Physiological and Pathological Androgen Actions in the Ovary
Open accessAbstract
Androgens, although traditionally thought to be male sex steroids, play important roles in female reproduction, both in healthy and pathological states. This mini-review focuses on recent advances in our knowledge of the role of androgens in the ovary. Androgen receptor (AR) is expressed in oocytes, granulosa cells, and theca cells, and is temporally regulated during follicular development. Mouse knockout studies have shown that AR expression in granulosa cells is critical for normal follicular development and subsequent ovulation. In addition, androgens are involved in regulating dynamic changes in ovarian steroidogenesis that are critical for normal cycling. Androgen effects on follicle development have been incorporated into clinical practice in women with diminished ovarian reserve, albeit with limited success in available literature. At the other extreme, androgen excess leads to disordered follicle development and anovulatory infertility known as polycystic ovary syndrome (PCOS), with studies suggesting that theca cell AR may mediate many of these negative effects. Finally, both prenatal and postnatal animal models of androgen excess have been developed and are being used to study the pathophysiology of PCOS both within the ovary and with regard to overall metabolic health. Taken together, current scientific consensus is that a careful balance of androgen activity in the ovary is necessary for reproductive health in women.
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These testosterone-induced alterations to female development are largely consistent across animal models.
“Importantly, these testosterone‐induced alterations to female development are largely consistent across animal models (Astapova et al., 2019; Roland & Moenter, 2014).”
From Endometriosis and polycystic ovary syndrome are diametric disorders (2021) · cites this paper as Astapova et al., 2019
High ovarian testosterone promotes early follicular growth, mediating recruitment of follicles from primordial to small pre-antral stage, and contributing to elevated antral follicle count, follicular arrest, anovulation, and cyst formation characteristic of PCOS.
“High ovarian testosterone promotes early follicular growth, mediating the recruitment of follicles from the primordial stage to the small, pre‐antral stage, and contributing to elevated antral follicle count, follicular arrest, anovulation, and the cyst formation characteristic of PCOS (Astapova et al., 2019).”
From Endometriosis and polycystic ovary syndrome are diametric disorders (2021) · cites this paper as Astapova et al., 2019
Cites
Chamberlain, N. L., Driver, E. D., & Miesfeld, R. L. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.15.3181 · Cited by 1,149 · see citing works
Androgens stimulate early stages of follicular growth in the primate ovary
Vendola, K. A., Zhou, J., Adesanya, O. O., Weil, S. J., & Bondy, C. A. (1998) · Journal of Clinical Investigation · doi:10.1172/jci2081 · Cited by 712 · see citing works
Yeh, S., Tsai, M.-Y., Xu, Q., Mu, X., Lardy, H. A., Huang, K., Lin, H., Yeh, S.-D., Altuwaijri, S., Zhou, X., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.212474399 · Cited by 668 · see citing works
Androgen and follicle stimulating hormone interactions in primate ovarian follicle development
Weil, S., Vendola, K., Zhou, J., & Bondy, C. A. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.8.5929 · Cited by 592 · see citing works
Abbott, D. H., Barnett, D. K., Bruns, C. M., & Dumesic, D. A. (2005) · Human Reproduction Update · doi:10.1093/humupd/dmi013 · Cited by 555 · see citing works
Tut, T. G., Ghadessy, F. J., Trifiro, M. A., Pinsky, L., & Yong, E. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.11.4385 · Cited by 520 · see citing works
A New Rat Model Exhibiting Both Ovarian and Metabolic Characteristics of Polycystic Ovary Syndrome
Mannerås, L., Cajander, S. B., Holmäng, A. B., Seleskovic, Z., Lystig, T., Lönn, M., & Stener‐Victorin, E. (2007) · Endocrinology · doi:10.1210/en.2007-0168 · Cited by 482 · see citing works
Cai, C., He, H. H., Chen, S., Coleman, I. M., Wang, H., Fang, Z., Chen, S., Nelson, P. S., Liu, X., Brown, M. A., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.09.001 · Cited by 456 · see citing works
Tut, T. G. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.82.11.3777 · Cited by 365 · see citing works
Weil, S. J., Vendola, K., Zhou, J., Adesanya, O. O., Wang, J., Okafor, J., & Bondy, C. A. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.7.4917 · Cited by 359 · see citing works
Sonneveld, E. (2004) · Toxicological Sciences · doi:10.1093/toxsci/kfi005 · Cited by 352 · see citing works
Premature ovarian failure in androgen receptor-deficient mice
