Steroids in the follicular fluid and the corpus luteum of the mare. A “two-cell type” theory of ovarian steroid synthesis

SHORT, R. V.

doi:10.1677/joe.0.0240059

Cited by 176Reproductive Physiology in LivestockOvarian function and disordersEstrogen and related hormone effects

Steroids in the follicular fluid and the corpus luteum of the mare. A “two-cell type” theory of ovarian steroid synthesis

SHORT, R. V.·1962·Journal of Endocrinology

DOI 10.1677/joe.0.0240059

Open this paper in CoChat — free account

Abstract

SUMMARY A comparison has been made between the steroids present in equine follicular fluid and luteal tissue. Follicular fluid was found to contain progesterone, 17α-hydroxyprogesterone, androstenedione, epitestosterone, 19-norandrostenedione, oestrone, oestradiol-17β and 6α-hydroxyoestradiol-17β, in confirmation of previous studies. On the other hand, luteal tissue contained large amounts of progesterone and 20α-hydroxypregn-4-en-3-one, and a small quantity of 17α-hydroxyprogesterone. No C18 or C19 steroids could be detected. These findings are therefore interpreted as evidence in favour of a 'two-cell type' theory of steroid formation in the ovary. One type, possibly the theca interna cell, has the ability to convert progesterone into oestrogens; the other type, possibly the luteinized granulosa cell, has a diminished 17-hydroxylating ability and is unable to cleave the C21 side chain to make C18 and C19 steroids. However, it does have an active 20-reductase enzyme system present.

Integrity signals

Registry

Crossref · 10.1677/joe.0.0240059

Cites

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Ovarian steroid output varies considerably during menstrual cycle - 17β-estradiol is primary steroid produced during follicular phase, while progesterone is principal steroid during luteal phase.
“Ovarian steroid output varies considerably during the course of the menstrual cycle – 17β-estradiol is the primary steroid produced during the follicular phase, while progesterone is the principal steroid during the luteal phase [[77], [78], [79]].”
From Human steroid biosynthesis, metabolism and excretion are differentially reflected by serum and urine steroid metabolomes: a comprehensive review (2019) · cites this paper as [77]

