The DOI matches its Crossref record; 46 of the 46 references it cites were found in a registry or an index.
Testosterone Stimulates Intracellular Calcium Release and Mitogen-Activated Protein Kinases Via a G Protein-Coupled Receptor in Skeletal Muscle Cells
Open accessAbstract
Involvement of intracellular Ca(2+) and ERK1/2 phosphorylation in the fast nongenomic effects of androgens in myotubes was investigated. Testosterone or nandrolone produced fast (<1 min) and transient increases in intracellular Ca(2+) with an oscillatory pattern. Calcium signals were slightly reduced in Ca(2+)-free medium, but lack of oscillations was evident. Signals were blocked by U-73122 and xestospongin B, inhibitors of inositol 1,4,5-trisphosphate (IP(3)) pathway. Furthermore, IP(3) increased transiently 2- to 3-fold 45 sec after hormone addition. Cyproterone neither affected the fast Ca(2+) signal nor the increase in IP(3). Calcium increases could also be induced by the impermeant testosterone conjugated to BSA, and the effect of testosterone was abolished in cells incubated with guanosine 5'-O-(2-thiodiphosphate) or pertussis toxin. Stimulation of myotubes with testosterone, nandrolone, or testosterone conjugated to BSA increased immunodetectable phosphorylation of ERK1/2 within 5 min, and this effect was not inhibited by cyproterone. Phosphorylation was blocked by the use of 1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid-acetoxymethylester, U-73122, and xestospongin B as well as by dominant negative Ras, MAPK kinase (MEK), or the MEK inhibitor PD-98059. In addition, guanosine 5'-O-(2-thiodiphosphate) or pertussis toxin blocked ERK1/2 phosphorylation. These results are consistent with a fast effect of testosterone, involving a G protein-linked receptor at the plasma membrane, IP(3)-mediated Ca(2+) signal, and the Ras/MEK/ERK pathway in muscle cells.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Mammalian steroid hormones increase Ca2+ influx in a variety of cell types, including cardiac myocytes and skeletal muscle182,183.”
From The Phytochemical, Biological, and Medicinal Attributes of Phytoecdysteroids: An Updated Review (2021) · cites this paper as [182]
Citations
Cites
Seger, R., & Krebs, E. G. (1995) · The FASEB Journal · doi:10.1096/fasebj.9.9.7601337 · Cited by 3,631
Calcium oscillations increase the efficiency and specificity of gene expression
Dolmetsch, R. E., Xu, K., & Lewis, R. S. (1998) · Nature · doi:10.1038/31960 · Cited by 1,896
Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores
Minta, A., Kao, J. P. Y., & Tsien, R. Y. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)83165-9 · Cited by 1,621
Organization and regulation of mitogen-activated protein kinase signaling pathways
Garrington, T. P., & Johnson, G. L. (1999) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(99)80028-3 · Cited by 1,268
Signal transduction via the MAP kinases: proceed at your own RSK.
Blenis, J. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.13.5889 · Cited by 1,233
Biological Actions of Androgens
MOORADIAN, A. D., MORLEY, J. E., & KORENMAN, S. G. (1987) · Endocrine Reviews · doi:10.1210/edrv-8-1-1 · Cited by 1,080
Migliaccio, A., Castoria, G., Domenico, M. D., de Falco, A., Bilancio, A., Lombardi, M., Barone, M. V., Ametrano, D., Zannini, M. S., Abbondanza, C., et al. (2000) · The EMBO Journal · doi:10.1093/emboj/19.20.5406 · Cited by 672
SPECIFIC, NONGENOMIC ACTIONS OF STEROID HORMONES
Wehling, M. (1997) · Annual Review of Physiology · doi:10.1146/annurev.physiol.59.1.365 · Cited by 663
Transcriptional activation and nuclear targeting signals of the human androgen receptor.
Simental, J. A., Sar, M., Lane, M. V., French, F. S., & Wilson, E. M. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)52466-2 · Cited by 631
Mechanisms of capacitative calcium entry
Putney, J. W., Broad, L. M., Braun, F.-J., Lièvremont, J.-P., & Bird, G. S. J. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.12.2223 · Cited by 524
Flagged first, then by citations
Cited by
Sorted by citations
Items 201–268 of 268
Cardiovascular Effects of Androgens
Wilson, C., Maass, R., & Estr, M. (2011) · InTech eBooks · doi:10.5772/17843 · Cited by 5
“Similar effects of testosterone have been identified in T-cells, skeletal muscle and neuroblastoma cells (Benten et al., 1999; Estrada et al., 2003, 2006).”