Shiina, H., Μatsumoto, T., Sato, T., Igarashi, K., Miyamoto, J., Takemasa, S., Sakari, M., Takada, I., Nakamura, T., METZGER, D., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506736102 · Cited by 332 · see citing works
Subfertility and defective folliculogenesis in female mice lacking androgen receptor
Hu, Y., Wang, P., Yeh, S., Wang, R.-S., Xie, C. L., Xu, Q., Zhou, X., Chao, H., Tsai, M., & Chang, C. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404372101 · Cited by 316 · see citing works
Sen, A., & Hammes, S. R. (2010) · Molecular Endocrinology · doi:10.1210/me.2010-0006 · Cited by 313 · see citing works
Self-citationSullivan, S. D., & Moenter, S. M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308058101 · Cited by 309 · see citing works
Sen, A., Prizant, H., Light, A., Biswas, A., Hayes, E. T., Lee, H., Barad, D. H., Gleicher, N., & Hammes, S. R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1318978111 · Cited by 283 · see citing works
Self-citationAbbott, D. H., Dumesic, D. A., Eisner, J. R., Colman, R. J., & Kemnitz, J. W. (1998) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(98)00019-8 · Cited by 228 · see citing works
Steckler, T. L., Wang, J., Bartol, F. F., Roy, S. K., & Padmanabhan, V. (2005) · Endocrinology · doi:10.1210/en.2004-1444 · Cited by 209 · see citing works
Reproductive and Metabolic Phenotype of a Mouse Model of PCOS
van Houten, E. L. A. F., Kramer, P., McLuskey, A., Karels, B., Themmen, A. P. N., & Visser, J. A. (2012) · Endocrinology · doi:10.1210/en.2011-1754 · Cited by 190 · see citing works
Prenatal androgen exposure programs metabolic dysfunction in female mice
Roland, A. V., Nunemaker, C. S., Keller, S. R., & Moenter, S. M. (2010) · Journal of Endocrinology · doi:10.1677/joe-10-0217 · Cited by 184 · see citing works
Foecking, E. M., Szabo, M., Schwartz, N. B., & Levine, J. E. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.105.039800 · Cited by 165 · see citing works
Moore, A. M., Prescott, M., & Campbell, R. E. (2012) · Endocrinology · doi:10.1210/en.2012-1954 · Cited by 153 · see citing works
Location and developmental regulation of androgen receptor in primate ovary
Hillier, S. G., TETSUKA, M., & Fraser, H. M. (1997) · Human Reproduction · doi:10.1093/humrep/12.1.107 · Cited by 149 · see citing works
Developmental regulation of androgen receptor in rat ovary
TETSUKA, M., Whitelaw, P. F., Bremner, W. J., Millar, M. R., Smyth, C. D., & Hillier, S. G. (1995) · Journal of Endocrinology · doi:10.1677/joe.0.1450535 · Cited by 138 · see citing works
Developmental programming: prenatal androgen excess disrupts ovarian steroid receptor balance
Ortega, H. H., Salvetti, N. R., & Padmanabhan, V. (2009) · Reproduction · doi:10.1530/rep-08-0491 · Cited by 133 · see citing works
Increased Adiposity in Female Rhesus Monkeys Exposed to Androgen Excess During Early Gestation
Eisner, J. R., Dumesic, D. A., Kemnitz, J. W., Colman, R. J., & Abbott, D. H. (2003) · Obesity Research · doi:10.1038/oby.2003.42 · Cited by 133 · see citing works
Hickey, T. E., Marrocco, D. L., Amato, F., Ritter, L. J., Norman, R. J., Gilchrist, R. B., & Armstrong, D. T. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.104.039362 · Cited by 123 · see citing works
Walters, K. A., Middleton, L. J., Joseph, S. R., Hazra, R., Jimenez, M., Simanainen, U., Allan, C. M., & Handelsman, D. J. (2012) · Biology of Reproduction · doi:10.1095/biolreprod.112.102012 · Cited by 123 · see citing works
Prenatal testosterone excess programs reproductive and metabolic dysfunction in the female
Padmanabhan, V., Manikkam, M., Recabarren, S. E., & Foster, D. L. (2006) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2005.11.016 · Cited by 119 · see citing works
ZIP9, a novel membrane androgen receptor and zinc transporter protein
Thomas, P., Converse, A., & Berg, H. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.04.016 · Cited by 116 · see citing works
Harlow, C. R., Shaw, H. J., Hillier, S. G., & Hodges, J. K. (1988) · Endocrinology · doi:10.1210/endo-122-6-2780 · Cited by 112 · see citing works
Sarma, H. N., Manikkam, M., Herkimer, C., Dell’Orco, J., Welch, K. B., Foster, D. L., & Padmanabhan, V. (2005) · Endocrinology · doi:10.1210/en.2005-0322 · Cited by 104 · see citing works
Ontogeny and reversal of brain circuit abnormalities in a preclinical model of PCOS
Silva, M. S. B., Prescott, M., & Campbell, R. E. (2018) · JCI Insight · doi:10.1172/jci.insight.99405 · Cited by 100 · see citing works
Yang, F., Ruan, Y. C., Yang, Y.-J., Wang, K., Liang, S.-S., Han, Y.-B., Teng, X.-M., & Yang, J.-Z. (2015) · Reproduction · doi:10.1530/rep-15-0044 · Cited by 98 · see citing works
Roland, A. V., & Moenter, S. M. (2010) · Endocrinology · doi:10.1210/en.2010-0823 · Cited by 92 · see citing works
Sen, A., O’Malley, K. J., Wang, Z., Raj, G. V., DeFranco, D. B., & Hammes, S. R. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.134064 · Cited by 89 · see citing works