Sorted by citations

Establishment and Characterization of a Steroidogenic Human Granulosa-Like Tumor Cell Line, KGN, That Expresses Functional Follicle-Stimulating Hormone Receptor
Nishi, Y., Yanase, T., Yi-ming, M., Oba, K., Ichino, I., Saito, M., Nomura, M., Mukasa, C., Okabe, T., Goto, K., et al. (2001) · Endocrinology · doi:10.1210/endo.142.1.7862 · Cited by 596 · see citing works
Manipulation of Human Ovarian Function: Physiological Concepts and Clinical Consequences*
Fauser, B. C. J. M., & van Heusden, A. M. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.1.0290 · Cited by 509 · see citing works
Follicular oestrogen synthesis: the ‘two-cell, two-gonadotrophin’ model revisited
Hillier, S. G., Whitelaw, P. F., & Smyth, C. D. (1994) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(94)90278-x · Cited by 456 · see citing works
Human steroid biosynthesis, metabolism and excretion are differentially reflected by serum and urine steroid metabolomes: a comprehensive review
Schiffer, L., Barnard, L., Baranowski, E. S., Gilligan, L. C., Taylor, A. E., Arlt, W., Shackleton, C. H. L., & Storbeck, K.-H. (2019) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2019.105439 · Cited by 450 · see citing works
Insulin-Like Growth Factor I and Insulin Potentiate Luteinizing Hormone-Induced Androgen Synthesis by Rat Ovarian Thecal-Interstitial Cells*
Cara, J. F., & Rosenfield, R. L. (1988) · Endocrinology · doi:10.1210/endo-123-2-733 · Cited by 333 · see citing works
Stimulation of Ovarian Follicular Maturation With Pure Follicle-Stimulating Hormone in Women with Gonadotropin Deficiency
Couzinet, B., Lestrat, N., Brailly, S., Forest, M. G., & SCHAISON, G. (1988) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-66-3-552 · Cited by 169 · see citing works
Results of ovulation induction using human menopausal gonadotropin or purified follicle-stimulating hormone in hypogonadotropic hypogonadism patients
Shoham, Z., Balen, A. H., Patel, A. K., & Jacobs, H. S. (1991) · Fertility and Sterility · doi:10.1016/s0015-0282(16)54715-3 · Cited by 170 · see citing works
Luteinizing hormone: its role, mechanism of action, and detrimental effects when hypersecreted during the follicular phase
Shoham, Z., Jacobs, H. S., & Insler, V. (1993) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55968-8 · Cited by 158 · see citing works
Recombinant Luteinizing Hormone (rLH) for controlled ovarian hyperstimulation in assisted reproductive cycles
Mochtar, M. H., van der Veen, F., Ziech, M. L. W., van Wely, M., & Musters, A. M. (2007) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd005070.pub2 · Cited by 160 · see citing works
Human menopausal gonadotropin versus recombinant follicle-stimulating hormone in normogonadotropic women down-regulated with a gonadotropin-releasing hormone agonist who were undergoing in vitro fertilization and intracytoplasmic sperm injection: a prospective randomized study
Westergaard, L. G., Erb, K., Laursen, S. B., Rex, S., & Rasmussen, P. E. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01973-2 · Cited by 150 · see citing works
Old yellow enzyme: Aromatization of cyclic enones and the mechanism of a novel dismutation reaction
Vaz, A. D. N., Chakraborty, S., & Massey, V. (1995) · Biochemistry · doi:10.1021/bi00013a014 · Cited by 151 · see citing works
17β-Estradiol Biosynthesis in Cultured Granulosa and Thecal Cells of Human Ovarian Follicles: Stimulation by Follicle-Stimulating Hormone*
Moon, Y. S., Tsang, B. K., SIMPSON, C., & Armstrong, D. T. (1978) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-47-2-263 · Cited by 144 · see citing works
Recombinant human LH supplementation during GnRH antagonist administration in IVF/ICSI cycles: a prospective randomized study
Cédrin‐Durnerin, I. (2004) · Human Reproduction · doi:10.1093/humrep/deh369 · Cited by 130 · see citing works
“These data confirm the key role of LH to ensure adequate steroidogenesis and are consistent with the two gonadotrophins–two cells theory (Short, 1962).”
Result
Fine structure of the human menstrual corpus luteum at its stage of maximum secretory activity,
Gillim, S. W., Christensen, A., & McLennan, C. E. (1969) · American Journal of Anatomy · doi:10.1002/aja.1001260403 · Cited by 123 · see citing works
A macrophage and theca cell-enriched stromal cell population influences growth and survival of immature murine follicles in vitro
Tingen, C. M., Kiesewetter, S. E., Jozefik, J. K., Thomas, C., Tagler, D., Shea, L. D., & Woodruff, T. K. (2011) · Reproduction · doi:10.1530/rep-10-0483 · Cited by 125 · see citing works
“Androgens can be aromatized to estrogens by the mature granulosa cells (Short 1962, Liu & Hsueh 1986); androgens have been shown to have a positive effect on follicle growth in mice, cows, and non-human primates (Murray et al. 1998, Vendola et al. 1998, Yang & Fortune 2006).”
Background
The fine structure of the human corpus luteum of early pregnancy and during the progestational phase of the menstrual cycle
Crisp, T. M., Dessouky, D. A., & Denys, F. R. (1970) · American Journal of Anatomy · doi:10.1002/aja.1001270105 · Cited by 120 · see citing works
Synergism between Granulosa and Theca-Interstitial Cells in Estrogen Biosynthesis by Gonadotropin-Treated Rat Ovaries: Studies on the Two-Cell, Two-Gonadotropin Hypothesis Using Steroid Antisera1
Liu, Y., & Hsueh, A. J. W. (1986) · Biology of Reproduction · doi:10.1095/biolreprod35.1.27 · Cited by 118 · see citing works
Anti-Müllerian hormone and anti-Müllerian hormone type II receptor polymorphisms are associated with follicular phase estradiol levels in normo-ovulatory women
Kevenaar, M. E., Themmen, A. P. N., Laven, J. S. E., Sonntag, B., Fong, S. L., Uitterlinden, A. G., de Jong, F. H., Pols, H. A. P., Simoni, M., & Visser, J. A. (2007) · Human Reproduction · doi:10.1093/humrep/dem036 · Cited by 120 · see citing works
