows, M., & Bird, S. R. (2000) · Sports Medicine · doi:10.2165/00007256-200030040-00004 · Cited by 57
Effects of ovarian hormones on exercise metabolism
Campbell, S. E., & Febbraio, M. A. (2001) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/00075197-200111000-00009 · Cited by 55
Frandsen, J., Pistoljevic, N., Quesada, J. P., Amaro‐Gahete, F. J., Ritz, C., Larsen, S., Dela, F., & Helge, J. W. (2020) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00774.2019 · Cited by 52
Impact of hormone replacement on myocardial fatty acid metabolism: Potential role of estrogen
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Gurd, B. J., Scheid, J. L., Paterson, D. H., & Kowalchuk, J. M. (2007) · European Journal of Applied Physiology · doi:10.1007/s00421-007-0505-9 · Cited by 31
“Estrogen supplementation has been shown to increase FFA availability in rats (Kendrick and Ellis 1991; Rooney et al. 1993; Ellis et al. 1994) and FFA oxidation in human males (Devries et al.”
Hügel, S., Reincke, M., Strömer, H., Winning, J., Horn, M., Dienesch, C., Mora, P., Schmidt, H. H. H. W., Allolio, B., & Neubauer, S. (1999) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(99)00368-x · Cited by 31
“In an experimental study, estrogen has been shown to inhibit the response to vascular injury in the mouse carotid artery, even without alterations in the systemic lipid profile (47).”
BackgroundGender differences in the endocrine and metabolic responses to hypoxic exercise
Sandoval, D. A., & Matt, K. S. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00526.2001 · Cited by 29
“Administration of estrogen to rats has been shown to spare glycogen during exercise, possibly by increasing lipid availability during exercise (18).”
BackgroundKushwaha, P., Alekos, N. S., Kim, S. P., Li, Z., Wolfgang, M. J., & Riddle, R. C. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.997358 · Cited by 29
“We reasoned that sexual dimorphism in the osteoblast knockout model may be due to an inability to modify fuel selection in female mice because estrogen favors fatty acid metabolism (Hatta et al., 1988; Kendrick and Ellis, 1991; Campbell and Febbraio, 2001).”
BackgroundImaging of myocardial metabolism
Herrero, P., & Gropler, R. J. (2005) · Journal of Nuclear Cardiology · doi:10.1016/j.nuclcard.2005.03.010 · Cited by 27
No effect of short-term testosterone manipulation on exercise substrate metabolism in men
Braun, B., Gerson, L., Hagobian, T., Grow, D., & Chipkin, S. R. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00565.2005 · Cited by 25
“Elevated concentrations of estradiol can increase lipolysis, upregulate enzymes related to -oxidation of fatty acids, and downregulate the use of carbohydrate for energy (9, 11, 14, 25, 33).”
BackgroundMenstrual cycle, exercise and health
Dawson, E. A., & Reilly, T. (2008) · Biological Rhythm Research · doi:10.1080/09291010802067213 · Cited by 25
“Oestrogen supplementation has been shown to increase free fatty acid availability (Kendrick and Ellis 1991; Rooney et al. 1993; Ellis et al. 1994) and maximal activity of enzymes associated with an increased fat metabolism (Campbell and Febbraio 2001, 2002) in rats.”
BackgroundOral contraception and energy intake in women: Impact on substrate oxidation during exercise
Isacco, L., Thivel, D., Meddahi‐Pellé, A., Zouhal, H., Duclos, M., Duché, P., & Boisseau, N. (2012) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h2012-031 · Cited by 24
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“Such treatment also increases lipid availability and cardiac and skeletal muscle lipoprotein lipase activity in exercised male rats (Ellis et al. 1994; Kendrick and Ellis 1991).”
Backgroundvan Breda, E., KEIZER, H. A., Geurten, P., van Kranenburg, G., Menheere, P. P. C. A., Kuipers, H., & Glatz, J. F. C. (1993) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00384355 · Cited by 24
“[20, 21] found noticeably less glycogen depletion after exercise in heart and skeletal muscles of ovariectomized female and intact male rats.”