Self-citationMa, Y., Andrisse, S., Chen, Y., Childress, S., Xue, P., Wang, Z., Jones, D., Ko, C. J., DiVall, S. A., & Wu, S. (2016) · Endocrinology · doi:10.1210/en.2016-1608 · Cited by 80 · see citing works
Laird, M., Thomson, K., Fenwick, M. A., Mora, J. M., Franks, S., & Hardy, K. (2017) · Endocrinology · doi:10.1210/en.2016-1538 · Cited by 79 · see citing works
Hickey, T. E., Marrocco, D. L., Gilchrist, R. B., Norman, R. J., & Armstrong, D. T. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.103.026484 · Cited by 71 · see citing works
Early Embryonic Androgen Exposure Induces Transgenerational Epigenetic and Metabolic Changes
Xu, N., Chua, A. K., Jiang, H., Liu, N., & Goodarzi, M. O. (2014) · Molecular Endocrinology · doi:10.1210/me.2014-1042 · Cited by 71 · see citing works
Introducing a rat model of prenatal androgen‐induced polycystic ovary syndrome in adulthood
Tehrani, F. R., Noroozzadeh, M., Zahediasl, S., Piryaei, A., & Azizi, F. (2014) · Experimental Physiology · doi:10.1113/expphysiol.2014.078055 · Cited by 68 · see citing works
Early origins of polycystic ovary syndrome
Dumesic, D. A., Schramm, R. D., & Abbott, D. H. (2005) · Reproduction Fertility and Development · doi:10.1071/rd04092 · Cited by 67 · see citing works
Unsworth, W. P., Taylor, J. A., & Robinson, J. E. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.104.035691 · Cited by 67 · see citing works
Reduced reproductive performance in androgen-resistant Tfm / Tfm female mice
Lyon, M. F., & Glenister, P. H. (1980) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1980.0040 · Cited by 66 · see citing works
Wu, Y.-G., Bennett, J., Talla, D., & Stocco, C. O. (2011) · Molecular Endocrinology · doi:10.1210/me.2010-0367 · Cited by 65 · see citing works
Does PCOS have developmental origins?
Franks, S., & Berga, S. L. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.11.029 · Cited by 64 · see citing works
Hogg, K., McNeilly, A. S., & Duncan, W. C. (2011) · Endocrinology · doi:10.1210/en.2010-1219 · Cited by 62 · see citing works
Li, J., Yuan, H., Chen, Y., Wu, H., Wu, H., & Li, L. (2015) · International Journal of Gynecology & Obstetrics · doi:10.1016/j.ijgo.2015.06.028 · Cited by 55 · see citing works
Škrgatić, L., Baldani, D. P., Cerne, J. Z., Ferk, P., & Geršak, K. (2011) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2011.11.006 · Cited by 55 · see citing works
Hu, Q., Hong, L., Nie, M., Wang, Q., Fang, Y., Dai, Y., Zhai, Y., Wang, S., Yin, C., & Yang, X. (2017) · Journal of Ovarian Research · doi:10.1186/s13048-017-0326-3 · Cited by 54 · see citing works
A regulatory role of androgen in ovarian steroidogenesis by rat granulosa cells
Hasegawa, T., Kamada, Y., Hosoya, T., Fujita, S., Nishiyama, Y., Iwata, N., Hiramatsu, Y., & Otsuka, F. (2017) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2017.07.002 · Cited by 49 · see citing works
Zhang, T., Liang, W., Fang, M., Yu, J., Ni, Y., & Li, Z. (2013) · Gene · doi:10.1016/j.gene.2013.04.040 · Cited by 48 · see citing works
Yazawa, T., Kawabe, S., Kanno, M., Mizutani, T., Imamichi, Y., Ju, Y., Matsumura, T., Yamazaki, Y., Usami, Y., Kuribayashi, M., et al. (2013) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2013.02.004 · Cited by 46 · see citing works
Otala, M., Mäkinen, S., Tuuri, T., Sjöberg, J., Pentikäinen, V., Matikainen, T., & Dunkel, L. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.06.032 · Cited by 37 · see citing works
Early prenatal androgenization results in diminished ovarian reserve in adult female rhesus monkeys
Dumesic, D. A., Patankar, M. S., Barnett, D. K., Lesnick, T. G., Hutcherson, B. A., & Abbott, D. H. (2009) · Human Reproduction · doi:10.1093/humrep/dep324 · Cited by 33 · see citing works
Băculescu, N. (2013) · Europe PMC (PubMed Central) · Cited by 32 · see citing works
Orphan Nuclear Receptor NR4A1 Is a Negative Regulator of DHT-Induced Rat Preantral Follicular Growth
Xue, K., Liu, J., Murphy, B. D., & Tsang, B. K. (2012) · Molecular Endocrinology · doi:10.1210/me.2012-1200 · Cited by 29 · see citing works
Converse, A., Zhang, C., & Thomas, P. (2017) · Endocrinology · doi:10.1210/en.2017-00087 · Cited by 29 · see citing works
Androgens Regulate Ovarian Gene Expression Through Modulation of Ezh2 Expression and Activity
Ma, X., Hayes, E. T., Biswas, A., Seger, C., Prizant, H., Hammes, S. R., & Sen, A. (2017) · Endocrinology · doi:10.1210/en.2017-00145 · Cited by 28 · see citing works
Self-citationJahromi, M. S., Hill, J. W., Tehrani, F. R., & Zadeh–Vakili, A. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.05.052 · Cited by 26 · see citing works
Zhang, D., Cong, J., Huanhuan, S., Wu, Q., & Wu, X. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.07.1203 · Cited by 24 · see citing works
Role of testosterone in normal female function.