“Under the influence of FSH, a significant increase in aromatase activity occurs in this dominant follicle, resulting in the conversion of theca cell-derived androgens into estrogens (Short, 1962; Hillier et al., 1981; van Santbrink et al., 1995; van Dessel et al., 1996; Macklon and Fauser, 2001).”
Background
Recombinant luteinizing hormone (rLH) and recombinant follicle stimulating hormone (rFSH) for ovarian stimulation in IVF/ICSI cycles
Mochtar, M. H., Danhof, N. A., Ayeleke, R. O., van der Veen, F., & van Wely, M. (2017) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd005070.pub3 · Cited by 115 · see citing works
Recombinant Follicle-Stimulating Hormone Induces Ovulation and Tissue Plasminogen Activator Expression in Hypophysectomized Rats*
Galway, A., LaPolt, P. S., TSAFRIRI, A., et al. (1990) · Endocrinology · doi:10.1210/endo-127-6-3023 · Cited by 103 · see citing works
Medical hypophysectomy: II. Variability of ovarian response to gonadotropin therapy
Kenigsberg, D., Littman, B. A., Williams, R. F., et al. (1984) · Fertility and Sterility · doi:10.1016/s0015-0282(16)47969-0 · Cited by 97 · see citing works
Role of periovulatory luteinizing hormone concentrations during assisted reproductive technology cycles stimulated exclusively with recombinant follicle- stimulating hormone
Esposito, M. A., Barnhart, K. T., Coutifaris, C., & Patrizio, P. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01745-3 · Cited by 94 · see citing works
Follicle-Stimulating Hormone and Advanced Follicle Development in the Human
Macklon, N., & Fauser, B. C. J. M. (2001) · Archives of Medical Research · doi:10.1016/s0188-4409(01)00327-7 · Cited by 95 · see citing works
A quantitative cytochemical study of glucose-6-phosphate dehydrogenase and ? 5-3?-hydroxysteroid dehydrogenase activity in the Membrana granulosa of the ovulable type of follicle of the rat
Zoller, L. C., & Weisz, J. (1979) · Histochemistry and Cell Biology · doi:10.1007/bf00493314 · Cited by 91 · see citing works
“Furthermore, the contribution of the granulosa cells of the preovulatory follicle to this preovulatory estrogen surge is thought to be the aromatization of C19 steroid precursors produced by the theca (Falck, 1959; Short, 1962; Makris and Ryan, 1975; Fortune and Armstrong, 1978).”
Background
Rescue of IVF cycles by HMG in pituitary down-regulated normogonadotrophic young women characterized by a poor initial response to recombinant FSH
Placido, G. D., Mollo, A., Alviggi, C., Strina, I., Varricchio, M. T., Ranieri, A., Colacurci, N., Tolino, A., & Wilding, M. (2001) · Human Reproduction · doi:10.1093/humrep/16.9.1875 · Cited by 90 · see citing works
“Theories of human folliculogenesis classically follow the two cell, two gonadotrophin theory which suggests that both FSH and LH are required for folliculogenesis in humans (Fevold, 1941; Short, 1962; Filicori, 1999; Lèvy et al., 2000).”
Background
Effect of testosterone and dibutyryl cAMP on the spontaneous maturation of pig oocytes
Rice, C., & McGaughey, R. W. (1981) · Reproduction · doi:10.1530/jrf.0.0620245 · Cited by 90 · see citing works
The role of LH in ovarian stimulation: Exogenous LH: let's design the future
Lévy, D. (2000) · Human Reproduction · doi:10.1093/humrep/15.11.2258 · Cited by 86 · see citing works
“The pharmacology of ovarian stimulation has been influenced by the 2-cell, two-gonadotrophin theory (Figure 1) (Fevold, 1941; Short, 1962) and, historically, follicular stimulation protocols have included both LH and FSH in an attempt to mimic the normal physiology of folliculogenesis.”
Background
Formation and maintenance of corpora lutea in laboratory animals.
Greenwald, G. S., & ROTHCHILD, I. (1968) · PubMed · Cited by 84 · see citing works
Rainbow trout cytochrome P‐450c17 (17α‐hydroxylase/17,20‐lyase) cDNA cloning, enzymatic properties and temporal pattern of ovarian P‐450c17 mRNA expression during oogenesis
Sakai, N., Tanaka, M., Adachi, S., Miller, W. L., & Nagahama, Y. (1992) · FEBS Letters · doi:10.1016/0014-5793(92)80210-8 · Cited by 82 · see citing works
Effects of recombinant LH (rLH) supplementation during controlled ovarian hyperstimulation (COH) in normogonadotrophic women with an initial inadequate response to recombinant FSH (rFSH) after pituitary downregulation
Placido, G. D., Alviggi, C., Mollo, A., Strina, I., Ranieri, A., Alviggi, E., Wilding, M., Varricchio, M. T., Borrelli, A. L., & Conforti, S. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02027.x · Cited by 81 · see citing works
“According to the two-cell, two-gonadotrophin theory, both FSH and LH are required for folliculogenesis in humans (Fevold, 1941; Short, 1962; Filicori, 1999; Lèvy et al ., 2000).”
Background
In vitro fertilization as a diagnostic and therapeutic tool in a patient with partial 17,20-desmolase deficiency
Pellicer, A., Miró, F., Sampaio, M., Gómez, E., & Bonilla-Musoles, F. M. (1991) · Fertility and Sterility · doi:10.1016/s0015-0282(16)54308-8 · Cited by 81 · see citing works
Estrogen biosynthesis—regulation, action, remote effects, and value of monitoring in ovarian stimulation cycles
Wallach, E. E., Shoham, Z., & Schachter, M. E. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58197-7 · Cited by 76 · see citing works
Induction of follicular growth using recombinant human follicle-stimulating hormone in two volunteer women with hypogonadotropic hypogonadism
Shoham, Z., Mannaerts, B. M. J. L., Insler, V., et al. (1993) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55852-x · Cited by 74 · see citing works
Expression of insulin-like growth factor (IGF), IGF-binding protein, and IGF receptor messenger ribonucleic acids in normal and polycystic ovaries.
Voutilainen, R., Franks, S., Mason, H. D., et al. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.3.8772565 · Cited by 74 · see citing works
A prospective, randomized comparison of ovulation induction using highly purified follicle-stimulating hormone alone and with recombinant human luteinizing hormone in in-vitro fertilization