Background[Extra nuclear localization of steroid receptors and non genomic activation mechanisms].
Bottino, M. C., & Lanari, C. (2010) · PubMed · Cited by 5
Testosterone therapy delays cardiomyocyte aging via an androgen receptor-independent pathway
Zhang, L., Wu, S., Ruan, Y. J., Li, H., Xing, X.-W., & Lai, W. (2011) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2011007500128 · Cited by 5
“Testosterone also protects skeletal muscle cells and neurons from cell death (26,27).”
BackgroundTestosterone acts through the membrane protein GPRC6A to cause cardiac edema in zebrafish embryos
Zadmajid, V., Shahriar, S., & Gorelick, D. A. (2024) · Development · doi:10.1242/dev.204390 · Cited by 6
Role of Androgens in Cardiovascular Diseases in Men: A Comprehensive Review
Mukherjee, D., Sen, K., Gupta, S., Chowdhury, P. D., Majumder, S., & Guha, P. (2020) · IntechOpen eBooks · doi:10.5772/intechopen.85852 · Cited by 5
Studencki, M., Ignatjeva, A., Nitychoruk, M., Gołaś, A., Smółka, W., & Maszczyk, A. (2021) · Physical Activity Review · doi:10.16926/par.2021.09.27 · Cited by 4
Dias-Rocha, C. P., de Almeida, M. M., Woyames, J., Mendonça, R., de Andrade, C. B. V., Pazos-Moura, C. C., & Trevenzoli, I. H. (2022) · Life Sciences · doi:10.1016/j.lfs.2022.120831 · Cited by 4
Morgentaler, A. (2020) · Androgens Clinical Research and Therapeutics · doi:10.1089/andro.2020.0009 · Cited by 4
Capacchione, J. F., Radimer, M. C., Sagel, J. S., Kraus, G. P., Sambuughin, N., & Muldoon, S. M. (2009) · Anesthesia & Analgesia · doi:10.1213/ane.0b013e31819240a5 · Cited by 4
“The genomic effects involve interactions with intracellular androgen receptors which mediate gene expression,(32,33) whereas the nongenomic effects are characterized by a rapid second messenger mechanism, increasing the release of calcium from SR via inositol-1,4,5-triphosphate (IP3) through phospholipase C activation…”
BackgroundThe Molecular Pathogenesis of Sarcopenia/Frailty in Cirrhosis
Jiao, H., Wang, H., Li, J. X., Yang, Z., & Sun, C. (2025) · Seminars in Liver Disease · doi:10.1055/a-2564-7551 · Cited by 3
“31 Kovacheva et al implicated that testosterone-triggered muscle fi ber hypertrophy was associated with inhibition of myostatin and p21 expression, inhibition of JNK signaling, stimulation of Akt and Notch signaling, and restoration of G6PDH levels.”
Ørnstrup, M. J., Høst, C., Rittig, N. F., & Gravholt, C. H. (2024) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00078.2024 · Cited by 3
Grandys, M., Majerczak, J., Karasiński, J., Kulpa, J., & Zoladz, J. A. (2012) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0b013e31827361d7 · Cited by 3
“and Ca2+-dependent pathways (15), and affects key regulatory factors for muscle differentiation because myostatin (30), insulinlike growth factor 1 (16), and FOXO1 transcription factor (42), which may all influence the skeletal muscle fiber–type transition.”
BackgroundSarcopenia and Androgens: A Link Between Pathology and Treatment
Basualto-Alarcón, C., Varela, D., Duran, J., Maass, R., & Estrada, M. (2016) · Apple Academic Press eBooks · doi:10.1201/b19985-16 · Cited by 4
Tang, X., Li, B., Li, D., & Wang, Y. (2025) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1619613 · Cited by 2
Anabolic/Androgenic Steroids in Skeletal Muscle and Cardiovascular Diseases
Basualto-Alarcn, C., Maass, R., Jaimovich, E., & Estr, M. (2013) · InTech eBooks · doi:10.5772/53080 · Cited by 2
Androgen receptor-dependent mechanisms mediating therapy resistance in prostate cancer
Saker, Z., Rizk, M., & Nabha, S. M. (2023) · Elsevier eBooks · doi:10.1016/b978-0-443-16032-5.00004-x · Cited by 2
Salter, D., Swamy, S., Salis, K. M., Deep, D. K., & Nadig, P. D. (2024) · Frontiers in Nutrition · doi:10.3389/fnut.2024.1393917 · Cited by 3
“T can also elicit an increase in intracellular calcium (49) to temporarily elevate the maximum force production (50) for greater training intensity.”
