Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2019

Open Access 01-12-2019 | Progesterone | Research

Relationships between the antral follicle count, steroidogenesis, and secretion of follicle-stimulating hormone and anti-Müllerian hormone during follicular growth in cattle

Authors: Kenichiro Sakaguchi, Yojiro Yanagawa, Koji Yoshioka, Tomoko Suda, Seiji Katagiri, Masashi Nagano

Published in: Reproductive Biology and Endocrinology | Issue 1/2019

Login to get access

Abstract

Background

The antral follicle count (AFC) in mammalian ovaries positively correlates with female fertility. To clarify the causes of differences in fertility between low and high AFC cows, we investigated follicular growth dynamics and hormone concentrations in plasma, follicular fluid, and in vitro growth (IVG) media at different stages of follicular growth.

Methods

Seven cows were divided into high AFC (n = 4, > 30 follicles) and low AFC (n = 3, < 30 follicles) groups based on the peak AFC detected by ultrasonography. These cows were subjected to estrous synchronization, daily ovarian ultrasonography, and blood collection. Their follicular fluid was collected from dominant follicles at different stages (selection, luteal, and ovulatory phases). In another experiment, we cultured oocyte-cumulus-granulosa cell complexes collected from early antral follicles (< 1 mm) for 12 days. Estradiol-17β (E2), testosterone (T), progesterone (P4), and anti-Müllerian hormone (AMH) concentrations in follicular fluids and plasma were measured. Plasma follicle-stimulating hormone (FSH) concentrations were examined. E2, P4, and AMH concentrations were also measured in IVG media.

Results

The numbers of small (< 4 mm) and intermediate (4–8 mm) follicles were larger in the high AFC group than in the low AFC group (P < 0.05). The number of intermediate follicles was stable in the low AFC group, indicating consistent development. However, the number of these follicles fluctuated in the high AFC group. Plasma FSH concentrations were higher, whereas E2 and T concentrations were lower in the low AFC group (P < 0.05). E2 concentrations and the E2/P4 ratio in ovulatory follicles and IVG media on day 8 were higher in the high AFC group (P < 0.05). AMH concentrations in plasma and IVG media (P < 0.01) were higher in the high AFC group.