Sills, E. S., Lévy, D., Moomjy, M., et al. (1999) · Human Reproduction · doi:10.1093/humrep/14.9.2230 · Cited by 73 · see citing works
Combined assessment of polymorphisms in theLHCGRandFSHRgenes predict chance of pregnancy afterin vitrofertilization
Lindgren, I., Bååth, M., Uvebrant, K., et al. (2016) · Human Reproduction · doi:10.1093/humrep/dev342 · Cited by 70 · see citing works
Steroid Biosynthesis by Isolated Human Ovarian Follicular Cells in Vitro*
Tsang, B. K., Armstrong, D. T., & Whitfield, J. F. (1980) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-51-6-1407 · Cited by 69 · see citing works
Follicular development induced by recombinant luteinizing hormone (LH) and follicle-stimulating hormone (FSH) in anovulatory women with LH and FSH deficiency: evidence of a threshold effect
O'Dea, L. S. L., O’Brien, F., Currie, K., et al. (2008) · Current Medical Research and Opinion · doi:10.1185/03007990802374815 · Cited by 60 · see citing works
Intraovarian mechanisms in the hormonal control of granulosa cell differentiation in rats
Hsueh, A. J. W., Jones, P., Adashi, E. Y., et al. (1983) · Reproduction · doi:10.1530/jrf.0.0690325 · Cited by 59 · see citing works
“…(Simpson, Li & Evans, 1951), as well as the participation of the two ovarian cell types (theca and granulosa; Falck, 1959), a 2-cell-2-gonadotrophin hypothesis has been formulated to explain the mechanism of oestrogen production (Short, 1962; Baird, 1977; Moor, 1977; Dorrington & Armstrong, 1979).”
Background
The Corpus Luteum and Steroid Hormone Formation
Huang, W. Y., & Pearlman, W. H. (1962) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)60284-4 · Cited by 59 · see citing works
Cycle changes in antral fluid hormone concentrations in humans
McNatty, K. P. (1978) · Clinics in Endocrinology and Metabolism · doi:10.1016/s0300-595x(78)80010-3 · Cited by 57 · see citing works
Differential production of steroids by dispersed granulosa and theca interna cells from developing preovulatory follicles of pigs
Tsang, B. K., AINSWORTH, L., Downey, B. R., et al. (1985) · Reproduction · doi:10.1530/jrf.0.0740459 · Cited by 57 · see citing works
BIOSYNTHESIS OF STEROIDS BY GRANULOSA CELLS OF THE PORCINE OVARY IN VITRO
Bjersing, L., & CARSTENSEN, H. (1967) · Reproduction · doi:10.1530/jrf.0.0140101 · Cited by 56 · see citing works
Review on crosstalk and common mechanisms of endocrine disruptors: Scaffolding to improve PBPK/PD model of EDC mixture
Sharma, R. P., Schuhmacher, M., & Kumar, V. (2016) · Environment International · doi:10.1016/j.envint.2016.09.016 · Cited by 53 · see citing works
“, 1982), and induces aromatase activity in the granulosa cells, which results inmore estradiol level (Short, 1962; Richards et al., 1976; Hillier et al., 1981).”
Reciprocal expression of 17α-hydroxylase-C17,20-lyase and aromatase cytochrome P450 during bovine trophoblast differentiation: a two-cell system drives placental oestrogen synthesis
Schuler, G. C., ÖZALP, G. R., Hoffmann, B., Harada, N., Browne, P., & Conley, A. J. (2006) · Reproduction · doi:10.1530/rep.1.01033 · Cited by 53 · see citing works
Induction of follicular growth using recombinant human follicle-stimulating hormone in two volunteer women with hypogonadotropic hypogonadism
Shoham, Z., Mannaerts, B. M. J. L., Insler, V., et al. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00517-7 · Cited by 53 · see citing works
Plasma progesterone in snakes
Chan, S. W. C., Ziegel, S., & Callard, I. P. (1973) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(73)90514-8 · Cited by 53 · see citing works
Bone Morphogenetic Protein Inhibits Ovarian Androgen Production
Dooley, C. A., Attia, G. R., Rainey, W. E., et al. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.9.6835 · Cited by 52 · see citing works
“This allows follicular thecal cells to secrete and provide 19 carbon (C19) steroids to the adjacent granulosa cells, for conversion to estrogens ( 1 , 2). Thus, the regulation of C19 steroid production in the thecal cell is a key component of estrogen biosynthesis.”
Background
LH in the follicular phase: neither too high nor too low
Balasch, J., & Fábregues, F. (2006) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)61991-8 · Cited by 51 · see citing works
Aromatase activity of isolated and recombined hamster granulosa cells and theca
Makris, A., & Ryan, K. J. (1977) · Steroids · doi:10.1016/0039-128x(77)90109-x · Cited by 49 · see citing works
Ovarian Hyperstimulation for Successful in Vitro Fertilization and Embryo Transfer
GRONOW, M. J. (1985) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016348509156384 · Cited by 49 · see citing works
Dynamics of the development of multiple follicles during ovarian stimulation for in vitro fertilization using recombinant follicle-stimulating hormone (Puregon) and various doses of the gonadotropin-releasing hormone antagonist ganirelix (Orgalutran/Antagon)
Jong, D. D., Macklon, N. S., Eijkemans, M. J. C., Mannaerts, B. M. J. L., Bennink, H. J. T. C., & Fauser, B. C. J. M. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01789-1 · Cited by 49 · see citing works
Estrogen 2-, 4-, 6- or 16-hydroxylation by human follicles shown by gas chromatography-mass spectrometry associated with stable isotope dilution
Dehennin, L., Blacker, C., Reiffsteck, A., et al. (1984) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(84)90255-3 · Cited by 49 · see citing works
The biosynthesis of estrogens by cow follicles
Lacroix, E. (1974) · Steroids · doi:10.1016/0039-128x(74)90086-5 · Cited by 46 · see citing works
Regulation of Microsomal P450, Redox Partner Proteins, and Steroidogenesis in the Developing Testes of the Neonatal Pig
Moran, F. M., Ford, J. J., Corbin, C. J., Mapes, S. M., Njar, V. C. O., Brodie, A. M., & Conley, A. J. (2002) · Endocrinology · doi:10.1210/en.2002-220329 · Cited by 44 · see citing works
Progestagen, androgen and oestrogen levels in plasma and ovarian follicular fluid during the oestrous cycle of the mare