BackgroundMcGrath, K. C. Y., Xh, L., & Williams, P. (2012) · Journal of Steroids & Hormonal Science · doi:10.4172/2157-7536.s2-005 · Cited by 2
“The existence of a novel plasma membrane receptor for androgens has been described for non-central nervous system tissue, vascular tissue, osteoblasts, macrophages, ovary and T cells [8-15] however, to date, no membrane receptor for androgens has been shown in human vascular endothelial cells.”
BackgroundThe Role of Hormones in Exercise-Induced Muscle Hypertrophy
Fink, J. E. (2020) · Contemporary Endocrinology · doi:10.1007/978-3-030-33376-8_21 · Cited by 2
Hormone-mediated strategies to enhance training and performance
Beaven, C. M. (2010) · Tuwhera (Auckland University of Technology) · Cited by 2
Physiological and perceptual responses to training and competition in elite female netball players
Birdsey, L. P. (2021) · Cronfa (Swansea University) · doi:10.23889/suthesis.58707 · Cited by 2
Tsutsumi, T., & Tsuchiya, K. (2026) · Frontiers in Bioscience-Landmark · doi:10.31083/fbl47713 · Cited by 1
Holschbach, M. A., & Handa, R. J. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-802175-0.00022-x · Cited by 1
Regulation of Muscle Proteostasis via Extramuscular Signals
Atherton, P. J., & Szewczyk, N. J. (2011) · Royal Society of Chemistry eBooks · doi:10.1039/bk9781849733434-00077 · Cited by 1
Chen, Q. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-23585-6.00006-6 · Cited by 1
Sadeghi, N., Saadatfard, S., Dianat, M., Abedi, H., & Dehghani, K. (2021) · Physiology and Pharmacology · doi:10.32598/ppj.25.2.80 · Cited by 1
“In accordance with previous reports, high calcium concentration induced by high number of depolarizations lead to extra heart beats and as a result, tendency to cardio myocytes (DAD) increases and at this time, arrythmias are induced (Estrada et al., 2003).”
BackgroundAnabolic and anticatabolic agents in kidney disease and kidney failure
Chiang, J. M., & Johansen, K. L. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-818540-7.00040-9 · Cited by 1
Sex-Steroid Rapid Action and Its Role in Invasiveness and Metastasis of Breast Cancer
Flamini, M. I., Sanchez, A. M., Fu, X., & Simoncini, T. (2011) · Springer eBooks · doi:10.1007/978-1-4614-1764-4_6 · Cited by 1
Chignalia, A. Z. (2009) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.42.2009.tde-02022010-114821 · Cited by 1
“A ativação de ERK1/2 pela testosterona já foi demonstrada em células não vasculares como, por exemplo, neurônios hipocampais (NGUYEN et al., 2005), células de músculo esquelético (ESTRADA et al., 2003) e células tumorais de carcinoma de adrenal humanas (BROWN et al., 2001).”