Conclusions

The weaker response to FSH of granulosa cells caused low E2 production in the low AFC group, resulting in high FSH concentrations and the consistent development of intermediate follicles. Conversely, higher E2 concentrations suppressed FSH secretion in the high AFC group. Granulosa cells in the high AFC group had the ability to produce more AMH than those in the low AFC group throughout IVG culture.
Literature
1.
Baerwald AR, Adams GP, Pierson RA. Ovarian antral folliculogenesis during the human menstrual cycle: a review. Hum Reprod Update. 2012;18:73–91.PubMedCrossRef
2.
3.
te Velde ER, Pearson PL. The variability of female reproductive ageing. Hum Reprod Update. 2002;8:141–54.CrossRef
4.
Broekmans FJ, Kwee J, Hendriks DJ, Mol BW, Lambalk CB. A systematic review of tests predicting ovarian reserve and IVF outcome. Hum Reprod Update. 2006;12:685–718.PubMedCrossRef
5.
Ireland JJ, Smith GW, Scheetz D, Jimenez-Krassel F, Folger JK, Ireland JL, Mossa F, Lonergan P, Evans AC. Does size matter in females? An overview of the impact of the high variation in the ovarian reserve on ovarian function and fertility, utility of anti-Mullerian hormone as a diagnostic marker for fertility and causes of variation in the ovarian reserve in cattle. Reprod Fertil Dev. 2011;23:1–14.PubMedCrossRef
6.
Ireland JL, Scheetz D, Jimenez-Krassel F, Themmen AP, Ward F, Lonergan P, Smith GW, Perez GI, Evans AC, Ireland JJ. Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biol Reprod. 2008;79:1219–25.PubMedCrossRef
7.
Burns DS, Jimenez-Krassel F, Ireland JL, Knight PG, Ireland JJ. Numbers of antral follicles during follicular waves in cattle: evidence for high variation among animals, very high repeatability in individuals, and an inverse association with serum follicle-stimulating hormone concentrations. Biol Reprod. 2005;73:54–62.PubMedCrossRef
8.
Mossa F, Walsh SW, Butler ST, Berry DP, Carter F, Lonergan P, Smith GW, Ireland JJ, Evans AC. Low numbers of ovarian follicles >/=3 mm in diameter are associated with low fertility in dairy cows. J Dairy Sci. 2012;95:2355–61.PubMedCrossRef
9.
Ireland JJ, Ward F, Jimenez-Krassel F, Ireland JL, Smith GW, Lonergan P, Evans AC. Follicle numbers are highly repeatable within individual animals but are inversely correlated with FSH concentrations and the proportion of good-quality embryos after ovarian stimulation in cattle. Hum Reprod. 2007;22:1687–95.PubMedCrossRef
10.
Nagai K, Yanagawa Y, Katagiri S, Nagano M. Fertilizability of oocytes derived from Holstein cows having different antral follicle counts in ovaries. Anim Reprod Sci. 2015;163:172–8.PubMedCrossRef
11.
Nagai K, Yanagawa Y, Katagiri S, Nagano M. The relationship between antral follicle count in a bovine ovary and developmental competence of in vitro-grown oocytes derived from early antral follicles. Biomed Res. 2016;37:63–71.PubMedCrossRef
12.
Sakaguchi K, Tanida T, Abdel-Ghani MA, Kanno C, Yanagawa Y, Katagiri S, Nagano M. Relationship between the antral follicle count in bovine ovaries from a local abattoir and steroidogenesis of granulosa cells cultured as oocyte-cumulus-granulosa complexes. J Reprod Dev. 2018;64:503-10.CrossRef
13.
Hirao Y, Itoh T, Shimizu M, Iga K, Aoyagi K, Kobayashi M, Kacchi M, Hoshi H, Takenouchi N. In vitro growth and development of bovine oocyte-granulosa cell complexes on the flat substratum: effects of high polyvinylpyrrolidone concentration in culture medium. Biol Reprod. 2004;70:83–91.PubMedCrossRef
14.
Huang W, Kang SS, Nagai K, Yanagawa Y, Takahashi Y, Nagano M. Mitochondrial activity during pre-maturational culture in in vitro-grown bovine oocytes is related to maturational and developmental competences. Reprod Fertil Dev. 2016;28:349–56.PubMedCrossRef
15.
Yang Y, Kanno C, Huang W, Kang SS, Yanagawa Y, Nagano M. Effect of bone morphogenetic protein-4 on in vitro growth, steroidogenesis and subsequent developmental competence of the oocyte-granulosa cell complex derived from bovine early antral follicles. Reprod Biol Endocrinol. 2016;14:3.PubMedPubMedCentralCrossRef
16.