Meinecke, B., Gips, H., & Meinecke‐Tillmann, S. (1987) · Animal Reproduction Science · doi:10.1016/0378-4320(87)90097-2 · Cited by 44 · see citing works
“Concentrations of E1 and E2 found in the follicular fluid (Table 2) are in agreement with those published earlier (Knudsen and Velle, 1961; Short, 1962; YoungLai, 1971; Bjersing and YoungLai, 1972; Kenney et al., 1979).”
BackgroundResult
Granulosa-thecal cell interaction in ovarian steroidogenesis
Ryan, K. J. (1979) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(79)90014-1 · Cited by 43 · see citing works
Aromatization of 19-norandrogens by equine testicular microsomes.
Gaillard, J., & Silberzahn, P. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)45634-7 · Cited by 43 · see citing works
The androgenic ovary, with special reference to the Stein-Leventhal syndrome
Jeffcoate, T. N. A. (1964) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(64)90248-0 · Cited by 42 · see citing works
A subovarian exchange mechanism for the countercurrent transfer of ovarian steroid hormones in the pig
Krzymowski, T., Kotwica, J., Stefańczyk, S., et al. (1982) · Reproduction · doi:10.1530/jrf.0.0650457 · Cited by 41 · see citing works
The cAMP/PKA pathway: steroidogenesis of the antral follicular stage
Riccetti, L., Sperduti, S., Lazzaretti, C., Casarini, L., & Simoni, M. (2018) · Minerva Obstetrics and Gynecology · doi:10.23736/s0026-4784.18.04282-x · Cited by 40 · see citing works
Nuclear receptors: Key regulators of somatic cell functions in the ovulatory process
Hughes, C. H. K., & Murphy, B. D. (2020) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2020.100937 · Cited by 40 · see citing works
Gas Chromatography-Mass Spectrometry of Androgens in Equine Ovarian Follicles at Ultrastructurally Defined Stages of Development. Identification of 19-Nortestosterone in Follicular Fluid
Silberzahn, P., Dehennin, L., Zwain, I. H., et al. (1985) · Endocrinology · doi:10.1210/endo-117-5-2176 · Cited by 40 · see citing works
Factors that predict the probability of a successful clinical outcome after induction of oocyte maturation with a gonadotropin-releasing hormone agonist
Kummer, N., Benadiva, C. A., Feinn, R., et al. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.04.050 · Cited by 38 · see citing works
Endocrine regulation of reproduction in elasmobranchs: Archetype for terrestrial vertebrates
Callard, I. P., Klosterman, L. L., Sorbera, L. A., et al. (1989) · Journal of Experimental Zoology · doi:10.1002/jez.1402520404 · Cited by 38 · see citing works
Estrogen metabolites in equine ovarian follicles: Gas chromatographic-mass spectrometric determinations in relation to follicular ultrastructure and progestin content
Silberzahn, P., Almahbobi, G., Dehennin, L., et al. (1985) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(85)90169-4 · Cited by 38 · see citing works
Molecular Mechanism for Repression of 17α-Hydroxylase Expression and Androstenedione Production in Granulosa Cells
Patel, S. S., Beshay, V. E., Escobar, J. C., Suzuki, T., & Carr, B. R. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-1341 · Cited by 35 · see citing works
“theca cell produces androstenedione (A4) (1, 2).”
Effect of Human Pituitary-follicle-stimulating Hormone and Chorionic Gonadotrophin in Stein-Leventhal Syndrome
Crooke, A. C., BUTT, W. R., Palmer, R., et al. (1963) · BMJ · doi:10.1136/bmj.1.5338.1119 · Cited by 34 · see citing works
Self-citation
The Corpus Luteum and Steroid Hormone Formation
Huang, W. Y., & Pearlman, W. H. (1963) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)81180-2 · Cited by 34 · see citing works
British Fertility Society: ‘Ovulation induction in WHO Type 1 anovulation: Guidelines for practice’ Produced on behalf of the BFS Policy and Practice Committee
Yasmin, E., Davies, M. C., Conway, G. S., & Balen, A. H. (2013) · Human Fertility · doi:10.3109/14647273.2013.829673 · Cited by 32 · see citing works
“This observation is consistent with the 2 cell, 2 gonadotropin theory of folliculogenesis (Short, 1962).”
Result
17α-Hydroxylase (CYP17) Expression and Subsequent Androstenedione Production in the Human Ovary
Patel, S. S., Beshay, V. E., Escobar, J. C., & Carr, B. R. (2010) · Reproductive Sciences · doi:10.1177/1933719110379055 · Cited by 32 · see citing works
Selection of the Dominant Ovarian Follicle and Hormonal Enhancement of the Natural Cycle
Hodgen, G. D., KENIGSBURG, D., Collins, R. L., & Schenken, R. S. (1985) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1985.tb37502.x · Cited by 32 · see citing works
Effects of growth hormone and growth hormone-releasing hormone on steroid synthesis in cultured human luteinizing granulosa cells
Doldi, N., Bassan, M., Bonzi, V., & Ferrari, A. G. (1996) · Gynecological Endocrinology · doi:10.3109/09513599609097899 · Cited by 31 · see citing works
Estrogen and Progesterone Production by Developing Porcine Folliclesin Vitro: Evidence for Estrogen Formation by Theca*
Haney, A. F., & Schomberg, D. W. (1981) · Endocrinology · doi:10.1210/endo-109-3-971 · Cited by 30 · see citing works
Regulation of ovarian steroidogenesis in vitro in the viviparous shark, Squalus acanthias
Tsang, P. C. W., & Callard, I. P. (1992) · Journal of Experimental Zoology · doi:10.1002/jez.1402610111 · Cited by 28 · see citing works
Human ovarian tumor cells: a potential model for thecal cell steroidogenesis
Rainey, W. E. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.81.1.257 · Cited by 28 · see citing works
4 Local control of ovarian steroidogenesis
Mason, H. D., & Franks, S. (1997) · Baillière s Clinical Obstetrics and Gynaecology · doi:10.1016/s0950-3552(97)80037-5 · Cited by 26 · see citing works
Transforming growth factor β inhibits steroidogenic acute regulatory (StAR) protein expression in human ovarian thecal cells
Attia, G. R., Dooley, C. A., Rainey, W. E., & Carr, B. R. (2000) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(00)00335-x · Cited by 25 · see citing works