Ohno, S., Christian, L., & Attardi, B. (1973) · PubMed · Cited by 20 · see citing works
Hay, C. W., Watt, K., Hunter, I., Lavery, D. N., MacKenzie, A., & McEwan, I. J. (2014) · Hormones and Cancer · doi:10.1007/s12672-014-0185-y · Cited by 20 · see citing works
Borgbo, T., Maçek, M., Chrudimská, J., Jeppesen, J. V., Hansen, L. L., & Andersen, C. Y. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.09.015 · Cited by 18 · see citing works
Androgens promote the acquisition of maturation competence in bovine oocytes
Makita, M., & Miyano, T. (2015) · Journal of Reproduction and Development · doi:10.1262/jrd.2014-161 · Cited by 17 · see citing works
Epigenetic pattern changes in prenatal female Sprague-Dawley rats following exposure to androgen
Xia, Y., Shen, S., Zhang, X., Deng, Z., Zou, X., Wang, H., Yi, L., Gao, Q., & Wang, Y. (2015) · Reproduction Fertility and Development · doi:10.1071/rd14292 · Cited by 15 · see citing works
Identification of androgen receptor phosphorylation in the primate ovary in vivo
McEwan, I. J., McGuinness, D., Hay, C. W., Millar, R. P., Saunders, P. T. K., & Fraser, H. M. (2010) · Reproduction · doi:10.1530/rep-10-0140 · Cited by 15 · see citing works
Mechanism underlying the retarded nuclear translocation of androgen receptor splice variants
Liu, Y., Wang, Y., Wang, F., Pan, J., Xu, J.-J., Li, J., Zhou, C., Ding, G., Wu, Y., Liu, X., et al. (2018) · Science China Life Sciences · doi:10.1007/s11427-018-9379-x · Cited by 8 · see citing works
Miedlich, S. U., Taya, M., Young, M. R., & Hammes, S. R. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.03.028 · Cited by 8 · see citing works
Self-citationWartalski, K., Knet, M., Hoja-Łukowicz, D., Tabarowski, Z., & Duda, M. (2016) · Acta Histochemica · doi:10.1016/j.acthis.2016.03.008 · Cited by 7 · see citing works
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Zhao, X., Wang, M., Wen, Z., Lu, Z., Cui, L., Fu, C., Xue, H., Liu, Y., & Zhang, Y. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.721135 · Cited by 463 · see citing works
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Aversa, A., Vignera, S. L., Rago, R., Gambineri, A., Nappi, R. E., Calogero, A. E., & Ferlin, A. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00516 · Cited by 159 · see citing works
Kamenov, Z., & Gateva, A. (2020) · Molecules · doi:10.3390/molecules25235566 · Cited by 100 · see citing works
The Crosstalk between Melatonin and Sex Steroid Hormones
Cipolla‐Neto, J., do Amaral, F. G., Soares, J. M., Gallo, C. C., Furtado, A., Cavaco, J. E. B., Gonçalves, I., Santos, C. R. A., & Quintela, T. (2021) · Neuroendocrinology · doi:10.1159/000516148 · Cited by 92 · see citing works
Endometriosis and polycystic ovary syndrome are diametric disorders
Dinsdale, N. L., & Crespi, B. J. (2021) · Evolutionary Applications · doi:10.1111/eva.13244 · Cited by 90 · see citing works
“…testosterone promotes early follicular growth, mediating the recruitment of follicles from the primordial stage to the small, pre- antral stage, and contributing to elevated antral follicle count, follicular arrest, anovulation, and the cyst formation characteristic of PCOS (Astapova et al., 2019).”
BackgroundWhat Is the Best Regimen for Ovarian Stimulation of Poor Responders in ART/IVF?
Blumenfeld, Z. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00192 · Cited by 54 · see citing works
Sun, J., Gan, L., Lv, S., Wang, T., Dai, C., & Sun, J. (2023) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2023.114625 · Cited by 48 · see citing works
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Gong, X., Zhang, Y., Ai, J., & Li, K. (2022) · Biomolecules · doi:10.3390/biom13010047 · Cited by 47 · see citing works
Dinh, D. T., Breen, J., Nicol, B., Foot, N. J., Bersten, D. C., Emery, A., Smith, K. M., Wong, Y. Y., Barry, S. C., Yao, H. H., et al. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad271 · Cited by 42 · see citing works
Dou, Y., Zhang, M., Zhang, H., Zhang, C., Feng, L., Hu, J., Gao, Y., Yuan, X.-Z., Zhao, Y., Zhao, H., et al. (2024) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2024.174972 · Cited by 40 · see citing works
Zhang, Y., Weng, Y., Wang, D., Wang, R., Wang, L., Zhou, J., Shen, S., Wang, H., & Wang, Y. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/7382900 · Cited by 38 · see citing works