BackgroundMethodStrategies for monitoring and training strength and power in elite rugby union players
Gannon, E. A. (2015) · The University of Bath Online Publications Store (The University of Bath)
The role of steroid hormones in skeletal muscle metabolism
Salehzadeh, F. (2011) · Figshare
Doping in Children and Adolescents
Rawson, E. S., & Persky, A. M. (2007) · Wiley eBooks · doi:10.1002/9780470696255.ch21
Hulmi, J. J. (2009) · Jyväskylä University Digital Archive (University of Jyväskylä)
Rodríguez, W. V., & Antonio, C. C. (2011) · Universidad de Chile
Sex Steroids and Gene Variants in Bipolar Disorder
Johansson, A. G. M. (2012) · Figshare
Toone, R. J. (2015) · The University of Bath Online Publications Store (The University of Bath)
Enhancing start performance in the sport of skeleton
Colyer, S. (2015) · The University of Bath Online Publications Store (The University of Bath)
del transportador GLUT4 a través del eje de señalización CaMKII/AMPK en cardiomiocitos"
Químicas, F. D. C., & Molecular, B. (2011)
MEMBRANE EFFECTS OF SEX HORMONES ON GROWTH
Chondrocytes, P. (2012)
Characterization of Myopathy in Mice Overexpressing Androgen Receptor in Skeletal Muscle
Musa, M. (2010) · TSpace (University of Toronto)
Immunization of Male Rabbits with Pseudomonas aeruginosa Increases Spermatogenesis
Zabbon, A. A. (2015) · World Journal of Experimental Biosciences
Williams, N. (2018) · Cronfa (Swansea University) · doi:10.23889/suthesis.43713
High‐Throughput Flow Cytometry
Sklar, L. A., Simons, P. C., Waller, A., Biggs, S. M., Young, S. M., Olah, M. M., Bologa, C., Oprea, T. I., Prossnitz, E. R., & Edwards, B. S. (2010) · Pharmaceutical Sciences Encyclopedia · doi:10.1002/9780470571224.pse006
Sex Steroid Hormones and Osteosarcopenia
Girgis, C. M. (2019) · Springer eBooks · doi:10.1007/978-3-030-25890-0_8
The Physiological and Perceptual Responses to Concurrent Training in Soccer Players
Sparkes, W. (2022) · Cronfa (Swansea University) · doi:10.23889/suthesis.60294
Androgen Receptor Signaling: A Central and Evolving Theme in Prostate Cancer Treatment
Banerjee, P. P., & Srivastava, S. K. (2023) · Springer eBooks · doi:10.1007/978-981-99-2196-6_24-1
Alexander, S. E., Gatto, B., Knowles, O., Williams, R. M., Fiebig, K. N., Jansons, P., Gatta, P. A. D., GARNHAM, A. P., Eynon, N., Wadley, G. D., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.12.593786
Androgen Receptor Signaling: A Central and Evolving Theme in Prostate Cancer Treatment
Banerjee, P. P., & Srivastava, S. K. (2024) · Springer eBooks · doi:10.1007/978-981-99-6263-1_24 · Cited by 1
Витальевна, А. С., Салухов, В. В., Kryukov, E. V., Эдуардовна, Р. С., Алексеевна, О. И., Khovpachev, A. A., Basharin, V. A., & Minakov, A. A. (2025) · Meditsinskiy sovet = Medical Council · doi:10.21518/ms2025-161
Kolliari-Turner, A., Lima, G. H. O., Wang, G., Malinsky, F. R., Karanikolou, A., Eichhorn, G., Tanisawa, K., Betancurt, J. A. O., Hamilton, B., Kumi, P. Y. O., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26586666
Kolliari-Turner, A., Lima, G. H. O., Wang, G., Malinsky, F. R., Karanikolou, A., Eichhorn, G., Tanisawa, K., Betancurt, J. A. O., Hamilton, B., Kumi, P. Y. O., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26586669
Kolliari-Turner, A., Lima, G. H. O., Wang, G., Malinsky, F. R., Karanikolou, A., Eichhorn, G., Tanisawa, K., Betancurt, J. A. O., Hamilton, B., Kumi, P. Y. O., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26586654
Kolliari-Turner, A., Lima, G. H. O., Wang, G., Malinsky, F. R., Karanikolou, A., Eichhorn, G., Tanisawa, K., Betancurt, J. A. O., Hamilton, B., Kumi, P. Y. O., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26586663
Kolliari-Turner, A., Lima, G. H. O., Wang, G., Malinsky, F. R., Karanikolou, A., Eichhorn, G., Tanisawa, K., Betancurt, J. A. O., Hamilton, B., Kumi, P. Y. O., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26586660