Sakaguchi K, Huang W, Yang Y, Yanagawa Y, Nagano M. Relationship between in vitro growth of bovine oocytes and steroidogenesis of granulosa cells cultured in medium supplemented with bone morphogenetic protein-4 and follicle stimulating hormone. Theriogenology. 2017;97:113–23.PubMedCrossRef
17.
La Marca A, Volpe A. Anti-Müllerian hormone (AMH) in female reproduction: is measurement of circulating AMH a useful tool? Clin Endocrinol. 2006;64:603–10.CrossRef
18.
Fleming R, Seifer DB, Frattarelli JL, Ruman J. Assessing ovarian response: antral follicle count versus anti-Mullerian hormone. Reprod Biomed Online. 2015;31:486–96.PubMedCrossRef
19.
Mossa F, Jimenez-Krassel F, Scheetz D, Weber-Nielsen M, Evans ACO, Ireland JJ. Anti-Mullerian hormone (AMH) and fertility management in agricultural species. Reproduction. 2017;154:R1–r11.PubMedCrossRef
20.
Mossa F, Ireland JJ. Physiology and endocrinology symposium: anti-Mullerian hormone: a biomarker for the ovarian reserve, ovarian function, and fertility in dairy cows. J Anim Sci. 2019;97:1446–55.PubMedCrossRefPubMedCentral
21.
Amer SA, Mahran A, Abdelmaged A, El-Adawy AR, Eissa MK, Shaw RW. The influence of circulating anti-Mullerian hormone on ovarian responsiveness to ovulation induction with gonadotrophins in women with polycystic ovarian syndrome: a pilot study. Reprod Biol Endocrinol. 2013;11:115.PubMedPubMedCentralCrossRef
22.
Broer SL, Mol BW, Hendriks D, Broekmans FJ. The role of antimullerian hormone in prediction of outcome after IVF: comparison with the antral follicle count. Fertil Steril. 2009;91:705–14.PubMedCrossRef
23.
Broer SL, Dolleman M, Opmeer BC, Fauser BC, Mol BW, Broekmans FJ. AMH and AFC as predictors of excessive response in controlled ovarian hyperstimulation: a meta-analysis. Hum Reprod Update. 2011;17:46–54.PubMedCrossRef
24.
Li HW, Lee VC, Lau EY, Yeung WS, Ho PC, Ng EH. Role of baseline antral follicle count and anti-Mullerian hormone in prediction of cumulative live birth in the first in vitro fertilisation cycle: a retrospective cohort analysis. PLoS One. 2013;8:e61095.PubMedPubMedCentralCrossRef
25.
Lukaszuk K, Kunicki M, Liss J, Lukaszuk M, Jakiel G. Use of ovarian reserve parameters for predicting live births in women undergoing in vitro fertilization. Eur J Obstet Gynecol Reprod Biol. 2013;168:173–7.PubMedCrossRef
26.
Panchal S, Nagori C. Comparison of anti-mullerian hormone and antral follicle count for assessment of ovarian reserve. J Hum Reprod Sci. 2012;5:274–8.PubMedPubMedCentralCrossRef
27.
Sunkara SK, Rittenberg V, Raine-Fenning N, Bhattacharya S, Zamora J, Coomarasamy A. Association between the number of eggs and live birth in IVF treatment: an analysis of 400 135 treatment cycles. Hum Reprod. 2011;26:1768–74.PubMedCrossRef
28.
Himabindu Y, Sriharibabu M, Gopinathan K, Satish U, Louis TF, Gopinath P. Anti-mullerian hormone and antral follicle count as predictors of ovarian response in assisted reproduction. J Hum Reprod Sci. 2013;6:27–31.PubMedPubMedCentralCrossRef
29.
Rosen MP, Johnstone E, McCulloch CE, Schuh-Huerta SM, Sternfeld B, Reijo-Pera RA, Cedars MI. A characterization of the relationship of ovarian reserve markers with age. Fertil Steril. 2012;97:238–43.PubMedCrossRef
30.
Tsakos E, Tolikas A, Daniilidis A, Asimakopoulos B. Predictive value of anti-mullerian hormone, follicle-stimulating hormone and antral follicle count on the outcome of ovarian stimulation in women following GnRH-antagonist protocol for IVF/ET. Arch Gynecol Obstet. 2014;290:1249–53.PubMedCrossRef
31.
Arce JC, La Marca A, Mirner Klein B, Nyboe Andersen A, Fleming R. Antimullerian hormone in gonadotropin releasing-hormone antagonist cycles: prediction of ovarian response and cumulative treatment outcome in good-prognosis patients. Fertil Steril. 2013;99:1644–53.PubMedCrossRef
32.
Brodin T, Hadziosmanovic N, Berglund L, Olovsson M, Holte J. Antimullerian hormone levels are strongly associated with live-birth rates after assisted reproduction. J Clin Endocrinol Metab. 2013;98:1107–14.PubMedCrossRef
33.