BackgroundResultInfluentialOral contraceptives augment the exercise pressor reflex during isometric handgrip exercise
MINAHAN, C. L., O'Neill, H., Sikkema, N., Joyce, S., Larsen, B., & Sabapathy, S. (2018) · Physiological Reports · doi:10.14814/phy2.13629 · Cited by 23
“Animal studies demonstrate that higher levels of estradiol are associated with enhanced lipid oxidation during exercise (Hatta et al. 1988; Kendrick and Ellis 1991; Ellis et al. 1994), minimising the interstitial concentrations of metabolic by-products responsible for activating the metaboreflex…”
BackgroundEvaluation of gender differences in physiology: an introduction
Tarnopolsky, M. A., & Saris, W. H. M. (2001) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/00075197-200111000-00004 · Cited by 23
Parent-of-origin effects on voluntary exercise levels and body composition in mice
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Substrate utilization during exercise in postmenopausal women on hormone replacement therapy
Johnson, L., Kraemer, R., Kraemer, G., Haltom, R., Cordill, A., A.Welsch, M., Durand, R., & Castracane, D. (2002) · European Journal of Applied Physiology · doi:10.1007/s00421-002-0686-1 · Cited by 20
“Earlier studies investigating metabolism in rats during rest and exercise have established that estrogen treatment enhanced fatty acid availability and oxidation and the performance of prolonged exercise (Hatta et al. 1988; Kendrick and Ellis 1991; Kendrick et al. 1987; Rooney et al. 1993).”
BackgroundEstrogen administration, postexercise tissue oxidative stress and vitamin C status in male rats
Tiidus, P. M., Bombardier, É., Hidiroglou, N., & Madère, R. (1998) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-76-10-11-952 · Cited by 20
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“Several studies in rats [11-14] and in humans [15] have shown that E2 supplementation influences substrate selection during endurance exercise.”
BackgroundEffect of Exercise Intensity on Fat Utilization in Males and Females
Kang, J., Hoffman, J. R., Ratamess, N. A., Faigenbaum, A. D., Falvo, M., & Wendell, M. (2007) · Research in Sports Medicine · doi:10.1080/15438620701525474 · Cited by 16
Menstrual Cycle Tracking in Sports Research: Challenges, Progress, and Future Directions
Dole, A., Beaven, C. M., & Sims, S. T. (2023) · Physiologia · doi:10.3390/physiologia3040044 · Cited by 19
“These differences are attributed to E2’s possible upregulation of fat breakdown through alterations in hormone and enzyme levels [53].”
BackgroundFemales and males: should nutritional recommendations be gender specific?
Tarnopolsky, M. A. (2003) · Schweizerische Zeitschrift für Sportmedizin und Sporttraumatologie · Cited by 14
Matsuda, T., Takahashi, H., Nakamura, M., Kanno, M., Ogata, H., Ishikawa, A., Yamada, M., Kamemoto, K., & Sakamaki‐Sunaga, M. (2022) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2021-0532 · Cited by 15
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“Since both women and men use glycogen from brain liver and muscle for fast energy during physical stress and during chess playing, mental fatigue occurs earlier in women [125,126], because their body glycogen content is lower if compared to men due to hormonal conditions [127-131] and chess demand for fast energy for…”
BackgroundVirgen‐Ortiz, A., Apolinar-Iribe, A., & Muñı́z, J. (2018) · Europe PMC (PubMed Central) · Cited by 11
Influence du sexe sur le métabolisme à l'exercice et en récupération. Implications nutritionnelles
Boisseau, N. (2004) · Science & Sports · doi:10.1016/j.scispo.2004.05.001 · Cited by 11
“[52] Kendrick ZV, Ellis GS.”