Rooda, I., Hasan, M. M., Roos, K., Viil, J., Andronowska, A., Smolander, O., Jaakma, Ü., Salumets, A., Fazeli, A., & Velthut‐Meikas, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21249550 · Cited by 39 · see citing works
Song, L., Yu, J., Zhang, D., Li, X., Chen, L., Cai, Z., & Yu, C. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.789008 · Cited by 38 · see citing works
Krishnan, A., Muthusami, S., Periyasamy, L., Stanley, J. A., Gopalakrishnan, V., & Ramachandran, I. (2020) · Medicina · doi:10.3390/medicina56030100 · Cited by 34 · see citing works
Scarfò, G., Daniele, S., Fusi, J., Gesi, M., Martini, C., Franzoni, F., Cela, V., & Artini, P. G. (2022) · Biomedicines · doi:10.3390/biomedicines10061305 · Cited by 32 · see citing works
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Panda, S. P., Kesharwani, A., Singh, G. D., Prasanth, D., Vatchavai, B. R., Kumari, P. V. K., Panda, S. K., & Mallick, S. P. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.102086 · Cited by 24 · see citing works
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Lin, L., Li, C., & Tsui, K. (2021) · Scientific Reports · doi:10.1038/s41598-021-85915-x · Cited by 21 · see citing works
Hamid, F. A., Abu, M., Karim, A. K. A., Ahmad, M., Aziz, N. A., Kamal, D. A. M., & Mokhtar, M. H. (2022) · Biomedicines · doi:10.3390/biomedicines10071705 · Cited by 17 · see citing works
Otoo, A., Czika, A., Lamptey, J., Yang, J.-P., Feng, Q., Wang, M., Wang, Y., & Ding, Y. (2023) · Reproduction · doi:10.1530/rep-22-0449 · Cited by 17 · see citing works
Angiotensin-(1-7), Angiotensin-Converting Enzyme 2 and Mas Receptor in Rat Polycystic Ovaries
Pereira, V. M., dos Reis, F. M., Casalechi, M., & dos Reis, A. M. (2020) · Protein and Peptide Letters · doi:10.2174/0929866527666200826104410 · Cited by 16 · see citing works
Rbpms2 promotes female fate upstream of the nutrient sensing Gator2 complex component Mios
Wilson, M., Romano, S. N., Khatri, N., Aharon, D. A., Liu, Y., Kaufman, O. H., Draper, B. W., & Marlow, F. L. (2024) · Nature Communications · doi:10.1038/s41467-024-49613-2 · Cited by 14 · see citing works
Chen, X., Hong, L., Diao, L., Yin, T., & Liu, S. (2024) · American Journal of Reproductive Immunology · doi:10.1111/aji.13854 · Cited by 15 · see citing works
Zhong, Y., Ding, J., & Xia, F. (2025) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-025-08048-w · Cited by 16 · see citing works
Correlation between ovarian follicular development and Hippo pathway in polycystic ovary syndrome
Huang, Z., Xu, T., Liu, C., Wu, H., Weng, L., Cai, J., Liang, N., & Ge, H. (2024) · Journal of Ovarian Research · doi:10.1186/s13048-023-01305-z · Cited by 15 · see citing works
Wang, Z., Zhang, W., Huang, D., Kang, H., Wang, J., Liu, Z., Jiang, G., & Gao, A. (2024) · Environmental Pollution · doi:10.1016/j.envpol.2024.124100 · Cited by 15 · see citing works
Hu, R., Huang, Y., Liu, Z., Dong, H., Ma, W., Song, K., Xu, X., Wu, X. W., Geng, Y., Li, F., et al. (2024) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2024.104296 · Cited by 14 · see citing works
Testosterone mediates life‐history trade‐offs in female mammals
Crespi, B. J., Bushell, A., & Dinsdale, N. L. (2024) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.13166 · Cited by 15 · see citing works
The impact of isotretinoin on the pituitary-ovarian axis: An interpretative review of the literature
Abdelhamed, A., Eldawla, R. E., Karadağ, A. S., Agamia, N., & Melnik, B. C. (2021) · Reproductive Toxicology · doi:10.1016/j.reprotox.2021.06.017 · Cited by 16 · see citing works
Intertwined reproductive endocrinology: Puberty and polycystic ovary syndrome
Witchel, S. F., & Plant, T. M. (2020) · Current Opinion in Endocrine and Metabolic Research · doi:10.1016/j.coemr.2020.07.004 · Cited by 14 · see citing works
Engberg, H., Nordenström, A., & Hirschberg, A. L. (2024) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgae696 · Cited by 13 · see citing works
Gao, L., Gao, H., & Wang, W. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.951928 · Cited by 14 · see citing works
Tang, Z.-R., Deng, S., Lian, Z., & Yu, K. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.12.016 · Cited by 13 · see citing works
Female Reproductive Systems: Hormone Dependence and Receptor Expression
Kuan, K., & Saunders, P. T. K. (2022) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-11836-4_2 · Cited by 12 · see citing works
Role of the mitophagy‐apoptosis axis in the pathogenesis of polycystic ovarian syndrome
