The DOI matches its Crossref record; 34 of the 34 references it cites were found in a registry or an index.
Androgens stimulate early stages of follicular growth in the primate ovary
Open accessAbstract
The concept that androgens are atretogenic, derived from murine ovary studies, is difficult to reconcile with the fact that hyperandrogenic women have more developing follicles than normal-cycling women. To evaluate androgen's effects on primate follicular growth and survival, normal-cycling rhesus monkeys were treated with placebo-, testosterone-(T), or dihydrotestosterone-sustained release implants, and ovaries were taken for histological analysis after 3-10 d of treatment. Growing preantral and small antral follicles up to 1 mm in diameter were significantly and progressively increased in number and thecal layer thickness in T-treated monkeys from 3-10 d. Granulosa and thecal cell proliferation, as determined by immunodetection of the Ki67 antigen, were significantly increased in these follicles. Preovulatory follicles (> 1 mm), however, were not increased in number in androgen-treated animals. Follicular atresia was not increased and there were actually significantly fewer apoptotic granulosa cells in the T-treated groups. Dihydrotestosterone treatment had identical effects, indicating that these growth-promoting actions are mediated by the androgen receptor. These findings show that, over the short term at least, androgens are not atretogenic and actually enhance follicular growth and survival in the primate. These new data provide a plausible explanation for the pathogenesis of "polycystic" ovaries in hyperandrogenism.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The text we found for this paper looks like another document, so the self-check wasn’t run.
Citations
Cites
Regulation of ovarian follicular development in primates: facts and hypotheses
GOUGEON, A. (1996) · Endocrine Reviews · doi:10.1210/edrv-17-2-121 · Cited by 1,497
Gerdes, J., Li, L., Schlueter, C. J., Duchrow, M., Wohlenberg, C., Gerlach, C., Stahmer, I., Kloth, S., Brandt, E., & Flad, H. D. (1991) · PubMed Central · Cited by 894
Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis.
Billig, H., Furuta, I., & Hsueh, A. J. W. (1993) · Endocrinology · doi:10.1210/endo.133.5.8404672 · Cited by 556
Morphology and Morphogenesis of the Stein-Leventhal Ovary and of So-called “Hyperthecosis”
Hughesdon, P. E. (1982) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-198202000-00001 · Cited by 429
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
Self-citationSchmitz, G. G., Walter, T., Seibl, R., & Keßler, C. (1991) · Analytical Biochemistry · doi:10.1016/0003-2697(91)90212-c · Cited by 318
MacDougall, M. J., Tan, S. L., Balen, A. H., & Jacobs, H. S. (1993) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a138029 · Cited by 240
Dunaif, A. E. (1995) · The American Journal of Medicine · doi:10.1016/s0002-9343(99)80057-6 · Cited by 235
Spinder, T., Spijkstra, J. J., van den Tweel, J. G., Burger, C. W., van Kessel, H. I., Hompes, P. G. A., & Gooren, L. J. (1989) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-69-1-151 · Cited by 206
Pache, T. D., Chadha, S., Gooren, L. J., Hop, W. C. J., JAARSMA, K. W., Dommerholt, H. B. R., & Fauser, B. C. J. M. (1991) · Histopathology · doi:10.1111/j.1365-2559.1991.tb00235.x · Cited by 194
Histopathological Effects of Exogenously Administered Testosterone in 19 Female to Male Transsexuals
Futterweit, W., & Deligdisch, L. (1986) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-62-1-16 · Cited by 194
Hormonal Effects of Flutamide in Young Women with Polycystic Ovary Syndrome
Leo, V. D., Lanzetta, D., D’Antona, D., Marca, A. L., & Morgante, G. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.1.4500 · Cited by 192
Wallach, E. E., Donesky, B. W., & Adashi, E. Y. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57408-1 · Cited by 170
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
Hillier, S. G., & Ross, G. T. (1979) · Biology of Reproduction · doi:10.1095/biolreprod20.2.261 · Cited by 144
Regulation of ovarian follicular development in primates: facts and hypotheses
Gougeon, A. (1996) · Endocrine Reviews · doi:10.1210/er.17.2.121 · Cited by 134
Hild-Petito, S. A., West, N. B., Brenner, R., & Stouffer, R. L. (1991) · Biology of Reproduction · doi:10.1095/biolreprod44.3.561 · Cited by 96
DIRECT ACTION OF ESTROGEN ON THE OVARY OF THE IMMATURE RAT1
Bradbury, J. T. (1961) · Endocrinology · doi:10.1210/endo-68-1-115 · Cited by 83
van der Meer, M., Hompes, P. G. A., de Boer, J. A. M., Schats, R., & Schoemaker, J. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.2.4585 · Cited by 83
Polycystic ovary syndrome: pathophysiology and outcome with in vitro fertilization