Correlation of serum inhibin concentrations with results in an ovarian hyperstimulation program
Tsuchiya, K., Seki, M., Itoh, M., et al. (1989) · Fertility and Sterility · doi:10.1016/s0015-0282(16)60795-1 · Cited by 25 · see citing works
Lower rate of early pregnancy loss in patients experiencing early-onset low LH in GnRH antagonist cycles supplemented with menotropin
Yang, P.-K., Wu, M., Chao, K., Chang, C., Chen, M., & Chen, S. (2018) · Journal of the Formosan Medical Association · doi:10.1016/j.jfma.2018.01.012 · Cited by 24 · see citing works
Mesenchymal-epithelial cell interactions in the ovary: estrogen-induced theca cell steroidogenesis
Roberts, A. J., & Skinner, M. K. (1990) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(90)90242-z · Cited by 24 · see citing works
Pregnancy after administration of high dose recombinant human LH alone to support final stages of follicular maturation in a woman with long-standing hypogonadotrophic hypogonadism
Balasch, J. C., & Fábregues, F. (2003) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)62162-1 · Cited by 24 · see citing works
Androgen synthesis and aromatization by equine corpus luteum microsomes
Al-Timimi, I. H., Gaillard, J., Amri, H., et al. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)83216-1 · Cited by 24 · see citing works
The effect of transforming growth factor-β on steroidogenesis and expression of key steroidogenic enzymes with a human ovarian thecal-like tumor cell model
Carr, B. R., McGee, E. A., Sawetawan, C., et al. (1996) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(96)70652-x · Cited by 22 · see citing works
Reproductive Physiology
Callard, I. P., Klosterman, L. L., & Callard, G. V. (1988) · Springer eBooks · doi:10.1007/978-3-642-73336-9_10 · Cited by 22 · see citing works
cAMP-dependent and tissue-specific expression of genes encoding steroidogenic enzymes in bovine luteal and granulosa cells in primary culture
Lauber, M., Kagawa, N., Waterman, M. R., & Simpson, E. R. (1993) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(93)90128-7 · Cited by 19 · see citing works
Steroid concentrations in follicular fluid aspirated repeatedly from transitional and cyclic mares
Bøgh, I. B., Høier, R., Synnestvedt, B., et al. (2000) · Theriogenology · doi:10.1016/s0093-691x(00)00398-8 · Cited by 21 · see citing works
Interaction and signal transduction between oocyte and samatic cells in the ovary
Liu, Y. (2006) · Frontiers in bioscience · doi:10.2741/2272 · Cited by 19 · see citing works
Developmental Changes in Steroidogenesis by Equine Preovulatory Follicles: Effects of Equine LH, FSH, and CG*
Sirois, J., Kimmich, T., & Fortune, J. E. (1990) · Endocrinology · doi:10.1210/endo-127-5-2423 · Cited by 20 · see citing works
Ovarian morphology and the concentration of steroids, and of gonadotrophins during the breeding season in ewes actively immunized against oestradiol-17β or oestrone
SCARAMUZZI, R. J., Martensz, N. D., & Look, P. F. A. V. (1980) · Reproduction · doi:10.1530/jrf.0.0590303 · Cited by 20 · see citing works
Metabolism in vitro of steroids in the canine ovary
Aakvaag, A., & Eik‐Nes, K. B. (1965) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(65)90494-0 · Cited by 20 · see citing works
Specific Cortisol Binding Protein in Porcine Follicular Fluid
Mahajan, D. K., & Little, A. B. (1978) · Biology of Reproduction · doi:10.1095/biolreprod18.5.834 · Cited by 19 · see citing works
“…2018 CORTISOL BINDING TO FOLLICULAR FLUID 835 Two hundred Ml of a 1:5 dilution of follicular fluid were incubated overnight with 1.9 pmol of tritiated been shown to contain higher concentrations of estradiol-1 7j3 and progesterone than ovarian vein blood or peripheral blood (Short, 1960, 1962).”
MethodInfluential
Effects of long-acting recombinant human follicle-stimulating hormone analogs containing N-linked glycosylation on murine folliculogenesis
Ruman, J. I., Pollak, S. V., Trousdale, R. K., et al. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.12.027 · Cited by 18 · see citing works
Die differenzierte Struktur und Funktion der Granulosa und Theka in verschiedenen Follikelstadien menschlicher Ovarien
Mestwerdt, W., M�ller, O., & Brandau, H. (1977) · Archives of Gynecology and Obstetrics · doi:10.1007/bf00667196 · Cited by 18 · see citing works
Metabolism in vitro of steroids in the canine ovary
Aakvaag, A., & Eik‐Nes, K. B. (1965) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(65)90493-9 · Cited by 18 · see citing works
Progestin‐primed ovarian stimulation with or without clomiphene citrate supplementation in normal ovulatory women undergoing in vitro fertilization/intracytoplasmic sperm injection: A prospective randomized controlled trial
Liu, Y., Chen, Q., Yu, S., Wang, Y., He, W., Chang, H. Y., Wang, B., Gao, H., Long, H., Wang, L., et al. (2017) · Clinical Endocrinology · doi:10.1111/cen.13532 · Cited by 17 · see citing works
Modulation of expression of 17-Hydroxylase/17,20 lyase (CYP17) and P450 aromatase (CYP19) by inhibition of MEK1 in a human ovarian granulosa-like tumor cell line
Huang, X. F., Jin, J., Shen, S., et al. (2015) · Gynecological Endocrinology · doi:10.3109/09513590.2015.1106470 · Cited by 16 · see citing works
Fibronectin concentrations correlate with ovarian follicular size and estradiol values in equine follicular fluid
Gentry, P. A., Zareie, M., & Liptrap, R. M. (1996) · Animal Reproduction Science · doi:10.1016/s0378-4320(96)01554-0 · Cited by 15 · see citing works
Pig Model to Study Dynamics of Steroids During Ovarian Follicular Growth and Maturation
Mahajan, D. K. (2008) · Humana Press eBooks · doi:10.1007/978-1-59745-285-4_45 · Cited by 14 · see citing works
Microvascular Endothelial Cells of the Bovine Corpus Luteum: A Comparative Examination of the Estrous Cycle and Pregnancy
CHERRY, J. A., Hou, X., Rueda, B. R., Davis, J. S., & Townson, D. H. (2008) · Journal of Reproduction and Development · doi:10.1262/jrd.19182 · Cited by 14 · see citing works