Kobayashi, H., Shigetomi, H., Matsubara, S., Yoshimoto, C., & Imanaka, S. (2024) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.15916 · Cited by 11 · see citing works
Panagiotou, E. M., Draskau, M. K., Li, T., Hirschberg, A. L., Svingen, T., & Damdimopoulou, P. (2022) · Reproductive Toxicology · doi:10.1016/j.reprotox.2022.07.004 · Cited by 11 · see citing works
Kamińska-Skrzyńska, W., Wiśniewska, K., Okręglicka, K., Pazura, I., & Nitsch-Osuch, A. S. (2023) · Annals of Agricultural and Environmental Medicine · doi:10.26444/aaem/159156 · Cited by 9 · see citing works
Deng, L., Min, W., Guo, S., Deng, J., Wu, X., Tong, D., Yuan, A., & Yang, Q. (2024) · Virology Journal · doi:10.1186/s12985-024-02289-y · Cited by 9 · see citing works
Velmurugan, S., Pauline, R., & Subbaraj, G. K. (2024) · Journal of the Turkish-German Gynecological Association · doi:10.4274/jtgga.galenos.2024.2024-1-7 · Cited by 9 · see citing works
Ma, X., Wang, Z., Zhang, C., Bian, Y., Zhang, X., Liu, X., Cao, Y., & Zhao, Y. (2022) · BMC Medical Genomics · doi:10.1186/s12920-022-01301-0 · Cited by 9 · see citing works
The role of zinc in follicular development
Liao, X., Wu, L., Yin, D., Tian, D., Zhou, C., Liu, J., Li, S., Zhou, J., Nie, Y., Liao, H., et al. (2023) · Molecular Biology Reports · doi:10.1007/s11033-023-08331-6 · Cited by 8 · see citing works
Cai, W.-Y., & Luo, X. (2024) · Combinatorial Chemistry & High Throughput Screening · doi:10.2174/0113862073321308240808075854 · Cited by 7 · see citing works
Bancos, I., Kim, H., Cheng, H. K.-H., Rodrı́guez-Lee, M., Coope, H., Cicero, S., Goldsmith, H., Lin, V. H., & Jeha, G. S. (2025) · Expert Review of Endocrinology & Metabolism · doi:10.1080/17446651.2025.2450423 · Cited by 7 · see citing works
Hristov, D., & Stojanov, D. (2025) · Receptors · doi:10.3390/receptors4030016 · Cited by 7 · see citing works
Lin, Y., Liu, X., Li, X., Tang, Q., Meng, F., & Chen, W. (2022) · Current Medicinal Chemistry · doi:10.2174/0929867329666220508180611 · Cited by 7 · see citing works
Zhou, Z., Zhang, Y., Zhang, X., Zhang, J., Yi, G., Wan, B., Li, Y., Lu, H., Tan, C., & Lu, W. (2023) · Reproductive Sciences · doi:10.1007/s43032-023-01251-7 · Cited by 6 · see citing works
Sziva, R. E., Kollarics, R., Pál, É., Bányai, B., Korsós-Novák, Á., Fontányi, Z., Magyar, P., Süli, A., Nádasy, G. L., Ács, N., et al. (2025) · Nutrients · doi:10.3390/nu17020201 · Cited by 6 · see citing works
Lin, L., & Tsui, K. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10061211 · Cited by 6 · see citing works
Randomized Controlled Study of the Effects of DHEA on the Outcome of IVF in Endometriosis
Zhang, Y., Li, M., Li, L., Xiao, J., & Chen, Z. (2021) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2021/3569697 · Cited by 6 · see citing works
RetractedYan, X., Gao, X., Shang, Q., Yang, Z., Wang, Y., Liu, L., Liu, W., Liu, D., Cheng, F., Zhao, S., et al. (2023) · Journal of Ovarian Research · doi:10.1186/s13048-023-01295-y · Cited by 5 · see citing works
Moh, M., Puzyrenko, A., Summey, R., Rader, J. S., Cano, G. E. H., Gavina, J. V., Rui, H., Sun, Y., & Hopp, E. E. (2024) · International Journal of Gynecological Pathology · doi:10.1097/pgp.0000000000001032 · Cited by 5 · see citing works
Paxillin regulates androgen receptor expression associated with granulosa cell focal adhesions
Weidner, A. E., Roy, A., Vann, K., Walczyk, A. C., & Astapova, O. (2024) · Molecular Human Reproduction · doi:10.1093/molehr/gaae018 · Cited by 5 · see citing works
Self-citationChen, K. L., Kenney, H. M., Schwarz, E. M., & Rahimi, H. (2024) · Journal of the Endocrine Society · doi:10.1210/jendso/bvae169 · Cited by 5 · see citing works
Salt-Inducible Kinases Regulate Androgen Synthesis in Theca Cells by Enhancing Creb Signaling
Esquivel, M. R., Hayes, E. T., Lakomy, O., Hassan, M., Foretz, M., & Stocco, C. O. (2023) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2023.112030 · Cited by 5 · see citing works
A meta-analysis: Effect of androgens on reproduction in sows
Guo, Z., Lv, L., Liu, D., Ma, H., & Radović, Č. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1094466 · Cited by 5 · see citing works
Mechanistic insight into nanomedicine for polycystic ovary syndrome
Butt, M. A., Tabassum, S., Hardy, R., & Kiyani, M. M. (2025) · Molecular Biology Reports · doi:10.1007/s11033-025-10709-7 · Cited by 11 · see citing works