Wallach, E. E., Buyalos, R. P., & Lee, C. T. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58017-0 · Cited by 82
Takayama, K., Fukaya, T., Sasano, H., Funayama, Y., Suzuki, T., Takaya, R., Wada, Y., & Yajima, A. (1996) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a019405 · Cited by 76
Dunaif, A. E., Scully, R. E., Andersen, R. N., Chapin, D. S., & Crowley, W. F. (1984) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-59-3-389 · Cited by 71
Transvaginal sonography and abnormal ovarian appearance in menstrual cycle disturbances
Pache, T. D., Hop, W. C. J., Wladimiroff, J. W., Schipper, J., & Fauser, B. C. J. M. (1991) · Ultrasound in Medicine & Biology · doi:10.1016/0301-5629(91)90029-v · Cited by 65
Pache, T. D., Hop, W. C. J., de Jong, F. H., Leerentveld, R. A., van Geldorp, H. J., de Kamp, T. M. M. V., Gooren, L. J., & Fauser, B. C. J. M. (1992) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1992.tb02266.x · Cited by 64
Erickson, G. F., & YEN, S. C. C. (1984) · Seminars in Reproductive Medicine · doi:10.1055/s-2008-1068381 · Cited by 58
IN VITRO PRODUCTION OF ANDROGENS BY A VIRILIZING ADRENAL ADENOMA AND ASSOCIATED POLYCYSTIC OVARIES
KASE, N. G., Kowal, J., Perloff, W. H., & Soffer, L. J. (1963) · European Journal of Endocrinology · doi:10.1530/acta.0.0440015 · Cited by 47
Koering, M. J., Danforth, D. R., & Hodgen, G. D. (1994) · Biology of Reproduction · doi:10.1095/biolreprod50.3.686 · Cited by 40
Androgens in the Ovarian Microenvironment
Daniel, S. A. J., & Armstrong, D. T. (1986) · Seminars in Reproductive Medicine · doi:10.1055/s-2007-1022489 · Cited by 39
Role and site of estrogen action in follicular atresia
Dierschke, D. J., Chaffin, C. L., & Hutz, R. J. (1994) · Trends in Endocrinology and Metabolism · doi:10.1016/1043-2760(94)90080-9 · Cited by 25
Effects of long‐term testosterone exposure on ovarian function and morphology in the rhesus monkey
Faiman, C., Reyes, F. I., Dent, D. W., Fuller, G. B., Hobson, W. C., & Thliveris, J. A. (1988) · The Anatomical Record · doi:10.1002/ar.1092220305 · Cited by 17
Steroid receptors and action in the primate follicle
Zelinski, M. B., & Stouffer, R. L. (1996) · Trends in Endocrinology and Metabolism · doi:10.1016/1043-2760(96)00061-6 · Cited by 17
Effects of Local Steroids on Follicular Development and Atresia in the Rabbit
Wallach, E. E., & Noriega, C. (1970) · Fertility and Sterility · doi:10.1016/s0015-0282(16)37393-9 · Cited by 15
Ovarian Weight Response to Varying Doses of Estrogens in Intact and Hypophysectomized Rats.
Smith, B. D., & Bradbury, J. T. (1961) · Experimental Biology and Medicine · doi:10.3181/00379727-107-26805 · Cited by 13
Histopathological Effects of Exogenously Administered Testosterone in 19 Female to Male Transsexuals
Futterweit, W., & Deligdisch, L. (1986) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-198609000-00017 · Cited by 7
Flagged first, then by citations
Cited by
Sorted by citations
Initial and cyclic recruitment of ovarian follicles
McGee, E. A., & Hsueh, A. J. W. (2000) · Endocrine Reviews · doi:10.1210/edrv.21.2.0394 · Cited by 1,771
Rosenfield, R. L., & Ehrmann, D. A. (2016) · Endocrine Reviews · doi:10.1210/er.2015-1104 · Cited by 1,603
Norman, R. J., Dewailly, D., Legro, R. S., & Hickey, T. E. (2007) · The Lancet · doi:10.1016/s0140-6736(07)61345-2 · Cited by 1,360
Franks, S. (1997) · Archives of Disease in Childhood · doi:10.1136/adc.77.1.89 · Cited by 802
Anti-Mullerian hormone: a new marker for ovarian function
Visser, J. A., de Jong, F. H., Laven, J. S. E., & Themmen, A. P. N. (2005) · Reproduction · doi:10.1530/rep.1.00529 · Cited by 801
Metadata
- Authors
- Vendola, K. A., Zhou, J., Adesanya, O. O., Weil, S. J., & Bondy, C. A.
- Affiliations
- National Institutes of Health (US)
- ORCID
- Zhou, J
- Venue
- Journal of Clinical Investigation
- Published
- 1998-06-15
- Volume
- 101
- Issue
- 12
- Pages
- 2622-2629
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC508852
- OpenAlex
- W2114124243
- Cited by
- 712
- References
- 33
- Citations by year
- 2026: 12 · 2025: 10 · 2024: 19 · 2023: 17 · 2022: 22 · 2021: 44 · 2020: 24 · 2019: 33 · 2018: 31 · 2017: 61 · 2016: 26 · 2015: 51 · 2014: 38 · 2013: 40 · 2012: 40
- FWCI
- 7.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Reproductive Physiology in Livestock
- Keywords
- androgens, folliculogenesis, follicular atresia, rhesus monkeys, testosterone, dihydrotestosterone, androgen receptor, granulosa cell proliferation, Ki-67, apoptosis, preantral follicles, polycystic ovary syndrome, hyperandrogenism, ovary
- MeSH terms
- Androgens, Animals, Cell Count, Cell Division, Female, Ovarian Follicle, Macaca mulatta, Organ Size, Ovary, Cell Death
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