THE ROLE OF PROLACTIN IN THE REGULATION OF TESTIS FUNCTION: THE EFFECTS OF PROLACTIN AND LUTEINIZING HORMONE ON THE PLASMA LEVELS OF TESTOSTERONE AND ANDROSTENEDIONE IN HYPOPHYSECTOMIZED RATS
Hafiez, A. A., Lloyd, C. W., & Bartke, A. (1972) · Journal of Endocrinology · doi:10.1677/joe.0.0520327 · Cited by 142 · see citing works
Evidence that the Maternal Pituitary Suppresses the Secretion of Relaxin in the Pregnant Rat*
Golos, T. G., & Sherwood, O. D. (1984) · Endocrinology · doi:10.1210/endo-115-3-1004 · Cited by 9 · see citing works
Effect of exposure to long days on the secretion of oestradiol, oestrone, progesterone, testosterone, androstenedione, cortisol and follicle-stimulating hormone in intact and spayed ferrets
Donovan, B. T., Matson, C., & Kilpatrick, M. J. (1983) · Journal of Endocrinology · doi:10.1677/joe.0.0990361 · Cited by 9 · see citing works
STEROID CONCENTRATIONS IN THE FOLLICULAR FLUID OF MARES AT VARIOUS STAGES OF THE REPRODUCTIVE CYCLE
Short, R. V. (1961) · Journal of Endocrinology · doi:10.1677/joe.0.0220153 · Cited by 40 · see citing works
Self-citation
Blood flow and metabolism in the corpus luteum of the rat : in vivo and in vitro studies on the ovarian luteal and follicular compartment of the rat
Gåfvels, M. E. (1987) · DiVA at Umeå University (Umeå University)