Thyroid, Adrenal, PRL Impairments and Ovarian Function
Tomatis, V., Battipaglia, C., & Genazzani, A. D. (2021) · Endocrines · doi:10.3390/endocrines2030021 · Cited by 4 · see citing works
Mineiro, R., Cardoso, M. R., Pinheiro, J. V., Cipolla‐Neto, J., do Amaral, F. G., & Quintela, T. (2024) · Advances in protein chemistry and structural biology · doi:10.1016/bs.apcsb.2024.06.005 · Cited by 4 · see citing works
Saedi, A., Zarei, S., Vatanparast, M., Hajizadeh, M. R., Hosseiniara, R., Esmaeili, O. S., Mohammad-Sadeghipour, M., Mirzaei, Z., & Mahmoodi, M. (2024) · Annales Pharmaceutiques Françaises · doi:10.1016/j.pharma.2024.08.008 · Cited by 4 · see citing works
Neonatal androgenization in rats affects oocyte maturation
Anesetti, G., & Chávez‐Genaro, R. (2021) · Reproductive Sciences · doi:10.1007/s43032-021-00559-6 · Cited by 4 · see citing works
The way toward adulthood for females with nonclassic congenital adrenal hyperplasia
Ntali, G., Charisis, S., Kylafi, C. F., Vogiatzi, E., & Michala, L. (2021) · Endocrine · doi:10.1007/s12020-021-02715-z · Cited by 4 · see citing works
A 7-nt nucleotide sequence variant within the sheep KDM3B gene affects female reproduction traits
Kang, Y., Bi, Y., Tang, Q., Xu, H., Lan, X., Zhang, Q., & Pan, C. (2021) · Animal Biotechnology · doi:10.1080/10495398.2021.1929270 · Cited by 4 · see citing works
Junior, J. B. (2024) · World Journal of Gynecology & Womens Health · doi:10.33552/wjgwh.2024.06.000632 · Cited by 2 · see citing works
Han, Y., Diao, J., Wang, X., Zhang, S., Yuan, L., Ping, Y., Zhang, Y., & Luo, H. (2024) · Journal of Inflammation Research · doi:10.2147/jir.s490996 · Cited by 3 · see citing works
Zhao, Y., He, F., Pan, P., Xu, W., Xu, H., Yang, D., & Zhao, X. (2025) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2025.02.018 · Cited by 3 · see citing works
MiR-34b/c play a role in early sex differentiation of Amur sturgeon, Acipenser schrenckii
Zhang, X., Wu, W., Zhou, J., Li, L., Jiang, H., & Chen, J. (2022) · Frontiers in Zoology · doi:10.1186/s12983-022-00469-6 · Cited by 3 · see citing works
Nascimento, A. E. D. J., Santos, L. C., Santos, B. R., Santos, E. O., Cunha, M. C. D. S. G., Snoeck, P. P. D. N., de Lavor, M. S. L., & Silva, J. F. (2023) · Theriogenology · doi:10.1016/j.theriogenology.2023.08.001 · Cited by 3 · see citing works
Wang, X., Zhang, Y., Diao, H., Jiang, S., & Zhang, C. (2024) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.15911 · Cited by 3 · see citing works
Shaaban, Z., Tamadon, A., Shirazi, M. R. J., Zamiri, M. J., & Derakhshanfar, A. (2022) · PubMed Central · doi:10.22038/ijbms.2022.60962.13499 · Cited by 3 · see citing works
Huang, Q., Chen, X., Shen, H. Y., Zhou, J. M., Zhang, H. Q., Wang, L., Chen, R., Cheng, J., Zhang, Y., Zhang, D. M., et al. (2023) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s400350 · Cited by 3 · see citing works
Kim, T. H., Memarzadeh, S., Vahdatshariatpanahi, S., Ostrzega, N. L., Kang, Y., & Moatamed, N. A. (2025) · PLoS ONE · doi:10.1371/journal.pone.0322744 · Cited by 2 · see citing works
Zhang, Y., Chen, M., Zhou, Z. G., Guo, Y., Zheng, L., Yu, Y., Liu, J., Zhou, Y., Lu, H., Yao, S., et al. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1517934 · Cited by 2 · see citing works
Adolescent hyperandrogenism: diagnostic challenges and therapeutic approaches
Concepción‐Zavaleta, M. J., Fuentes‐Mendoza, J. M., Zavaleta‐Gutiérrez, F. E., Arias-Cantor, B. Y., Figueredo-Rueda, M. V., Arroyo, J., & Paz‐Ibarra, J. (2025) · World Journal of Pediatrics · doi:10.1007/s12519-025-00972-w · Cited by 2 · see citing works
Kongsomnuan, S., Niransuk, P., Singwongsa, A., & Satirapod, C. (2026) · PLoS ONE · doi:10.1371/journal.pone.0342463 · Cited by 2 · see citing works
Hamidi, O., Auchus, R. J., Correa, R. R., Levine, A. C., Wierman, M. E., Hartzell, A. L., Lin, V. H., & Bancos, I. (2026) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgag147 · Cited by 2 · see citing works
What is the Role of Testosterone Therapy in Postmenopausal Women? A SWOT Analysis
Aktöz, F., Güneş, A. C., & Erel, C. T. (2023) · Clinical and Experimental Obstetrics & Gynecology · doi:10.31083/j.ceog5008159 · Cited by 2 · see citing works
Zhao, Y., Jiao, X., Xu, J., Chu, C., Cao, Y., Xu, H., Xu, W., & Zhao, X. (2023) · Medicine Advances · doi:10.1002/med4.41 · Cited by 2 · see citing works
Kumar, M. (2024) · Medical Hypotheses · doi:10.1016/j.mehy.2024.111286 · Cited by 2 · see citing works