Durlinger AL, Kramer P, Karels B, de Jong FH, Uilenbroek JT, Grootegoed JA, Themmen AP. Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary. Endocrinology. 1999;140:5789–96.PubMedCrossRef
34.
Yang MY, Cushman RA, Fortune JE. Anti-Mullerian hormone inhibits activation and growth of bovine ovarian follicles in vitro and is localized to growing follicles. Mol Hum Reprod. 2017;23:282–91.PubMedPubMedCentralCrossRef
35.
Durlinger AL, Gruijters MJ, Kramer P, Karels B, Kumar TR, Matzuk MM, Rose UM, de Jong FH, Uilenbroek JT, Grootegoed JA, Themmen AP. Anti-Mullerian hormone attenuates the effects of FSH on follicle development in the mouse ovary. Endocrinology. 2001;142:4891–9.PubMedCrossRef
36.
Grossman MP, Nakajima ST, Fallat ME, Siow Y. Mullerian-inhibiting substance inhibits cytochrome P450 aromatase activity in human granulosa lutein cell culture. Fertil Steril. 2008;89:1364–70.PubMedCrossRef
37.
Chang HM, Klausen C, Leung PC. Antimullerian hormone inhibits follicle-stimulating hormone-induced adenylyl cyclase activation, aromatase expression, and estradiol production in human granulosa-lutein cells. Fertil Steril. 2013;100:585–92 e581.PubMedCrossRef
38.
Campbell BK, Clinton M, Webb R. The role of anti-Mullerian hormone (AMH) during follicle development in a monovulatory species (sheep). Endocrinology. 2012;153:4533–43.PubMedCrossRef
39.
Monniaux D, Clemente N, Touze JL, Belville C, Rico C, Bontoux M, Picard JY, Fabre S. Intrafollicular steroids and anti-mullerian hormone during normal and cystic ovarian follicular development in the cow. Biol Reprod. 2008;79:387–96.PubMedCrossRef
40.
Rico C, Fabre S, Medigue C, di Clemente N, Clement F, Bontoux M, Touze JL, Dupont M, Briant E, Remy B, et al. Anti-mullerian hormone is an endocrine marker of ovarian gonadotropin-responsive follicles and can help to predict superovulatory responses in the cow. Biol Reprod. 2009;80:50–9.PubMedCrossRef
41.
Scheetz D, Folger JK, Smith GW, Ireland JJ. Granulosa cells are refractory to FSH action in individuals with a low antral follicle count. Reprod Fertil Dev. 2012;24:327–36.PubMedCrossRef
42.
Ireland JJ, Zielak-Steciwko AE, Jimenez-Krassel F, Folger J, Bettegowda A, Scheetz D, Walsh S, Mossa F, Knight PG, Smith GW, et al. Variation in the ovarian reserve is linked to alterations in intrafollicular estradiol production and ovarian biomarkers of follicular differentiation and oocyte quality in cattle. Biol Reprod. 2009;80:954–64.PubMedCrossRef
43.
Mossa F, Jimenez-Krassel F, Folger JK, Ireland JL, Smith GW, Lonergan P, Evans AC, Ireland JJ. Evidence that high variation in antral follicle count during follicular waves is linked to alterations in ovarian androgen production in cattle. Reproduction. 2010;140:713–20.PubMedCrossRef
44.
de Vries MJ, Veerkamp RF. Energy balance of dairy cattle in relation to milk production variables and fertility. J Dairy Sci. 2000;83:62–9.PubMedCrossRef
45.
Rizos D, Ward F, Duffy P, Boland MP, Lonergan P. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev. 2002;61:234–48.PubMedCrossRef
46.
Berfelt DR, Lightfoot KC, Adams GP. Ovarian synchronization following ultrasound-guided transvaginal follicle ablation in heifers. Theriogenology. 1994;42:895–907.PubMedCrossRef
47.
Hayashi KG, Matsui M, Acosta TJ, Kida K, Miyamoto A. Effect of the dominant follicle aspiration before or after luteinizing hormone surge on the corpus luteum formation in the cow. J Reprod Dev. 2006;52:129–35.PubMedCrossRef
48.
O'Hara L, Scully S, Maillo V, Kelly AK, Duffy P, Carter F, Forde N, Rizos D, Lonergan P. Effect of follicular aspiration just before ovulation on corpus luteum characteristics, circulating progesterone concentrations and uterine receptivity in single-ovulating and superstimulated heifers. Reproduction. 2012;143:673–82.PubMedCrossRef
49.
Bao B, Garverick HA, Smith GW, Smith MF, Salfen BE, Youngquist RS. Changes in messenger ribonucleic acid encoding luteinizing hormone receptor, cytochrome P450-side chain cleavage, and aromatase are associated with recruitment and selection of bovine ovarian follicles. Biol Reprod. 1997;56:1158–68.PubMedCrossRef
50.