Authors: SHORT, R. V.
Corresponding author: SHORT, R. V.
Venue: Journal of Endocrinology
Publisher: Bioscientifica
Published: 1962-03-01
Volume: 24
Issue: 1
Pages: 59-63
ISSN: 0022-0795 (ISSN-L)
1479-6805
DOI: 10.1677/joe.0.0240059
OpenAlex: W2168319499
Cited by: 176
References: 0
Citations by year: 2025: 2 · 2024: 5 · 2023: 1 · 2021: 2 · 2020: 2 · 2019: 2 · 2018: 3 · 2017: 3 · 2016: 3 · 2015: 3 · 2013: 2 · 2012: 2
FWCI: 12.32
Type: journal article
Language: en
Open access: closed
Locations: Journal of Endocrinology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Reproductive Physiology in Livestock
Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Keywords: ovarian steroids, follicular fluid, corpus luteum, mares, horses, progesterone, 17-hydroxyprogesterone, androstenedione, epitestosterone, estradiol, estrone, 20α-hydroxypregn-4-en-3-one, theca interna cells, luteinized granulosa cells, steroidogenesis
MeSH terms: Animals, Corpus Luteum, Corpus Luteum Hormones, Female, Ovarian Follicle, Horses, Humans, Steroids, Follicular Fluid

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

Steroids in the follicular fluid and the corpus luteum of the mare. A “two-cell type” theory of ovarian steroid synthesis

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cited by

Related

Record

About these checks