Boyle, P. C., Pandalache, C., & Turczynski, C. (2024) · Frontiers in Medicine · doi:10.3389/fmed.2024.1358563 · Cited by 2 · see citing works
Bosdou, J. Κ., Venetis, C. A., Anagnostis, P. G., Savvaidou, D., Chatzimeletiou, K., Zepiridis, L. I., Goulis, D. G., Grimbizis, G., & Kolibianakis, E. M. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26041656 · Cited by 2 · see citing works
Paquette, A., Cavaneau, E., Haimbaugh, A. S., Meyer, D. N., Akemann, C., Dennis, N. M., & Baker, T. R. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26146839 · Cited by 2 · see citing works
Campos, A. H. A. D. S. B. E., Dias, J. S., Lopes, G. F., Pires, T. M., da Silva, D. C., Ruiz, T. F. R., Martins, T. M. M., & Perez, A. P. D. S. (2025) · Histochemistry and Cell Biology · doi:10.1007/s00418-025-02389-y · Cited by 1 · see citing works
Zhao, Y., Xu, J., Liu, C., Chen, J., Deng, M., Fan, Q., & Zhao, X. (2025) · Placenta · doi:10.1016/j.placenta.2025.07.073 · Cited by 1 · see citing works
Pei, Z., Deng, K., Cao, H., Ding, Z., Xu, C., & Zhang, S. (2026) · Journal of Ovarian Research · doi:10.1186/s13048-026-02023-y · Cited by 1 · see citing works
Zhang, Y., Hu, Y., Xu, Y., Kuai, Y., Wang, S., & Yu, J. (2026) · PeerJ · doi:10.7717/peerj.21194 · Cited by 1 · see citing works
Marijančević, D., Goreta, S., Bokulić, A., & Zec, I. (2023) · Biochemia Medica · doi:10.11613/bm.2023.020706 · Cited by 1 · see citing works
Garashova, M. A., Əliyeva, E. M., & Məmmədova, L. C. (2024) · Azerbajdžanskij medicinskij žurnal · doi:10.34921/amj.2024.3.007 · Cited by 1 · see citing works
IVF Protocols: Past, Present, and Future
Hizkiyahu, R., & Kadour‐Peero, E. (2025) · Springer eBooks · doi:10.1007/978-3-031-77255-9_6 · Cited by 1 · see citing works
Introduction to Biological and Psychobiological Aspects of PCOS
Barry, J. A. (2019) · Springer eBooks · doi:10.1007/978-3-030-30290-0_1 · Cited by 1 · see citing works
Simultaneous alterations in ovaries and bone as a result of Polycystic Ovary Syndrome
Bonfá, A. L. D. O., Alves, E. D., Fabrício, V., Nonaka, K. O., Anselmo-Franci, J. A., Achcar, J. A., & Montrezor, L. H. (2021) · International Journal of Advances in Medical Biotechnology - IJAMB · doi:10.25061/ijamb.v3i2.81 · Cited by 1 · see citing works
Simultaneous alterations in ovaries and bone as a result of Polycystic Ovary Syndrome
Bonfá, A. L. D. O., Alves, E. D., Fabrício, V., Nonaka, K. O., Anselmo-Franci, J. A., Achcar, J. A., & Montrezor, L. H. (2021) · International Journal of Advances in Medical Biotechnology - IJAMB · doi:10.52466/ijamb.v3i2.81 · Cited by 1 · see citing works
Salehi, R., Wyse, B. A., Asare-Werehene, M., Esfandiarinezhad, F., Abedini, A., Pan, B., Urata, Y., Gutsol, A. A., Viñas, J. L., Jahangiri, S., et al. (2023) · Research Square · doi:10.21203/rs.3.rs-2599745/v1 · Cited by 1 · see citing works
Long, Y., Long, X., Zhao, Y., Zhao, F., Tu, W., Yang, Q., Qian, J., Zhai, J., Wang, M., Hu, Y., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.14.553309 · Cited by 1 · see citing works
Impact of Testosterone on Aspects of Psychology
Barry, J. A. (2019) · Springer eBooks · doi:10.1007/978-3-030-30290-0_4
- Authors
- Astapova, O., Minor, B. M. N., & Hammes, S. R.
- Affiliations
- University of Rochester Medicine (US)
- Corresponding author
- Hammes, Stephen R
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2019-03-26
- Volume
- 160
- Issue
- 5
- Pages
- 1166-1174
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- PMC
- PMC6937455
- OpenAlex
- W2923411756
- Cited by
- 133
- References
- 70
- Citations by year
- 2026: 9 · 2025: 17 · 2024: 30 · 2023: 26 · 2022: 21 · 2021: 18 · 2020: 10 · 2019: 2
- FWCI
- 1.80
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Endocrinology (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Department of Health (F32HD097939-01)
- National Institutes of Health
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Keywords
- androgens, androgen receptor, ovary, folliculogenesis, ovulation, ovarian steroidogenesis, menstrual cycle, diminished ovarian reserve, polycystic ovary syndrome, hyperandrogenism, theca cells, granulosa cells, oocytes, anovulatory infertility, reproductive health
- MeSH terms
- Androgens, Animals, Female, Ovarian Follicle, Granulosa Cells, Humans, Receptors, Androgen, Theca Cells, Gene Expression, Mice, Knockout
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