Ginther OJ, Kastelic JP, Knopf L. Composition and characteristics of follicular waves during the bovine estrous cycle. Anim Reprod Sci. 1989;20:187–200.CrossRef
51.
Harada M, Miyano T, Matsumura K, Osaki S, Miyake M, Kato S. Bovine oocytes from early antral follicles grow to meiotic competence in vitro: effect of FSH and hypoxanthine. Theriogenology. 1997;48:743–55.PubMedCrossRef
52.
Yanagawa Y, Matsuura Y, Suzuki M, Saga S, Okuyama H, Fukui D, Bando G, Nagano M, Katagiri S, Takahashi Y, Tsubota T. Accessory corpora lutea formation in pregnant Hokkaido sika deer (Cervus nippon yesoensis) investigated by examination of ovarian dynamics and steroid hormone concentrations. J Reprod Dev. 2015;61:61–6.PubMedCrossRef
53.
Kaneko H, Noguchi J, Kikuchi K, Todoroki J, Hasegawa Y. Alterations in peripheral concentrations of inhibin a in cattle studied using a time-resolved immunofluorometric assay: relationship with estradiol and follicle-stimulating hormone in various reproductive conditions. Biol Reprod. 2002;67:38–45.PubMedCrossRef
54.
Ginther OJ, Bergfelt DR, Kulick LJ, Kot K. Selection of the dominant follicle in cattle: role of estradiol. Biol Reprod. 2000;63:383–9.PubMedCrossRef
55.
Endo M, Kawahara-Miki R, Cao F, Kimura K, Kuwayama T, Monji Y, Iwata H. Estradiol supports in vitro development of bovine early antral follicles. Reproduction. 2013;145:85–96.PubMedCrossRef
56.
Mossa F, Jimenez-Krassel F, Walsh S, Berry DP, Butler ST, Folger J, Smith GW, Ireland JL, Lonergan P, Ireland JJ, Evans AC. Inherent capacity of the pituitary gland to produce gonadotropins is not influenced by the number of ovarian follicles > or = 3 mm in diameter in cattle. Reprod Fertil Dev. 2010;22:550–7.PubMedCrossRef
57.
Erickson BH. Development and senescence of the postnatal bovine ovary. J Anim Sci. 1966;25:800–5.PubMedCrossRef
58.
Randolph JF Jr, Zheng H, Sowers MR, Crandall C, Crawford S, Gold EB, Vuga M. Change in follicle-stimulating hormone and estradiol across the menopausal transition: effect of age at the final menstrual period. J Clin Endocrinol Metab. 2011;96:746–54.PubMedCrossRef
59.
Knight PG. Roles of inhibins, activins, and follistatin in the female reproductive system. Front Neuroendocrinol. 1996;17:476–509.PubMedCrossRef
60.
Pellatt L, Rice S, Dilaver N, Heshri A, Galea R, Brincat M, Brown K, Simpson ER, Mason HD. Anti-Mullerian hormone reduces follicle sensitivity to follicle-stimulating hormone in human granulosa cells. Fertil Steril. 2011;96:1246–51 e1241.PubMedCrossRef
61.
Luo W, Wiltbank MC. Distinct regulation by steroids of messenger RNAs for FSHR and CYP19A1 in bovine granulosa cells. Biol Reprod. 2006;75:217–25.PubMedCrossRef
Metadata
Title
Relationships between the antral follicle count, steroidogenesis, and secretion of follicle-stimulating hormone and anti-Müllerian hormone during follicular growth in cattle
Authors
Kenichiro Sakaguchi
Yojiro Yanagawa
Koji Yoshioka
Tomoko Suda
Seiji Katagiri
Masashi Nagano
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2019
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-019-0534-3

Other articles of this Issue 1/2019

Reproductive Biology and Endocrinology 1/2019 Go to the issue

Research

Letrozole-associated controlled ovarian hyperstimulation in breast cancer patients versus conventional controlled ovarian hyperstimulation in infertile patients: assessment of oocyte quality related biomarkers

Short communication

Blastomere movement post first cell division correlates with embryonic compaction and subsequent blastocyst formation

Research

Low dose of flurochloridone affected reproductive system of male rats but not fertility and early embryonic development

Research

The impact of previous live births on peripheral and uterine natural killer cells in patients with recurrent miscarriage

Research

Entry into puberty is reflected in changes in hormone production but not in testicular receptor expression in Atlantic salmon (Salmo salar)

Research

The impact of follicle-flushing during oocyte collection on embryo development of in-vitro fertilization