Kolliari-Turner, A., Lima, G. H. O., Wang, G., Malinsky, F. R., Karanikolou, A., Eichhorn, G., Tanisawa, K., Betancurt, J. A. O., Hamilton, B., Kumi, P. Y. O., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26586657
Kolliari-Turner, A., Lima, G. H. O., Wang, G., Malinsky, F. R., Karanikolou, A., Eichhorn, G., Tanisawa, K., Betancurt, J. A. O., Hamilton, B., Kumi, P. Y. O., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26586651
Increase in testosterone and cortisol one week after repeated exercise in a cold environment
Dytrtová, J. J., Jakl, M., Jebavý, R., Máčová, L., Hornikova, D., Novak, F. J., Vodička, P., Navrátil, T., Bičı́ková, M., Elsnicová, B., et al. (2026) · Frontiers in Physiology · doi:10.3389/fphys.2025.1731242
Schindler, M. (2010) · theses.fr (ABES) · doi:10.70675/cee355aez4f3cz472bz8dd9z2880a141df1c
Genome-wide analyses of signaling pathways controlled by steroid receptors
Rerra, A. (2019) · theses.fr (ABES) · doi:10.70675/d10332bfzd22cz480cz8f5czc0114d6c93c5
Associations between outdoor light exposure and low muscle mass: An NHANES 2011 to 2014 analysis
Xue, Z., Sun, D., Wang, Z., Yan, D., Deng, F., Yu, Z., & Liu, P. (2026) · Medicine · doi:10.1097/md.0000000000048257
“…by improving the efficiency of intracellular amino acid recycling [54] ; stimulating satellite cell activity [55] ; activating G protein-coupled receptors to increase intracellular calcium concentration [56] ; and influencing muscle hypertrophy via increased insulin-like growth factor-1 expression.”
MetAR : A semi-automated meta-analysis of skeletal muscle androgen receptors association with agePreprint
Williams, R. M., Engman, V., Soria, M., Wadley, G. D., Hiam, D., & Lamon, S. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.04.21.719741 · Cited by 1
Akyüz, O., Alimoradi, M., Alghosi, M., Özaltaş, H. N., Cengiz, C., Ceylan, L., Barut, Y., & Konrad, A. (2026) · Frontiers in Physiology · doi:10.3389/fphys.2026.1797234
Factors affecting the hourly distribution of calving in Holstein cows in a hot environment
Treviño, N., Mellado, M., Morales-Cruz, J. L., Contreras-Villarreal, V., García, J. E., Ávila‐Serrano, N. Y., & Mellado, J. (2026) · Ciência Animal Brasileira · doi:10.1590/1809-6891v27e-84360e
Metadata
- Authors
- Estrada, M., Espinosa, A., Müller, M., & Jaimovich, E.
- Affiliations
- University of Chile (CL)
- Corresponding author
- Jaimovich, Enrique
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2003-08
- Volume
- 144
- Issue
- 8
- Pages
- 3586-3597
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- OpenAlex
- W2134223482
- Cited by
- 264
- References
- 46
- Citations by year
- 2026: 6 · 2025: 8 · 2024: 17 · 2023: 14 · 2022: 8 · 2021: 11 · 2020: 13 · 2019: 9 · 2018: 8 · 2017: 8 · 2016: 14 · 2015: 13 · 2014: 8 · 2013: 13 · 2012: 9
- FWCI
- 5.16
- Type
- journal article
- Language
- en
- Open access
- green
- americanae.aecid.es
- Licence
- other-oa
- Locations
- Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Americanae (AECID Library) (submittedVersion, other-oa)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
- Funders
- Olympus
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Keywords
- testosterone, nandrolone, intracellular calcium release, calcium oscillations, inositol 1,4,5-trisphosphate, IP3 receptor, ERK1/2 phosphorylation, Ras/MEK/ERK signaling, G protein-coupled receptors, skeletal muscle myotubes, cyproterone, pertussis toxin, MEK inhibitors
- MeSH terms
- Androgens, Animals, Animals, Newborn, Calcium, Chelating Agents, Nandrolone, Phosphorylation, Testosterone, Transfection, Calcium Channels, Inositol 1,4,5-Trisphosphate, Gene Expression, Protein Serine-Threonine Kinases, Cyclic AMP Response Element-Binding Protein, Cyproterone Acetate, Receptors, Cytoplasmic and Nuclear, Muscle, Skeletal, Muscle Fibers, Skeletal, ras Proteins, GTP-Binding Proteins, Mitogen-Activated Protein Kinase 1, Mitogen-Activated Protein Kinases, Mitogen-Activated Protein Kinase 3, Rats, Inositol 1,4,5-Trisphosphate Receptors, Androgen Receptor Antagonists
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review