Body Composition and Gender Differences in Performance
Cheuvront, S. N., Moffatt, R. J., & DeRuisseau, K. C. (2002) · CRC Press eBooks · doi:10.1201/9781420041323.ch8 · Cited by 10
van Breda, E., KEIZER, H. A., Kuipers, H., & van Kranenburg, G. (2003) · British Journal of Sports Medicine · doi:10.1136/bjsm.37.4.345 · Cited by 10
INFLUENCE OF ESTROGEN ON MUSCLE PLASTICITY
Tiidus, P. M. (2011) · Redalyc (Universidad Autónoma del Estado de México) · Cited by 9
Sandoval, D. A., Gong, B., & Davis, S. N. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00340.2007 · Cited by 8
“Glycogen content of cardiac muscle after exhaustive exercise was similarly preserved following 1 h or 6 days of estradiol treatment in male rats (1, 20, 42).”
BackgroundEffects of Exercise Training on Fat Oxidation in Untrained Overweight and Obese Females
Manning, K. (2022) · Digital Archive @ GSU · doi:10.57709/2102854 · Cited by 6
Effects of the Oral Contraceptive Pill Cycle on Physiological Responses to Hypoxic Exercise
Sandoval, D. A., & Matt, K. S. (2003) · High Altitude Medicine & Biology · doi:10.1089/152702903321488997 · Cited by 5
“Although, again, we do not know whether a lower lactate response is due to decreased production or increased clearance, estradiol administration in rats does reduce glycogen use and plasma lactate response to exercise (Kendrick and Ellis, 1991), suggesting that reduced production rather than increased clearance is res…”
InfluentialMuscle Physiology in Healthy Men and Women and Those with Metabolic Myopathies
Devries, M. C., & Tarnopolsky, M. A. (2008) · Neurologic Clinics · doi:10.1016/j.ncl.2007.11.010 · Cited by 6
EFFECT OF MENSTRUAL CYCLE PHASE ON THE GLUCOSE-INSULIN RELATIONSHIP AT REST AND DURING EXERCISE.
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Differential Proneness to Obesity in Two Rat Strains with Diverse Immune Responses
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“Having in mind sex differences in adipose tissue distribution and in metabolic inflammation [52], as well as the fact that sex steroids can alter both lipid and carbohydrate metabolism [53,54], only male rats were used in the study.”
Ghanbari–Niaki, A. (2010) · Intern J Endocrinol Metab · Cited by 3
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
Post-exercise muscle glycogen repletion in horses
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PET Imaging of Myocardial Metabolism in Health and Disease
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Substrate Utilization in Female Athletes
Maher, A. C., & Tarnopolsky, M. A. (2013) · CRC Press eBooks · doi:10.1201/b13743-2 · Cited by 1
Myocardial Metabolism in Health and Disease
Gropler, R. J., Peterson, L. R., & Dilsizian, V. (2010) · Wiley eBooks · doi:10.1002/9781444323894.ch5
Neural cardiovascular control during exercise: influence of sex and ovarian hormones
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Effects of the ovarian cycle on sympathetic neural
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Nutritional Implications of Sex and Age Differences in Energy Metabolism
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Metadata
- Authors
- Kendrick, Z. V., & Ellis, G. S.
- Affiliations
- Temple University (US)
- Venue
- Journal of Applied Physiology
- Publisher
- American Physiological Society
- Published
- 1991-11-01
- Volume
- 71
- Issue
- 5
- Pages
- 1694-1699
- ISSN
- 0161-7567 (ISSN-L)
- 8750-7587
- 1522-1601
- OpenAlex
- W2257228634
- Cited by
- 114
- References
- 0
- Citations by year
- 2026: 3 · 2025: 2 · 2023: 3 · 2022: 3 · 2020: 3 · 2019: 4 · 2018: 2 · 2017: 3 · 2015: 4 · 2014: 1 · 2013: 4 · 2012: 4
- FWCI
- 3.45
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Applied Physiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Cardiovascular and exercise physiology
- Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Sports Performance and Training
- Keywords
- estradiol, exercise performance, glycogen metabolism, lipid availability, myocardial glycogen, liver glycogen, plasma fatty acids, plasma lactate, submaximal running, male rats
- MeSH terms
- Animals, Estradiol, Physical Exertion, Fatty Acids, Glycogen, Lipids, Male, Muscles, Myocardium, Physical Endurance, Rats, Inbred Strains, Lipid Metabolism, Rats
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